Rehabilitating Captive Wild-Born Yellow Baboons (Papio Cynocephalus) for Re-Introduction Into the Wild

Full Length Research Paper

Rehabilitating captive wild-born yellow baboons (Papio cynocephalus) for re-introduction into the wild

Valentine Buh Ebua¹*, Tsi Evaristus Agwafo², Mpoame Mbida1 and Jonathan Vaughan3

¹University of Dschang, Department of Animal Biology Cameroon. ²University of Dschang, Department of Forestry, Cameroon. 3Lilongwe wildlife Center, Malawi.

Accepted 12 December, 2013

With the increasing number of rescued orphan primates in wildlife centers, most of these centers are faced with the problem of providing shelter to all the continuously saved individuals. A solution to this is to rehabilitate some of the captive wild-born individuals through a systematic approach and reintroduce them back into the wild for a conservation and welfare purpose. We have developed and made use of a scientific approach in rehabilitating yellow baboons’ in-situ prior to release. This approach may not be practicable to all programmes but can be used as a model to adapt a similar or succinct approach to other species. It is intended to set a pace and to encourage many centers to get involved in the rehabilitation process and reduce the problems of accommodating space faced in their centers. This model come up is to add to other standardizing methods in the world concerned with reintroduction and help to prevent most unsuccessful releases carried out across the sphere.

Key words: Re-introduction, rehabilitation, conservation, welfare, systematic approach, yellow baboons, captive wild-born individuals.

INTRODUCTION

Rehabilitation and Re-introduction programs have been and reintroduction may play a significant role in supporting used recently for decades as a method of conservation the wild populations, as well as raising awareness of the for mammal species for some time (Kleiman, 1989) and plight of these species (Cheyne et al., 2008). these programs have also provided an opportunity for It is estimated that almost half of the world’s nonhuman animals that have lived in captivity to have another chance primates are threatened with extinction and 29% are at living in the wild, and it is considered as one way of re- categorized as endangered or critically endangered establishing populations that have become locally extinct [International Union for Conservation of Nature and (Komdeur and Deerenberg, 1997). Reintroduction Natural Resources (IUCN, 2010]. Current conservation addresses conservation on two different levels. First, efforts seek to preserve the diversity of the primate order animals that are kept illegally as pets are rescued, rehabi- and to ensure the survival of representative populations litated, and then returned to the wild; and secondly, by of species in their natural habitats. reintroducing animals into areas where they are locally The primary extrinsic threats to the majority of primates extinct, the wild populations are supplemented and are undoubtedly loss of habitat and hunting. In addition, potentially more forest can be protected (Cheyne, 2006; as remaining populations continue to decrease, the Kleiman, 1989). It has been acknowledged that presser- effects of secondary threats, such as the use of primates vation of wild populations and their habitats is imperative for traditional purposes and the illegal pet trade, become for the conservation of wild species, and rehabilitation more important (Cowlishaw and Dunbar, 2000; Nijman et

*Corresponding author. E-mail: [email protected] 160 Int. J. Biodivers. Conserv.

al., 2009). The illegal trade of primates can have a drastic hensive study of the rehabilitation process and effect on the last surviving populations of already rare reintroduction of primates to date. As they demonstrated species. Young primates are removed from the wild and in their work, during the rehabilitation process, it is crucial most often, reproductively viable adults are killed in the to document the behaviour of individuals in captivity prior process. In addition, as a result of the illegal trade to their release, so that we are able to compare the pre- network, primates are becoming displaced and orphaned, and post-release behaviour as a way to determine the These orphans are brought into various types of rescue relative success of the reintroduction projects. Therefore, and rehabilitation centers when the owners realize they monitoring their behaviour before they are released is a can no longer control them or when siezed (Cheney et al., crucial component in the reintroduction program for the 2004). This has brought about the increasing number of species and hopefully it will ensure a successful release. Baboons in most Wildlife Centers like is the case of This study constitutes the first step at developing a Lilongwe Wildlife Centre (Malawi) and likewise the Limbe more systematic approach to the re-introduction of yellow Wildlife Centre (Cameroon) where baboons are the highest baboons’ by conducting a rehabilitation of 28 wild-born species of primates at the Centers (per. obs.). All species captive Yellow Baboons through a scientific behavioural of Baboons (Cercopithecinae sub-family) have declined training (how to feed/forage, locomote, rest in safe over the past 30-40 years, primarily due to loss of habitat location, recognize their predators, etc) so as to determine and the subsequent fragmentation of forests through which of these individuals show behaviours that could timber felling, charcoal burning, encroachment for permit them survive in the wild. cultivation of plantations and industrial settlement Releasing rescued primates back into the wild requires (Cheney et al., 2004; Nijman and van Balen, 1998). Other careful thinking, research and planning. Unfortunately, factors contributing to their demise include the illegal the release of wild born/captive animals can be disastrous wildlife trade, hunting, and the use of their body parts in to individual animals, entire populations, species and traditional medicine (Cheney et al., 2004). ecosystems if not done correctly (Kleiman, 1989). This Most Wildlife Center receives donated or confiscated failure had generated significant scientific skepticism, pets and other species with the goal of restoring their fuelled in large part by the tendency for the initial deci- physical and psychological health back to a high level as sions concerning the design of release programmes to be possible. This process includes assessing their medical informed by pragmatism rather than sound science and behavioural status and placing them into an (Sarrazin and Barbault, 1996; Ewen and Armstrong, appropriate social environment of an adult male and 2007). An historic absence of scientific rigor within the female. These species have been removed from the wild framework of release schemes has certainly contributed at a young age and have lived as pets for most of their to poor overall success rates, and may in some instances adult lives and are facing a lot of challenges because the have even lead to animals being harmed (Moinde et al., complex social, psychological and physical needs of 2004). In light of such risks, and as a direct consequence primates cannot be meet when they are kept as pets or in of the increase in reintroduction programmes, the Interna- captivity. These challenges include: learning how to tional Union for Conservation of Nature (IUCN) set up the vocalize in the appropriate social context (predators, repro- Reintroduction Specialist Group of the Species Survival duction etc), appropriately socializing with conspe-cifics Commission (SSC/RSG) to develop Guidelines for the (Mootnick and Nadler, 1997), overcoming the potential Reintroduction of Non-Human Primates into the wild. prevalence of stereotypic or human-directed behaviours, These internationally accepted, best practice guidelines learn how to locomote efficiently (brachiate, developing cover the main steps and considerations of a reintro- balance), and learning how to locate and procure food duction effort and suggests an order of execution (Farmer (Cheney et al., 2004; Kleiman, 1989). et al., 2006; Farmer and Courage, 2008; Soorae and It is imperative to have an understanding of species Baker, 2002). The deployment of such scientific guide- behaviour during the rehabilitation process before re- lines within reintroduction programmes, akin to long-term introduction, in order to help ensure the troop or funding procurement, is considered absolutely essential individual(s) will have the best opportunity to adapt to a for the implementation of a successful release scheme life free from human dependency in the wild. Behavioral (Kleiman et al., 1994; Sarrazin and Barbault, 1996; studies can contribute a significant amount of knowledge Armstrong and Seddon, 2007). The guidelines are a to reintroduction programs by examining the underlying ‘best-practice’ model or an ideal code of conduct. evolutionary mechanisms of species’ behaviour, such as For the past decades, most re-introduction programmes the driving forces behind social and spatial organization, have existed but failed or always unsuccessful because and by developing an understanding of how they respond of no proper rehabilitation approach of captive wild-born to different social and environmental conditions (Clemmons individuals who have lost their natural talents due to and Buchholz, 1997). There are very few data available captivity (IUCN, 2002). Secondly, even if there is a rehabi- on the behaviour of reintroduced primates and their ability litation process, it is done without a good knowledge of to adapt to a new environment (Grooves, 2001; Kleiman, the species’ ecological behaviour, no feasibility studies 1989; Cheney et al. (2004), present the only compre- carried out to assess if the release site has a good habitat Ebua et al. 161

