AFRICAN PRIMATES the Journal of the Africa Section of the IUCN SSC Primate Specialist Group

Volume 10 2015 ISSN 1093-8966 AFRICAN PRIMATES The Journal of the Africa Section of the IUCN SSC Primate Specialist Group

Editor-in-Chief: Janette Wallis

PSG Chairman: Russell A. Mittermeier PSG Deputy Chair: Anthony B. Rylands Red List Authorities: Sanjay Molur, Christoph Schwitzer, and Liz Williamson African Primates The Journal of the Africa Section of the IUCN SSC Primate Specialist Group ISSN 1093-8966

African Primates Editorial Board IUCN/SSC Primate Specialist Group Chairman: Russell A. Mittermeier Janette Wallis – Editor-in-Chief Deputy Chair: Anthony B. Rylands University of Oklahoma, Norman, OK USA Vice Chair, Section on Great Apes:Liz MacFie Deputy Vice Chair, Section on Great Apes: Serge Wich Simon Bearder Vice-Chair, Section on Small Apes: Benjamin M. Rawson Oxford Brookes University, Oxford, UK R. Patrick Boundja Regional Vice-Chairs – Neotropics Mesoamerica: Liliana Cortés-Ortiz Wildlife Conservation Society, Congo; Univ of Mass, USA Andean Countries: Erwin Palacios and Eckhard W. Heymann Edem A. Eniang Brazil and the Guianas: M. Cecília M. Kierulff, Fabiano Rodrigues Biodiversity Preservation Center, Calabar, Nigeria de Melo, and Maurício Talebi Colin Groves Regional Vice Chairs – Africa Australian National University, Canberra, Australia W. Scott McGraw, David N. M. Mbora, and Janette Wallis Michael A. Huffman Kyoto University, Inuyama, Japan Regional Vice Chairs – Madagascar Lynne A. Isbell Christoph Schwitzer and Jonah Ratsimbazafy University of California, Davis, CA USA Regional Vice Chairs – Asia Gladys Kalema-Zikusoka China: Long Yongcheng Conservation through Public Health, Kampala, Uganda South-east Asia/Indochina: Jatna Supriatna, Christian Roos, Shadrack Kamenya Benjamin M. Rawson, and Ramesh Boonratana South Asia: Sally Walker and Sanjay Molur Jane Goodall Institute-Tanzania, Kigoma, Tanzania Inza Kone Red List Authorities Université Félix Houphouet Boigny, Abidjan, and Centre Sanjay Molur, Christoph Schwitzer, and Liz Williamson Suisse de Recherches Scientifiques en Côte d'Ivoire Joanna E. Lambert University of Colorado, Boulder, CO USA David N. M. Mbora Whittier College, Whittier, CA USA William Olupot Nature and Livelihoods, Kampala, Uganda Shirley C. Strum This issue of African Primates was produced with the assistance of University of California, San Diego, CA USA a grant from The Margot Marsh Paul T. Telfer Biodiversity Foundation, through Wildlife Conservation Society, Brazzaville, Congo Conservation International’s Tharcisse Tukizintambara Primate Action Fund. Stony Brook University, Pretoria, South Africa Edward Wiafe Presbyterian University College, Akuapem, Ghana Dietmar Zinner German Primate Center, Göttingen, Germany

Layout, design, and copy-editing:Janette Wallis IUCN SSC logo: Stephen D. Nash, 2014 Front Cover: Young adult male Tantalus Monkey (Chlorocebus tantalus) in northeastern Nigeria. Photo by Janette Wallis Printed by: University of Oklahoma Printing Services African Primates online: All volumes of African Primates are available online at www.primate-sg.org/african_primates African Primates 10: 1-12 (2015)/ 1

Characterization of Nest Sites of Chimpanzees (Pan troglodytes schweinfurthii) in Kibira National Park, Burundi

Dismas Hakizimana1,2, Alain Hambuckers1, Fany Brotcorne1, and Marie-Claude Huynen1

1Primatology Research Group, Behavioral Biology Unit, University of Liège, Liège, Belgium 2Department of Biology, University of Burundi, Burundi

Abstract: Kibira National Park is the only site in Burundi that harbors a large number of chimpanzees (Pan troglodytes schweinfurthii). While information on factors influencing the selection of nest sites by chimpanzees is available for other locations of the species’ range, this information is lacking for Kibira National Park. This is mainly due to the political troubles that prevailed in the country from 1993 until 2007, making study there difficult. To better protect this chimpanzee population, it is crucial to survey nest sites to identify the tree species, physical characteristics of the trees and habitat type that chimpanzees preferentially use for nesting. Therefore, in this study, we investigated: 1) the tree species used by chimpanzees for building their nests; 2) nest tree availability in the study area; 3) whether chimpanzee selection of a nest tree is based on physical characteristics such as diameter at breast height, lowest branch height, tree size and crown height; and 4) whether chimpanzees choose their nest sites according to topography and canopy types. We collected data monthly along 16 transects of 3 km each, from September 2011 to February 2013 (18 months). However, data related to the measurements of nests and nest trees were collected for only the last 12 months, from March 2012 to February 2013. We identified tree species used for nesting, and measured physical characteristics of trees used as opposed to surrounding trees unused. The results showed that chimpanzees select certain tree species to build their nests. Among the 32 species of trees bearing nests, chimpanzees used 12 species significantly more frequently than expected and 11 species significantly less frequently than expected. In addition, trees bearing nests were significantly larger and taller than the surrounding trees and had higher lowest branch and bigger canopies.

Key words: chimpanzees, nest sites, nesting behavior, Kibira National Park, Pan troglodytes schweinfurthii

Résumé: Le Parc National de la Kibira est le seul site au Burundi qui abrite un grand nombre de chimpanzés (Pan troglodytes schweinfurthii). Alors que des informations sur les facteurs influençant le choix des sites de nidification par les chimpanzés sont disponibles dans les autres parties de leur aire de distribution, ces informations manquent pour le Parc National de la Kibira. Ceci s’explique principalement par les troubles politiques qu’a connus le pays depuis 1993 jusqu’en 2007. Afin de mieux protéger cette population de chimpanzés, il est intéressant de mener des études sur les sites de nidification pour identifier les espèces, les caractéristiques physiques des arbres et le type d’habitat que les chimpanzés considèrent de préférence pour la construction des nids. Au cours de cette étude, nous avons cherché à déterminer: 1) les espèces d’arbres les plus utilisées par les chimpanzés pour la construction de leurs nids; 2) la disponibilité de ces espèces d’arbres dans la zone d’étude; 3) si la sélection d’un arbre de nidification est basée sur ses caractéristiques physiques telles que le diamètre à hauteur de poitrine, la hauteur au-dessus du sol de la première branche, la taille de l’arbre et la hauteur de la couronne; 4) si les chimpanzés choisissent leurs sites de nidification en fonction de

Correspondence to: Dismas Kakizimana, Primatology Research Group, Behavioral Biology Unit, University of Liège, Liège, Belgium E-mail: [email protected]. 2 / Hakizimana et al.

la topographie et du type de canopée. Nous avons collecté les données mensuelles sur 16 transects de 3 km de long chacun, de septembre 2011 à février 2013 (18 mois). Toutefois, les données relatives aux mesures des nids et des arbres nids sont celles des 12 derniers mois, de mars 2012 à février 2013. Nous avons identifié les espèces d’arbres dans lesquelles les nids étaient construits, et nous avons mesuré les caractéristiques physiques de ces arbres ainsi que celles des arbres environnants non utilisés. Nos résultats montrent que les chimpanzés sélectionnent préférentiellement certaines espèces d’arbres pour la construction de leurs nids. Parmi les 32 espèces d’arbres porteurs de nids, ils ont utilisé 12 espèces significativement plus fréquemment qu’attendu et 11 espèces significativement moins fréquemment qu’attendu. De plus, les arbres porteurs de nids étaient significativement plus gros et plus hauts que les arbres environnants, leur première branche était plus élevée et leur couronne plus grande que celle des arbres environnants.

INTRODUCTION

Nesting behavior has been observed in the four Studies in Mount Assirik, Senegal (Baldwin types of nonhuman great apes: chimpanzee (Koops et al. 1981), in Kahuzi-Biega, DRC (Basabose & et al. 2007; Samson et al. 2013), bonobo (Mulavwa et Yamagiwa 2002), in Kalinzu, Uganda (Furuichi & al. 2010; Serckx et al. 2014), orangutan (Ancrenaz et Hashimoto 2004), in Ugalla, Tanzania (Hernandez- al. 2004; Prasetyo et al. 2009) and gorilla (Mehlman Aguilar et al. 2013), in the Goualougo Triangle, & Doran 2002; Matthews & Matthews 2004; Sanz Republic of Congo (Sanz et al. 2007), in Bwindi, et al. 2007). The choice of a nest site, i.e., any Uganda (Stanford & O’Malley 2008) and in place containing one or more nests, is thought to Seringbara, Nimba Mountains, Republic of Guinea be influenced by several environmental factors, (Koops et al. 2012) showed that chimpanzees including: predation avoidance strategies that reduce selected particular tree species for nest construction. potential detection of the primates, decreased access Furthermore, other studies specified that nest tree of predators, improved early detection of danger species had particularly strong and elastic branches, (Anderson 1998; Kortlandt 1992; Pruetz et al. 2008), with small and abundant leaves (Goodall 1962; comfort and hygiene (Goodall 1962; Mackinnon Izawa & Itani 1966; Hernandez-Aguilar 2009). 1974; Anderson 1998; Nunn & Heymann 2005; The choice of nest sites by chimpanzees is thought Stewart et al. 2007), habitat types (Baldwin et al. to be based on safety concerns (Baldwin 1979; 1981; Basabose & Yamagiwa 2002; Furuichi & Kortlandt 1992; Hernandez-Aguilar 2009). Others Hashimoto 2004), and climatic conditions (Kappler noted that chimpanzees tend to prefer primary 1998; Koops et al. 2012). forest for nesting, which can relate to their use of In general, all weaned great apes build fresh nests ecological resources such as food availability (Tutin every night (Plumptre & Reynolds 1996; Rothman et & Fernandez 1984; Basabose & Yamagiwa 2002), or al. 2006), and occasionally during the day (Goodall to a thermoregulation function such as humidity 1962; Fruth & Hohmann 1994; Plumptre & Reynolds avoidance (Koops et al. 2012). 1997; Stanford & O’Malley 2008), while nest reuse We conducted a survey on chimpanzee nest sites is rare (Goodall 1962; Plumptre & Reynolds 1997; in Kibira National Park in Burundi. Prior to our Blom et al. 2001). If building nests aims at providing study, data on environmental factors influencing conditions favoring sleep (Stewart 2011), one nesting behavior of chimpanzees at this site were can hypothesize that fresh foliage provides more lacking. The park has been subject to many changes warmth and comfort, and that building a new nest over the past two decades. The rebels who occupied every day reduces the risk of predation by lowering the forest during the armed conflict (1994 – 2007) the probability of detection by predators (Nissen cut trees and extensively hunted large mammals. 1931). Mackinnon (1974) proposed that building a This occupation led to a deterioration of the new nest every night could also reduce ectoparasite habitat of the remnant chimpanzee population, exposure. Finally, Stewart (2011) and Koops et potentially causing changes in nesting behavior. It is al. (2012) proposed that fresh plants used in nest therefore important to provide information on the building may release chemical compounds repelling environment and the characteristics of the trees used insects or masking the odor of the ape, thereby by the chimpanzees in Kibira National Park, since it lowering the probability of detection by predators. could change in the future with forest recovery. Nest Sites of Chimpanzees in Kibira National Park / 3 Understanding which tree species are preferred 400 km² (FAO 2002). Indeed, in the 1970s, the for nest building and the type of habitat where nest Burundian government established a tea plantation sites are located can help in generating informed extension program. As the climate surrounding conservation plans about particular areas in the Kibira National Park is particularly suitable for tea park where chimpanzees occur. The first objective of cultivation, hundreds of square kilometers of the this study was to identify the tree species preferred forest were destroyed for the program. One portion by chimpanzees for nest building. As data on was reserved for tea plantations, and another available tree density in the chimpanzee habitat are reforested with exotic tree species (e.g., eucalyptus necessary to determine if chimpanzees choose nest and grevillea) to be used as fuel for processing tea trees randomly in relation to tree species abundance plants (Dennison et al. 1989). The remaining park (Stanford & O’Malley 2008), the second objective area is divided into four sectors, from south to north: was to assess nest tree species availability in the Teza, Musigati, Rwegura and Mabayi, covering study area. The third objective was to investigate 57.94 km2, 154.24 km2, 124.23 km2 and 63.59 km2, whether nest tree selection is based on physical tree respectively. characteristics such as diameter at breast height Kibira National Park is one of the two remaining (DBH), lowest branch height (LBH), total tree tropical highland forests in Burundi. It is located in height (TH) or crown height (CH). Finally, this the northwestern part of Burundi (Figure 1) on the study aimed to see if chimpanzees in Kibira National Congo-Nile Divide, between latitude 2°36’52’’ and Park showed preference for specific topography and 3°17’08’’ South and between longitude 29°13’31’’ canopy types. and 29°39’09’’ East. The altitude varies between 1,600 and 2,666 m (Arbonier 1996). Kibira National Park’s altitude gives it a temperate climate with an average yearly temperature of around 15°C. The METHODS temperature in the montane forest is relatively stable throughout the year ranging between 9 and 22°C Study Site although in some areas, particularly in the valleys, From 1933 to 1980, the Kibira forest was classified it may drop below 0°C (Trenchard, unpublished as a Forest Reserve. It was declared a National Park data). Relief, more marked on the western side, is in 1980. Initially, Kibira forest covered an area characterized by steep slopes on both sides of the of about 900 km², but this area is now reduced to Congo-Nile Divide.

Figure 1. Map of study site and distribution of observed chimpanzee nests. 4 / Hakizimana et al.

The forested zone receives the highest rainfall in the country with more than 2,000 mm per year. The rainy season occurs between September and May; November and April receive the heaviest rainfall. The main dry season is from June to August and a short dry season occurs in January and February. The diversity of the Kibira National Park biotopes, its primary forest relics, the richness of its fauna, and its hydrologic regulation role are of considerable importance for the country. The local human population does not yet fully appreciate the importance of the forest in this role, and promoting the awareness of its value should be a major component of any conservation program. Figure 2. A fresh chimpanzee nest in Kibira National Despite protection status, the surrounding human Park. Photograph by D. Hakizimana. population, living in great deprivation, still uses the forest for firewood and timber collection, clears changing color; c) old: all leaves dead but nest parcels of the forest for agriculture, poaches and still intact (Figure 2) hunts, all of which constitutes a significant threat for 2. Nest height (NH): measured from the ground at the remaining forest and wildlife. the base of the tree to the base of the nest, with a clinometer Data Collection and Analysis 3. Nest position within the crown: calculated by We studied nesting patterns of chimpanzees in dividing the distance between nest and lowest Kibira National Park for eighteen months, between branch by the height of crown: (1) bottom: 0 – September 2011 and February 2013. We used 16 0.33, (2) middle: 0.34 – 0.66, (3) top: 0.67 – 1.0 transects of 3 km each and running north-south, 4. Number of nests per tree: the total number at the most having been part of the only previous census end of our study study in the area (Barakabuye et al. 2007). As the park 5. Topography type recorded at a nest site: valley vs. was divided into 4 sectors (Teza, Musigati, Rwegura slope vs. hill top and Mabayi) (Figure 1), we chose 4 transects per 6. Forest type recorded at a nest site: open canopy sector, covering as much as possible all the habitat vs. closed canopy types present in the 4 sectors surveyed within the park. We travelled each transect 18 times (864 km in Nest Tree Selectivity total). All nests visible from transects and built since To assess the availability of nest tree species previous visits were recorded and marked in order to and preference by the chimpanzees, we conducted avoid counting the same nest twice. We recorded the regular vegetation surveys in nest sites and along the following variables for the nest trees and the nests 16 transects. We considered nests as being part of using an adaptation of the methods in Hernandez- the same nest group when the maximum distance Aguilar (2006, 2009) and Koops et al. (2012): between two nests of the same age did not exceed 20 m (Tutin & Fernandez 1984). We set up vegetation Nest Trees plots of 20 m radius around a nest or group of nests 1. Tree species (N = 118 nest sites or nest plots: NP), with the 2. Diameter at breast height (DBH): measured with nest as the middle point if isolated, and with the DBH tape measure central nest as the middle point in cases of groups 3. Total tree height (TH): measured from the of nests. We also established control plots (CP; N = ground to the top of the tree with a clinometer 256) of 20 m radius at 200 m intervals along the 16 4. Lowest branch height (LBH): measured from the transects which had no nests. Within all vegetation ground to the lowest branch, with a clinometer plots (NP and CP), we sampled all trees of DBH 5. Crown height (CH): calculated by subtracting ≥ 10 cm, assumed to be strong enough to support the height of the lowest branch from the total chimpanzees’ weight. height of the tree. To analyze preference for tree species, we compared the frequencies of species bearing nests in Nests NP with the frequencies of the same tree species in 1. Nest age (Tutin & Fernandez 1984): a) fresh: the CP using the chi-squared test of independence all leaves still green and fresh; b) recent: leaves and the analysis of standardized residuals (SR) for Nest Sites of Chimpanzees in Kibira National Park / 5 post-hoc comparisons (Sheskin 2004). When the RESULTS absolute value of SR is larger than 1.96, the observed frequency of the species is significantly different We recorded a total of 471 nests of chimpanzees from the expected value at a probability level of 0.05. at 118 nest sites throughout the study period. To analyze preferences of physical characteristics These nests were recorded in 365 trees belonging of the nest trees, we compared TH, DBH, LBH to 36 species, including four tree species (Grewia and CH of nest trees, with the mean values of the mildbraedii, Alchornea hirtella, Trema orientalis and surrounding trees without nests present in the same Croton megalocarpus) not recorded in the control NP. Since the assumption of normality, tested with plots. These four tree species accounted for 8.9% a Kolmogorov-Smirnov test, was rejected for all the (42/471) of all nests. Nest trees harbored a single variables, we used the Wilcoxon rank test for paired nest in 73.6% (N = 347) of the cases, two nests in samples for the mean comparisons (Sokal & Rohlf 23.4% (N = 110) and three or more nests in 3% (N 1995). = 14) of the cases. Finally, to test site selection for nesting, we compared the class frequencies of plot Nest Tree Species Preference characteristics between nest plots (2519 trees) and Chimpanzees used 32 of the 70 tree species control plots (6504 trees) using the chi-squared test recorded in the control plots for nesting. Selection of independence and the analysis of standardized of species as nest trees was statistically significant residuals for post-hoc comparisons. We tested the (χ2 = 1518.60, P < .0001, Figure 3). Chimpanzees effects of tree size (DBH classes in cm: 0 – 5; > 5 – used 12 tree species significantly more frequently 10, > 10 – 15, > 15 – 20, > 20 – 25, > 25 – 30, > 30), than expected: Parinari excelsa, Carapa grandiflora, local topography (hilltop vs. valley vs. slope) and Strombosia scheffleri, Ekebergia capensis, canopy type (open vs. closed). Beilschmiedia rwandensis, Aningeria adolfi-friderici,

Figure 3. Preferred and less preferred nest tree species – observed and expected frequencies and post-hoc tests. Crossed circles give the standardized residuals: when they fall outside the space delimited by the horizontal lines, the difference are significant at the 0.05 level; if they are over the lines, the species are preferred, below, they are less preferred. 6 / Hakizimana et al.

Ardisia kivuensis, Newtonia buchananii, Casearia runssorica, Ocotea michelsonii, Prunus africana and Strophanthus bequaertii. In contrast, 11 tree species, Macaranga kilimandscharica, Faurea saligna, Myrianthus holstii, Xymalos monospora, Alangium chinense, Polyscias fulva, Maytenus acuminata, Dracaena steudneri, Ficalhoa laurifolia, Neoboutonia macrocalyx and Tabernaemontana stapfiana, were used significantly less frequently than expected.

Physical Characteristics of Nest Trees and Nests Position The measurements presented here represent 341 nests recorded during the last 12 months of the Figure 4. Nest height classes in Kibira National Park. study, from March 2012 to February 2013. For nest trees with more than one nest, we measured only the lowest one, to save time on the task. Nest Site Selection The mean height of the 341 nests measured was Considering the DBH of all trees sampled along 12.11 m ± SD 5.8 m (range: 3 – 33.2). However, the transects and trees used for nest construction, fact that we measured only the lowest nest for nest chimpanzees built nests in trees with mean DBH trees bearing more than one nest may have led to between 30 and 50 cm more frequently than an underestimated nest height. Chimpanzees built expected based on availability (χ2 = 114.99, df = 13, P most of their nests (75.4%) between 5 m and 15 m < .0001; Figure 6). Chimpanzees preferred sites with above the ground, 19% of the nests between 15 and a closed canopy (56.1% of nests) to an open canopy 25 m, 9.4% at a height ≥ 25 m, and only 0.9% of nests (43.9% of nests) to build their nests (χ2 = 60.29, df at a height less than 5 m (Figure 4). In this study, we = 1, P < .0001; SR = 14.75 for close canopy and SR did not find any nests on the ground. = -11.67 for open canopy). The frequencies of nests Regarding the position of nests inside the tree located on slopes (77.3% of nests), hilltops (16.1% of crown, most nests (71.6%) were located in the nests) and valleys (6.6% of nests) were significantly middle third of the crown, 22.3% in the lower third, different (χ2 = 61.35, df = 2, P < .0001; SR = 20.48 and 6.2% at the top third. We noted that nests at the for slopes, SR = -12.55 for hilltops and SR = -6.16 top were built in small trees. The height of nests was for valleys). significantly correlated with tree height (r = 0.9648, df = 339, p = .00001) (Figure 5). In addition to their preference for certain tree species, chimpanzees also selected trees of specific size. Trees bearing DISCUSSION nests were significantly larger and taller than the surrounding trees and they had the highest lowest In Kibira National Park, chimpanzees were branches and the largest canopies (Table 1). selective in their choice of nest trees. This is well

Table 1. Means (± SD) of physical characteristics of nest trees (N = 341) with the mean values of the surrounding trees (N = 2,519): diameter at breast height (DBH), tree height (TH), lowest branch height (LBH), crow height (CH) and results of the Wilcoxon rank test for paired comparisons: W, sample sizes (N) and P values.

Surrounding Variables Nest Trees W N P Value Trees DBH (cm) 36.3 + 16.2 30.9 + 8 3.12 118 .0018 TH (m) 17 + 5 14.6 + 3.7 4.87. 118 < .0001 LBH (m) 7.8 + 3.1 6.6 + 1.9 3.61 118 .0003 CH (m) 9.2 + 2.3 8 + 2.1 4.64 118 < .0001 Nest Sites of Chimpanzees in Kibira National Park / 7

Figure 5. Relationship between nest height and tree height (r = 0.9648, df = 339, p = .00001). illustrated by data from Parinari excelsa, a tree species physical characteristics of the tree, and tree species, which occurred at a relatively low density (2 trees/ all influenced the pattern of nest tree selection in ha), but bore 15.5% of all nests. On the other hand, variable proportions. Macaranga kilimandscharica, the most abundant in Our results showed that chimpanzees in Kibira Kibira National Park (42 trees/ha), supported only National Park preferred to nest in trees with 9.6% of all nests. In agreement with previous studies physical characteristics that can potentially make (e.g., Hashimoto, 1995; Brownlow et al., 2001; Koops access difficult to predators able to climb. Nest trees et al., 2012; Hernandez-Aguilar et al., 2013), these had a significantly greater DBH and height, higher results indicate that chimpanzees do not randomly lowest branch height, and higher crown height than use tree species to build their nest. However, the the surrounding trees not used for nesting. These importance of factors influencing the choice of nest findings are in accordance with those reported tree species may vary according to the study site. At by Hernandez-Aguilar et al. (2013) for Ugalla, Kahuzi-Biega National Park (Democratic Republic who argued that such preferences supported the of Congo), Basabose & Yamagiwa (2002) reported hypothesis that elevated height of a sleeping place is that chimpanzees tend to build nests in fruiting a predator avoidance strategy. trees that they used as food sources. Similarly, Fruth Regarding the position of the nest within the & Hohmann (1996) found that bonobos at Lomako crown, Hernandez-Aguilar (2006) noted that, in (DRC) built nests close to fruiting trees. In Bwindi Ugalla, 17.8% of the nests were made at the top of Impenetrable National Park (Uganda), the choice of the crown, 45.4% in the middle and 36.8% at the nest tree species did not appear to strictly depend on bottom. Data from Seringbara, Nimba Mountains, their value as a food resource (Stanford & O’Malley, Republic of Guinea, showed similar results: most of 2008). The authors suggested that Cassipourea sp. the nests (50%) were built in the middle third of the and Drypetes gerrardii, two out of the four tree crown, 27% at the bottom and 23% at the top (Koops species preferred for nest building, may have been et al., 2012). Our findings in the Kibira National chosen because of their density. In Budongo Forest Park are in agreement with these, most nests being (Uganda), chimpanzees preferred to nest in trees made mainly in the middle segment of the crown. with small and dense foliage (Brownlow et al. 2001). The few nests atop the crown were built on trees Koops et al. (2012) showed that choice for specific smaller than the surrounding trees; this was also tree species could not be explained solely based on found by Goodall (1962) at Gombe National Park in physical properties. Finally, Furuichi & Hashimoto Tanzania. Ultimately, as the height of the nests was (2004) and Stanford & O’Malley (2008) reported that highly correlated with the height of the nest trees, combined factors such as fruit abundance, size and we can conclude that the choice of a place in the tree 8 / Hakizimana et al.

Figure 6. Preferred and less preferred classes of DBH in nest sites – observed and expected frequencies and post-hoc tests (crossed circles give the standardized residuals: when they fall outside the space delimited by the horizontal lines, the differences are significant at the 0.05 level; if they are over the lines, the classes are preferred, below, the classes are less preferred)

crown to build a nest is a compromise between the predators might be too recent in Kibira National Park constraints of the habitat (high trees are not always to have triggered a change in the nesting behavior, available) and the necessity to make the access to the or the continued presence of a human threat might nest as difficult as possible for predators. explain the subsistence of exclusive arboreal nesting. Chimpanzee nesting habits in the montane forest This behavior could also be related to the last of Kibira National Park are similar to those observed armed conflict in this region, which subjected large in other sites, particularly in Ugalla (Hernandez- mammals to heavy hunting pressure and ended in Aguilar et al. 2013). Data on both trees and nests are 2007. This assumption is supported by observations presented for comparison in Table 2. reported by Hicks (2010) on chimpanzees of Pruetz et al. (2008) suggested that if arboreal Democratic Republic of Congo, where nest height nesting by great apes evolved primarily to avoid increases with increasing human pressure. predation, release from predation pressure should Previous studies (Baldwin 1979; Furuichi & result in more frequent terrestrial nesting. In Kibira, Hashimoto 2004; Hernandez-Aguilar 2009) showed we did not see any evidence of potential predators, that nests most often occurred on slopes. The results except humans, during the 18 months of the study, from our study are congruent with these earlier yet all the nests we found were above the ground. reports. Several factors that might explain the Trenchard (unpublished data) indicated that selection of slopes for nest building by chimpanzees leopards, the main predator of chimpanzees, had have been proposed. Nishida (1989) argued that already disappeared from Kibira National Park. chimpanzees may prefer hilly terrain in Ugalla However, the disappearance of potential nonhuman because of the abundance of Brachystegia bussei, a Nest Sites of Chimpanzees in Kibira National Park / 9 . 1997 . 2007 . 2008 et al. 1983 al. et Reference Baldwin 1979 Anerson 1992 Wrogemann et al Furuichi Brownlow al. et 2001 Basabose & 2002 Yamagiwa et al Ogawa 2007 al. et Sanz Pruetz et al & Stanford 2008 O’Malley 2011; Koops Koops 2012 al. et Hernandez- 2013 al. et Aguilar study This 41 - 60 5 - 400 4.5 - 121.3 8.3 - 147.4 Range 21.9 19.3 SD DBH of Tree (cm) Tree of DBH 52 34.6 25 35.3 24.5 18.9 19.5 Mean Median Range 5.46 2 - 40 4.3 5.5 5 - 35 39.6 4.42 SD Tree Height (m) Height Tree 18 12.6 11.15 16.3 15 7.3 Mean Median 2 - 45 Range 5.16 2 - 40 14.22 3.2 5.1 3 - 307.4 19.8 4.13 SD Nest Height (m) Height Nest Mean Median11.3 11.7 12 10 12.5 12.1 9.8 13.4 17.3 8.33 16.06 1511.3 10.5 6.2 12.15 11.93 6.3 12.11 4.19 10.6 1.17 - 33.02 17.69 5.8 17.39 3 - 33.2 5.66 3.14 - 43.76 17 35.6 16 33.4 15.8 5 3 - 45.24 36.3 31 16.2 9.5 - 200 1 1 Savanna 2 1 1 1 2 1 2 2 1 1 1 2 Rainforest; Rainforest; Assirik Study Site Sapo Lope Petit Loango Budongo Kahuzi-biega Ugalla Goualougo Triangle Fongoli Bwindi Seringbara Issa Kibira 1 Table 2. Physical characteristics of nests and nest trees of chimpanzees in different study sites. study chimpanzees trees of nest and in different nests of characteristics 2. Physical Table 10 / Hakizimana et al.

tree species preferred for nesting, which happens Kibira National Park, we report only preliminary to grow in hilly areas. However, Baldwin (1979) information regarding the factors influencing nest reported that nests were more frequently built tree selectivity. This study provides initial results on slopes both in woodland and in gallery forest on nest tree choice by chimpanzees, but further despite the difference in vegetation composition, research needs to be done, for instance focusing on arguing that trees of these locations had similar phenological studies and fruit availability, on feeding characteristics. Hernandez-Aguilar (2009) proposed ecology and tree species consumed by chimpanzees, that an important factor leading chimpanzees to or on chemical characteristics of trees used for nest build nests on slopes may be a lower density of building. These and other characteristics, such as predators in these locations. In our study, we suggest quality and quantity of leaves and elasticity of the that chimpanzees choose slopes for safety reasons, branches, need to be assessed to better understand especially to keep a good view over wide areas and the factors influencing nest building by chimpanzees monitor for danger (e.g., Kortlandt 1992; Furuichi at Kibira National Park. & Hashimoto 2004). Even though we could not find any sign of chimpanzee predator presence, human ‘predation’ (poaching activity) still occurs in the ACKNOWLEDGEMENTS park. Most nest trees (73.6%) in our study area This work was supported by the Burundian carried only one nest (median = 1). This result is Government, the University of Liège, the similar to findings by Hernandez-Aguilar (2006), International Foundation for Science (IFS) and the who reported that the majority of trees (69.5%) Ecole Régionale Post-universitaire d’Aménagement had a single chimpanzee nest in Ugalla, western et de Gestion Intégrée des Forêts Tropicales Tanzania, and by Baldwin et al. (1981) in Rio (ERAIFT) via WBI program. We are grateful to Muni, in Equatorial Guinea. Baldwin et al. (1981), the following: E. Muhitira, E. Gabo, M. Niyonkuru, however, obtained a median of 2 nests per tree in M. Ndikuriyo and W. Bindariye, guards of Kibira Assirik (Senegal). They explained this difference National Park, for their help in data collection. by the lower availability of suitable nest trees in Finally, we would like to thank the anonymous Assirik, a drier site, in comparison with Rio Muni, reviewers and the Editor for their very constructive in Equatorial Guinea. As the Kibira National Park is and helpful comments on earlier versions of this a rainforest, the density of suitable trees for nesting manuscript. is high, which could explain the fact that most of the trees bore a single nest.

