Volume 12 2017 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 Chairs: Anthony B. Rylands and Christoph Schwitzer Red List Authority Coordinators: 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 Janette Wallis – Editor-in-Chief Chairman: Russell A. Mittermeier University of Oklahoma, Norman, OK USA Deputy Chairs: Anthony B. Rylands and Christoph Schwitzer

Simon Bearder Vice Chair, Section on Great Apes: Liz Macfie Oxford Brookes University, Oxford, UK Deputy Vice Chair, Section on Great Apes: Serge Wich Vice Chair, Section on Small Apes: Benjamin M. Rawson R. Patrick Boundja Wildlife Conservation Society, Congo; Univ of Mass, USA Regional Vice-Chairs – Neotropics Colin A. Chapman Mesoamerica: Liliana Cortés-Ortiz McGill University, Montreal, Quebec, Canada Andean Countries: Erwin Palacios, Eckhard W. Heymann, Fanny M. Cornejo, Stella de la Torre, and Diana C. Guzmán Edem A. Eniang Brazil and the Guianas: M. Cecília M. Kierulff, Fabiano Rodrigues Biodiversity Preservation Center, Calabar, Nigeria de Melo, Maurício Talebi, and Leandro Jerusalinsky Colin Groves Australian National University, Canberra, Australia Regional Vice Chairs – Africa Rachel Ashegbofe Ikemeh, Inza Koné, David Osei, and Janette John Hart Wallis Foundation Lukuru, Kinshasa, DRC Michael A. Huffman Regional Vice Chairs – Madagascar Kyoto University, Inuyama, Japan Christoph Schwitzer, Jonah Ratsimbazafy, and Steig Johnson

Lynne A. Isbell Regional Vice Chairs – Asia University of California, Davis, CA USA China: Baoguo Li Gladys Kalema-Zikusoka South-east Asia/Indochina: Jatna Supriatna, Christian Roos, Conservation through Public Health, Kampala, Uganda Benjamin M. Rawson, Ramesh Boonratana, Le Khac Quyet, and Duc Hoang Minh Shadrack Kamenya South Asia: Sanjay Molur and Dilip Chetry Jane Goodall Institute-Tanzania, Kigoma, Tanzania Inza Koné Red List Authority Coordinators 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 This issue of African Primates was produced with the University of Colorado, Boulder, CO USA assistance of a grant from the Margot Marsh Biodiversity Foundation, through Conservation International’s Primate Judith Masters Action Fund. University of Fort Hare, Alice, South Africa William Olupot Nature and Livelihoods, Kampala, Uganda Shirley C. Strum University of California, San Diego, CA USA Paul T. Telfer Wildlife Conservation Society, Brazzaville, Congo Tharcisse Ukizintambara 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 PSG logo: Stephen D. Nash Front Cover: Adult male red-bellied guenon (Cercopithecus erythrogaster erythrogaster) at Drabo Monkey Sanctuary, Benin. Photo by Maya MT Goodwin. 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 12: 1-8 (2017)/ 1

Species Density of Galago moholi at Loskop Dam Nature Reserve, South Africa

Ian S. Ray1,2,3, Brandi T. Wren2,4, and Evelyn J. Bowers1

1Department of Anthropology, Ball State University, Muncie, IN USA; 2Applied Behavioural Ecology and Ecosystem Research Unit, University of South Africa; 3Department of Social Sciences, Community College of Aurora, Aurora, Colorado USA;4Department of Anthropology, Purdue University, West Lafayette, IN USA

Abstract: Galagos are a poorly studied group of nocturnal primates endemic to sub-Saharan Africa, particularly in regard to distribution in southern Africa. We conducted a population survey of Galago moholi along the road system of Loskop Dam Nature Reserve in Mpumalanga, South Africa, during the winter months of June and July, 2011. Results from 151 km of transects that were driven over 23 survey hours indicate that the population density of G. moholi is several times lower than previously reported in similar areas. We estimate the population density at Loskop Dam to be between 1.4 and 5.1 animals/km2, suggesting a population estimate for the entire reserve of 296-1029 animals. This number is substantially lower than the expected density of 95 animals/km2 and total population of 20,000 animals based on previously published density estimates. Low population density may be due to an unknown environmental condition that, in addition, excludes other Galago species from the reserve.

Key words: Galago, population density, strepsirrhine, bushbaby

INTRODUCTION

Bushbabies, or galagos, are small nocturnal Galago moholi averages 158 g and 438 mm in primates endemic to sub-Saharan Africa. Many total length, with a 288 mm tail and a 150 mm head species of galago inhabit overlapping geographical and body (Nash et al. 1989). Previous reports have ranges, though most have differing habitat listed primary food sources of G. moholi to consist preferences when found sympatrically (Nash et al. exclusively of tree gums and small arthropods 1989; Pozzi 2016). The only member of the genus (Bearder & Martin 1980; Harcourt 1986), though Galago endemic to this study’s research site in recent findings have noted the inclusion of plant Mpumalanga, South Africa, is the southern lesser parts in the diet (Scheun et al. 2014; Ray et al. 2016). bushbaby (Galago moholi A. Smith 1836). Based No observations of heterothermy during the winter on current published distribution data (Bearder months of June and July, when insects are scarce, et al. 2008), the thick-tailed bushbaby (Otolemur have been recorded in natural settings (Mzilikazi et crassicaudatus É. Geoffroy Saint-Hilaire 1812) is al. 2006; Nowack et al. 2010, 2013). not found within this study’s locality, although Bearder & Doyle (1974) reported population greater galagos have been observed nearby. There densities of G. moholi that ranged from a low is a significant lack of published field studies on of 95 animals/km2 in escarpment riparian bush galago behavior and ecology, particularly recent and scrub habitat to a high of 500 animals/km2 in studies. This makes it difficult to establish a baseline Vachellia karoo (previously Acacia karoo) thickets. understanding of galago ecology and distribution in That research, however, commenced in 1968 and is southern Africa. now approaching 50 years old. It is likely that those

Correspondence to: Ian S. Ray, Department of Social Sciencs, Community College of Aurora, 16000 East CentreTech Parkway, Aurora, Colorado 80011 USA; Email: [email protected]. 2 / Ray et al.

numbers are no longer representative due to human 2007). Daily temperatures within the reserve ranged encroachment, habitat changes, anthropogenic from 7°C to 21°C during the study period, and climate change, and changes in land-use patterns from 7°C to 29°C during 2011 (National Center across southern Africa (Hoffman & Ashwell 2001; for Environmental Information 2016). Monthly Thomas et al. 2004; McCusker & Carr 2006). precipitation in 2011 ranged from 0 cm (July) to Further, those estimates vary greatly from 95-500 19 cm (January), with no rainfall occurring during animals/km2 and later studies using radio tracking the study period. The reserve is managed by the found significantly lower densities of 31 animals/ Mpumalanga Tourism and Parks Agency, and the km2 (Bearder 1987). University of South Africa’s Applied Behavioural The goal of this study was to survey the Ecology and Ecosystem Research Unit maintains population of G. moholi at Loskop Dam Nature a research camp within its boundaries. To our Reserve in South Africa to assess its abundance and knowledge, no other research has been conducted distribution. Specifically, our objectives were to: 1) on galagos in LDNR. record sightings of G. moholi; and 2) calculate an estimated population density of G. moholi at the Survey Methods study site. Transects were driven throughout LDNR’s tourist road system between the hours of 1800 and 2200 on MATERIALS AND METHODS 12 nights between June 29 and July 12, 2011 (winter Research Site at the study site). We surveyed a total of 151 km over This project was conducted between June and 23 hours. Transects were driven, not walked, due to July, 2011 at Loskop Dam Nature Reserve (LDNR). safety concerns expressed by reserve management LDNR is located in northern Mpumalanga province, owing to the presence of predators (e.g., leopard) South Africa, with a portion of the reserve extending and large dangerous game (e.g., rhinoceros and into Limpopo province (25°259’ S, 29°189’ E). The buffalo). Transects were selected based on major reserve measures 22,000 ha in size including the road landmarks and driven for approximately three reservoir created by Loskop Dam (Ferrar & Lotter hours per night (Figure 1). Fifteen minute breaks

Figure 1. Map of driven transects and sightings in Loskop Dam Nature Reserve, Mpumalanga, South Africa Species Density of Galago moholi in Loskop Dam Nature Reserve / 3 were taken after each transect to avoid observer by selecting cutoff distances, as it was unlikely that fatigue. Transects were between 2.4 km and 7.5 km. all individuals were sighted beyond this distance. All roads were driven at the beginning, middle, and Maximum reliable perpendicular distance was end of a night and in each direction, resulting in a determined by: 1) constructing a histogram of all total of six separate surveys of each transect. Surveys perpendicular distances at which a subject was were scheduled to ensure each segment had not been sighted (Figure 2) and, 2) selecting any low points driven for at least two hours before collecting data. in sighting frequency as cutoffs. In this study, these The following habitat types are present within low points occurred at 15 m and 30 m. Maximum the survey area of this study: Senegalia caffra–Setaria observer-to-animal distance assumes that all sphacelata var. sphacelata woodland, Vachellia individuals within the distance to the farthest karoo–Dichrostachys cinerea shrubland, Vachellia sighting were observed. Maximum reliable observer- nilotica–Senegalia caffra woodland, Heteropogon to-animal distance was determined by constructing contortus–Sclerocarya birrea woodland, Hyperthelia a histogram of all observer-to-animal distances and dissoluta grassland, Lippia javanica–Loudetia simplex selecting any low points in sighting frequency as shrubland, and Olea europea subsp. africana–Rhus cutoffs. In this study, these low points occurred at leptodictya woodland (Barrett et al. 2010). Although 30 m and 50 m. a comprehensive vegetation survey of LDNR has not For all analytical methods, perpendicular been conducted, these habitat types appear to be distance was calculated using the degrees off transect representative of the areas of the reserve that were of the farthest sighting with the formula (sighting surveyed in this study (Barrett et al. 2010; Filmalter distance) sinθ. Observer-to-animal distance was 2010; Nkosi et al. 2016). determined using a laser rangefinder, and thus A Nissan pick-up truck with an open bed (i.e., needed no mathematical adjustment. We used Excel bakkie) was used for surveys. One member of the for all statistical analyses. research team was chosen as the driver and two team members knelt in the bed of the truck behind the RESULTS cab. This provided 360° visibility for the observers above the cab of the truck. Speed varied from 4-13 We recorded a total of 29 individual encounters km per hour with a target speed of 10 km per hour, of G. moholi (Appendix 1). Observer to animal consistent with the methodologies of other vehicle distance ranged from 5 m to 95 m. Calculated surveys (Nekaris & Jayewardene 2004; Offet al. 2008; perpendicular distances ranged from 0 m to 65 Leca et al. 2013; Acharya et al. 2015). Galago moholi m. The various methods used yielded a range of were spotted by the distinctive red tapetal reflections estimates from 0.96 ± 0.02 animals/km2 to 5.02 ± using 600 lumen LED torches with an illumination 0.11 animals/km2 (Table 1). Due to the low number distance of 412 m. We recorded measurements for of sightings, it was possible to determine only a each of the following variables for every sighting: maximum reliable sighting distance for the entire distance to the individual using a laser rangefinder, a survey area and not for each individual transect. compass bearing to the individual from the transect, The mean perpendicular distance method resulted and GPS coordinates of the vehicle. in the highest density estimate of 5.02 animals/km2, while the mean observer to animal distance method Analysis resulted in a more conservative estimate of 2.97 Transect data were analyzed using six animals/km2. The maximum perpendicular distance methods presented by the (National Research method yielded a density estimate of 1.58 animals/ Council Subcommittee on Conservation of km2, while the maximum observer to animal Natural Populations 1981). These were maximum distance method yielded a density estimate of 0.96 perpendicular distance, maximum reliable animals/km2. Standard deviations were calculated perpendicular distance at 15 m and 30 m, maximum based purely on statistical error and not systematic observer-to-animal distance, maximum reliable error. observer-to-animal distance at 30 m and 50 m, mean With a cut-off of 15 m, the maximum reliable perpendicular distance, and mean observer-to- perpendicular distance method yielded an estimate animal distance. Maximum perpendicular distance of 3.77 animals/km2, or 773 animals throughout the analysis used the greatest perpendicular distance reserve. If a 30 m cut-off is used, that estimate drops at which a subject was spotted to determine the to 2.51 animals/km2 or 515 animals throughout area analyzed from the area sampled. Maximum the reserve. These estimates differ from the similar reliable perpendicular distance truncates these data maximum reliable observer-to-animal distance 4 / Ray et al.

(A) (B)

Figure 2. Histogram of sighting distance to Galago moholi individuals at Loskop Dam Nature Reserve as: (A) calculated perpendicular sighting distance, and (B) linear distances from observers.

method. For this method, a cut-off of 30 m yields an of sites are imperative for understanding galago estimated population density of 1.78 animals/km2 or population distribution and ecology. 365 animals throughout the reserve. If a cut-off of 50 Nash & Whitten (1989) discuss density estimates m is used, the estimate drops to 1.45 animals/km2 or of the similar Galago senegalensis in Kenya (Table 2). 296 animals throughout the reserve. Analytical methods used in their study were similar to the present study, though data were collected DISCUSSION on foot rather than from a driven vehicle (Nash & Whitten 1989). The population density estimate The National Research Council of the United for the area was found to be 1.5 animals/ha, or States determined that the most reliable protocols for approximately 150 animals/km2 (Nash & Whitten determining population density are the maximum 1989). This estimate, while still lower than Bearder reliable perpendicular distance method and the & Doyle’s (1974) estimates, is substantially greater maximum reliable observer-to-animal distance than the estimated population density of LDNR. method (National Research Council Subcommittee Off et al. (2008) also reported population on Conservation of Natural Populations 1981). densities of G. senegalensis in another area of Kenya, Regardless of the method used, the estimated and used the same methods as the present study density of G. moholi at LDNR is lower than the (Table 2). Their analysis resulted in estimates similar estimate of 95 animals/km2 reported by Bearder & to those found by Nash & Whitten (1989). Galago Doyle (1974) (Table 2). Cold temperatures, a higher senegalensis was found to have a population density latitude, higher altitude, and decreased activity of of between 40 and 240 animals/km2, with variation G. moholi during winter months may have resulted largely due to differences in dry bush and riverine in underestimates of the population. Because no habitats (Off et al. 2008). The area surveyed at LDNR study to date has noted such extreme differences contained similar proportions of each habitat and in population structure between seasons (Bearder included a larger overall area of sampling (Table 2). & Doyle 1974; Harcourt 1980), and because this Individuals were most frequently spotted in riverine study occurred during mating season, it is not likely areas or trees adjacent to known waterways, though that the season alone accounts for the substantial the low population density prevented any statistical difference in population estimates. The galago analysis of this observation. population at LDNR could also experience more Vehicular surveys have been used with a wide ecological stress than populations at lower latitudes variety of taxa and terrain, including Myrmecophaga and altitudes. Some stress may be a result of the dam tridactyla in Brazil (de Miranda et al. 2006); Loris and its effects on microhabitats within the reserve tardigradus in Sri Lanka (Nekaris & Jayewardene as well as documented water pollution in the dam 2004); Sus scroffa, Capreolus capreolus, and (Oberholster et al. 2011; Dabrowski et al. 2013). It is Vulpes vulpes in Belgium (Morrelle et al. 2012); also possible that population numbers have declined Trachypithecus auratus in Indonesia (Leca et al. since the previous studies were conducted nearly 2013); and Macaca mulatta in urban India (Acharya fifty years ago. More studies at a greater number et al. 2015). There is debate over the utility of Species Density of Galago moholi in Loskop Dam Nature Reserve / 5 Table 1. Estimated Species Density of G. moholi Using Multiple Analytical Techniques.

Estimated Density Estimated Population in Analytical Method (animals/km2) Reserve (animals) Maximum Perpendicular Distance 1.58 ± 0.03 324 ± 7 Maximum Reliable Perpendicular Distance (15m) 3.77 ± 0.14 773 ± 30 Maximum Reliable Perpendicular Distance (30m) 2.51 ± 0.07 515 ± 15 Maximum Observer to Animal Distance 0.96 ± 0.02 197 ± 5 Maximum Reliable Observer to Animal Distance (30m) 1.78 ± 0.07 365 ± 15 Maximum Reliable Observer to Animal Distance (50m) 1.45 ± 0.04 296 ± 9 Mean Perpendicular Distance 5.02 ± 0.11 1029 ± 23 Mean Observer to Animal Distance 2.97 ± 0.06 609 ± 13 population surveys conducted on foot and those other Galago species in Africa (Bearder & Doyle conducted from a vehicle. We believe that, because 1974; Nash & Whitten 1989; Off et al. 2008). These similar results were obtained by Nash & Whitten findings highlight the lack of knowledge on the (1989) and Offet al. (2008), both methods are ecology and distribution of galagids, especially comparable with regard to galago research. those within southern Africa. Further, recent work Recent fieldwork on strepsirrhines in southern on G. moholi suggests that we have a great deal to Africa has revealed that our understanding of learn still about galago dietary ecology (Scheun et galago distribution and ecology still contains many al. 2014; Ray et al. 2016). This study contributes to gaps (Génin et al. 2016). One major development that gap in knowledge by providing current data on is the recent discovery of Galagoides granti (the galago population size and distribution in southern Mozambique lesser bushbaby) populations within Africa. South Africa (Génin et al. 2016). The species was previously believed not to be present near the South ACKNOWLEDGEMENTS African border, let alone within South Africa, which means that the published distributions of G. moholi We would like to thank Ruby Malzoni and and O. crassicaudatus in southern Africa need to be Michele Mignini for their assistance in conducting revised. the population survey. We are also grateful for the We have noted the marked absence of O. aid provided by Jannie Coetzee and the staff of crassicaudatus from many areas of its range (Ray et the Applied Behavioural Ecology and Ecosystem al. unpublished data). In particular, O. crassicaudatus Research Unit (ABEERU) of the University of South was not observed in the area of the Tuli Block of Africa (UNISA), and for being allowed to work at Botswana during preliminary field excursions for Loskop Dam Nature Reserve. future projects. Because the habitat at LDNR is similar to other nearby areas where O. crassicaudatus LITERATURE CITED is known to exist, it is unclear why that species has not been found at this study site as well (Bearder Acharya, P., A. Sadar & S. Ray. 2015. Determining the 2008). Regardless, the lack of O. crassicaudatus interrelationship between macaque population at LDNR suggests that the low population sizes of and land cover/use type in Delhi, using line G. moholi are not due to competition from larger- transect method. Biological Forum 7(2): 903-943. bodied strepsirrhines, or that G. moholi out- Barrett, A., L.R. Brown, L. Brown & P. Henzi. 2010. competes O. crassicaudatus. A floristic description and utilisation of two home ranges by vervet monkeys in Loskop Dam CONCLUSIONS Nature Reserve, South Africa. Koedoe 52(1). DOI: 10.4102/koedoe.v52i1.990. The density of G. moholi at Loskop Dam Nature Bearder, S.K. & G.A. Doyle. 1974. Ecology of Reserve, at an estimated 2.5-3.8 animals/km2, is bushbabies Galago senegalensis and Galago particularly low compared both to the density crassicaudatus. In Prosimian Biology. R.D. Martin, observed at other sites in southern Africa and to G.A. Doyle & A.C. Walker, eds. Duckworth 6 / Ray et al.

Table 2. Estimates of Galago Population Densities in Africa.

Population Area Estimate Number of Species Location(s) Method Sampled Source (individuals / Observations hectare) (hectares) Galago Ewaso Nyiro maximum 0.4 - 2.4 25.2 185 individuals Off et al. 2008 senegalensis River, Kenya perpendicular 152 encounters

Galago ADC Mutara direct count 1.5 3.5 n/a Nash & senegalensis Cattle Ranch, of focal Whitten 1989 Kenya groups

Galago South Africa, unreported 0.878 - 5.0 unreported unreported Bearder & moholi Rhodesia Doyle 1974

Galago South Africa radio 0.31 100 9000 positional Bearder & moholi telemetry records Martin 1979

Galago Loskop maximum 0.01 284.3 29 individuals present study moholi Dam Nature perpendicular 28 encounters Reserve, South Africa

Publishers, London. Pp 109-130. http://www.scielo.org.za/scielo.php?script=sci_ Bearder, S.K. & R.D. Martin. 1979. The social arttext&pid=S1816-79502013000500010&lng=e organization of a nocturnal primate revealed by n&tlng=pt. radio tracking. In A Handbook on Biotelemetry de Miranda, G.H.B., W.M. Tomás, C.B. Valladares- and Radio Tracking. C.J. Amlaner & D.W. Páuda & F.H.G. Rodrigues. 2006. Giant anteater Macdonald, eds. Pergamon Press, Elmsford, NY. (Myrmecophaga tridactyla) population survey Pp 635-648. in Emas National Park, Brazil: a proposed Bearder, S.K. & R.D. Martin. 1980. Acacia gum monitoring program. Endangered Species and its use by bushbabies, Galago senegalensis. UPDATE 23(3): 96-103. International Journal of Primatology 1(2): 103- Ferrar, T.A. & M.C. Lotter. 2007. Mpumalanga 128. Biodiversity Conservation Plan Handbook. Bearder, S.K. 1987. Bushbabies, lorises, and tarsiers: Nelspruit, Mpumalanga Parks and Tourism diverse societies in solitary foragers. In Primate Agency, Nelspruit, South Africa. Societies. B.B. Smuts, D.L. Cheney, R.M. Seyfarth, Filmalter, N. 2010. A vegetation classification and R.W. Wrangham, and T.T. Struthsaker, eds. management plan for the Hondekraal section Chicago: University of Chicago Press. Pp. 11-24. of the Loskopdam Nature Reserve. Magister Bearder, S. 2008. Otolemur crassicaudatus. The technologiae dissertation, University of South IUCN Red List of Threatened Species 2008: Africa, Johannesburg, South Africa. e.T15643A4943752. http://dx.doi.org/10.2305/ Génin, F., A. Yokwana, N. Kom, S. Couette, T. IUCN.UK.2008.RLTS.T15643A4943752.en. Dieuleveut, S.C. Nash & J.C. Masters. 2016. A Bearder, S., T.M. Butynski & M. Hoffmann. New galago species for South Africa (Primates: 2008. Galago moholi. The IUCN Red List of Strepsirhini: Galagidae). African Zoology 51(3): Threatened Species 2008: e.T8788A12932349. 135-143. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS. Harcourt, C. S. 1980. Behavioural adaptations T8788A12932349.en. in South African Galagos. Unpublished Dabrowski, J., P.J. Oberholster, J.M. Dabrowski, MsC dissertation from University of the J. Le Brasseur & J. Gieskes. 2013. Chemical Witwatersrand, Johannesburg, South Africa. characteristics and limnology of Loskop Dam Harcourt, C. 1986. Seasonal variation in the diet of on the Olifants River (South Africa), in light of South African galagos. International Journal of recent fish and crocodile mortalities.Water SA Primatology 7(5): 491-506. 39(5): 675-686. Retrieved August 01, 2016, from Hoffman, T., & A. Ashwell. 2001.Nature Divided: Species Density of Galago moholi in Loskop Dam Nature Reserve / 7

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Appendix 1. Sighting of Galago moholi at Loskop Dam Nature Reserve, South Africa.

Distance to Degrees off Perpendicular Sighting Location Animal (m) Transect Distance (m) S 25°25.2902' E 29°18.0666' 43 272° 42 S 25°25.8526' E 29°18.1345' 25 245° 1 S 25°24.6606' E 29°19.0892' 18 338° 17 S 25°23.7967' E 29°19.6454' 15 35° 6 S 25°24.2260' E 29°20.7792' 43 284° 41 S 25°24.4770' E 29°20.8126' 60 0° 0 S 25°24.4770' E 29°20.8126' 36 7° 24 S 25°24.7977' E 29°18.8458' 15 123° 7 S 25°25.1446' E 29°18.4181' 5 323° 3 S 25°24.5522' E 29°19.1752' 95 355° 0 S 25°24.6681' E 29°20.6992' 25 75° 10 S 25°24.8473' E 29°20.4168' 33 343° 18 S 25°25.0282' E 29°20.3030' 13 90° 12 S 25°24.4531' E 29°19.0862' 15 321° 8 S 25°24.6125' E 29°19.0329' 19 338° 18 S 25°24.9950' E 29°17.9791' 68 122° 34 S 25°24.3271' E 29°20.7715' 19 285° 15 S 25°24.8282' E 29°18.8129' 24 60° 7 S 25°24.9700' E 29°18.3440' 39 310° 33 S 25°24.6516' E 29°20.7517' 11 80° 11 S 25°24.7895' E 29°20.4585' 44 55° 44 S 25°24.8258' E 29°20.4275' 14 45° 12 S 25°25.0305' E 29°20.2947' 55 65° 45 S 25°24.0658' E 29°20.7500' 5 270° 1 S 25°24.0658' E 29°20.7500' 18 50° 5 S 25°24.3191' E 29°20.7726' 20 313° 18 S 25°26.0207' E 29°15.4519' 53 10° 29 S 25°24.3478' E 29°21.0374' 39 310° 33 S 25°23.9261’ E 29°19.0912' 68 350° 65 African Primates 12: 9-22 (2017)/ 9

Presence of Alkaloids and Cyanogenic Glycosides in Fruits Consumed by Sympatric Bonobos and the Nkundo People at LuiKotale/Salonga National Park, Democratic Republic of Congo and Its Relationship to Food Choice

Nono Bondjengo1,2,3, Gaby Kitengie1,2, Dieudomé Musibono4, Constantin Lubini3, Gottfried Hohmann1 and Barbara Fruth1,5,6

1 Max Planck Institute for Evolutionary and Anthropology, Leipzig, Germany; 2 Institut Congolais pour la Conservation de la Nature, Kinshasa, DRC; 3Université de Mbandaka, Faculté des Sciences, Département de l’Environnement B.P 10, Mbandaka, DRC; 4 Université de Kinshasa, Faculté des Sciences, Département d’Environnement, Kinshasa, DRC; 5 Ludwig Maximilian University of Munich, Faculty of Biology / Department Biology II, Germany; 6 Centre for Research and Conservation/KMDA, Antwerp, Belgium

Abstract: The importance of secondary compounds remains poorly studied in wild plants eaten by bonobos (Pan paniscus) and humans. As part of this study, alkaloids and cyanogenic glycosides (cyanide) were investigated in wild fruits consumed by bonobos at LuiKotale in Salonga National Park. In high concentrations, the two components can become toxic. Therefore, we investigated whether the bonobos and the Nkundo people avoid high concentrations of these components in their food. To analyze alkaloids and to detect the presence of cyanogenic glycosides, we used semi-quantitative methods. Of the 75 species of fruit analyzed, 28 species (37%) were revealed to have alkaloids at different proportions and 47 species (63%) were shown to be without alkaloids, 12 species (16%) with low concentrations (+), 14 species (19%) with moderate concentrations (++), and two species (3%) with high concentrations (+++). Of the 75 species, 60 were eaten, of which 46 were consumed only by bonobos, 13 were eaten by both bonobos and the Nkundo people, and one species (Piper guinensis) was eaten only by the Nkundo people. In total, bonobos ate 59 species and the Nkundo people 14 species. Of the 60 species consumed, the majority, i.e., 39 species (65%) did not show the presence of alkaloids, while 11 species (18%) showed a low concentration and 10 species (17%) moderate concentrations. As for cyanogenic glycosides (cyanide), this was detected in only three of the 75 species of fruit analyzed. Two species, Camptostylus mannii and Dasylepsis seretii, belong to the Achariaceae family, with Oncoba welwitschii in the Salicaceae family. The two species of Achariaceae both contain alkaloids and cyanogenic glycosides. No species eaten by the Nkundo contained cyanogenic glycosides. Hence, we infer that bonobos and the Nkundo people both avoid eating fruit species that contain high concentrations of alkaloids and cyanogenic glycosides, and this might have relevance linked to the evolution of seed dispersal.

Key words: Secondary compounds, fruits, bonobo, Nkundo, Salonga National Park

Résumé: L’importance des composés secondaires dans les plantes sauvages consommées par Pan paniscus (bonobo) reste encore peu étudiée. Dans le cadre de cette étude, les alcaloïdes et les hétérosides cyanogénétiques (cyanures) ont été recherchés dans les fruits consommés par la population Nkundo et les bonobos de Luikotale,

Correspondence to: Nono Bondjengo, Max Planck Institute for Evolutionary and Anthropology, Deutscher Platz Nr.6, D- 04103 Leipzig; E-mail: [email protected]. 10 / Bondjengo et al.