quality fit for the release individuals (Kleiman et al., to prepare the animals for release. It can be divided into four 1994). The complex social, physical and psychological compartments of varying sizes, allowing for human access to the needs of primates cannot be met when they are kept as enclosure for feeding and cleaning purposes, without incurring direct contact with the Baboons. The enclosure had two fences: the pets, are lonely or in deprivation (Cheyne et al., 2008) first is with barked wires electrified and the second screened on all which leads to the lost of natural talents which when four sides by makuti fencing, with eight viewing windows. This acts released, do not permit them to compete with wild as a barrier between humans and the monkeys, while also allowing conspecifics. Lastly most of these re-introduction pro- for inconspicuous monitoring of the animals, observation and grammes have concentrated in re-introducing a few collection of data, essential for performing life skills training. All interaction with humans is minimised to allow de-humanisation. individuals (< 8) wherein this small number of individuals The size of the enclosure for 31 individual approximate natural cannot constitute a cohesive group to defend their troops in terms of size and composition. territory, resources and mates against most powerful wild troop. The lack of a proper scientific approach before reintroduction, has also led to some many unsuccessful re- Study troop introduction programmes where the released individuals All the animals within the release stock were rescued from inside are unable to reproduce for fitness. Even if these small Malawi and are indigenous to Malawi. They are therefore predo- numbers of individuals are released, they end up migra- minately wild born, captive stock, which is important distinction to ting because of no proper studies done on group make as wild born animals fair better in reintroduction programmes cohesion and maintenance of proximity, and the biology than captive born animals (Kleimen, 1996); and strategies used in of the conspecifics in the wild. Another weakness in these the introduction of wild-born captive individuals can be different re-introduction programmes has been the release of from those used with captive born individuals (Chivers, 1991). All of the potential release stock animals have been at the centre for one animals without any training awareness on the identify- or more years, but rarely more than four years. Most of the animals cation and recognition of predators and how to defend or have come out of the illegal pet trade, have been confiscated in escape from the predators. All this therefore require the Malawi or handed over out of free will to the LLWC; most were need for a scientific rehabilitation approach where the orphaned upon arrival. Two individuals arrived at the Centre after biology and the ecology of the species are taken into being orphaned at approximately 10 days old and majority of the remaining individuals were anything from a few weeks old to less considerations, alongside an assessment of the release than six months when removed from the wild. site (to determine if it has a good habitat quality fit as a carrying capacity). Data collection