CONCLUSIONS LITERATURE CITED As in other sites surveyed, chimpanzees in Kibira National Park select particular tree Ancrenaz, M., R. Calaque & I. Lackman-Ancrenaz. species for nest building. Therefore, attention 2004. Orangutan nesting behavior in disturbed must be given to the conservation of the twelve forest of Sabah, Malaysia: implications for nest preferred tree species (Parinari excelsa, Carapa census. International Journal of Primatology 2: grandiflora, Strombosia scheffleri, Ekebergia capensis, 983-1000. Beilschmiedia rwandensis, Aningeria adolfi-friderici, Anderson, J.R., E.A. Williamson & J. Carter. 1983. Ardisia kivuensis, Newtonia buchananii, Casearia Chimpanzees of Sapo Forest, Liberia: density, runssorica, Ocotea michelsonii, Prunus africana and nests, tools and meat-eating. Primates 24: 594- Strophanthus bequaertii) in any management plan of 601. the Kibira National Park, because of the likely impact Anderson, J.R. 1998. Sleep, sleeping sites, and sleep- that changes in tree density may have for the long- related activities: awakening to their significance. term conservation of chimpanzees. This is illustrated American Journal of Primatology 46: 63-75 by Parinari excelsa, a tree species selected for nesting Arbonier, M. 1996. Parc National de la KIBIRA, by chimpanzees that occurred at a low density in the Plan de Gestion. Unpublished report to INECN, park, but is also overexploited for building materials, Burundi. firewood and charcoal production. Baldwin, P.J. 1979. The Natural History of the As the first survey on chimpanzee nest sites in Chimpanzee (Pan troglodytes verus), at Mt. Nest Sites of Chimpanzees in Kibira National Park / 11

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Seed Dispersal by the Tantalus Monkey, Chlorocebus tantalus: Implications for Forest Restoration and Expansion within an Afromontane Landscape in Nigeria

Abigail M. Grassham1, Britta K. Kunz2 , Stephen L. Goldson3, Musa Bawaro4, and Hazel M. Chapman1,4

1University of Canterbury, Christchurch, New Zealand; 2University of Siegen, Siegen, Germany; 3Bio-protection Research Centre, Lincoln University, New Zealand; 4Nigerian Montane Forest Project

Abstract: Although the frugivorous tantalus monkey (Chlorocebus tantalus Ogilby 1841) is widespread throughout much of Central and West Africa, its ecology remains largely unexplored. We therefore investigated aspects of the species’ ecology with a focus on seed dispersal in a Nigerian montane forest-grassland mosaic. We compared the results of our investigation with those of other studies on seed dispersal by cercopithecines. At our study site tantalus monkeys frequented both forest edge and grassland daily, spending an average of 6.5% (93.6 minutes) of the day in grassland and the remainder of the time in forest edge. Of the 164 tantalus monkey faecal samples obtained, 95.7% contained intact seeds. Faecal samples collected from the grassland contained significantly more seeds (median = 20) than faecal samples from the forest edge habitat (median = 4), however a greater proportion of the grassland seeds were small-sized (2-5 mm). Given this, an estimated 28.0 + 10.8 tantalus monkey individuals per km2 dispersed 356 and 124 seeds > 2 mm in diameter km-2 d-1 in the forest edge and grassland habitats, respectively.

Key words: Cercopithecine, forest regeneration, habitat loss, primates, seed dispersal

INTRODUCTION

Primates are an important guild of frugivores in considered to be poor seed dispersers because of tropical forests (Garber & Lambert 1998; Lambert & their tendency toward seed predation and/or seed Garber 1998), primarily because most disperse large spitting (Corlett & Lucas 1990; Lambert 1999). numbers of seeds (Lambert & Garber 1998; Link However, more recent evidence suggests that they & Di-Fiore 2006; Kunz & Linsenmair 2008) and in defecate large numbers of viable seeds (Lambert turn influence forest structure (Webb & Peart 2001; 2001; Kaplin & Lambert 2002; Gross-Camp & Wright et al. 2007; Nuñez-Iturri et al. 2008). Kaplin 2011; Albert et al. 2014) and that spitting One prominent group of frugivorous African can be advantageous for seedling recruitment (see primates are the cercopithecines, which are Albert et al. 2014 for a review, but see Dominy & characterised by the presence of cheek pouches and Duncan 2005). typically have long daily ranges and lengthy gut The tantalus monkey (Chlorocebus tantalus) retention times (Kaplin & Lambert 2002; Lambert is a medium-sized monkey (females = 4.1 kg, 2002). Historically, cercopithecines have been males = 5.5 kg; Figure 1) possessing several traits

Correspondence to: Hazel M. Chapman, Biological Sciences, University of Canterbury, Te Whare Wananga O Waitaha, Private Bag 4800, Christchurch 8140, New Zealand; Phone: +64 211064628; E-mail: [email protected]. 14 / Grassham et al.

with respect to their potential to move seed from the forest into degraded landscapes. Because spitting by tantalus monkeys was almost never observed in the grassland (Bawaro, pers. obs.) we decided to concentrate on endozoochory (the dispersal of seeds by animals after passage through the gut) and ask the following questions: 1. How do tantalus monkeys compare with other cercopithecines in their seed dispersal behaviour?; 2. Taking population density into consideration, how do seed dispersal rates compare to those of other cercopithecines?; 3. Do tantalus monkeys spend sufficient time in the grasslands to disperse significant quantities of seed into these degraded habitats?; and 4. what type of plant species are dispersed?

METHODS

Study Site We conducted our study at in the Ngel Nyaki Forest Reserve situated on the western escarpment of Figure 1. A tantalus monkey in a Ficus tree. Photograph the Mambilla Plateau (7°30’ N, 11°30’ E), Taraba State, by M. Walters. Nigeria, within the Cameroon Highlands ecoregion (Olson et al. 2001). This location comprises habitats ranging from intact submontane forest, forest edge, indicating that it is likely to be an effective seed riverine forest fragments and open grassland (Figure disperser with the potential to contribute to the 2). It is floristically diverse, being rich in endemic or restoration of Afrotropical forests. Its diet comprises near-endemic plant species (Chapman & Chapman approximately 50% fruit (Agmen et al. 2009) with 2001). The mean annual rainfall is approximately a gut retention time of approximately 30 h (Wallis 1800 mm p.a., most of which occurs between mid- et al. 2008), allowing the potential for seed dispersal April and mid-October (Nigerian Montane Forest via faeces. The species is semi-terrestrial, spending Project (NMFP) Weather Data). The forest reserve one-third of its time on the ground and visiting is subjected to frequent fires and cattle grazing. Of both forest and grassland habitats daily (Kavanagh the six primate species present, three (Cercopithecus 1980; Agmen et al. 2009; Grassham 2012), thereby nictitans (putty nose monkey), Ce. mona (mona enabling the potential for dispersal of forest seeds monkey), and Colobus guereza occidentalis (black into grassland areas. The tantalus monkey is also and white colobus monkey) are restricted to the relatively common with an IUCN rating of ‘least forest, while the other three, Pan troglodytes ellioti concern’ (Kingdon & Gippoliti 2008; Wallis 2013). (Nigerian/Cameroon chimpanzee), Papio anubis In spite of such characteristics and its widespread (olive baboon), and tantalus monkey venture into distribution throughout Central and West Africa the surrounding grassland areas. Of these latter (Kingdon & Gippoliti 2008), much of the seed three, the tantalus monkey is the most commonly dispersal ecology of tantalus monkeys remains observed at Ngel Nyaki (Agmen et al. 2009). under-studied (but see Agmen et al. 2009). It is For the purpose of this study, grassland is therefore important to learn more of its seed dispersal characterised as the area comprising over-grazed ecology, especially as the widespread decline in Sporobolus dominated tussock grassland interspersed forest primate species is now adversely affecting seed with very occasional savanna tree species and small dispersal services and plant recruitment throughout streamside forest remnants. Ngel Nyaki forest is tropical forests (Webb & Peart 2001; Wright et al. confined to the steep slopes of an ancient volcano 2007; Nuñez-Iturri et al. 2008; Markl et al. 2012; and much of the 5.2 square km of forest can be McConkey et al. 2012). considered as edge, which is approximately 200m The overall aim of this contribution was to wide (Aliyu et al. 2014) (Figure 2). Forest edge explore the ecology of tantalus monkeys, particularly habitat differs from forest core in as much as there Seed Dispersal by Tantalus Monkeys / 15

Figure 2. Map showing the field site with grassland and forest habitat, as well as the fenced-off grassland protected from burning and grazing. Not to scale. Map drawn by M. Walters, 2007. is evidence of past and/or current cattle presence from November 2008 until January 2009 and from in the edge and in comprising a high frequency of November 2009 until November 2010 to determine light demanding, pioneer species such as Bridelia the time spent in the forest, forest edge and grassland speciosa, Trema orientalis, and Psychotria succulenta habitats. relative to core forest. Light demanding forest species Upon locating a troop, two of us took scan such as Albizia gummifera, Anthonotha noldeae and samples (Altmann 1974) every 10 minutes. Scan Polyschius fulva are common in both core and edge. sampling was stopped after the troop was out of sight Occasionally shade loving forest core species such as for two consecutive scan samples. Our observations Pouteria altissima are found in forest edge habitat. were between 0700 and 1800 hours, during which The forest edge has a relatively open understory with time we recorded the number of individuals visible shrubs, herbs and vines including Clausena anisata in each of the forest and grassland habitats. and Aframomum angustifolium (Chapman et al. Usually the tantalus monkey troops disappeared 2010). The Sporobolus grassland is burnt annually into the forest undergrowth during the heat of the by the Fulani pastoralists to stimulate new grass day and/or at dusk and we never observed monkeys growth, but close to Ngel Nyaki forest large areas of between the hours of 1300 and 1500. After 1500 this grassland have been fenced off by the Nigerian hours, the troops had to be located again before Montane Forest Project to protect it from burning sampling could resume. In total our study comprises and grazing in order to encourage forest expansion data from a total of 2270 scans amounting to 378.3 into areas which historically are likely to have been hours of observations. We observed troops from a forested (Barnes & Chapman 2014). distance of between 20 to 50 m using binoculars to minimise disturbance and potentially altering their Data Collection behaviour.

Time spent in each habitat Density We observed three semi-habituated tantalus To estimate the density of tantalus monkeys in monkey troops (ranging in size from 16 to 38 the Ngel Nyaki Forest Reserve, we used distance individuals) approximately twice a week in the sampling (Buckland et al. 2001) and analysed the dry season and once a week in the rains along the data using the software DISTANCE 6.0 release 2 northern boundary of Ngel Nyaki Forest Reserve (Thomas et al. 2010). This involved walking along 16 / Grassham et al.

six line transects, 800 m apart set perpendicular Seed removal from the faecal samples in the wet- to the forest edge, providing a combined length laboratory was based on the methods of Kunz and of 4.69 km. These transects passed through forest, Linsenmair (2008). We formed a slurry from each forest edge and grassland areas and two observers sample that was then sieved through a 2 mm mesh. walked quietly at c. 1 – 1.5 km h-1 to avoid disturbing For comparison with other studies all trapped seeds any tantalus monkeys present. This procedure was > 2 mm in diameter were counted and identified repeated 18 times between December 2009 and where possible; seeds < 2mm were not considered. September 2010, with at least one walk a month. The Two millimetres has frequently been used in other total distance surveyed was 84.5 km. Throughout studies (Wrangham et al. 1994; Kaplin & Moermond each transect walk, we made regular pauses to scan 1998; Poulsen et al. 2001) as the point below which the surroundings for tantalus monkeys and thereby seeds were not counted due to difficulties in their minimise the chances of missing a troop in the vicinity. removal and counting. We identified seeds > 2 mm When one or more tantalus monkey individuals to species level when possible using the NMFP were observed, a GPS location was taken from a reference collection. Seed sizes were obtained from position on the transect that was perpendicular to Agmen et al. (2009), Chapman et al. (2010) and the animals’ location. At the same time an estimate Dutton and Chapman (2015). These values were was made of the distance to the centre of the troop means of n = 20 seeds per species. Seed sizes of and the number of individuals was noted along with species of seeds not included in any of these studies the date and time of observation. The same observer were measured with digital callipers to the nearest always made the estimate of distance to the centre of mm. the group to ensure consistency. Defecation Rate Seeds per faecal deposit In order to estimate the daily quantity of seeds We opportunistically collected faeces from across dispersed per monkey, it was necessary to estimate forest edge and grassland, the two habitats in which the defecation rate of tantalus monkeys and then we recorded tantalus monkeys, between October multiply this by the mean number of seeds per 2009 until January 2010 and again during April faecal deposit. As it is usually impractical to obtain 2010. These intervals coincided with those periods accurate data on defecation rates from primates of peak fruiting (NMFP unpublished phenological observed in the wild, captive individuals are often records) that occurred outside of the rainy season. used instead (e.g., Poulson et al. 2001; Lambert The avoidance of the wet season was necessary 2002). Thus, we used three captive tantalus monkey because under such conditions the samples were individuals (one adult male, one adult female and frequently washed away by the rain and any data one sub-adult female) to estimate tantalus monkey that we did collect would have been spurious. While defecation rates. The captive monkeys were part of concentrating on dry season data will have inevitably a (cancelled) release program (Wallis, pers. comm.) biased our results and altered interpretation and temporarily housed close to the NMFP field somewhat, nevertheless our dry season data provide station and were fed a diet of fruits and vegetables important information regarding seed dispersal by (bananas, pineapples, tomatoes, onions, carrots) as tantalus monkeys. During the collection intervals, well as locally-collected forest fruits of Aframomum we also recovered faecal samples from the sleeping angustifolium and Leea guineensis. While this diet sites of the three semi-habituated troops. We located did not completely reflect the feral diet, it was seen these sites by following a troop in the late afternoon to provide an adequate estimate of field defecation until it settled down for the night. The following rates. morning, we searched the ground and undergrowth Two of us observed the captive subject animals for faecal deposits which we uplifted with trowels for three consecutive days in November 2010, and placed into labelled polythene bags. The samples during which time records were kept of individual were relatively easy to locate and identify based on defecation events. their size and shape. Of the 164 tantalus monkey faecal samples collected, 129 were from the forest Statistical Analyses edge and 35 from the grassland areas. While we could not be completely certain that all our samples Time spent in each habitat were from tantalus monkeys, we never observed For ease of analysis, we grouped individual scan other primate species sharing sleeping sites with samples together into six two-hour time periods. them. We used a binomial generalised linear mixed model Seed Dispersal by Tantalus Monkeys / 17 Table 1. Mean and median values of the number of seeds collected per faeces from Chlorocebus tantalus in forest and grassland habitats. Q1 = first quartile and Q3 = the third quartile. Median Number Mean + SD Number Range of Seeds per Q1 - Q3 of Seeds per Faeces Faeces Total seeds 0 – 551 5 2 – 23.25 29.0 + 65.2 Forest total seeds 0 – 258 4 1 – 14 20.3 + 44.9 Forest small seeds 0 – 258 2 0 – 8 18.2 + 45.2 Forest medium seeds 0 – 54 0 0 – 2 2.1 + 5.8 Grassland total seeds 0 – 551 20 4 – 64.5 60.8 + 107 Grassland small seeds 0 – 551 19 2 – 64 59.5 + 106.8 Grassland medium seeds 0 – 9 0 0 – 1.5 1.3 + 2.3

(GLMM) to test for significance differences in the sizes among habitats and months. Overdispersion of proportion of time spent in the grassland versus data for seeds was accommodated by including an forest during each of the two hour time intervals. additional random factor at the observational level to Date was included as a random factor to account for create a Poisson-lognormal GLMM as suggested by a possible lack of independence of scans taken on Elston et al. (2001). We determined the significance the same day. Additionally, an observational level of a factor using a log-likelihood ratio test. random factor was included to account for overdispersion of the data. We used a log-likelihood ratio Difference in size of dispersed seed between habitats test (using the ANOVA function in R) to determine The seeds collected from faeces were placed into the significance of time of day on the proportion of one of two categories: small (2-5 mm) and medium time spent in the grassland. (5-20 mm), following Wrangham et al. (1994) and Kunz and Linsenmair (2008). Density of tantalus monkeys We used a binomial GLMM model to test if We used DISTANCE (Thomas et al. 2010) to the proportion of small seeds collected per deposit estimate the density of tantalus monkeys from the found in the forest and grassland habitats differed observational data collected along the transects. significantly. Habitat was included as a fixed factor, A half-normal detection function with cosine while month and an observational level factor were adjustment model (AIC = 103.53) provided an included as random factors. A log-likelihood ratio effective strip width of 33.8 m. test was used to test the significance of habitat.

Difference in the number of seeds per faecal deposit in Difference in the number of seeds dispersed into forest each habitat and grassland The number of seeds per faecal deposit were To estimate the seed dispersal rate into each not normally distributed, hence it was necessary to habitat, we used the following equation: calculate the median and 1st and 3rd quartiles, instead of mean and standard deviation. These values were S = Dsdt then used in subsequent calculations. However, we where, included the corresponding mean and standard deviation values in Table 1 to allow comparison with S = rate of seed dispersal by C. tantalus into a other studies. habitat We used only intact seed data and these were D = C. tantalus population density analysed using Poisson GLMMs to test for differences s = median number of seeds released per in the number of seeds per faecal deposit in the defecation in the habitat forest edge and grassland habitats. We included d = number of defecations per day month as a random factor to control for variation t = average proportion of time spent by C. among months. Data were entered whereby seeds in tantalus in the habitat per day each faecal deposit constituted one observation. This allowed the model to account for unequal sample 18 / Grassham et al.

Table 2. Species of seed collected from 164 Chlorocebus tantalus faeces at Ngel Nyaki Forest Reserve, with basic information.

Total Seeds Seed Size Species Family Habitata Life Form Collected (mm) Aframomum Zingiberaceae 2244 4.5 E Herb angustifolium (Hook.f) K. Schum. Species 2 1755 4 Leea guineensis G. Don Leeaceae 196 4.5 E, G Shrub Croton macrostachyus Euphorbiaceae 185 7 E, SF Tree Hochst ex Del. Species 1 77 3 Grewia sp. Tiliaceae 47 9 E Shrub Species 21 38 3 Species 9 35 2.5 Psychotria peduncularis Rubiaceae 27 5.5 (Salisb.) Steyerm Psychotria succulenta Rubiaceae 23 6 E Tree (Hiern) E.M.A. Petit Species 6 15 10 Liana Landolphia sp. Apocynaceae 9 12 F, E Liana Species 12 8 2.5 Species 14 8 10 Species 10 6 2.5 Syzygium guineense Myrtaceae 4 12 F, S Tree (Willd.) DC. Species 18 3 4 Species 5 2 4 Species 16 2 3 Species 7 1 7 Vitex doniana (Sweet) Verbenaceae 1 20 F, E, S Tree Pouteria altissima (A. Sapotaceae 1 19 F Tree Chev.) Baehni Synsepalum sp. Sapotaceae 1 15.5 Tree Bridelia speciosa Müll. Euphorbiaceae 1 8 E Tree Arg. a Abbreviations as follows: E = Forest edge; F = Forest; L = Light gaps; S = Savanna/Grassland; SF = Secondary forest

RESULTS in the grassland habitat, with the remainder of the Time in Each Habitat day spent in the forest edge. Across the two- hourly We found that the tantalus monkeys never intervals, tantalus monkey presence in the grassland ventured more than 100m into the forest, so that they varied significantly (χ2 = 68.75, df = 4, P < 0.0001) were confined to forest edge habitat. On average, showing peaks in the grassland between 0700 – 0900 the monkeys spent 6.5% of the day (93.6 minutes) hours and 1700 – 2100 hours. Seed Dispersal by Tantalus Monkeys / 19 Distance Analysis The estimated troop density of tantalus monkeys in this study was 2.1 + 0.8 per km2 and the average troop size was 13.3 + 1.8. The density of tantalus monkey individuals in the area was 28.0 + 10.8 per km2.

Numbers of Seeds Of the 164 tantalus monkey faecal samples we collected 84.1% contained at least one intact seed > 2 mm. Overall, the number of seeds found per faecal deposit was highly variable, ranging from zero to 551 (Table 1). The median number of seeds per faecal deposit differed significantly between habitats Figure 3. The proportion of small (2-5 mm) and medium (χ2 = 12.5, df = 1, P = 0.0004) with five times as many (5-20 mm) sized seeds in the forest edge and in the seeds in the grassland deposits as in the forest (Table grassland. 1). In total we recovered 4748 seeds and, irrespective of the habitat they were collected from, DISCUSSION a high proportion belonged to either the forest herb Aframomum angustifolium (47.3%) or an Our study highlights that the tantalus monkey unidentified seed species designated sp. 2 (40%). is a regular and potentially important disperser of The remaining 749 seeds comprised an additional seeds from a number of plant species across forest 22 species (Table 2). edge and into grassland areas in the degraded landscape of the study area. Size of Dispersed Seed Tantalus monkeys dispersed seeds up to 20 mm How Does C. tantalus Compare with Other long and 12 mm diameter, with the largest seed being Cercopithecines in Their Seed Dispersal from the forest tree Pouteria altissima. Small seeds Behaviour? were more abundant in faeces from both habitats We found that tantalus monkeys at Ngel Nyaki than medium seeds (Table 1), however the relative dispersed a median of five seeds and a mean of proportion of small seeds dispersed in grassland 29.0 ± 65.2 (SD) seeds per faecal deposit, which is faeces was significantly higher than in those from considerably more than the reported mean numbers the forest edge (χ2 = 6.64, df = 1, P = .010, Figure 3). of seeds dispersed by several other Cercopithecus spp. such as Cercopithecus mitis (blue monkeys) Seed Dispersal Rates and Lophocebus albigena albigena (grey cheeked Individual captive tantalus monkeys defecated mangabey) but slightly less than that of Cercopithecus 3.4 ± 1.5 times per day. The monkey spends an l’hoesti (L’Hoest’s monkey) and a mixed group of average 6.5% of its day in the grassland and 93.5% Cercopithecus spp. (Table 3). The tantalus rates in the forest edge. Assuming the defecation rate in were similar to the much larger olive baboon (Table each habitat is a function of the amount of time 3). Thus tantalus monkeys also appear to be a spent in these habitats, a tantalus monkey defecates quantitatively important disperser of seeds, at least 0.22 times per day in the grassland and 3.18 times in during the dry season when this study was carried the forest. An individual tantalus monkey therefore out. defecates an estimated 4.4 and 12.7 seeds per day in Tantalus monkeys dispersed seeds up to 12 x 20 the grassland and forest habitats, respectively. mm in size, which is among the larger sizes reported Using the estimated population density of 28 for most other cercopithecines (Albert et al. 2014) tantalus monkey individuals per km2, the mean daily although, as would be expected, this seed size is defecation rate in the forest and grassland and the smaller than what can be dispersed by baboons median number of seeds dispersed per defecation, (Table 3). Some cercopithecines have a very low we estimate that at Ngel Nyaki tantalus monkeys swallowing size threshold, e.g., Macaca fascicularis disperse 356 and 124 seeds km-2 d-1 for the forest (crab-eating macaque) and Ce. ascanius (red tailed edge and grassland habitats respectively. monkey) which typically swallow seeds up to only 4 mm in diameter (Corlett & Lucas 1990; Lambert 20 / Grassham et al. . 2001 . 2001 . 2001 . 2001 . 1990 Isbell etIsbell al & Kaplin 1998 Moermond et al Poulsen et al Poulsen et al Poulsen et al Poulsen Lambert 1999 1998 Moermond 1998 Moermond 2010 2008 Reference 20study This 4 6.86.8 & Kaplin & Kaplin 13.7942 2011 et al. Tsuji 27 & Waltert Astaras & Linsenmair Kunz Max SeedMax Size (mm) ) -1 d -2 129 Grassland: 124 Grassland: Population Seed Dispersal Rate (km ) 2 28 96 to Up 356 Forest: 14.724.6 73.5 10.3 258.3 19.7 77.3 158.6 130 Population Density (Indiviuals km per 29.0 + 65.2 = 5) (median Mean Number Seedsof per Faeces (> 2 mm) 8.58 + 19.58 2.33 + 1.45 6.43 + 8,27 1.0 + 1.9 2.1 + 3.4 1.5 + 2.9 1.6 + 26.4 54.7 60.0 69.0 37.3 28.2 + 70.5 = 7) (median 51.0 % Faeces Containing SeedsIntact > 2 mm seed dispersal ecology species. Cercopithecine with other 75 164 87.9 50 58 83 3070 33.7 55 402 42.8 396 N Faecal Samples Analyzed spp. Cercopithecus ascanius Cercopithecus pogonias mona Cercopithecus Mona monkey fuscataMacaca macaque Japanese Chlorocebus tantalus monkeyTantalus Cercopithecus aethiops monkey Green monkey tailed Red doggetti mitis Cercopithecus monkey blue Doggett’s Cercopithecus l’hoesti monkey L’Hoest’s Cercopithecus cephus cephus guenon Moustached Lophocebus albigena albigena Grey cheeked Mangabey leucophaeusMandrillus Drill Cercopithecus nictitans nictitans Cercopithecus nosed monkey Putty Papio anubis Olive baboon Species Table 3. Comparison of C. 3. Comparison of tantalus Table Seed Dispersal by Tantalus Monkeys / 21 1999). However, some cercopithecines can spit troops per km2 corresponding to 30 individuals per large seeds (e.g., Corlett & Lucas 1990; Lambert km2 can be calculated. While this troop density is 2001; Gross-Camp & Kaplin 2011) which may be less than the 2.1 per km2 measured in the Ngel Nyaki an important method of seed dispersal (see Albert Forest Reserve, the overall density of 30 individuals et al. 2014 and references within) but is unlikely per km2 is comparable to the 28 individuals per to result in the transfer of seeds across habitats. km2 found by Nakagawa (1999). Such density Irrespective, tantalus monkeys swallow and disperse estimates are greater than the reported densities via defecation seeds as large as those that other for many other cercopithecine populations (Table cercopithecines are likely to spit. In terms of moving 3). However, notable exceptions do occur; higher seeds of tree species into grassland however, seed population densities of red tailed monkeys have size is not important; it is the pioneer tree species been measured at Kibale National Park, Uganda with small seeds adapted for germination under (Lambert 1999) and Ch. pygerythrus (formerly high light conditions that are most likely to establish. Cercopithecus aethiops, vervet monkey at Amboseli There was a large difference in the number National Park, Kenya (Isbell et al. 1990). These were and size of seeds per faecal deposit collected reported to be 130 per km2 and up to 96 per km2, from the grassland versus the forest edge. Faeces respectively (Table 3). collected in the forest edge contained fewer seeds Based on the population data discussed above, than the grassland samples (medians of four and tantalus monkeys at Ngel Nyaki moved more than 20, respectively) but a higher proportion of seeds twice as much seed through defecation within the of medium size, whereas the material collected forest edge habitat than into the grassland, dispersing in the grassland areas typically contained more 356 and 124 seeds km-2 d-1, respectively. The forest seeds in the small size class. This is likely at least edge dispersal rate of swallowed seeds is greater than in part to be a reflection of daily foraging patterns. most other reports for Cercopithecus spp. (Table 3), The possibility that faeces may be overlooked by and is closer to the 369 seeds km-2 d-1 dispersed searchers in the forest cannot be dismissed and this by chimpanzees at Kibale National Park, Uganda may have contributed to the discrepancy in our (Wrangham et al. 1994). Conversely the grassland findings between forest edge and grassland in terms seed dispersal rate for the tantalus monkeys in our of number of seeds dispersed. However, searches study is in the middle of the range of seed dispersal for faecal deposits in the forest edge habitat were rates for other Cercopithecus spp. (Table 3) and is painstakingly carried out. similar to the 129 km-2 d-1 seeds dispersed by the olive baboon in the Comoé National Park, Ivory Variation in Tantalus Monkey Seed Dispersal Coast (Kunz & Linsenmair 2008). The absolute rates Rates Compared with Other Cercopithecines of seed dispersal by tantalus monkeys are greater During the transect walks, the small number of than those reported here as the faeces also contained tantalus monkey sightings (n = 12) was not ideal for an unquantified number of seeds < 2 mm, such as the DISTANCE analytical technique (Buckland et al. Ficus spp. Moreover Lambert (1999, 2011) illustrated 2001). However, in the absence of any other tantalus how dispersal rates of cercopithecines in Kabale monkey population density data, the DISTANCE National Park, which included both defecated and technique was applied in order to provide a spat seeds, were considerably higher than dispersal reference point for future studies of tantalus rates based on defecation rates alone and easily monkey populations. Additionally, the measured equated to dispersal rates of larger primate taxa such mean tantalus monkey troop size of 13.3 could have as chimpanzees. been an underestimate; tantalus monkey troop sizes may vary considerably from 11 to 70 individuals The Potential for Tantalus Monkeys to Disperse (Kavanagh 1980) with troop sizes of 18 to 40 being Significant Quantities of Seed into the Degraded most commonly reported (Nakagawa 1999; Agmen Grassland Habitat et al. 2009). The three semi-habituated tantalus In general, the rate of seed dispersal into monkey troops used in this study to calculate the grassland areas from forest remnants can be slow amount of time spent in forest edge and grassland as few animal dispersers make the required inter- habitats ranged between 16 and 38 individuals. habitat movements (Wunderle 1997; Cordeiro & There is sparse reference to tantalus monkey Howe 2001). However, we have shown that, not population densities in the literature. However, only do tantalus monkeys frequent grassland, but using the data from Nakagawa’s (1999) Cameroon they disperse seeds of pioneer, light demanding, study, a tantalus monkey population density of 1.7 early successional species and deep forest species 22 / Grassham et al.