Parc National de la Salonga ainsi que dans ceux qui ne sont pas consomés. A travers cette étude, nous avons cherché à connaître si les bonobos et les Nkundo évitent de fortes concentrations en ces éléments dans leur nourriture. Notre méthodologie a consisté à rechercher les alcaloïdes et les glycosides cyanogénétiques en utilisant la méthode semi-quantitative. Sur les 75 espèces de fruits analysées, 28 (37%) ce sont révélées avec alcaloïdes à différentes proportions et 47 (63%) espèces de fruits ce sont révélées sans alcaloïdes. Parmi les 75 espèces de fruits analysées, 60 ont été mangés dont, 59 ont été mangés par les bonobos parmi lesquelles, 13 ont été mangées par les Nkundo et par les bonobos et une espèce (Piper guineensis) a été mangée uniquement par les Nkundo. Parmi les 60 espèces mangées, la grande majorité, soit 39 espèces (65%) n’ont pas montré la présence d'alcaloïdes, onze espèces (18 %) ont montré une faible concentration et dix espèces (17%) ont montré une concentration moyenne. Quant aux hétérosides cyanogénétiques (cyanures), les tests fait sur les 75 espèces de fruits nous ont permis d’identifier trois (4%) espèces qui en contiennent. Parmi ces trois espèces, deux d’entre elles appartiennent à la famille des Achariaceae, il s’agit de: Camptostylus mannii, et Dasylepsis seretii. L’espèce Oncoba welwitschii par contre appartient à la famille des Salicaceae. La proportion de fruits sans alcaloïdes était plus élevée que ceux avec alcaloïdes. Ces proportions sont plus élevées pour les glycosides cyanogénétiques. Par conséquent, nous pouvons dire que les bonobos et la population Nkundo évitent de manger des espèces de fruits qui contiennent une forte concentration en alcaloïdes et glycosides cyanogénétiques.

Mots clés : Composés secondaires, fruits, bonobo, Nkundo, Parc National de la Salonga

INTRODUCTION

The forests of the Central Congo Basin contain 2012). These forests provide a high diversity of a diverse mix of plants and animals, including ligneous plants bearing fruit, 85 % of which produce many plants producing a wide variety of fruits, of fleshy fruits to attract animals for primary seed which most are edible by animals (FAO 2006). dispersal (Beaune et al. 2013). In addition, the habitat Much scientific research looking at animal food is not markedly seasonal, providing fruit throughout choice has concentrated on the nutrient content the year. This is similar to Rubondo National Park, an (e.g., Hohmann et al. 2006; Kamungu et al. 2015). island in the southwestern corner of Lake Victoria, This approach assumes that foraging is focused Budongo Forest, and Bwindi Impenetrable National on optimizing the supply of macronutrients, such Park in Uganda, where important chimpanzee fruit as fats, carbohydrates, and proteins (Pasquet et al. foods are available across all months, with no distinct 2011). periods of habitat-wide fruit scarcity (Newton- However, other studies have shown that food Fisher 1999; Newton-Fisher et al. 2000; Stanford choice is influenced by the avoidance of substances & Nkurunungi 2003; Moscovice et al. 2007). Thus, that alter the organoleptic quality (Hohmann et as bonobos are primarily frugivores (Badrian et al. al. 2006; Doran-Sheehy et al. 2009). Some field 1981; Kano 1983; Wrangham 1986), it is likely that and experimental studies have indicated that the they avoid foods containing high concentrations of choice of foods as well as food intake efficiency antifeedants, and rather select for macronutrients, are affected by a number of parameters, including including sugars. This avoidance of toxic secondary nutritional quality, distribution, and abundance of metabolites may be triggered by an unpleasant resources (Carlo et al. 2003; Saracco et al. 2004). taste, which for most primates has been shown to Some studies even suggest that the presence of correspond to a primary rejection reaction by the secondary compounds may be the major driver of gusto-facial reflex, considered as an adaptation for food selection by animals (Alm et al. 2000; Clauss avoiding more or less toxic plant products (Hladik et al. 2003). For example, fruits may occasionally 2002). contain undesirable substances for nutrition, such The prevalence of secondary metabolites, as secondary compounds, and depending on their including alkaloids and cyanogenic glycosides, in concentration, these substances may become toxic wild plant foods consumed by bonobos and the local for their consumers. These include very active plant Nkundo population is almost completely unknown. poisons with a specific action, some of which can be As with other secondary metabolites, there are used medicinally (Hopkins 2003; Irina et al. 2012). a number of arguments in favor of a defensive Bonobos (Pan paniscus) live only in the equatorial (antifeedant) role for alkaloids (Hartmann 1991; forests south of the Congo River (IUCN & ICCN Lebreton 1982; Douglas & Martin 1998). However, Alkaloids and Cyanogenic Glycosides in Bonobos / 11 alkaloids also have diverse medicinal properties alkaloids or the presence of cyanogenic glycosides in (Bernhoft 2008). their food. In addition, we investigate bonobo and Cyanogenic glycosides are present in some species human food choice with respect to the concentration of plants and offer an immediate chemical defense of these components. against herbivores and pathogens causing damage to the plant tissue (Moller 2010). Nevertheless, the MATERIALS AND METHODS sensitivity of animals towards cyanogenic glycosides varies considerably, depending on the species (Jones This investigation was conducted between June 1988). 2007 and March 2008 at the study site of LuiKotale, Here, we investigate alkaloids and cyanogenic located at the southwestern fringe of Salonga National glycosides in both fruits consumed and not Park (2° 45.610 S, 20° 22.723 E; Hohmann & Fruth consumed by bonobos and the Nkundo population, 2008; Figure 1). The study site was started in 2002 the local human inhabitants of the neighboring area. and hosts projects focusing on plant diversity and Through this investigation, we seek to understand bonobo behavioral ecology, conducted by shifting whether bonobos avoid high concentrations of teams of researchers, students, and volunteers. The

Figure 1. Location of the study site at LuiKotale, in Salonga National Park, Democratic Republic of Congo. Map courtesy (http://scalar.usc.edu/works/graphics-for conservation/media/LuiKotale_781.jpg). 12 / Bondjengo et al.

climate is equatorial with abundant rainfall (>2000 occur. In the cases where alkaloids were present, the mm/year), a short dry season in February and a long reaction produced a precipitate. The concentration dry season between May and August. The monthly of alkaloids in the filtrate was ranked on a scale of average temperature ranges between 18 and 29° C, 0 – 3. When almost all the reagent reacted with the with a minimum of 15.7° C and a maximum of 37.3° filtrate, it was assigned a 3 or +++, when half of the C (Fruth et al. 2014). filtrate reacted it was assigned a 2 or ++ and when We focused our investigation on those species 1/3 of the filtrate reacted, it was assigned a 1 or +. that produce fruits seasonally. Identification was When there was no precipitate formation in the confirmed with the help of a reference herbarium, filtrate it was assigned a 0. established during the framework of the long- Similarly, semi-quantitative analyses were used term project, "The Cuvette Central as a reservoir for the detection of cyanogenic glycosides according of medicinal plants" (Fruth 2011). After cross- to the method of Feigl and Anger (1966). This checking, plant samples were deposited at the simple field detection method detects the presence herbarium of the INERA, located at the University of cyanide from small amounts of plant material. of Kinshasa. Fruits were crushed in a mortar, mixed with distilled Fruits were collected along standardized water, and poured into a tube. Feigl-Anger paper was phenological transects, as well as opportunistically placed in the tube without contacting the solution, outside transects when following bonobos, and and the top was sealed. Within approximately five brought back to camp for analysis (Figure 2). Only minutes, if cyanide was present, a reaction turned ripe fruit was taken into consideration as the state the paper from white to blue. that is eaten by both bonobos and the Nkundo people. Alkaloids were identified following a semi- RESULTS quantitative method described by Ganzhorn (1989) using three reagents: Dragendorff´s, Wagner´s, 1. Alkaloids and Mayer's. The fruit pulp was crushed using a Almost 2/3 of the 75 species (63%) did not porcelain or steel mortar. Sulfuric acid (0.1 M) was show the presence of alkaloids, while 28 species added, and the solution was passed through filter (37%) revealed alkaloids of different proportions: paper (Rotilabo R, 80 mm in diameter). A drop 12 species (16%) showed a low concentration (+), of the filtrate was deposited in each of four petri 14 species (19%) showed an average concentration dishes. One served as a control. Next, a drop of each (++), and 2 species (3%) had a high concentration reagent was pipetted onto the filtrate. The reaction (+++). Of the 75 species of fruit analyzed, 60 were was either immediate or took up to a few minutes to eaten, of which 46 were eaten only by bonobos, 13

(A) (B)

Figure 2. (A) Analyses of the alkaloids and cyanogenic glycosides in the laboratory at Luikotale, (B) Results of the analysis of alkaloids in the fruit of Picralima nitida. Alkaloids and Cyanogenic Glycosides in Bonobos / 13 were eaten by both bonobos and the Nkundo people, (Badrian et al. 1981; Kano 1983; Boesch et al. 2002). while one species (Piper guinensis) was eaten only The fruits observed to be consumed here are also by the Nkundo. In total, bonobos ate 59 species and consumed by bonobos elsewhere: most of these the Nkundo consumed 14 species. Of the 60 species species are cited by Idani et al. (1994) as part of the eaten, 11 species (18%) showed a low concentration bonobo diet at Wamba/Lopori, while the fruit of (+) of alkaloids, while 10 species (17%) showed a Dialium zenkeri is noted in other studies (Yamamoto moderate concentration (++). No species of fruit et al. 2009; Beaune et al. 2013). consumed by bonobos and the Nkundo people The alkaloid tests carried out on 75 different showed an alkaloid abundance rank of +++ (Table species of fruit showed that 47 species (63%) did 1). not show the presence of alkaloids, while 28 species Table 2 indicates the number of species consumed (37%) contained alkaloids of different proportions: by humans and bonobos. Looking at the alkaloid 12 species (16%) showed low concentration (+), 14 content, nine (64%) of the 14 species consumed by species (19%) a moderate concentration (++) and the Nkundo people had no alkaloids, while four 2 species (3%) a high concentration (+++). Of the species (29%) contained low (+) concentrations, 60 species of fruit consumed by bonobos and the with just one species (7%), Canarium schweinfurthii, local population of Nkundo people, 39 fruit species having a moderate concentration (++) of alkaloids. (65%) did not contain alkaloids; 11 species (18%) None of the fruits consumed by the Nkundo had a showed a low concentration (+) and 10 species high concentration (+++) of alkaloids. (17%) a moderate concentration (++), but no As for the fruits not consumed by the local species contained alkaloids in high concentration. people and bonobos, these comprise a total of 15 To confirm the presence or absence of alkaloids, our species. Of these, seven species (47%) contained procedure involved using three reagents, including alkaloids, with three fruit species found to have a Dragendorff, Wagner and Mayer. Chapmanet al. high concentration (+++), three species with an (2003) used only Dragendorff’s reagent to test for average concentration (++), and one species with a the presence of alkaloids, which sometimes produces low concentration (+). The eight remaining species false positive results (Waterman 1993). (53%) did not contain alkaloids (Table 3). In Gabon, tests carried out on samples of 382 plant species collected at random in the Ipassa- 2. Cyanogenic glycosides Mingouli rainforest and on 38 plant species eaten by Table 4 indicates the results of the 75 species of chimpanzees gave only 15% positive results for the fruits analyzed for cyanogenic glycosides content. presence of alkaloids, using Mayer and Dragendorff Only 3 (4%) of the 75 species tested contained reagents (Hladik & Hladik 1977). These results cyanogenic glycosides: Camptostylus mannii, indicate that chimpanzees, like bonobos, showed Dasylepsis seretii and Oncoba welwitschii. The first little selection against plants containing alkaloids two species belong to the Achariaceae family and (Clutton-Brock 1977). Oncoba welwitschii is in the Salicaceae family. According to Whitten (1980), the Kloss gibbon (Hylobates klossi), found on islands off the west coast DISCUSSION of Sumatra, has been observed to eat the fruits of Arenga obtusifolia which contain oxalate, though Out of the 75 species of fruit collected, we have the gibbon may avoid toxicity by careful selection identified 59 species of fruit consumed by bonobos, of ripe fruit. Moreover, Waser (1977) recorded of which 13 are consumed concurrently by both that mangabeys (Lophocebus albigena) avoid the bonobos and the Nkundo, and one species consumed alkaloid-rich fruits of Rauvolfia and Strychnos. only by the Nkundo people (Piper guinensis). These Similarly, chimpanzees avoid alkaloid-rich fruits results show that bonobos consume a larger number of Picralima (Hladik & Hladik 1977). Meanwhile, of species compared to the local Nkundo population. Remis et al. (2001) concluded that lowland gorillas This can be explained partly by the fact that fruits in the Central African Republic appear to avoid comprise only a minor part of the human diet, and nitrogen-based alkaloids, even when preferred that a number of cultivated fruits are also available foods are scarce. such as oranges, papayas, mangoes, pineapples, etc. The chimpanzee’s food selection strategy may In contrast, wild fruits form the main component be to prefer non-poisonous alkaloid-free foods, of the bonobo diet (Rafert & Vineberg 1997). Like ingest astringent foods when they are also sweet, chimpanzees, bonobos are primarily frugivorous, and consume some foods containing alkaloids when with fruit accounting for 49-63% of their diet they have some nutritional or possibly medicinal 14 / Bondjengo et al. 0 0 0 0 0 HCN + + 0 0 0 0 0 0 0 0 0 0 0 +++ +++ 0 ++ 0 ++ 0 0 0 0 + + 0 ++ 0 0 ++ 0 Result 3 3 0 2 0 FrWa 2 0 0 0 0 1 1 0 2 0 0 2 0 FrMa 3 3 0 0 0 2 0 0 0 0 1 1 0 2 0 0 2 0 FrDr 3 3 0 2 0 0 0 0 0 1 1 0 2 0 0 2 0 2 HS 0 0 0 1 0 0 1 0 0 1 0 0 0 0 0 1 1 0 0 0 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 BFT Elongo kodzi ya moindo kodzi Elongo Losekola Boele Saw saw Imbedzi ya pembe Imbedzi Bokongwende II Ipambua Bohungwu Bodzingo Ikodzi konga ya pembe Impimbo Bodzinda Bodzungu IIa Bodzungu IIb Baole Botsuatope Botolo Bonkasa ya esobe Nkundo name Pleiocarpa pycnantha Pleiocarpa pycnantha iboga Tabernanthe Canarium schweinfurthii yangambiensis Dacryodes Dasylepis cfr.seretii Dasylepis Antrocaryon nannanii Sorindea sp. arborescens Trichoscypha Anonidium mannii olivacea Enantia enghiana Friesoldielsia suaveolens Polyalthia Uvariopsis letestui solheidii Uvariopsis ochracea Dictyophleba Landolphia owariensis nitida Picralima Camptostylus mannii Species Burseraceae Achariaceae Anacardiaceae Annonaceae Apocynaceae Families Achariaceae BFT: Bonobo Feeding Tree, FrDr: Fruit analyzed with Dragendorff's reagent, FrMa: Fruit analyzed with Mayer's reagent, FrWa: Fruit analyzed with Wagner´s Wagner´s analyzed with Fruit FrWa: reagent, Mayer's analyzed with Dragendorff's with Fruit analyzed FrDr: Fruit FrMa: reagent, Tree, Bonobo Feeding BFT: paniscus. , Pp: Pan sapiens Homo Hs: CN: Cyanide, reagent, Table 1. The 75 speciesof 1. The 75 alkaloids both presence of humans. the fruits,by and and indicating bonobos cyanides,well as as consumption Table Alkaloids and Cyanogenic Glycosides in Bonobos / 15 0 0 HCN 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 + + 0 0 0 0 0 0 +++ 0 0 0 0 0 0 0 0 0 Result FrWa 1 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 0 FrMa 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 0 0 1 0 1 FrDr 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 1 0 HS 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 1 1 1 1 1 1 0 1 1 1 1 1 0 1 0 BFT 1 1 1 1 Boseki ya moindo Boseki ya pembe Bodzilompongo Botendo Bosepe Itatalongo Bokoli Mandza Bopambe ya pembe Kalanga Bontepfu ya zamba Bondenge pembe Maku Maku rouge Atsangila Buaka Bofulu Nkundo name Bondzale II rouge Maku Klainedoxa gabonensis gabonensis Klainedoxa Irvingia gabonensis gabonensis Irvingia Parinari excelsa chromocarpa Garcinia Garcinia punctata Garcinia smeathmannii africana Mammea melanocarpa Diospyros Drypetes gossweileri Drypetes leonensis pynaertii Phyllantus africana Plagiostyles angolense Dialium Dialium corbisieri fragrans Macrolobium africana Tessmannia soyauxii Pterocarpus Parinari congensis congensis Parinari Dialium zenkeri zenkeri Dialium Species Irvingiaceae Clusiaceae/ Clusiaceae/ Clusiodeae Ebenaceae Euphorbiaceae Fabaceae/ Caesalpinioideae Fabaceae/ Faboideae Families Chrysobalanaceae BFT: Bonobo Feeding Tree, FrDr: Fruit analyzed with Dragendorff's reagent, FrMa: Fruit analyzed with Mayer's reagent, FrWa: Fruit analyzed with Wagner´s Wagner´s analyzed with Fruit FrWa: reagent, Mayer's analyzed with Dragendorff's with Fruit analyzed FrDr: Fruit FrMa: reagent, Tree, Bonobo Feeding BFT: paniscus. , Pp: Pan sapiens Homo Hs: CN: Cyanide, reagent, Table 1. The 75 speciesof 1. The 75 alkaloids both presence (Cont.)of humans. the fruits,by and and indicating bonobos cyanides,well as as consumption Table 16 / Bondjengo et al. 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 HCN + + + 0 0 0 0 ++ 0 ++ 0 ++ 0 + + 0 ++ ++ Result 1 1 1 0 0 0 0 2 0 2 0 2 0 1 1 0 2 2 FrWa 1 1 1 0 0 0 0 1 0 2 0 1 0 1 1 0 1 0 FrMa 1 0 1 0 0 0 0 2 1 3 0 2 0 1 1 0 2 2 FrDr 1 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 HS 0 0 1 0 1 1 0 1 0 1 1 0 0 1 1 1 0 1 BFT Boleleko Bongondo Enkendu ya bundo Enkendu Bokolombe Lokumo Boimbo Boala Bokungu II Bokungu Lopetu ya bonkoko Lopetu NID( B 3000) Eonge Nkokoloko Bomomongo Bopfumo Bonkasa ya mai Londaa Bomposo ya pembe Loote Nkundo name Piper guineensis schum. schum. guineensis Piper Strombosiopsis zenkeri zenkeri Strombosiopsis Not identified Not Staudtia kamerunensis kamerunensis Staudtia Ficus sp. Ficus Treculia africanaTreculia Pentaclethra macrophylla macrophylla Pentaclethra Parkia bicolorParkia Penianthus longifolius Stephania laetificata Stephania Trichilia heudalotii heudalotii Trichilia Sarcophrynium schweinfurthianum Hypselodelphis poggeana Hypselodelphis Grewia coriacea Cola griseiflora griseiflora Cola Ceiba pentandra Ceiba Hugonia gilletti gilletti Hugonia Irvingia grandifolia Species Piperaceae Olacaceae Not identified Not Myristicaceae Moraceae Fabaceae/ Mimosoideae Menispermaceae Menispermaceae Meliaceae Marantaceae Malvaceae/ Tilioideae Malvaceae/ Sterculioideae Malvaceae/ Bombacoideae Linaceae Families Table 1. The 75 speciesof 1. The 75 alkaloids both presence (Cont.)of humans. the fruits,by and and indicating bonobos cyanides,well as as consumption Table BFT: Bonobo Feeding Tree, FrDr: Fruit analyzed with Dragendorff's reagent, FrMa: Fruit analyzed with Mayer's reagent, FrWa: Fruit analyzed with Wagner´s Wagner´s analyzed with Fruit FrWa: reagent, Mayer's analyzed with Dragendorff's with Fruit analyzed FrDr: Fruit FrMa: reagent, Tree, Bonobo Feeding BFT: paniscus. , Pp: Pan sapiens Homo Hs: CN: Cyanide, reagent, Alkaloids and Cyanogenic Glycosides in Bonobos / 17 0 0 0 0 0 0 0 0 0 0 0 0 0 + 0 0 0 0 0 0 HCN 0 0 + 0 0 0 0 0 + ++ 0 + ++ ++ 0 0 0 ++ 0 0 Result 0 2 0 0 FrWa 0 0 1 0 0 0 0 0 1 2 0 1 2 2 0 0 0 2 0 0 FrMa 0 0 0 0 0 0 0 0 1 1 0 0 2 2 0 0 0 0 1 0 0 0 0 0 1 2 0 1 2 2 0 0 0 2 0 0 FrDr 0 0 0 1 HS 0 0 0 0 0 0 1 0 1 0 0 1 0 0 1 0 1 0 1 1 BFT 1 0 1 0 1 1 1 1 1 1 1 1 1 1 1 1 Lilala ya dzamba Welo Isilalongi Boseke Botaatata Bontole badzumba Bontole Ilonge Pambu Ilonge Bosanga Pepepe Bopfunga totodu II totodu Bopfunga Bopfunga Bopfunga Boonya Bopambu Etende Nkema Etende Mpanda Botende Booso Saake Mbole ya mai NID (comme Bota - NID (comme atata) Nkundo name - Cissus sp Cissus dinklagei dinklagei Cissus Dicranolepis disticha disticha Dicranolepis Zeyherella longepedicellata longepedicellata Zeyherella poides poides Tridesmostemon omphalocarTridesmostemon Synsepalum sp. Synsepalum subcordatum subcordatum Synsepalum Synsepalum longecuneatum Manilkara obovata Gambeya lacourtiana lacourtiana Gambeya Placodiscus paniculatus Pancovia sp Pancovia Pancovia laurentii Blighia welwitschii welwitschii Blighia Oncoba welwitschii welwitschii Oncoba Afromomum alboviolaceaum Vangueriella orthancantha Massularia acuminata acuminata Massularia Colletoecema dewevreiColletoecema Carpolobia glabrescens Species Vitaceae Thymeleaceae Sapotaceae Sapotaceae Rubiaceae Rubiaceae Sapindaceae Polygalaceae Salicaceae Zingiberaceae Families Table 1. The 75 speciesof 1. The 75 alkaloids both presence (Cont.)of humans. the fruits,by and and indicating bonobos cyanides,well as as consumption Table Wagner´s analyzed with Fruit FrWa: reagent, Mayer's analyzed with Dragendorff's with Fruit analyzed FrDr: Fruit FrMa: reagent, Tree, Bonobo Feeding BFT: paniscus. , Pp: Pan sapiens Homo Hs: CN: Cyanide, reagent, 18 / Bondjengo et al.

Table 2. The number of species with alkaloids, cyanogenic glycosides, and consumed by the Nkundo and bonobos.

n=75 species Yes No With alkaloids 27 48 With cyanogenic glycosides 3 72 Consumed by H. sapiens 14 61 Consumed by P. paniscus 59 16

value, as observed in Mahale National Park, western environment such as the LuiKotale Forest reveals Tanzania (Nishida 2012). This may similarly explain few fruits rich in alkaloids (Hladik et al. 2011). the absence of a high concentration of alkaloids in Abiodun et al. (2014) reported that high alkaloid the fruits consumed by bonobos and humans in content causes toxicity when ingested by human this study. Among the species eaten by the Nkundo beings, which is linked primarily with their ability people, only Canarium schweinfurthii showed a to interfere with various neurotransmitters (Krief moderate concentration of alkaloids in the raw state 2003). Alkaloid over-consumption could be the as consumed by the bonobo. However, before being origin of many cases of poisoning in veterinary eaten by humans, the fruit is softened in hot water medicine, as is the case in domestic herbivores (Bondjengo 2011). Therefore, it is likely that the after ingestion of excessive amounts of lupine, rich fruit of Canarium schweinfurthii is not only cooked in alkaloids known as quinolizidiniques (Mazid to be softened, but also to eliminate some alkaloids et al. 2011). These items when consumed in small that give a bad taste to the fruit in its raw state. This amounts have been referred to as ‘medicinal foods’ treatment is also known to occur in Cameroon by Huffman (1997), and by Masi et al. (2012) as (Njoukan 1998; Tchouamo et al. 2000). According unusual items of consumption; both propose some to Irina et al. (2012), humans have used alkaloid- kind of medicinal value. The great ape diet is indeed containing plants and animals since ancient times rich in plants containing secondary compounds of as poisons, stimulants, aphrodisiacs, and medicines. non-nutritional, sometimes toxic, and medical value Indeed, alkaloid-containing plants have been – and (Huffman 2003). still are – part of our regular diet (Irina et al. 2012). Regarding cyanogenic glycosides, we used the However, it is not only alkaloids that give a bad taste same test of Feigl-Anger as Chapman et al. (2003). to fruits, but also other compounds (such as tannin) Only three species were found to contain these that may prevent bonobos from eating these fruit substances out of the 75 species surveyed. Our species (Hladik et al. 2011). Nevertheless, great apes results are in line with Bouquet and Fournet (1975), may be more tolerant to bitter tastes than humans. who also found the same species with cyanogenic For example, Hladik and Simmen (1996) showed glycosides: Oncoba welwitschii, Camptostylus that Pan troglodytes can drink bitter solutions mannii and Dasylepis cfr. seretii. The two species containing almost 150 micromoles of quinine, a of the Achariaceae family contain both alkaloids concentration four times higher than the median and cyanogenic glycosides. Indeed, Bouquet threshold measured for humans. Furthermore, (1972) confirmed that all Congolese species of the Nishida et al. (2000) found that chimpanzees are Salicaceae family contain cyanogenic glycosides. able to tolerate food species that to humans taste However, according to Conn (1979), cyanogenesis unpleasant, bitter, or astringent, as well as others appears to be limited only to certain families such that are neutral or sweet. But, in general, a diverse as the Leguminosae, Rosaceae, Euphorbiaceae and

Table 3. The number of species consumed by humans and bonobos that contain alkaloids or not. Species Hs Pp Species with 7 (50%) 20 (34%) Species without 7 (50%) 39 (66%) Sample size 14 59 Alkaloids and Cyanogenic Glycosides in Bonobos / 19 Table 4. Number of species consumed by humans and bonobos, with respect to cyanogenic glycosides content.

Species Hs Pp Species with 0 (0%) 3 (5%) Species without 14 (100%) 56 (94%) Species size 0 3

Passifloraceae. Nevertheless, our study reconfirms pour la Conservation de la Nature (ICCN) for the work of Bouquet (1972) that some species in allowing access into the study site and accepting us as the Achariaceae and Salicaceae families contain researchers. Our gratitude also goes to the villagers cyanogenic glycosides. of Lompole, particularly Booto Lambert and Etike Rothman et al. (2006) analyzed the chemical Joseph Mara for contributing to the data collection. content of a total of 127 food plant parts, representing We would like to acknowledge the international 84 plant species, eaten by two groups of mountain staff of Luikotale, who have contributed also to gorillas, from Bwindi Forest National Park, Uganda, data collection during the habituation of bonobos but found only two foods that contained cyanogenic during our study period: Cintia Garai and Andrew glycosides. Fowler. We give special thanks to Barbara Decrosac Thus, the small proportion (5%) found among who agreed to complete our analysis in the field and the fruits consumed by bonobos at LuiKotale is in to our colleague Musuyu Desiré for his advice. We line with what has been reported elsewhere, e.g., the would like to thank also Lys Alcayna Stevens who results found by Bouquet and Fournet (1975) in the quickly agreed to read this work. Lastly, we thank Jo study of the Congolese flora and the investigation Thompson for editorial assistance and our reviewers by Rothman et al. (2006). Similarly, independent Michael A. Huffman and Alex Chepstow-Lusty for findings show that red colobus monkeys in Kibale their insightful suggestions. National Park, Uganda also avoid plants with high levels of secondary compounds (Chapman & Chapman 2002). LITERATURE CITED In summary, the results provided here show that none of the ingested fruit species showed high Abiodun, O. A., A.A. Amanyunose, O.O. Olosunde concentrations of either alkaloids or cyanogenic & J.A. Adegbite. 2014. Sugar and alkaloid profiles glycosides. Using semi-quantitative analyses of of serendipity berry. Food Science and Quality bonobo and local human fruit foods, we have Management 28: 83-89. provided an overview into the presence/absence of Alm, U., B. Birgersson & O. Leimar. 2000. The effect two major secondary metabolite groups in the diet. of food quality and relative abundance on food However, future studies should quantify and qualify choice in fallow deer. Animal Behaviour 64: 439- these compounds to assess their importance for the 435. health of bonobos and humans. This investigation Badrian, N., A. Badrian & R. Susman. 1981. has contributed to our understanding the food Preliminary observations on the feeding behavior choices in bonobos and the Nkundo people, as of Pan paniscus in the Lomako Forest of Central they relate to the presence or absence of alkaloids Zaire. Primates 22(2): 173-181. and cyanogenic glucosides. Furthermore, we have Beaune, D., F. Bretagnolle, L. Bollache, G. Hohmann, contributed valuable data about the presence of M. Surbeck & B. Fruth. 2013. Seed dispersal secondary compounds in the fruits of certain species strategies and the threat of defaunation in a from the African rainforest. Congo forest. Biodiversity and Conservation 22: 225-238 Bernhoft, A. 2008. Bioactive compounds in ACKNOWLEDGMENTS plants: benefits and risks for man and animals. Proceedings from a Symposium held at The We thank the Max Planck Institute for all the Norwegian Academy of Science and Letters, logistics and financial support for conducting this Oslo, 13 – 14. P253. research. We also acknowledge the Institut Congolais Boesch, C., G. Hohmann & L. Marchant. 2002. 20 / Bondjengo et al.