MATERIALS AND METHODS Rehabilitation data

A multidisciplinary technique of data collection was employed based Rehabilitation site on the various aspects involved in the data collection process (behaviour, proximity, feeding/foraging training techniques and The Lilongwe Wildlife Center (LLWC) is a wildlife rescue, conservation veterinary and body condition checks). Data was collected for six and environmental education facility. It is Malawi’s only rehabilitation days a week and for 8-12 h a day. Censuses for sleeping sites sanctuary for orphaned, injured and rescued wildlife and it is fully selection were done at 6.00 to 7.00 h and later in the evening at registered as a Malawian not-for-profit trust and non-governmental 17.00-18.00 h while focal and scan sampling of individuals was organisation (NGO). The LLWC works in partnership with the carried out from 7.00 to 18.00 h in order not to miss important early Department of National Parks and Wildlife (DNPW) of Malawi to morning and late evening behaviours and proximities. Because of ensure that all political, cultural and legal requirements of their work the long hours of data collection, four people were involved in the are met. At present, the LLWC is home for more than 150 Malawian data collection process. primates, mainly vervet monkeys (Chlorocebus pygerythrus In an effort to collect equivalent amount of data for each individual, rufoviridus) and yellow baboons (Papio cynocephalus we rotated the order of observation for each day following the cynocephalus). The majority of these animals have been rescued or recommendations of Cheney et al. (2004). We collected a total of confiscated from persons or organisations involved in the illegal 96 h (5,760 min) for each individual during the rehabilitation period wildlife trade and exploitation. One of the main goals of the LLWC is of 18 months with a total of 2,880 hspent in 18 months to observe to release these successfully rehabilitated animals back into the the entire group. For proximity, each individual was observed 288 wild, whenever it is possible and appropriate. It is located in times for 20 min each in 18 months. Lilongwe Town along the Kenyatta drive. It has a land surface of 33 hectares with natural trees, captive and non-captive animals. Behavioural data collection

Behavioural data was collected using focal, instantaneous Enclosure design sampling. Focal animals were selected using random sampling; rotating according to a fixed, randomly selected schedule, through The yellow baboons were located in a pre-release rehabilitation all individuals (Altmann, 1974). This method prevents prominent enclosure, 180 x 200 x 4.5 m located in the Wildlife Centre’s individuals from being studied more frequently than non-prominent grounds, surrounded by Coral Rag Forest and visited almost daily individuals and ensures that different age and sex classes of the by wild troops of each primate species occurring in this area. The troop are studied at different times of the day, reducing bias in pre-release enclosure is vital for the successes of the release possible time associated behaviours such as feeding behaviour and programme as it incorporates designs that allow the research team species eaten. Focal follows were done all day for eight to 12 h a 162 Int. J. Biodivers. Conserv.

day (individuals were observed in the morning or afternoon study records observed in their major activities to the guidelines we periods, depending on the research timetable). Each observer proposed and adapted from those recommended by Cheyne et al. conducted 10 focal follows of 30 min (the first 5 min started with the (2008) for the Javan Gibbon rehabilitated project. Table 1 highlights selection of a focal individual, 20 min of focal sampling and the last the important aspects of wild behaviour that a rehabilitated yellow remaining 5 min were used to ensure the correct identity of plant baboon troop should master before they are reintroduced. It is also and animal species eaten during the focal or the collection and crucial that the individuals solicit little to no human interaction labeling of samples for identification) a day. In order to generate an (soliciting grooming from keepers, begging, aggressive behavior) activity budget for each individual, we recorded the individual states because once they are released this behaviour could potentially be observed with major activities including: feeding/foraging, harmful and can hinder their chances of survival in the wild. We locomotion, vocalization and others. We recorded socio-positive calculated the average percent of observation records of each association behaviour such as grooming, playing, copulation and baboon spent in major activities (rest, feed/forage, social, other. Human-directed and stereotype behaviours were recorded as locomotion, and vocalization) during the observation period. either events or states depending on the duration and frequency of occurrence. In addition, all interactions with other wildlife species that pass by the enclosure from the neigbouring forest were RESULTS recorded using all occurrences sampling. When an individual was recorded as feeding/foraging, additional dietary data was collected, recording the food type item (young leaves, mature leaves, roots, Out of the thirty-one individuals rehabilitated, data or stems, flowers, shoots or animals prey) and the species. information was collected only for 28 individuals. The Unidentified species were collected for later taxonomic iden- other three individuals were not considered for two tification. reasons: because they were yearlings (less than or equal

to one year old) and lastly because they are captive born Proximity, socio-positive data individuals and according to IUCN guideline (2002) these types of non human primates are not supposed to be In addition to recording the behavioural states at 1 min interval, we recorded the focal individual’s proximity to one another and their reintroduced because it would be difficult for them to location in the enclosure every ten minute interval for 20 min (0th, acquire skills that permit them to survive in the wild. 10th and 20th min). Scan samplings were used to record all groups members that were in contact (<1 m, 1-3 m, 3-5 m and >5 m) to the focal subject. Instances of socio-positive behaviours including Activity budget grooming, play and body contact occurring between the focal subject and group members were recorded during the 20 minute focal follows, discussed above, using instantaneous sampling and The average percent of observation records that each recording the identities of the individuals involved. When more than member of the troop spent engaged in particular activities two individuals are involved in the socio-positive behaviour each during the 18 months of the rehabilitation process was considered a separate partner to the focal individual and indicates that all the individuals show similar activity therefore considered as separate dyads. Distances between patterns but with some disparity in time spent at a individuals were estimates that is why this aspect of data collection was done by a single individual. particular activity by each member of the troop. Only two individuals (Richard and Baby Mckenzie) spent less than 25% of their time feeding/foraging (23.2 and 15.8% Feeding/foraging training techniques respectively) while the other 26 individuals were engaged The second part of the pre-release training involved the training in more than 25% of their activities feeding/foraging. techniques for foraging as well as accustoming the animals to a Chico, Magda and Secha spent above 70% of their time new diet which approximates their future diet in the wild. During the in feeding/foraging. Baby Mckenzie that spent less than rehabilitation period, the animals were fed from a screened fence 25% of its activity time feeding/foraging, 71.2% of its total by animal careers that did not have any contact with the animals. time was engaged in resting. No individual spent more Food was spread out all round the enclosure so as to encourage the animals to forage. 60% of the food was spread out at night or than 25% of its activities vocalizing. As concerns loco- very early in the morning and the troop would only discover food as motion, Baby Jane was the only individual that spent 30% they forage along their paths. The food provided to the troop was of its time moving round the enclosure. They were two void of any foodstuff they would find in the wild or nearby farms like individuals (Baby Jane and Baby Malinga) that did not tubers, corn, bananas and other fruits; it involves mostly wild fruits engage in any other activity apart from feeding/foraging, and leaves. This was to limit human wildlife conflicts. In order to build up their body weights, each individual was entitled to half a resting, locomotion and vocalization. chicken each week and three eggs weekly. The animals were fed on a carefully planned workable random calendar and not on a fixed timetable as it were previously done where they fed daily at Social behavior 8.30 and 17.00 h. It’s also worth noting here that there was no data collection during and one hour after they have been provided with any foodstuff. Information on social behavior was recorded as “other behaviour” and these information included grooming, playing, copulation and agonistic behavior. Lucky had the Data analysis highest social behavior (17.13%) and was involved most In order to determine whether the individuals were behaviorally in grooming with Yari and Magda. The alpha males all ready for release, we compared the average percent of observation copulated with the alpha females, Buddy copulated most Ebua et al. 163