into grassland habitats, making tantalus monkeys faeces, suggests that the conservation contribution potentially important for forest expansion. While made by tantalus monkeys - in conjunction with the overall rate of seed dispersal by tantalus other species, particularly birds such as pigeons and monkeys into grassland habitats (at least during the doves (Roselli 2014) in Afromontane ecosystems, dry season) is less than their rate of seed dispersal lies in their dispersing of pioneer species into within forest edge habitats, the number of seeds the grassland habitats and degraded forest edge habitat. species dispersed into the grassland appears to be Within Ngel Nyaki Forest Reserve tantalus disproportionately high, given they spend only 6.5% monkeys are frequently seen and are additionally of their time in the grassland. Additionally, tantalus important for conservation as the abundance monkeys at Ngel Nyaki feed primarily on the forest of other primates capable of dispersing seeds of edge (70% of feeding time), with only 8% of feeding pioneer tree species into grassland habitats (olive occurring in grassland areas where non-fruit items baboon and chimpanzee) are generally thought to be such as invertebrates are consumed (Agmen et al. insufficient at Ngel Nyaki Forest Reserve to provide 2009). effective seed dispersal services (Beck & Chapman Considering the proportion of seeds from each 2008, Chapman et al. 2010). size class distributed in the forest edge and grassland In summary, this contribution provides an ecosystems, the disproportionate number of seeds important addition to the knowledge of tantalus dispersed by tantalus monkeys into grassland in part monkey ecology, particularly in relation to seed reflects diurnal foraging patterns. While Wallis et al. dispersal. At the individual level, they disperse (2008) report a gut retention time of 30 ± 2.83 hours at least as many seeds, and in some cases larger for captive tantalus monkeys, defecation rates have seeds, than most other cercopithecine species, been shown to be influenced by diet and activity and the tantalus population at Ngel Nyaki Forest levels of the individuals (Lambert 2002). In addition, Reserve disperses a similar number of seeds as some seed size affects gut passage time, with smaller seeds chimpanzee populations elsewhere. Furthermore, being defecated significantly sooner than larger, tantalus monkeys not only regularly spend time in heavier seeds (Tsuji et al. 2010). This study and the grassland habitats but also disperses the seeds of work of Agmen et al. (2009), suggests that with a pioneer and secondary forest plant species from the slightly shorter gut retention time than estimated by forest edge into such habitats, suggesting they may be Wallis et al. (2008), faeces deposited in the grassland an important source of seed rain into such degraded could be associated with forest edge feeding, which habitats. While it is recognised that gaining an could explain why grassland-deposited faeces understanding of the ecology of rare or threatened contained more seeds. Additionally, seed-size is species is important, our study also highlights the an influence; a greater number of small seeds than importance of gaining an ecological understanding medium seeds can be swallowed before reaching the of relatively common species that are less affected by threshold volume at which too much nutritious gut anthropogenic habitat modifications. content becomes displaced by undigestible seeds (Lambert 1999). Of those seeds dispersed into grassland areas ACKNOWLEDGMENTS by tantalus monkeys, the vast majority were small- seeded understory herbs/shrubs associated with We wish to thank the North of England the forest edge such as Aframomum angustifolium Zoological Society, the A. G. Leventis Foundation and Leea guineensis. The few medium-sized seeds and Nexen Inc. for funding this research through the dispersed into grassland included pioneer species University of Canterbury New Zealand, Nigerian such as Croton macrostachyus and Bridelia speciosa, Montane Forest Project. This was in collaboration again associated with the forest edge habitats. with the Biodiversity and Climate Research Centre In terms of practical conservation value, such (BiK-F), Frankfurt, with additional financial support observations indicate that, providing the dispersed to B.K. through “LOEWE – Landes-Offensive seeds germinate and are given adequate protection zur Entwicklung Wissenschaftlich-ökonomischer from regular burning and grazing, such dispersal into Exzellenz” of Hesse’s Ministry of Higher Education, grassland could support forest regeneration through Research, and the Arts.” tantalus monkeys. This and the fact that larger seeds, such as Pouteria sp., associated mainly with forest core were relatively rare in any tantalus monkey Seed Dispersal by Tantalus Monkeys / 23 LITERATURE CITED primates and the conservation and dispersion of large-seeded trees. International Journal of Agmen, F.L., H.M. Chapman & M. Bawaro. 2009. Primatology 26: 631–649. 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First Sightings of the Roloway Monkey (Cercopithecus diana roloway) in Ghana in Ten Years and the Status of Other Endangered Primates in Southwestern Ghana

David Osei1, Robert H. Horwich2 , and Jeanne Marie Pittman1

1West African Primate Conservation Action, Accra, Ghana; 2Community Conservation, Gays Mills, WI USA

Abstract: Primate surveys were conducted in community controlled peat swamp forest along Ghana’s Tano River by West African Primate Conservation Action (WAPCA), the Wildlife Division of the Ghana Forestry Commission, and members of local communities in 2011 and 2012. The 2011 survey revealed the first sightings in Ghana of the Critically Endangered roloway monkey (Cercopithecus diana roloway) in ten years. A follow-up survey in 2012 indicated that despite a great deal of illegal logging and some hunting, this forest, informally known as the Kwabre Peat Swamp Forest, hosted all of Ghana’s forest primate species with the exception of the Miss Waldron’s red colobus (Procolobus waldroni), considered extinct by some scientists since 2000. These species included the Endangered white-naped mangabey (Cercocebus lunulatus), the Vulnerable white-thighed black-and-white colobus (Colobus vellerosus), the Near Threatened olive colobus (Procolobus verus), the Least Concern eastern spot-nosed guenon (Cercopithecus petaurista petaurista) and Lowe’s guenon (Cercopithecus campbelli lowei). The results of the surveys are compared to encounter rates of earlier primate surveys in the region. With the continuous decline and extirpation of the roloway and other primates in Ghana and Ivory Coast, the last forests where these rarer primate species still exist center on the extreme corners of southwestern Ghana and southeastern Ivory Coast, composed of a complex of two community- owned peat swamp forests in Ghana and Ivory Coast, a few government protected areas and an un-explored wetland. Future recommendations for the protection of these species and their habitat are provided here.

Key words: Ghana, roloway monkey, white-naped mangabey, white-thighed black-and-white colobus, olive colobus, Miss Waldron’s red colobus, community forest

INTRODUCTION

Although deforestation is occurring worldwide to protect the last remaining forests in southwestern at an escalating rate, it has been especially rapid Ghana, the Cape Three Points Reserve Forest, and extreme in Ghana and Ivory Coast in the last and the forests along the Tano River, informally decade due to the clear cutting of mature rainforest known as the Kwabre Peat Swamp Forest. These for the cultivation of cocoa, rubber, and palm oil forests, along with similar areas in southeastern (Boafo 2013; Mongabay.com/20ghana.htm 2014). In Ivory Coast, are some of the few remaining forests 2011, WAPCA (West African Primate Conservation in an area of secondary primate endemism that is Action), in collaboration with Coastal Resources isolated probably by geological history (Oates 1988). Center, initiated a community conservation project Oates noted Booth’s argument that dry periods in

Correspondence to: Robert Horwich, Community Conservation, 50542 One Quiet Lane, Gays Mills, WI 54631 USA; Phone: +1 (608) 735-4717; E-mail: [email protected]. Contacts in Ghana: West African Primate Conservation Action, P.O. Box 1319, Accra, Ghana; +233 (0) 244 72 9116; [email protected]. 26 / Osei et al.

Figure 1. Survey team members in Kwabre Peat Swamp Forest.

the Pleistocene in West African forests resulted in monkey and white-naped mangabey are IUCN listed a refuge in eastern Ivory Coast and western Ghana as Endangered, although the roloway should be which was enforced by the Baoule-V savanna and considered Critically Endangered (Magnuson 2002- the Dahomey gap isolating Miss Waldron’s red 3; Oates 2011), while the black-and-white colobus is colobus (Procolobus waldroni), the roloway monkey Vulnerable and the olive colobus is Near Threatened. (Cercopithecus diana roloway), and the white-naped Only the Lowe’s guenon and the spot-nosed guenon mangabey (Cercocebus lunulatus). are still Red Data listed as Least Concern. These forests once hosted viable populations of The goal of this survey was to verify the presence seven nonhuman primates including Miss Waldron’s of roloway monkeys, white-naped mangabeys and red colobus, roloway monkey, the white-naped potentially even Miss Waldron’s red colobus in the mangabey, the olive colobus (Procolobos verus), the Kwabre Peat Swamp Forest, a forest, previously white-thighed black-and-white colobus (Colobus unknown to primatologists, which had not yet been vellerosus), Lowe’s guenon (Cercopithecus campbelli surveyed for primates. lowei), and eastern spot-nosed guenon (Cercopithecus petaurista petaurista). Within the past two decades both the forest and nearly all the primate species METHODS in it have decreased to a precarious level. Despite Study Site cautionary warnings (Roberts & Kitchener 2006), The southwestern corner of Ghana is considered primate numbers continue to decline and recent wet evergreen forest (Sayer et al. 1992), while the surveys have not given any indications that differ Kwabre Peat Swamp Forest, which runs north to from an assessment declaring that Miss Waldron’s south and follows the Ghana-Ivory Coast border on red colobus is probably locally extinct (Oates et al. the eastern side of the Tano River, is a peat swamp 2000) and the remaining primate species appear ecosystem that floods seasonally and annually to be following in its footsteps. Both the roloway (Figure 1). It is composed of approximately 4,000 First Sighting of Roloway Monkeys in Ten Years / 27 hectares of forest fragments along the lower Tano seasonally flooded sites, while 31 species were in River on the southwestern border of Ghana. the permanently flooded sites with 21 tree species This area forms part of a complex of forests in occurring only in seasonally flooded areas, and 11 eastern Ivory Coast and western Ghana that are species occurring only in permanently flooded areas. probably the last forests inhabited by the endemic A list taken from the study (Asante & Jengre 2012) of roloway monkey (McGraw & Oates 2014), some trees observed over 25 times in either site indicated of the last remaining habitat of the white-naped Raphia hookeri, Amanoa bracteosa, and Manikara mangabey and currently represents the last possible sylvestris were the dominant species in the seasonally hope for the persistence of Miss Waldron’s red flooded sample areas, while Uapaca paludosa was colobus. Since the 1940s, over 90% of Ghana’s closed the dominant species in the permanently flooded canopy forest has been clear cut for rubber, palm area (see Table 1). oil and cocoa and this peat swamp forest ecosystem represents one of the last remaining coastal forests 2011 Survey in Ghana and Ivory Coast. Figures 2 through 6 show In 2011, a team of six people conducted this complex that includes the Tanoé Forest in Ivory preliminary ad lib recce surveys of five areas from Coast, the Kwabre Peat Swamp Forest previously March to May to investigate the presence of the unknown to primatologists, the Amanzule Wetlands three focal primates, the roloway monkey, the (yet to be studied) and Ankasa Conservation Area white-naped mangabey and Miss Waldron’s red and Nin-Suhien National Park, a government colobus. The survey team spent nine days in the Protected Area. Kwabre area, three days in Nawule, two days in A study of carbon sequestering of Kwabre Peat Takinta and one day in Agyeza (Figure 3). The team Swamp Forest and Amanzule Wetlands noted it as was composed of the lead author, a Ghana Wildlife a unique ecosystem with a total of 52 tree species Division wildlife guard, two members of the Ivorian recorded in all sites, some of which are endemic team experienced in wildlife censusing and two to West Africa and some endemic only to eastern members of the rural community (which varied Ivory Coast and western Ghana (Asante & Jengre depending on which forest area was surveyed). Five 2012). Forty-one tree species were found in the forest areas were surveyed (Anwiafutu, Kwabre,

Figure 2. Map of area showing significant forests for the focal species. 28 / Osei et al.

Figure 3. Map showing areas where 2011 recce surveys were conducted. The black dots indicate direct signs of primates, either audio or visual. First Sighting of Roloway Monkeys in Ten Years / 29 Table 1. List of most common tree species in the peat swamp forests (from Asante & Jengre 2012).

# in # in # in # in Seasonally Flooded Seasonal Annual Annually Flooded Seasonal Annual Forest Trees Flooded Flooded Forest Trees Flooded Flooded Forest Forest Forest Forest Amanoa bracteosa 1549 35 Uapaca paludosa 65 260 Raphia hookeri 1101 0 Syzygium rowlandii 140 136 Manilkara sylvestris 401 0 Xylopia rubescens 47 95 Lonchocarpus santalinoides 81 0 Anthostema aubryanum 27 91 Spondianthus preussi 78 8 Hallea ledermannii 54 90 Gardenia imperialis 72 0 Symphonia globulifera 81 79 Millettia spp. 57 0 Coffea humilis 1 62 Sarcocephalus pobeguinii 35 1 Garcinia smeathmannii 32 0 Lijndenia barteri 27 0 Cuviera subuliflora 25 0 Diospyros chevalieri 25 9 Mediewie, Nawule and Takintka) by conducting a of six people was divided into two groups of three total of 15 line transects of four kilometers length members, a team leader (either David Osei from using the path of least resistance. The transects were WAPCA or Victor Agyeman Duah of the Wildlife traversed for two kilometers in one direction, with Division), an experienced Ivorian team member and the team then moving perpendicular 500 meters a newly trained Ghanaian community member. and returning for two kilometers in the opposite Surveys were conducted using existing wildlife direction. Additionally, during that same period, pathways combined with paths of least resistance. WAPCA and the Wildlife Division of the Ghana Due to high water levels and dense vegetation in Forestry Commission distributed questionnaires to the Kwabre Peat Swamp Forest survey, sufficient selected community members to obtain traditional distances and time were covered despite the and historic knowledge about the local primates. difficulties in walking through the wetland mud. The two teams walked in parallel at a distance of 2012 Survey approximately 500 meters apart until they reached Surveys were conducted over a forty-one day the forest boundary where the teams then moved period between March and May 2012, with 28 two hundred meters to the right and reversed effective days of survey and a total survey time of direction back to the other boundary. The teams about 300 hours covering a total of 167.9 kilometers. remained in contact with each other with walkie- Prior to the surveys, training sessions were held talkies throughout the survey and notified each in the communities surrounding the Kwabre Peat other with the direction and coordinates regarding Swamp Forest to teach community members to primate sightings to reduce the possibility of assist with the surveying. The survey team also met counting any monkey group twice. Surveys began with the village chiefs of each area prior to surveying early in the morning, and lasted on average of 5 – 6 to gain permission to access the forest and then hours. Due to the dense forest cover, high canopy again after the surveys to report results to the chief trees and shy nature of the endemic primates, and community members. positive identification can be challenging. The teams The surveys, conducted on foot, began in the addressed these challenges by walking at a slow Takinta area close to the town of Half Assini and speed (1–2 km/hr) and stopping approximately ended in Mansah Nkwanta close to Elubo near the every 200 meters to listen for sounds of primates Ivorian border (Figure 3). The survey team consisting or other animals. When a primate call was heard, 30 / Osei et al.

the team spread out in an attempt to circumscribe Nsuoano (8), Mediewie (17), Medina (6), Nawule the group, using silent hand signals to coordinate (4), Nyameadom (3), Nzalenu (23), Takinta (20). their movements and positions. When the primate Of the respondents, 72.5% were male, 27.5% were group eventually dispersed at the sight of the female. Ninety-two percent of the respondents researchers, each team member counted the number stated that they were not native to the area and had of animals that passed their direction. The team emigrated from other areas of Ghana and West also used additional methods to get closer to the Africa for farming (87%) mainly for cocoa, coconut, primate groups for greater identification, including oil palm, rubber, cassava and other food crops. The mimicking the calls and branch shaking behavior remaining 13% were fishermen, gin distillers, and of the primate species sighted to draw the animals soap and coconut oil producers. Over a third (34%) closer. of the respondents hunted bush meat, however some The data recorded included all primate sightings, had abandoned the work due to old age or lack of primate calls, feeding and other signs as well as illegal animals to hunt. activities (traps, gun cartridges, etc.). Opportunistic Most respondents reported sightings of monkeys, data on other mammalian and reptilian species were giant rats (Cricetomys gambianus), grasscutters or also recorded. For direct sightings, as far as possible, cane rats (Thryonomys swinderianus), bushbuck the numbers of individuals were counted. (Tragelaphus scriptus), monitor lizards (Varanus niloticus), mongoose (sp.?) and striped ground squirrels (Xerus erythropus) in the area. Sightings RESULTS of large yellow backed duikers (Cephalophus silvicultor), bongos (Tragelaphus eurycerus), red 2011 Surveys river hogs (Potamochoreus porcus), brush tailed The presence of roloway monkeys in the Kwabre porcupines (Artherurus africanus) and endangered Peat Swamp Forest was confirmed. In Kwabre (Area primate species were less common or rare. A in Figure 3) groups of Lowe’s guenon numbering Species with totem or other significance included 10-15 were recorded and on one occasion a mixed rock pythons (Python sebae), dwarf crocodiles species group of more than 30 individuals was seen (Osteolaemus tetraspis) and monitor lizards. Species which included white-thighed black-and-white that caused crop damage problems included cane colobus, Lowe’s guenon, and the spot-nosed guenon. rats, bushbuck, giant rats and occasionally monkeys. In this area there were high levels of disturbance One section of the questionnaire used primate from hunters and chainsaw operators. In Nawule photographs, drawings and recordings to assess (Area B), on two consecutive mornings in different the respondent’s knowledge of primates. Most parts of the forest, the field team encountered large respondents (81%) had hunted primates but mixed-species groups of primates feeding on Parkia showed great variability in terms of when they bicolar, Uapaka guineansis and a species called had last sighted a primate. Most said they thought locally “subaha”, including roloway monkeys, the there were still monkeys in the area but admitted first sighting of the species in Ghana in over ten not seeing them personally for a long time, and years. On the first day, the mixed group consisted of reported that there were fewer than in the past approximately five roloway monkeys, 14 spot-nosed due to deforestation, farming and hunting. Ad lib guenons, 15 Lowes’ guenons, five white-thighed comments from respondents included questions colobus and 10 olive colobus. On the second day the with regard to prevention of crop raiding and the mixed group consisted of 20 spot-nosed guenons, support of wildlife and forest protection for the 15 Lowe’s guenons, five white-thighed colobus and future and ecotourism. 10 olive colobus. No roloway monkeys were seen in that mixed group. In Agyeza (Area D), only one 2012 Survey survey was conducted. Primates were heard moving Figure 4 indicates all general primate activity through the tree canopy by their multiple loud noted during the 2012 survey. Figure 5 indicates the crashing sounds, but species could not be identified six primate species sightings by individual symbols visually or audibly. during the 2012 survey and the sightings of mixed species groups indicated by symbols. 2011 Questionnaires The presence of roloway monkeys was confirmed A total of 142 questionnaires were administered by two sightings in Takinta and Nawule (Figure 5). to 12 communities: Agyeza (12), Anawhiafutu (20), However, although the overall encounter rate for Atsyimenu (7), Elokobabo (2), Kwabre (20), Kwabre common species of primates such as Lowe’s guenons First Sighting of Roloway Monkeys in Ten Years / 31

Figure 4. Map of all primate sightings and activities.

(18 sightings) and eastern spot-nosed guenons (19 felled trees and charcoal burning were observed sightings) was high, encounter rates for the rare (Table 3). Kwabre and Allowuley recorded the species, roloway monkey (2 sightings) and white- highest level of illegal logging. Nawule recorded naped mangabey (1 sighting), were relatively low the least. Eight chainsaws were confiscated in and no Miss Waldron’s red colobus were found Allowuley, four in Kwabre and one each in Nawule (Table 2). There was additionally one sighting of the and Ellenda. Illegal logging was so prevalent that it black-and-white colobus and three sightings of olive often disrupted the survey work. The noise from the colobus groups (Table 2). chain saws drove the primates away making it very Data from the surveys indicate a high level of difficult to find their locations. The illegal logging human (illegal) activity indicating hunting and was very indiscriminate with 10 to 15 trees being cut deforestation; snares, traps, gunshot cartridges, in one trip to Kwabre, Allowuley or Takinta. 32 / Osei et al.

Figure 5. Map of area surveyed with primate species of concern. First Sighting of Roloway Monkeys in Ten Years / 33 Table 2. Encounter rates of groups per kilometer of primates in the Kwabre Peat Swamp Forest survey in 2012 (see Figure 3). Miss White- Waldron’s Black & 2012 Census Roloway naped Red White Olive Lowe’s Spotnose Monkey Mangabey Colobus Colobus Colobus Guenon Guenon Takinta .18 .26 0 0 .13 1.26 1.00

Nawule .22 0 0 .24 .14 .84 1.39

Allowuley 0 0 0 0 0 .62 .69

Ellendra 0 0 0 0 .24 3.86 1.79

Kwabre 0 0 0 0 0 .67 .78

Mansah 0 0 0 0 0 0 0 Nkwanta

Total .012 .006 0 .006 .018 .11 .12

Evidence of wildlife poaching on the other hand animal trapping. No traps set for mammals were was minimal. Throughout the surveys, only three seen but a number of fish traps were recorded. The bush meat hunters were spotted. One hunter had entire forest area is flooded throughout most of the two brush-tailed porcupines and the other had two year, so the most common hunting activity is fishing. giant wild rats and one gun was seized from a hunter Illegal fishing in the forest can lead to illegal hunting who confessed to killing bushbuck, brush-tailed of mammals if the fishing trip is unsuccessful. porcupine and even a Lowe’s guenon. During the Occasionally, dugout canoes crafted from large surveys, the forest was scanned for signs of illegal forest trees were seen.

Table 3. Illegal activities encountered in 2012 survey of the Kwabre Peat Swamp Forest.

Illegal Poaching Equipment Community Lumber Activities Arrests Made Date of Arrest Seized Encounter Encounter Takinta 7 1 1 poacher 1 gun 31 March 2012

Nawule 4 1 3 chainsaw operators 1 chainsaw 11 April 2012

Allowuley 10 1 6 chainsaw operators 8 chainsaws 24 April 2012 1 gun Ellendra 1 0 3 chainsaw operators 1 chainsaw 21 April 2012

Kwabre 8 0 3 chainsaw operators 4 chainsaws 28 April 2012

Mansah 0 0 No arrests None --- Nkwanta 34 / Osei et al.

Table 4. Comparison of encounter rates/km in other studies. Miss Year Surveyed/ White- Waldron’s Black & Surveyor km Roloway naped Red White Olive Lowe’s Spotnose Monkey Mangabey Colobus Colobus Colobus Guenon Guenon 1976 820 .17 .03 .02 .18 .04 .09 .03 Martin et al.1 1996 90 .008 0 0 0 .07 .21 .28 Oates et al.2 2001 216.9 .04 .02 0 .03 .003 .39 .11 Magnusen (2002-3) 2003 175 0 0 0 0 + + + Dershner & Kpelle (2005) 2004-6 + + 0? + + + + Bi et al. (2008) 2006 5614 .0002 .0005 0 .0013 .0012 .0352 .0231 Gatti3 (2010) 2006 448 0 0 .018 .012 .053 .032 Oates4 (2006) 2009 429.3 .38 .28 0? .04 .11 .58 .44 Bi et al. (2013) 2011 131.6 0 0 0 0 0 0 0 Wiafe (2013) 2011 125.6 0 0 0 0 0? .075 .075 Buzzard & Parker (2012) 2012 167.9 .0119 .0059 0 .0059 .018 .107 .113 WAPCA 1 from Oates et al 1996-7, averaged 3 sites by Martin et al.; averaged 5 sites surveyed by Oates and Struhsaker 2 converted encounters/hour to encounters/km 3 averaged 4 sites 4 averaged 4 sites and converted from encounters/hour. ? = no data; 0? = not encountered but indirect evidence of presence

DISCUSSION

Of the 16 primates found in Ghana, 12 reside areas since that time, which has documented a steady mainly in the high forest that covers a large area decline of rare primate species and the eventual of southwestern Ghana composed of mainly four report of extinction of the Miss Waldron’s red forest types (Booth 1979; Sayer et al. 1992) (Figure colobus and potential local extinction of the roloway 6). However, Ghana’s high forest primates have been monkey in Ghana. Table 4 shows a compilation disappearing at an alarming rate due to deforestation of the surveys that occurred from 1976 to 2012. and hunting for bush meat. Even in the 1950s, the Figure 6 shows a map of southwestern Ghana and its roloway monkey was considered Ghana’s (then Gold vegetation types and the areas that were surveyed in Coast’s) rarest primate (Booth 1979). There has the past for the seven forest primate species. been continuous surveying of the roloway and other In the late 1970s roloway monkeys and white- arboreal primates in Ghana’s southwestern protected naped mangabeys were still common in Bia (Rucks First Sighting of Roloway Monkeys in Ten Years / 35 in Magnuson 2002-3). Struhsaker and Oates (1995) colobus were sighted in Ankasa, Bia and Krokosua surveyed Bia, Ankasa and Kakum National Parks in Hills. Spot-nosed and Lowe’s guenons were seen in 1993 and noted the isolated nature of the parks and all four sites. Later surveys by Buzzard and Parker degradation due to logging and hunting. They found (2012) in Subri River and by Wiafe (2013) in Dadieso no Miss Waldron’s red colobus, roloway monkeys or RF in 2011 found none of the four most endangered white-naped mangabeys in Kakum but there were primates. Horwich in 2011 (pers. obs.) saw olive some black-and- white colobus. Struhsaker found colobus, Lowe’s Guenon and spot-nosed guenons in none of the three species in Bia but according to the tiny Monkey Hill city park in Takoradi. Table 5 park staff black-and-white colobus occurred but shows which species are thought to currently occur were extremely rare. Oates heard only one roloway in the various areas surveyed in the past (Figure 6). call in Ankasa and saw no red colobus or white- When we compare the encounter rates of this naped mangabeys. In 1995 Whitesides and Abedi- study with other surveys in Ghana (Table 4), it can Lartey saw roloways in Ankasa as did Oates and be seen that roloway monkey and white-naped Abedi-Lartey later the same year (Oates 1999). mangabey occurrence had already decreased by Magnuson (2002–3) surveyed nine areas in the 1996 in all sites except in Tanoé forest and Kwabre. high forest zone in 2001. She noted that roloway Tanoé as of 2009 had an extremely high population monkeys were found in only four forests at that time (Bi et al. 2013). Krokosua Hills Forest Reserve (FR), Dadieso FR, Although the encounter rate for primates was Yoyo FR, and Ankasa noting that they had likely low in much of the Kwabre Peat Swamp Forest, been extirpated from Bia National Park (NP), Cape it is encouraging that it was possible to confirm Three Points FR, Draw River FR, and Nini-Suhien the presence of most forest primate species, most NP. Three years later in 2004, Deschner and Kpelle notably the Critically Endangered roloway monkey (2005) surveyed Draw River, Boi-Tano, Tano Nimiri and the Endangered white-naped Mangabey. It was and Krokosua Hills FRs. No roloways, white-naped also encouraging to see that the primates were often mangabeys, red colobus or black-and-white colobus moving in relatively large groups. Despite the low were found in any of the sites. The olive colobus primate encounter rates compared to anticipated was found in Draw River and spot-nosed guenons levels, there were significantly more primate and Lowe’s guenon were found in Draw River FR sightings and more primate species diversity than and Krokosua Hills FR. However, interviews with noted during 2008 primate surveys in the nearby local poachers gave more hope claiming that white- Cape Three Points Forest Reserve and Ankasa naped mangabeys, roloways, and Miss Waldron’s red Conservation Area. Gatti (2010) indicated no colobus were present in Boi-Tano, Tano-Nimiri, and sightings of roloway monkeys in either Cape Three Kroskosua Hills FR and white-naped mangabeys Points or Ankasa. were in Draw River FR. However, from the hunter survey and But later surveys by Oates (2006) in 2005–6 observations by community patrols (Table 3), the in Mamiri FR, Boi-Tano FR, Krokosua Hills FR, extent of illegal human activities is very high in Bia NP, Bia RR saw no roloways or white-naped the Kwabre Peat Swamp Forest, particularly in mangabeys in any of the sites. Spot-nosed guenons Allowuley and Kwabre areas of the forest where there and Lowe’s guenons were found in three sites and appears to be virtually open access. Illegal logging is olive and black-and-white colobus were found at indiscriminate and of greatest threat to the primates Krokosua and Bia. due to loss of habitat. Hunting with guns is a much Gatti (2010) spent two years from 2006-2008 greater threat to primates, but its incidence was very surveying Bia, Krokosua, Ankasa, and Cape Three minimal in this location. Points RF. Miss Waldron’s red colobus was absent The bright spot for the more endangered species in all four sites. At the time, Wildlife Division staff is with the Tanoé Forest in Ivory Coast in which reported seeing roloway monkeys in Ankasa but the encounter rates in 2009 was 19 times higher there was no direct evidence. Ben Phalan reported for roloway monkeys than that of Kwabre and 47 hearing the call of roloway monkeys and a young times higher for the white-naped mangabey. This captive roloway was found in a nearby village by high population seems to be due to the inaccessible WAPCA staff. White-naped mangabeys were seen nature of the Tanoé Forest and the protection by the in Ankasa and Phalan heard them in Cape Three local communities. The Tanoé Forest is the last place Points. Black-and-white colobus were seen in in which the roloway monkeys are found in Ivory Krokosua Hills and heard by Phalan in Cape Three Coast (see Koné et al, this issue). Points with possible signs in Bia and Ankasa. Olive 36 / Osei et al.

