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African 13: 47-56 (2019)/ 47 Case Study:

Death of a Trapped Chimpanzee: Survival and Conservation of Great in Unprotected Agricultural Areas of

Marie Cibot1,2,3, Le Roux⁴, Jacqueline Rohen2, and Matthew R. McLennan1,2,5

1Department of Social Sciences, Faculty of Humanities and Social Sciences, Oxford Brookes University, Oxford, United Kingdom; 2Bulindi Chimpanzee and Community Project, Hoima, Uganda; 3Anicoon Vétérinaires, Ploemeur/ Larmor- Plage, France; 4Département de Pathologie Cellulaire et Tissulaire, Centre Hospitalier Universitaire d’Angers, Angers, France; 5Centre for Ecology and Conservation, University of Exeter, Cornwall, United Kingdom

Abstract: Rural, -dominated landscapes present substantial risks to chimpanzees and other primates. In western Uganda, some farmers guard against crop losses to wildlife by placing large steel leg-hold traps (‘mantraps’) near their agricultural fields. Chimpanzees ( troglodytes schweinfurthii) can step in these illegal devices, resulting in severe injury or death. Here, we report a case of trapping and subsequent death of a wild chimpanzee from the Bulindi community (Hoima District). The elderly female chimpanzee died 13 days after being injured by a mantrap. Her injury could have contributed to the cause of death by impacting her balance in low trees above a stream; her body was subsequently found in the water. Behavioural observations prior to death and evidence from physical inspection of her injured suggest she may have otherwise recovered from her injury. Together with previous reports of chimpanzee trappings regionally, this case underlines the urgent need for a dedicated conservation program to reduce risks of inhabiting unprotected agricultural areas for chimpanzees. We propose an integrated strategy including (1) increased presence of wildlife authorities outside protected areas, (2) strengthening of existing legislation prohibiting use of mantraps, (3) targeted education programs and media campaigns, (4) and increased engagement of local people in chimpanzee conservation.

KEY WORDS: ; crop protection; leg-hold traps; injury description; agriculture; anthropogenic landscapes; human–wildlife conflict

Résumé: Les environnements ruraux et anthropisés présentent des risques importants pour les chimpanzés et les autres espèces de primates. À l’ouest de l’Ouganda, certains agriculteurs préviennent le pillage de leurs cultures par la faune sauvage en plaçant de larges pièges à mâchoires à l’abord de leurs champs. Les chimpanzés (Pan troglodytes schweinfurthii) peuvent marcher sur ces dispositifs illégaux, entraînant de graves blessures aux individus et pouvant conduire à leur mort. Dans cette étude, nous rapportons le cas d’un piégeage et de la mort consécutive d’un chimpanzé de la communauté de Bulindi (District d’Hoima). La vieille femelle chimpanzé est morte 13 jours après avoir été blessée par un piège. Sa blessure pourrait avoir contribué à sa mort en entraînant une perte d’équilibre dans les arbres alors qu’elle était au-dessus d’une rivière, son corps ayant été retrouvé dans l’eau. Les observations comportementales avant sa mort et les lésions mises en évidence lors de l’inspection physique de sa main blessée suggèrent qu’elle aurait pu guérir de ses blessures. Nos données soulignent l’urgent besoin de mettre en place des programmes de conservation afin de réduire les risques pour les chimpanzés d’habiter des zones agricoles non protégées. Nous proposons une stratégie intégrative incluant (1) une augmentation de la présence des autorités de protection de la faune sauvage

Correspondence to: Marie Cibot, Department of Social Sciences, Faculty of Humanities and Social Sciences, Oxford Brookes University, Oxford, United Kingdom; Phone: +33 658056191; E-mail: [email protected]. 48 / Cibot et al.

hors des zones protégées, (2) un renforcement des lois existant sur l’interdiction de l’utilisation des pièges à mâchoires, (3) la mise en place de programmes d’éducation dédiés et de campagnes médiatiques, (4) et un renforcement de l’engagement des populations locales dans la conservation des chimpanzés.

