Cause of stereotypies in captive rhesus macaques (Macaca Mulatta)

Stereotypic behaviour in captive rhesus macaques (Macaca Mulatta) is common, predominantly in singly-housed rhesus macaques. There are numerous causes for this type of abnormal behaviour and it is normally assumed that stereotypies signal poor welfare, although this is not always the case. Rhesus macaques are held in captivity for entertainment, research and sometimes at pets, therefore it is important to understand how to prevent stereotypic behaviour in order to provide a good quality of life for these primates.

It is important to ensure good welfare for captive macaques primarily for their own health, but also for accuracy in research involving non-human primates. This essay will explore the possible environmental and intrinsic causes of stereotypic behaviour and how to prevent or reduce such behaviours.

Natural habitat of rhesus macaques

Rhesus macaques are referred to as Chinese- and Indian- derived. They are the only primates with a larger geographic distribution than humans. Rhesus macaques are found all over mainland Asia; from Afghanistan to India and Thailand to southern China (Lang, 2005). As rhesus macaques are found in such a broad geographic area, it is difficult to summarise their typical habitat. Generally, they are located in both tropical and temperate climates including semi-desert, dry deciduous, mixed deciduous and bamboo, and temperate forests as well as in tropical forests and mangrove swamps. Rhesus macaques are also found in areas close to humans in urban settings or near cultivated fields, relying on humans for food (Lang, 2005).

Because of their anatomical and physiological closeness to humans, the relative ease at which they can be maintained and bred in captivity, and the available supply from India, rhesus macaques have long been the non-human primate of choice on which to conduct research on human and animal health-related topics. Some of the direct benefits to human health that would not have been possible without the use of rhesus macaques include: development of the rabies, smallpox, and polio vaccines, discovery of rhesus factor in blood, creation of drugs to manage HIV/AIDS, understanding of the female reproductive cycle and development of the embryo, propagation of embryonic stem cells, and a number of behavioral discoveries.

Natural behaviours

Natural behaviour of rhesus macaques is the behaviour they tend to display in their natural habitat and that which is accepted of physically and psychologically healthy animals. Alterations in this behaviour or the absence of particular behaviours can indicate compromised state of welfare. All animals’ needs are not limited to the need for food, water and shelter; they also require the ability to exercise natural behaviours (Bracke and Hopster, 2006).

Expressively social primate species, such as rhesus macaques, should exhibit appropriate social behaviours, including physical, vocal and visual displays. These behaviours may include but are not limited to, interactive play, food sharing, social grooming and communal resting. The natural group size and composition varies between different species and this should be taken into account when housing macaques (Mallapur, 2005).

Social behaviours such as grooming and interactive play with conspecifics are educational, stimulating and enjoyable. Separating a rhesus macaque from its group can have negative psychological effects on both the individual and the rest of the group, especially for an infant and mother. Grooming is an important social activity. It retains and reinforces social bonds, builds companionship between group members and maintains coat condition. Interactive play is a good indicator of psychological and physical well-being although older primates may not take part in this activity (Mallapur, 2005).

Stereotypies

Rhesus macaques housed in a captive environment can exhibit different kinds of stereotypies. Stereotypies in animals are atypical behaviours, usually repetitive, fixed behaviour patterns with no obvious purpose (Lutz, 2018). They are thought to be the result of frustration, stress or fear in an abnormal environment, either past or present, that prevents the animal from performing natural behaviours (Mason, 1991; Garner, 2005). Other factors including maternal deprivation at a young age and social isolation are also thought to produce stereotypic behaviours. Stereotypies are considered an indicator of poor welfare.

Stereotypic behaviours vary and can include repetitive behaviours such as pacing, bouncing, circling, head-bobbing, bar-biting, rocking and swaying. Determining whether or not a behaviour is a stereotypy can be challenging. The differences between stereotypies and normal behaviour patterns can merge; stereotypies may be fused with normal behaviours, and many normal behaviour patterns are stereotyped. Therefore, in some cases distinguishing between normal and abnormal behaviour can be complicated (Lutz, 2014).