Table 5. Best current knowledge of species occurrence.

Miss White- Waldron’s Black & Areas Km2 Roloway naped Red White Olive Lowe’s Spotnose Monkey Mangabey Colobus Colobus Colobus Guenon Guenon Kwabre 50 + + 0 + + + +

Tanoe 120 + + 0? + + + +

Ankasa/Nini Suhien 509 0 + 0 0 +2008 + +

Amanzule ????????

Draw River 235 0 0? 0 0 +2005 ? ?

Cape 3 Points 51 0 0? 0 + 0 + +

Subri 45 0 0? 0 0 + + +

Boi-Tano 129 0 0 0 0 0 + +

TanoNimri 206 0 0 0 0 0? ? ?

Mamiri 206 0 0 0 0 ? + +

Dadieso 171 0 0 0 0 0 0? 0?

Yoyo 236 ? ? 0 ? ? ? ?

Bia 306 0 0 0 + + + +

Krokosua 481 0 0 0 +2008 + + +

Kakum 375 0 0 0 + + + +

Monkey Hill .12 0 0 0 0 + + +

? = no information; 0? = not encountered but indirect evidence of its presence; year indicates when last seen with no more recent surveys

CONCLUSION

The world’s only remaining forests where forests, also one of the last remaining habitats for roloway monkeys, one of the three endemic the white-naped mangabey, currently represent the primate taxa in this region, can still be found only possible hope for the continued persistence of are in community-owned peat swamp forests in Miss Waldron’s red colobus. There is an additional southeastern Ivory Coast (Tanoé Forest) (Bi et large swamp forest, the Amanzule Wetland forest, al. 2008, 2013) and southwestern Ghana. These east of the Kwabre Forest (Figures 2, 3, 6) that may First Sighting of Roloway Monkeys in Ten Years / 37

Figure 6. Map of Southwestern Ghana locating areas surveyed by all researchers (from authors cited and web search) and vegetation types. WE=wet evergreen, ME=moist evergreen, MS=moist semi-deciduous, DS=dry semi-deciduous, S M=southern marginal. 38 / Osei et al.

also host this endemic primate community but it areas; then, encouraging them to form conservation has only been explored in a preliminary manner. groups and larger federations for regional protection The Draw River and Cape Three Point Forest is at the base of success in most areas and countries. Reserves still hold some possibility for the white- These simple steps engender sustainability as naped mangabey. These community-owned forests, 96% of 26 projects carried out by Community along with the Ankasa/Nini-Suhien National Park, Conservation in 30 years are on-going many for form a complex that is the last stronghold for the 23 to 30 years (Horwich pers. obs., and see www. roloway monkey and the white-naped mangabey, communityconservation.org). which if strengthened and managed could provide The CREMA (Community Resource protection to the endangered primates as well as the Management Area) policy was developed in 2000 whole primate community. Work with local human to devolve management authority to community- communities in the Ivory Coast over the past nine based organizations (Forestry Commission 2004). years and our work with Ghanaian communities Physically, CREMA is defined as an area including could help create a community protective complex one or more communities that agree to manage for those primate species. resources sustainably. It focuses on sustainable use of wildlife which is usually not a possible goal, CREMAS and Community Protection especially in forested areas. However, in African Governments throughout the world are savannas with large ungulates and high biomass such beginning to understand the importance of as in Namibia, it has been very successful (Horwich incorporating communities into conservation et al. 2012). So, with our work with communities in strategies and within the past 20 years, some, the Kwabre area, we have instead emphasized other perhaps many, have incorporated policies and more altruistic, conservation minded incentives and laws that involve communities in conservation as have helped the 12 communities around the Kwabre partners. Some examples, include the conservancies Peat Swamp Forest to create the Ankasa Tano of Namibia (Horwich et al 2012), the Gelose law CREMA, which in turn has organized community (gestion local sécurisee) in Madagascar, CAMPFIRE patrols. (Communal Areas Management Programme for The Tanoé forest has been protected by the Indigenous Resources) in Zimbabwe, laws for local communities for over nine years and the community management in Peru (Shanee et al. Kwabre Peat Swamp Forest is now protected by 2014), community co-management policy in Belize 12 community forest protection teams under the (Young & Horwich 2007; Horwich et al. 2012), Ankasa-Tano CREMA. The Ankasa complex has the community forests in Nepal (Ojha 2011), and the Amokwaw CREMA that, while active, is not actively CREMA (Community Resource Management protecting the area. The Amanzule Working Group, Area) law in Ghana (Forestry Commission 2004). formed under the Coastal Resource Center project This is an important trend because community (Adupong et al. 2013), has adopted a plan to create members are proving to be stronger and more a protected area for the Amanzule Wetlands using a consistent conservationists than governments that modified CREMA plan (Adupong & Gormey 2013). change as different political parties come to power. West African Primate Conservation Action and For example, recently in Belize political change is Community Conservation Inc. have been working threatening a 30 year old successful co-management together to help form the Ankasa-Tano CREMA system for oil exploration in protected areas. Only and bring them together with the communities community co-manager and indigenous groups are of Tanoé forest to create a trans-border protected actively resisting this illegal activity (Horwich pers. area. Presently, the communities of Ivory Coast obs.). and Ghana have been conducting joint community Success of any of these policies or programs patrols to reduce illegal activities on a limited basis. depends on the government or NGO individuals who introduce communities to the ideas. Success in motivating communities depends on simple RECOMMENDATIONS human interactions based in trust and transparency. Explaining that the species are specific to their areas • Survey the Amanzule Wetlands for primates and that government and NGOs cannot protect the • If Amanzule contains roloway monkeys species without the community’s help and asking and white-naped mangabeys, work with the for their help is the first step in empowering the Amanzule Working Group to develop a CREMA communities and engendering pride in their natural or a modified CREMA and forest protection First Sighting of Roloway Monkeys in Ten Years / 39 forces as in Kwabre (Cercocebus atys lunulatus) prefer mangrove • Work with the Amokwaw CREMA around habitats in Tanoé forest, south-eastern Ivory Ankasa to further develop forest protection Coast. Journal of Ecosystem and Ecography 3: forces to prevent hunting of primates in the 126. doi:10.4172/2157-7625.1000126 reserve Boafo, J. 2013. The impact of deforestation on forest • Develop forest corridors between Ankasa livelihoods. Africa Portal Backgrounder 49: 1-6. and Kwabre and conduct reforestation in Booth, A.H. 1979. The distribution of primates in discontinuous areas within the Kwabre Peat the Gold Coast. In Primate Ecology: Problem- Swamp Forest Oriented Field Studies. R.W. Sussman, ed. John • Stimulate primate surveys in Ankasa/Nini- Wiley & Sons, New York. Pp. 139-153. Suhien, Draw River FR and Tanoé forest Buzzard. P.J & A.J.A. Parker. 2012. Surveys from • Bring Ankasa-Tano, Amokwaw, Amanzule and the Subri River Forest Reserve, Ghana. African Tanoé community groups together to create a Primates 7(2): 175-183 regional plan of protection for the forests and Deschner, T. & D.G. Kpelle. 2005. Rapid assessment primates. of the primates of Draw River, Boi-Tano and Krokosua Hills. In A Biological Assessment of the Terrestrial Ecosystems of the Draw River, Boi-Tano, ACKNOWLEDGEMENTS Tano Nimiri and Krokosua Hills Forest Reserves, Southwestern Ghana. J. McCullough, J. Decher We would especially like to thank the following & D.G. Kpelle, eds., RAP Bulletin of Biological people: Nana Kofi Adu Nsiah, Executive Director Assessment 36. Conservation International, of the Wildlife Division of the Ghana Forestry Washington DC. Chapter 9, Pp. 73-78. Commission, Cletus Balangtaa, Ankasa National Forestry Commission. 2004. A Brief Guide Park manager, Awulae Annor Adjaye III, Paramount to Establishment of Community Resource Chief and President, of the Western Nzema Management Area (CREMA). Collaborative Traditional Area Council and the census team Resource Management Unit, Wildlife Division, members: Victor Agyeman Auah, Salasie Tsogali, Accra. Nda Aboa. We would also like to thank the Margot Gatti, S. 2010. Status of Primate Populations in Marsh Biodiversity Foundation for their financial Protected Areas Targeted by Community Forest support of the project. Biodiversity Project. Unpublished Report for WAPCA and WD/FC, Accra LITERATURE CITED Horwich R.H., J. Lyon, A. Bose & C.B. Jones. 2012. Preserving biodiversity and ecosystems: Adupong, R. & B. Gormey. 2013. Development of catalyzing conservation contagion. In Conservation Scenarios: The Case of Amanzule Deforestation Around the World. P. Moutinho, ed. Wetlands. USAID. CRC, FoN, Accra InTech, Rijeky. Pp. 283-318. Adupong, R., D.D.N. Nortey & J. Asiedu. 2013. Magnuson, L. 2002-3. Distribution and abundance Customary Laws and Practices in the Greater of the roloway monkey Cercopithecus diana Amanzule Wetland Areas. USAID, Accra roloway and other primate species in Ghana. Asante, W. & N. Jengre. 2012. Carbon Stocks and Soil African Primates 6(1-2): 19-26. Nutrient Dynamics in the Peat Swamp Forests of McGraw, W.S. & J.F. Oates. 2014. Roloway monkey the Amanzule Wetlands and Ankobra River Basin. Cercopithecus diana roloway (Schreber, USAID, CRC, NCRC, Accra. 1774). In Primates in Peril The World’s Most Bi, S.G., I. Koné, J-C.K. Bené, A.E. Bitty, B.K. Endangered Primates 2012-2014. C. Schwitzer, Akpatou, Z. Goné Bi, K. Ouattara & D.A. R.A. Mittermeier, A.B. Rylands, L.A. Taylor, F. Koffi. 2008. Tanoé forest, south-eastern Côte- Chiozzo, E.A. Williamson, J. Wallis & F.E. Clark, d’Ivoire identified as a high priority site for the eds. IUCN SSC Primate Specialist Group (PSG), conservation of critically endangered primates in International Primatological Society (IPS), West Africa. Tropical Conservation Science 1(3): Conservation International (CI), and Bristol 265-278. Zoological Society, Arlington, VA. Pp. 14-16. Bi, S.G., J-C.K. Béné, E.A. Bitty, B.K. Kassé, Mongabay.com/20ghana.htm. 2014. Forest data: A.N. Guessan, A.D. Koffi, B. Akpatou & I. Ghana Deforestation Rates and Related Forestry Koné. 2013. Roloway guenon (Cercopithecus Figures. Accessed 8/24/14. diana roloway) and white-naped mangabey Oates, J.F. 1988. The distribution of Cercopithecus 40 / Osei et al.

monkeys in West African forests. In A Primate we too quick to write off Miss Waldron’s Radiation: Evolutionary Biology of the African red colobus Monkey (Piliocolobus badius Guenons. A. Gautier-Hion, F. Bouliere, J.P. waldronae)? Biological Conservation 128: 285- Gautier & J. Kingdon, eds. Cambridge University 287. Press, New York. Pp. 79-103. Sayer, J.A., C.S. Harcourt & N.M. Collins (eds.). Oates, J.F. 1999. Myth and Reality in the Rain Forest. 1992. The Conservation Atlas of Tropical Forests University of California Press, Berkeley, CA. Africa. IUCN, Simon and Schuster, NY. Oates, J. F. 2006. Primate Conservation in the Shanee, N., S. Shanee & R.H. Horwich. 2014. Forests of Western Ghana: Field Survey Results, Effectiveness of locally run conservation 2005-2006. Unpublished Report to the Wildlife initiatives in north-east Peru. Oryx 49(2): 239- Division, Forestry Commission, Ghana. 247. Oates, J.F. 2011. Primates of West Africa. Conservation Struhsaker, T.T. & J.F. Oates. 1995. The biodiversity International, Arlington, VA. crisis in south-western Ghana. African Primates Oates, J.F., T.T. Struhsaker, & G.H. Whitesides. 1(1): 5-6, 1996/1997. Extinction faces Ghana’s red colobus Wiafe, E.D. 2013. Status of the critically endangered monkey and other locally endemic subspecies. roloway monkey (Cercopithecus diana roloway) Primate Conservation 17: 138-144. in Dadieso Forest Reserve, Ghana. African Oates, J.F., M. Abedi-Lartey, W. McGraw, T.T. Primates 8: 9-16. Struhsaker & G.H. Whitesides. 2000. Extinction Young, C. & R.H. Horwich. 2007. History of of a West African red colobus monkey. protected area designation, co-management Conservation Biology 14(5): 1526-1532. and community participation in Belize. In Ojha, H.R. 2011. The evolution of institutions for Taking Stock: Belize at 25 Years of Independence. multi-level governance of forest commons: the B.S. Balboni & J.O. Palacio, eds. Cubola Books, case of community forest user groups federation Benque Viejo del Carmen, Belize. Pp. 123-150. in Nepal. In Sustaining Commons: Sustaining Our Future. 13th IASC International Conference. January 2011. Roberts, D.L. & A.C. Kitchener. 2006. Inferring Received: 5 December 2014 extinction from biological records: were Accepted: 27 July 2015 African Primates 10: 41-52 (2015)/ 41

Why Don’t Chimpanzees Eat Monitor Lizards?

William C. McGrew

Division of Biological Anthropology, Department of Archeology and Anthropology, University of Cambridge, UK

Abstract: Chimpanzees (Pan troglodytes) do not eat monitor lizards (Varanus spp.), despite these reptiles appearing to be suitable prey. At least 10 hypotheses might explain this lack of predation and consumption by the apes: (1) availability, (2) habitat, (3) abundance, (4) size, (5) edibility, (6) danger, (7) difficulty, (8) incongruence, (9) optimality, (10) taboo. These are tested via data collected on encounters with monitors while seeking wild chimpanzees at Mt. Assirik, Senegal, and by using published ethnographic data on wild chimpanzees and human foragers. The eight behavioral ecological hypotheses fall short of explaining the absence of monitors in the chimpanzee diet, but the two remaining hypotheses remain to be tested adequately. Chimpanzees ‘should’ eat monitor lizards.

Key words: Pan troglodytes, Varanus, predation, diet, Squamata

Résumé: Pourquoi les chimpanzés ne mangent-t’ils pas le varan ? Même si ces reptiles semblent être une proie adaptée, les chimpanzés (Pan troglodytes) ne consomment pas de varans (Varanus spp.). Au moins 10 hypothèses peuvent expliquer l’absence de prédation et de consommation de varans par les grands singes : (1) la disponibilité, (2) l’habitat, (3) l’abondance, (4) la taille, (5) la comestibilité, (6) le danger, (7) la difficulté, (8) la sur-généralisation, (9) l’optimalité, (10) le tabou. Ces hypothèses sont testées à partir (1) de données enregistrées lors de rencontres avec des varans par les chercheurs à la recherche de chimpanzés sauvages au Mt. Assirik, Sénégal, et (2) de documentations ethnographiques publiées sur les chimpanzés sauvages et les chasseurs-cueilleurs humains. Les huit hypothèses écologiques ne peuvent expliquer l’absence du varan dans le régime alimentaire des chimpanzés, mais les deux hypothèses alternatives restent à vérifier. Les chimpanzés « devraient » manger le varan.

Mots-clés: Pan troglodytes, Varanus, prédation, régime alimentaire, Squamata

INTRODUCTION

Chimpanzees (Pan troglodytes) are omnivores 2015) or predatory crocodilians (McGrew 2014). that consume a wide variety of plants and animals. Given that chimpanzees stalk, pursue, subdue, kill, Their range of faunivory covers multiple orders of eat, share, and occasionally scavenge mammals and mammals, birds and insects but notably absent are birds of similar body-size to some reptiles, then why reptiles (but for one case of eating a shed snake skin, do not medium-sized monitor lizards (Varanus spp., see McGrew et al. 1978). There is no a priori reason Varanidae) feature in the apes’ diet? why this class of vertebrates should be ignored, Monitor lizards are a cosmopolitan family of although the hazards are obvious of obtaining certain lizards (Squamata) found naturally in Africa, Asia, types of reptile, such as venomous snakes (McGrew and Oceania, including Australia. The genus Varanus

Correspondence to: William C. McGrew, Division of Biological Anthropology, Department of Archaeology and Anthropology, University of Cambridge, Cambridge CB2 1QH, UK; Phone: +44 1223 764706; E-mail: [email protected]. 42 / McGrew

includes 75–80 species, depending on taxonomic too risky to prey upon, then monitors might be classification. Body-size in living species ranges avoided by mistake. up to 3 m long (the famous Komodo dragon, V. 9. Optimality. Chimpanzees that obtain enough komodoensis); body weight varies similarly. Monitor animal matter in the diet from other, better lizards are basically faunivorous (Losos & Greene sources might not need to go after monitors. 1988); most are terrestrial but some are semi-aquatic 10. Taboo. Chimpanzees might have socially learned or arboreal (Pianka 1994a, b; Figure 1). As short- cultural prohibitions from eating monitor lizards. legged, diurnal quadrupeds, they would seem to be promising candidate prey for chimpanzees. If all but one of these hypotheses can be falsified, Humans eat monitor lizards widely, in Africa (Lee then the remaining one is the most likely of these 1979, Silberbauer 1981, Tanaka 1976), New Guinea alternative explanations for why chimpanzees do (Hide et al. 1984, Iyai et al. 2011), and especially not eat monitor lizards. If two or more cannot be Australia (Meehan 1982, Mountford 1960). For falsified, then further, focused data should be sought example, the sand monitor lizard (V. gouldii) is a to distinguish among the remaining alternatives. If keystone food species for Aborigines in the Western all of the hypotheses can be falsified, then further Desert, who selectively burn patches of vegetation to research, both empirical (more data) and conceptual increase hunting returns (Bird et al. 2013). Monitors (new hypotheses) is needed. At present, I know of figure prominently in the diets of humans living in no prior study seeking to link chimpanzees and arid environments, e.g., southern Africa, the !Kung monitor lizards, despite the former’s behavior in San hunt Varanus, as do the Gwi San and #Kade San. nature having been studied for more than 50 yr. This paper aims to test 10 hypotheses that might account for the lack of predation by chimpanzees on monitor lizards. In brief, these hypotheses METHODS relate to: 1. availability; 2. habitat; 3. abundance; 4. size; 5. edibility; 6. danger; 7. difficulty; 8. over- The Stirling African Primate Project studied generalization; 9. optimality; and 10. taboo. The unhabituated wild chimpanzees (Pan troglodytes rationales for these hypotheses are: verus) at Mt. Assirik, in the Niokolo-Koba National Park in southeastern Senegal, from February 1. Availability. Although the species ranges of 1976 to December 1979. Assirik is a hot, dry and chimpanzees and monitors in Africa are both mosaic ecosystem dominated by grassland and large, they might be locally allopatric. If they do open, deciduous woodland (McGrew et al. 1981; not meet, then neither can interact with, much Figure 2). During the study period, it had a median less eat, the other. annual rainfall of 885 mm, and daily maximum air 2. Habitat. Although the two taxa might occur temperatures ranged from mean monthly highs of in the same locale, they might exploit different 35 degrees C to lows of 23 C. habitat-types, so that they never or rarely Observers seeking chimpanzees focussed their encounter one another at close quarters. activities on ribbons of gallery forest along seasonal 3. Abundance. Although both taxa might occupy watercourses, which although comprising only 3% a similar range of habitats in a given locale, of the 50 km2 study area, yielded most (54%) of the monitor lizards might be too few in number to chimpanzee contacts (Tutin et al. 1983). Observers interest chimpanzees. spent each working day walking through various 4. Size. Although some monitor species are large types of habitat, opportunistically searching for, enough to make a meal, sympatric species might tracking, and observing chimpanzees. Overall, the be too small to be of interest to chimpanzees. median number of days spent in the field per month 5. Edibility. Although available in sufficient was 27 (range: 12–31). When a monitor lizard was numbers and weight, monitors might taste bad sighted, we recorded date, location, and habitat type; or might lack sufficient nutritional content. almost all the sightings were terrestrial. 6. Danger. Obtaining monitors might entail too Many encounters with monitors were fleeting, much risk of morbidity or even mortality. consisting of a minimal, momentary sighting before 7. Difficulty. Monitors might be too hard to catch the lizard disappeared into the undergrowth, or less and subdue. commonly, into the water. This made it virtually 8. Over-generalization. Monitors might too closely impossible to obtain photographic vouchers for resemble snakes in appearance, and if snakes are species identification. (Without identification, we Chimpanzees and Monitor Lizards / 43

c. Figure 1. African monitor lizards (a) on land, (b) in vegetation, and (c) in water: a. Mahale Mountains National Park, Tanzania. Probably Varanus niloticus or V. albigularis. Photograph by M. Nakamura; b. Dja Biosphere Reserve, Cameroon. Probably V. niloticus or V. ornatus. Photograph by I. Deblauwe; c. Ruaha National Park, Tanzania. Probably V. niloticus or V. albigularis. Photograph by A. Nicholas. 44 / McGrew

Figure 2. Deciduous wooded grassland at Mt. Assirik, Senegal, with green riverine forest in background. Photograph by W.C. McGrew.

could work only at the level of genus, so data for At a subsample of sites (n=9), I sought corroborating two species, V. niloticus and V. exanthematicus are answers independently from two field workers; pooled here. A third species, V. ornatus, is primarily many persons provided unsolicited further details, found in Central Africa, with only one record from which were useful. Of the 38 sites queried, 33 (87%) Senegal. See Bayless 2002). responded. Often in the dry season, we were alerted to monitors by the distinctive sound of them moving off through the dry leaf litter. Our encounters RESULTS cannot be compared with randomised transects, and lacking individual identification, a lizard seen 1. Availability today also could have been seen the day before. We Perhaps the crudest measure is national sympatry. recorded only one encounter per location per day, Much overlap in distribution exists between the seeking to avoid duplication and data inflation. five recognised African species of Varanus and Records were biased toward habitat types favoured chimpanzees (Bayless 2002). V. niloticus is found by chimpanzees, as they were the primary objects in all 26 countries in which chimpanzees now or of study. These caveats make the data set a non- recently occurred, while V. exanthematicus occurs random sample, but at least it proxies as closely as in 20 such countries, V. ornatus in 15 countries, possible the apes’ exposure to monitor lizards, given V. griseus in 5 countries, and V. albigularis in 4 that we saw no encounters between chimpanzees countries (Table 1). All but two chimpanzee habitat and monitors. countries have more than one species of monitor I sent an email enquiry to field workers from as available (median number of monitor species = 2, many chimpanzee study sites as possible, asking only range = 1–4). two questions: (1) ’Are there monitor lizards at your A more precise indicator of sympatry is presence study site?’, and (2) ‘Do the chimpanzees eat monitor or absence of monitor lizards at field sites where lizards?’ If the answer to (2) was no, but there were chimpanzees have been studied long term, as noted other pertinent observations, such as chimpanzees by field primatologists. Of 33 field sites reporting, chasing monitors, I asked for additional information. all but eight have monitors. Five of the eight sites Chimpanzees and Monitor Lizards / 45

Table 1. Range overlap between Varanus spp. and Pan troglodytes in sub-Saharan Africa and list of chimpanzee study sites reporting Varanus data, by country.

Countries with V. niloticus V. exanthematicus V. ornatus V. griseus V. albigularis Chimpanzee study wild chimpanzees (n = 40) (n = 24) (n = 16) (n =13) (n =17) sites (n = 33) (n = 26) Angola (Cabinda) ✓ ✓ ? Maiombe Benin ✓ ✓ Burkina Faso ✓ ✓ ✓ Burundi ✓ Cameroon ✓ ✓ ✓ ✓ Ebo, La Belgique Central Afr. Rep. ✓ ✓ Congo Rep. ✓ ✓ ✓ Goualougo Congo Dem. Rep. ✓ ✓ ✓ ✓ Bili, Kahuzi-Biega Gabon ✓ ✓ ✓ Loango, Lopé, Moukalaba Gambia ✓ ✓ ✓ Abuko Ghana ✓ ✓ ✓ Guinea-Bissau ✓ ✓ ✓ Cantanhez Guinea Equatorial ✓ ✓ Guinea Rep. ✓ ✓ Bossou, Nimba Ivory Coast ✓ ✓ TaÏ Liberia ✓ ✓ ✓ Sapo Mali ✓ ✓ ✓ Bafing Niger ✓ ✓ ✓ Nigeria ✓ ✓ ✓ Gashaka Rwanda ✓ Nyungwe Senegal ✓ ✓ ✓ Assirik, Fongoli Sierra Leone ✓ ✓ ✓ Tenkere Sudan (South) ✓ ✓ ✓ ✓ Tanzania ✓ ✓ Gombe, Issa, Mahale, Rubondo Togo ✓ ✓ ✓ Uganda ✓ ✓ ✓ Budongo, Bulindi, Bwindi, Kalinzu, Kanyawara, Kasokwa, Ngogo, Toro-Semliki

Total 26 20 15 5 4

n = number of African countries containing species; ✓= Varanus present 46 / McGrew

lacking Varanus (Budongo, Bwindi, Kalinzu, formula to Varanus, the probability of an encounter Kanyawara, Toro-Semliki) are in Uganda, but in the with chimpanzees was 0.45, ranking it third most same country, Bulindi, Kasokwa and Ngogo do have likely by comparison with 19 species of medium- monitor lizards. The sites reporting cover all four sized mammals. subspecies of chimpanzee (Table 2), and they come It seems that chimpanzees have plenty of chances from 18 of the 26 (69%) range countries for Pan to encounter monitor lizards. troglodytes. (Sympatry also occurs elsewhere, where neither species has been studied in detail, such as 3. Abundance Comoe National Park, Ivory Coast, Muehlenberg Even when monitor lizards are present and & Steinhauer n.d.) However, few chimpanzee study likely to be encountered, they might not be worth sites report on their herpetofaunas (for an exception, preying upon if they are too scarce. Basic optimal see McGrew 2014, 2015), and almost none name foraging theory suggests that rare prey species will their monitor species. be superseded by more common ones, all other Conclusion: It seems that most chimpanzees have things being equal, and plenty of mammalian prey access to monitor lizards. are available, at least at some chimpanzee field sites, including Assirik (McGrew et al. 2014). However, 2. Habitat I can find no published data on the abundance of Chimpanzees occur in a wide variety of ecotypes monitor lizards at other chimpanzee field sites, from savanna to rainforest, and most points in collected by either primatologists or herpetologists. between (McGrew et al. 1981; Stanford 1998). In At Assirik, we systematically noted encounters East and West Africa, populations of the same with monitor lizards over a continuous 12-month subspecies span this range of vegetation types, period, from October 1978 – September 1979. often within the same area, in mosaics that may Over 339 field days, we encountered 243 monitor include all the types found in the species range. For lizards, for a mean contact rate of a lizard every 1.4 example, Toro-Semliki Wildlife Reserve in western days. Field days varied in length, so more complete Uganda includes evergreen gallery forest, deciduous encounter data based on full 12-hr (dawn to dusk) woodland of both open and closed canopy, Acacia- field days would yield a frequency higher than 1.4. dominated scrub, tall grassland, and swamp (Hunt & Most days with sightings were of a single lizard, but McGrew 2002). At most of these sites, chimpanzees on 45 days, two or more lizards were encountered use all of these vegetation types, albeit to different (median = 1, range = 1–8). extents, as was the case at Mt. Assirik (Baldwin et Monitors were met in each of the 12 months al. 1982). (monthly median = 12 lizards, range = 5–31), Varanus exploits an even wider range of habitats, but encounter rate varied seasonally: Dry (June extending into true desert and also aquatic habitats. –October, n = 196 field days) = every 1.1 days vs. The most widely-distributed African species, V. Wet (November–May, n = 143 field days) = every 2.0 niloticus, is equally at home on land or in the trees or days (N=339 days, Chi-squared test, df =1, Chi2 = in the water (Cisse 1972). 18.24, p < 0.001). Thus, monitors were met almost Assirik is the only site that provides data that twice as often in the 7 months of the dry season than more precisely put ape and lizard in the same places: in the 5 months of the rainy season, perhaps because overall chimpanzees were encountered there 55% of their greater detectability when moving through of times in forest, 31% in woodland, and 14% in the dry leaf litter. grassland. Comparable figures for monitors were: It seems that monitor lizards are abundant 68% forest, 20% woodland, and 12% grassland. enough to be worth preying on. All monitors were first encountered on land in the daytime. McGrew et al. (2014) presented a 4. Size formula by which sightings of wild chimpanzees As a genus, Varanus varies hugely in body size, at Assirik could be compared with those of other at least as manifest in wild-caught body length. mammals, across habitat types. It calculates the (Herpetologists normally measure this by snout- relative probability of two species meeting as a vent length (SVL), that is, from the tip of the function of observers encountering each species in ‘nose’ to the cloaca, thus excluding the tail. Such forest, woodland, and grassland. For example, the measurement requires handling the lizard, which probabilities of Assirik chimpanzees encountering we did not do at Assirik.) The within-genus size leopard (Panthera pardus) versus lion (P. l e o ) were range of this lizard radiation is almost five orders 0.47 vs. 0.29, a substantial difference. Applying this of magnitude, equivalent to that of a mouse and an Chimpanzees and Monitor Lizards / 47 Table 2. Field sites of chimpanzee research (n = 33) reporting on presence/absence of monitor lizards (Varanus spp.) and their consumption by chimpanzees. Monitors Monitors Field Site Country Sub-species Comments present? eaten? Abuko Gambia Ptv YN Sanctuary Assirik Senegal Ptv Y N NP Bafing Mali Ptv YN Bili Congo Dem. Rep. Ptt YN Bossou Guinea Rep. Ptv YN Budongo Uganda Pts N N Bulindi Uganda Pts YN Bwindi Uganda Pts N? N NP Cantanhez Guinea-Bissau Ptv Y N NP Ebo Cameroon Ptt YN Fongoli Senegal Ptv YN Gashaka Nigeria Pte Y N Gashaka-Gumti NP Gombe Tanzania Pts Y N NP Goualougo Congo Rep. Ptt YN Nouabalé-Ndoki NP Issa Tanzania Pts YN Kahuzi-Biega Congo Dem. Rep. Pts N N NP Kalinzu Uganda Pts N N Kanyawara Uganda Pts N N Kibale NP Kasokwa Uganda Pts YN La Belgique Cameroon Ptt YN Dja Loango Gabon Ptt Y N NP Lopé Gabon Ptt Y N NP Mahale Tanzania Pts Y N NP Maiombe Angola Ptt YN Cabinda Moukalaba Gabon Ptt N N NP Ngogo Uganda Ptt Y N Kibale NP Nimba Guinea Rep. Ptv YN Nyungwe Rwanda Pts Y N NP Rubondo Tanzania ?? Y N NP, colonized Sapo Liberia Ptv Y N NP TaÏ Ivory Coast Ptv Y N NP Tenkere Sierra Leone Ptv Y N NP Toro-Semliki Uganda Pts N N NP = national park, Pte = Pan troglodytes ellioti, Pts = P. t. schweinfurthii, Ptt = P. t. troglodytes, Ptv = P. t. verus. All sources are personal communications from individuals named in the Acknowledgements, or my unpublished observations. 48 / McGrew