INTRODUCTION

Across the tropics nonhuman primates The threat to chimpanzees from mantraps in increasingly inhabit modified environments Uganda, especially in farming areas in Hoima and dominated by agriculture (Estrada et al. 2012; Masindi districts, was highlighted in several previous McKinney 2015), especially outside of formally publications (Munn & Kalema 1999–2000; Waller protected areas. Among African great apes, & Reynolds 2001; Reynolds 2005; McLennan 2008; chimpanzees (Pan troglodytes) appear most resilient McLennan et al. 2012). For example, McLennan et to agricultural expansion and can persist in mosaic al. (2012) reported that at least five chimpanzees in habitats alongside rural farming communities Bulindi (representing ca. 20% of this small group) (Reynolds et al. 2003; Hockings & McLennan were trapped during 2007–2011. Despite this, little 2016; Garriga et al. 2018), owing in part to their concerted effort has been made to mitigate the propensity to integrate agricultural foods into their problem of chimpanzee trappings in agricultural diets (commonly termed ‘crop raiding’; Hockings habitats outside or at the edge of protected areas – & McLennan 2012; McLennan & Hockings 2014). besides direct interventions to treat victims once Rural, human-dominated landscapes present a trapping incident has occurred (see McLennan substantial risks to chimpanzees and other primates, et al. 2012). Here, we (i) report a new case of however. Risks include encounters with domestic trapping and subsequent death of an elderly female (Anderson 1986; Waters et al. 2017), power chimpanzee – a member of the long-term study lines (Moore et al. 2010; Katsis et al. 2018), roads group at Bulindi, and (ii) offer suggestions to reduce (Cibot et al. 2015; McLennan & Asiimwe 2016), exposure to pesticides (Krief et al. 2017) and novel pathogens (Parsons et al. 2015; McLennan et al. 2018), persecution or retaliatory (Paterson 2005; Hyeroba et al. 2011) and other crop protection methods (Osborn & Hill 2005; Warren 2008). The 1996 Uganda Wildlife Act prohibits the possession, sale or use of traps, snares, or ‘similar substance or device capable of killing, capturing or wounding any protected species’ (Government of Uganda 1996). Thus, steel leg hold traps (or ‘mantraps’) are illegal in Uganda. Nevertheless, in parts of western Uganda, it is not uncommon for farmers to use mantraps to protect crops from wildlife (Figure 1). As with snares, mantraps may also be used by hunters to procure wild game (Weeden 2016); however, unlike snares which are usually set within forests, mantraps are most often set by agricultural fields (Webber et al. 2007; Tumusiime et al. 2010; McLennan et al. 2012). Mantraps weigh 10–15 kg or more and are extremely strong. The parallel jaws are held open by a spring mechanism; when stepped in the jaws snap shut, entrapping the ’s limb firmly and causing severe injury or death. Traps are typically concealed beneath vegetation making them difficult to detect and avoid by . Mantraps are non-selective, Figure 1. Steel mantraps (encircled) openly on sale in an i.e., an animal is vulnerable to trapping regardless of ironmongers store at a market in Hoima Town (September whether it is the intended target or not. 2018). Photograph by J. Rohen. A Trapped Chimpanzee in an Unprotected Agricultural Landscape / 49