Many factors have been shown to increase the risk of rhesus macaques developing stereotypic behaviours. Infancy is an especially vulnerable stage, early experiences and rearing environments can have a profound effect on an animal’s behavioural development, possibly leading to poor social outcomes, abnormal behaviour, increased anxiety and stereotypies (Novak et al., 2012). It is also possible for older rhesus macaques to develop stereotypies, particularly when separated from social companions and placement in individual cage housing. Increased risk is influenced by the exposure to stressful events, clinical procedures and intrinsic variables such as species, age and sex (Novak et al., 2012; Lutz, 2018).

Environmental Causes of Stereotypies

Environments that are prone to a high rate of stereotypic behaviours in rhesus macaques are regarded as having a lower standard of welfare than those environments within which stereotypic behaviours are uncommon. The relative frequency of stereotypies in captive animals is often used as an indicator of the level of welfare across various environmental conditions. Rhesus macaques housed in an environment full of enrichment are less likely to develop stereotypic behaviours and often display physical signs of positive welfare, such as reduced heart rate and cortisol levels, compared to rhesus macaques housed in an environment lacking enrichment (Gottlieb et al., 2015). A study conducted by Gottlieb et al. (2015) found that foraging devices and full contact socialization are particularly beneficial in preventing stereotypies when known predictors of stereotypies such as age and sex were controlled.

Nursery rearing is one of the primary causes of stereotypic behaviour later in life and should be employed only as a last resort. To ensure the good welfare, Gottlieb at al. (2013) recommend rhesus macaques should be reared in a spacious outdoor enclosure within a social group when possible. As it is not always possible to raise rhesus monkeys in this type of environment, effort should be made to ensure opportunities for group socialisation are put in place from infancy through to adulthood.

If group socialisation is not possible, full contact socialisation is recommended over partial contact and single housing. Furthermore, if rhesus monkeys have established relationships in full contact pairs it is imperative that these partnerships are maintained as separation from a partner is stressful and can cause abnormal behaviours and stereotypies. Likewise, moving primates from one enclosure to another or transporting them to a different location can cause further stress (Gottlieb et al., 2013).

Another cause of stress in caged rhesus macaques is the level of the cage and also its proximity to the entrance of the room. Research has shown that rhesus macaques housed in cages at the lowest level are more susceptible to stress than those in cages at a higher level, and primates housed next to the entrance of the room also present higher levels of stress than those further away. If signs of abnormal behaviour occur, relocation to a cage on the top row further away from the door could improve stress levels (Gottlieb et al., 2013).

Intrinsic Causes of Stereotypies

Intrinsic factors can also influence the probability of developing stereotypic behavior. Studies have shown that bold monkeys and of Chinese origin are more likely to exhibit stereotypic behaviours than introverted and Indian descent primates, respectively. Although it is easy to assume that primates with bold characteristics and of Chinese origin are more likely to experience compromised welfare in captivity, it is possible that expression through stereotypic behaviour should not be the only factor used to assess the welfare of individuals (Mason and Latham, 2004). In any environment, NHP displaying high levels of stereotypic behaviour may not be housed in poor conditions. The underlying reason for stereotypic behaviour could be the result of various factors including past experiences and intrinsic factors, not only the current environment. All factors should be taken into account when using primates in laboratories or exhibiting them in zoos (Gottlieb et al., 2015).

Preventative methods

One strategy to reduce or prevent stereotypic behaviour in captive rhesus macaques is the supply of enrichment within the enclosure. This could be in the form of an object covered or filled with food, hanging devices and toys. This type of enrichment encourages primates to perform species-typical behaviour such as foraging, exploring and playing which reduces boredom (Gottlieb et al., 2015). The effectiveness of providing foraging enrichment is unclear as some studies have shown a decrease in stereotypic behaviours (Novak et al., 1998), while other studies have found no effect on stereotypic behaviour when primates were supplied with foraging enrichment (Schapiro and Bloomsmith, 1995). An explanation for this could be that present environmental factors were not the cause of stereotypies but either intrinsic factors or rearing history.