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Primate Communities Along a Protected Area Border: A Two-site Comparison of Abundance and Hunting Response in Bioko, Equatorial Guinea

Daniel L. Forrest1,2,3, Fermin Muatiche3, Cirilo Riaco3, Mary Katherine Gonder2,3,4, and Drew T. Cronin3,5

1Department of Ecology, Evolution, and Natural Resources, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA; 2Department of Biodiversity, Earth and Environmental Science, Drexel University, Philadelphia, PA, USA; 3Bioko Biodiversity Protection Program, Malabo, Bioko Norte, Equatorial Guinea; 4Department of Biology, Drexel University, Philadelphia, PA, USA; 5SMART Partnership, Wildlife Conservation Society, Bronx, NY, USA

Abstract: Bioko Island, Equatorial Guinea is home to seven diurnal primate taxa, threatened with extinction largely due to high rates of illegal bushmeat hunting. The Gran Caldera Scientific Reserve (GCSR), one of two protected areas on Bioko, is the only remaining site where all seven taxa can be found. Historically, much of the wildlife in the GCSR has been passively protected due to its isolation, but a lack of effective law enforcement has allowed hunting to proliferate, and recent road and infrastructure development threatens more hunting in the future. Many calls have been made for the development of a comprehensive management plan to effectively protect the GCSR, but data are needed to understand the dynamics of the varying human-wildlife systems along its borders to develop well-informed and cost-effective management strategies. This study investigated the abundance and species richness of primates along the GCSR border near the village of Moka over four years (2011-2014), and compared results to those of a previous study near a similar GCSR-border village, Belebu. Although we found considerable inter-annual variation in the relative abundance of primates at Moka, the overall relative abundance there was significantly higher than at Belebu. We attribute this primarily to the higher observed hunting intensity at Belebu, differences in historical hunting patterns and accessibility, and the presence of a long-term research site and activities at Moka, which may deter hunters in the area. Further research is needed to provide greater resolution on complementary factors influencing abundance and distribution patterns. However, our results highlight the persistence of a notable primate community near Moka and emphasize the importance of understanding dynamics along protected area borders when planning for conservations. Relatively similar sites may require different approaches for effective management.

Key words: Bioko, hunting, bushmeat, surveys, protected areas

INTRODUCTION

Bushmeat, or the meat of wildlife from forests, population growth, increased use of firearms, has long been a dietary staple of people in tropical and greater accessibility to remote forests has led African forests (Asibey 1977; Afolayan 1980; Fa et to the commercialization of the bushmeat trade al. 2002; Robinson & Bennett 2004). While wild (Abernethy et al. 2013; Albrechtsen et al. 2007; Fa harvest can be a sustainable and accessible protein- et al. 2005; Ziegler et al. 2016). The rapid growth of source (Albrechtsen et al. 2007), accelerating human the bushmeat trade now threatens many taxa with

Correspondence to: Daniel L. Forrest, Rutgers, The State University of New Jersey, New Brunswick, NJ, USA; Email: daniel.l.forrest@ gmail.com. 24 / Forrest et al.

Figure 1. (A) A map of Bioko Island, Equatorial Guinea, including the study sites, major towns and roads, and Bioko’s two protected areas: Pico Basilé National Park (PBNP), and the Gran Caldera Scientific Reserve (GCSR). Ureca, the only village within the GCSR is also shown. (B) A magnification of the Moka study area and the survey transects used to assess primate abundance and hunting pressure.

extinction (Oates et al. 2004). In central Africa, extinction (IUCN 2016). The primary threat to these hunting is one of the leading causes of decline of species is bushmeat hunting to supply the capital city most larger-bodied mammals, especially primates of Malabo, where there is a large, thriving bushmeat and ungulates (Oates et al. 2004). Diurnal primates market (Fa et al. 2000; Albrechtsen et al. 2007; are among the most heavily hunted taxonomic Cronin et al. 2015). Over 100,000 kg of bushmeat groups in the region, comprising approximately 10- are consumed annually on Bioko alone, according to 20% of carcasses recorded in market studies (Fa et al. several estimates (Fa et al. 2000; Albrechtsen et al. 2000, 2006; Cronin et al. 2015). Extinction or decline 2007), of which primates comprise approximately of primate species can lead to negative cascading 20% of all carcasses (Cronin et al. 2015). While ecological effects in their communities (Wright et al. the causes of decline in diurnal primates on Bioko 2000, 2007; Abernethy et al. 2013, Effiomet al. 2013). are well established, government led conservation Many primates have a primarily frugivorous diet, efforts and management plans on Bioko have yet to and thus provide crucial ecosystem maintenance lead to any profound successes, despite a presidential functions, such as seed dispersal (Chapman & decree that bans primate hunting (Republic of Onderdonk 1998; Lambert 2001; Poulsen et al. Equatorial Guinea 2007). Approximately 40% of 2001, 2002). Tree diversity in hunted forests is lower the island falls within the borders of two protected than in non-hunted forests, and their composition areas, giving Bioko great potential for conservation. is significantly different from non-hunted forests, The protected areas, however, have done little to largely due to the absence of large-bodied frugivores impede hunting, as protected area borders are not (e.g., primates) (Sork 1985; Chapman & Chapman well-marked, and environmental legislation is not 1996; Chapman & Onderdonk 1998; Effiomet al. strongly enforced (Colell et al. 1994; Cronin et al. 2013) . 2010; 2016; Grande-Vega et al. 2013, 2016). Over Bioko Island, Equatorial Guinea (Figure 1) is time, the threat to primates on Bioko has continued home to numerous endemics, namely, six diurnal to increase, due to an increase in hunting and primate subspecies, and one endemic primate demand for bushmeat (Butynski & Koster 1994; Fa species (Table 1), all of which are threatened with 2000; Hearn et al. 2006; Cronin et al. 2010, 2015). Primate Communities Along a Protected Area on Bioko Island / 25 Table 1. Diurnal primate taxa present on Bioko Island, Equatorial Guinea and their IUCN Red List threatened category (IUCN 2016). Table adapted from Cronin et al. (2016).

Red List category Vernacular name Binomial name Species Subspecies Bioko black colobusa Colobus satanas satanas Vulnerable Endangered Pennant’s red colobusa,b Procolobus pennantii pennantii Critically Endangered Endangered Bioko drilla Mandrillus leucophaeus poensis Endangered Endangered Bioko Preuss’s monkeya,c Allochrocebus preussi insularis Endangered Endangered Bioko red-eared monkeya Cercopithecus erythrotis erythrotis Vulnerable Vulnerable Crowned monkey Cercopithecus pogonias pogonias Least Concern Vulnerable Bioko putty-nosed monkey Cercopithecus nictitans martini Least Concern Vulnerable aRecognized by Grubb et al. (2003) as subspecies endemic to Bioko. bRecognized by Groves (2007) as a species (Piliocolobus pennantii) endemic to Bioko. cAllocated to the genus Allochrocebus following Grubb (2006).

Several previous surveys (Schaaf et al. 1990; richness, and gun hunting between the two sites; Butynski & Koster 1994; Hearn et al. 2004; Cronin and 4) provide recommendations to improve the et al. 2013) focused primarily on remote areas of efforts to conserve Bioko’s primate populations. the island, and especially on areas within the GCSR. Primate abundance and hunting levels in areas METHODS bordering the reserve, however, have gone relatively understudied, with the exception of a brief study at Study Area Moka by Colell et al. (1994), undergraduate surveys Bioko Island, Equatorial Guinea (2017 km2), a as part of annual field courses at the Moka Wildlife volcanic, continental island, located 37 km off of Center (MWC) over the past decade, and surveys the coast of Cameroon (Figure 1), is a biodiversity conducted by Cronin et al. (2016) at Belebu, another hotspot and a key site for the conservation of town bordering the GCSR. Colell et al. (1994) African primate diversity (Oates 1996; Myers et al. studied hunting in the Moka area by both surveying 2000; Oates et al. 2004). Bioko spans an elevational hunters and conducting hunter follows in 1992, range from 0-3,011 m asl, and a north-south finding that hunters more commonly used traps precipitation gradient from 2,000 mm/year in the than guns, and that hunters gradually increased north to over 10,000 mm/year in the south (Font the length and extent of their hunting trips over Tullot 1951; de Terán 1962). Two protected areas, the course of their study. At Belebu, Cronin et al. Pico Basilé National Park (330 km2; PBNP) and the (2016) encountered dramatically fewer primates Gran Caldera Scientific Reserve (510 km2; GCSR), and more hunting signs than at other more remote encompass approximately 40% of the island’s land sites, which was attributed to its long-term history of area. The GCSR encompasses the southern 25% of organized bushmeat hunting and transport and its the island, which has far less human development close proximity to Luba, Bioko’s second largest city. and impact than the northern end of the island. This study makes use of student survey data Aside from the village of Ureka (< 80 individuals), from 2011-2014 at Moka, and incorporates data no permanent human settlements exist within the collected by Cronin et al. (2016) at Belebu to GCSR. compare differences in primate abundance and This study took place near the village of Moka, hunting intensity between the two sites to inform located along the northeastern border of the GCSR conservation planning. We sought to: 1) describe at an elevation of 1,400 m asl on the eastern slope primate abundance and species richness at Moka; of Pico Biao. Moka is largely surrounded by an 2) quantify the hunting intensity at the site, and, if agricultural mosaic which transitions into montane possible, its impact on Moka’s primate community forest away from the village. Annual precipitation (e.g., decreased abundance or reduced species at Moka is estimated to be 3,700 mm/year, with richness); 3) compare data from Moka and Belebu to approximately 131 mm falling on average each evaluate differences in primate abundance, species November (when the surveys were conducted) 26 / Forrest et al.

(Font Tullot 1951). Moka is a key agricultural site detection of hunted primates in steep terrain with on Bioko, predominantly inhabited by the Bubi dense vegetation (Whitesides et al. 1988). Upon each ethnic group, with an established history of hunting primate encounter, the following data were recorded: (Colell et al. 1994), although Bubis have restricted (1) time of observation (2) type of encounter (visual/ gun access (Butynski & Koster 1994; Grande-Vega et auditory), (3) location (GPS coordinates), (4) al. 2013). In recent years, agricultural activities have elevation, (5) species, (6) number of individuals, (7) expanded greatly around the town (D.T. Cronin, sex of individuals, (8) vocalization type, (9) height in pers. obs.), despite its location on the border of the trees/canopy (Schaaf et al. 1990; Butynski & Koster GCSR. 1994; Cronin et al. 2013). Any encounter within 50 m of the previous encounter was considered part Data Collection of the same group (same species) or a polyspecific Surveys were conducted from 2011 to 2014, association, and was not recorded separately (Oates between 04 November and 26 November of each et al. 1990). year along established multi-use footpaths near the To quantify hunting pressure, any sign of Moka Wildlife Center (MWC) (a facility operated hunting, such as shotgun shells, traps, batteries, by the Bioko Biodiversity Protection Program, an hunting camps, carcasses, and gun shots were tallied academic partnership between Drexel University categorically, and summed (Linder 2008; Cronin and the National University of Equatorial Guinea). et al. 2013). Each individual sign was treated as a Reconnaissance (“recce”) walk methodology separate encounter, and no signs were collected to (Walsh & White 1999) was used following Cronin avoid detection, hostility from hunters, and hunter et al. (2013, 2016) to travel more quickly, cover interference in data quality (picking up shotgun more ground, avoid unnecessarily cutting trails/ shells, batteries, etc.) (Linder & Oates 2011; Cronin destroying habitat, and to increase the likelihood of et al. 2013, 2016). primate encounters. In recce sampling, two to four researchers walk along the path of least resistance Data Analysis through the forest, following natural geographic Sighting frequencies were calculated as the features, and existing human and game trails to number of social groups, including solitary maintain a general compass bearing, and cutting primates, sighted per kilometer of transect walked. vegetation only when necessary (Walsh & White We did not analyze the data to produce sighting 1999). Three recce transects were surveyed, San frequencies of individuals, as estimating group size Joaquin, Balacha Sur, and Balacha Norte, all of of primate groups in hunted forests is particularly which were approximately 4 km in length. Transects unreliable (Ferrari et al. 2010), and previous primate were measured and marked by researchers prior to surveys conducted on Bioko calculated group, not beginning surveys using either a hip chain or 50 m individual, encounter rates (Butynski & Koster 1994; tape measure. Surveys were conducted at a speed Cronin et al. 2010, 2013, 2016). Sighting frequency of approximately 1.15 km hr-1, similar to the 1 km (groups/km) is a measure of relative density, used hr-1 rate established by Whitesides et al. (1988), in place of absolute density measurements (groups/ and used in previous surveys on Bioko (Butynski km2) due to small sample sizes of each species and & Koster 1994; Cronin et al. 2013, 2016). One inherent difficulties in detecting hunted primates transect was surveyed each day, twice per day (once in dense forest (Fashing & Cords 2000; Marshall in each direction), from approximately 0700–1100, et al. 2008). Sighting frequencies and hunting and 1400–1800, unless faced with an extenuating sign encounter rates were compared to surveys circumstance (e.g., heavy rain). We alternated conducted by Cronin et al. (2016) at Belebu, to transects each day, in order to walk each transect compare abundance and hunting patterns between an approximately equal number of times within our the two sites. study period. Primate sighting frequencies were compared All survey data were collected by students among survey sites and years using the non- trained by DTC (including DLF) and FM, who parametric test (Wilcoxon–Mann–Whitney test was present for all surveys, and recorded using a (Linder & Oates 2011; Cronin et al. 2013, 2016). The customized Cybertracker (v3.248) data collection alpha level was set at 0.05 for all statistical tests and program (Steventon 2002). Primate groups were adjusted using Bonferroni correction procedures. counted to estimate relative primate abundance All statistical analyses were conducted using R following Schaaf et al. (1990) and Cronin et al. (v3.2.2; R Core Team 2015). (2013, 2016) due to difficulties associated with Primate Communities Along a Protected Area on Bioko Island / 27 RESULTS In all four years, C. erythrotis was the most frequently sighted primate (Table 2). In 2011, the only Sighting frequency and temporal change in Moka other primate species sighted was M. leucophaeus The three transects were surveyed a total of (Table 2). In 2012, the only other sighted primate 57 times (San Joaquin: 24 surveys - 81.28 km; species was A. preussi (Table 2). In 2013, three Balacha Norte: 13 surveys - 46.66 km; Balacha Sur: species were sighted at relatively low frequencies (M. 20 surveys - 70.26 km), resulting in a total survey leucophaeus, A. preussi, and C. nictitans) (Table 2). In effort of 198.2 km and 151 total encounters, for an 2014, three species were sighted, again, at relatively average encounter rate of 0.75 groups/km. Visual low frequencies (M. leucophaeus, C. nictitans, and C. identifications were confirmed for 119 encounters, pogonias) (Table 2; Figure 2). resulting in a sighting frequency of 0.56 groups/km. Five of the seven diurnal primate species occurring Species richness in Moka on Bioko were encountered in the Moka area: Species richness (i.e., the number of species Cercopithecus erythrotis, C. pogonias, C. nictitans, encountered) varied by year, and by transect. More Allochrocebus preussi, and Mandrillus leucophaeus. species were observed in 2013 and 2014 (4 species) The two colobine species present on Bioko, than in 2011 and 2012 (2 species), but within years, Colobus satanas and Procolobus pennantii were not the composition of species encountered varied encountered. among transects (Figure 2). The most species were Overall sighting frequencies of all primate observed on Balacha Sur in 2011 (2 species), 2013 (3 species each year in Moka were compared to every species), and 2014 (3 species) (Figure 2). In 2012, the other year using the Wilcoxon–Mann–Whitney test. most species were sighted on San Joaquin (2 species) Sighting frequency was significantly higher in 2013 (Figure 2). Across all years, the fewest species were (0.82 groups/km) and 2014 (0.72 groups/km) than sighted on Balacha Norte, as only C. erythrotis was in 2011 (0.45 groups/km), and significantly higher sighted on this trail (Figure 2). in 2013 (0.72 groups/km) than in 2012 (0.37 groups/ km) (Wilcoxon–Mann–Whitney: 2011-2013: W Hunting in Moka = 101.5, p < 0.005; 2011-2014: W = 157, p < 0.01; Both gun hunting and trapping signs were 2012-2013: W = 61.5, p < 0.05) (Table 2). encountered on all trails each year, with some

Figure 2. The percentage of each species sighted per transect per year during surveys in Moka from 2011 – 2014. 28 / Forrest et al. 5 0 0 6 0 % 53 35 0 0 0 S.F. Belebu* (grps/km) 0.11 (0.045) 0.18 (0.061) 0.047 (0.023) 0.007 (0.007) 0.016 (0.016) 9 6 1 0 1 0 0 N 17 5 0 3 0 3 % 78 11 0 0 2014 S.F. (grps/km) 0.57 (0.16) 0.72 (0.21) 0.08 (0.024) 0.042 (0.012) 0.021 (0.006) 0.021 (0.006) 2 0 1 0 1 4 N 29 37 ; Apr - ; Apr nictitans ; Cni - Cercopithecus pogonias - Cercopithecus ; Cpo 0 7 0 % 76 10 3.5 3.5 0 0 S.F. 2013 (grps/km) 0.60 (0.19) 0.82 (0.26) 0.026 (0.008) 0.026 0.047 (0.015) 0.047 0.023 (0.007) 0.023 0.085 (0.027) 0.085 1 0 2 1 0 3 ; Cer - Cercopithecus erythrotis N 22 29 Moka 0 0 0 0 5 % 76 19 0 0 0 0 2012 S.F. (grps/km) 0.31 (0.078) 0.39 (0.098) 0.085 (0.021) 0.016 (0.004) Piliocolobus pennantii ; Ppe - Piliocolobus 4 0 0 0 0 1 N 16 21 0 0 3 0 0 3 % 94 ; Csa - Colobus satanas 0 0 0 0 S.F. 2011 0.45 (.11) (grps/km) 0.43 (0.10) 0.14 (0.003) 0.014 (0.003) . 0 0 0 1 0 1 N 30 32 a

Species Cer Apr Cpo Cni Mle Csa Unk Total Mandrillus leucophaeusMle - Mandrillus a Allochrocebus preussi Table 2. Primate sighting data for each species from 2011 to 2014 (N = number of groups sighted, S.F. = sighting frequency (groups/km), % = % frequency(groups/km), sighting = S.F. sighted, groups of number 2014 (N = 2011 to species each from for data sighting 2. Primate Table all sightings). of percentage Primate Communities Along a Protected Area on Bioko Island / 29 variation by trail and year (Table 3). Hunting signs become a key portion of the bushmeat market in largely comprised of shotgun shells, followed by Malabo, the capital of Bioko. traps, batteries, and miscellaneous hunting signs Of Bioko’s seven diurnal primate species, our (e.g., carcasses, entrails). The highest gun sign surveys revealed the presence of five species persisting encounter rate occurred in 2013, with a considerable at Moka, and four at Belebu (Cronin et al. 2016). decrease in 2014 (Table 3). Snares were encountered While species composition and abundance in our an average of 4.07 times more frequently in 2011 and surveys varied from year to year, the regularity with 2012 than in 2013 and 2014 (Table 3). which primates were encountered at Moka suggests that five species continue to persist in the area, and Differential species composition and sighting the comparably sparse encounters at Belebu suggests frequency per site the contrary. C. erythrotis was the most commonly While species richness was comparable at sighted species at Moka and Belebu, in accordance both sites (Belebu, 4 species; Moka, 5 species), the with previous studies on Bioko (Butynski & Koster overall primate sighting frequency was significantly 1994; Cronin et al. 2016), while the other five species higher at Moka (0.56 groups/km) than Belebu (0.18 [A. preussi (Moka, Belebu), C. satanas (Belebu), C. groups/km) (Wilcoxon–Mann–Whitney: W = pogonias (Moka, Belebu), C. nictitans (Moka), and 534, p <0.00001) (Figure 3). All individual species M. leuocophaeus (Moka)] were encountered at a sighting frequencies were higher at Moka, except much lower frequency. P. pennantii and C. satanas for C. satanas, of which no sightings were made at were not encountered in the Moka area, implying Moka, while a single sighting occurred at Belebu extremely low densities, as in the case of C. satanas, resulting in a sighting frequency of 0.016 groups/ or extirpation in the areas surrounding Moka, as has km. Two species were sighted at Moka that were not been suggested for P. pennantii (Cronin et al. 2013, sighted at Belebu (M. leucophaeus, 0.017 groups/km; 2016, 2017). C. satanas has recently been observed C. nictitans 0.009 groups/km). opportunistically near Moka along the rim of the Biao crater (1 individual; D. Montgomery, pers. obs. Differential response to gun hunting per site 2013), and on the northwest flank of Pico Biao (1 Belebu (5.56 signs/km) had a higher overall individual: D. Venditti, pers. obs. 2016; 2 groups: hunting sign presence than Moka (1.22 signs/km), a D. L. Forrest, pers. obs. 2017). Colell et al. (1994) higher gun sign encounter rate (Belebu, 2.89 signs/ described a single P. pennantii carcass, reported km; Moka, 0.83 signs/km), and a higher trap sign to be taken near Pico Biao in 1992; however, P. encounter rate (Belebu, 2.66 signs/km; Moka, 0.40 pennantii is now believed to be restricted to a single signs/km). Overall sighting frequency of primates small population in the southwestern corner of was higher in Moka, where fewer hunting signs were Bioko (Cronin et al. 2016, 2017). Colobus monkeys encountered. are largely understood to be highly sensitive to hunting, due to their large body size, their sluggish DISCUSSION and conspicuous manner of movement, and low level of visual alertness (Oates 1996). On Bioko, While several other studies have documented Cronin et al. (2016) found that both C. satanas primate abundance and hunting pressure on Bioko and P. pennantii are the most vulnerable species to Island and Cronin et al. (2015) assessed the impact hunting. Examples with other colobine species from of gun hunting on Bioko’s diurnal primate species, mainland Equatorial Guinea (Kümpel et al. 2008), this is the first study to highlight and assess relative Uganda (Struhsaker 1999), Tanzania (Marshall abundance of primates and hunting pressure near 2007), and a comprehensive analysis of all red two semi-urbanized towns on Bioko. Prior to this colobus species (Struhsaker 2005) substantiate this study, no primary data in the Moka area on Bioko claim. The high vulnerability to hunting of both was published. Overall primate sighting frequency colobine species on Bioko likely account for their was higher in Moka, where fewer hunting signs absence at our study site. were encountered; however, differences in elevation Despite the higher sighting frequency at Moka, (Cronin et al. 2016), distance from roads (Cronin et the primate communities of both Moka and Belebu al. 2017) and habitat may also play a role, and require are reflective of hunted forests on Bioko (Croninet further research. A prominent hunting presence al. 2016) and the Congo Basin (Linder & Oates 2011; was revealed at both of the census locations in this Rovero et al. 2012). As in other recent surveys on study (Belebu, 5.56 signs/km; Moka, 1.22 signs/km). the island (Cronin et al. 2013, 2016), the majority According to Cronin et al. (2015), primates have of sightings consisted of smaller bodied primates 30 / Forrest et al.

Table 3. Hunting sign totals and encounter rates per km during surveys at Moka (2011 – 2014; this study) and Belebu (2011-2012; Cronin et al. 2016).

Moka Hunting Sign Type Belebu 2011 2012 2013 2014

Gun Hunting Signs Balacha Norte 5 16 24 9 - Balacha Sur 22 18 19 8 - San Joaquin 11 17 14 6 - All Trails 38 51 57 23 354 Trap Hunting Signs Balacha Norte 0 24 0 5 - Balacha Sur 18 10 3 4 - San Joaquin 15 0 0 0 - All Trail 33 34 3 9 284 Total Hunting Signs Balacha Norte 5 40 24 14 - Balacha Sur 40 28 22 12 - San Joaquin 26 17 14 6 - All Trails 71 85 60 32 638 Gun Sign E. R. (km-1) Balacha Norte 0.69 1.13 2.36 0.45 - Balacha Sur 1.07 1.05 1.64 0.43 - San Joaquin 0.30 0.77 1.46 0.52 - All Trails 0.59 0.96 1.64 0.46 2.89 Trap Sign E. R. (km-1) Balacha Norte 0.00 1.70 0.20 0.25 - Balacha Sur 0.40 0.58 1.57 0.22 - San Joaquin 0.88 0.00 0.00 0.00 - All Trails 0.51 0.64 0.09 0.18 2.66 Overall Hunting Sign E.R. (km-1) Balacha Norte 0.69 2.83 2.56 0.70 - Balacha Sur 1.95 1.64 1.64 0.65 - San Joaquin 0.97 0.77 1.46 0.52 - All Trails 1.25 1.60 1.72 0.64 5.56 Primate Communities Along a Protected Area on Bioko Island / 31

Figure 3. Comparison of primate sighting frequencies at Belebu and Moka. Notches indicate standard deviations from the mean sighting frequency values.