Figure 3. Varanus exanthomaticus en route to market, Nigeria. Photograph by J. Wallis.

elephant (Pianka 1995). Given that half (22 of 44) of 5. Edibility the living Varanus species have SVL of less than 35 Prey should be palatable and yield enough energy cm (Pianka 1995, Table 1), then many might be too or nutrients to be of interest to a predator. Some small to be on interest to a medium-bodied predator monitors, such as V. komodoensis, have toxic saliva, such as a chimpanzee. However, all five African and their closest living relatives, the Helodermatidae, species average SVL of 49 cm or longer; worldwide, are venomous (Pianka 1995). Thus, monitors might V. niloticus ranks 4th of 44 species at 78 cm; if the tail be unsuitable for consumption, especially if eaten length is added, the actual body length may double raw. However, neither of these potential constraints to ca. 150 cm. If smaller, juvenile monitors were applies to the five African Varanus. preferable, then presumably they would be more Direct assessment of edibility for chimpanzees easily dispatched. cannot be assessed, given the absence of data on More pertinent to a predator might be the body- predation. However, data on consumption by weight of a potential prey, especially in terms of soft sympatric humans provides a proxy measure (Figure tissue. De Buffrenil and Hemery (2002) sampled 3). Asibey’s (1974) data on bush meat sales in a three populations of V. niloticus from Lake Chad; Ghanaian market showed Varanus to average USA $ their largest sample (n = 336) had a median live 0.30 per pound in cost, which was the same price as body mass of 4.7 kg. Asibey (1974) provided weights bushbuck (Tragelaphus scriptus) and slightly lower for 203 Varanus on sale in a bushmeat market in than that of red river hog (Potamochoerus porcus). Accra Ghana; these averaged 4.2 kg. For comparison On Bioko Island, Equatorial Guinea, V. niloticus with other vertebrate prey taken by chimpanzees, ranked fourth in human preference for bushmeat, the bushbaby species (Galago senegalensis) taken after two species of rodents and one of duiker, of by Senegalese chimpanzees at Fongoli (Pruetz & 55 species available in markets there (Fa et al. 2002, Bertolani 2007) weighs less than 1 kg. The weight Table II). Reptiles, including Varanus, provided up to of a young duiker (Cephalophus spp.) probably 13.5% percent of the total diet by weight and 15.6% approximates to that of a typical adult monitor. of total protein, second only to fish, for northern It seems that African monitor lizards are big Australian Aborigines (Meehan 1982, p. 152). Not enough to be worth pursuing. all human foragers eat Varanus, such as the Hadza of Tanzania (Marlowe 2010, p. 102). Comprehensive Chimpanzees and Monitor Lizards / 49 analyses of why some humans do but others do not such as land to water, which may make them more is beyond the scope of this paper. elusive to less amphibious predators. They also ‘go to I can find no published data on composition ground’, seeking refuge in burrows, thus frustrating of African monitors, but quantitative data are non-fossorial pursuers. None of these tactics seem available on Australian ones. Miller et al. (1993, insuperable to chimpanzees, who commonly catch Table 3) provided data on several unspecified types fast-moving prey, both terrestrial (e.g., duikers) of Varanus. Mean values per 100 g of edible portion and arboreal (e.g., squirrels). Aquatic monitors of flesh, cooked, were: 1579 kJ of energy, 16.5 g of might well frustrate chimpanzees, however. All of protein, and 33.8 g of fat for one species, and 821 this speculation is moot, as no one has reported kJ, 30.5, and 7.2 g for another. No data on raw food chimpanzees even trying to catch monitor lizards, were given. Miller et al. also gave comparable values much less succeeding. for mammalian species of similar body size, hunted Lacking data on chimpanzees seeking to capture and eaten by Australian aborigines. For example, and to subdue monitors, one can turn again to the cooked flesh of the northern brushtail possum human foragers who hunt monitors. Many of the (Trichosurus arnhemensis) yielded 703 kJ, 33.6 g of techniques used by Australian Aborigines to get protein, and 3.5 g of fat, which is a similar or inferior monitors (e.g., Australian Institute of Aboriginal yield to the values for Varanus. Studies 1966) are available to chimpanzees, such as It seems that African monitor lizards are worth capture by bare hands, excavation by digging stick, eating. and even spearing. Men and women, adults and children, all gathered goannas (Varanus) (Meehan 6, Danger 1982, p. 35). Roth (1901) reported the inhabitants Monitors might be too dangerous to secure as of Princess Charlotte Bay to spear monitors and to potential prey. Although African monitors lack extract them from burrows or hollow logs, after first venom or toxic saliva, as top predators, they have inserting a vegetative probe to test the occupancy effective, pointed teeth and sharp, powerful claws. of the cavity. Varanus was among a variety of Thus, in principle, they might inflict potentially reptilian prey caught and roasted by Arnhem Land health-threatening wounds on a chimpanzee Aborigines, e.g., water snakes, long-necked turtles, that handled them, which, if infected might yield etc. (Mountford 1960, p. 113ff). morbidity, or even mortality. Finally, big monitors Chimpanzees catch most prey by hand, even might be potential predators on chimpanzees, but as arboreal squirrels, but they also use sharpened sticks shown above, the body sizes of the African monitors to probe and to spear/skewer bushbabies (Galago are too small to present such a threat. senegalensis) in their tree-holes (Pruetz & Bertolani Lacking behavioral data on such handling, one 2007). Chimpanzees also use digging sticks to obtain again turns to humans. Australian Aborigines, subterranean food-items (Hernandez-Aguilar et al. including children, of the Western Desert catch 2007). Killing prey by bashing their heads against small monitors by hand on the surface and extract hard objects or the substrate is common to both larger ones from their burrows by digging and then humans and apes. Finally, several field researchers, reaching inside to grab the prey (Australian Institute including the author, have caught monitor lizards for Aboriginal Studies 1966). Cine footage shows by hand, despite our being slower movers than this to be done without signs of injury to the human chimpanzees. handler. By comparison, some chimpanzees subdue It seems that monitor lizards are obtainable and and consume adult male monkeys possessing manageable by chimpanzees. notable canine teeth, e.g., Procolobus spp., apparently without concern for possible injury, suggesting that 8. Over-generalization they could safely handle monitors. Monitors are the most serpentine of limbed It seems that monitor lizards are safe enough to lizards, with their long, thin body shape and some hunt. particular snake-like characteristics: Varanids are one of the few lizards with flicking, forked tongues 7. Difficulty (Pianka 1994b). The larger body-sized forms lie Monitor lizards are fast runners on the ground in wait as ambush predators, as do many snakes. but seem to be less swift in undergrowth or canopy Further, in Africa, monitors are the only lizards large or water, although I can find no quantitative data enough to be mistaken for the only snake genus on any of these variations in locomotion. Further, large enough to prey on chimpanzees, Python. Thus, they quickly move from one medium to another, they might be avoided by perceptual confusion; 50 / McGrew

or perhaps chimpanzee almost-total avoidance of monitor lizard consumption versus other animal reptilian prey is prudent caution. foodstuffs. However, Varanus’ tetrapod anatomy is clearly It seems that monitors cannot be excluded yet visible, unlike other lizards (e.g., Anguidae, ‘glass from chimpanzee diet on grounds of optimality. snakes’) that lack external limbs. Further, their locomotion is typically quadrupedal, with a usual 10. Taboo vertebrate running gait, and so is totally unlike the Human beings universally impose dietary sinuous locomotion of snakes. constraints upon themselves (Aunger 1996). These It seems unlikely that chimpanzees would mistake taboos have in common various mechanisms of monitor lizards for snakes. social sanctions, often starting in child-rearing. Some of these food avoidance customs seem arbitrary 9. Optimality (e.g., ‘we eat goats but not sheep’), and some even All wild chimpanzee populations studied in may lead to nutritional deficits that compromise the long-term show faunivory, and most consume fertility. Reptiles are among the animals often vertebrate prey, largely mammals and birds. tabooed, for example in north Australia (Altman However, no systematic comparison has been done 1987, p. 177). To show satisfactorily the existence across a wide range of study sites with regard to the of a food taboo requires more than data on eating varied sources of nutrients from animal prey that are behaviour, as other, less cognitive explanations may contained in the apes’ diets. Furthermore, relative suffice, such as optimal foraging theory (as above). availability of types of animal prey has not been Anthropological studies of food taboos usually rely investigated comprehensively and quantitatively. on verbal-self-report from informants, but these Lacking these basic data, the optimality hypothesis data are unavailable from non-linguistic subjects. cannot be tested properly. It may be that the costs Instead, we can seek to infer the operation of certain of preying on Varanus (pursuit, capture, processing, elements of cognition that might contribute to consumption, etc.) are greater than those for a taboo formation, such as arbitrary conformity based comparable mammal, but no evidence has been on social learning, as seen in wild vervet monkeys presented. (Chlorocebus aethiops) (van de Waal et al. 2013). However, consider this specific if limited Such effects have been demonstrated in captive example: red colobus monkeys (Procolobus spp.) are chimpanzees (see Whiten et al. 2005 for a review) the most-often-eaten species of mammalian prey but have not been studied in wild chimpanzees. for wild chimpanzees across the apes’ species range So, whether or not chimpanzee forbearance to eat (Stanford 1998). In some cases, colobus represent monitor lizards results from a cultural taboo remains the majority of prey consumed, and whenever the to be seen. two species are sympatric, red colobus rank first in Information to test this hypothesis is currently preference. So, chimpanzee populations that lack lacking. red colobus might be more inclined to eat monitors, or those that lack monitor lizards might be more inclined to eat red colobus (all other things being DISCUSSION equal). Neither is the case: chimpanzee populations lacking red colobus (e.g., Assirik, Bossou, Fongoli) Trying to ‘prove’ the negative is scientifically refrain from eating available monitors, just as do perverse, given that it is logically impossible. One high-colobus-consuming populations (Gombe, can never eliminate all of a potentially infinite Mahale, Ngogo). Further, populations lacking number of factors that might account for an monitors (Budongo, Kalinzu, Kanyawara) eat no or absence. (Consider the difference between testing no more red colobus (or other monkeys) than do these two hypotheses: ‘All swans are white’ versus populations that have monitors available (Gashaka, ‘No swans are black’.) Thus, the titular aim of this Goualougo, Tai). There seems to be no link between paper is questionable, in logical positivist terms, these two prey taxa, one proven vs. the other but such efforts, although ultimately doomed, may potential, but similar analyses remain to be done for be informative. To put it simply, if something seems other chimpanzee prey. like it should happen, but does not, then it is worth Although consumption of Varanus is mentioned investigating, as chimpanzees cannot help but notice in passing for several African foraging societies (Lee monitor lizards. 1979, p. 228, Silberbauer 1981, p. 74; Tanaka 1976, p. Of the 10 hypotheses posed, all but two seem 119), no source gives sufficient information to rate at least notionally falsified: The lizards are widely Chimpanzees and Monitor Lizards / 51 available to the apes (Hypothesis 1). They occupy the Wallis, David Watts, Elizabeth Williamson, same habitats (2). They are accessible and plentiful Richard Wrangham, Juichi Yamagiwa for providing (3). They are big enough prey (4). They are edible information on monitor lizards at chimpanzee field (5). They are safe to secure (6). They are catchable sites; Isra Deblauwe, Michio Nakamura, Aaron (7). They are recognizable (8). Nicholas, and Janette Wallis for photographs; Robert Hypotheses (9) and (10) cannot yet be tested: Attenborough and Robin Hide, for providing source There are insufficient data on lizards versus other material on Australian and New Guinean monitor sympatric prey to know what the apes ‘should’ eat, lizards; Robert Attenborough, Jim Moore, Aaron in optimal foraging terms. At Assirik, colobine Nicholas, Alejandra Pascual-Garrido, Janette monkeys are absent but present are a wide range of Wallis and three anonymous reviewers for critical African carnivores (lion, leopard, wild dog, spotted comments on the manuscript; Agumi Inaba for help hyena, side-striped jackal, ratel, etc.) (McGrew et al. in manuscript preparation; Marian Verhaeren for 2014). Thus, chimpanzees would have to compete French translation of the abstract. with these predators for a wide range of vertebrates, including monitor lizards. Until comprehensive ecological data are available on both predators and LITERATURE CITED prey that co-exist with chimpanzee, the optimality hypothesis remains viable. Altman, J.C. 1987. Hunter-gatherers Today: The taboo hypothesis is even more daunting. An Aboriginal Economy in North Australia. Until we have evidence of this cognitively-based Australian Institute of Aboriginal Studies, sanction being applied directly, that is, behaviorally, Canberra. or until ingenious proxy measures are invented, Asibey, E.O.A. 1974. Wildlife as a source of the phenomenon is opaque. Lacking access to the protein in Africa south of the Sahara. Biological individual, much less the collective, consciousness Conservation 6: 32-39. of the apes, we are unable even to assess probabilities Aunger, R. 1996. Acculturation and the persistence of the existence or not of dietary taboos. of indigenous food avoidances in the Ituri Forest, So, what can be said in summing up? There seems Zaire. Human Organization 55: 206-218. to be no good ecological reason why chimpanzees Australian Institute of Aboriginal Studies. 1966. do not eat monitor lizards, so perhaps we should Desert People. Black and white film, 52 min. look elsewhere for an explanation, either to new data Baldwin, P.J., W.C. McGrew & C.E.G.Tutin. 1982. or new hypotheses. Wide-ranging chimpanzees at Mt. Assirik, Senegal. International Journal of Primatology 3: 367-385. ACKNOWLEDGEMENTS Bayless, M.K. 2002. Monitor lizards: A pan- African check-list of their zoogeography Thanks to: Direction des Parcs Nationaux du (Sauria: Varanidae: Polydaedalus). Journal of Senegal for permission to do field research in Biogeography 29: 1643-1701. the Parc National du Niokolo-Koba; American Bird, R.B., N. Taylor, B.F. Codding & D.W. Bird. Philosophical Society, Carnegie Trust for the 2013. Niche construction and dreaming Universities of Scotland, Leakey Foundation, Science logic: Aboriginal patch mosaic burning and Research Council (UK), Wenner-Gren Foundation varanid lizards (Varanus gouldii) in Australia. for Anthropological Research for funding; 15 Philosophical Transactions of the Royal Society, B colleagues, especially Caroline Tutin and the late 280: 20132297. Pamela Baldwin, for collecting data at Mt. Assirik; de Buffrenil, V. & G. Hemer. 2002. Variation in Rosalind Alp, Joana Bessa, Isra Deblauwe, Chris longevity, growth, and morphology in exploited Duvall, Takeshi Furuichi, Chie Hashimoto, Cleve Nile monitors (Varanus niloticus) from Sahelian Hicks, Mike Huffman, Kevin Hunt, Kat Koops, Africa. Journal of Herpetology 36: 419-426. Lydia Luncz, Tetsuro Matsuzawa, Matt McClennan, Cisse, M. 1972. L’alimentaire des varanides du Bethan Morgan, Liza Moscovice, Josephine Senegal. Bulletin d’Institut Fondamental Afrique Msindai, Michio Nakamura, Rob O’Malley, Chris Noire 34: 503-515. Orbell, Alejandra Pascal-Garrido, Alex Piel, Andy Fa, J.E., J. Juste, R.W. Burn & G. Broad. 2002. Plumptre, Klara Petrzelkova, Vernon Reynolds, Bushmeat consumption and preferences of two Crickette Sanz, Volker Sommer, Craig Stanford, ethnic groups in Bioko Island, West Africa. Fiona Stewart, Nikki Tagg, Caroline Tutin, Janette Human Ecology 30: 397-416. 52 / McGrew

Hernandez-Aguilar, A., J. Moore& T.R. Pickering. Meehan, B. 1982. Shell Bed to Shell Midden. Australian 2007. Savanna chimpanzees use tools to harvest Institute of Aboriginal Studies, Canberra. the underground storage organs of plants. Miller, J.B., K.W. James & P.M.A. Maggiore. 1993. Proceedings of the National Academy of the United Tables of Composition of Australian Aboriginal States of America 104: 19210-19213. Foods. Aboriginal Studies Press, Canberra. Hide, R.L., J.C. Pernetta & T. Senabe. 1984. Utilization Mountford, C.P. 1960. Records of the American- of wild animals. In South Simbu: Studies in Australian Scientific Expedition to Arnhem Demography, Nutrition, and Subsistence. R. L. Land. 2. Anthropology and Nutrition. Melbourne Hide, ed. Research Report of the Simbu Land University Press, Melbourne. Use Project Vol. VI. Institute of Applied Social Muehlenberg, M. & B. Steinhauer. n.d. Parc National and Economic Research, Port Moresby, Pp. 291- de la Comoe. Abidjan. [national park guide book, 379. date and publisher not given] Hunt, K.D. & W.C. McGrew. 2002. Chimpanzees in Pianka, E.R. 1994a. Comparative ecology of Varanus the dry habitats of Assirik, Senegal and Semliki in the Great Victoria Desert. Australian Journal Wildlife Reserve, Uganda. In Behavioural of Ecology 19:395-408. Diversity in Chimpanzees and Bonobos. C. Pianka, E.R. 1994b. The Lizard Man Speaks. Boesch, G. Hohmann & L.F. Marchant, eds., University of Texas Press, Austin. Cambridge University Press, Cambridge, Pp. 35- Pianka, E.R. 1995. Evolution of body size: Varanid 51. lizards as a model system. American Naturalist Iyai, D.A., A.G. Murwanto & A.M. Killian. 2011. 146: 398-414. Hunting and ethnozoology systems of monitor Pruetz, J.D. & Bertolani, P. 2007. Savanna lizards (Fam. Varanidae) utilized by Yaur tribe chimpanzees hunt with tools. Current Biology 17: at National Park of Cenderawasih Gulf. Biota 16: 412-417. 278-286. Roth, W.E. 1901. Food: its search, capture and Lee, R.B. (1979) The !Kung San. Men, Women, and preparation. North Queensland Ethnography Work in a Foraging Society. Cambridge University Bulletin, 3: 1-34. Press, Cambridge. Silberbauer, G.B. 1981. Hunter and Habitat in the Losos, J.B. & H.W. Greene. 1988. Ecological and Central Kalahari Desert. Cambridge University evolutionary implications of diet in monitor Press, Cambridge. lizards. Biological Journal of the Linnean Society Stanford, C.B. 1998. Chimpanzee and Red Colobus. 35: 379-407. The Ecology of Predator and Prey. Harvard Marlowe, F.W. 2010. The Hadza. Hunter-gatherers University Press, Cambridge, MA. of Tanzania. University of California Press, Tanaka, J. 1976. Subsistence ecology of the Central Berkeley. Kalahari San. In Kalahari Hunter-gatherers. McGrew, W.C. 2014. Encountering crocodiles while Studies of the !Kung San and Their Neighbors. Lee chasing chimpanzees. Pan Africa News 21: 2-3. R.B. & I. DeVore, eds. Harvard University Press, McGrew, W.C. 2015. Snakes as hazards: modelling Cambridge, MA, Pp. 98-119. risk by chasing chimpanzees. Primates 56: 107- Tutin, C.E.G., W.C. McGrew & P.J. Baldwin. 111. 1983. Social organization of savanna-dwelling McGrew WC, P.J. Baldwin, L.F. Marchant, J.D. chimpanzees, Pan troglodytes verus, at Mt. Pruetz & C.E.G. Tutin. 2014. Chimpanzees (Pan Assirik, Senegal. Primates 24: 154-173. troglodytes) and their mammalian sympatriates: van de Waal, E., N. Cladiere & A. Whiten. 2013. Mt. Assirik, Niokolo-Koba National Park, Potent social learning and conformity shape a Senegal. Primates 55: 525-532. wild primate’s foraging decisions. Science 340: McGrew, W.C., P.J. Baldwin & C.E.G. Tutin. 1981. 483-485. Chimpanzees in a hot, dry and open habitat: Mt. Whiten, A., V. J. Horner & F.B.M. de Waal. 2005. Assirik, Senegal, West Africa. Journal of Human Conformity to cultural norms of tool use in Evolution 10: 227-244. chimpanzees. Nature 437: 737-740. McGrew, W.C., C.E.G. Tutin, P.J. Baldwin, M.J. Sharman & A. Whiten. 1978. Primates preying upon vertebrates: new records from West Africa. Received: 18 June 2015 Carnivore 1: 41-45. Accepted: 2 November 2015 African Primates 10: 53-56 (2015)/ 53 Brief Communication:

Barbary Macaque Group Size and Composition in Bouhachem Forest, North Morocco

Siân Waters1,2, Ahmed El Harrad2, Mohamed Chetuan2, and Zouhair Amhaouch3

1Department of Anthropology, Durham University, UK; 2Barbary Macaque Awareness and Conservation, Touta, Morocco; and 3Haut Commissariat des Eaux et Forets et La Lutte Contre le Desertification, Rabat, Morocco

INTRODUCTION

The Barbary macaque (Macaca sylvanus) is an endangered primate species with fragmented populations in Morocco and Algeria. In Morocco, Barbary macaque populations are reported to be decreasing in both the Middle and High Atlas Mountains (El Alami et al. 2013; Menard et al. 2013). In the north of Morocco, reported reasons for the species decline include overgrazing by livestock communally pastured on the mountains, along with habitat fragmentation and destruction for agriculture (Fa 1982; Fa et al. 1984). The topography of the north of Morocco is steep, rocky and, occasionally, inaccessible. The macaques in the region are very wary of people, making them a difficult species to observe (Mehlman 1989). Two previous surveys of the Barbary macaque populations in the north of Morocco concluded that group sizes were small and the species was in danger of extinction in the region (Fa 1982; Waters et al. Figure 1. A Barbary macaque in the mixed oak forest of Bouhachem. Photograph by A. El Harrad. 2007). One area included in both these surveys is the mixed oak forest of Bouhachem (Figure 1). Previously documented group sizes for Bouhachem ranged 8 – 27 individuals in five STUDY SITE AND METHODS groups with a mean group size of 13.6 (Fa 1982) and two groups of 7 – 16 individuals, with a mean The study area, Bouhachem, is in the Tangier- group size of 11.5 (Waters et al. 2007). As part of Tétouan region of northern Morocco (Figure 2). a larger investigation into whether the inclusion of Bouhachem is a mountainous forested area of local people in a larger survey effort can effectively approximately 142km² comprising three species of co-produce information on the status of Barbary oak - the evergreen cork oak (Quercus suber), the macaques in Bouhachem (Waters 2014), we deciduous zeen oak (Q. canariensis) and Pyrenean collected group size and composition for four oak (Q. pyrenaica). An area encompassing 8,000 ha, Barbary macaque groups adjacent to one another in constituting about 75% of the total area of forest has Bouhachem forest. protected status as a Site of Biological and Ecological

Correspondence to: Siân Waters, Department of Anthropology, Durham University, South Road, Durham DH1 UK, and Barbary Macaque Awareness & Conservation, Rue Fez 22 Tétouan, Touta, 93000, Morocco; E-mail: [email protected]. 54 / Waters et al.

Figure 2.-- Location of Bouhachem protected area in the north of Morocco. Landsat map LC82010352014217LGN00 courtesy of the US Geological survey. Prepared by M. Ikssi.

Interest. At the time of the study there was one paved last to flee, so we paid close attention to males during road through the forest and one track accessible to observations of groups whilst in the vehicle and 4WD vehicles. used those with easily observed physical features Barbary macaques occur throughout the to identify individual groups. By January 2010, we forest but are hard to observe because they flee on could confidently identify four macaque groups encountering people on foot. During the first three that contained at least two males that exhibited months of our study (October – December 2009), distinct physical characteristics such as scars or we noted that the macaques tolerated a stationary limps that we were able to observe with binoculars vehicle from a distance of about 30 m. However, if from a distance of ~30 m. If no such individual was we were on foot, the macaques moved out of sight observed, we recorded the group as unidentified. We quickly unless situated on escarpments or rocky recorded one observation per day of each group for outcrops inaccessible to people. We therefore two days per week during February and March 2010 located macaque groups by patrolling the paved (eight weeks). road in a vehicle at an average speed of 15 km/h in We recorded macaque group counts and the morning (7 – 11 am) and late afternoon/evening composition when groups crossed an open area (3 – 5pm), two days per week. such as the paved road, or open clearings. We On encountering a group, we stopped and began distinguished four age-sex categories (Table 1). To to count individuals. Adult males were always the avoid errors due to the often rapid movement of Barbary Macques in Bouhachem Forest, North Morocco / 55 Table 1. Age-sex class of Barbary macaques used to determine group composition.

Age-Sex Class Definition

Adult male > 5 years Full body size; fully developed testicles

Adult female > 5 years Full body size; differentiated from males at distance by appearance of genitals and/or presence of elongated nipples

Unknown adults > 5 years Adults of unidentified sex; full body size

Sub-adults > 3 - 5 years old and Blonde in colour; slender body; smaller than full body size juveniles > 1 - 3 years old

individual macaques across open spaces both sub- the survey period. Barbary macaque group sizes in adult and juvenile age classes are counted together. this study ranged 52 – 72 individuals with a mean We do not include newborn infants in this study due group size of 62. Due to the rapid movement of to the lack of information regarding infant mortality group members we could not always identify the sex in this area. of some adults. The mean overall adult sex ratio was 1:1.1. RESULTS DISCUSSION We were able to clearly identify each Barbary macaque group at least eight times during the study Preliminary results from this study suggest that and recorded its size and composition. We labelled current Barbary macaque group size in Bouhachem the groups after the location where we observed is larger than those reported in previous surveys them most often. by Fa (1982) and Waters et al. (2007) of 7 – 27 In Table 2, we present the most comprehensive individuals. A group in deciduous oak forest in counts and composition of each group taken during Algeria numbered 53 individuals (Menard & Vallet

Table 2. Group numbers and composition of four Barbary macaque groups in Bouhachem, February and March 2010.

Sub- Adult Adult Unknown Date Study Group Name Adults & Total Males Females Adults Juveniles 27.3.10 Handak Kherba (HK) 24 16 11 1 52

28.2.10 Dar de Monte (DM) 17 28 20 7 72

10.3.10 Marja Ghatwil (MG) 22 25 18 1 66

13.2.10 Lota Teshta (LT) 18 21 18 2 59

Total 249 56 / Waters et al.

1993) suggesting the group sizes we report here macaque Macaca sylvanus in the Central High may be the norm for this species in such habitat. Atlas Mountains of Morocco. Oryx 47: 451-456. The previous surveys in Bouhachem took place Fa, J.E. 1982. A survey of population and habitat of before the construction of the paved road through the Barbary macaque Macaca sylvanus L in north the forest and so those group sizes may be lower Morocco. Biological Conservation 24: 45-66. due to the difficulty in encountering and observing Fa, J.E., D.M. Taub, N. Menard & P.J. Stewart macaques on foot. Low group counts were noted 1984. The distribution and current status of during a study in another area of Barbary macaque the Barbary macaque in North Africa. In The habitat in the region and were updated when further Barbary Macaque: A Case Study in Conservation. opportunities for observation allowed more accurate J.E. Fa, ed. Plenum Press, London. Pp. 79-111. counts (Mehlman 1984). The ratio of adult males to Mehlman, P.T. 1984. Aspects of the ecology and females concurs with studies of the species in other conservation of the Barbary macaque in the fir areas of its distribution (Menard & Vallet 1996). forest habitat of the Moroccan Rif Mountains. October has been suggested as the best period In The Barbary Macaque: A Case Study in for Barbary macaque surveys because macaque Conservation. J.E. Fa, ed. Plenum Press, London. activity patterns remain relatively stable allowing Pp. 165-199. easier detection of groups (Menard & Vallet 1997). Mehlman, P.T. 1989. Comparative density, However, in our experience in Bouhachem, the demography and ranging behaviour of Barbary winter months (December –- February) are more macaques (Macaca sylvanus) in marginal and conducive to counting non-habituated Barbary prime conifer habitats. International Journal of macaques in deciduous forest due to less foliage Primatology 10: 269-292. and vegetation which can obscure our view of Menard, N., A. Foulquier, D. Vallet, M. Qarro, P. macaque groups feeding in grassy clearings. Le Gouar & J.S. Pierre. 2013. How tourism and These data provide a baseline for a wider survey pastoralism influence population demographic of the conservation status of Barbary macaques in changes in threatened large mammal species. Bouhachem and provide evidence that Bouhachem Animal Conservation 17: 115-124. may be an important area for the species’ long-term Menard, N. & D. Vallet. 1993. Population dynamics conservation. of Macaca sylvanus in Algeria - an 8-year study. American Journal of Primatology 30: 101-118. Menard, N. & D. Vallet 1996. Demography and ACKNOWLEDGEMENTS ecology of Barbary macaques (Macaca sylvanus) in two different habitats. In Evolution and Ecology We thank the Moroccan Haut Commissariat des of Macaque Societies. J.E. Fa and D.G. Lindburgh, Eaux et Forets et la Lutte Contre le Desertification eds. Cambridge University Press, Cambridge. Pp. for permission to conduct this research. We are 106-131. grateful to the Royal Zoological Society of Scotland, Menard, N. & D. Vallet. 1997. Behavioural responses the Mohamed Bin Zayed Endangered Species of Barbary macaques (Macaca sylvanus) to Fund and Conservatoire pour la protection des variations in environmental conditions in primates for financial support during this study. SW Algeria. American Journal of Primatology 43: is indebted to Joanna Setchell and Sandra Bell for 285-304. their support and guidance throughout the larger Waters, S. 2014. Including People in Primate study of which this report is a small part. We thank Conservation: A Case Study of Shepherds and Mustafa Aksissou and Lahcen Taiqui of University Barbary Macaques in Bouhachem forest, North Abdelmalek Essaadi, Tetouan for their assistance Morocco. Anthropology Department, Durham with permit applications. Two anonymous reviewers University. PhD. provided helpful comments improving an earlier Waters, S., M. Aksissou, A. El Harrad, M.E. version of this manuscript. Mohamed Ikssi kindly Hobbelink & J.E. Fa. 2007. Holding on in the prepared Figure 2. Djebela: Barbary macaque Macaca sylvanus in northern Morocco. Oryx 41: 106-108.