Another approach to improving welfare and decreasing expression of stereotypies is introducing caged rhesus macaques to a social partner. Single housing is known to cause stereotypies so housing rhesus macaques in pairs or groups reduces the risk of developing or continuing stereotypic behaviours. Full contact pairing has shown to correlate with decreased stereotypic behaviour in rhesus macaques (Baker et al., 2012a; Baker et al., 2013). On the other hand, protected contact, when two rhesus macaques are housed adjacently but are partially separated by a divider that allows some contact, does not show the same results. Rhesus macaques housed in this way have displayed higher levels of stereotypies than in full contact housing (Baker et al., 2012b; Baker et al., 2013). This is likely because the separation barrier only allows limited physical contact between the individuals. However, studies on longtailed macaques have found that using bars to separate two enclosures with space allowing for more contact showed no significant differences between this type of housing and full contact housing (Baker et al., 2012b). Reasons for this could be due to more contact between the non-human primates or it could be species-specific.

Positive reinforcement training

Positive reinforcement training (PRT) has shown to reduce stereotypic behaviour in the short term. A 2010 study (Coleman and Maier) analysed the effects of PRT on female rhesus macaques housed in a research facility. Researchers used PRT on one group of monkeys while another group were not trained and monitored their behaviour over a period of four months. After one month, they found that stereotypic behaviour was reduced by 85% in trained monkeys while the control monkeys actually showed an increase in stereotypic behaviour. This shows PRT had a positive impact on the monkeys during the first month, although the group differences were not maintained. In months two to four, there were no significant differences between trained and control monkeys in reduction of stereotypy. However, for the first three months of the study, stereotypical behaviour was reduced by at least 85% in half of the trained monkeys. This percentage increased in month four.

These results could be due to the training methods utilised during the experiment. For months one and two, the training mostly consisted of target training and extending limbs out of the cage to accept venipuncture. During the third month, the main focus was desensitizing the monkeys to the presence of a syringe by touching them with a capped syringe. This could have caused the monkeys some stress which could explain the increase in stereotypy. Furthermore, the monkeys could have experienced more boredom or frustration compared to the first two months as there were less new tasks to learn.

Additionally, the decrease in statistical significance after the first month of the study was not due to an increase in stereotypic behaviour in the trained animals, but rather from a decrease in stereotypy in the control monkeys. The researchers were unable to conclude the reason for this although it is possible that the control monkeys reduced stereotypical behaviour as they got used to the presence of an observer. Other factors such as new caretakers, changes in environmental enrichment or the movement of conspecifics into or out of rooms could have affected the amount of stereotypy displayed by the control animals.

The results of this study suggest that PRT can help reduce stereotypic behaviour in some captive rhesus macaques, at least for the short term. Further, the results suggest that PRT may be more effective in alleviating stereotypy in some individuals than in others. Future studies should examine potential sources of this variation in response to PRT among subjects with stereotypy, including the type of training as well as the underlying cause of the stereotypical behaviour (Coleman and Maier, 2010).

Conclusion

Research shows that environment is an important factor in the cause of stereotypies although it is important to note that rearing history, past experiences, group composition and primate personality should also be considered when determining the cause of stereotypies. To reduce the risk of stereotypic behaviour, rhesus macaques should be provided with a large enclosure with appropriate enrichment and ideally with a group of conspecifics, taking into consideration appropriate group sizes and sex ratios.

Stereotypies caused by rearing history or past experiences cannot always be lessened by improvements to current welfare although it is possible that positive reinforcement training could reduce stereotypies short-term and more research needs to be done in this area with experimentation on the training methods and more varied tasks over longer periods of time.

References

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