Figure 2. Map showing the location of Bulindi (encircled) in relation to the Budongo Forest Reserve in Masindi District (western Uganda) and the Bugoma Forest Reserve in Hoima District. Between these two government forest reserves is a network of unprotected, highly degraded riverine forest fragments surrounded by farmland and villages. These disappearing forest fragments support a sizeable population of 260–320 wild chimpanzees (McCarthy et al. 2015), including the Bulindi chimpanzee community. use of these inhumane and nonselective devices by the 1990s unprotected forest throughout Hoima farmers, to increase the welfare and conservation of and Masindi was converted to farmland (Mwavu & chimpanzees and other wildlife in rural landscapes Witkowski 2008). Despite this, 260–320 chimpanzees in Uganda. in at least nine resident groups (‘communities’) survive across this dynamic human-dominated landscape (McCarthy et al. 2015), including the METHODS Bulindi chimpanzee community. Additional chimpanzee populations occur in farming areas Bulindi (1°29’N, 31°28’E) is situated in Hoima further south (e.g., Kagadi and Kibaale districts). District, 25 km south of the nearest main forest At Bulindi, ca. 80% of forest was lost between block, Budongo Forest, in neighbouring Masindi 2006 and 2014 alone, shrinking the chimpanzees’ District (Figure 2). South of Budongo, the landscape home range, depleting wild food resources and is a mosaic of unprotected and degraded riverine reducing opportunities for female dispersal. In forest fragments amid farmland and villages. Since response, the chimpanzees’ use of farmland for 50 / Cibot et al.

travel and has increased (McLennan 2013). She had re-joined the group and presented a swollen While the local Banyoro people do not traditionally right hand with wounds visible on both sides: on the eat chimpanzees or other primates, chimpanzees medial side of the palm, a circumscribe lesion with at Bulindi – as elsewhere regionally – encounter an exteriorisation of flesh; and on the dorsal side, daily, often when foraging on agricultural an extended lesion which appeared more superficial crops, and associated ‘human–wildlife conflicts’ are (Figure 3a, b). Joyce walked slowly and tripedally, commonplace (McLennan 2008). stopping regularly to rest. Senior veterinarians Chimpanzees at Bulindi were first studied from Budongo Conservation Field Station and during 2006–8 (McLennan 2013). Since 2014 the Chimpanzee Sanctuary and Wildlife Conservation chimpanzees have been monitored continuously; in Trust were called to intervene. After observing March 2018 the Bulindi community comprised 21 Joyce, it was decided that she did not need to be chimpanzees. On 18 March 2018, a field assistant anesthetised, in part owing to her advanced age, but received a call from an unidentified person also because she was moving with the group, feeding, informing him that a chimpanzee had been caught and attending to her wounds, which were positive in a mantrap the day before (the exact location of signs. However, it was decided it would be beneficial the trap remains uncertain). The trapped individual to administer her antibiotics (by darting her from a was subsequently confirmed to be ‘Joyce’, an elderly distance of 5–7 m without anaesthesia) to counter adult female first identified in 2007 and estimated to any infection. Nevertheless, despite efforts over two be ca. 50–55 old in 2018. Researchers located days (23 and 24 March), the veterinary team could her on 23 March when she presented wounds on not get close enough to Joyce to dart her safely and her right hand that appeared consistent with a trap without other chimpanzees in close proximity. injury. The trap was not attached to her hand, but On 25 March, researchers could not find Joyce. how or when she was able to free herself is unknown. From 26 to 28 March, she was again observed Thereafter, maximum efforts were made to monitor travelling with other individuals, walking tripedally. Joyce daily and, where possible, throughout the Although her right hand remained swollen, she day. Veterinary clinical inspections were performed was observed using her right wrist to climb small including (i) monitoring the of the injury, trees to eat young leaves and cultivated jackfruit and (ii) looking for possible associated pathology (Artocarpus heterophyllus). She even transported of respiratory, digestive, urinary and locomotive a heavy jackfruit (weighing up to 20 kg) using her functions, in addition to (iii) behavioural indicators mouth, occasionally stabilising the fruit with her of ill health such as decreased appetite, lethargy, and injured hand, and walking tripedally or bipedally isolation from the rest of the group. (Figure 3c). Joyce often attended to her wounds by Joyce’s dead body was discovered on 30 March licking them and removing the whitish dead parts 2018. An external bodily examination, including with her teeth (Figure 3d). She was once observed dissection of the injured hand, was subsequently cleaning her wounds using leaves. On 29 and 30 performed on the same day. However, a full March, researchers located all the chimpanzees, necropsy was not conducted since researchers were except Joyce. Following a search, they discovered not fully equipped and incising the body to evaluate her dead body at 11:05 am on 30 March 2018, i.e., the internal organs carried a significant risk of ca. 13 days after she was injured. contamination (cf. Gilardi et al. 2015). Clinical and pathological observations RESULTS The carcass was found in a small stream, 2 m below a low, fresh night nest (Figure 4a). To access Behavioural observations this nest, a chimpanzee had to use a horizontal At 11:00 am on 19 March 2018, Joyce was branch of 12 cm diameter, while climbing above the observed in a small patch of forest resting in a low water. Joyce died in a huddled posture with half her nest. As an old female who often spent long periods in face submerged in water. Her body appeared fresh. nests, researchers were not initially concerned about She was found holding a dry and broken branch her and, unfortunately, did not wait for her to leave (Macaranga schweinfurthii) with her healthy left the nest or attempt to assess her physical condition. hand (Figure 4b). The second half of this dry branch Between 20 and 22 March, Joyce was not observed was discovered floating 1 m from her. Extraction of with other community members. On 23 March, the body from the water and physical inspection was researchers discovered that Joyce was evidently the performed on the same day at 17:00 pm, directly at chimpanzee reportedly trapped ca. 6 days previously. the site. A Trapped Chimpanzee in an Unprotected Agricultural Landscape / 51