(e.g., C. erythrotis), while larger, more conspicuous opportunistically encountered or absent in our species were encountered at either low rates (e.g., surveys. The high proportion ofC. erythrotis M. leucophaeus, C. satanas), or not at all (e.g., P. encountered during our surveys relative to larger- pennantii). C. erythrotis is the smallest diurnal bodied primate taxa lends further support to Cronin primate occurring on Bioko (Butynski et al. 2009), et al.’s (2016) suggestion that C. erythrotis may and is most resilient to hunting pressure (Cronin compensate for the loss of other diurnal primate et al. 2016). In contrast, the larger-bodied species, taxa on Bioko. Other recent studies in Cameroon M. leucophaeus, C. satanas, and P. pennantii, are (Linder & Oates 2011) and Tanzania (Rovero et al. all vulnerable to hunting pressure and, thus, are 2012) have shown similar trends with respect to the expected to be encountered at lower frequencies primate community composition in highly-hunted (Cronin et al. 2016). P. pennantii and C. satanas, versus lesser-hunted forests (fewer larger-bodied respectively, had the highest and second-highest primates, chiefly colobines, and equal or greater vulnerability indices of all of Bioko’s primates smaller-bodied primates, chiefly cercopithecines). (Cronin et al. 2016) and, accordingly, were only Both Linder & Oates (2011) and Cronin et al. (2016) 32 / Forrest et al.

propose that this phenomenon could be attributed (lowland forest) indicate that hunting pressure likely to competitive release, which may also be the case has the dominant impact on primate abundance. in our study. Other environmental factors may also play a role Habitat degradation is often cited as a leading in the species richness and abundance at each site, cause of primate population decline in west and and further research is necessary to investigate the central Africa (Oates 1996; Rovero et al. 2012; impact of these ecological differences. Barelli et al. 2015) and may play an important role in The results from these two towns on the primate community dynamics at both of our study boundary of the GCSR support the persistence sites. The abandonment of former pastureland in of a number of significant issues: (1) the borders Moka in the early 1990s allowed secondary forest of the GCSR are permeable to hunters; (2) the to reclaim some areas of previously lost or degraded legal existence of protected areas on Bioko is not habitat. This potentially led to increased habitat, sufficient to deter hunting, especially of threatened in some areas around Moka (Butynski & Koster primates, which are critically important to the 1994). However, in recent years, there has been maintenance of ecosystem processes; and (3) the considerable habitat loss near both Moka and Belebu, development of management strategies for the concentrated along their primary access roadways GCSR needs to account for site-specific differences (main road to Luba and Malabo, Moka; Luba-Ureka in accessibility, long-term history, hunting patterns, road, Belebu), due to agricultural expansion (D.T. and species assemblages, such as prioritization of the Cronin, D.L. Forrest, pers. obs.). Net habitat gain location of forest patrols, and selective positioning may be insignificant or even negative, as a result, but of bushmeat checkpoints. With the understanding it is also likely that hunting efforts will be, at least of the limitations in implementing a management in the short term, concentrated in areas just beyond strategy for a protected area (limited funding, agricultural expansion and along roads, due to easier personnel, equipment, etc.), it is imperative to accessibility. consider key access points, hunted areas, and the While both the towns of Moka and Belebu are current ecological state of the area. Belebu and Moka positioned along the border of the GCSR, relative are two of only four large towns within 2 km of the primate abundance and hunting sign encounter GCSR, and are the most accessible of the four. By rates differed between the two, likely due to the studying the primate abundance and hunting levels accessibility and land-use history of these towns. in key locations nearing the reserve borders, we Our results indicate a higher hunting presence in can better understand the pathways of entry into Belebu than in Moka, and correspondingly fewer the reserve, level of use in different portions of the primates in Belebu than in Moka. The forest near reserve, and prioritize limited resources. We contend Belebu is more accessible to most hunters, as Belebu that the difference between primate abundance in is only 7.5 km from Luba, Bioko’s second largest Belebu and Moka is due, in large part, to the greater town, on the Luba-Ureka Road, and, as a result, accessibility and history of hunting in Belebu. nearer to Malabo, the largest town and location of With this understanding, the current expansion the main bushmeat market. Belebu also has a long of agriculture at Moka, and the completion of the history of plantation agriculture of both cocoa and new road through the GCSR to Ureka, we reiterate palm, fueling both forest loss and/or conversion, the recommendation made in Cronin et al. (2017) and gun hunting for bushmeat and management that the implementation of a management plan of agricultural pests, e.g., squirrels (Butynski & for the GCSR is of critical importance to the Koster 1994). Small-scale commercial agriculture preservation of its diurnal primate taxa. Included also occurs in Moka, but expansion has occurred in their recommendations were the creation and more recently, and a greater amount of intact implementation of ‘ranger bases’ at primary access forest remains directly surrounding the town (D. T. points to the GCSR and ‘bushmeat checkpoints’ Cronin, D. L. Forrest, pers. obs.). Elevation is often along key transit routes between protected areas. considered an important environmental predictor of Belebu, situated 7.5 km from the entrance to the primate abundance, as higher elevation are typically Luba-Ureka road (Figure 1), is highly accessible to associated with lower densities of primates (Barelli hunters coming from Luba. A checkpoint directly et al. 2015). This holds true on Bioko (Croninet after Belebu along the Luba-Ureka road, coupled al. 2016); however, our high elevation site (Moka) with vehicle searches by INDEFOR-AP, the protected had a higher sighting frequency than the lowland area management authority would limit the amount site (Belebu). Higher sighting frequency on trails of off-take by preventing vehicle access to the reserve. around Moka (montane forest) than Belebu There are two major roadways leading directly to Primate Communities Along a Protected Area on Bioko Island / 33 Moka, and an extensive trail system surrounding the ACKNOWLEDGEMENTS town. While this accessibility, coupled with the Moka Wildlife Center, have provided the infrastructure for We would like to thank the government of ecotourism, and has already lead to some success in Equatorial Guinea and la Universidad Nacional de this area, heavy hunting pressure and subsequent Guinea Ecuatorial, including H.E. Carlos Nse Nsuga decreases in primate abundance near the town and Jose Manuel Esara Echube for permission threatens to reduce, if not eliminate, the ecotourism to conduct this research. We thank the people of market in the town. Increasing the number of eco- Moka, as well as Julia Dagum, Gustavo Mbomio, guard patrols in the area, coupled with military Rachael Disciullo, Piotr Jurgielewicz, Angel Etame support may decrease the hunting presence. Etame, Stephen Dench, Faith Roser, and Erica Both Belebu and Moka were put forth as sites in Tuttle for assistance with data collection. The Bioko Cronin et al.’s (2017) GCSR conservation strategy, Biodiversity Protection Program is supported by and our study highlights the importance of these two the ExxonMobil Foundation and Mobil Equatorial sites to primate conservation along the GCSR border, Guinea, Inc. and as access points for illegal activities. Continued hunting and defaunation in towns like Belebu and LITERATURE CITED Moka along the GCSR border will, in time, lead to hunters moving further into the GCSR, reaching Abernethy, K.A., L. Coad, G. Taylor, M.E. Lee & F. core areas which still maintain high densities of all Maisels. 2013. 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The First Sightings of the Red-Bellied Guenon (Cercopithecus erythrogaster erythrogaster) on the Western Edge of Southwestern Nigeria

Reiko Matsuda Goodwin1, Jacob Oluwafemi Orimaye2, Francis E. Okosodo3, Babafemi G. Ogunjemite3, and Mariano G. Houngbedji4

1Department of Sociology and Anthropology, Fordham University, Bronx, NY, USA; 2Department of Forestry, Wildlife and Fisheries Management, Ekiti State University, Ado-Ekiti, Nigeria; 3Department of Ecotourism and Wildlife Management, Federal University of Technology, Akure, Nigeria; 4Organisation pour le Développement Durable et la Biodiversité, Cotonou, Benin

Abstract: To better understand the status and distribution patterns of threatened anthropoids, we conducted walking surveys and interviews on the western edge of southwestern Nigeria. As we surveyed, we recorded all sightings of the monkeys and evidence of anthropogenic disturbance. We also examined the extent of forest in the southern part of our study area, in particular, Eggua Forest Reserve and Ohumbe Forest Reserve, using Landsat 8 band images. The number of anthropoid species encountered during the surveys varied from zero to four. We sighted C. erythrogaster at Atola community forest (Encounter rate = 0.27 group/km), Royal Forest (private forest) (Encounter rate = 0.08 group/km), and Bola Camp community forest. These are seasonally inundated or riverine forests. The bellies of theC. erythrogaster individuals we saw at the two latter localities indicate that they are C. erythrogaster erythrogaster. No other threatened anthropoids were sighted. At Igboju community forest (part of Eggua FR), where an interviewee stated that C. e. erythrogaster occurs, we only saw mona monkeys (Cercopithecus mona). Bola Camp and adjacent communities, where about 9 km2 of riverine forest still remains and hunting is limited, have a potential to develop a conservation program. Creating corridors to connect Igboju, Royal Forest, and southern forest fragments in Eggua FR for the conservation of C. e. erythrogaster is also recommended. With our new information, the distribution range of C. e. erythrogaster has now been expanded to east of Benin, but it is still uncertain how widespread this subspecies is. The future of this taxon in this region, however, does not look bright considering the levels of hunting, logging, farming, cattle herding, and fire set by cattle herders that we witnessed. Thorough surveys along Yewa River including Igboju, and fragmented forests in two forest reserves are necessary in the near future.

Key words: Nigeria, red-bellied guenon, Nigeria white-throated monkey, conservation, reconnaissance survey, semi-structured interview, community forest, forest reserve

Résume: Dans une visant à mieux comprendre le statut et la répartition des espèces de singes menacés, en se concentrant sur Cercopithecus erythrogaster, nous avons réalisé des randonnées de 49,5 km et des entretiens sur le bord ouest du sud-ouest du Nigeria. Au cours des prospections pédestres, nous avons enregistré toutes les observations et vocalisations de singes et les signes de perturbation anthropique. Nous avons par la suite examiné la superficie de la forêt dans la partie sud de notre zone d’étude, en particulier la Réserve Forestière d’Eggua et la Réserve Forestière d’Ohumbe, sur des images de Landsat 8. Le nombre d’espèces des singe anthropoïde rencontrées lors des prospections pédestres varie de zéro à quatre (moyenne = 1,6). Nous avons observé C. erythrogaster dans la forêt communautaire d’Atola (0,27 groupe/km), dans la Forêt Royale (forêt privée)(0,08 groupe/km) et

Correspondence to: Reiko Matsuda Goodwin, Department of Sociology and Anthropology, Fordham University, Bronx, NY, USA; E-mail: [email protected]. 38 / Matsuda Goodwin et al.

dans la forêt communautaire de Bola Camp. Ce sont des forêts galeries ou saisonnièrement inondées. Les ventres des individus de C. erythrogaster que nous avons vus dans les deux dernières localités indiquent qu’il sagit de C. erythrogaster erythrogaster. Aucun autre anthropoïde menacé n’a été aperçu. Dans la forêt communautaire d’Igboju (partie de la Réserve Forestière d’Eggua), où un interviewé a déclaré que C. e. erythrogaster se trouve, nous avons seulement vu le singe mona (Cercopithecus mona). Bola Camp et ses communautés avoisinantes, où il reste environ 9 km2 de forêt fluviale et où la chasse est limitée, ont un potentiel pour un programme de conservation et d’écotourisme. Créer des couloirs pour relier Igboju, Forêt Royale et les ilôts foretiers fragmentés à la Réserve Forestière d’Eggua pour la conservation de C. e. erythrogaster est également recommandé. Avec nos nouvelles informations, l’aire de distribution de C. e. erythrogaster a maintenant été élargie, mais il reste encore à préciser l’étendue exacte de cette sous-espèce. L’avenir de ce taxon dans cette région, cependant, ne semble pas brillant compte tenu des niveaux de la chasse, l’exploitation forestière, l’élevage, l’élevage du bétail, et le feu allumé par les éleveurs de bétail que nous avons vu. Des études approfondies le long du Fleuve Yewa, y compris Igboju, et d’autres zones forestières fragmentées des deux Réserves Forestières sont nécessaires dans un proche avenir.

INTRODUCTION

The western edge of Southwestern Nigeria low rainfall and lower biodiversity situated between (hereafter “our study area”) in Ogun and Oyo states the Upper Guinean Forests and the Lower Guinean is a transition zone from the moist Lower Guinean Forests in West Africa (Jenik 1994). During the Forest to the drier Dahomey Gap climate (White Pleistocene, large rivers such as the Niger River 1983). The vegetation of this region is a mosaic of in the east and Ouémé in the west did not act as lowland rain forest, riverine forest, swamp forest, effective physical barriers for the distribution of seasonally inundated forest, savanna woodland, and this species (Oates 1988, Harcourt & Wood 2012). thicket (Ern 1988). It is a poorly studied area in regard The presence or absence of one or both subspecies to biodiversity. Nevertheless, it is an area that has of C. erythrogaster in our study area has not been been said to harbor at least eight anthropoid species; examined since Oates (pers. comm. 2014) searched the red-capped mangabey (Cercocebus torquatus); for this species by interviewing communities white-thighed colobus (Colobus vellerosus); olive neighboring Eggua Forest Reserve (FR) in 1992, but colobus (Procolobus verus), which is the smallest the results of interviews were not promising. For colobine; white-throated monkey (Cercopithecus this reason, in 1994 and 1995, Oates (1996) went erythrogaster); mona monkey (Cercopithecus mona); to look for the species’ presence in southern Benin tantalus monkey (Chlorocebus tantalus); patas and discovered the red-bellied guenon in the Lama monkey (Erythrocebus patas); and the olive baboon Forest (44.47 km2, 7.017°-6.857° N, 2.078°-2.217° (Papio anubis). Additionally, the putty-nosed E) (Figure 1). The Nigeria white-throated monkey monkey (Cercopithecus nictitans) may be included. is known to occur east of Lagos in Sapoba, Okomu, The 2008 IUCN Red List categorized the species C. Gilli-Gilli, Udo, Ohosu, and Omo Forest Reserves, erythrogaster as Vulnerable (Oates et al. 2008a) while probably a few other forests, and in the Niger Delta the red-bellied subspecies, the red-bellied guenon (Oates 1985, 2011a; Grubb et al. 1999). The red- (C. e. erythrogaster) was categorized as Endangered bellied guenon has been known to occur only in (EN) (Oates & Butynski 2008a) and the gray-bellied eastern Togo and southern Benin. In Togo, it occurs subspecies, the Nigeria white-throated monkey (C. in Togodo National Park (1.333° - 1.667° E, 6.666° - e. pococki) as Vulnerable (VU) (Oates & Butynski 6.833° N), and Godjin-Godjè sacred forest (1.520° 2008b). Because C. erythrogaster, C. torquatus, C. E, 6.719° N) (Matsuda Goodwin et al. 2017a; G. vellerosus, and P. verus are all threatened species Segniagbeto pers. comm. 2016). In Benin, it occurs (Oates et al. 2008a, b, c, d) they are referred to as at several localities in the south (e.g., Lama, Lokoli, the “threatened anthropoids of the region” in this Bonou, Togbota) (Matsuda Goodwin 2007; Nobimè paper. The status of these anthropoids in this region et al. 2011; Matsuda Goodwin et al. 2017a). It is not has been largely unknown, although some anecdotes known whether the distribution ranges of the two and reports suggested that at least some of these subspecies have been allopatric or parapatric with species occur (Ogunjemite 2014). a potential zone of hybridization somewhere in our This report focuses on C. erythrogaster, which study area. Without precise knowledge of the two is one of the anthropoid species present in the subspecies’ distribution limits, the Primates of West Dahomey Gap. The Dahomey Gap is the area of Africa (PWA) (Oates 2011a) mapped the eastern First Sightings of the Red-Bellied Guenon in Nigeria / 39

Figure 1. Study localities in the western edge of Southwestern Nigeria. Where both surveys and interviews were conducted, only the survey localities are shown. Iwoye is located at the northen edge of Imeko FR along Okparo River. The Royal Forest, Igboju (Part of Eggua FR), Odoafanla, Ajileté, Bola Camp are all along or near the downstream of Yewa River. Atola and Ibese are east of Yewa River. Ibeku is a town, but because of the proximity to Ohumbe FR, an interview was conducted. The Old Oyo NP is well drained by Ogun, Owu, Owe Rivers and their tributaries. limit of C. e. erythrogaster’s range as discontinuous low, C. erythrogaster can even inhabit areas that have from the western edge of the range of C. e. pococki, been somewhat disturbed and modified by human while the 2008 IUCN Red List mapped the limit activities (Matsuda Goodwin, pers. obs., Oates along the border of Benin and Nigeria (Oates et al. 2011a). 2008a). To obtain data and local knowledge regarding Both subspecies of C. erythrogaster are known the status and the distribution patterns of the to inhabit a variety of lowland habitats; rain threatened anthropoids of the region, we conducted forest, semideciduous forest, seasonally inundated reconnaissance surveys and semi-structured semideciduous forest, riverine forest, and swamp interviews. We then examined the current extent of forest. In particular, C. e. erythrogaster often is forests in our study area using a Landsat 8 composite found in riverine and swamp forest (Oates 1985, image taken during the major dry season. Nobimé et al. 2009). As long as hunting pressure is We sighted C. erythrogaster at three new localities 40 / Matsuda Goodwin et al.

in this region, but we observed no other threatened inside the surveyed forests to obtain complimentary monkey taxa. We discuss the significance of our information regarding the presence or absence of observations, revise distribution range maps of C. e. anthropoid species (Bernard 2006; Kühl 2008). The erythrogaster and C. e. pococki, make conservation location of each interview was georeferenced. We did recommendations, and address some factors that not conduct interviews at the Royal Forest in Eggua, should be carefully considered when conducting a small private forest belonging to the Onigua (king) semi-structured interviews. of Eggua, HRM Oba Adeleye Dosunmu. The Onigua has been protecting the forest and planting trees such METHODS as teak since 1991, but natural forest comprises less than one third of the forest. Hunting is prohibited, Following initial scouting (i.e., visiting but there was no one willing to talk with us. We were communities to conduct informal interviews) in our careful in the manner we conducted the interviews; study area on January 5 - 10, 2015, we selected eight what questions to ask and in what order (Kühl localities to conduct reconnaissance surveys (Figure 2008; Meijaard et al. 2011). The interviews were 1). Old Oyo National Park (OONP) is outside the conducted one hunter at a time. Even when other distribution range of C. erythrogaster, but because we villagers surrounded an interviewee, we asked them were also searching for C. vellerosus, which Happold not to intervene by asking questions, commenting, (1987) had reported occurred there more than 25 or providing an answer while an interview was being years ago, it was included in our study localities. conducted. Because we wanted to hear his own Iwoye riverine forest at the intersection of Imeko FR opinion not influenced by others, we had explained and Okpara FR was also surveyed in our search for this protocol to each interviewee before we began. C. vellerosus. At each survey locality, we noted signs However, when multiple villagers were interviewed, of human modification and five to ten commonly second and later interviewees had already heard occurring tree species we observed as a rapid the answers given by previous interviewees. This measure of describing the habitat characteristics represents a potential bias regarding the answers (Table 1). given by later interviewees that we could not avoid. At each survey locality, we walked slowly at We asked them to provide the names of different 1-1.5 km/hr on bush paths or hunter paths, noting monkeys, to describe various body parts of each the mammalian species we encountered, along monkey, when they had last seen the monkeys, and with the time, GPS coordinates, and the mode of to imitate the calls of each monkey. We used images detection (heard or seen) (White & Edwards 2000). of the anthropoids of the region from PWA or PWA As much as possible, when an animal was sighted pocket guide (Oates 2011a, 2011b) only when we felt in a tree, we recorded the height (HT) of the tree, the use of images would clarify some ambiguities. HT of the individual from the ground, the sighting Our experience was that small color images of the distance, and the number of individuals seen. Each monkeys confused many hunters in rural areas who survey was 0.3 - 3.74 km in length and the paths were not used to seeing them in two-dimensional were approximately linear. We obtained presence space. We determined whether the interviewees’ or absence information from the recce surveys answers provided credible local knowledge by and group encounter rates (R) (R = N groups finding out how many years the interviewees have sighted/distance walked). We reported encounter hunted in the forest and by also comparing what rates where we walked ≥ 1 km. During our foot we know about the names, pelage patterns, activity surveys, we tried to record vocalizations of the levels, and behavior of the monkeys and their monkeys using a Zoom H2N digital recorder with responses. a Sennheiser ME66/K6 super-cardioid microphone. In order to examine the extent of remaining As we walked, we also recorded and photographed forested areas in the southern part of our study evidence of anthropogenic disturbance (e.g., spent area, in particular Eggua FR and Ohumbe FR, as shotgun cartridges, hunters’ footprints, gunshots, an a posteriori analysis, we first downloaded and hunters’ camps, burned logs, felled trees) and examined the maps of the two forest reserves from estimated the date of occurrence. These are reported the World Database on Protected Areas (WDPA) as frequencies rather than indices of occurrence; (IUCN & UNEP-WCMC 2015). However, we found i.e., herds of cattle that crisscross a forest leaving large discrepancies in the reserve size between numerous footprints cannot be easily quantified. officially declared size and downloaded polygons. In addition, we conducted semi-structured The official sizes of Eggua FR and Ohumbe FR interviews at seven villages that lie adjacent to or are 41.47 km2 and 46.08 km2, respectively (Ogun First Sightings of the Red-Bellied Guenon in Nigeria / 41 spp.; spp.; Ficus ; Destruction is due to ; Destruction to due is ; Hunting occurs. ; Hunting ; Severely degraded ; Severely guineense D. Spondias mombin Daniella oliveri Daniella ; Hunting occurs. ; Hunting Hunting is officially prohibited, but prohibited, officially is Hunting C. pendandra; ; Bola Camp villagers do not hunt, but there is no no is there but hunt, do not villagers ; Bola Camp Cattle grazing and forest burning are the major forces of of forces the major are burning forest and grazing Cattle Habitat Characteristics Habitat R. africana Raphia africana Raphia Diospyros alboflavescens; Diospyros Afzelia Afzelia are trees woodland; Common and savanna, farmbush, into Degraded fragmented and and oliveri, D. guineense, Dialium pentandra, Ceiba liebrechtsiana, Anthocleista africana, occurs. hunting and burning, tree grazing, Cattle Much of the forest has been converted to farms, pastureland, and villages; The only remaining remaining only villages; The and pastureland, farms, to been has converted the forest of Much Khaya sapida, Blighia africana, Afzelia include trees River; Common the Okparo along is forest and thonningiana, Ficus thonningii, Millettia senegalensis, Cola nigerica, Brachystegia are: trees Common areas; forested more are there but Marguba, to Similar and excelsa, Milicia angolense, Entandrophragma gigantea, cattle grazing and forest burning; Hunting occurs. Hunting burning; forest and grazing cattle cattle herders illegally enter into the forest on a daily basis. a daily on the forest into illegally enter herders cattle Musanga Musanga are trees Eggua FR; Common A part of forest; the riveine of strip degraded narrow Severely C. hispidum, Canthium cordifolia, zygia, Alchornea Albizia arboreus, Myrianthus cercropioides, and gigantea, hunted. not are primates destruction; Nonhuman The forested; 1/3 is Only buildings; and farmland by surrounded forest Seasonally inundated tree Common land; bare and teak plantation, shrubs, farmbush, of a mixture is area remaining Albizia sp., Diospyros nigerica, Brachystegia guineense, D. biglobosa, Parkia oliveri, D. species are and ivorensis, Khaya exasperata, Ficus lebbeck, Alchornea are: trees comon Some savanna; derived and farmbush, forest, Seasonally inundated and millenii, Cola elastica, Funtumia nobilis, Anthocleista cordifolia, due to logging, cattle grazing, and burning; Hunting occurs. Hunting burning; and grazing, logging, cattle to due Myrianthus arboreus, A. arboreus, Myrianthus are plants Dominant cocoa and plantations; farming Degraded to due cordifolia, Alstonia boonei, and Degraded due to farming and cocoa plantations; Remaining forest is in the riverine forests where where forests in the riverine is forest Remaining cocoa and plantations; farming Degraded to due A. M. arboreus, gingantea, Cola exasperata, Ficus are: plants Common enter; cannot humans and guineensis, Uapaca cordifolia, communities. in neighboring hunting against prohibition ) 2 1 9** Size 11** 1.5** 2.4** (km 751.4* 2,512*

(m) 21.7 34.4 61.4 25.4 69.3 133.8 307.3 354.3 Altitude (E) 2.693 3.773 3.998 2.923 2.928 3.077 2.928 2.863 Longitude (N) 7.918 8.454 8.448 6.998 7.046 6.964 6.731 6.768 Latitude

FR = Forest Reserve; NP = National Park; CF = Community Forest; PF = Private Forest = Private PF Forest; CF = Community Park; Reserve; NP = National FR = Forest Localities FR Imeko Iwoye, (Marguba) OyoOld NP (Yemeso) (Eggua FR) Eggua CF Atola Odoafanla CF CF Bola Camp Old OyoOld NP CF Igboju Royal Forest PF; Forest Royal Table 1. Habitat characteristics of survey of characteristics localities. (*Official size.) 1. Habitat size; **Estimated Table 42 / Matsuda Goodwin et al.

Forestry Dept. 2016), while the WDPA maps show at Marguba Range of OONP, with an encounter rate 49.4 km2 and 98.32 km2, respectively. For this of 0.62, 0.26, and 0.88 group/km, respectively. We reason, we georeferenced the scanned images of the confirmed the presence of C. erythrogaster at three 1971 physical maps (1:100,000) of Nigeria (Sheets localities, Atola community forest (0.27 group/km), 278 and 259) using the polynomial 1 transformation Royal Forest (private forest) in Eggua (0.08 group/ type with the Nearest Neighbor resampling km), and Bola Camp community forest (encounter method (Grosso 2010; Fleet et al. 2012). The image rate is not given because we walked less than 1 km). resolution of the northern section (Sheet 259) was No other threatened anthropoids of the region 1700 × 2338 pixels and the southern section (Sheet were observed. On December 28, 2015, at Atola, we 278) was 2337 × 1699 pixels. The locations of many sighted a group of C. mona and C. erythrogaster more villages were used as ground control points (GCP) than 100 m away from us in a degraded seasonally- during georeferencing. Small differences in reserve inundated forest and recorded a loud call of the size remained, however. The sizes of Eggua FR and adult male C. erythrogaster, but we were unable to Ohumbe FR calculated from the georeferenced map determine the color of the belly. At the Royal Forest, were 44.25 km2 (6.7% greater than the official size) a fleeing red-bellied monkey C.( e. erythrogaster) and 45.22 km2 (8.5 % smaller than the official size). was sighted once on December 30, 2015. At Bola Then, we used the Semi-Automatic Classification Camp, we saw two red-bellied individuals in a group PlugIn (SCP) v. 5.0.8 in QGIS v.2.18.2 to download once on January 3, 2016. This was an interspecies and process the cloud-free Landsat 8 OLI/TIRS interaction where members of a C. mona group were band images dated December 8, 2015 (Scene No. locomoting in a ~8 m HT Bombax buonopozense LC81910552015342LGN00, WRS Path = 91, WRS tree. Then, as a group ofC. e. erythrogaster was Row = 55, USGS 2016) during the long dry season in approaching the C. mona group, the adult male of this region from the US Geological Society (https:// the C. e. erythrogaster group began giving the loud earthexplorer.usgs.gov/). The band images 2-7 were call, which was immediately followed by an adult preprocessed for radiometric calibration and DOS1 male C. mona’s loud call. We recorded this chorus (Dark Object Subtraction 1) atmospheric correction of loud calls. (Chavez 1996), converted to surface reflectance, and Table 3 shows the result of interviews and viewed as color composite raster images using bands Appendix 1 lists the binominal terms and the 3-5 (Congedo & Munafò 2012; Congedo 2016). local names of the anthropoid taxa of the region. Land cover classifications were established using the Because Holi Nagot, Egun, and Egba are spoken Region of Interest (ROI) tool within the SCP based in our study area, this complicated our work of upon different spectral signatures and analyzed with deciphering what each interviewee stated, and it was the maximum likelihood method (Congedo 2016). not always possible to find villagers who could act as 0.3 % and 0.1 % of the land covers of Eggua FR and interpreters. At all sites, almost all interviewees stated Ogumbe FR, respectively, were unclassified. The C. mona occurred. There are a few uncertainties results of land cover classification were raster images regarding the result. For example, at Oloka, a village that were converted to polygons, and from which adjacent to the Marguba range of the OONP, the measurements of the size of classified areas were interviewee gave us the name “Kure”, but we could taken. By using the vector editing tools in QGIS, we not conclude what it meant, even though the mother manually delineated fragmented forests in the two tongue of one of us (FEO) is Yoruba. Given the fact forest reserves. that we observed C. mona, Ch. tantalus, P. anubis, and E. patas here, and this interviewee gave the first RESULTS three species’ names, “Kure” may mean the patas monkey, but his description that it has a white belly, Table 2 shows the results of our surveys. Path a dark back, and a black tail does not match E. patas, lengths walked were 0.03-3.74 km. The total length and he imitated the call of C. mona. At Igboju, one walked was 49.46 km. The number of primate interviewee described that “Okele” has the whitish- species encountered varied from zero to four. C. thing, which runs above the eyes, and the back is mona was most frequently seen, with the average black with the red band on the spine; the tail is long encounter rate of 0.65 (range = 0.26 - 1.5) group/km. and mostly yellow and the tip is black, but he could The highest encounter rate of 1.5 group/km of this not describe the color of the rump. As for “Erenoké”, species was found at Igboju community forest, two- he stated that the monkey’s body is red, but the hands thirds of which belongs to Eggua Forest Reserve. are black striped, and the tail is long and black, and Ch. tantalus, E. patas, and P. anubi s were seen only it moves on the ground. His descriptions of the two First Sightings of the Red-Bellied Guenon in Nigeria / 43 1 1 2 0 4 1 2 2 Taxa No. of , Cht = , Cht – – – – – – – – Pt – – – – – – – Pa 0.88 – – – – – – – Ep 0.26 – – – – – – – Cht 0.62 – + + Cm 0.50 0.27 0.71 1.50 0.26 – – – – – – – – Cn – – – – – – – – Pv , Cm = Cercopithecus mona nictitans , Cn = Cercopithecus – – – – – – – – Cv – – – – – – – – Cto ? – – – – – Ce Cee Cee ssp. Procolobus verus, Pv = Procolobus – – – – – + Ce 0.27 0.08 3.61 3.60 0.90 8.00 2.50 0.60 Total (km)* 11.45 18.80 walked ; + = Present or – = Absent if no encounter rates are given are rates encounter if no – = Absent or ; + = Present troglodytes , Pt = Pan , Cv = Colobus, Cv vellerosus 2 2 1 4 4 3 5 2 freq. Survey 1.8 0.9 2.0 0.3 Path Path (km) 0.3-1.1 0.5-1.9 length 2.0-3.74 1.77, 1.84 , Pa = Papio anubis , Pa Date 12/20/15 12/28/15 01/02/16 12/24/15 Erythrocebus patas 12/22-12/24/15 12/26-12/27/15 12/29-12/31/15 01/03-01/04/16 , Ep = , Ep