LITERATURE CITED Received: 14 July 2015 El Alami, A., E. van Lavieren, R. Aboufatima & A. Accepted: 30 October 2015 Chait. 2013. A survey of the Endangered Barbary African Primates 10: 57-58 (2015)/ 57 Brief Communication:

Liberian Chimpanzees Abandoned by New York Blood Center

Kathleen Conlee1 and Jennifer A.Z. Desmond1,2

1The Humane Society of the United States, Washington, DC, USA; 2Liberia Chimpanzee Rescue

Background Figure 1. a. During times of irregular feeding, the anxious chimpanzees met In the early 1970s, the the boats delivering food New York Blood Center with screams; b. In sharp (NYBC) established a contrast, the chimpanzees’ chimpanzee laboratory demeanor is very different after the feeding schedule in the West African became reliable and on a country of Liberia. NYBC daily basis. Now, they wait built their inventory patiently for the boat; c. A of study subjects with mother shares food with her chimpanzees captured a. offspring. from the wild in Liberia or purchased from people keeping them as pets. In the early 1980s, the b. establishment of an onsite breeding facility added hundreds more to the population. The chimpanzees were used as human models in invasive biomedical research focused on a variety of diseases, primarily hepatitis. It is estimated that approximately 400 chimpanzees died over the course of NYBC’s operation. NYBC’s research at the facility gradually decreased over the years and, in 2006, the program was ended. The remaining chimpanzees were New York Blood Center transferred from the laboratory to six Withdraws Support and mangrove islands located on nearby Refuses Responsibility estuarine rivers, leaving them with little to no natural sources of food or In March 2015, NYBC water. Though the islands provide a halted all financial support, more spacious and natural home than c. despite the fact that many the laboratory cages, the chimpanzees individuals within the are still completely reliant on humans organization had promised for their survival (Figure 1). For approximately ten lifetime care for the remaining 66 chimpanzees. years, NYBC provided $30,000 per month to care for Withdrawal of funds left the chimpanzees in a the chimpanzees, delivering food and water by boat life threatening situation. All caregiver staff were to the islands at irregular intervals. immediately unemployed and, thus, delivery of

Correspondence to: Kathleen Conlee, The Humane Society of The United States, 2100 L Street NW, Washington, DC 20037; Phone: +1 (301) 258-3043; E-mail: [email protected]. 58 / Conlee and Desmond

b. c.

Figure 2. a. A typical delivery of food for the chimpanzees consists of a wide variety of fresh fruits and vegetables, including leafy greens. They also receive fresh water; b. The dedicated staff members who prepare and deliver food each day to the chimpanzees. During the early days of NYBC funding withdrawal, staff worked without a salary; c. A caregiver offers a young chimpanzee a drink. All photographs a. by J.A.Z. Desmond for The Humane Society of the United States.

food to the islands was reduced to volunteers who include a decrease in the support required. Despite collected food on their own. Moreover, during that a large public outcry from more than 200,000 time, the islands’ fresh water systems were broken, individuals and widespread media coverage leaving the chimpanzees with no fresh water, except demanding they accept responsibility for the that brought to them by the volunteers. chimpanzees, NYBC has refused to engage in direct As a large nonprofit blood services organization communication and have made clear their position based in New York City, with approximately $475 through public statements on their website. million in assets and annual revenues of more than $300 million, NYBC is fully capable of continuing Working Toward a Better Future for the to provide lifetime support for the chimpanzees Chimpanzees they used for over thirty years in their research. In withdrawing their support, New York Blood Center Thanks to the generosity of thousands of people has left the full financial burden of care on animal around the world, The HSUS-led coalition has raised protection organizations and the government of funds to help improve life for the chimpanzees Liberia. abandoned by New York Blood Center in Liberia. Water systems have been repaired, the chimpanzees Formation of a Coalition are being fed a nutritious and diverse diet every day, additional birth control measures have been The former NYBC research chimpanzees are alive implemented, and a full time team has been put in today only because dedicated caregivers voluntarily place to ensure proper care and management. continued feeding them and brought international Liberia Chimpanzee Rescue has the ultimate awareness to their dire situation (Figure 2). Once goal of providing true sanctuary for the former alerted to the emergency faced by the chimpanzees research chimpanzees with care that meets the and former NYBC staff, The Humane Society of the highest standards, such as those established by the United States and Humane Society International Pan African Sanctuary Alliance. The development stepped in to provide for their immediate care by of in-country solutions will not only provide proper establishing Liberia Chimpanzee Rescue. They also care for the chimpanzees but also social, economic began building a coalition of over 35 organizations and environmental benefits for the surrounding focused on raising additional support and awareness communities. about the situation, while encouraging NYBC to A commitment from New York Blood Center resume their responsibility to the chimpanzees. to resume their financial responsibility combined Prior to public awareness of the chimpanzees’ with a clear plan developed and implemented by abandonment, The Humane Society of the United experienced and reputable local and international States made multiple attempts to contact New York animal welfare and conservation partners will Blood Center, urging the organization to renew ensure a positive long term outcome for all involved. its funding for the chimpanzees and to discuss the For more information and to learn how you can potential for a long term solution, which would help, go to www.facebook.com/abandonedchimps. African Primates 10: 59-60 (2015)/ 59 Brief Communication:

A Top Priority Site for Primate Conservation in CÔte d’Ivoire Soon Designated as a Protected Area?

Inza Koné1,2, Karim Ouattara1,2, André Djaha Koffi1,3

1Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS); 2Laboratoire de Zoologie, Université Félix Houphouët-Boigny, Abidjan, Côte d’Ivoire; 3UFR Environnement, Université Jean Lorougnon Guédé, Daloa, Côte d’Ivoire

The Rainforest Trust is working with the Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS) to create a community forest reserve protecting the Tanoé-Ehy Forest. Ensuring the success of this project is critical to protecting Côte d’Ivoire’s remaining rainforests and safeguarding the future of some of Africa’s most critically endangered primates. Indeed the Tanoé-Ehy Forest, 12,000 ha in southeast Côte d’Ivoire, provides habitat for a number of rare and highly threatened primate species and is a priority area for primate conservation in West Africa (Gonedelé et al. 2008). The Tanoé-Ehy Forest is considered the only forest where the possibly extinct Miss Waldron’s red colobus (Piliocolobus badius waldronae) may be rediscovered, where a viable population of the critically endangered diana roloway guenon (Cercopithecus diana roloway; Figure 1) was confirmed, and where a viable population of the endangered white-naped mangabey (Cercocebus atys lunulatus) still occurs. The Tanoé-Ehy forest is also one of the last refuges for the vulnerable white-thighed colobus (Colobus vellerosus). Despite its importance, the Tanoé-Ehy forest Figure 1. Diana Roloway Monkey of CÔte d’Ivoire. and wetland area has received little attention until Photograph by J.M. Lernould. recently and primate habitat is threatened by unsustainable land use, such as oil palm farming and of local and international partners including chainsaw milling. Meanwhile, monkeys living in this WAPCA and Mulhouse Zoo, the Wildlife Division forest are killed for bushmeat by the impoverished of Côte d’Ivoire, and three local conservation NGOs and ill-informed local communities. (SOS Forêts, ACB-CI, and SCNCI). The project’s In 2006, a community-based management approach is based on a combination of conservation- project for the Tanoé-Ehy forest was initiated by oriented scientific studies, pragmatic conservation eight neighbouring communities with the support field actions, and flanking measures. The main

Correspondence to: Inza Koné, Centre Suisse de Recherches Scientifiques en Côte d’Ivoire (CSRS), 01 BP 1303 Abidjan 01 Côte d’Ivoire; E-mail: [email protected]. 60 / Koné et al.

Figure 2. The Tanoé-Ehy Forest of CÔte d’Ivoire. Map prepared by RASAPCI-CSRS.

activities of the project comprise awareness raising of the creation of a transboundary conservation campaigns, forest surveillance, and biological and area. socio-economic surveys. The project is actively So far, the major obstacle to the designation of involved in the formalities of obtaining an official the Tanoé-Ehy Forest as an official community- status for the community-managed reserve, while it managed forest has been the cost of its demarcation provides support of local development, community- by an official geometrician. More than USD 80,000 organization and capacity building for conducting is needed and this is far beyond the amount the conservation activities. communities can contribute. A call for donations Management committees were formed in initiated by the Rainforest Trust will no doubt enable eight different villages with their bylaws officially us to overcome this obstacle. For more information registered by the national administration. In the two on the fund-raising initiative see https://www. districts of the project area a paramount association rainforesttrust.org/project/cote-divoire/ and for comprising the different management committees more information on the Tanoé-Ehy conservation was officially established as well. The last step of project see http://www.panorama.solutions/content/ the community organization process will consist community-empowerment-conservation-critically- of establishing a “federal association” comprising endangered-primates. both paramount associations. The future federation will be the main interlocutor of the government and will work with external institutions for policy LITERATURE CITED making, while the two paramount associations will play a coordinating role for the field-based activities Gonedelé Bi, S., Koné I., Béné J-C. K., Bitty A. E., carried out by the eight management committees Akpatou B. K., Goné Bi. Z., Ouattara K., & Koffi (Koné, 2015). D. A. (2008). Tanoé forest, South-eastern Côte- For the established committees and associations d’Ivoire identified as a high priority site for the to be functional they are offered regular training conservation of critically endangered Primates sessions, continued coaching, and logistic support as in West Africa. Tropical Conservation Science 1 this experience is new in Côte d’Ivoire and carried (3):263-276. out by rural communities with little experience with Koné I. (2015). Community empowerment for the modern standards of forest management. conservation of critically endangered primates Surveillance patrols and awareness raising and their habitat in south-eastern Côte d’Ivoire. campaigns have been successfully initiated by the In IUCN PAPACO. Twenty-two Stories of communities to stop oil palm expansion and to Conservation in Africa: Key Elements for Effective mitigate the threats posed by illegal chainsaw milling and Well-governed Protected Areas in Sub- and poaching. Particular attention is paid to trans- Saharan Africa. IUCN PAPACO, Nairobi, pp 36- border synergy with Ghanaian stakeholders in view 39. African Primates 10:61-63 (2015)/ 61 Obituary:

Geza Teleki, Ph.D. (7 December 1943 - 7 January 2014)

by Dale Peterson

Geza Teleki was born Left: Geza Teleki (L) and David in Kolozsvar, Hungary, Bygott (R) photographing a on December 7, 1943, colobus kill, Gombe National scion of a distinguished Park, 1970. Photograph branch of the old courtesy D. Bygott. Hungarian aristocracy. One of his ancestors, Below: Geza Teleki and his dog Newt, in Maryland. Count Samuel Teleki, Photograph by H. McGiffin. famously explored large areas of East Africa during 1887 and 1888. His grandfather, Count Paul Teleki, served two times as Prime Minister of Hungary, while his father, Geza Teleki, an Olympic athlete, became Hungary’s Minister of Education during World War II. When the Soviets took over Hungary at the end of the war, his father’s name was placed on the list of politicians to be executed. Geza and his father and mother were able to escape the Soviets in 1949, and they found their way to America, where the father became a professor of geology at George Washington University. Geza became a naturalized American citizen in 1956 and attended the Harvey School in Katonah, New York, and St. George’s School in Newport, Rhode Island. After completing undergraduate studies in anthropology at George Washington University (B.S. 1967), he enrolled for anthropology graduate work at Pennsylvania State University under the guidance of C. R. Carpenter, one of the great pioneers in American primatology. After receiving the degree, he taught at George His early field work brought Geza to Gombe Washington University as an Associate Professorial Stream National Park in Tanzania (from 1968 to Lecturer beginning in 1977, and he wrote some forty 1971), where he was supervised by Jane Goodall, professional papers for scientific publication as well the distinguished pioneer in research on wild as two dozen articles for popular magazines including chimpanzees. The field work at Gombe resulted in a Scientific American, Smithsonian, Zoonooz, and book, The Predatory Behavior of Wild Chimpanzees Wildlife News. His wildlife photographs, meanwhile, (Bucknell UP, 1973); a dissertation and degree from found an audience in more than 150 magazines and Pennsylvania State University (Ph.D. in 1977); and books. a lifelong passion for conserving and protecting But Geza’s heart was in conservation, not chimpanzees. academics. In 1977, he became Scientific Advisor 62 /Peterson

to the International Primate Protection League and had manufactured, tested, and then buried in the the International Union for the Conservation of area during World War I. His wife, Heather, rescued Nature, and by 1978 he had begun compiling data him from debilitating rounds of dialysis by donating to describe the conservation status of chimpanzees one of her kidneys for transplant. The family moved across Africa for the IUCN Red Data Book. In 1979, from Washington, D.C., to Bethesda, Maryland, in he became the Project Head for a national survey 2003, and in 2012 they returned to Geza’s childhood of primates and primate habitats in Sierra Leone, land of Hungary. West Africa (under the sponsorship of the New York Geza’s commitment to conservation was founded Zoological Society, the World Wildlife Fund, the on his love for chimpanzees and on his recognition Fauna Preservation Society, and the Sierra Leone of them as individuals with minds, emotions, and Nature Conservation Association). And in 1981, personalities. He was a passionate and powerful Geza returned to Sierra Leone (for the WWF and at personality whose presence was impossible to the invitation of President Siaka Stevens) to establish ignore, and he used that presence tirelessly for the that country’s first national park, the Outamba- causes he believed in. The world will miss him, as Kilimbi National Park. He was also Park Director for will his grieving family and his many friends and Sierra Leone’s Wildlife Conservation Branch from admiring colleagues. The chimpanzees have lost a 1981 to 1984. friend. After contracting the parasitic disease onchocerciasis (“river blindness”) during his time in the back country of Sierra Leone, Geza withdrew A Selection of Geza Teleki’s Publications from field work in 1984 and settled in Washington, D.C., to continue his career as a conservationist. He Baldwin, L.A. & G. Teleki. 1972. Field research served as Associate Scientist for the World Wildlife on baboons, drills, and geladas: An historical, Fund in Washington, DC from 1985 to 1991; during geographical, and bibliographical listing. this period he wrote 18 technical reports for NGOs Primates 13(4): 427-432. and governments on conservation issues while Teleki, G. 1973. The Predatory Behavior of Wild promoting public awareness of those issues as a Chimpanzees. Bucknell University Press, consultant for public media documentaries. And Lewisburg. 232 pp. then, in 1986, in partnership with Dr. Jane Goodall Teleki, G. 1973. Notes on chimpanzee interactions and the Jane Goodall Institute, Geza established with small carnivores in Gombe National Park, the Committee for the Conservation and Care of Tanzania. Primates 14(4): 407-411. Chimpanzees (CCCC), which was a non-profit Teleki, G. 1973. Group responses to the accidental organization made up of primate and conservation death of a chimpanzee in Gombe National Park, professionals with members in more than 25 Tanzania. Folia Primatologica 20(2-3): 81-94. countries. Geza served as the Chairman of CCCC Baldwin, L.A. & G. Teleki. 1973. Field research until 1994. During this period, the CCCC became on chimpanzees and gorillas: An historical, a powerful voice for protecting chimpanzees in the geographical, and bibliographical listing. wild as well as ensuring their appropriate treatment Primates 14(3): 315-330. in captivity. He also, from 1986 to 1991, was Teleki, G. 1974. Chimpanzee subsistence technology: Associate Scientist with the WWF and, in 1991 and materials and skills. Journal of Human Evolution 1992, was Director of the Africa Programs for the 3(6): 575-594. Jane Goodall Institute. Baldwin, L.A. & G. Teleki. 1974. Field research He married Heather McGiffin in 1991, and on gibbons, siamangs, and orangutans: An in 1995, they had a son named Aidan. Starting in historical, geographical, and bibliographical 1995, Geza returned to teaching graduate courses listing. Primates 15(4): 365-376. at George Washington University and continued in Teleki, G. 1975. Primate subsistence patterns: that position until early in the twenty-first century, Collector-predators and gatherer-hunters. when his health was devastated by a complex group Journal of Human Evolution 4(2): 125-184. of diseases – including hypothyroidism, diabetes, Baldwin, L.A., M. Kavanagh & G. Teleki. 1975. Field gall stones, and kidney failure. He eventually research on langur and proboscis monkeys: An concluded that the diseases were a consequence of historical, geographical and bibliographical massive soil contamination in his Washington, D.C. listing. Primates 16(3): 351-363. suburban neighborhood by toxic chemical-warfare Teleki, G., E.E. Hunt, Jr. & J.H. Pfifferling. 1976. agents that the U.S. Army Chemical Warfare division Demographic observations (1963-1973) on the Geza Teleki / 63 chimpanzees of Gombe National Park, Tanzania. 1990, Federal Register 55(48): 9129-9136.] Journal of Human Evolution 5(6): 559-595. Teleki, G. 1988. The Chimfunshi Wildlife Baldwin, L.A. & G. Teleki. 1976. Patterns of Orphanage: A sanctuary in Africa for confiscated gibbon behavior on Hall's Island, Bermuda: chimpanzees. Journal of Medical Primatology 17: A preliminary ethogram for Hylobates lar. In 113. Gibbons and Siamangs: A Series of Volumes on Teleki, G. 1988. Chimfunshi Wildlife Orphanage for the Lesser Apes. D.M. Rumbaugh, ed. S. Karger, chimpanzees. Primate Conservation 9: 15. Basel. Pp. 21-105. Teleki, G. 1988. Chimpanzee: Pan troglodytes Baldwin, L.A., G. Teleki & M. Kavanagh. 1976. Field Blumenbach, 1799. In The IUCN Red Data research on colobus, guenon, mangabey, and Book: Threatened Primates of Africa. P.C. Lee, J. patas monkeys: An historical, geographical, and Thornback & E.L. Bennett, eds. IUCN, Gland. bibliographical listing. Primates 17(2): 233-251. Pp. 107-122. Teleki, G.G. 1977. Still more on predatory behavior Teleki, G. 1988. Circumvention of CITES restrictions in nonhuman primates. Current Anthropology on chimpanzee trade. Frame News 19: 4-5. 18(1): 107-108. Teleki, G. 1988. Circumvention of CITES restrictions Baldwin, L.A., T.L. Patterson & G. Teleki. 1977. Field on chimpanzee trade. CCCC, Washington, DC. research on callitrichid and cebid monkeys: An 7pp. + documentation. [Testimony submitted historical, geographical, and bibliographical 13 July 1988 to the Subcommittee on Oversight listing. Primates 18(4): 985-1007. and Investigations of the House Committee on Baldwin, L.A. & G. Teleki. 1977. Field research Merchant Marine and Fisheries concerning on tree shrews and prosimians: An historical, implementation of CITES, 13 July 1988.] geographical, and bibliographical listing. Teleki, G. 1988. Pygmy or Dwarf chimpanzee or Primates 18(4): 985-1007. bonobo: Pan paniscus Schwarz, 1929. In The Baldwin, L.A., N. Koyama, N. & G. Teleki. 1980. IUCN Red Data Book: Threatened Primates of Field research on Japanese monkeys: An Africa. P.C. Lee, J. Thornback & E.L. Bennett, eds. historical, geographical, and bibliographical IUCN, Gland. Pp. 125-130. listing. Primates 21(2): 268-301. Teleki, G. & J. Goodall. 1988. Recommendations to Teleki, G. 1981. The omnivorous diet and eclectic USDA on improving conditions of psychological feeding habits of chimpanzees in Gombe National well-being for captive chimpanzees. Alternatives Park, Tanzania. In Omnivorous Primates: to Laboratory Animals 15(3): 255-259. Gathering and Hunting in Human Evolution. Teleki, G. 1989. Population status of wild R.S.O. Harding & G. Teleki, eds. Columbia chimpanzees (Pan troglodytes) and threats University Press, New York. Pp. 303-343. to survival. In Understanding Chimpanzees. Galdikas, B. & G. Teleki. 1981. Variations on the P.O. Heltne & L.A. Marquardt, eds. Harvard subsistence activities of female and male pongids: University Press, Cambridge. Pp. 312-353. New perspectives on the origins of labor division. Teleki, G. 1989. Recommendations to USDA on Current Anthropology 22(3): 241-256, 316-320. formulating new standards to promote the Harding, R.S.O. & G. Teleki. 1981. Introduction. In psychological well-being of captive chimpanzees. Omnivorous Primates: Gathering and Hunting in 1 Opp. CCCC, Washington, DC. [Petition Human Evolution. R.S.O. Harding & G. Teleki, submitted on 20 July 1989 to US Department eds. Columbia University Press, New York. Pp. for review of Animal Welfare Act under for 1-9. Laboratory Animals Act.] Teleki, G. 1987. Current threats to the survival of the Teleki, G. 1992. Action Plan I: Conservation of once "common" chimpanzee (Pan troglodytes) Chimpanzees (Pan troglodytes) in Africa. CCCC of equatorial Africa. 49pp. + maps and tables. Special Report, Washington, DC. CCCC, Washington, DC. [Report accompanied Teleki, G. 1994. Evaluation of proposed criteria petitions to US Fish and Wildlife Service to revisions for listing species on CITES appendices. classify chimpanzees as Endangered Species, Report commissioned by Humane Society of the process successfully completed on 12 March United States, Washington, DC. 64 /Struhsaker Obituary:

Jeremiah Ssali Lwanga, Ph.D. (7 June 1960 - 31 August 2015)

by Thomas T. Struhsaker Department of Evolutionary Anthropology, Duke University

On August 31, 2015, we were up early and having a lost a true friend, colleague, quick breakfast before setting and dedicated conservationist out. Just then Jerry turned with the passing of Dr. up. It seems he had forgotten Jeremiah Ssali Lwanga. to take a flashlight with him I first met Jerry in 1984 and when his study group of when he came to the Kibale monkeys finally settled down Forest as part of a field trip for for the night, it was dark and Makerere University zoology Jerry was a very long way from students. Dr. Gilbert Isabirye camp. So, he climbed into a Basuta led this trip and Chaetacme tree, thinking that afterwards he expressed his the long and sharp spines of view that Jerry would make this tree would protect him an excellent field biologist, from any predator. He slept urging us to make it possible very little, if at all. When for him to study in Kibale. So, Jerry arrived in camp he between Dr. Tom Butynski looked exhausted. We gave and myself, we supervised Jerry Lwanga at the Ngogo camp, Kibale Forest, him breakfast and I suggested Jerry’s study of blue monkey Uganda. Photograph by S. Gunter. he take the day off and get behavioral ecology at the some rest. But no, Jerry was Ngogo study site in Kibale. Jerry, of course, did a determined to complete his sample of the monkeys. superb study, earning his M.Sc. in zoology from After eating, he picked up his backpack, complete Makerere University in 1987. with flashlight, and set off to find his monkeys. That’s A story from Jerry’s research on blue monkeys the kind of guy Jerry was. shows how committed he was to his field studies. Jerry was obviously a hardworking, dedicated, The traditional sampling method at that time was and bright field biologist. So, it was with pleasure that to spend 5 consecutive days (12-13 hours per day) I agreed to supervise his Ph.D. studies through the following a specific group of monkeys, keeping Department of Wildlife at the University of Florida. detailed records of their social interactions, what Jerry continued to be an outstanding student, both they ate, and where they went. Jerry was on day 3 in the classroom and in the field. Back in Kibale of his 5-day sample. His study group often took him for his Ph.D. field work, he pursued an important to the far western side of the Ngogo study area and study on the role of seed and seedling predators and several kilometers from camp. On this particular browsers in the regeneration of two important tree day nightfall arrived without a sign of Jerry. Those species. Most of this study focused on the impact of of us in camp began calling out in hopes that he rodents and elephants. Once again, Jerry excelled was nearby. We then took our hurricane lamps and and finished his thesis in 1994. He was one of the torches (flashlights) into the forest, shouting out for best graduate students I have ever worked with. Jerry. After a few hundred meters we realized this While he was doing his thesis research in Kibale, was hopeless. We decided it was best to wait until Jerry also helped with my studies of red colobus and daylight to launch a search party. The next day we of hybridization between blue and redtail monkeys. Jerry Lwanga / 65

Upon completion of his Ph.D., Jerry was involved and Strombosia scheffleri) in Kibale Forest with a number of other studies, including a survey of Reserve, Uganda. Ph.D. thesis. University of ferns in several of Uganda’s forests. Eventually, Jerry Florida, Gainesville, Florida. returned to the Ngogo study site in Kibale where Lwanga J.S, A. Balmford & R. Badaza. 1998. he managed the research camp and participated Assessing fern diversity: relative species richness in studies of chimpanzees, redtail monkeys, long- and its environmental correlates in Uganda. term monitoring of primate populations, and forest Biodiversity & Conservation 7(11): 1387-1398. regeneration. As a result of all this field work, Jerry Lwanga J.S. 2003. Forest succession in Kibale became a first-class tropical forest ecologist and National Park, Uganda: implications for forest naturalist. He really loved working in the forest. restoration and management. African Journal of On top of all this, Jerry was an excellent teacher, Ecology 41(1): 9-22. administrator, and diplomat. Before long Jerry began Lwanga J.S. 2006. The influence of forest variation teaching at Makerere University, while maintaining and possible effects of poaching on duiker his research and administrative responsibilities at abundance at Ngogo, Kibale National Park. Ngogo. This must have been a serious challenge in African Journal of Ecology 44(2): 209-218. time-management. Lwanga J.S. 2006. Spatial distribution of primates in As if Jerry did not already have enough to do, he a mosaic of colonizing and old growth forest at was appointed Director of the Makerere University Ngogo, Kibale National Park, Uganda. Primates Biological Field Station (MUBFS) in Kibale National 47(3): 230-238. Park. This was in 2010-2011 when MUBFS was in Lwanga J.S., T.M. Butynski & T.T. Struhsaker. 2000. serious financial debt. Cleaning up this financial Tree population dynamics in Kibale National mess and getting MUBFS back on track was no easy Park, Uganda 1975-1998. African Journal of task, but within a few years Jerry did this through a Ecology 38(3): 238-247. combination of his diplomacy, administrative skill, Lwanga J.S, T.T. Struhsaker, P.J. Struhsaker, T.M. integrity, and dedication. I’ll not forget the last time Butynski & J.C. Mitani. 2011. Primate Population I saw Jerry in 2014. We were at the Kanyawara camp Dynamics over 32.9 years at Ngogo, Kibale where both of us were helping teach a field course National Park, Uganda. American Journal of being offered by the Tropical Biology Association. I Primatology 73(10): 997-1011. told Jerry how happy I was to see the field station Mitani J.C., T.T. Struhsaker & J.S. Lwanga. 2000. running so smoothly. He smiled and then told me Primate community dynamics in old growth that MUBFS had saved enough money to afford a forest over 23.5 years at Ngogo, Kibale National new pickup truck to replace one of the antiques they Park, Uganda: implications for conservation had been relying on. He was very proud of this and and census methods. International Journal of I was very proud of him. Jerry was the best director Primatology 21(2): 269–286. MUBFS ever had. Mitani J.C., W.J. Sanders, J.S. Lwanga & T.L. Jerry was respected and liked by all who knew Windfelder. 2001. Predatory behavior of crowned him, not just because of his professional skills and hawk-eagles (Stephanoaetus coronatus) in Kibale work ethic, but because he was trustworthy, reliable, National Park, Uganda. Behavioral Ecology and and a truly kind and considerate person. Sociobiology 49(2-3): 187–195. I cannot adequately express my sense of loss with Potts K.B., C.A. Chapman & J.S. Lwanga. 2009. Jerry’s passing, but I will always remember him, Floristic heterogeneity between forested sites in especially when I am in Kibale. Kibale National Park, Uganda: insights into the fine-scale determinants of density in a large- bodied frugivorous primate. Journal of Animal Ecology 78(6): 1269–1277. A Selection of Jeremiah Lwanga’s Publications Struhsaker T.T., T.M. Butynski & J.S. Lwanga. Hybridization between redtail (Cercopithecus Lwanga, J.S. 1987. Group fission in blue monkeys ascanius schmidti) and blue (Cercopithecus (Cercopithecus mitis stuhlmanni): effects on the mitis stuhlmanni) monkeys in the Kibale socioecology in Kibale Forest, Uganda. M.Sc. Forest, Uganda. 1988. In A Primate Radiation: thesis, Makerere University, Kampala, Uganda. Evolutionary Biology of the African Guenons. Lwanga J.S. 1994. The role of seed and seedling Gautier-Hion A., F. Bourliere, J.-P. Gautier & predators and browsers in the regeneration of J. Kingdon, eds. Cambridge University Press, two forest canopy species (Mimusops bagshawei Cambridge. Pp. 477-497. 66 /Struhsaker