a. b.

c. d.

Figure 3. Images of Joyce taken between 23rd and 27th March 2018, 6–10 days after she was injured by a mantrap: a) Joyce presenting a swollen right hand and walking tripedally; b) wound visible on palm of her right hand probably caused by a of the trap; c) Joyce walking bipedally and transporting a large, heavy jackfruit (Artocarpus heterophyllus) using her teeth. At times, she supported the fruit using the wrist of her injured right hand; d) Joyce licking the lesion on the back of her hand. Photographs by J. Rohen (b & d) and M. Cibot (a & c).

External body examination up to the metacarpo-phalangeal joints, and (2) a No anomaly was noted on the external body, circumscribe wound (2x2x2 cm) on the medial side except for the injured right hand (see below). All of the palm of the hand (likely the former place of teeth were present and appeared worn, as expected one tooth of the trap) (Figure 5b, c). These lesions in an aged chimpanzee. While the buccal mucosa were semi-recent, largely damaged with loss of appeared pale on the gums close to the teeth, the rest substances, and with ulcerative and fibrino-necrotic of the mucosa was pink, with an inflammatory area tissue at the bottom of the wounds. The edges of the (ca. 2 cm x 1 cm) on the right side of the upper jaw wounds were contused on the back of the hand but (Figure 5a). Joyce also presented signs of bilateral sharp on the palm of the hand. One finger suspensory cataract. ligament was visible (finger 4) (Figure 5b). After incision of the medial side of the hand, we noticed Detailed description of the trapped hand that the metacarpus of the forefinger (finger 2) was Two major lesions were observed on either side broken and displaced (Figure 5d). No broken bones of the hand: (1) a large wound on the dorsal side were observed elsewhere. Tendons were present (7x5x2 cm) from the distal part of the 4 metacarpi and not affected, and no pus was noticed. Tissues 52 / Cibot et al.

Figure 4. a) Joyce’s dead body (encircled) discovered in a stream below a fresh nest; b) the body extracted from the water, with the left hand still holding a dry branch (indicated by arrow). Photographs by M. Cibot.

after falling into the stream. Indeed, it appears that she tried to get out of the water by grabbing hold of a branch, which unfortunately broke. We cannot explain the origin of the inflammatory patch in Joyce’s mouth but we could hypothesise that, when she was in the water, she attempted to grasp branches with her mouth and damaged her buccal mucosa. Her severe hand injury could have contributed to the cause of death by impacting her balance as she climbed in small trees above the water. In addition, her bilateral cataract could have impacted her ability to negotiate branches above the stream; this pathology may also have contributed to her failure to see the trap. Finally, since (1) Joyce had resumed travelling with the group, (2) ate, (3) provided care to a. her wounds, (4) used her injured hand to climb into small trees and to carry heavy food items, and since (5) the lesions showed signs of gradual healing, we could have expected her to recover from her injury had she not nested above water and fallen.