Cep = erythrogaster, erythrogaster (Cee = Cercopithecus erythrogaster Ce = Cercopithecus Forest; = Private PF Forest; CF = Community Park; Reserve; NP = National FR = Forest = Cercocebus), Cto torquatus pococki erythrogaster Cercopithecus Chlorocebus tantalus Localities FR Imeko Iwoye, (Marguba) (Eggua FR) Eggua Ibese Odoafanla CF CF Bola Camp Old OyoOld NP Igboju CF Igboju Old OyoOld NP (Yemeso) PF; Forest Royal Atola CF, Atola Table 2. Survey results with group encounter rates. (*Encounter rates are given for walks > 1 km.) for given are rates (*Encounter rates. 2. Survey encounter with results group Table 44 / Matsuda Goodwin et al. , 3 4 3 2 2 4 2 1 3 3 2? Sp. No. of ‡ ‡‡ Kure Iga Iga UNK Okele Opro Erenoké Asoroboa Kwagyedu Pt , Ep = Erythrocebus, Ep patas ✓ Pa ✓ Ep ? ✓ ✓ ✓* ✓** Cht , Cht = Chlorocebus, Cht tantalus ? ? ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ Cm

Cn

Pv ✓ Cv Cto Cep ? ✓ ✓ ✓ ✓ Cee No No No No Yes Yes Yes Yes Yes Yes Yes ability Credit- Cm = Cercopithecus mona nictitans, , Cn = Cercopithecus ## 35 45 35 55 35 45 45 68 42 20 56 Age . Date 12/23/15 12/27/15 12/27/15 12/27/15 12/19/15 01/02/16 01/03/16 12/25/15 12/27/15 12/27/15 12/27/15 Procolobus verus, Pv = Procolobus (m) Alt. 21.7 21.7 89.8 51.3 69.3 93.2 21.7 21.7 21.7 309.3 167.6 (E) Long 3,772 2.927 2.927 3.039 2.683 2.933 2.865 2.799 2.927 2.927 2.927 Colobus vellerosus Lat (N) 8,456 6.997 6.997 6.957 7.886 6.703 6.763 7.010 6.997 6.997 6.997 , Cv = , Cv ; UNK = unknown species (species' local names given by interviewees are written in appropriate cells); #This is the closest village to Iwoye Iwoye to closest is village #This the cells); in appropriate written interviewees species are ; UNK = unknown by (species' local given names troglodytes , Pt = Pan # Bola Ibese Ibeku Camp Oloka Igboju Ajileté Jabata (OONP, (OONP, Locality Marguba) , but he imitated the loud call of adult male C. mona call adult the loud of imitated he , but

State Oyo Ogun Pa = Papio anubis Pa . However, "kaka" means C. e. "kaka" means . However, Ch. tantalus for termis the “Aiya” kaka". "aiya name us the interviewee * = The gave √ = Present; Ghana; from surveyed; FR we ##A migrant in Imeko or large. high means Yoruba in ‡‡ = "Iga" and squirrel; monkey, arboreal baboon, for names Ashanti ‡ = is correct; our interpretation if unsure are we Thus, in Yoruba. erythrogaster Ch. means which "aiya", name us the species. interviewee ** = The gave primate large-sized another or C. mona adult an is it say to the interviewee meant that speculate only can We tantalus Table 3. The results of interviews.results 3. The Table = , Cto pococki erythrogaster , Cep = Cercopithecus erythrogaster erythrogaster Cee credible); = Cercopithecus (not No (credible); Credibility: Yes = Longitude; Long =Latitude; Lat Cercocebus torquatus First Sightings of the Red-Bellied Guenon in Nigeria / 45 species do not match with any monkeys in our study DISCUSSION AND CONCLUSION area. Also, the 42-yr-old hunter here described three monkey species only in relation to large, medium, We confirmed the presence ofC. erythrogaster and small body size, and the 56-yr-old hunter, who in patches of lowland seasonally inundated forest was a migrant from Ghana, gave us three monkey in southwestern Nigeria during our surveys. C. names, “Kwagyedu (baboon)”, “Asoroba (arboreal erythrogaster has been assumed to occur here for monkey)”, and “Opro (squirrel)” in Ashanti, one a long time (Oates 1985, 1996, 2011a), but this is of the Ghanaian languages. With help from an the first confirmation of the red-bellied subspecies’ anonymous reviewer of this manuscript we were able occurrence at two forests, Royal Forest and Bola to decipher the meaning of these words. The 35-yr- Camp, in this region. Still, we cannot be certain old hunter gave us an unknown monkey name, “Iga”, to which C. erythrogaster ssp. the monkeys we which means high or tall in Yoruba, but we could saw at Atola belong although the name given by not decipher which species he was referring to. the interviewee suggests it is C. e. erythrogaster. Furthermore, although the 45-yr-old hunter gave us The loud call of the adult male C. erythrogaster we the name for the red-bellied guenon, “Ogbé” with a recorded at Atola cannot resolve this matter because red belly, the only monkey we saw at Igboju was C. various calls given by different subspecies are usually mona. At Atola, the interviewee told us that when indistinguishable unless a detailed sound analysis is “Okaka” (= C. e. erythrogaster) comes to raid the conducted using adequate samples (Dallmann & bananas, unripe mangos, and unripe plantains, they Geissmann 2001; J. Fuller pers. comm. 2016). shoot them. Lastly, the interviewee at Ajieté village As of now, the forests where we found C. stated that the mona monkey and the red-bellied erythrogaster in our study area are small and largely guenon occur in the Odoafanala community forest, unprotected. Atola, for example, is a small forest but our short survey found only mona monkeys where hunting is unregulated. About 15 years ago, there. logging companies had mostly cut down the large At almost all sites there was evidence of negative trees (J. Tella pers. comm. 2016). Currently, the human activities except at Odoafanala, where we remaining forest is severely degraded, although the spent very little time (Table 4). Six gunshots we heard red-bellied guenon may be somewhat protected at the Royal Forest occurring beyond the boundary in the inundated area, deterring hunters, even of the forest indicate high hunting pressure in the during the major dry season. Demonstrated by surrounding area. The one gunshot we heard at Bola the interviewee’s description of the crop-raiding Camp also occurred outside the community forest. behavior of “Okaka” (C. e. erythrogaster), if hunting Furthermore, at all sites except Odoafanala and Bola can be curtailed there is a potential for a population Camp, we either encountered herds of cattle or saw increase for this adaptive monkey. However, a numerous footprints made by cattle. limestone quarry site belonging to the Ibese Cement The Landsat 8 composite image and land cover Plant (7.009˚ N, 3.041˚ E) is not far from this forest. classificaitons show that within Eggua FR and The air is polluted, and oversized vehicles routinely Ohumbe FR there is a lack of large areas of contiguous pass along the nearby main road. green color, which indicates forest, and forests are The Royal Forest is one of the two forests where fragmented (Figures 2-4). The forested area in Eggua we confirmed the occurrence ofC. e. erythrogaster. FR encompasses about 7.1 km2, which is 16.1 % of The greatest threat toC. e. erythrogaster here appears the total area (Figure 3). Almost all fragmented to be the trespassing of the livestock (HRM Oba forests are small (less than 1 km2). Total fragmented Adeleye Dosunmu pers. comm. 2016). The cows forests within Ohumbe FR encompass only 3.6 destroy small trees and tree seedlings (Laurance km2 or 7.9 % of the total area (Figure 4). Although 2010). The increasing demand for livestock products we attempted to resolve the size discrepancies of in this region is threatening the continued existence the two reserves between our calculations and the of small forests like the Royal Forest (Thornton gazetted size (both reserves were gazetted in 1931) 2010). A hopeful development is that the Onigua by contacting forestry officials, our attempts were (pers. comm. 2016) has recently created a non-profit unsuccessful. Our land cover classifications should organization, which plans to expand the forest by be considered preliminary until we obtain ground- purchasing an adjacent piece of land. Currently, verification data and conduct accuracy assessment. he is not sure how long he can continue to combat Bola Camp and neighboring communities appear to external pressures in the face of a lack of financial have about 9 km2 of forested area and Igboju, about resources. 1.5 km2 (Figure 2). 46 / Matsuda Goodwin et al. 1 1 1 1 1 1 Cattle & Cattle footprints 1 1 tree Felled felling tree(s) or 1 trees Pile of Pile of logged 1 bird Plucked feathers 1 1 grass Burned 1 trap Steel 1 footprint Poachers’ 1 camp Poachers’ 3 6 1 1 Gunshot .90 .60 3.61 3.60 8.00 2.50 (km) 11.45 18.80 Length Date 12/20/15 12/28/15 01/02/16 12/24/15 12/22-12/24/15 12/26-12/27/15 12/29-12/31/15 01/03-01/04/16

Localities FR Imeko Iwoye, (Marguba) (Eggua FR) Eggua Ibese Odoafanla CF CF Bola Camp Old OyoOld NP Old OyoOld NP (Yemeso) CF Igboju Royal Forest PF; Forest Royal CF, Atola Table 4. Frequency of occurrence of anthropogenic disturbance. anthropogenic occurrence 4. Frequency of of Table Forest. = Private PF Forest; CF = Community Park; Reserve; NP = National FR = Forest First Sightings of the Red-Bellied Guenon in Nigeria / 47

Figure 2. The Landsat 8 composite image of the southern part of our study area (Ibese is not shown). There is a lack of large areas of contiguous deep green color that indicate old growth (or closed) natural forest. However, there are some small forested areas including riverine forests in Bola Camp and Igboju. Patches of contiguous forest fragments are small in Eggua FR.

Although we did not findC. erythrogaster at such as duikers (genus Cephalophus), bushbucks Igboju, one interviewee gave us the local name for (Tragelaphus scriptus), giant pouched rats C. e. erythrogaster. Given the proximity of Igboju (Cricetomys gambianus), and cane rats (Thryonomys to the Royal Forest, it is probable this taxon occurs swinderianus). If C. erythrogaster indeed occurs in Igboju. The village chief informed us that they here, creating a forest corridor to connect Igboju, used to hunt monkeys, but stopped hunting them the Royal Forest, and the southern forest fragments about 15 years ago because the wives of the hunters of Eggua FR is recommended and establishing a who had eaten the monkey meat during pregnancy >10 km2 of a faunal reserve. In addition, there still often gave birth to deformed newborns; most of remains about 9 km2 of forest around Bola Camp these were twin births. To avoid recurring tragedies, communities where hunting pressure is minimal. he said, they have ceased to hunt any monkeys, Establishing a conservation program to protect the although they still continue to hunt other animals red-bellied guenon is recommended here. 48 / Matsuda Goodwin et al.

Figure 3. Land cover classification of Eggua FR.

No conservation plan is without challenges. The deforested, degraded, and fragmented, surveying main road cuts across the potential corridor between the remaining forests in Eggua FR and Ohumbe FR the Royal Forest and Igboju where cattle constantly is needed in the near future. Furthermore, we could trespass the area. Our guides at Igboju refused to not adequately conduct a study along the Yewa River lead us too far away from the village for fear of being (Figure 1), where the Landsat 8 composite image killed by Fulani herders’ poison-tipped arrows. To show narrow strips of seasonally inundated riverine create a corridor also requires rehabilitating the forests between south of Igbojou and northeast of habitat between Igbojou and the forest fragments Bola Camp (Figure 2). in Eggua FR. These challenges are surmountable Until now, C. e. erythrogaster has been known to if there is the will and the resources, and we plan occur only in eastern Togo and southern Benin. All to submit this recommendation to the community the forests where C. e. erythrogaster inhabit in Benin stakeholders and to the government authorities. and Togo are lowland seasonally inundated forest or As our surveys were limited in scope, time spent riverine forest, reinforcing the idea that this taxon at each locality and the number of localities visited is adapted to such habitats (Nobimè et al. 2009; and surveyed was less than ideal. Although severely Matsuda Goodwin et al. 2017a). Figure 5 shows the First Sightings of the Red-Bellied Guenon in Nigeria / 49

Figure 4. Land cover classification of Ohumbo FR. modified distribution ranges of the two subspecies, two countries, the 2016 IUCN Red List has elevated incorporating our new information. The growing the threatened status of this subspecies to Critically human populations and the never-ending expansion Endangered (CR) (Matsuda Goodwin et al. 2017a). of farmland exacerbated by mining, illegal logging, A similar analysis also elevated the status of C. e. cattle grazing, and uncontrolled hunting (Geist & pococki to Endangered (EN), and at the species Lambin 2002; NPC Nigeria 2016; World Bank 2016) level, the threatened category of C. erythrogaster might have already disconnected the previously was also elevated to EN (Ikemeh et al. 2017; contiguous ranges of the two subspecies. If so, Matsuda Goodwin et al. 2017b). The prospect for we may never be able to find out whether the two the conservation of the red-bellied guenon in this subspecies shared any overlapping ranges and the region, unfortunately, does not look bright unless extent of any possible hybridization between them. all three range-countries take action to install strong Given the fact that the populations of C. e. conservation measures. erythrogaster in Togo and Benin have declined by The semi-structured interview has been ≥ 80% in the past three generations (27 years) and widely used as a preferred method to obtain local their habitats have been significantly reduced in the knowledge regarding presence or absence of some 50 / Matsuda Goodwin et al.

Figure 5. The modified distribution ranges of Cercopithecus erythrogaster erythrogaster and Cercopithecus erythrogaster pococki in Nigeria, Benin, and Togo. Green areas show protected areas and forest reserves (IUCN & UNEP-WCMC. 2015). The demarcation line between the two subspecies has now been moved to the east of the Benin-Nigeria border, although how far east the eastern end of C. e. erythrogaster goes is still unknown. The growing human populations and never-ending expansions of farmlands and pastureland coupled with deforestation and mining might have already isolated the previously contiguous ranges of the two subspecies. If so, we may never be able to find out whether, where, and how the subspecies shared any overlapping ranges.

primate species to find potential survey sites and varying degrees of credibility of the responses (Campbell & Hadley 2005; Urbani 2006; Campbell we obtained from interviewing several hunters at et al. 2008; Parker et al. 2008; Starr et al. 2011; Chi Igboju underscores the importance of conducting et al. 2014; Ginn & Nekaris 2014) or even to map interviews on multiple hunters at each locality distribution ranges of some taxa (Sinsin et al. 2002; and indicates that preparations of questions and Djègo-Djossou & Sinsin 2009; Nobimè et al. 2009; the interpretation of results require care. If we had Djègo-Djossou et al. 2014). Often, however, primate interviewed only the 42-yr-old hunter, we could not field studies that use semi-structured interviews do have learned that C. erythrogaster might occur (or not provide detailed descriptions of the method. might have occurred) at Igboju. We recommend that We consider that more serious attention needs to interviews need to be conducted on more than one be paid to this method. The variation in responses individual and ideally 5-10 interviews per site are First Sightings of the Red-Bellied Guenon in Nigeria / 51 recommended to obtain credible information. We LITERATURE CITED also recommend that, when possible, any potential bias that may occur during each interview should Anderson, J., J.M. Rowcliffe & G. Cowlishaw. 2007a. be minimized. A limited scope of the study and the The Angola black-and-white colobus (Colobus brevity of time have precluded us from conducting angolensis palliatus) in Kenya: Historical range a systematic broad-scale use of the method, which contraction and current conservation status. is gaining ground in primatology (c.f., Anderson American Journal of Primatology 69(6): 664-680. et al. 2007a, b; Meijaard et al. 2011). Interviewing Anderson, J., J.M. Rowcliffe & G. Cowlishaw. 2007b. young inexperienced hunters or migrants should Does the matrix matter? A forest primate in be avoided. Nevertheless, our study has shown a complex agricultural landscape. Biological that there are dangers to solely relying upon local Conservation 135: 212-222. knowledge to map primate distribution patterns. Bernard, H.R. 2006. Research Methods in Extreme care is needed to assess the costs and Anthropology: Qualitative and Quantitative benefits of all aspects of the method in order to Approaches. AltaMira Press. effectively complement primate surveys in Africa. Campbell, G. & P. Hadley. 2005. Primate and bird diversity in the Fazao-Malfakassa National ACKNOWLEDGEMENTS Park, Togo. Unpublished Report submitted to Conservation International (CI) and Critical We are grateful to Joseph Asipaiwoye at Imeko Ecosystem Partnership Fund (CEPA). FR for giving us permission to conduct a survey at Campbell, G., J. Teichroeb & J.D. Paterson. 2008. Iwoye. The commissioner of the OONP, Yohanna Distribution of diurnal primate species in Togo Seidu kindly gave us permission to conduct a survey and Bénin. Folia Primatologica 79(1): 15-30. in the park and helped us with accommodations. We Chavez, P. S. 1996. Image-based atmospheric appreciate Mr. Tamu and Mr. Kola for guiding us in corrections-revisited and improved. the park and Felicia for providing some valuable Photogrammetric Engineering and Remote information regarding the park. We would like to Sensing 62(9): 1025-1035. thank the HRM Oba Adeleye Dosunmu, Onigua Chi, M., H. Zhi-Pang, Z. Xiao-Fei, Z. Li-Xiang, of Eggua who gave us permission to conduct our S. Wen-Mo, M.B. Scott, W. Xing-Wen, C. studies at Igboju and the Royal Forest. We appreciate Liang-Wei & X. Wen. 2014. Distribution and the logistical support we received from Isola Samuel conservation status of Rhinopithecus strykeri in Olugbemiga of Igbogila. Prince Bode Akinola Tella China. Primates 55(3): 377-382. and Jimmy Tella of Ibese kindly guided us to Atola. Congedo, L.M. 2016. Semi-Automatic Classification We are appreciative of the hospitality we received Plugin Documentation. DOI:http://dx.doi. from the Baale (chiefs) and hunters at Jabata, org/10.13140/RG.2.2.29474.02242/1. Igboju, Bola Camp, and Ajileté who facilitated our Congedo, L. & M. Munafò. 2012. Development of study. RMG would like to thank Luca Congedo a methodology for land cover classification in (Sapienza Università di Roma, Italy) and Kasey Dar es Salaam using Landsat imagery. Rome: Wilson (Michigan State University Map Library) Sapienza University. Working paper. for answering many questions regarding the SCP Dallmann, R. & T. Geissmann. 2001. Different levels and map transformation, respectively. We thank of variability in the female song of wild silvery four anonymous reviewers for their constructive gibbons (Hylobates moloch). Behaviour 138(5): criticism on our earlier manuscript. One of the 629-648. anonymous reviewers has kindly helped us with Djègo-Djossou, S. & B. Sinsin. 2009. Distribution the Ashanti language. Evrard Akpla, Allan Gilbert, et statut de conservation du colobe de Geoffroy and one anonymous reviewer generously assisted us (Colobus vellerosus) au Bénin. International with French translation of the abstract. We would Journal of Biological and Chemical Sciences 3(6): like to express sincere gratitude to John F. Oates for 1386-1397. his guidance, identification of the giant pouched Djègo-Djossou, S., J.G. Djego, G.A. Mensah, M.C. rat at Igboju, providing the 1971 maps of Nigeria, Huynen & B. Sinsin. 2014. Distribution du Colobe and reading earlier drafts of this manuscript. This Vert Olive, Procolobus verus, au Bénin et Menaces research was made possible by funds and supplies Pesant sur sa Conservation. African Primates 9: provided by Chester Zoo, Primate Conservation, Inc., 23-34. International Primatological Society, Conservation Fleet, C., K.C. Kowal & P. Pridal. 2012. Georeferencer: International, and Fordham University. Crowdsourced georeferencing for map library 52 / Matsuda Goodwin et al.

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Appendix 1. Anthropoid names used in southwestern Nigeria. Some of the names differ from Happold (1987) and Oates (2011a). For example, Happold (1987) states ambè is the “white-nosed monkey,” but our interviewee’s description was that of C. mona. In Yoruba, “o” is a prefix, meaning something exists or lives. The list under Yoruba contain names in Holi Nagot, Egun, and Egba.

Taxa Fon Yoruba Cercopithecus erythrogaster erythrogaster zinkaka ogbè, ugbia, kaka, okaka Cercopithecus erythrogaster pococki ? edun olokun, oloyo, Idji oloyo Cercopithecus mona zin houi, zin houm, zin ho edun, lambè, zin ambè, ambè gidi Chlorocebus tantalus zin ahiwé aya, aiya efun Erythrocebus patas ijimere idji-mere Cercopithecus nictitans ? okin Colobus vellerosus zin klan donko Procolobus verus zin gbo chike-chike Papio anubis akato, ato obo (in llobi), akiti, laguido Cercocebus torquatus ? owe, okpe (Ijaw) Pan troglodytes loki etiemi, inaki, elegbebe African Primates 12: 55-58 (2017)/ 55 Brief Communication:

Dogs Disrupting Wildlife: Domestic Dogs Harass and Kill Barbary Macaques in Bouhachem Forest, Northern Morocco

Siân Waters1,2, Ahmed El Harrad2, Mohamed Chetuan2, Sandra Bell1, and Joanna M. Setchell1

1Department of Anthropology, Durham University, Durham, UK; 2Barbary Macaque Awareness & Conservation, Tétouan, Morocco

INTRODUCTION

The domestic dog (Canis familiaris) is the most (Camperio-Ciani & Mouna 2006). Shepherds abundant carnivore in the world (Gompper 2014). and their dogs are reported to harass macaques People and dogs have a complex relationship, with in Talassemtane National Park in north Morocco dogs performing important roles in human society (Mehlman 1984). Here, we report observations (Serpell 1995). Due to their presence in many of domestic dogs disturbing and killing Barbary regions of the world, conflicts involving dogs and macaques in Bouhachem forest, north Morocco. wildlife have been cited as a serious problem for wildlife conservation (Young et al. 2011; Hughes & METHODS Macdonald 2013; Weston & Stankowich 2014; Peltola & Heikkila 2015). The presence of domestic dogs in The study site, Bouhachem forest, is an area rural or protected areas increases the risks of disease of mixed oak forest covering ~140km² in north transmission to and from wildlife and interferes Morocco (Figure 1). The communities around the with the spatial distribution of wildlife populations forest are agropastoralists. There has been no recent (Young et al. 2011; Hughes & Macdonald 2013; census at a household level so no population data are Sepulveda et al. 2015; Lessa et al. 2016). Reports of available. Cows graze in the forest unattended but domestic dog disturbance and predation on primates goats are regularly herded into and out of the forest are scarce, probably due to the rarity of observing by shepherds. All shepherds use livestock guarding such events in the field. Dogs of undetermined status dogs to protect their goats from predators. (i.e., whether feral or free roaming) were reported to We identified and observed four groups of kill commensal macaques in India (Anderson 1986) Barbary macaques (Waters et al. 2015) and observed and Japanese macaque (Macaca fuscata) infants in each group for two days a week from February- Japanese monkey parks (Knight 2011), whilst feral November 2010, recording all harassment of the dogs were observed killing a juvenile long-tailed study groups by dogs during these observation macaque (M. fascicularis) in Singapore (Riley et al. periods. The length of observation periods depended 2015). on the macaque groups’ tolerance of observers, The Barbary macaque M.( sylvanus) is the varying from five minutes to >three hours. We only macaque species found outside Asia, and is supplement this with information on direct dog- present in Morocco and Algeria, with an introduced macaque interactions up to and including October population on Gibraltar (Fa 1981; Modolo et al. 2016, obtained during conservation activities, 2005). Researchers have observed dogs snatching including Barbary macaque monitoring, by the infants from adult Barbary macaques on six Barbary Macaque Awareness & Conservation team. occasions in the Middle Atlas Mountains, Morocco

Correspondence to: Siân Waters, Department of Anthropology, Durham University, Durham UK; [email protected]; Phone: +44 1495 722117. 56 / Waters et al.

Figure 1. The location of Bouhachem forest in northern Morocco and the Mediterranean

RESULTS 19% by dogs accompanying mushroom collectors. It was unclear whether dogs in the remaining 3% of Barbary macaques always emitted alarm attacks were accompanied, but we did not detect any vocalisations on sighting domestic dogs in the humans in the vicinity. The largest pack of 18 dogs forest, and climbed into trees or onto high rocks was unaccompanied. to avoid them. We recorded a total of 30 events of We recorded three Barbary macaque mortalities dogs harassing macaque groups. The highest rates of that were due (or very likely due) to dogs. In April occurrence (N = 17) happened during the months 2010, we observed a livestock guarding dog carrying of April and May. Shepherds and dogs accompanied an infant macaque’s head. Two weeks later, in early the goat herds on their ascent to pastures and dogs May, we heard the vocalisations of macaques and harassed any macaque groups they encountered dogs. When we arrived at the scene, we found a dead on the way. The general pattern of an interaction male infant with bite wounds. In February 2014, we involved the sudden appearance of dogs running came across unaccompanied dogs harassing a group towards the macaque group. On sighting the dogs, of macaques and a male macaque about 9 months the macaques would alarm call and ascend into trees old with bite wounds. Both bodies were still warm whilst the dogs ran around and barked beneath. and dogs were still in the vicinity. Disturbances lasted from seven minutes to two hours Not all dog-macaque interactions ended in the and 15 minutes, with a mean length of 42 minutes death of a macaque. In May 2011, MC disturbed a (N = 9). When goat herds returned to their villages livestock guarding dog with a live infant in its mouth. in the late afternoon, the interactions were much On sighting MC, the dog dropped the infant and shorter and lasted 8 to 27 minutes with a mean of 15 fled. MC was able to return the infant, uninjured, to minutes (N = 21). The mean number of dogs taking its group. In March 2015, we were alerted by alarm part in harassment events was four, with a range of calls and screams from one of our study groups. 1 - 18. The dogs were accompanying shepherds and We intervened to stop an attack on a young female herds on the majority of occasions (59%), with 19% Barbary macaque by five unaccompanied dogs. The of harassment events by unaccompanied dogs and macaque survived, albeit quite badly wounded, and Domestic Dogs and Barbary Macaques / 57 managed to climb into a tree about 35 minutes after groups of Burmese long-tailed macaques (M. the attack (Figures 2a and 2b). At this point we left fascicularis aurea) although no actual predation the scene, not wanting to disturb the returning group events were observed (Gumert et al. 2013). members. Finally, in October 2016, an adult male We also observed a Barbary macaque attack a macaque attacked and bit the throat of a domestic dog. To the best of our knowledge, this is the first dog attempting to guard fields when macaques were report of a wild Barbary macaque attacking a dog in feeding on crops. North Africa. Human-habituated Barbary macaques living on Gibraltar sometimes attack pet dogs (L. DISCUSSION Radford, unpublished data), and there are reports of primate males attacking dogs in other regions. Barbary macaques are mainly terrestrial and For instance, adult male long-tailed macaques (M. thus susceptible to harassment from domestic dogs. fascicularis) attack dogs in Bali (Anderson 1986) The longer morning harassment events in spring and adult male baboons (Papio ursinus) kill dogs may result in increased stress and energetically when baboons feed on crops in Africa (Butler et al. costly behaviour for lactating or pregnant female 2004). Such examples illustrate that primates are not macaques, due to the dogs’ presence impeding always the victims in dog-macaque interactions. macaque foraging. Such effects have been observed These physical interactions also present a potential for other species (Anderson 1986; Gumert et al. for interspecies disease transmission, particularly 2013; Riley et al. 2015). Barbary macaque infants rabies. There are also implications for human begin to spend time away from carers at around four and macaque health due to the indirect spread of weeks old and are not vigilant toward predators, pathogens from dog faeces in both village and forest. likely leaving them more susceptible than adult Controlling the dog population in Bouhachem and macaques to fatal interactions with dogs. Such a lack deterring the dogs’ behaviour toward the macaques of vigilance in response to the ubiquitous presence can only be done by understanding the relationship of domestic dogs may have the potential to affect they have with their owners and developing a Barbary macaque infant survival in Bouhachem mitigation strategy inclusive of such considerations. substantially. In Laem Son National Park in The success of this strategy may be more likely if Thailand, the presence of domestic dogs is negatively it incorporates the provision of salient benefits to correlated with a low proportion of infants in some people and their dogs.

a. b. Figure 2. a: A young female Barbary macaque, immediately after being attacked by five dogs. b: The same young female 35 minutes later. Photographs by A. El Harrad. 58 / Waters et al.