Struhsaker T.T., J.S. Lwanga & J.M. Kasenene. 2012b. Diet of chimpanzees (Pan troglodytes 1996. Elephants, selective logging, and forest schweinfurthii) at Ngogo, Kibale National Park, regeneration in the Kibale Forest, Uganda. Uganda, 2. Temporal variation and fallback Journal of Tropical Ecology 12(1): 45-64. foods. American Journal of Primatology 74(2): Watts, D.P., K.B. Potts, J.S. Lwanga, & J.C. Mitani. 130-144. 2012a. Diet of chimpanzees (Pan troglodytes Windfelder T.L & J.S. Lwanga. 2002. Group fission schweinfurthii) at Ngogo, Kibale National Park, in red-tailed monkeys (Cercopithecus ascanius) Uganda, 1. Diet composition and diversity. in Kibale National Park, Uganda. In Glenn M.E. American Journal of Primatology 74(2): 114-129. & M. Cords, eds. New York: Kluwer Academic/ Watts, D.P., K.B. Potts, J.S. Lwanga, & J.C. Mitani. Plenum Publishers. Pp 147-159. African Primates 10 (2015) / 67 Joint Meeting of the International Primatological Society and the American Society of Primatologists

August 21 – 27 2016, Lincoln Park Zoo, Chicago, USA

In August 2016, Lincoln Park Zoo’s This is the first time that a zoo has hosted Lester E. Fisher Center for the Study an IPS congress and this meeting also and Conservation of Apes will host the marks the 50th anniversary of the first IPS International Primatological Society’s congress (held in Frankfurt, Germany) and biennial congress, in concert with the the 20th anniversary since the most recent American Society of Primatologists’ annual joint IPS/ASP meeting (held in Madison, meeting. These societies were founded Wisconsin). to promote primate conservation and to The deadline for abstract submissions is increase understanding and awareness of December 1st 2015; we encourage you to primate behavior and biology. submit your proposals and register early to This will likely be the largest ever qualify for the special registration rate. gathering of primatologists, with attendees Information about registration, abstract coming from all over the world to Chicago. preparation and accommodation options We will kick off the congress with an opening can be found on the conference website: reception on the grounds of Lincoln Park http://www.ipschicago.org/. You can also Zoo on Sunday 21 August 2016, while the follow us on social media to get the most conference itself will be held at Navy Pier in up to date information about the meeting downtown Chicago. (See Facebook page: https://www.facebook. We have secured rooms at reduced rates com/IPS2016; Twitter: @IPS_2016). at two hotels within walking distance of the If you’re coming to the IPS/ASP conference venue and travel within the city conference, remember to bring is very easy thanks to our extensive public donation items for the Conservation transport system. Silent Auction! Questions? E-mail [email protected]

IPS 2016 - Pre-Congress Training Program (PCTP)

The IPS Conservation Committee careers, and cannot have participated invites applications for the 2016 Pre- in a previous IPS Pre-Congress Congress Training Program (PCTP) Training Programs. Participants must for Conservation. This four day event be able to understand and speak is held before each IPS Congress. English well enough to follow and We seek applicants who are currently participate in all aspects of the PCTP focused on primate conservation in workshop. Applicants must complete their work or study program, especially those the official IPS PCTP 2016 Application Form dealing with the conservation of endangered and submit one letter of reference. See: primate species. Applicants must be citizens http://internationalprimatologicalsociety.org/ of a primate habitat country, be early in their conservation.cfm 68 /Meetings

Fourth Understanding Chimpanzees symposium: Chimpanzees in Context Hosted by Lincoln Park Zoo’s Lester E. Fisher Center for the Study and Conservation of Apes August 18-20 2016

Over the course of three days in August 2016, At the meeting, invited talks will be given in Lincoln Park Zoo will host Chimpanzees in Context, eight themed sessions, each hosted by an eminent a symposium showcasing 40 invited presenters, and primatologist: Mollie Bloomsmith, Frans de an open-call ePoster session, for discussions of all Waal, Tetsuro Matsuzawa, William McGrew, John that is Pan! Mitani, Anne Pusey, Andrew Whiten, and Richard In 1986, Dr. Jane Goodall and Paul Heltne Wrangham. In addition to the eight themed sessions, organized the unprecedented ‘Understanding we will also host an open-call ePoster session to Chimpanzees’ conference to bring together field ensure a forum for students, field assistants, and biologists from the different chimpanzee study other primatologists to present their research. sites across Africa, along with researchers studying Abstract guidelines can be found here: http://www. captive chimpanzees, to discuss contemporary chimpsymposium.org/poster-abstract-guidelines- research findings, and to expand their knowledge of and-submission/ chimpanzee behavior and ecology. Two subsequent For more information about the meeting, conferences have been held in Chicago, in 1991 please visit the conference website http://www. and 2007, with three important volumes resulting chimpsymposium.org/ or email the conference from these meetings: Understanding Chimpanzees, organizers at [email protected]. You can Chimpanzee Cultures and The Mind of the also get Chimpanzees in Context updates on social Chimpanzee. media via Facebook (https://www.facebook.com/ To continue this important tradition, Lincoln chimpanzeesincontext) and Twitter (https://twitter. Park Zoo’s Lester E. Fisher Center for the Study com/IPS_2016). and Conservation of Apes, will host the fourth symposium in the series: Chimpanzees in Context. The meeting will be held at Lincoln Park Zoo, The conference organizers will Chicago, USA, between 18th – 20th August 2016. be awarding up to five travel Chimpanzees in Context will directly precede the joint meeting of the International Primatological scholarships for ape range country Society and the American Society of Primatologists, nationals to attend Chimpanzees also to be held in Chicago (21st – 27th August 2016). in Context. These scholarships will To help inform our understanding of chimpanzee cover the cost of travel to Chicago behavior and cognition, as well as the conservation and accommodation during the and welfare issues that impact the lives of chimpanzees, primatologists must engage in dialogue meeting. Details on the application and collaboration with researchers working with process can be found here: http:// other taxa and from different disciplines. The title of www.chimpsymposium.org/travel- this meeting, Chimpanzees in Context, reflects our scholarship/ aim to promote interdisciplinary discussions. African Primates 10 (2015) / 69 News

IPS Grants and Awards for Primate Work Gorilla Action Plans Available The International Primatological Society (IPS) has three grant The Convention on the Conservation and award programs. See the of Migratory Species (CMS) Secretariat has IPS web site for details about released two regional Action Plans for the conservation, research, and Gorilla Agreement. Many gorilla populations are education grants (be sure you transboundary, and therefore much of the success submit applications to the grant of conservation efforts depends on transnational program that fits your goal to cooperation and coordination. Thus, the Gorilla maximize chances for funding). See http://www. Agreement was developed under the auspices of internationalprimatologicalsociety.org. The next CMS and has been in force since 2008. All CMS deadline for grant submissions: March 1, 2016. Notifications can be accessed online at http:// www.cms.int/en/news/notifications

Multiple Opportunities from the Education for Nature Program Youth Forum for People and Wildlife

WWF 2016 Education for Nature Program offers Applications are now open for the first-ever Youth the following fellowship opportunities for 2016, Forum for People and Wildlife in Johannesburg, for rising leaders pursuing MSc and PhD in South Africa in September 2016. The International conservation-related fields: Fund for Animal Welfare (IFAW) will identify 20 • Freshwater Fellowship - eligible for Uganda young leaders in conservation and animal protection, and Zambia aged 18 to 25, to debate issues, explore solutions, • WWF Wildlife Fellowship - Cameroon, network with delegates from around the world, and Democratic Republic of Congo, Kenya, build skills that will empower them to contribute to Namibia, Tanzania and Zambia protecting wildlife and promote a better world for • Mozambique fellowship - exclusively for animals and people. Travel and participant costs will diverse ecological projects in Mozambique be fully funded. • Faculty fellowship - for current or aspiring The Youth Forum for People and Wildlife will be university faculty in Cameroon, Central held immediately prior to the 17th meeting of the African Republic, Democratic Republic Convention on International Trade in Endangered of Congo, Gabon, Kenya, Madagascar, Species (CITES). Delegates will represent not only Mozambique, Namibia, Republic of Congo, the CITES host country of South Africa, but also Tanzania, Uganda and Zambia. other key source, transit and consumer nations in • In addition, there is professional development Africa, Asia, Europe and the Americas. An online grants, workshop grants and training Forum website will connect the global community fellowships. with forum participants before, during and after the Details for all of these can be found at: www. onsite event. To apply or learn more about the Youth worldwildlife.org/efn. Forum, go to www.ifaw.org/youthforum. Key dates: • The Youth Forum will take place in South Free Online Training Course on Africa 17-25 September 2016, and will include an overnight field excursion and four days in Conservation Johannesburg. • The application deadline is 4 December 2015. The Conservation Leadership Program Visit www.ifaw.org/youthforum to apply online, is introducing a free online conservation download the application and learn more. course. Find details at: http://www. • Applicants will be chosen in January 2016 and conservationleadershipprogramme.org/ announced publicly on World Wildlife Day, 3 news/free-online-course/. March 2016. 70 / News News

Call for Applications: 2016 Conservation September 2015 and/or 2016, and two (2) two-year Team Awards Masters scholarships in September 2016 and 2018. Applications for the 2016 Conservation Leadership Students will be based at McGill University, Programme (CLP) Conservation Team Awards Canada or at one of the other I-CAN partner are now open. CLP aims to advance biodiversity universities – i.e., Carleton University and University conservation globally by building the leadership of Victoria, Canada, University of Utrecht in the capabilities of early-career conservation Netherlands, and the Max Planck Institute of Social professionals working in high-priority places with Anthropology in Germany. The field work will be limited capacity to address conservation issues. carried out in at least one of the eight (8) project This partnership initiative, including BirdLife study sites in Kenya and/or Tanzania. International, Fauna & Flora International and the Interested candidates should send their Wildlife Conservation Society, has been helping Curriculum Vitae and a Letter expressing their young conservationists across the world achieve interest in pursuing graduate studies with the I-CAN their goals for 30 years. CLP offers three levels of project to Professor John Galaty, the I-CAN Project Conservation Awards: Co-Director, at McGill University, at john.galaty@ • Future Conservationist Awards: Up to $12,500 mcgill.ca. Interested candidates should make first per project contact by November 15, 2015, or earlier, to facilitate • Conservation Follow-Up Awards: Up to formal graduate applications as early as December $20,000 per project (available only to previous 15, 2015. CLP Future Conservationist Award winners) • Conservation Leadership Awards: Up to New MSc Advanced Wildlife Conversation $40,000 per project (available only to previous in Practice course, designed and delivered in CLP Follow-Up Award winners) collaboration with Bristol Zoological Society In 2016 CLP will only accept proposals for projects This program comprises four taught modules, to be implemented in the following 22 countries: delivered at Bristol Zoo in eight four-day blocks Algeria, Angola, Azerbaijan, Brazil, China, Egypt, throughout the year interspersed with online Georgia, India, Indonesia, Iraq, Kuwait, Libya, learning activities, and an extended research project. Malaysia, Mexico, Mozambique, Oman, South Whether full or part-time, the structure of our Africa, Thailand, Trinidad and Tobago, Turkey, programme has been designed to work around you. United Arab Emirates and Vietnam. The application Hands-on conservation experience: Teaching is deadline for ALL award types is 7 December 2015. split equally between Bristol Zoo and UWE Bristol Visit the CLP website for detailed eligibility criteria, staff, and unlike most other University courses, we guidelines and application form or email clp@ start in January meaning that we can make use of birdlife.org. the spring and summer wildlife for practical, hands- on learning. With many of the theoretical elements Doctorate and Masters Students Scholarships of the course delivered online, you’ll be free to - The Institutional Canopy of Conservation: develop vital skills in areas such as advanced survey Governance and Environmentality in East techniques, species identification, environmental Africa entrepreneurship and communication for The Institutional Canopy of Conservation conservation. (I-CAN) project holds an International Partnerships You can find out more about our MSc Advanced for Sustainable Societies (IPaSS) award. The project Wildlife Conservation in Practice on our website addresses the challenge of combining protection of http://courses.uwe.ac.uk/C1841/2015?dm_ biodiversity with strengthened livelihoods, whether t=0,0,0,0,0 or by e-mailing Mark Steer, Mark.Steer@ through recognizing local rights over resources, uwe.ac.uk to set-up an informal chat. livelihood diversification, or tourism. The project Benefits of studying with UWE Bristol: will focus on the rangelands, wetlands and forests taught by international conservation experts; of the East African savannah, especially in the work in partnership with leading conservation borderlands between Kenya and Tanzania, where organisations; emphasis on practical skills – gain the world’s most significant repository of wildlife the knowledge and skills that employers seek, lies. including advanced survey techniques and species The I-CAN project will support four (4) identification; research abroad – the possibility scholarships for Doctoral and Masters studies. Two to carry out international research projects at our (2) four-year Doctoral scholarships will start in research stations in Madagascar and South Africa. African Primates 10 (2015) / 71

The University of Arizona Summer 2016 Primate Field Primate Studies Field School in Rwanda Schools in This unique and exciting study abroad program focuses on experiential learning in one of Central East Africa's most progressive Africa countries and home to over a dozen species of monkeys and apes, including the famed mountain gorilla. Students will go on adventure treks to observe gorilla families and golden monkeys on the slopes of the extinct Virunga volcanoes; follow groups of chimpanzees, black and white colobus and guenon monkeys in an afro-alpine jungle; and travel on Safari to watch wildlife and study troops of baboons and vervet monkeys in a savanna setting. The Primate Studies Field School promotes a strong interdisciplinary and comparative approach to primate social behavior, family systems, ecology, and conservation, combining perspectives from evolutionary biology, psychology, anthropology, and human development. Participants will have the opportunity to: • Follow and observe in the wild 7-9 monkey and ape species • Learn field methods for behavioral data collection • Walk in Dian Fossey's footsteps with mountain gorillas • Take in Rwanda's scenic beauty-- Africa's little Switzerland • Explore Rwanda's natural and cultural heritage The four-week, six-credit field school held June 2016 is led by University of Arizona faculty primatologists Dieter and Netzin Steklis. Completed applications due by February 15, 2016. More info, photos and journals: www.primatefieldschool.arizona.edu; Dieter and Netzin Steklis (faculty leaders) [email protected].

Sepela Field Programs offers a variety of primate, anthropology, and ecology themed field courses that are perfect for students looking for opportunity to earn their WFA & field experience. CPR certification. Courses are taught by qualified All 2016 field courses will take instructors, and students may place in South Africa and last arrange to receive course credit 3-4 weeks. Students will travel through their home institution. In throughout Limpopo, Mpumalanga, 2016, Sepela will offer field courses & Gauteng, South Africa, visiting including Advanced Methods in Field an array of sites. Courses include Ecology, Field Primatology, and lectures and readings but focus on Primate Veterinary Care. hands-on field experience. More Each field course also includes a information about Sepela Field Wilderness First Aid (WFA) & CPR Programs’ courses can be found at component, allowing students the www.sepela.org. 72 / News

Bioko Island Study Abroad m in elevation, its For over 12 years, the Bioko seven species of Study Abroad program has taken rare monkeys, and students to Bioko as part of an its four species of immersive experience with the nesting sea turtles.Primate Field Bioko Biodiversity Protection • Work in Schools in Program (BBPP) that focuses on collaboration with hands-on experiential learning experienced African Africa and training in biodiversity research. This unique field biologists on program includes individual field research projects an individual research at the Moka Wildlife Center in the highlands of project, and thus Bioko, academically rigorous coursework at the adding to the biodiversity National University of Equatorial Guinea in the database being created for capital city of Malabo, expeditions into Bioko's Bioko Island. tropical forests, and cultural excursions to explore • Work in collaboration with an established Bioko's diverse and storied past. Students have come conservation program on the political, from a wide array of backgrounds, but they have all economic and ecological issues involved in left transformed, with a broadened worldview and a biodiversity conservation, thereby building depth of experience that can only result from study personal credentials and contacts. of complex environmental challenges in a global • Explore the linguistic and cultural diversity of context. To maintain this high level of individualized Equatorial Guinea by collaborating with local study, the program is offered twice a year (September university students on research projects and on - December and January - March) to a class of eight Spanish language skills. students. For more information, please visit www.drexel. The program offers a unique opportunity for edu/studyabroad or contact either Study Abroad undergraduates and recent graduates to: at Drexel University (Daniela Ascarelli; ascareld@ • Study tropical biodiversity and its drexel.edu; 215-895-6280) or Dr. Mary Katherine conservation, with an emphasis on field work Gonder ([email protected]; 215-571-4638). For that takes advantage of Bioko Island's pristine more information on the BBPP and its activities, rainforests ranging from sea level to over 3,000 please visit www.bioko.org.

Field Course in This field course in Methods in Animal Behaviour is designed to provide students with South Africa field experience in biology, ethology and ecology. It is intended for undergraduates, who want to Mawana Game get first experience in working with wild animals. Reserve is a 12,000h Students will acquire knowledge of methods in: privately owned ranch, • measuring environmental variables, such as primarily used as GPS data and phenology a game reserve for • collecting and analysing the natural recreational hunting. Most local wildlife is present, behaviour of free-ranging animals, using with the exception of rhinos, buffalos and lions. telemetry, camera traps, ethograms and A typical day during the field course consists of standard behavioural sampling techniques a one hour introduction to the different methods • field experimentation, including food and used in animal behaviour studies, followed by predator model experiments practical exercises and/or experiments in the field • acoustic analyses, including natural with wild animals. Since this course is operated recordings and playback experiments in collaboration with the Inkawu Vervet Project, For more information, please visit http://www2. eight groups of vervet monkeys that are habituated unine.ch/compcog/field_course_south_africa to the presence of researchers can therefore be or contact Stéphanie Mercier (Stephanie. approached closely. [email protected]; 0041.32.718.24.69). For more The study site is located in Kwazulu-Natal, information on the Inkawu Vervet Project and about 250km from Durban (airport) and about its activities, please visit http://www2.unine. 50km from Vryheid, a large town with shops and ch/compcog/page-27575_fr.html or contact Dr a hospital. Erica van de Waal ([email protected]). African Primates 10 (2015) / 73 Recent Publications*

Ackermann, R.R., L. Schroeder, J. Rogers & J.M. Kibale National Park, Uganda. PLoS ONE 9(7): Cheverud. 2014. Further evidence for phenotypic e102177. signatures of hybridization in descendant baboon Boyer-Ontl, K. & J. Pruetz. 2014. Giving the Forest populations. Journal of Human Evolution 76: 54- Eyes: The benefits of using camera traps to study 62. unhabituated chimpanzees (Pan troglodytes verus) Adeola, A.J., A.N. Apapa, A.I. Adeyemo, S.A. Alaye & in Southeastern Senegal. International Journal of J.A. Ogunjobi. 2014. Seasonal variation in plants Primatology 35(5): 881-894. consumption pattern by foraging olive baboons Brockmeyer, T., P.M. Kappeler, E. Willaume, L. Benoit, (Papio anubis. Lesson, 1827) inside Kainji Lake S. Mboumba & M.J.E. Charpentier. 2015. Social National Park, Nigeria. Journal of Applied Sciences organization and space use of a wild mandrill and Environmental Management 18(3): 481-484. (Mandrillus sphinx) group. American Journal of Araldi, A., C. Barelli, K. Hodges & F. Rovero. 2014. Primatology 77(10): 1036-1048. Density estimation of the endangered Udzungwa Butel, C., S. Mundeke, P. Drakulovski, D. Krasteva, red colobus (Procolobus gordonorum) and other E. Ngole, M. Mallié, E. Delaporte, M. Peeters & arboreal primates in the Udzungwa Mountains S. Locatelli. 2015. Assessment of infections with using systematic distance sampling. International Microsporidia and Cryptosporidium spp. in fecal Journal of Primatology 35(5): 941-956. samples from wild primate populations from Aronsen, G.P., M.M. Beuerlein, D.P. Watts & R.G. Cameroon and Democratic Republic of Congo. Bribiescas. 2015. Redtail and red colobus monkeys International Journal of Primatology 36(2): 227- show intersite urinary cortisol concentration 243. variation in Kibale National Park, Uganda. Caillaud, D., F. Ndagijimana, A.J. Giarrusso, V. Conservation Physiology 3: 10.1093/conphys/ Vecellio & T.S. Stoinski. 2014. Mountain gorilla cov006. ranging patterns: influence of group size and Bădescu, I., P. Sicotte, N. Ting & E.C. Wikberg. 2015. group dynamics. American Journal of Primatology Female parity, maternal kinship, infant age and 76(8): 730-746. sex influence natal attraction and infant handling Cancelliere, E.C., N. Deangelis, J.B. Nkurunungi, D. in a wild colobine (Colobus vellerosus). American Raubenheimer & J.M. Rothman. 2014. Minerals Journal of Primatology 77(4): 376-387. in the foods eaten by mountain gorillas (Gorilla Baker, L.R., A.A. Tanimola & O.S. Olubode. 2014. beringei). PLoS ONE 9(11): e112117. Sacred populations of Cercopithecus sclateri: Carlson, B.A. & J.D. Kingston. 2014. Chimpanzee analysis of apparent population increases from isotopic ecology: a closed canopy C3 template for census counts. American Journal of Primatology hominin dietary reconstruction. Journal of Human 76(4): 303-312. Evolution 76: 107-115. Barelli, C., R. Mundry, A. Araldi, K. Hodges, D. Carne, C., S. Semple, H. Morrogh-Bernard, K. Rocchini & F. Rovero. 2015. Modeling primate Zuberbühler & J. Lehmann. 2014. The risk of abundance in complex landscapes: a case study disease to great apes: simulating disease spread from the Udzungwa Mountains of Tanzania. in orang-utan (Pongo pygmaeus wurmbii) and International Journal of Primatology 36(2): 209- chimpanzee (Pan troglodytes schweinfurthii) 226. association networks. PLoS ONE 9(4): e95039.. Basabose, A.K., E. Inoue, S. Kamungu, B. Murhabale, Carvalho, J.S., C.F.J. Meyer, L. Vicente & T.A. Marques. E.-F. Akomo‐Okoue & J. Yamagiwa. 2015. 2015. Where to nest? Ecological determinants Estimation of chimpanzee community size and of chimpanzee nest abundance and distribution genetic diversity in Kahuzi‐Biega National Park, at the habitat and tree species scale. American Democratic Republic of Congo. American Journal Journal of Primatology 77(2): 186-199. of Primatology 77(9): 1015-1025. Chapman, C.A., V.A.M. Schoof, T.R. Bonnell, J.F. Beamish, E. & M. O’Riain. 2014. The effects of Gogarten & S. Calmé. 2015. Competing pressures permanent injury on the behavior and diet of commensal chacma baboons (Papio ursinus) in the Cape Peninsula, South Africa. International Journal of Primatology 35(5): 1004-1020. * This is not an exhaustive list and focuses mostly Bortolamiol, S. , M. Cohen, K. Potts, F. Pennec, P. on publications from peer-reviewed journals. To Rwaburindore, J. Kasenene, A. Seguya, Q. Vignaud have your new publications listed in this section & S. Krief. 2014. Suitable habitats for endangered frugivorous mammals: small-scale comparison, of future African Primates, please send an e-mail regeneration forest and chimpanzee density in notice to [email protected]. 74 / Recent Publications Recent Publications

on populations: long-term dynamics of food American Journal of Physical Anthropology 158(1): availability, food quality, disease, stress and animal 55-67. abundance. Philosophical Transactions of the Royal Fourie, N., T. Turner, J. Brown, J. Pampush, J. Society of London. Series B, Biological Sciences Lorenz & R. Bernstein. 2015. Variation in vervet 370(1669) DOI: 10.1098/rstb.2014.0112. (Chlorocebus aethiops) hair cortisol concentrations Clay, Z., J. Archbold & K. Zuberbühler. 2015. reflects ecological disturbance by humans. Functional flexibility in wild bonobo vocal Primates 56(4): 365-373. behavior. PeerJ 3: e1124. Fruth, B., N.B. Ikombe, G.K. Matshimba, S. Metzger, Coleman, B.T. & R.A. Hill. 2014. Biogeographic D.M. Muganza, R. Mundry & A. Fowler. 2014. variation in the diet and behaviour of Cercopithecus New evidence for self-medication in bonobos: mitis. Folia Primatologica 85(5): 319-334. Manniophyton fulvum leaf- and stemstrip- Cronin, K.A., E.J.C. van Leeuwen, V. Vreeman & swallowing from LuiKotale, Salonga National D.B.M. Haun. 2014. Population-level variability in Park, DR Congo: Bonobo Self-Medication. the social climates of four chimpanzee societies. American Journal of Primatology 76(2): 146-158. Evolution and Human Behavior 35(5): 389-396. Fuller, J.L. 2014. The vocal repertoire of adult male Danish, L. & R. Palombit. 2014. “Following,” an blue monkeys (Cercopithecus mitis stulmanni): alternative mating strategy used by male olive A quantitative analysis of acoustic structure. baboons (Papio hamadryas anubis): quantitative American Journal of Primatology 76(3): 203-216. behavioral and functional description. Fünfstück, T., M. Arandjelovic, D.B. Morgan, C. International Journal of Primatology 35(2): 394- Sanz, T. Breuer, E.J. Stokes, P. Reed, S.H. Olson, 410. K. Cameron, A. Ondzie, M. Peeters, H.S. Kühl, C. Douglas, P. 2014. Female sociality during the daytime Cipolletta, A. Todd, S. Masi, D.M. Doran‐Sheehy, birth of a wild bonobo at Luikotale, Democratic B.J. Bradley & L. Vigilant. 2014. The genetic Republic of the Congo. Primates 55(4): 533-542. population structure of wild western lowland Dunham, N. 2015. Ontogeny of positional behavior gorillas (Gorilla gorilla gorilla) living in continuous and support use among Colobus angolensis rain forest. American Journal of Primatology 76(9): palliatus of the Diani Forest, Kenya. Primates 868-878. 56(2): 183-192. Ginn, L.P. & K.A.I. Nekaris. 2014. The first survey of Dutton, P. & H. Chapman. 2015. Dietary preferences the conservation status of primates in Southern of a submontane population of the rare Nigerian‐ Burkina Faso, West Africa. Primate Conservation Cameroon chimpanzee (Pan troglodytes ellioti) 28: 129-138. in Ngel Nyaki Forest Reserve, Nigeria. American Gogarten, J., T. Bonnell, L. Brown, M. Campenni, Journal of Primatology 77(1): 86-97. M. Wasserman & C. Chapman. 2014. Increasing Eberhard, M.L., J.R. Owens, H.S. Bishop, M.E. De group size alters behavior of a folivorous primate. Almeida & A.J. Da Silva. 2014. Cyclospora spp. in International Journal of Primatology 35(2): 590- drills, Bioko Island, Equatorial Guinea. Emerging 608. Infectious Diseases 20(3): 510-511. Gogarten, J.F., A.L. Jacob, R.R. Ghai, J.M. Rothman, El Alami, A. & A. Chait. 2014. Comparison of the D. Twinomugisha, M.D. Wasserman & C.A. terrestriality of Barbary macaques (Macaca Chapman. 2015. Group size dynamics over 15+ sylvanus) between tourist and wild sites in years in an African forest primate community. the region of Ouzoud, Morocco. Mammalia: Biotropica 47(1): 101-112. International Journal of the Systematics, Biology Gomez, A., K. Petrzelkova, C.J. Yeoman, K. Vlckova, and Ecology of Mammals 78(4): 539-542. J. Mrázek, I. Koppova, F. Carbonero, A. Ulanov, D. El Alami, A. & A. Chait. 2015. Distribution of the Modry, A. Todd, M. Torralba, K.E. Nelson, H.R. endangered Barbary macaque and human‐ Gaskins, B. Wilson, R.M. Stumpf, B.A. White & macaque interaction in the tourist region of S.R. Leigh. 2015. Gut microbiome composition Ouzoud, Central High Atlas of Morocco. African and metabolomic profiles of wild western lowland Journal of Ecology 53(3): 375-377. gorillas (Gorilla gorilla gorilla) reflect host ecology. Fernández, D., D. Doran-Sheehy, C. Borries & J.L. Molecular Ecology 24(10): 2551-2565. Brown. 2014. Reproductive characteristics of wild Gonedelé Bi, S., A. Bitty, K. Ouatara & W.S. McGraw. Sanje mangabeys (Cercocebus sanjei). American 2014. Primate surveys in Côte d'Ivoire's Sassandra– Journal of Primatology 76(12): 1163-1174. Bandama interfluvial region with notes on a Foerster, S., K. Kithome, M. Cords & S.L. Monfort. remnant population of black‐and‐white colobus. 2015. Social status and helminth infections in African Journal of Ecology 52(4): 491-498. female forest guenons (Cercopithecus mitis). Grimm, D. 2015. Animal welfare. New rules may end African Primates 10 (2015) / 75 Recent Publications