Table 1. Summary of an evaluation of behavioural criteria for pre-release observations.

Proximity Predatory and group Sexually Good Appropriate Appropriate Appropriate Criteria Human response cohesion for mature health and foraging/feeding rest locomotory Individual avoidance and territorial and physical behaviour behaviour behaviour avoidance defense and active conditions reproduction Buddy √ √ √ √ √ √ √ √ Juri √ √ √ √ √ √ √ √ Lucky √ √ √ √ √ √ √ √ Dedza √ √ √ √ √ √ √ √ Archie √ √ √ √ √ √ √ √ Mary √ √ √ √ √ √ √ √ Jane √ √ √ √ √ √ √ √ Mackenzie √ √ √ √ √ √ √ √ Malinga √ √ √ √ √ √ √ √ Mandy √ √ √ √ √ √ √ √ Magda √ √ √ √ √ √ √ √ Hastings √ √ √ √ √ √ × √ Chico √ √ × × × √ √ × Richard √ √ √ √ √ √ × √ Eddie √ √ √ √ √ √ √ √ Josua √ √ √ √ √ √ √ √ Baldwin √ √ √ √ √ √ × √ Kiiko √ √ √ √ √ √ × √ Yari √ √ √ √ √ √ × √ Wingnut √ √ √ √ √ √ × √ Zilly √ √ √ √ √ √ × √ Secha √ √ √ √ √ √ × √ Baby Mary √ √ √ √ √ √ × √ Baby Jane √ √ √ √ √ √ × √ Baby √ √ √ √ √ √ × √ Malinga Baby √ √ √ √ √ √ × √ Mandy Jane’s √ √ √ × × √ × × Baby Baby √ √ √ × × × × × Mackenzie Nam-Nam o o o o o o o o Malinga's o o o o o o o o Baby Freedom o o o o o o o o

×= did not meet the criteria; √= Satisfied the criteria; o = not consider. Source: Author.

as the highest ranking alpha male while the others (Juri, dominance copulate the more with all the alpha females. Lucky and Dedza) copulated with the other alpha females Mounting (not copulation) was a behavior that was mostly through sneak copulation. Mckenzie was the most noticed amongst the low ranking males (Eddie, Kiiko, groomed and highly copulated female. Agonistic behaviour Josua and Yari). During the day, individuals spent at least typically involved a “Swat” or a quick grap. Most agonistic 3.5% of the total observation records engaged in allo- behavior resulted during copulation amongst the alpha grooming. However, they engaged in play behaviour for males and females, this behaviour was rampant during 2.5% of their time most especially the young ones and the estrus periods as it is a period to demonstrate the sub adults. Yari had 16% of its time engaged in dominance and hierarchy in the troop since the most grooming and playing with baby Mckenwie, Kiiko, Zilli and 164 Int. J. Biodivers. Conserv.

Josua. We did not observe any playing between the It was a common phenomenon that all the individuals adults males, between the adults females or between the grunted (vocalized) at any human spotted at a distance the adults males and female. Common playing bouts around the enclosure. They would climb up the trees and were between the sub adults and the young ones or vocalized and scan for any other human presence in the between the adults and the young ones. Dedwa and area. This was peculiar with strange or new faces. Malinga where the only adults that did not spent a lot of time engaged in social behaviour (3 and 1% respectively). Dedza was hardly observed in the enclosure because he Maintenance of proximity was always hiding from other adult males especially after an attempted fight between him and Buddy and Juri in Being a group of 31 individuals, the group spent the the tussle for hierarchy or dominance. majority of the observation records (83.49%) at a distance There was a siginificant increase in the troop’s social of between 1 m and 5 m (at least 1 m apart but rarely behaviour as the troop spent more time together spent time more than five meters away from our focal especially during the last 3 months of the rehabilitation individuals). However, the percent of observation records period (t-test, t=2.185, df=27, p=0.012). these individuals spent in actual contact was relatively low (11.97%). They also rarely were more than 5 m away from each other (4.54%) when we focused on our focal Stereotype behaviour individuals but yet there were instances of some Buddy, Juri, Lucky, Archie and Dedza spent a total of individuals being more than 20 m apart from the central 4.35% (21 h) of their observation records engaged in core. This was mostly displayed by Richard (4.69%) of its stereotype behaviour. The nature of their stereotype total observation records. behaviour consisted of repetitive masturbation and the Jane, Lucky, Dedza, Magda and Richard spent more licking of their sperms. Buddy and Juri spent 1.19% than 10% of their time actually in contact with some swinging on a substrates and branches followed by members of the troop. Jane was the highest individual bouncing up and down on top of the substrates and (with 19.5% of its total observation time being in direct branchiation. The onset of such behaviour typically contact with other individuals (sitting next to or touching occurred during feeding times. The highest fighting and each other) while Malinga and Josua had the lowest chasing was noticed most especially when the troop is (<2%) time spent in actual contact. being fed with eggs and chicken. The alpha males and Malinga and Baby Mandy were the only individuals females running round the whole enclosure picking up at recorded as not maintaining any measures of proximity least 40% of the eggs and pieces of chicken but this was above 5 min. Others like Joshua, Baldwin, Wingnut, Baby not considered stereotype behaviour. Mary, Baby Jane, Juri, Archie, Mary, Jane, Mckenzie and Pregnant and nursing females (Mandy, Mckenzie and Magda usually spent a negligible time of observation Malinga) had the lowest percent of stereotype behaviour (<1%) at a distance more than 5 m thus they were within of all the rehabilitated individuals. The most observed relatively close proximity of between one meter and five stereotype behaviour observed from these females was meters to one another. teeth scraping. However, it was a common phenomenon displayed by all the individuals especially during feeding Location in the enclosure and mostly by low ranking individuals when approached by a dominant member of the troop. Another common The result show that troop would occasionally forage for stereotype behaviour noticed was “leg presenting” to food at the lower levels (1-3 m) of the canopy (18.51%) humans. as well as coming down to the floor of the enclosure