Anthropogenic threats to chimpanzee survival in unprotected areas Data from Bulindi indicate that human actions are a primary cause of mortality in this community b. of chimpanzees, and presumably in other ‘village chimpanzee’ communities regionally. All three confirmed deaths of independent chimpanzees at Bulindi since 2012 (when all community members were in the phase of regenerating and healing at the were identified) were human-caused, including edges of the lesions (Figure 5b, c). Some black spots the present trapping case (2018), the trapping of a were observed, but because of the extended period young adult male (2015), and the death of an adult spent in the water (likely up to 36 or 48 hours), we female (and her infant) in a vehicle collision in 2015 could not determine whether these were gangrenous (McLennan & Asiimwe 2016). A fourth individual necrosis or post-mortem putrefaction (Figure 5d). – a wide-ranging adult male who disappeared in The degloving lesions observed on fingers are linked 2014 – is suspected to have been killed by villagers to maceration in water (Figure 5b). There is no outside the community range (M.R. McLennan, doubt that these injuries resulted from a large steel unpublished data). Thus, long-term research at mantrap. Bulindi confirms the risks of inhabiting unprotected agricultural areas for chimpanzees. DISCUSSION Mantraps are not a problem at Bulindi only: evidence indicates they pose a threat to chimpanzee Cause of death conservation regionally (i.e., cases have been Since an examination of internal organs was reported from multiple agricultural areas in Hoima not performed, it is impossible to determine the and Masindi districts; McLennan et al. 2012). exact cause of death. However, Joyce may have died Mantraps are most often set to trap animals regarded either from exhaustion, coldness, and/or drowning as agricultural pests including other primates (Papio A Trapped Chimpanzee in an Unprotected Agricultural Landscape / 53

a.

c.

d. b.

Figure 5. Physical examination: a) Worn teeth and an inflammatory patch on right side of upper jaw; b) wound on back of right hand; c) wound on palm of right hand; d) the back of the hand after incision. Photographs by M. Cibot.

anubis, Colobus guereza and tantalus) Recommendations for a targeted strategy to and wild pigs (Potamochoerus sp.). Although most outlaw use of mantraps in agricultural areas of chimpanzee trappings are probably unintentional, Uganda some farmers also consider chimpanzees serious To effectively address the problem of mantraps pests, especially of jackfruit and commercial crops in agricultural areas of Uganda, we propose an such as sugarcane and cocoa (Reynolds et al. integrated strategy including (1) increased presence 2003; McLennan & Hill 2012). Thus, occasional of wildlife authorities outside protected areas, (2) deliberate trapping of chimpanzees likely occurs. strengthening of existing legislation prohibiting use Many chimpanzee trappings in rural areas probably of mantraps, (3) targeted education programs and go unreported; as noted by McLennan et al. (2012) media campaigns, (4) and increased engagement of cases at Bulindi are known primarily because the local people in chimpanzee conservation. chimpanzees there are subjects of long-term research Conservation conflicts associated with and monitoring, increasing both the likelihood chimpanzees are widespread in village areas in that local persons will report a trapping and the Hoima and Masindi districts (Reynolds et al. 2003; likelihood that researchers or other concerned McLennan 2008; McLennan & Hill 2012). The individuals will discover an injured chimpanzee. Uganda Wildlife Authority (UWA) is mandated 54 / Cibot et al.