ACKNOWLEDGEMENTS 341-351. Knight, J. 2011. Herding Monkeys to Paradise: How We are indebted to the Royal Zoological Society Macaque Troops are Managed for Tourism in of Scotland for supporting our research 2009-2012. Japan. Leiden, Brill. We thank the Haut Commissariat des Eaux et Forêts Lessa, I., Guimaraes, T.C.S., de Godoy Bergallo, H., et la Lutte Contre le Désertification for granting our Cunha, A. & E. Vierira. 2016. Domestic dogs in research permit and University Abdelmalek Essâadi, protected areas: a threat to Brazilian mammals? Tétouan for assistance with our permit applications. Brazilian Journal of Nature Conservation 14: 46- We are extremely grateful to; Association Française 56. des Parcs Zoologiques; Association Beauval Nature; Mehlman, P.T. 1984. Aspects of the ecology and Conservatoire pour la protection des primates conservation of the Barbary macaque in the fir France; Folly Farm, UK; GaiaZoo, The Netherlands; forest habitat of the Moroccan Rif Mountains. Zoo Helsinki, Finland; Tiergarten Schönbrunn, In The Barbary Macaque: A Case Study in Austria; Parco Natura Viva, Italy; Blair Drummond Conservation. J. E. Fa, ed. London. Plenum Press. Safari Park; Ouwehands Zoo, The Netherlands; Pp. 165-199. International Primate Protection League, USA; Modolo, L., Salzburger, W. & R.D. Martin. 2005. NaturZoo Rheine, Germany; Alameda Wildlife Phylogeography of Barbary macaques (Macaca Conservation Park, Gibraltar; Mohamed Bin sylvanus) and the origin of the Gibraltar colony. Zayed Endangered Species Fund for supporting Proceedings of the National Academy of Sciences our research and conservation work. We are very of the United States of America 102(20): 7392- grateful to Lucy Radford and two anonymous 7397. reviewers for their comments on an earlier version Peltola, T. & J. Heikkila. 2015. Response-ability in of this manuscript. wolf-dog conflicts. European Journal of Wildlife Research 61: 711-721. LITERATURE CITED Riley, C.M., Koenig, B.L. & M.D. Gumert. 2015. Observation of a fatal dog attack on a juvenile Anderson, J.R. 1986. Encounters between domestic long-tailed macaque in a human-modified dogs and free-ranging non-human primates. environment in Singapore. Nature in Singapore Applied Animal Behavior Science 15: 71-86. 8: 57-63. Butler, J.R.A., du Toit, J.T. & J. Bingham. 2004. Free- Sepulveda, M., Pelican, K., Cross, P., Eguren, A. & ranging domestic dogs (Canis familiaris) as R. Singer. 2015. Fine-scale movements of rural predators and prey in rural Zimbabwe: threats of free-ranging dogs in conservation areas in the competition and disease to large wild carnivores. temperate rainforest of the coastal range of Biological Conservation 1195: 369-378. southern Chile. Mammalian Biology 80(4): 290- Camperio-Ciani, A. & M. Mouna. 2006. Human 297. and environmental causes of the rapid decline of Serpell, J.A. 1995. The Domestic Dog: Its Evolution, Macaca sylvanus in the Middle Atlas of Morocco. Behaviour and Interactions with People. in The Barbary Macaque: Biology, Management Cambridge, Cambridge University Press. and Conservation. J. K. Hodges & J. Cortes, eds. Waters, S., El Harrad, A., Chetuan, M. & Z. Nottingham, Nottingham University Press: 257- Amhaouch. 2015. Barbary macaque group size 275. and composition in Bouhachem forest, North Fa, J. 1981. Apes on the rock. Oryx 16(1): 73-76. Morocco. African Primates 10: 53-56. Gompper, M.E. 2014. The dog-human-wildlife Weston, M.A. & T. Stankowich. 2014. Dogs as agents interface: assessing the scope of the problem. of disturbance. In Free-ranging Dogs and Wildlife In Free-ranging Dogs and Wildlife Conservation. Conservation. M. E. Gompper, ed. Oxford, M. E. Gompper, ed. Oxford, Oxford University Oxford University Press: 94-116. Press: 9-54. Young, J.K., Olson, K.A., Reading, R.P., Gumert, M.D., Hamada, Y. & S. Malaivijitnond. Amgalanbaatar, S. & J. Berger. 2011. Is wildlife 2013. Human activity negatively affects stone going to the dogs? Impacts of feral and free- tool-using Burmese long-tailed macaques roaming dogs on wildlife populations. Bioscience Macaca fascicularis aurea in Laem Son National 61: 125-132. Park, Thailand. Oryx 47: 535-543. Hughes, J. & D.W. Macdonald. 2013. A review of the interactions between free-roaming domestic Received: 17 November 2016 dogs and wildlife. Biological Conservation 157: Accepted: 18 January 2017 African Primates 12: 59-64 (2017)/ 59 Brief Communication:

Pan African Sanctuary Alliance: Primate Welfare, Conservation, and Research

Rachel Stokes¹, Gregg Tully¹, and Alexandra Rosati²

1Pan African Sanctuary Alliance, Portland, Oregon, USA; 2Department of Psychology, University, of Michigan, Ann Arbor, Michigan, USA

PASA’S WORK

The Pan African Sanctuary Alliance (PASA), of advisors and other specialists. Additionally, the largest association of wildlife centers in Africa, PASA helps its members succeed by advocating includes 22 organizations that collectively house for them internationally, providing funding more than 3,000 rescued primates (Table 1; Figure and technical support during emergencies, and 1). Prior to PASA’s formation, these organizations building their capacity through training in topics had similar goals and were facing similar such as strategic planning, public education and challenges, but typically did not communicate community engagement, veterinary treatment, and with one another. In 2000, conservationists and animal care. primatologists arranged a meeting in Uganda to In addition to advocating for and supporting bring these groups together for the first time. The its member organizations, PASA collaborates with directors of the organizations agreed there was a them on large-scale conservation initiatives. Some need for improved ongoing communication and, of PASA’s newest projects include: as a result, PASA was formed. Although PASA’s Cameroon Conservation Education Program: headquarters is now in Portland, Oregon and it is In 2015, PASA and its member organizations a registered nonprofit in the United States, it was in Cameroon launched the Cameroon created by the African wildlife centers. Conservation Education Program with the goals Despite working in extraordinarily challenging of: (1) determining the most effective approach to conditions, members of the Alliance are inspiring Cameroonian children to protect their making significant strides in primate welfare country’s wildlife and other natural resources, and conservation. They collaborate with law and (2) integrating it into school curricula, so enforcement agencies to reduce wildlife crime by that children in Cameroon will learn the value rescuing confiscated animals, give lifelong care of protecting animals and their habitats. This is to primates orphaned by the bushmeat trade and expected to engender a long-term nationwide shift the illicit pet trade, work to stop the hunting and in the population’s attitudes and behavior regarding trafficking of endangered species, defend critical conservation, resulting in an increase in the habitat from exploitation, and conduct community number and size of protected areas, stronger legal development and education programs reaching protections for natural habitat, and an increase in more than 500,000 people each year across Africa. the abundance of endangered species in Cameroon. Additionally, PASA member wildlife centers After a very successful pilot, PASA, Sanaga-Yong provide employment for nearly 700 Africans and Chimpanzee Rescue, and Ape Action Africa are inject millions of dollars into local economies. expanding this program to reach 4,500 youth in PASA’s unique accreditation process brings 2017. credibility to wildlife centers, and PASA Edutainment Films Program: The Edutainment membership gives them access to a global network Films Program is a pioneering initiative in Africa

Correspondence to: Gregg Tully, Pan African Sanctuary Alliance, Portland, Oregon, USA; E-mail: [email protected]; Web site: www.pasaprimates.org. 60 / Stokes et al.

Figure 1. Map of members of the Pan African Sanctuary Alliance.

to distribute high-quality, engaging films that and failures of African primate release efforts. were primarily created for African audiences. Although reintroductions can be highly valuable The flagship movies of the program were for conservation in that they increase the produced by the nonprofit Nature for Kids, which population sizes of endangered species in the wild creates entertaining films with messages about and bring stronger protection to their habitats, environmental conservation. In a pilot program, many reintroductions of African primates have hundreds of thousands of people in Cameroon saw been conducted by trial-and-error, and some are the films on national television and on the national unsuccessful. In order to increase the success rate, it train system (Figure 2). Following this tremendous is valuable to outline the best practices for primate success, PASA is expanding this program to include reintroductions based on a comprehensive review of ten African countries. the methods and results of releases that have been Reintroduction Data Synthesis Project: conducted across Africa. PASA will work closely Currently, PASA is developing a Reintroduction with the staff of wildlife centers to analyze their Data Synthesis Project, which will be the first data and quantify aspects of individual survival, known comprehensive synthesis of successes reproduction, and integration into wild groups. Pan African Sanctuary Alliance / 61

Figure 2. Staff from Chimfunshi Wildlife Orphanage showing an Edutainment film to students.

Table 1. PASA Member Wildlife Centers.

Center Country Ape Action Africa Cameroon Centre pour Conservation des Chimpanzees (CCC) Guinea Chimfunshi Wildlife Orphanage Zambia Chimpanzee Eden South Africa Chimpanzee Rehabilitation Project The Gambia Colobus Conservation Kenya Lwiro Primate Rehabilitation Centre (CPRL) D.R. Congo Drill Ranch Nigeria Fernan-Vaz Gorilla Project Gabon HELP-Congo Congo Jeunes Animaux Confisques au Katanga (J.A.C.K.) D.R. Congo Lilongwe Wildlife Centre Malawi Limbe Wildlife Centre Cameroon Lola Ya Bonobo D.R. Congo Ngamba Island Uganda Project Protection des Gorilles-Congo Congo Project Protection des Gorilles-Gabon Gabon Sanaga-Yong Chimpanzee Rescue Cameroon Sweetwaters Chimpanzee Sanctuary Kenya Tacugama Chimpanzee Sanctuary Sierra Leone Tchimpounga Chimpanzee Rehabilitation Centre Congo Vervet Monkey Foundation South Africa 62 / Stokes et al.

Figure 3. Nyango, a Cross River gorilla at Limbe Wildlife Centre in Cameroon, relaxing in the shade.

The combination of PASA’s global network children on many different cognitive tests have and its member organizations’ local expertise and shown that apes and children solve problems connections uniquely positions the Alliance to involving physical reasoning—for example, produce lasting changes to protect Africa’s great distinguishing different quantities, using tools, apes and monkeys (Figure 3). and remembering the locations of objects—fairly similarly. However, children quickly surpass apes PASA WILDLIFE CENTERS WELCOME when faced with problems about social reasoning, RESEARCHERS such as imitating others’ actions or inferring others’ mental states. This has provided support for the In addition to playing an essential role in “cultural intelligence hypothesis”— the idea that securing a future for Africa’s primates and their what is special about human cognition is not that habitat, almost all PASA member wildlife centers we are generally smarter than other species, but that are willing to host researchers. Their cooperation we specifically excel at skills needed for cultural with academics has helped to shed light on learning and transmission (Herrmann et al. 2007; numerous topics in primatology and evolutionary Wobber et al. 2014). anthropology. Additionally, over the past 10 years, research in PASA wildlife centers has reinvigorated the study Scientific Findings from PASA Member of ape cooperation, sharing, and helping (Melis Sanctuaries et al. 2006a, b; Warneken et al. 2007; Melis et al. Research in PASA member sanctuaries has 2009; Hare & Kwetuenda 2010; Bullinger et al. helped to elucidate the evolutionary roots of 2011; Melis et al. 2011; Rekers et al. 2011; Schneider human cognition through large-scale comparisons et al. 2012; Tan & Hare 2013; Bullinger et al. 2014; of how human children and apes solve different Engelmann et al. 2015; Engelmann & Herrmann kinds of problems. Studies directly comparing 2016). This work has shown that chimpanzees, in the performance of chimpanzees, bonobos, and particular, are incredibly sophisticated at working Pan African Sanctuary Alliance / 63 together to gain mutual benefits (Meliset al. CONCLUSION 2006a, b; Melis et al. 2009). Moreover, they help others solve their own problems; for example, by Although PASA and its member sanctuaries providing conspecifics with access to out-of-reach may be known primarily as animal welfare objects or food (Warneken et al. 2007; Melis et al. organizations, they also play a vital role in the 2011). This work has also revealed an important conservation of, and research on, African primates. difference between how chimpanzees and humans If you are interested in learning more about PASA’s cooperate. Whereas humans tend to want to solve programs, how you can help, or opportunities to problems together, chimpanzees often prefer to conduct research at a PASA-member sanctuary, solve problems individually unless they absolutely please visit https://www.pasaprimates.org. need a partner (Melis et al. 2006a; Bullinger et al. 2011; Rekers et al. 2011). ACKNOWLEDGEMENTS Recent work in sanctuary populations has also been critical for our understanding of bonobos We thank Brian Hare for providing us with in comparison to chimpanzees. Bonobos and information on noteworthy research projects chimpanzees are both equally related to humans, conducted at PASA-member sanctuaries. and yet bonobos’ relative rarity means that most models of human evolution focus exclusively on chimpanzees. Research in PASA wildlife centers LITERATURE CITED has provided a major wave of evidence that chimpanzees and bonobos often differ in how Bullinger, A. F., A. P. Melis & M. Tomasello. 2011. they behave socially (Hare et al. 2007; Wobber, Chimpanzees, Pan troglodytes, prefer individual Wrangham et al. 2010; Woods & Hare 2011), make over collaborative strategies towards goals. decisions (Rosati & Hare 2012a; Rosati & Hare Animal Behaviour 82(5): 1135-1141. 2013), remember spatial locations (Rosati & Hare Bullinger, A. F., A.P. Mellis & M. Tomasello. 2014. 2012b; Rosati 2015), and even react hormonally Chimpanzees (Pan troglodytes) instrumentally to different situations (Wobber, Hareet al. 2010; help but do not communicate in a mutualistic Wobber et al. 2013). Furthermore, non-invasive cooperative task. Journal of Comparative biological samples collected from apes living at Psychology 128(3): 251. sanctuaries have allowed researchers to map the Engelmann, J. M. & E. Herrmann. 2016. bonobo genome, reconstruct the evolutionary Chimpanzees trust their friends. Current Biology history of chimpanzees and bonobos, and identify 26(2): 252-256. genetic differences in these species (Prüferet al. Engelmann, J. M., E. Herrmann & M. Tomasello. 2012). 2015. Chimpanzees trust conspecifics to engage Finally, research in sanctuaries has revealed in low-cost reciprocity. Proceedings of the new insights about the course of human evolution. Royal Society of London B: Biological Sciences Humans exhibit several special traits compared 282(1801): 20142803. to other primates, such as a large brain and more Hare, B. & S. Kwetuenda. 2010. Bonobos voluntarily frequent reproduction. A comparative study on share their own food with others. Current Biology energy expenditure showed that humans have a 20(5): R230-R231. higher metabolic rate than other apes, helping to Hare, B., A.P. Melis, V. Woods, S. Hastings & R. explain how humans evolved these energetically- Wrangham. 2007. Tolerance allows bonobos to costly traits (Pontzer et al. 2016). One proposal about outperform chimpanzees on a cooperative task. this energetic shift in human history is Richard Current Biology 17(7): 619-623. Wrangham’s influential “cooking hypothesis,” Herrmann, E., J. Call, M. V. Hernández-Lloreda, arguing that a early adoption of a high-energy B. Hare & M. Tomasello. 2007. Humans have cooked diet played a critical role in our species’ evolved specialized skills of social cognition: ability to grow such large brains (Wrangham 2009). The cultural intelligence hypothesis.Science Research in PASA sanctuaries has revealed that 317(5843): 1360-1366. chimpanzees possess some foundational cognitive Melis, A.P., B. Hare & M. Tomasello. 2006a. and behavioral skills needed to engage in cooking Chimpanzees recruit the best collaborators. behaviors, providing important behavioral tests of Science 311(5765): 1297-1300. this hypothesis (Wobber et al. 2008; Warneken & Melis, A.P., B. Hare & M. Tomasello. 2006b. Rosati 2015). Engineering cooperation in chimpanzees: 64 / Stokes et al.

tolerance constraints on cooperation. Animal London B: Biological Sciences. rspb20121948. Behaviour 72(2): 275-286. Tan, J., & B. Hare. 2013. Bonobos share with Melis, A.P., B. Hare & M. Tomasello. 2009. strangers. PLoS One 8(1): e51922. Chimpanzees coordinate in a negotiation game. Warneken, F., B. Hare, A. P. Melis, D. Hanus & Evolution and Human Behavior 30(6): 381-392. M. Tomasello. 2007. Spontaneous altruism by Melis, A. P., F. Warneken, K. Jensen, A. C. Schneider, chimpanzees and young children. PLoS Biology J. Call & M. Tomasello. 2011. Chimpanzees help 5(7): e184. conspecifics obtain food and non-food items. Warneken, F., & A.G. Rosati (2015). Cognitive Proceedings of the Royal Society of London B: capacities for cooking in chimpanzees. Biological Sciences 278(1710): 1405-1413. Proceedings of the Royal Society of London B: Pontzer, H., M. H. Brown, D. A. Raichlen, H. Biological Sciences 282: 20150229. Dunsworth, B. Hare, K. Walker, A. Luke, L.R. Wobber, V., B. Hare, S. Lipson, R. Wrangham & P. Dugas, R. Durazo-Arvizu, D. Schoeller, J. Plange- Ellison. 2013. Different ontogenetic patterns of Rhule, P. Bovet, T.E. Forrester, E.V. Lambert, testosterone production reflect divergent male M.E. Emery Thompson & R.W. Schumaker. reproductive strategies in chimpanzees and 2016. Metabolic acceleration and the evolution bonobos. Physiology & Behavior 116: 44-53. of human brain size and life history. Nature 533: Wobber, V., B. Hare, J. Maboto, S. Lipson, R. 390-395. Wrangham & P. T. Ellison. 2010. Differential Prüfer, K., K. Munch, I. Hellmann, K. Akagi, J.R. changes in steroid hormones before competition Miller, B. Walenz, S. Koren, G. Sutton, C. Kodira, in bonobos and chimpanzees. Proceedings of the R. Winer & J.R. Knight, 2012. The bonobo National Academy of Sciences 107(28): 12457- genome compared with the chimpanzee and 12462. human genomes. Nature 486 (7404): 527-531. Wobber, V., B. Hare & R. Wrangham. 2008. Great Rekers, Y., D. B. Haun & M. Tomasello. 2011. apes prefer cooked food. Journal of Human Children, but not chimpanzees, prefer to Evolution 55(2): 340-348. collaborate. Current Biology 21(20): 1756-1758. Wobber, V., E. Herrmann, B. Hare, R. Wrangham Rosati, A. G. & B. Hare. 2012a. Decision making & Tomasello, M. 2014. Differences in the early across social contexts: competition increases cognitive development of children and great preferences for risk in chimpanzees and bonobos. apes. Developmental Psychobiology 56(3): 547- Animal Behaviour 84(4): 869-879. 573. Rosati, A. G. & B. Hare. 2012b. Chimpanzees and Wobber, V., R. Wrangham, & B. Hare. 2010. Bonobos bonobos exhibit divergent spatial memory exhibit delayed development of social behavior development. Developmental Science 15(6): 840- and cognition relative to chimpanzees. Current 853. Biology 20(3): 226-230. Rosati, A. G. & B. Hare. 2013. Chimpanzees and Woods, V., & B. Hare. 2011. Bonobo but not bonobos exhibit emotional responses to decision chimpanzee infants use socio-sexual contact outcomes. PLoS One 8(5): e63058. with peers. Primates 52(2): 111-116. Rosati, A. G. 2015. Context influences spatial Wrangham, R. 2009. Catching fire: How cooking frames of reference in bonobos (Pan paniscus). made us human. Basic Books, New York. Behaviour 152(3-4): 375-406. Schneider, A. C., A. P. Melis & M. Tomasello. 2012. How chimpanzees solve collective action Received: 30 March 2017 problems. Proceedings of the Royal Society of Accepted: 31 March 2017 African Primates 12: 65-67 (2017)/ 65 Brief Communication:

Extending the Northeastern Distribution of Mandrills (Mandrillus sphinx) into the Dja Faunal Reserve, Cameroon

Madeleine Ngo Bata1, Julian Easton¹, Oliver Fankem¹, Tim Wacher2, Tom Bruce1, Tchana Eliseé¹, Pierre Augustin Taguieteu¹, and David Olson1

1Zoological Society of London - Cameroon, Yaoundé, Cameroon; 2Zoological Society of London - London, United Kingdom

Mandrills (Mandrillus sphinx, Linnaeus, 2 km apart in a square grid pattern, was in place 1758) are restricted to forests of the Atlantic for approximately 3,725 trap days for a wildlife Equatorial Forests Ecoregion, eastern portions survey in late 2015 and early 2016. All cameras of the Northwestern Congolian Lowland Forest were in primary tropical lowland rainforest. Two Ecoregion, and northern portions of the Western cameras (C11 at N3.2621 E12.83306 and C39 at Congolian Forest-Savanna Mosaic Ecoregion of N3.17567 E12.81618) photographed a single mature Central Africa (Olson et al. 2001; Oates & Butynski male mandrill on March 1, 2016 and April 9, 2016 2008). The species distribution is imperfectly (Figure 1). It is not known if they are different males known, especially the northeastern limits of its or the same individual and if groups of mandrills, estimated range. Here we report on the presence in addition to wandering males, also occur east of of mandrills in the northwestern region of the the Dja River. The two locations were 10.5 km apart. Dja Faunal Reserve in south-central Cameroon, a Each camera took six sequential images of each protected area with no known published records animal within six seconds (Figure 1). for this species. Given the clear documentation of mandrills east We found no published records after evaluating of the Dja River presented here, we recommend the available surveys and faunal lists for the reserve primary distribution for the species of Oates and (specifically, Bergmans 1994; Lejoly 1995; Butynski (2008) and Abernethy and White (2013) Williamson & Usongo 1995; Nzooh Dongmo 1999; be extended to encompass the new localities. MINFOF/IUCN 2015; GBIF 2016) and no reports through consultations with specialists who had worked within the reserve for several years (T. ACKNOWLEDGEMENTS Smith, pers. comm. 2016). The current IUCN Red List description states mandrills are not known east We are grateful for permission and collaboration of the Dja River (Oates & Butynski 2008). on this project from the Ministère des Forêts et de la This new locality documents the species in the Faune (MINFOF), the Conservator of the Dja Faunal northwest sector of the Dja Faunal Reserve (which Reserve, the Ecoguards who assisted with camera lies entirely east of the Dja River) and extends the placement, and retrieval, and the Government of IUCN Red List primary range map approximately the Republic of Cameroon. We thank E. Milnes for 20 km towards the northeast (Oates & Butynski research assistance and F. Maisels and K. Abernethy 2008). for technical review. We thank two anonymous An array of 40 infrared-triggered trail cameras reviewers for their helpful contributions. (Bushnell Trophy Cam Aggressor), each roughly

Correspondence to: Madeleine Ngo Bata, Zoological Society of London - Cameroon, Yaoundé, Cameroon; Phone: +237 676969242; E-mail: [email protected]. 66 / Bata et al.

Figure 1. Male mandrills photographed by two infrared trail cameras in the Dja Faunal Reserve, Cameroon. The black dots on the range map show the approximate location of cameras that documented mandrills. The dark shade represents the IUCN Red List distribution of the mandrill and protected areas are shown in light shade. The disjunct range polygon to the north of the Dja Reserve is likely an error (F. Maisels & K. Abernethy, pers. comm. 2016; range map source: Oates & Butynski 2008). The lower map shows the approximate location of the camera trap grid used in the survey with the cameras that photographed mandrills shown in circles. Extending the Distribution of Mandrills / 67 LITERATURE CITED Réserve de Biosphère du Dja et ses environs (Cameroun). Volumes 1 & 2. MINEF–ECOFAC, Abernethy, K.A. & L.J.T. White. 2013. Mandrillus Brussels. sphinx Mandrill, In Mammals of Africa: Oates, J.F. & T.M. Butynski. 2008. Mandrillus sphinx. Primates. Butynski, T., J. Kingdon, J. Kalina, The IUCN Red List of Threatened Species 2008: eds. Bloomsbury, London, New Delhi, New e.T12754A3377579. http://dx.doi.org/10.2305/ York, Sydney. Pp. 192-196. IUCN.UK2008.RLTS.T12754A3377579.en. Bergmans, W. 1994. Liste provisoire des Mammifères Downloaded on 22 October 2016. de la Réserve de faune du Dja et de sa périphérie. Olson, D., E. Dinerstein, E.D. Wikramanayake, Rap. Comité Néerlandais pour l’UICN. IUCN, N.D. Burgess, G.V.N. Powell, E.C. Underwood, Amsterdam, Netherlands. J.A. D’Amico, H.E. Strand, J.C. Morrison, GBIF. 2016. Global Biodiversity Information C.J. Loucks, T.F. Allnutt, J.F. Lamoreux, T.H. Facility. http://www.gbif.org/occurrence/ Ricketts, I. Itoua, W.W. Wettengel, Y. Kura, search?TAXON_KEY=5219555&q=dja. P. Hedao, & K. Kassem. 2001. Terrestrial Accessed on November 1, 2016. ecoregions of the world: A new map of life on Lejoly, J. 1995. Biodiversité des ligneux sur le Earth. BioScience 51: 933-938. transect d’Alat Makay dans la réserve de faune Williamson, E. & L. Usongo. 1995. Réserve de du Dja (Cameroun). Rapport technique, Projet faune du Dja: recensement des populations de ECOFAC, AGRECO. ECOFAC, Brussels. primates et inventaire des grands mammifères. MINFOF/IUCN. 2015. Caractérisation de la ECOFAC, Brussels. population de grands et moyens mammifères dans la Reserve de Faune du Dja: Potentiel et menaces. MINFOF/IUCN, Yaoundé, Cameroon. Received: 3 December 2016 Nzooh Dongmo, Z.L. 1999. Dynamique de la faune Accepted: 16 December 2016 sauvage et des activités anthropiques dans la 68 / Alberts & Rubenstein Obituary:

Stuart A. Altmann, Ph.D. (8 June 1930 - 13 October 2016)

by Susan C. Alberts1 and Daniel I. Rubenstein2

1Departments of Biology and Evolutionary Anthropology, Duke University, Durham, NC, USA; 2Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

Stuart Altmann was born in St. Louis, Missouri and grew up in Los Angeles, California. Left: Stuart Altmann in 1964, during the He was both a scientist and an Altmanns’ first trip to Amboseli. artist, working as a biologist Below: Stuart Altmann collecting data for his professional life and on yellow baboons (Papio cynocephalus), pursuing ceramics expertly as Amboseli, circa 1975. Photographs an avocation. courtesy of Jeanne Altmann. His formal scientific training began at University of California, Los Angeles (UCLA), where he first completed a Bachelor’s degree and then a Master’s degree in Biology in 1953. He studied under George Bartholomew, researching the mobbing behavior of birds. He was drafted into the Army and served from 1954 to 1956 as a research scientist at Walter Reed Army Medical Center. At the end of his army service, he hitched a ride to Panama on army transport planes and used his carefully accumulated leave time to study the Barro still commonly cited in the twenty-first century, Colorado howler monkeys, publishing a paper that and Altmann’s “priority of access” model has greatly is still cited today for its descriptions of primate influenced subsequent work on the relationship vocalizations. He attended Harvard University between dominance rank and mating success in between 1956 and 1960 as E. O. Wilson’s first Ph.D. male mammals. student, adopting a decidedly sociobiological What set Altmann apart from his peers was perspective that he and Wilson developed in his ability to frame problems conceptually, use extensive conversations comparing primates and mathematical models to make strong predictions social insects. He conducted his Ph.D. research on and then draw on his natural history insights and the rhesus macaques on Cayo Santiago in Puerto systematic observations to test them. What emerged Rico, while he was revitalizing and managing the was a new way of thinking and framing of behavioral colony under the sponsorship of W. F. Windle at the questions. His quantitative approach transformed National Institutes of Health (NIH). the study of primate behavior. In addition, in an This research, motivated by his interest in era when interest in behavior as an adaptation communication, produced a series of papers was burgeoning, Altmann set high standards for between 1962 and 1968 that represent a seminal a very detailed understanding of the functional contribution to primate behavioral ecology. The consequences of behaviors such as foraging, and of first of these analyzed reproductive behavior; it is how we evaluate adaptation in nature. Stuart A. Altmann / 69

Stuart Altmann with Jeanne Altmann, in Amboseli circa 1987. Photo by O. Douglas-Hamilton, courtesy of J. Altmann.