(4.33%) but would rarely spent more than five minutes Human-directed behaviour there. The troop spent most of the observation records at a level greater than 3 meters above the ground (77.16%). Out of a total of 86,400 observation behavior in 5,184 Some of the individuals would often come down to the hfor 18 months, most of the individuals did not exhibit any lower levels of the enclosure not only to forage on tubers, human-directed behavior, affiliative or aggressive. Buddy grasses, seeds and insects but also to play and sit on the (alpha male) had two instances of human-directed floor of the enclosure. A majority of their time was spent behavior and it was an open mouth threat directed at me between the mid and upper levels (<3 m) of the enclosure when we passed through the screened fence to check (82.90%) why there was current failure in the pre-release In comparison, most of the individuals came to the floor enclosure. Each time an individual passed through the during feeding time, to drink, play and to forage when a screened fence to go round the release fence, the alpha food particle is spotted on the ground thus would spent a male would descend the trees and closely followed with minimal time on the floor. During foraging, an individual snatching teeth, body fur raised up and turning the head that spotted any food stuff would run down pick it up and at all corners. rush back to the upper or mid level to munch. Ebua et al. 165

Locomotion modes the baboons the opportunity to engage in forms of enrichment and stimulation from the natural environment Out of the 28 individuals rehabilitated, 26 of these individuals by foraging for leaves, fruits, seeds, tubers and small spent more than 54 percent of their observation records animals like insects. The difference in percentage of their brachiating with the exception of Lucky and secha whose observed time feeding/foraging between the rehabilitated primary mode of locomotion was climbing (67 and 50% and wild troops again is most likely due to the fact that respectively). During playing, most of them would pop up 1/3 of their food was provisioned for them and they do not and down on the branches but this was not considered as have to search for it. The issue of being confined to an branchiation but as jumping. Out of all the individuals, enclosure would explain the difference in percentages for none had more than 10 percent of walking bipedally. The the two groups. But all the individuals were observed lowest was Buddy (1%) because it primary mode of travel using appropriate foraging behavior and showed proper around the enclosures was brachaition (94%). feeding techniques. However, it should be noted that the yellow baboons spent 10.47% of their observed time traveling, or engaged in particular modes of locomotion at DISCUSSION different heights. This aspect was displaced with on a satisfactory note as most of the movement was through The objective of this study was to examine whether brachiation avoided the going to the ground before Rescued and Rehabilitation yellow baboons housed in a climbing the next tree thus to limit their encounter with release enclosure at the Lilongwe Wildlife Center have predators. developed the appropriate behavioural repertoire neces- The average percent of observation records that the sary to be reintroduced and survive in the wild. Results yellow baboons spent vocalizing was 9.05%. This is are interpreted based on other comparative studies of considerably lower than wild troops that spent approxi- behavioural and ecological characteristics of wild yellow mately 13.3% of the observed time vocalizing; both male baboons. We first discuss the general behavioural patterns and female yellow baboons will attempt to defend their observed, and we further discuss and interpret my territories by engaging in physical displays and vocali- observations with particular regards to social behavior, zing. Therefore, the wild troops’ higher rate of vocalizing stereotypic and human-directed behaviour, maintenance could be due to their engagement in vocal territorial of proximity, location in enclosure, and locomotion in disputes on a regular basis. While the rehabilitating troops more detail. We also debate how these captive yellow are in enclosures that are hidden amongst trees and not baboons responded during the predator awareness entirely visible to one another but are still relatively close training. Furthermore, we provide a discussion as to how to each other. It is possible that rehabilitating troop could the rescued and rehabilitated yellow baboons behave not vocalize in the same social context as wild yellow compare to the criteria recommended. baboons (not needing to physically defend their territories from each other). Most of the vocalization was as a result

of other wildlife that came near their enclosure and some Behavioural patterns human influences like workers in at the Center. Mean-