to conserve wildlife outside as well as inside throughout Hoima and Masindi districts suffer protected areas. However, chimpanzee conservation from chimpanzees eating their crops (McLennan programs including conflict mitigation outside 2008; McLennan & Hill 2012), which generates protected areas are currently implemented mostly anger and resentment towards chimpanzees and by nongovernment organisations. Thus, greater those organisations involved in their conservation. allocation of resources to enable UWA to protect Meetings and programs need to be set up to support chimpanzees and other wildlife and mitigate farmers and help them develop and improve the conflicts in agricultural areas is recommended, effectiveness of non-lethal crop protection methods similar to the dedicated anti-poaching programs and (including systematic evaluation of techniques; e.g., snare removal patrols implemented in partnership Hill & Wallace 2012; O’Brien & Hill 2018). These with research and conservation organisations within methods must integrate local people’s knowledge government managed protected areas (i.e., Kibale and be conducive to their own needs. National Park: Wrangham & Mugume 2000; Kalinzu These actions require involvement of government Forest Reserve: Hashimoto et al. 2007; Budongo agencies at the district level and increased Forest Reserve: Babweteera et al. 2008). coordination between them and nongovernment Mantraps are illegal in Uganda (Government of organisations. The programs proposed here are Uganda 1996). Nevertheless, the law is unenforced essential for the sustainability of a strategy to outlaw and mantraps are sold openly in markets regionally the use of mantraps by farmers, but will require large (Figure 1). Strengthening existing legislation funds given the wide area of farmer–chimpanzee to outlaw the use of mantraps including their coexistence, i.e. >1200 km2 in Hoima and Masindi manufacture, possession, transport and sale at a districts alone (McCarthy et al. 2015, 2018), with national level is thus urgently needed; clearly, for further chimpanzee populations known to occur legislation to act as an effective deterrent, violations outside of protected areas in additional farming must be punishable by heavy fines or prosecution. districts to the south (e.g., Kibaale and Kagadi Targeted conservation education programs for districts). local schools and villages where farmers interact daily with chimpanzees are vital. Media including ACKNOWLEDGMENTS photographs and video should be utilised to promote understanding of chimpanzee behaviour Research at Bulindi was approved by the Uganda and encourage towards them. Local National Council for Science and , people are traditionally tolerant of chimpanzees the President’s Office, and the Uganda Wildlife (McLennan & Hill 2012), and most residents Authority. We thank the veterinarian doctors Dr. consider that killing and wounding chimpanzees is Caroline Asiimwe (Budongo Conservation Field unacceptable (M.R. McLennan, unpublished data). Station) and Dr. Joshua Rukundo (Chimpanzee Therefore, conservation education can utilise this Sanctuary and Wildlife Conservation Trust), and traditional tolerance to increase awareness about the their teams, for support and assistance on 23 and suffering inflicted by mantraps. Education outreach 24 March. We thank Patrick Baruzaliire and Moses should be implemented in partnership with Aganyira for help trying to locate Joyce on 19 March. scientists, educators and local administrators, and We are grateful to Tom Sabitii for his long-term evaluated carefully to assess impact and potential monitoring of the chimpanzees in Bulindi. Finally, changes in attitudes and behaviour (e.g., Kuhar et we thank Moses Ssemahunge, Georgia Lorenti, al., 2010). Additionally, a dedicated media campaign Benjamin Hintz, Alastair Bigger, Vicent Kiiza and involving programs and announcements on local Lorian Mutegeki for help during the autopsy and radio (widely listened to by farmers in western of Joyce on 30 March 2018. Uganda) and articles in national newspapers would raise awareness substantially regarding legislation REFERENCES surrounding use of traps and their impact on chimpanzee welfare and conservation. Anderson, J.R. 1986. Encounters between domestic This proposed strategy must involve local dogs and free-ranging non-human primates. people as partners in proposing and integrating Applied Animal Behaviour Science 15(1): 71-86. solutions. Indeed, as indicated above, while use of Babweteera, F., V. Reynolds & K. Zuberbühler. 2008. traps is not uncommon regionally, only a very small Conservation and research in the Budongo Forest minority of farmers actually use mantraps to target Reserve, Masindi District, western Uganda. In chimpanzees. However, a large number of farmers Science and Conservation in African Forests: The A Trapped Chimpanzee in an Unprotected Agricultural Landscape / 55

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