In the summer of 1958, he met his future wife Jeanne when they were both working for the NIH, and they married in 1959. He began his first faculty position at the University of Alberta in 1960, and moved to Yerkes National Primate Research Center in 1965. In 1970, he moved to a joint appointment in the Biology Department (which later became the Department of Ecology and Evolution) and the Anatomy Department at the University of Chicago. He became Emeritus Professor at University of Chicago in 1995, and beginning in 1998 was a Senior Lecturer at rank of Professor in the Department of Ecology and Evolutionary Biology at Princeton University. In 1963–64, Stuart and Jeanne Altmann made their first trip to what was then the Amboseli- Maasai Game Reserve, later Amboseli National Park, in southern Kenya, to study the Amboseli baboons. They returned to Amboseli for short trips in 1969 and 1970. In 1971, they returned again, and began collecting the longitudinal data on the Amboseli baboon population that is still being collected today. The establishment of the Amboseli research site proved to be a foundational contribution to the study of primates. The research at this site continues to provide new knowledge Stuart trimming a pot on his wheel, early 2000s. and insights about primate behavior and 70 / Alberts & Rubenstein

evolution, 54 years after Stuart and Jeanne arrived in Altmann, S.A. 1979. Baboon progressions: order Amboseli and 46 years after the establishment of the or chaos? A study of one-dimensional group long-term research. geometry. Animal Behaviour 27: 46-80. Stuart was a mentor and friend to us and to Altmann, S.A. 1981. Dominance relationships: the many others. Through both his science and his art, Cheshire cat’s grin. Behavioral and Brain Sciences he influenced so many lives in complex, unexpected, 4: 430-431. and remarkable ways. He is deeply missed, and will Hausfater, G., J. Altmann & S. Altmann. 1982. Long- always be with us in spirit. Term Consistency of Dominance Relations Among Female Baboons (Papio cynocephalus). A selection of Stuart Altmann’s publications Science 217: 752-755. Altmann, J., G. Hausfater & S.A. Altmann. 1985. Altmann, S.A. 1958. How to predict what an animal Demography of Amboseli baboons, 1963-1983. will do next. Anatomical Record 131: 527-527. American Journal of Primatology 8: 113-125. Altmann, S.A. 1962. A field study of the sociobiology Altmann, S.A., D.G. Post & D.F. Klein. 1987. of rhesus monkeys, Macaca mulatta. Annals of Nutrients and toxins of plants in Amboseli, the New York Academy of Sciences 102: 338-435. Kenya. African Journal of Ecology 25: 279-293. Altmann, S.A. 1965. The sociobiology of rhesus Altmann, S.A. 1987. The impact of locomotor monkeys. 2. Stochastics of social communication. energetics on mammalian foraging. Journal of Journal of Theoretical Biology 8: 490-522. Zoology 211: 215-225. Altmann, S.A. 1968. The sociobiology of rhesus Welsh, A.H., A.T. Peterson & S.A. Altmann. 1988. monkeys. 3. Basic communication network. The fallacy of averages.American Naturalist 132: Behaviour 32: 17-32. 277-288. Altmann, S.A. 1968. The sociobiology of rhesus Muruthi, P., J. Altmann & S. Altmann. 1991. Resource monkeys. 4. Testing Mason’s hypothesis of sex base, parity, and reproductive condition affect differences in affective behaviour.Behaviour 32: females’ feeding time and nutrient intake within 49-69. and between groups of a baboon population. Altmann, S.A. & J. Altmann. 1970. Baboon Ecology. Oecologia 87: 467-472. University of Chicago Press, Chicago. Altmann, S.A. 1991. Diets of yearling female Altmann, S.A. 1974. Baboons, space, time, and primates (Papio cynocephalus) predict lifetime energy. American Zoologist 14: 221-248. fitness. Proceedings of the National Academy of Altmann, S.A. & J. Altmann. 1977. On the analysis Sciences of the United States of America 88: 420- of rates of behaviour. Animal Behaviour 25: 364- 423. 372. Altmann, S.A. 1998. Foraging for Survival. University Altmann, S.A., S.S. Wagner & S. Lenington. 1977. of Chicago Press, Chicago. Two models for the evolution of polygyny. Altmann, S.A. & J. Altmann. 2003. The Behavioral Ecology and Sociobiology 2: 397-410. transformation of behaviour field studies. Animal Altmann, J., S.A. Altmann & G. Hausfater. 1978. Behaviour 65: 413-423. Primate infant’s effects on mother’s future Altmann, S.A. 2009. Fallback foods, eclectic reproduction. Science 201: 1028-1030. omnivores, and the packaging problem. Altmann, S.A. 1979. Altruistic behavior: the fallacy American Journal of Physical Anthropology 140: of kin deployment. Animal Behaviour 27: 958- 615-629. 959. African Primates 12:71-73 (2017)/ 71 Obituary:

Deborah L. Moore, Ph.D. (8 October 1964 - 22 March 2016)

by Gráinne McCabe1 and Carolyn Ehardt2

1Institute of Conservation Science & Learning, Bristol Zoological Society, Clifton, Bristol, UK; 2Department of Anthropology, University of Texas at San Antonio, Texas, USA

Deborah L. Moore lost her six-year battle with cancer on 22 March 2016, at age 51. With her passing, the primatological community has lost a professional who had, in her all too brief career, contributed in exceptional ways to our understanding of Africa’s great apes, while seeking to translate scientific study to effective conservation for these highly threatened primates. Born in Montreal, Quebec, Canada, Deb pursued undergraduate training in biological anthropology at Georgia State University, completing a comparative paleoanthropological honor’s thesis examining hominin skeletal morphology with Frank Williams. It was post her BA degree that she first honed and focused her professional interest on the behavioural ecology of chimpanzees, participating in a multi- year research project at the Yerkes National Primate Research Center in association with Drs. Frans de Waal and Kristin Bonnie. Inspired to pursue behavioural ecology research with chimpanzees in Africa and motivated to effectively merge field- based ecological study with conservation, Deb Deborah Moore in Ugalla, Tanzania. began pursuit of a Ph.D. at the University of Georgia, working with Carolyn L. Ehardt in the Department they also represented opportunity to investigate of Anthropology’s focused doctoral program in how a population living under significant resource Environmental and Ecological Anthropology. constraints and exhibiting exceptionally large home Transferring to the University of Texas at San ranges could differ in their socioecology from Antonio with Ehardt to become one of the original the more traditionally studied forest populations. cohort in UTSA’s new Ph.D. program in Ecological Faced with addressing fundamental questions of Anthropology, Deb began to formulate a dissertation population demography and behavioural ecology, project which would take her to the savanna- such as the stability of male philopatric community woodlands of the Ugalla region of western Tanzania structure, in such an unusual and non-habituated to investigate the population of Endangered Pan population, Deb turned to non-invasive, innovative troglodytes schweinfurthii in this environment, one application of genetic analysis of systematically of the most seasonal, dry, and open of chimpanzee collected fecal samples. Through demanding field habitats. work (during which she first detected the cancer The Ugalla chimpanzees, at the easternmost that would ultimately take her life) and genetic range of this subspecies, are not only an important analyses in collaboration with Linda Vigilant in population for the conservation of the species, the Department of Primatology at Max Planck 72 / McCabe & Ehardt

Deborah Moore searching for chimpanzees in Ugalla, western Tanzania.

Institute for Evolutionary Anthropology in Leipzig, Deb is and will be greatly missed by all who knew Germany, Deb’s research revealed the efficacy of her her and had the privilege of working with her. To innovative techniques and approach in revealing share some of those personal remembrances: environmentally-stable aspects of socioecology, and contributed valuable data for the Ugalla From Gráinne McCabe: chimpanzees with direct application to conservation of this important and exceptional population. I first met Deborah in the Caribbean lowlands Following receipt of her Ph.D. in 2013, Deb of northwestern Costa Rica in the summer of 2005. began postdoctoral association with the Bonobo At the time, she was finishing up her undergraduate Conservation Initiative as a Research Associate and degree at Georgia State University, planning to became one of the very first scientists to work with pursue a PhD in the near future. It was my first time the bonobo population at the Kokolopori Bonobo as a teaching assistant on a field course and one of Reserve in the Democratic Republic of Congo. Deb’s first experiences studying primates in the wild; Excited about this opportunity to again contribute to an experience that got her hooked. conservation science for highly threatened primates, We didn’t meet up again until the fall of 2007 and despite the challenges of the field site (echoing when we bumped into one another in the hallway what she overcame at Ugalla), she initiated protocols of Baldwin Hall at University of Georgia. Two to guide the work, only to again be stricken by cancer. brand new PhD students about to embark on a Forced to return home to Canada, Deb exhausted rollercoaster adventure together across several every avenue to combat the recurrence and continue states and continents: from Athens, Georgia to with the research that so highly motivated her as the San Antonio, Texas to the forests of Tanzania. The professional and exceptionally caring person who journey would be filled with many highs and lows, was admired and cared about by all of her friends, great accomplishments and inevitable failures, family, and colleagues around the world. Deborah L. Moore / 73 and thankfully for me it resulted in an incredible A selection of Deborah Moore’s publications friendship as well. Deb will be deeply missed by all who knew Rudicell, R.S., A.K. Piel, F. Stewart, D.L. Moore, G.H. her. In her honour, we have established the Dr Learn, Y. Li, J. Takehisa, L. Pintea, G.M. Shaw, Deborah Moore Memorial Grant for Early Career J. Moore & P.M. Sharp. 2011. High prevalence Primatologists, which will be hosted by the American of simian immunodeficiency virus infection in a Society of Primatologists. This grant will be for community of savanna chimpanzees. Journal of researchers that have recently completed their PhDs Virology 85(19): 9918-9928. but have not yet acquired full-time employment in Moore, D.L. 2013. Genetic investigation of an academia. If you wish to donate to the fund, please unhabituated, savanna-woodland chimpanzee see https://www.crowdrise.com/o/en/campaign/ (Pan troglodytes schweinfurthii) population in annual-dr-deborah-moore-memorial-grant-for- Ugalla, western Tanzania. The University of early-career-primatologists. Texas at San Antonio. Moore, D.L. & L. Vigilant. 2014. A population From Carolyn Ehardt: estimate of chimpanzees (Pan troglodytes schweinfurthii) in the Ugalla region using It was a privilege to have been part of Deb’s standard and spatially explicit genetic capture– journey from student to professional colleague, recapture methods. American Journal of and to know her as the motivated, dedicated, Primatology 76(4): 335-346. joyful person she was throughout all phases of that Moore, D.L. & L. Vigilant. 2014. Genetic diversity journey. As Deb’s research demonstrated, she had at the edge: comparative assessment of much to contribute to advancing our knowledge Y-chromosome and autosomal diversity of highly threatened primates, including posing in eastern chimpanzees (Pan troglodytes seminal questions that only could be addressed schweinfurthii) of Ugalla, Tanzania. Conservation through innovative and difficult approaches, free of Genetics 15(3): 495-507. the risks sometimes attendant to more traditional Moore, D.L., K.E. Langergraber & L. Vigilant. 2015. research strategies. We regret the loss of those Genetic analyses suggest male philopatry and certain future contributions to the understanding territoriality in savanna-woodland chimpanzees and conservation of African primates. I also know (Pan troglodytes schweinfurthii) of Ugalla, that a number of colleagues admired and respected Tanzania. International Journal of Primatology how she handled the sometimes unpleasant 36(2): 377-397. ‘quagmires’ that can accompany pursuit of research, Tokuyama, N., D.L. Moore, K.E. Graham, A. especially in a field where competitiveness can over- Lokasola & T. Furuichi. 2016. Cases of maternal shadow collaborative advancement of knowledge. cannibalism in wild bonobos (Pan paniscus) Always the professional, she placed the science and from two different field sites, Wamba and the long-term welfare of the animals first. For all of Kokolopori, Democratic Republic of the Congo. these reasons, she will be deeply missed. Primates 58(1): 7-12. 74 / de Jong & Butynski Photographic Maps for the Primates, Warthogs, Dik-diks, and Hyraxes of Africa

Yvonne A. de Jong and Thomas M. Butynski Eastern Africa Primate Diversity and Conservation Program & www.wildsolutions.nl Lolldaiga Hills Research Programme

The design and implementation of effective conservation measures for primates, warthogs, dik-diks, and hyraxes requires an efficient, low cost, and accessible resource for the identification of species and subspecies. Although photographs cannot replace an adequate museum collection as a resource for assessing species variation, geotagged photographs are a relatively fast, inexpensive, convenient, and unobtrusive means for detecting and assessing phenotypic variation within a species/subspecies over large areas. The use of photographs to document phenotypic characters will become increasingly important as the collection of specimens for hands-on assessments becomes ever more difficult.

Our 15 newly up-graded on-line photographic maps (or ‘PhotoMaps’; wildsolutions.nl), with over 3165 images (November 2017) of African primates, warthogs, dik-diks, and hyraxes, together with the latest distribution maps, provide insight into each taxon’s phenotypic characters, diversity and biogeography. These ‘living’ collections of geotagged images are a practical tool for documenting and discussing diversity, taxonomy, biogeography, distribution and conservation status and, therefore, for planning actions for conservation. The 15 PhotoMaps at wildsolutions.nl

PhotoMaps are useful to those who want to: • identify species/subspecies; • know which species/subspecies occur in which areas; • obtain species/subspecies photographs; PhotoMaps are • confirm species/subspecies distribution; free-access at: • describe variation within a species/subspecies, especially as it relates to geographic distribution. wildsolutions.nl PhotoMaps for East African Primates / 75

Gentle monkey, Cercopithecus mitis, PhotoMap provided by wildsolutions.nl

If you have photographs of African primates, warthogs, dik-diks, or hyraxes from the less documented areas of Africa (i.e., gaps on the PhotoMaps), please consider contributing them to the PhotoMaps. The photographers name is attached to each photograph. Anyone wishing to use a PhotoMap photograph must obtain both permission and the photograph from the photographer. Send your photographs, and the coordinates and/or place name Juvenile and subadult Kolb’s monkeys, Cercopithecus of the site where the photographs were mitis kolbi, in Aberdares National Park, Kenya. obtained, to [email protected]. Besides PhotoMaps, the website of the Eastern Africa Primate Diversity and Conservation Program (wildsolutions.nl) hosts the ‘Vocal Profiles for the Galagos’, a joint initiative with the Nocturnal Primate Research Group, blogs, primate and warthog videos, project information, and publications by Thomas M. Butynski and Yvonne A. de Jong.

We thank Arnoud de Jong for his technical expertise and great help Adult male eastern patas monkey, Erythrocebus patas pyrrhonotus, in Kidepo Valley National Park, with the PhotoMaps. Uganda. 76 / Laurance

I would like to introduce the primatology community to We use a range of social-media outlets to increase ALERT—an international scientific and environmental- 6our impact, including our website, Facebook, and advocacy group run entirely by leading scientists and Twitter. We pay a part-time social-media strategist to environmental journalists. design and update our social-media outlets, and a part- time environmental journalist to help us deal with the I founded ALERT in 2013 after spending some two decades rapidly growing volume of material we receive at ALERT. trying to help major scientific organisations—including the Association for Tropical Biology and Conservation and We do not shy away from controversial issues. We the Society for Conservation Biology—to become more 7openly advocate for nature conservation while engaged in real-world conservation issues. For various carefully maintaining our scientific credibility. reasons my earlier efforts with traditional scientific organisations were met with mixed success. Still, since Our blogs are written in a simple and engaging its inception in late 2013, ALERT has grown dramatically 8manner, so they are easily readable by anyone. and now reaches a million or more informed readers worldwide each week. We are closely plugged into the broader 9conservation and NGO communities, so are very The following 12 factors have made ALERT successful: well informed about timely and emerging conservation issues. Scientific organisations typically generate only a few 1resolutions or declarations on conservation issues In advocating for environmental conservation per year. ALERT runs 1–2 major blogs per week and 10we try to build a ‘broad church’, working with we produce a number of press releases annually on groups dealing with indigenous peoples, environmental particularly urgent issues. economics, and social-justice issues, so that our blogs and campaigns appeal to a large segment of society, not Most actions by scientific organisations are just ‘greenies’. 2produced far too slowly to respond to fast-changing environmental concerns. This tends to limit them to ALERT is completely free; we charge no dues addressing long-term problems but not the many specific, 11or membership fees. ALERT’s efforts are fully real-world challenges, such as fast-moving development supported by external grants from scientific and projects, which can be a grave and direct threat to nature philanthropic donors. conservation. ALERT has a broad global focus. Although most of In my experience some members of traditional 12our initiatives and campaigns focus on terrestrial 3scientific groups do not understand the inherently environments, we work on many issues of conservation political nature of many conservation issues. This importance. Key foci include emerging environmental slows and complicates their efforts to produce timely threats, tropical forests, developing nations, Australasia, conservation initiatives. ALERT’s core members, climate change, conservation policy, endangered species however, are world-leading conservation scientists or and the drivers of land-use change. environmental journalists who understand and accept these political realities. Joining ALERT is easy. Simply visit our website and insert your email into the box at the top of the page. ALERT is very much connected to the journalistic world. 4Our press releases reach over 800 environmental Becoming an ALERT member is an excellent way to track journalists worldwide and we have invested considerable key trends and stay on top of the rapidly changing world effort in compiling and automating this distribution list. of nature conservation and environmental sustainability.

Many of our blogs are translated into Spanish and 5Portuguese by allied websites in Latin America, and some are translated into French by another allied William F. Laurance website in Europe. Many overseas members actually College of Science and Engineering, read the English version but comment in their native James Cook University language. African Primates 12 (2017) / 77 What is the Nagoya Protocol and How Does it Affect Your Research? The Nagoya Protocol on Access and Benefits resources and traditional knowledge associated with Sharing is part of the international treaty known biodiversity, the Protocol provides incentives for as the Convention on Biological Diversity (CBD). both conservation and research. The CBD was opened for signature at the 1992 The Nagoya Protocol has been ratified by nearly Earth Summit in Brazil, and entered into force in 100 countries, including many UN member states 1993. The Nagoya Protocol is a and the European Union. The US Supplementary Agreement to the has not ratified the Protocol, and CBD that was adopted in 2010. In hence is not a party to it. However, spite of the 17-year gap between because many countries worldwide the CBD and the Nagoya Protocol, are now parties to this treaty, the purpose of the Nagoya scientists who export biological Protocol – the fair and equitable materials from one country to sharing of benefits arising from another need to be cognizant of genetic resources – has been one the country-specific requirements of the goals of the CBD since its of the protocol, whether or not inception. their home country is a party to Aim and implementation of the it. Penalties for non-compliance in Nagoya Protocol. The aim of the the countries that are parties to the Nagoya Protocol is to ensure that treaty can be stiff. the benefits associated with genetic Most (not all) countries that resources, and also with traditional are home to nonhuman primates knowledge of biodiversity, are are parties to the Nagoya Protocol. shared fairly and equitably. The This means that in addition to the Protocol formalizes the idea that countries in research permits, collection permits, and CITES which genetic resources and traditional knowledge export permits that researchers already obtain, they originate should have the option of retaining some will also need to be compliant with the requirements rights over those resources and knowledge. Another of the Nagoya Protocol as implemented in the underlying principle of the Nagoya Protocol is the country where they conduct research. idea that Access and Benefits Sharing is critically Resources for learning more about the Nagoya important for conservation and for the sustainable Protocol. Researchers will find the following use of biodiversity. By providing countries with fair websites very useful in learning more about the and equitable access to benefits from the genetic Nagoya Protocol.

1. The Access and Benefit-Sharing Clearing-House (ABSCH) 3. Knowledge about the Nagoya Protocol is includes valuable general information about the highly variable across universities, museums, Nagoya Protocol, as well as detailed country-specific and captive primate facilities. Consider information. Under the ‘Country Profiles’ link, 198 contacting the central research administration countries are listed. Their status with respect to the office at your institution to learn what they Protocol is indicated (party versus non-party), as well as know, and what types of support they can each country’s national point of contact for information offer to researchers. If they are new to the about the protocol, the national authority that oversees Nagoya Protocol, you can give them the the implementation of the protocol, and a range of other information provided here, and also point useful information. them to the following link, with information https://absch.cbd.int/help/about on access and benefit sharing geared towards administrators. 2. The Convention on Biological Diversity, the umbrella https://scbd.unssc.org/course/ treaty under which the Nagoya Protocol falls, has a index.php?categoryid=4 comprehensive website with basic information, news links, updates, and program information. https://www.cbd.int/ Photo: C. Whittier/MGVP 78 / Announcement

27th INTERNATIONAL PRIMATOLOGICAL SOCIETY CONGRESS 19-25 AUGUST 2018 http://www.ipsnairobi.org/

The Congress theme is "Global Connectivity to Ensure the Future of Primates." Nairobi's central location in East Africa will offer primatologists from African range states the opportunity to attend.

Deadline for submission of oral, symposium, and poster presentation abstracts and Early Bird registration: January 5, 2018

The XXVII International Primatological Society (IPS) Congress will be held at the United Nations Office in Nairobi (UNON), Kenya. African Primates 12 (2017) / 79

Bioko Island Study Abroad Primate Field Schools in Study in Monkey Paradise! AFRICA The Bioko Island Study Abroad Program takes place in the Spanish-speaking central African country of Equatorial Guinea and is built upon the long term academic partnership between Drexel University, the Bioko Biodiversity Protection Program (BBPP), and the National University of Equatorial Guinea (UNGE). The island of Bioko is one of the most many European capitals. Moving south the beautiful and biologically-significant places in island becomes increasingly rural, devolving all of Africa. It is home to one of Africa's greatest into large swaths of undisturbed virgin rain concentrations of endangered primates forest. and to numerous unique species Drexel University’s Bioko Study of frogs, plants, insects, and Abroad Program includes many more species. During individual field research the dry season (November projects at the Moka Wildlife to February), butterflies Center in the southern gather in the rain forest highlands of Bioko, and endangered marine coursework at UNGE in turtles come ashore the capital city of Malabo, to nest on the black and additional fieldwork sand beaches. Nearly in the tropical forests, 200 species of birds fly mountains, lakes and amongst the island's beaches of Bioko Island. three volcanic peaks, To maintain the high level the highest almost 3000 of individualized study, the meters above sea level program is offered once (~ 10,000 ft). Located 20 yearly (January - March) miles (37 km) off the coast to a class of ten American of Cameroon in west central students. Africa, Bioko is a part of the African Drexel students registering for country of Equatorial Guinea. At Bioko's the course receive a full term of course northern tip is the country's capital city, Malabo credits. Students from other other institutions (population: 100,000), a city pulsing with receive a full term of Drexel credits that can petroleum wealth and easily accessible from usually be transferred to their home institutions.

For more information see:

• BBPP’s Website: www.Bioko.org • Bioko Study Abroad: https://studyabroad.drexel.edu/index.cfm?FuseAction=programs. ViewProgram&Program_ID=10116 • Video about Bioko Study Abroad: https://youtu.be/g4kkhbrKCGk • For questions, email Katy Gonder ([email protected]) or Hilton Oyamaguchi ([email protected]) Photo: Bioko red colobus monkey (Piliocolobus pennantii) in the Gran Caldera de Luba Scientific Reserve (by Ian Nichols). 80 / Field Schools & News

Primate Field Schools in AFRICA African Primates 12 (2017) / 81

Primate Field Schools in AFRICA

Field Projects International

The Wildlife of Uganda May 21-31, 2018

In this course, we’ll explore wildlife conservation in Uganda, focusing on chimpanzees and monkeys, as well as other megafauna including elephants, giraffes, lions, and crocodiles. We’ll be based in the Budongo Forest and explore several wildlife sites, include national parks, forest reserves, and wildlife sanctuaries. Lecture and group discussion topics will include: Course Instructor: Janette Wallis, Ph.D. • Animal Behavior & Ecology • Wildlife Management Application Deadline: • Community Conservation April 15, 2018 • Habitat Fragmentation For more information: • Human-Wildlife Conflict Field Projects International • Ecotourism https://fieldprojects.org/ course/uganda/#ffs-tabbed-11 Students will also learn basic skills in: data collection, [email protected] animal tracking, camera trapping, and GPS use/map-making. 82 / News and Announcements News

IPS Grants for Primate Work The International Primatological AuthorAID Travel Grants Society (IPS) has several grant and award programs. See the AuthorAID will award five travel grants (USD IPS web site for details about 1500 each) for early-career researchers conservation, research, captive to present their research at an academic care, and education grants conference. The application deadline is 3rd (be sure you submit applications of January 2018. http://www.authoraid.info/ to the grant program that fits your goal to en/news/details/1253/. maximize chances for funding). See http://www. internationalprimatologicalsociety.org. The next deadline for grant submissions: March 1, 2018. Primate Films Database Now Available! The Primate Films Database includes information Awards for Leadership in Conservation about films featuring wild primates produced since the beginning of the twentieth century. The database The annual National Geographic/Buffett Awards contains entries for films (including feature films), for Leadership in Conservation were established by TV specials, TV series, and single episodes of series. the Society and The Howard G. Buffett Foundation Currently the Primate Films Database focuses on to recognize and celebrate unsung heroes working films in which the main focus is on primates in in the field. Two awards are presented each year: wild settings, but it may be expanded in the future one for achievement in Africa (established in 2002) to include more films focusing on captive primates. and the other for achievement in Latin America The database includes general information about (established in 2005). each film such as runtime, the featured species, and Recipients of these awards have demonstrated the narrator or host. A brief review of each film is outstanding leadership in managing and protecting also provided which focuses on the film’s usefulness the natural resources in their regions and countries. in teaching and educational settings. In addition, they are each inspirational conservation This database was created specifically as a advocates who serve as role models and mentors. resource for educators, but it may also be useful to The awardees chosen each year are honored at a members of the general public with an interest in ceremony in Washington, D.C., and receive a one- primatology or nature documentaries. It could also time grant of $25,000 to support their ongoing work. be a valuable tool for researchers in primatology, Nominations are being accepted now through visual anthropology, and film studies. The database January 8, 2018, for the 2018 awards. Winners will be updated as new films are released. https:// will be announced in June. https://www. anthropology.artsci.wustl.edu/primate-films- nationalgeographic.org/awards/buffett. database.

The African Journal of Ecology will be publishing a themed issue on primates in June 2018 to coincide with the International Primate Society’s biennial congress in Nairobi, Kenya, in August 2018. The journal’s publisher, Wiley, has said that AJE can have a bumper issue packed with the most current research in the field’. Papers to be included in the issue should be submitted early in 2018 and will go through the journal’s normal review process. AJE publishes papers on ecology and conservation of indigenous African flora and fauna in three formats: Original Articles, Short Communications and Notes and Records. The journal does not publish papers on taxonomy or species inventories, though lists can be included in Supplementary Information.- - Jon Lovett and Katherine Abernethy http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2028 African Primates 12 (2017) / 83

IUCN SSC Primate Specialist Group’s

“Primates in Peril: The World’s Most Endangered Primates - 2016-2018”

Now available!

Pick up a hard copy at the Primate Specialist Group's table at IPS in Nairobi.

Or visit the Primate Specialist Group web site for a digital copy.

http://www.primate-sg.org/special_reports/

Colin P. Groves 24 June 1942 - 30 November 2017 Shortly before this issue of African Primates was finalized, we learned of the passing of our friend and colleague, Professor Colin Groves.

The next issue of African Primates will include a special tribute and obituary for this remarkable man, whose work helped shape the careers and research of so many primatologists.