while wild troops would often begin vocalizing upon All the yellow baboons in this study spent a small amount hearing other wild yellow baboons in the park vocalized. of the observation records resting (average 22.76%) and on a saved place. Most of the individuals were observed resting at positions higher than 5 m (upper level of the Social behaviour enclosure) which was in accord to the criteria developed as recommendations for a suitability in the wild and no Yellow Baboons have traditionally been believed to individual was found resting in a position easily reach by engage in very high affiliative social behaviour in predators. The low percentage of time resting (13.11%) comparison to other primates like gibbons (Smith, 2011). for wild yellow baboons seems more appropriate After an extensive review of field studies on yellow considering they spend more time foraging/feeding and baboons behaviour and ecology, Altmann (1974) con- locomotion. A relatively high percentage of time spent cluded that: “Yellow Baboons spend surprisingly a lot of resting by captive yellow baboons is likely unavoidable time socializing with one another. Mating takes up about considering the fact that these captive yellow baboons 4% of the activity period, grooming and social play are confined to their enclosures and have 1/3 of their usually more (20.3%) thus a total of 24.3 percent. Only food provided for them. When wild yellow baboons are the lack of social partners may contribute to any low not traveling through the forest, they tend to spend the levels of interaction”. The rates of social behavior majority of their time resting and feeding (pers.obs.). In observed in yellow baboons are dependent on the fact, the majority of time (42.77 %) observed for the number of available social partners, and since yellow captive yellow baboons was during foraging and feeding baboons live in larger family units, this could explain why which is similar to the wild yellow baboons observed in there are higher rates of social behavior observed in the Kasungu National Park (48.98%). This enclosure allows wild (pers.obs. Juvenile and subadult are primarily 166 Int. J. Biodivers. Conserv.

responsible for the majority of social behavior observed in their sperms, repetitive bouncing on a fixed substrate, wild troops, and for initiating social behavior with the repetitive brachiation, and less frequently, teeth scraping. adult. This social behavior linked to juveniles and sub- The baboons would most often engage in repetitive adults is similar to what was observed in gibbons by swinging or brachiation around feeding times and mostly Bartlett (2003). In a similar study carried out Cheney et the females exhibited a mild form of teeth scraping, al. (2004), she included juveniles and subadults in her usually upon my arrival for observations. The stereotypic study, which was potentially the reason why the gibbons behavior of masturbation and licking of sperms displayed at Kalaweit had a relatively higher average of time spent by the males of this captive yellow baboon have never in social behavior (8%) while Gibbons are known to have been reported in the wild. This would seem to suggest very low activity time in social behavior (Smith, 2011) that stereotypic behaviour could be caused by captivity, where wild Javan gibbons at had an average of 6.7 or at least exacerbated by captivity. We believed that percent observed time spent in social behavior. aspect of masturbation is a welfare effect due to lack of Regardless, the display of grooming, playing, and sufficient females in the troop for enough and constant copulation suggest a well bonded pair. Playing and copulation to be carried. Some researchers believe that grooming were the two most commonly observed beha- stereotypic behavior is a means of coping with a present viours. It was interesting to observe how the whole troop or past aversive situation (Mason, 1991; Mason and engaged in more social behaviour (play, grooming, and Berkson, 1975). Stereotypic behaviors become ingrained copulation). They also spent more time in close proximity in the behavioral repertoire of the animal and are and hundreds of instances of copulation were observed. probably the result of poor rearing conditions from when Close-proximity (within one meter), or “sitting together”, they were kept as pets, or can develop in any captive without allogrooming or copulating, was considered to be animal as the result of a stressful environment (Mason, one of the primary social interactions of adult yellow 1991). The most dangerous form of stereotype baboons (pers. Obs.). The increase in social behaviour behaviour was that of “leg presenting” to humans done by may have been due to the fact that there were not any two individuals (Hasting and Yari) which if they do the other baboons in the area and there was far less of a same in the wild, they would be easily trapped by human presence around the rehabilitating enclosure. poachers. Considering the fact that each yellow baboon Their overall behavioural profile would seem to indicate a included in this study exhibited a relatively low level of cohesive pair-bond, which will be beneficial for their harmless stereotypic behaviour, it is unlikely these survival in the wild. Wild yellow baboons will not neces- behaviors would persist once they are released or hinder sarily feed, forage, or even sleep in the same tree, but for their survival in any way and should not prevent an this study measuring how much time they spend in close individual from being reintroduced. proximity was useful for learning more about the nature of the pair-bond in captivity. For example, it was observed with other troop of yellow baboons at the centre (not Human-directed behavior included in this study) that would not even sit on the same side of the enclosure as one another. The males Human-directed behavior was relatively uncommon in the would chase any adult male that came close any all the individuals included in our study except a few. It resource. While the females would move around the was more common for Buddy (the alpha male) to exhibit enclosure more, engage in a physical display, consisting human-directed behavior than any other individual. of vigorously brachiating around the enclosure and Buddy had two instances of human-directed behaviour shaking substrates or the fence. The nature of this while the rest rarely exhibited any human-directed behaviour is not indicative of a cohesive pair-bond. behaviour. As part of the criteria for deeming a pair Considering the point that these captive yellow baboons suitable for release, we expected to observe very little did not meet the percent of total activity time engaged in human-directed behaviour from the yellow baboons. It social behavior by wild troops, they do show slightly could prove detrimental to the survivability of any similar results to other wild troops (~2-3%) in terms of individual if it was still domesticated and sought after social behaviour (Altmann, 1974), this study do not think human attention once released into the forest. All of the that the behavioural criteria of positive pair association as yellow baboons did not solicit grooming or petting. displayed by wild troops necessarily corresponds to pair- Hasting and Yari, on the other hand, had a comparatively bond cohesiveness for the captive yellow baboons. high rate of human-directed behaviour (Hasting: 9 instances/86,400 behavioral records; Yari: 34 instances/86,400 behavioural records) by running Stereotypic behavior towards any human who passed through the screened fence into the released enclosure and presented their The observed troop of captive yellow baboons did exhibit legs, a behaviour never observed with wild troop. This mild forms of stereotypic behavior. Most commonly particular behaviour could be explained by the type of observed was masturbation by the males and licking of individual who kept these two individuals as pets and the Ebua et al. 167