U.S. chimpanzee research. Science (New York, Tanzania. Primate Conservation 28: 109-116. N.Y.) 349(6250): 777. Kinani, J.F. & D. Zimmerman. 2015. Tool use for food Haslam, M. 2014. On the tool use behavior of the acquisition in a wild mountain gorilla (Gorilla bonobo-chimpanzee last common ancestor, and beringei beringei). American Journal of Primatology the origins of hominine stone tool use. American 77(3): 353-357. Journal of Primatology 76(10): 910-918. King, T., C. Chamberlan & A. Courage. 2014. Haurez, B., C.-A. Petre, C. Vermeulen, N. Tagg & J.- Assessing reintroduction success in long-lived L. Doucet. 2014. Western lowland gorilla density primates through population viability analysis: and nesting behavior in a Gabonese forest logged western lowland gorillas Gorilla gorilla gorilla in for 25 years: implications for gorilla conservation. Central Africa. Oryx 48(2): 294-303. Biodiversity and Conservation 23(11): 2669-2687. Koops, K., C. Schöning, M. Isaji & C. Hashimoto. 2015. Hobaiter, C. & R.W. Byrne. 2014. The meanings of Cultural differences in ant-dipping tool length chimpanzee gestures. Current Biology 24(14): between neighbouring chimpanzee communities 1596-1600. at Kalinzu, Uganda. Scientific Reports 5: 12456. Hongo, S. 2014. New evidence from observations of Kopp, G.H., J. Fischer, A. Patzelt, C. Roos & D. Zinner. progressions of mandrills (Mandrillus sphinx): a 2015. Population genetic insights into the social multilevel or non-nested society? Primates 55(4): organization of Guinea baboons (Papio papio): 473-481. evidence for female‐biased dispersal. American Hoppe E., M. Pauly, T.R. Gillespie, C. Akoua-Koffi, Journal of Primatology 77(8): 878-889. G. Hohmann, B. Fruth B, S. Karhemere, N.F. Kopp, G.H., C. Roos, T.M. Butynski, D.E. Wildman, Madinda, L. Mugisha, J. Muyembe, A. Todd, K.J. A.N. Alagaili, L.F. Groeneveld & D. Zinner. 2014. Petrzelkova, M. Gray, M. Robbins, R.A. Bergl, R.M. Out of Africa, but how and when? The case of Wittig, K. Zuberbühler, C. Boesch, G. Schubert, hamadryas baboons (Papio hamadryas). Journal of F.H. Leendertz, B. Ehlers & S. Calvignac-Spencer. Human Evolution 76: 154-164. 2015. Multiple cross-species transmission events Kouassi, R.Y.W., S.W. McGraw, P.K. Yao, A. Abou- of human adenoviruses (HAdV) during hominine Bacar, J. Brunet, B. Pesson, B. Bonfoh, E.K. N'Goran evolution. Molecular Biology and Evolution 32(8): & E. Candolfi. 2015. Diversity and prevalence of 2072-2084. gastrointestinal parasites in seven non-human Hvilsom, C., F. Carlsen, R. Heller, N. Jaffre & H.R. primates of the Taï National Park, Côte d'Ivoire. Siegismund. 2014. Contrasting demographic Parasite 22:1. doi: 10.1051/parasite/2015001. histories of the neighboring bonobo and Langergraber, K.E., C. Rowney, G. Schubert, C. chimpanzee. Primates 55(1): 101-112. Crockford, C. Hobaiter, R. Wittig, R.W. Wrangham, Johnson, C., A.K. Piel, D. Forman, F.A. Stewart & A.J. K. Zuberbühler & L. Vigilant. 2014. How old King. 2015. The ecological determinants of baboon are chimpanzee communities? Time to the most troop movements at local and continental scales. recent common ancestor of the Y-chromosome Movement Ecology 3:14 doi:10.1186/s40462-015- in highly patrilocal societies. Journal of Human 0040-y. Evolution 69: 1-7. Kalan, A., & C. Boesch. 2015. Audience effects Le Flohic, G., P. Motsch, H. Denys, S. Childs, A. in chimpanzee food calls and their potential Courage & T. King. 2015. Behavioural ecology for recruiting others. Behavioral Ecology and and group cohesion of juvenile western lowland Sociobiology 69(10): 1701-1712. gorillas (Gorilla g. gorilla) during rehabilitation Kalan, A.K., R. Mundry, O.J.J. Wagner, S. Heinicke, C. in the Batéké Plateaux National Park, Gabon. PloS Boesch & H.S. Kühl. 2015. Towards the automated ONE 10(3): e0119609. detection and occupancy estimation of primates Lubbe, A., R. Hetem, R. McFarland, L. Barrett, P. using passive acoustic monitoring. Ecological Henzi, D. Mitchell, L. Meyer, S. Maloney & A. Indicators 54: 217-226. Fuller. 2014. Thermoregulatory plasticity in free- Kessler, S., M. Scheumann, D. Hanbury, L. Nash, E. ranging vervet monkeys, Chlorocebus pygerythrus. Zimmermann & S. Watson. 2015. Screams in the Journal of Comparative Physiology B 184(6): 799- night: pilot study reveals moderate evidence for 809. individual differences in Lorisoid vocalizations. Luncz, L.V. & C. Boesch. 2015. The extent of cultural International Journal of Primatology 36(3): 666- variation between adjacent chimpanzee (Pan 678. troglodytes verus) communities: a microecological Kibaja, M. 2014. Diet of the Ashy Red Colobus approach. American Journal of Physical (Piliocolobus tephrosceles) and crop-raiding in Anthropology 156(1): 67-75. a forest-farm mosaic, Mbuzi, Rukwa Region, Luncz, L.V. & C. Boesch. 2014. Tradition over trend: 76 / Recent Publications Recent Publications

neighboring chimpanzee communities maintain data. American Journal of Primatology 77(10): differences in cultural behavior despite frequent 1060-1074. immigration of adult females. American Journal of Narat, V., F. Pennec, B. Simmen, J. Ngawolo & S. Krief. Primatology 76(7): 649-657. 2015. Bonobo habituation in a forest–savanna Macho, G.A. & J.A. Lee-Thorp. 2014. Niche mosaic habitat: influence of ape species, habitat partitioning in sympatric Gorilla and Pan from type, and sociocultural context. Primates 56(4): Cameroon: implications for life history strategies 339-349. and for reconstructing the evolution of hominin Noser, R. & R. Byrne. 2015. Wild chacma baboons life history. PloS ONE 9(7): e102794. (Papio ursinus) remember single foraging Masette, M., G. Isabirye‐Basuta, D. Baranga, C.A. episodes. Animal Cognition 18(4): 921-929. Chapman & J.M. Rothman. 2015. The challenge Paige, A., S. Frost, M. Gibson, J. Jones, A. Shankar, of interpreting primate diets: mangabey foraging W. Switzer, N. Ting & T. Goldberg. 2014. Beyond on Blighia unijugata fruit in relation to changing bushmeat: animal contact, injury, and zoonotic nutrient content. African Journal of Ecology 53(3): disease risk in western Uganda. EcoHealth 11(4): 259-267. 534-543. Masters, J.C. & S. Couette. 2015. Characterizing cryptic Parsons M.B., T.R. Gillespie, E.V. Lonsdorf, D. species: A morphometric analysis of craniodental Travis, L. Lipende, B. Gilagiza, S. Kamenya, L. characters in the dwarf galago genus Galagoides. Pintea & G.M. Vazquez-Prokopec. 2014. Global American Journal of Physical Anthropology 158(2): positioning system data-loggers: a tool to quantify 288-299. fine-scale movement of domestic animals to Mbora, D.N.M. & M.A. Mcpeek. 2015. How monkeys evaluate potential for zoonotic transmission to an see a forest: genetic variation and population endangered wildlife population. PLoS ONE 9(11): genetic structure of two forest primates. e110984. Conservation Genetics 16(3): 559-569. Parsons M.B., D. Travis, E.V. Lonsdorf , I. Lipende, Ménard, N., P. Motsch, A. Delahaye, A. Saintvanne, G. D.W. Roellig, A. Collins, S. Kamenya, H. Zhang, Le Flohic, S. Dupé, D. Vallet, M. Qarro, M.I. Tattou l. Xiao & T.R. Gillespie. 2015. Epidemiology and & J.-S. Pierre. 2014. Effect of habitat quality on diet molecular characterization of Cryptosporidium flexibility in Barbary macaques. American Journal spp. in humans, wild primates, and domesticated of Primatology 76(7): 679-693. animals in the Greater Gombe Ecosystem, Ménard, N., Y. Rantier, A. Foulquier, M. Qarro, Tanzania. PLoS Neglected Tropical Diseases 10(2): L. Chillasse, D. Vallet, J.-S. Pierre & A. Butet. e0003529. 2014. Impact of human pressure and forest Petre, C.A., N. Tagg, R.C. Beudels-Jamar, B. Haurez fragmentation on the Endangered Barbary & J.-L. Doucet. 2015. Western lowland gorilla seed macaque Macaca sylvanus in the Middle Atlas of dispersal: Are seeds adapted to long gut retention Morocco. Oryx 48(2): 276-284. times? Acta Oecologica 67: 59-65. Metsio Sienne, J., R. Buchwald & G. Wittemyer. 2014. Phillips, C. & C. Lancelotti. 2014. Chimpanzee diet: Plant mineral concentrations related to foraging phytolithic analysis of feces. American Journal of preferences of western lowland gorilla in central Primatology 76(8): 757-773. African forest clearings. American Journal of Pradhan, G.R., S.A. Pandit & C.P. van Schaik. 2014. Primatology 76(12): 1115-1126. Why do chimpanzee males attack the females of Milich, K.M., J.M. Bahr, R.M. Stumpf & C.A. neighboring communities? American Journal of Chapman. 2014. Timing is everything: expanding Physical Anthropology 155(3): 430-435. the cost of sexual attraction hypothesis. Animal Price, T. & J. Fischer. 2014. Meaning attribution in the Behaviour 88: 219-224. West African green monkey: influence of call type Milich, K.M. R.M. Stumpf, J.M. Chambers & C.A. and context. Animal Cognition 17(2): 277-286. Chapman. 2014. Female red colobus monkeys Price, T., O. Ndiaye, K. Hammerschmidt & J. Fischer. maintain their densities through flexible feeding 2014. Limited geographic variation in the acoustic strategies in logged forests in Kibale National structure of and responses to adult male alarm Park, Uganda. American Journal of Physical barks of African green monkeys. Behavioral Anthropology 154(1): 52-60. Ecology and Sociobiology 68(5): 815-825. Motsch, P., G. Le Flohic, C. Dilger, A. Delahaye, C. Reiner, W.B., C. Petzinger, M.L. Power, D. Hyeroba Chateau‐Smith & S. Couette. 2015. Degree of & J.M. Rothman. 2014. Fatty acids in mountain terrestrial activity of the elusive sun‐tailed monkey gorilla diets: implications for primate nutrition (Cercopithecus solatus) in Gabon: comparative and health. American Journal of Primatology 76(3): study of behavior and postcranial morphometric 281-288. African Primates 10 (2015) / 77 Recent Publications

Rosenbaum, S., J.P. Hirwa, J.B. Silk, L. Vigilant & T.S. macaque (Macaca sylvanus). Primates 55(3): 369- Stoinski. 2015. Male rank, not paternity, predicts 375. male–immature relationships in mountain gorillas, Vale, C.G., M.J. Da Silva, C. Ferreira, C. Joao, J. Torres Gorilla beringei beringei. Animal Behaviour 104: & J.C. Brito. 2015. Applying species distribution 13-24. modelling to the conservation of an ecologically Rovero, F., A. Mtui, A. Kitegile, P. Jacob, A. Araldi plastic species (Papio papio) across biogeographic & S. Tenan. 2015. Primates decline rapidly in regions in West Africa. Journal for Nature unprotected forests: evidence from a monitoring Conservation 27: 26-36. program with data constraints. PLoS ONE 10(2): Van Andel, A.C., S.A. Wich, C. Boesch, L.P. Koh, M.M. e0118330. Robbins, J. Kelly & H.S. Kuehl. 2015. Locating Roy, J., L. Vigilant, M. Grav, E. Wright, R. Kato, P. chimpanzee nests and identifying fruiting trees Kabano, A. Basabose, E. Tibenda, H.S. Kuhl & with an unmanned aerial vehicle. American M.M. Robbins. 2014. Challenges in the use of Journal of Primatology 77(10): 1122-1134. genetic mark-recapture to estimate the population Van Nguyen, D., H. Harvala, E.M. Ngole, E. size of Bwindi mountain gorillas (Gorilla beringei Delaporte, M.E.J. Woolhouse, M. Peeters & P. beingei). Biological Conservation 180: 249-261. Simmonds. 2014. High rates of infection with Salmi, R. & D.M. Doran‐Sheehy. 2014. The function novel enterovirus variants in wild populations of of loud calls (Hoot Series) in wild western gorillas mandrills and other old world monkey species. (Gorilla gorilla). American Journal of Physical Journal of Virology 88(11): 5967-5976. Anthropology 155(3): 379-391. Webster, T.H., W.C. McGrew, L.F. Marchant, C.L.R. Sanz, C.M., I. Deblauwe, N. Tagg & D.B. Morgan. Payne & K.D. Hunt. 2014. Selective insectivory 2014. Insect prey characteristics affecting regional at Toro-Semliki, Uganda: comparative analyses variation in chimpanzee tool use. Journal of suggest no ‘savanna’ chimpanzee pattern. Journal Human Evolution 71: 28-37. of Human Evolution 71: 20-27. Sibley, S.D., M. Lauck, A.L. Bailey, D. Hyeroba, A. Weyher, A.H., J.E. Phillips-Conroy, M.S. Fourrier & Tumukunde, G. Weny, C.A. Chapman, D.H. C.J. Jolly. 2014. Male-driven grooming bouts in O'Connor, T.L. Goldberg & T.C. Friedrich. 2014. mixed-sex dyads of Kinda baboons (Papio kindae). Discovery and characterization of distinct simian Folia Primatologica 85(3): 178-191. pegiviruses in three wild African Old World Wikberg, E.C., N. Ting & P. Sicotte. 2014. Kinship monkey species. PLoS ONE 9(2): e98569. and similarity in residency status structure female Sistiaga, A., R.W. Wrangham, J.M. Rothman & R.E. social networks in black‐and‐white colobus Summons. 2015. New insights into the evolution monkeys (Colobus vellerosus). American Journal of of the human diet from faecal biomarker analysis Physical Anthropology 153(3): 365-376. in wild chimpanzee and gorilla faeces. PLoS ONE Wren, B.T., T.R. Gillespie, JW. Camp & M.J. Remis. 10(6): e0128931. 2015. Helminths of vervet monkeys, Chlorocebus Steel, R. 2015. Using multiple travel paths to estimate aethiops, from Loskop Dam Nature Reserve, South daily travel distance in arboreal, group-living Africa. Comparative Parasitology 82(1): 101-108. primates. Primates 56(1): 71-75. Wright, E. & M.M. Robbins. 2014. Proximate Stephan, C. & K. Zuberbühler. 2014. Predation mechanisms of contest competition among affects alarm call usage in female Diana monkeys female Bwindi mountain gorillas (Gorilla berengei (Cercopithecus diana diana). Behavioral Ecology beringei). Behavioral Ecology and Sociobiology and Sociobiology 68(2): 321-331. 68(11): 1785-1798. Teichroeb, J., M. White & C. Chapman. 2015. Vervet Yildirim S, C.J. Yeoman, S.C. Janga, S.M. Thomas, (Chlorocebus pygerythrus) intragroup spatial M. Ho & S.R. Leigh. 2014. Primate Microbiome positioning: dominants trade-off predation risk Consortium including Gillespie TR, et al. 2014. for increased food acquisition. International Primate vaginal microbiomes exhibit species Journal of Primatology 36(1): 154-176. specificity without universal Lactobacillus Teichroeb, J.A., E.C. Wikberg, N. Ting & P. Sicotte. dominance. ISME Journal 8:2431–2444. 2014. Factors influencing male affiliation and Young, C., B. Majolo, O. Schülke & J. Ostner. 2014. coalitions in a species with male dispersal Male social bonds and rank predict supporter and intense male–male competition, Colobus selection in cooperative aggression in wild Barbary vellerosus. Behaviour 151(7): 1045-1066. macaques. Animal Behaviour 95: 23-32. Thunström, M., P. Kuchenbuch & C. Young. 2014. Zschoke, A. & R. Thomsen. 2014. Sniffing behaviours Concealing of facial expressions by a wild Barbary in guenons. Folia Primatologica 85(4): 244-251. 78 / Connections: E-news, Web Sites, and Social Media

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Africa Biodiversity Collaborative Group Centre de Conservation pour Chimpanzes • Website: www.abcg.org • Website: http://www.projetprimates.com/en/ • E-newsletter contact: Kamweti Mutu • Facebook: https://www.facebook.com/Cen- ([email protected]) treDeConservationPourChimpanzes • Facebook: www.facebook.com/ ABCGconserve Centre for Education, Research and Conservation • Twitter: http://twitter.com/ABCGconserve of Primates and Nature (CERCOPAN) • Website: www.cercopan.org African Primates (for journal and group) • Facebook: www.facebook.com/CERCOPAN • Website: www.primate-sg.org/african_ • E-newsletter contact: webmaster@cercopan. primates/ org • Facebook: https://www.facebook.com/ • Twitter: http://twitter.com/CERCOPANHQ groups/232900723505713/ • Twitter: http://twitter.com/africanprimates Chimp Eden (JGI Sanctuary, South Africa) • Website: chimpeden.com African Wildlife Foundation • Twitter: https://twitter.com/jgisachimpeden • Website: www.awf.org • Facebook: https://www.facebook.com/Africa Chimpanzee Sanctuary & Wildlife Conservation nWildlifeFoundation?fref=ts&ref=br_tf Trust (Ngamba Island) • Twitter: http://twitter.com/AWF_Official • Website: www.ngambaisland.com/ • E-newsletter contact: info@ngambaisland. Amboseli Baboons org • Website: amboselibaboons.nd.edu • Facebook: www.facebook.com/ngambaisland • Twitter: https://twitter.com/ AmboseliBaboons Colobus Conservation • Website: www.colobusconservation.org Barbary Macaque Awareness and Conservation • Facebook: www.facebook.com/pages/ • Newsletter: Contact: sian@barbarymacaque. Colobus-Conservation/137445029669543 org • Twitter: http://twitter.com/ColobusConserva • Facebook: www.facebook.com/ BarbaryMacaqueAwarenessandConservation Conservation through Public Health • Twitter: http://twitter.com/BMCRif • E-newsletter contact: [email protected] • Facebook: Conservation Through Public The Bioko Biodiversity Protection Program Health https://www.facebook.com/ (BBPP) pages/Conservation-Through-Public- • Website: www.bioko.org Health/115176086614; CTPH Gorilla • Facebook: English - www.facebook.com/ Conservation Camp: https://www.facebook. pages/Bioko-Biodiversity-Protection- com/pages/CTPH-Gorilla-Conservation- Program/107673299261496; Spanish - www. Camp/239975179417714 facebook.com/BiokoBiodiversidad • Twitter: http://twitter.com/CTPHuganda • Twitter: http://twitter.com/Bioko_BBPP The Drill Project The Bonobo Conservation Initiative (BCI) • Website: thedrillproject.org/ • Website: www.bonobo.org • Facebook: https://www.facebook.com/The- • Facebook: www.facebook.com/ Drill-Project-258035237544233/ bonobodotorg • Twitter: http://twitter.com/Bonobodotorg East Africa Primate Diversity and Conservation Program Budongo Conservation Field Station • Website: http://www.wildsolutions.nl/ • Website: www.budongo.org • Twitter: https://twitter.com/WildSolutions • Facebook: www.facebook.com/ pages/Budongo-Conservation-Field- Ebo Forest Research Project Station/111160629076237 • Website: www.eboforest.org • E-Newletter contact: [email protected] African Primates 10 (2015) / 79 Connections: E-News, Web Sites, and Social Media

Falémé Chimpanzees Jane Goodall Institute • Twitter: http://twitter.com/FalemeChimps • Website: janegoodall.org • Facebook: https://www.facebook.com/jane- Fossey Gorilla Fund goodallinst?_rdr=p • Website: gorillafund.org • Twitter: https://twitter.com/JaneGoodallInst • Twitter: https://twitter.com/SavingGorillas Kasanka Baboon Research Project GAIA – Great Ape Institute for Awareness • Website: www.kasankababoonproject.com • Website: www.gaiasanctuary.org/ • Twitter: http://twitter.com/KindaCamp • Facebook: https://www.facebook.com/Pro- tectApes KasokwaForestProject Gorillas Across Africa • Facebook: www.facebook.com/pages/ • Facebook: https://www.facebook.com/Goril- Kasokwa-Forest-Project/159230490821336 lasAcrossAfrica • Twitter: http://twitter.com/KasokwaForest

Great Ape Survival Partnership (GRASP) Le Projet Gorille Fernan-Vaz (Gabon) • Website: www.un-grasp.org • Website: gorillasgabon.org/ • Facebook: www.facebook.com/ • Facebook: https://www.facebook.com/pgfv. graspunep?ref=stream fvgp • Twitter: http://twitter.com/graspunep LimbeWildlifeCentre Guenon Conservation Community • Facebook: www.facebook.com/pages/Limbe- • Facebook: www.facebook.com/pages/ Wildlife-Centre/504832002861894 Guenon-Conservation-Community/2031800 • Twitter: http://twitter.com/LimbeWildlife 09723143?ref=stream Lukuru Foundation HELP Congo (Chimpanzee Sanctuary) • Website: www.lukuru.org • Website: www.help-primates.org/ • Facebook: https://www.facebook.com/ • Facebook: https://www.facebook.com/ LukuruFoundation?fref=ts HELP-Congo-29693148237/ Lwiro Sanctuary Imfene Education and Conservation (Baboons) • Website: www.lwiroprimates.org • Website: www.imfene.org/ • Facebook: www.facebook.com/lwiro • Facebook: https://www.facebook.com/Imfe- • Twitter: https://twitter.com/lwirosanctuary neOutreach Mbeli Bai Study International Gorilla Conservation Programme • Website: www.mbelibaistudy.org • Website: www.igcp.org • Facebook: https://www.facebook.com/Mbe- • Twitter: http://twitter.com/IGCP li-Bai-Study-137426999658859/ • Twitter: https://twitter.com/mbelibai International Primate Protection League • Website: www.ippl.org Ngogo Chimp Project • Facebook: www.facebook.com/ • Website: www.ngogochimpanzeeproject.org/ InternationalPrimateProtectionLeague • Facebook: https://www.facebook.com/ • Twitter: http://twitter.com/ipplprimate NgogoChimps/ • Twitter: https://twitter.com/ngogochimps International Primatological Society – Conservation Pan African Sanctuary Alliance • Website: www. • Website: www.pasaprimates.org internationalprimatologicalsociety.org • E-newsletter contact: [email protected] • Twitter: http://twitter.com/ipsconservation • Facebook: www.facebook.com/pages/PASA- Primates/150322194563 • Twitter: http://twitter.com/pasaprimates 80 / Connections: E-news, Web Sites, and Social Media

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Pandrillus (Primate Sanctuary, Nigeria) Tacugama Chimpanzee Sanctuary • Website: www.pandrillus.org/ • Website: www.tacugama.com/ • Facebook: https://www.facebook.com/Pan- • Facebook: https://www.facebook.com/Tacu- drillus-379304355421353/ gama • Twitter: http://twitter.com/Tacugama PEGG – The South Africa Primatology Associa- tion Tai Chimp Project • Website: www.peggweb.com/index.php • Website: www.wildchimps.org • Facebook: https://www.facebook.com/ • Twitter: http://twitter.com/TaiChimpProject PEGG-The-South-African-Primatology- Association-112433812122602/ Ugalla Primate Project • Website: www.ugallaprimateproject.com Red-bellied Guenon • Facebook: www.facebook.com/ Vervet Monkey Foundation Cercopithecuserythrogastererythrogaster • Facebook: www.facebook.com/groups/vervet • Twitter: http://twitter.com/VervetMonkeys Samango Monkey Project • Facebook: www.facebook.com/groups/ West African Primate Conservation Action samango/ (WAPCA) • WAPCA News contact: jeannemarie. Save the Abandoned Chimps (Liberia) [email protected] • Facebook: https://www.facebook.com/aban- • Facebook: www.facebook.com/pages/ donedchimps West-African-Primate-Conservation- Action/427913537273055 Society for Conservation Biology – Africa Section • E-mail list contact: Beth Kaplin bkaplin@ Wild Chimpanzee Foundation anticho.edu • Website: www.wildchimps.org/ • Facebook: https://www.facebook.com/wildchimps

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Research Articles and Brief Reports: See the inside back cover for details. News: African Primates lists grant opportunities, conferences, job announcements, etc. However, please keep in mind that the journal is published only once or twice per year. Thus, dates for time-sensitive announcements should be considered carefully. Recent Publications: Send the details of any new papers, books, reports published since the last publication of African Primates. Connections - E-News, Web Sites, Social Media: The last three pages of this issue lists ways you can stay connected with the African primatology community. Have we listed your information? Help keep this list up to date and accurate!

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African Primates, a journal of the IUCN SSC Primate • All photographs must be of high quality and Specialist Group, publishes research articles, field submitted electronically. Each should be labeled on reports, review articles, position papers, book reviews, a separate page with a caption and photographer and other news focused on the nonhuman primates of credit. Africa. We welcome submissions focused on behavior, • Maps and sketches should be submitted in ecology, taxonomy, or conservation. The journal is electronic form (e.g., jpeg, tif, gif). produced in both print and digital versions and is • References should be provided in an alphabetical list provided free of charge. The aim of African Primates is and conform to the format used in previous issues to promote conservation of Africa’s primates by: of African Primates. Examples are shown below. 1) enhancing interest in Africa’s primates and • Each author should provide name, affiliation, increasing knowledge about them that is address, telephone and/or fax number, and E-mail relevant to their survival; address. 2) transmitting information about factors and situations that promote or work against Please use the following formats: conservation of African primate species or populations; and Book: 3) providing a forum for discussion and debate Groves, C.P. 2001. Primate Taxonomy. Smithsonian regarding all aspects of knowledge relevant Institution Press, Washington, D.C. to conserving Africa’s primate fauna and their habitats. Journal Article: Chapman, C.A., L. Naughton-Treves, M.J. Lawes, M.D. African Primates encourages submission of relevant Wasserman & T.R. Gillespie. 2007. Population declines information in the form of research findings, field of colobus in western Uganda and conservation survey results, advances in field and laboratory value of forest fragments. International Journal of techniques, field action alerts, and book reviews, as Primatology 28(3): 513–528. well as notification of events, funding opportunities, grassroots efforts such as letter-writing campaigns, Book Chapter: and recent publications in other formats (including Eniang, E.A. 2003. Effects of habitat fragmentation reports and theses). All submissions should be sent on the Cross River gorilla (Gorilla gorilla diehli): to the Editor-in-Chief; research articles will be peer- Recommendations for conservation. In Primates in reviewed before acceptance for publication. Fragments: Ecology and Conservation. L.K. Marsh, ed. Contributors may consult past issues of African Kluwer Academic/Plenum Publishers, New York. Pp. Primates for stylistic guidance. (Previous volumes are 343–363. accessible through the PSG website. See http://www. primate-sg.org/african_primates/.) Unpublished Report: Hearn, G.W., W.A. Morra, M.A. Ela Mba & C. Posa The following guidelines are recommended: Bohome. 2001. The approaching extinction of • Manuscripts (not to exceed 15 pages) should be monkeys and duikers on Bioko Island, Equatorial in English or French, double-spaced, with 1-inch Guinea, Africa. Unpublished report of the Bioko margins. All articles must include an English Biodiversity Protection Program, Arcadia University, abstract. If possible, please provide a French Glenside PA. abstract for English manuscripts. • Authors submitting manuscripts in a language that is Government Document: not their first are encouraged to seek guidance from Ministry of Environment and Natural Resources. 1994. a speaker of that language to insure the manuscript The Kenya National Environment Action Plan (NEAP). is well-written. Ministry of Environment and Natural Resources, • Manuscripts should be produced with PC- Nairobi, Kenya. compatible software (e.g., Microsoft Word) and submitted as an e-mail attachment in *.doc; *docx, or *.rtf format. All reviews and revisions will be conducted via e-mail. Please submit all manuscripts and materials • Use metric units only and define all abbreviations. electronically to: [email protected] • Current taxonomic classifications should be used. However, if species or subspecies’ names have Janette Wallis, Ph.D. undergone recent revision, include mention of African Primates, Editor-in-Chief recent names as a service to readers adjusting to Interdisciplinary Perspectives on the Environment new naming conventions. University of Oklahoma • Tables, figures, and photographs are encouraged. 630 Parrington Oval All require accurate and concise captions listed on a Monnet Hall, Rm 555 separate sheet. Norman, Oklahoma 73019 • Research articles should be accompanied by a map Phone: +1 405.446.9188 indicating location of any place names mentioned in E-mail: [email protected] the text. Please include a map legend. African Primates A Journal of the IUCN SSC Primate Specialist Group Africa Section Volume 10, 2015

Research Articles

Characterization of Nest Sites of Chimpanzees (Pan troglodytes schweinfurthii) in Kibira National Park, Burundi...... 1 Dismas Hakizimana, Alain Hambuckers, Fany Brotcorne, & Marie-Claude Huynen

Seed Dispersal by the Tantalus Monkey, Chlorocebus tantalus: Implications for Forest Restoration and Expansion within an Afromontane Landscape in Nigeria ...... 13 Abigail M. Grassham, Britta K. Kunz, Stephen L. Goldson, Musa Bawaro, & Hazel M. Chapman

First Sightings of the Roloway Monkey (Cercopithecus diana roloway) in Ghana in Ten Years and the Status of Other Endangered Primates in Southwestern Ghana ...... 25 David Osei, Robert H. Horwich, & Jeanne Marie Pitman

Why Don’t Chimpanzees Eat Monitor Lizards? ...... 41 William C. McGrew

Brief Communications

A Note on Barbary Macaque Group Size and Composition in Bouhachem Forest, North Morocco ...... 53 Sián Waters, Ahmed El Harrad, & Mohamed Chetuan

Liberian Chimpanzees Abandoned by New York Blood Center ...... 57 Kathleen Conlee & Jennifer A.Z. Desmond

Top Priority Site for Primate Conservation in Côte d’Ivoire Soon Designated as a Protected Area? ...... 59 Inza Koné, Karim Ouattara, & André Djaha Koffi

Obituary: Geza Taleki ...... 61 Dale Peterson

Obituary: Jerry Lwanga ...... 64 Thomas Struhsaker

News ...... 67 Primatology Field Schools ...... 71 Recent Publications ...... 73 Connections: E-News, Web Sites, and Social Media ...... 78