Visit this page to view a celebration of Colin’s life and achievements: https://colingrovesmemorium. blog/2017/11/30/first-blog-post/#comments 84 / Recent Publications Recent Publications*

Abie, K., A. Bekele, & A. Sebbenn. 2016. American Journal of Primatology 79(3) 79: Threats to gelada baboon around Debre e22624. Libanos, Northwest Shewa Zone, Ethiopia. Deem, S. L. 2016. Conservation medicine: International Journal of Biodiversity Vol a solution-based approach for saving 2016, 7 pages. nonhuman primates. In M.T. Waller, ed. Ancrenaz, M., S. Wich, E. Meijaard, & J. Simery. Ethnoprimatology: Primate Conservation in 2016. Palm oil paradox: sustainable solutions the 21st Century. Springer, Switzerland. Pp. to save the great apes. UNEP/GRASP. 2016. 63-76. Ben Salem, N., F.H. Leendertz & B. Ehlers. 2016. Dunham, N.T. 2017. Feeding ecology and Genome sequences of polyomaviruses from dietary flexibility of Colobus angolensis the wild-living red colobus (Piliocolobus palliatus in relation to habitat disturbance. badius) and western chimpanzee (Pan International Journal of Primatology 38(3): troglodytes verus). Genome Announcements, 553–571. 13 October 2016, Vol.4(5). Dunham, N.T. & P. O. Opere. 2016. A unique Bobo, K.S., C.B. Ntumwel, F.F. Aghomo, & K.G. case of extra-group infant adoption in free- Aurele Ayemele. 2017. The conservation ranging Angola black and white colobus status of two threatened primates in the monkeys (Colobus angolensis palliatus). Korup Region, Southwest Cameroon. Primates 57(2): 187-194. Primate Conservation (31): Published Dunham, N.T. & A.L. Lambert. 2016. The role electronically prior to print. of leaf toughness on foraging efficiency in Bortolamiol, S., M. Cohen, F. Jiguet, F. Pennec, Angola black and white colobus monkeys A. Seguya, & S. Krief. 2016. Chimpanzee (Colobus angolensis palliates). American non‐avoidance of hyper‐proximity to Journal of Physical Anthropology 161(2): humans. Journal of Wildlife Management 343-354. 80(5): 924-934. Estrada et al. 2017. Impending extinction Brand, C.M., F.J. White, M.L. Wakefield, crisis of the world’s primates: Why primates M.T. Waller, M.J. Ruiz-López, & N. Ting. matter. Sci. Adv. 2017;3: e1600946. 2016. Initiation of genetic demographic Fedurek, P. & J. Lehmann. 2017. The effect of monitoring of bonobos (Pan paniscus) excluding juveniles on apparent adult olive at Iyema, Lomako Forest, DRC. Primate baboons (Papio anubis) social networks. Conservation 30: 103–111. PLoS ONE, Vol.12(3), p.e0173146. Butynski, T.M. & Y. A. de Jong. 2017. The Freeman, N.J., C. Young, L. Barrett & S.P. Henzi. Mount Kenya potto is a subspecies of the 2016. Coalition formation by male vervet Eastern Potto Perodicticus ibeanus. Primate monkeys (Chlorocebus pygerythrus) in South Conservation 31: Published electronically Africa. Ethology 122(1): 45-52. prior to print. Fujisawa, M., K.J. Hockings, A.G. Soumah, Carlson, B.A. & B.E. Crowley. 2016. Variation & T. Matsuzawa. 2016. Placentophagy in in carbon isotope values among chimpanzee foods at Ngogo, Kibale National Park and Bwindi Impenetrable National Park, Uganda. American Journal of Primatology * This is not an exhaustive list and focuses mostly 78(10): 1031-1040. on publications from peer-reviewed journals. To Chancellor, R.L., A. S. Rundus & S. Nyandwi. have your new publications listed in this section 2017. Chimpanzee seed dispersal in a of future African Primates, please send an e-mail montane forest fragment in Rwanda. notice to [email protected]. African Primates 12 (2017) / 85 Recent Publications

wild chimpanzees (Pan troglodytes verus) at Primatology, 07 April 2017. DOI: 10.1002/ Bossou, Guinea. Primates 57(2): 175-180. ajp.22661. Galbany, J., D. Abavandimwe, M. Vakiener, W. Goffe, A.S. & J. Fischer. 2016. Meat sharing Eckardt, A. Mudakikwa, F. Ndagijimana, T.S. between male and female Guinea baboons Stoinski & S.C. Mcfarlin. 2017. Body growth (Papio papio). Primate Biology 3(1): 1-8. and life history in wild mountain gorillas Habumuremyi, S., C. Stephens, K.A. Fawcett, T. (Gorilla beringei beringei) from Volcanoes Deschner & M.M. Robbins. 2016. Endocrine National Park, Rwanda. American Journal of assessment of ovarian cycle activity in wild Physical Anthropology 163(3): 570-590. female mountain gorillas (Gorilla beringei Gippoliti, S. 2017. On the taxonomy of beringei). Physiology & Behavior 157: 185- Erythrocebus with a re-evaluation of 195. Erythrocebus poliophaeus (Reichenbach, Haurez, B., N. Tagg, C.-A. Petre, C. Vermeulen 1862) from the Blue Nile Region of Sudan & J.-L. Doucet. 2016. Short term impact of and Ethiopia. Primate Conservation (31): selective logging on a western lowland gorilla Published electronically prior to print. population. Forest Ecology and Management Glowacka, H., S.C. Mcfarlin, E.R. Vogel, T.S. 364: 46-51. Stoinski, F. Ndagijimana, D. Tuyisingize, Hobaiter, C., L. Samuni, C. Mullins, W.J. A. Mudakikwa, & G.T. Schwartz. 2017. Akankwasa, & K. Zuberbühler. 2016. Toughness of the Virunga mountain gorilla Variation in hunting behaviour in (Gorilla beringei beringei) diet across an neighbouring chimpanzee communities in altitudinal gradient. American Journal of the Budongo forest, Uganda. PLoS ONE,

This online book was written as a tool for anyone interested in increasing the efficiency and success of future reintroductions and to improve the wellbeing of reintroduced primates. It provides information about 202 primate reintroduction programs involving almost 23,000 inidivdual prosimians, monkeys, and apes. For free access, go to: http://www.drbenjaminbeck.com/index.html 86 / Recent Publications Recent Publications

Vol.12(6), p.e0178065. Rothman. 2017. Macronutrient balancing Hockings, K.J. 2016. Chimpanzee behavioural affects patch departure by guerezas Colobus( flexibility and the sustainability of human- guereza). American Journal of Primatology chimpanzee interactions at Cantanhez 79(4): 1-9. National Park, Guinea-Bissau. Etnografica Jolly, C.J. & F.L. Brett. 2017. Genetic markers 20(3): 659-662. and baboon biology. Journal of Medical Hussein, I., B. Afework & Y. Dereje. 2017. Primatology 2(2): 85-99. Population structure and feeding ecology Kühl, H.S., T. Sop, E.A. Williamson, R. Mundry, of Guereza (Colobus guereza) in Borena- D. Brugière, G. Campbell, H. Cohen, E. Sayint National Park, northern Ethiopia. Danquah, L. Ginn, I. Herbinger, S. Jones, International Journal of Biodiversity and J. Junker, R. Kormos, C.Y. Kouakou, P.K. Conservation 9(11): 323-333. N' Goran, E. Normand, K. Shutt‐Phillips, Isbell, L.A. & L.R. Bidner. 2016. Vervet monkey A. Tickle, E. Vendras, A. Welsh, E.G. (Chlorocebus pygerythrus) alarm calls to Wessling &. C. Boesch. 2017. The critically leopards (Panthera pardus) function as a endangered western chimpanzee declines by predator deterrent. Behaviour 153(5): 591- 80%. American Journal of Primatology 79(9) 606. pp.n/a-n/a. Isbell, L.A., L.R. Bidner, M.C. Crofoot, A. Lonsdorf EV, Gillespie TR, Wolf TM, Lipende I, Matsumoto‐Oda & D.R. Farine. 2017. GPS‐ Raphael J, Bakuza J, Murray CM,Wilson ML, identified, low‐level nocturnal activity of Kamenya S, Mjungu D, Collins DA, Gilby vervets (Chlorocebus pygerythrus) and olive IC, Stanton MA, Terio KA, Barbian HJ, Li baboons (Papio anubis) in Laikipia, Kenya. Y, Ramirez M, Krupnick A, Seidl E, Goodall American Journal of Physical Anthropology J, Hahn BH, Pusey AE, Travis DA. 2016. 164(1): 203-211. Socioecological correlates of clinical signs Isbell, L.A. & S. Etting. 2017. Scales drive in two communities of wild chimpanzees detection, attention, and memory of snakes (Pan troglodytes) at Gombe National Park, in wild vervet monkeys (Chlorocebus Tanzania. American Journal of Primatology. pygerythrus). Primates 58(1): 121-129. In Press. Ito A., W. Eckardt, T.S. Stoinski, T.R. Gillespie, McGrew, W.C. 2017. Field studies of Pan & T. Tokiwa. 2016. Prototapirella ciliates troglodytes reviewed and comprehensively (Entodiniomorphida) from wild habituated mapped, focussing on Japan’s contribution Virunga mountain gorillas (Gorilla beringei to cultural primatology. Primates 58(1): beringei) in Rwanda with the descriptions 237–258. of two new species. European Journal of Neumann, C. & K. Zuberbühler. 2016. Vocal Protistology. In Press. correlates of individual sooty mangabey Janmaat, K.R.L., C. Boesch, R. Byrne, C.A. travel speed and direction. PeerJ, July 2016, Chapman, Z.B. Goné Bi, J.S. Head, M.M. Vol.4, p.e2298. Robbins, R.W. Wrangham & L. Polansky. Oates, J.F. & N. Ting. 2015. Conservation 2016. Spatio‐temporal complexity of consequences of unstable taxonomies: The chimpanzee food: how cognitive adaptations case of the red colobus monkeys. In A.M. can counteract the ephemeral nature of ripe Behie & M.F. Oxenham, eds. Taxonomic fruit. American Journal of Primatology 78(6): Tapestries: The Threads of Evolutionary, 626-645. Behavioural and Conservation Research. Johnson, C.A., D. Raubenheimer, C.A. Australian National University Press, Chapman, K.J. Tombak, A.J. Reid & J.M. Canberra. Pp. 321-343. African Primates 12 (2017) / 87 Recent Publications

Luef, E.M., T. Breuer, & S. Pika. 2017. Food- and non-birth seasons in wild female patas associated calling in gorillas (Gorilla g. monkeys. Primates 58(1): 115-119. gorilla) in the wild. PLoS ONE, Vol.11(2), Murray, C.M., M.A. Stanton, K.R. Wellens, R.M. p.e0144197. Santymire, M.R. Heintz, & E.V. Lonsdorf. Lynch, E., A. de Fiore, R. Lynch & R. Palombit. 2016. Maternal effects on offspring stress 2017. Fathers enhance social bonds among physiology in wild chimpanzees. American paternal half-siblings in immature olive Journal of Primatology doi:10.1002/ baboons (Papio hamadryas anubis). ajp.22525. Behavioral Ecology and Sociobiology 71(8): Nishie, H. & M. Nakamura. 2017. A newborn 1-11. infant chimpanzee snatched and cannibalized Madisha, M.T., D.L. Dalton, R. Jansen & immediately after birth: Implications for A. Kotze. 2017. Genetic assessment of "maternity leave" in wild chimpanzee. an isolated endemic Samango monkey American Journal of Physical Anthropology, (Cercopithecus albogularis labiatus) Oct 6. doi: 10.1002/ajpa.23327. [Epub ahead population in the Amathole Mountains, of print]. Eastern Cape Province, South Africa. Nowak, K., K. Wimberger, S. Richards, R. Primates, in press. Hill & A. Roux. 2017. Samango monkeys Mekonnen, A., P.J. Fashing, A. Bekele, R. (Cercopithecus albogularis labiatus) manage A. Hernandez-Aguilar, E.K. Rueness, N. risk in a highly seasonal, human-modified Nguyen & N.C. Stenseth. 2017. Impacts landscape in Amathole Mountains, South of habitat loss and fragmentation on the Africa. International Journal of Primatology activity budget, ranging ecology and 38(2): 194-206. habitat use of Bale monkeys (Chlorocebus Phillips, C.A. & T.C. O'Connell, Tamsin C. djamdjamensis) in the southern Ethiopian 2016. Fecal carbon and nitrogen isotopic Highlands. American Journal of Primatology, analysis as an indicator of diet in Kanyawara 09 February 2017. chimpanzees, Kibale National Park, Minhós, T., L. Chikhi, C. Sousa, L.M. Uganda: Isotope values in chimpanzee feces. Vicente, M. Ferreira Da Silva, R. Heller, C. American Journal of Physical Anthropology Casanova & M.W. Bruford. 2016. Genetic 161(4): 685-697. consequences of human forest exploitation Phillips, C.A., R.W. Wrangham, & W.C. in two colobus monkeys in Guinea Bissau. McGrew. 2016. Non-dietary analytical Biological Conservation 194: 194-208. features of chimpanzee scats. Primates 58(3): Moore, J., J. Black, R.A. Hernandez-Aguilar, 393-402. G. Idani, Gen'Ichi, A. Piel & F. Stewart. Piel, A.K., F.A. Stewart, L. Pintea, Y. Li, M.A. 2017. Chimpanzee vertebrate consumption: Ramirez, D.E. Loy, P.A. Crystal, G.H. Learn, Savanna and forest chimpanzees compared. L.A. Knapp, P.M. Sharp & B.H. Hahn. 2017. Journal of Human Evolution 112: 30-40. Correction: the Malagarasi River does not Motsch, P., C. Dilger, B. Ngoubangoye, J.-P. form an absolute barrier to chimpanzee Gonzalez & G. Le Flohic. 2016. The sun‐ movement in western Tanzania. PLoS ONE, tailed monkey (Cercopithecus solatus): first Vol.12(8), p.e0182723. report of mother‐infant dorsal carrying Plumptre, A.J., S. Nixon, D.K. Kujirakwinja, G. behaviour in a forest guenon, Gabon. African Vieilledent, R. Critchlow, E.A. Williamson, Journal of Ecology 54(2): 252-255. R. Nishuli, A.E. Kirkby, & J.S. Hall. 2017. Muroyama, Y. 2017. Variations in within-group Catastrophic decline of world's largest inter-individual distances between birth- primate: 80% loss of Grauer's Gorilla 88 / Recent Publications Recent Publications

(Gorilla beringei graueri) population justifies Society open science, February 2016, Critically Endangered status. PLoS ONE, Vol.3(2), pp.150639. Vol.11(10), p.e0162697. Struhsaker, T.T. 2017. Dietary variability in Rowe, N. (ed.) 2017. All The World's Primates. redtail monkeys (Cercopithecus ascanius Pogonias Press, Charlestown, Rhode Island, schmidti) of Kibale National Park, Uganda: USA. the role of time, space, and hybridization. Ruiz-Lopez, M. J., C. Barelli, F. Rovero, K. International Journal of Primatology 38(5): Hodges, C. Roos, W.E. Peterman, & N. 914–941. Ting. 2016. A novel landscape genetic Svensson, M.S., E. Bersacola, M.S.L. Mills, R.A. approach demonstrates the effects of human Munds, V. Nijman, A. Perkin, J.C. Masters, S. disturbance on the Udzungwa red colobus Couette, K.A. Nekaris & S.K. Bearder. 2017. monkey (Procolobus gordonorum). Heredity A giant among dwarfs: a new species of 116(2): 167-76. galago (Primates: Galagidae) from Angola. Schlenker, P., E. Chemla, & K. Zuberbühler. American Journal of Physical Anthropology 2016. What do monkey calls mean? Trends 163(1): 30-43. in Cognitive Sciences 20(12): 894-904. Tapanes, E., K. Detwiler & M. Cords. 2016. Schoeninger, M. J., C.A. Most, J.J. Moore & A.D. Bat predation by Cercopithecus monkeys: Somerville. 2016. Environmental variables implications for zoonotic disease across Pan troglodytes study sites correspond transmission. EcoHealth 13(2): 405-409. with the carbon, but not the nitrogen, stable Terio, K.A., E.V. Lonsdorf, M.J. Kinsel, J. isotope ratios of chimpanzee hair. American Raphael, I. Lipende, D.A. Collins, Y. Li, Journal of Primatology 78(10): 1055-1069. B.H. Hahn, D.A. Travis, & T.R. Gillespie. Schwitzer, C., Mittermeier, R.A., Rylands, 2016. Oesohagostomiasis in non-human A.B., Chiozza, F., Williamson, E.A., Macfie, primates of Gombe National Park, Tanzania. E.J., Wallis, J. and Cotton, A. (eds.). 2017. American Journal of Primatology. In Press. Primates in Peril: The World’s 25 Most Turner, T. R., W.G. Coetzer, C.A. Schmitt, J.G. Endangered Primates 2016–2018. IUCN Lorenz, N.B. Freimer & J.P. Grobler. 2016. SSC Primate Specialist Group (PSG), Localized population divergence of vervet International Primatological Society (IPS), monkeys (Chlorocebus spp.) in South Africa: Conservation International (CI), and Bristol Evidence from mtDNA. American Journal of Zoological Society, Arlington, VA. 99 pp. Physical Anthropology 159(1): 17-30. Sicotte, P., J.A. Teichroeb, J.V. Vayro, S.A. Vayro, J., L. Fedigan, T. Ziegler, A. Crotty, R. Fox, I. Bădescu & E.C. Wikberg. 2017. Ataman, R. Clendenning, E. Potvin-Rosselet, The influence of male takeovers on female E. Wikberg & P. Sicotte. 2016. Hormonal dispersal in Colobus vellerosus. American correlates of life history characteristics in Journal of Primatology 79(7). wild female Colobus vellerosus. Primates Silk, J.B., E.R. Roberts, B.J. Barrett, S.K. 57(4): 509-519. Patterson & S.C. Strum. 2017. Female–male Weary, T., R. Wrangham, & M. Clauss. 2017. relationships influence the form of female– Applying wet sieving fecal particle size female relationships in olive baboons, Papio measurement to frugivores: A case study anubis. Animal Behaviour 131: 89-98. of the eastern chimpanzee (Pan troglodytes Stephan, C. & K. Zuberbühler. 2016. schweinfurthii). American Journal of Physical Social familiarity affects Diana monkey Anthropology 04 April 2017. (Cercopithecus diana diana) alarm call Wiafe, E.D. 2016. Population studies of responses in habitat-specific ways. Royal Lowe’s Monkey (Mammalia: Primates: African Primates 12 2017 / 89 Recent Publications

Cercopithecidae: Cercopithecus lowei EcoHealth. In Press. Thomas, 1923) in Kakum Conservation Wrangham, R.W., K. Koops, Z.P. Machanda, S. Area, Ghana. Journal of Threatened Taxa Worthington, A.B. Bernard, N.F. Brazeau, R. 8(2): 8434-8442. Donovan, J. Rosen, C. Wilke, E. Otali & M.N. Wimberger, K., K. Nowak & R. Hill. 2017. Muller. 2016. Distribution of a chimpanzee Reliance on exotic plants by two groups of social custom is explained by matrilineal threatened Samango monkeys, Cercopithecus relationship rather than conformity. Current albogularis labiatus, at their southern range Biology 26(22): 3033–3037. limit. International Journal of Primatology Wren, B.T., M.J. Remis, J.W. Camp, & T.R. 38(2): 151-171. Gillespie. 2016. Number of grooming Wolf, T.M., S. Sreevatsan, R.S. Singer, I. Lipende, partners is associated with hookworm D.A. Collins, T.R. Gillespie, E.V. Lonsdorf, & infection in wild vervet monkeys D.T. Travis. 2016. Noninvasive tuberculosis (Chlorocebus aethiops). Folia Primatologica screening in free-living primate populations 87:168-179. in Gombe Stream National Park, Tanzania.

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Africa Biodiversity Collaborative Group The Bonobo Conservation Initiative (BCI) • Website: www.abcg.org • Website: www.bonobo.org • E-newsletter contact: Kamweti Mutu • Facebook: www.facebook.com/ ([email protected]) bonobodotorg • Facebook: www.facebook.com/ • Twitter: http://twitter.com/Bonobodotorg ABCGconserve • Twitter: http://twitter.com/ABCGconserve Budongo Conservation Field Station • Website: www.budongo.org African Primates (for journal and group) • Facebook: www.facebook.com/ • Website: www.primate-sg.org/african_ pages/Budongo-Conservation-Field- primates/ Station/111160629076237 • Facebook: https://www.facebook.com/ • Twitter: @Budongochimps (http://www. groups/232900723505713/ twitter.com/budongochimps) • Twitter: http://twitter.com/africanprimates Centre de Conservation pour Chimpanzes African Primatological Society • Website: http://www.projetprimates.com/en/ • Facebook: https://www.facebook.com/ • Facebook: https://www.facebook.com/ African.Primatological.Society/?fref=ts CentreDeConservationPourChimpanzes • Twitter: https://twitter.com/AfricanPs Chimp Eden (JGI Sanctuary, South Africa) African Wildlife Foundation • Website: http://www.chimpeden.com/ • Website: www.awf.org • Twitter: https://twitter.com/jgisachimpeden • Facebook: https://www.facebook.com/ AfricanWildlifeFoundation Chimpanzee Sanctuary & Wildlife Conservation • Twitter: http://twitter.com/AWF_Official Trust (Ngamba Island) • Website: www.ngambaisland.com/ Amboseli Baboons • E-newsletter contact: info@ngambaisland. • Website: www.amboselibaboons.nd.edu org • Twitter: https://twitter.com/ • Facebook: www.facebook.com/ngambaisland AmboseliBaboons Colobus Conservation Barbary Macaque Awareness and Conservation • Website: www.colobusconservation.org • Website: www.barbarymacaque.org • 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: https://twitter.com/Barbarymacaque • E-newsletter contact: [email protected] • Instagram: https://www.instagram.com/ • Facebook: Conservation Through Public barbary_macaque/ Health https://www.facebook.com/ pages/Conservation-Through-Public- The Bioko Biodiversity Protection Program Health/115176086614; CTPH Gorilla (BBPP) Conservation Camp: https://www.facebook. • Website: www.bioko.org com/pages/CTPH-Gorilla-Conservation- • Facebook: English - www.facebook.com/ Camp/239975179417714 pages/Bioko-Biodiversity-Protection- • Twitter: http://twitter.com/CTPHuganda Program/107673299261496; Spanish - www. facebook.com/BiokoBiodiversidad Comoe Chimpanzee • Twitter: http://twitter.com/Bioko_BBPP • Facebook: www.facebook.com/ • Instagram: https://www.instagram.com/ comoechimpanzeecp/ bioko_BBPP/ The Drill Project • Website: thedrillproject.org/ • Facebook: https://www.facebook.com/The- Drill-Project-258035237544233/ African Primates 12 (2017) / 91 Connections: E-News, Web Sites, and Social Media

East Africa Primate Diversity and Conservation HELP Congo (Chimpanzee Sanctuary) Program • Website: www.help-primates.org/ • Website: http://www.wildsolutions.nl/ • Facebook: https://www.facebook.com/ • Twitter: https://twitter.com/WildSolutions HELP-Congo-29693148237/

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GAIA – Great Ape Institute for Awareness International Primatological Society – • Website: www.gaiasanctuary.org/ Conservation • Facebook: https://www.facebook.com/ • Website: www. ProtectApes internationalprimatologicalsociety.org • Twitter: http://twitter.com/ipsconservation The Gishwati Foundation • Facebook: https://www.facebook.com/ Jane Goodall Institute GishwatiFoundation/ • Website: www.janegoodall.org • Facebook: https://www.facebook.com/ Gorilla Doctors janegoodallinst?_rdr=p • Website: http://www.gorilladoctors.org • Twitter: https://twitter.com/JaneGoodallInst • Facebook: https://www.facebook.com/ gorilladoctors/ Kasanka Baboon Research Project • Website: www.kasankababoonproject.com Gorillas Across Africa • Twitter: http://twitter.com/KindaCamp • Facebook: https://www.facebook.com/ GorillasAcrossAfrica KasokwaForestProject • Facebook: www.facebook.com/pages/ Goualougo Triangle Ape Project Kasokwa-Forest-Project/159230490821336 • Website: http://www.congo-apes.org/ • Twitter: http://twitter.com/KasokwaForest • Facebook: https://www.facebook. com/Goualougo-Triangle-Ape- Kibale Chimpanzee Project Project-282194681876/ • Facebook: https://www.facebook.com/ kibalechimpanzeeproject/ Great Ape Survival Partnership (GRASP) • Blog: https://kibalechimpanzees.wordpress. • Website: www.un-grasp.org com/ • Facebook: www.facebook.com/ graspunep?ref=stream Kyambura Gorge Chimpanzee Community • Twitter: http://twitter.com/graspunep • Facebook: https://www.facebook. com/Kyambura-Gorge-Chimpanzee- Guenon Conservation Community Community-119478481457652/ • Facebook: www.facebook.com/pages/ Guenon-Conservation-Community/2031800 09723143?ref=stream 92 / Connections: E-news, Web Sites, and Social Media

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Le Projet Gorille Fernan-Vaz (Gabon) Samango Monkey Project • Website: www.gorillasgabon.org/ • Facebook: www.facebook.com/groups/ • Facebook: https://www.facebook.com/pgfv. samango/ fvgp Save the Abandoned Chimps (Liberia) LimbeWildlifeCentre • Facebook: https://www.facebook.com/ • Facebook: www.facebook.com/pages/Limbe- abandonedchimps Wildlife-Centre/504832002861894 • Twitter: http://twitter.com/LimbeWildlife Society for Conservation Biology – Africa Section • E-mail list contact: Beth Kaplin bkaplin@ Lukuru Foundation anticho.edu • Website: www.lukuru.org • Facebook: https://www.facebook.com/ Tacugama Chimpanzee Sanctuary LukuruFoundation?fref=ts • Website: www.tacugama.com/ • Facebook: https://www.facebook.com/ Lwiro Sanctuary Tacugama • Website: www.lwiroprimates.org • Twitter: http://twitter.com/Tacugama • Facebook: www.facebook.com/lwiro • Twitter: https://twitter.com/lwirosanctuary Tai Chimp Project • Website: www.taichimps.org Mbeli Bai Study • Twitter: http://twitter.com/TaiChimpProject • Website: www.mbelibaistudy.org • Facebook: https://www.facebook.com/Mbeli- Uaso Ngiro Baboon Project Bai-Study-137426999658859/ • Website: http://www.baboonsrus.com/6.html • Twitter: https://twitter.com/mbelibai Ugalla Primate Project Ngogo Chimp Project • Website: www.ugallaprimateproject.com • Website: www.ngogochimpanzeeproject.org/ • Facebook: https://www.facebook.com/ Vervet Monkey Foundation NgogoChimps/ • Facebook: www.facebook.com/groups/vervet • Twitter: https://twitter.com/ngogochimps • Twitter: http://twitter.com/VervetMonkeys

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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. It is recommended that contributors consult • Use metric units only and define all abbreviations. recent issues of African Primates for more • Current taxonomic classifications should be used. details on the journal’s format and content. However, if species or subspecies’ names have undergone recent revision, include mention of recent names as a service to readers adjusting to Please submit all manuscripts and materials new naming conventions. electronically to: [email protected] • Tables, figures, and photographs are encouraged. All require accurate and concise captions listed on a Janette Wallis, Ph.D. separate sheet. African Primates, Editor-in-Chief • 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 12 2017

Research Articles

Species Density of Galago moholi at Loskop Dam Nature Reserve, South Africa ...... 1 Ian S. Ray, Brandi T. Wren, and Evelyn J. Bowers

Presence of Alkaloids and Cyanogenic Glycosides in Fruits Consumed by Sympatric Bonobos and the Nkundo People at LuiKotale/Salonga National Park, Democratic Republic of Congo and Its Relationship to Food Choice ...... 9 Nono Bondjengo, Gaby Kitengie, Dieudomé Musibono, Constantin Lubini, Gottfried Hohmann, and Barbara Fruth

Primate Communities Along a Protected Area Border: A Two-site Comparison of Abundance and Hunting Response in Bioko, Equatorial Guinea ...... 23 Daniel L. Forrest, Fermin Muatiche, Cirilo Riaco, Mary Katherine Gonder, and Drew T. Cronin

The First Sightings of the Red-Bellied Guenon (Cercopithecus erythrogaster erythrogaster) on the Western Edge of Southwestern Nigeria ...... 37 Reiko Matsuda Goodwin, Jacob Oluwafemi Orimaye, Francis E. Okosodo, Babafemi G. Ogunjemite, and Mariano G. Houngbedji

Brief Communications

Dogs Disrupting Wildlife: Domestic Dogs Harass and Kill Barbary Macaques in Bouhachem Forest, Northern Morocco ...... 55 Siân Waters, Ahmed El Harrad, Mohamed Chetuan, Sandra Bell, and Joanna M. Setchell

Pan African Sanctuary Alliance: Primate Welfare, Conservation, and Research ...... 59 Rachel Stokes, Gregg Tully, and Alexandra Rosati

Extending the Northeastern Distribution of Mandrills (Mandrillus sphinx) into the Dja Faunal Reserve, Cameroon ...... 65 Madeleine Ngo Bata, Julian Easton, Oliver Fankem, Tim Wacher, Tom Bruce, Tchana Eliseé, Pierre Augustin Taguieteu, and David Olson

Obituary: Stuart A. Altmann ...... 68 Susan C. Alberts and Daniel I. Rubenstein

Obituary: Deborah L. Moore ...... 71 Gráinne McCabe and Carolyn Ehardt

Announcements ...... 74 Recent Publications ...... 84 Connections: E-News, Web Sites, and Social Media ...... 90