environment they were kept, thus could be some sort of a mimic their natural environment where they would be human habituated behaviour. This behavior has not been released in Kasungu national park. documented in the literature. In addition, if someone After these individuals were introduced into their approached their enclosure Buddy would typically enclosure, they all spent the whole day onto of the trees present a posterior display or behave in a display like and immediately developed the innate habits of spending manner by brachiating around the top of the enclosure, most of their time on the canopy and not the ground as bouncing and shaking the substrates. We believe that the was the case while they were in their previous enclo- posterior display is a signal to conspecifics and could be sures. They only came down to the floor of their a result of fear, or anger followed by aggression. The enclosures to retrieve fallen food or forage, but rarely will “anger followed by aggression” behaviour was the most spend more than a few minutes there; typically grabbing common observed response from Buddy. While it was the food and then quickly climbing back up to the higher clear that humans were the focus of this behaviour, we level of the enclosure. This behaviour would seem to never had the opportunity to observe if yellow baboons indicate an innate desire for the yellow baboons to would also display this behaviour to conspecifics. The remain within a higher level of space. However, some of most directed conspecific anger or aggressive behaviour the individuals would often sit on the floor of the was chasing and fighting. One explanation for the enclosure to drinking. Resting and playing was only done aggressive behaviour is that the yellow baboons are in a clear area where their vision is at least 180 degrees. treating humans as potential threats, specifically when This is because we never observed any individual the behaviour is directed at the same sex human. resting, sitting or playing in tall grass. Juveniles also Altmann, 1974 states that aggressive or territorial appeared to be quite comfortable spending time in the behaviour in wild yellow baboons is almost always lower levels of the enclosure; they are seen intrasexual; males displace males and females displace climbing/swinging branches at lower levels. If captive females. The posterior display, in addition to other forms yellow baboons are to avoid predators and parasites of human-directed behavior, is most likely a construct of once they are released, they must be encouraged to captivity and of being in continuous close proximity to spend time at the higher levels of their enclosures and humans. The levels at which yellow baboons in captivity, must demonstrate a preferred use of the top of the who are also candidates for release, engage in forms of enclosure. All of the individuals rehabi-litated in this study aggressive human-directed behaviour should be met a satisfactory result (in percent of time spent at the monitored more closely and can potentially provide some upper level of their enclosure) to survive in the wild. insight in to how the yellow baboons will respond to humans once they are released (see discussion on post- release behavioral observation with regards to human- Locomotion directed behaviour). Primates that were former pets (human-raised) can sometimes be aggressive towards While studying wild troops of yellow baboons, we humans upon reaching sexual maturity and tend to direct observed that they cover approximately 60-68% of their this aggression at the same sex individual. territory by brachiation. Therefore, for a rehabilitation program, yellow baboons should be utilizing brachiation as their main mode of locomotion. Yellow baboons in Location in enclosure captivity often do not have the space in their enclosures to brachiate for long distances, which may also explain Yellow baboons are canopy occupant and professional at why some individuals engage in stereotypic forms of feeding from the terminal branches and seeds of the tall repetitive brachiation. However, in order for rehabilitated trees. They make use of their home range three-dimen- yellow baboons to be suitable for release, they must sionally in space, as they exploit the canopy upwards and demonstrate they are capable of effectively traveling downwards to about 8th m above the ground. Wild yellow around their enclosure while utilizing natural locomotive baboons rarely come to the ground due to higher risk of movements as are observed in wild troops. predation, though captive-raised individuals are very The captive yellow baboons being rehabilitated are comfortable spending time on the ground and will walk on somewhat restricted with the size limitation of their the ground bipedally. Yellow baboons from the illegal pet enclosures, but are still capable of acquiring the trade were removed from the wild as infants or adults and appropriate forms of locomotion and utilizing them within most likely never had the opportunity to learn valuable their enclosure. All individuals in this study demonstrated predator avoidance behaviours from their parents. their ability to effectively locomote, and utilized Furthermore, they probably were kept in small cages brachiation as their primary mode of locomotion with the relatively low to the ground, if not actually on the ground, exception of Lucky and Secha whose primary mode of hence never being able to spend time at a higher level. locomotion was climbing (67 and 50% respectively). With This explains why during the rehabilitation process, an regards to walking, none had above 10% by bipedally. area full of tall trees with many branches was selected to Buddy had a high level mode of stereotypic brachiation 168 Int. J. Biodivers. Conserv.

thus why his primary mode of locomotion was 94% of spending at least fifteen percent of their time engaged in brachiation, though at times it was difficult to ascertain positive pair association (that groom, play, copulation), between simply traveling around the enclosure and when with at least five percent of total activity time spent it became “stereotypic.” Therefore, there could be a allogrooming. Most of the individuals in this study discrepancy in the data between the levels of stereotypic satisfied these criteria with the exception of few that were behavior and brachiation displayed by Buddy. However, often seen isolated from the group. However, the criteria what is important is that they are capable of effectively as proposed acknowledge that one of the primary forms brachiating and if they are going to be released into the of social interaction for adult yellow baboons is “sitting wild, they would be able to successfully traverse through together” within close proximity (within 1 m) thus it is the canopy. included as a positive association behaviour. All individuals in this study met the suggested requirement of observation records in close proximity, we would suggest Evaluation of behavioral criteria that including the maintenance of close proximity in positive association behaviour category as part of the Based on the research we conducted with wild troops of necessary criteria for rehabilitated programmes is a factor yellow baboons during a habitat assessment to determine that determines the cohesiveness existing with the group. its quality as a suitable release site for yellow baboons, The guidelines also state that the individuals should be we collected data on some non-habituated wild troops of copulating successfully and each individual should be yellow baboons and then developed a “Behavioural able to initiate copulation with the other. All the adult Cheklist” for yellow baboons in our rehabilitation program males and females were at one time observed initiating (Table 1). We highlighted important behavioural aspects or displaying copulation. However, this was not taken into of wild yellow baboons that a rehabilitated troop of yellow consideration when it came to the juveniles and some baboons should master before they are released. We subadults but we took keen interest to see if all then evaluated the rehabilitating group of yellow baboons individuals would at least display behaviour of copulation. based on these criteria to determine which individuals When it came to the juveniles, any behaviour of attempted met these criteria to be suitable for reintroduction. mounting both for females and males was considered as The first recommendation is that the yellow Baboons copulation but with reference to their ages. The breeding should be able to move around their enclosure efficiently individuals were observed copulating all the times and should be utilizing brachiation as their primary mode especially during the breeding season. This at times led of travel, then climbing as the second option and the least to a lot of fighting amongst the males and females. It is option to employ should be bipedally. Bipedally should necessary that yellow baboons in a rehabilitation program only be employed when drinking, foraging/feeding are observed copulating, via human observation or video because yellow baboons spent a great deal of time on camera, prior to their release, so that they do contribute the ground when foraging/feeding, moving in grassland to the wild population. areas because of no trees to brachiate. All of the yellow In general, the yellow baboons in this study showed baboons in this study, except a few, satisfied this similar models of behaviour with regards to the activity requirement. Considering it is crucial that yellow baboons budgets of wild troops of yellow baboons. The ways in in the wild are able to effectively traverse through the which they differ were most likely due to the captive forest using brachiation as their main form of travel, we environment. For example, the rehabilitating troop in this would say this is a necessary criterion that yellow study spent more time resting and less time baboons in the rehabilitation program should meet if they feeding/foraging than their wild counterparts, this is likely are to be considered for release. It is suggested that because wild troops do have to spend more time yellow baboons should spend no more than eight percent traveling to locate food source while the rehabilitating of their time on the ground level of their enclosure, and troop was provided with some food during the process. they should be at the upper level of their enclosure at We expected higher percent of resting in captive yellow least 35 percent of the time. All of the yellow baboons in baboons because they do not have the space to travel this study met this requirement. farther distances and they have their food provisioned. In Once released, if the yellow baboons are to avoid risk an ideal manner, yellow baboons in a rehabilitation of predation and survive in the wild, they must remain in program should exhibit similar behavioural patterns to the upper level of the canopy especially during rest or their wild conspecifics, while at the same point in time we sleep. Former pet yellow baboons may be very com- must concede the limitations placed on them as a result fortable spending time on the ground and if this behavior of a captive environment. is present during the rehabilitation program, it must be The guidelines state that yellow baboons in a eliminated prior to release. This requirement is a neces- rehabilitation program should not be exhibiting severe sary part of the rehabilitation procedure. According to stereotypic behavior (rocking or self harm). Considering data collected on wild troops of yellow baboons, we the nature of the stereotypic behaviour displayed by the recommend that a troop of yellow baboons should be yellow baboons in this study, we think it was not severe, Ebua et al. 169

we considered all individuals to have satisfied this cannot locate human primates like Chimpanzees, criterion. The primary stereotypic behavior observed was Gibbons, Gorillas, and Bonobos for bushmeat. The repetitive brachiation or swinging on a substrate, and it is rehabilitation and reintroduction of former pet and most unlikely that when the individuals are released these especially primates may play a significant role in the behaviours will continue; these behaviours are the result preservation of many of these threatened species. of a captive atmosphere. However, stereotypic behaviour However, it is crucial that the rehabilitation procedure is should be monitored during the rehabilitation program fully documented. This is the only way to establish a well- and depending on the nature of the behaviour, the formed rehabilitation/reintroduction program that adheres decision to deem an individual suitable for release can be to methodical guidelines and principles of rehabilitating assessed based on the severity of the behaviour. We yellow baboons and other primates. recommend that if a troop member exhibits severe stereotypic behaviour, it should not be released into the wild. Perhaps the individual would be more beneficial ACKNOWLEDGEMENT remaining at the centre and could be used for a captive breeding program, and then any future offspring may be We would like to thank the following for making this released into the wild. research a success: the Malawian Department of The rehabilitating troop in their pre-release enclosure National Park and Wildlife for their help, the people of had fruit, tubers, seeds, roots, insects and foliage and Kasungu for their hospitality, the Rangers of Kasungu they were also provisioned with some that were collected National Park for collaboration; Funding organizations: from the forest in the areas of Kasungu incorporated into the Born Free Foundation (BFF); Stichting AAP, the Tusk their diet. This was done so that the yellow baboons Trust; the United Nations Development Programme- would be accustomed to eating a more natural diet. It is Global Environment Fund (UNDP-GEF); Gesellschaft Fur important that any yellow baboon who is a candidate for Internationale (GIZ); the International Primate Protection reintroduction must show a preference for wild fruit and League (IPPL); and, the International Primate Society foliage before they are released. They must enjoy eating (IPS). We would like to thank all the staff of Lilongwe these sources of food and become familiar with them Wildlife Centre especially the care-takers, our families for visually, so that when they are living in the wild, they are their relentless efforts and for supporting our absence able to identify them in the canopy. during this study period. Most importantly, all great and Another aspect is that any individual to be released honour goes to the Almighty God for supplying our needs must be in good health and physically strong to avoid the according to his riches in Heaven. risk and susceptibility of zoonotic infections. 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