Volume 11, Issue 1 2016 ISSN 1093-8966 AFRICAN PRIMATES The Journal of the Africa Section of the IUCN SSC Primate Specialist Group
Editor-in-Chief: Janette Wallis
PSG Chairman: Russell A. Mittermeier PSG Deputy Chair: Anthony B. Rylands Red List 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 Chairman: Russell A. Mittermeier Janette Wallis – Editor-in-Chief Deputy Chair: Anthony B. Rylands University of Oklahoma, Norman, OK USA Vice Chair, Section on Great Apes:Liz Macfie Deputy Vice Chair, Section on Great Apes: Serge Wich Simon Bearder Vice Chair, Section on Small Apes: Benjamin M. Rawson Oxford Brookes University, Oxford, UK R. Patrick Boundja Regional Vice-Chairs – Neotropics Mesoamerica: Liliana Cortés-Ortiz Wildlife Conservation Society, Congo; Univ of Mass, USA Andean Countries: Erwin Palacios and Eckhard W. Heymann Edem A. Eniang Brazil and the Guianas: M. Cecília M. Kierulff, Fabiano Rodrigues Biodiversity Preservation Center, Calabar, Nigeria de Melo, and Maurício Talebi Colin Groves Regional Vice Chairs – Africa Australian National University, Canberra, Australia W. Scott McGraw, David N. M. Mbora, and Janette Wallis John Hart Foundation Lukuru, Kinshasa, DRC Regional Vice Chairs – Madagascar Michael A. Huffman Christoph Schwitzer and Jonah Ratsimbazafy Kyoto University, Inuyama, Japan Regional Vice Chairs – Asia Lynne A. Isbell China: Long Yongcheng University of California, Davis, CA USA South-east Asia/Indochina: Jatna Supriatna, Christian Roos, Gladys Kalema-Zikusoka Benjamin M. Rawson, and Ramesh Boonratana South Asia: Sally Walker and Sanjay Molur Conservation through Public Health, Kampala, Uganda Shadrack Kamenya Red List Authority Coordinators Jane Goodall Institute-Tanzania, Kigoma, Tanzania Sanjay Molur, Christoph Schwitzer, and Liz Williamson Inza Koné Université Félix Houphouet Boigny, Abidjan, and Centre Suisse de Recherches Scientifiques en Côte d'Ivoire Joanna E. Lambert University of Colorado, Boulder, CO USA This issue of African Primates was produced with the Judith Masters assistance of a grant from the Margot Marsh Biodiversity University of Fort Hare, Alice, South Africa Foundation, through Conservation International’s Primate David N. M. Mbora Action Fund, and the cooperation of the Oklahoma Zoological Society and Oklahoma City Zoo. Whittier College, Whittier, CA USA 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 Olive Baboon (Papio anubis) in Manyara National Park, Tanzania. Photo by Janette Wallis Printed by: University of Oklahoma Printing Services African Primates online: All volumes of African Primates are available online at www.primate-sg.org/african_primates African Primates 11(1): 1-18 (2016)/ 1
A New Report of Chimpanzee Ant-fishing from the Issa Valley, Tanzania
Eden M. Wondra1, Adam van Casteren2 , Alejandra Pascual-Garrido3, Fiona Stewart1,4, and Alexander K. Piel1,5
1Ugalla Primate Project, Box 108, Uvinza, Tanzania; 2Max Planck Weizmann Center for Integrative Archaeology and Anthropology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany; 3Leverhulme Trust Early Career Fellow, School of Archaeology, University of Oxford, Oxford, UK; 4Department of Archaeology and Anthropology, University of Cambridge, Cambridge, UK; 5School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK
Abstract: Tool use in chimpanzees (Pan troglodytes) is widespread across their geographical distribution, having been documented in all populations studied to date. Ant-fishing, specifically, is less frequently observed, reported so far in only ten different communities. We describe the first observations of ant-fishing of Camponotus chrysurus by chimpanzees living in the mosaic landscape of the Issa Valley, western Tanzania. After two separate bouts, both occurring in the same position in a fig treeFicus ( lutea vahl), we recovered five ant-fishing tools made from the liana Dichapetalum crassifolium chodat. Tool types closely resemble those described for earlier reports of the same behavior in near-by Mahale Mountains chimpanzees, and thus may have implications for cultural diffusion of the habit across populations.
Key words: Chimpanzee, Camponotus, ant-fishing, insectivory, Issa Valley
INTRODUCTION
Tool use in chimpanzees (Pan troglodytes) is for termites and to access plant underground storage widespread across their geographical distribution, organs (Hernandez-Aguilar et al. 2007; Stewart & having been documented in all populations that have Piel 2014). been thoroughly studied to date (McGrew 2010). The Probably because of the lower mass intake rate type, function, and prevalence in tool use behaviors of ant-fishing (chimpanzee predation of carpenter differ widely, however, suggesting that an interplay ants through the use of tools – Camponotus spp.), between culture, where the behavior is transmitted compared to that of ant-dipping for Dorylus repeatedly through social or observational learning ants (with a higher mass intake rate) and termite to become a community-level-characteristic, and fishing, carpenter ants Camponotus( spp.) are not as the environment explains such variation (McGrew commonly consumed by chimpanzees as are other 1992; Whiten et al. 1999; Koops et al. 2013; Sanz et invertebrates (O’Malley & Power 2014). Compared al. 2014). Chimpanzees exhibit a rich repertoire of to the 21 communities of chimpanzees where tool-use behaviors, used most often to improve or termite fishing has been described, ant-fishing has gain access to a variety of foods including termites, been described in only 10 different communities bees and honeycomb, nuts, and ants (McGrew (Table 1; Figure 1). This is surprising given that 1992). Chimpanzees of the Issa Valley are known to Camponotus has the most ecologically diverse manufacture and use tools made from plants to fish geographical range, and the broadest distribution of
Correspondence to: Alex Piel, School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Building, Byrom Street, L33AF, Liverpool, UK; Phone: +44 7557915813; E-mail: [email protected]. 2 / Wondra et al.
2005; et al. et et al. et 2014 References 1991 Muroyama Deblauwe & 2006; Deblauwe 2008 Janssens 1997 Ingmanson 1994 & Carroll Fay 1994 & Carroll Fay Hicks 2010 Hicks & Morgan Sanz 2007, 20013; Sanz al. et Bermejo & Illera 1999
? ? ants +/+/H Camponotus ants ? ? +/+/T +/+/T +/+/T +/+/H Dorylus foraging for this region. this region. for foraging ) Pan +?/- +/+/T +/+/T +/+/T +/+/T +/+/T +/+/T Termites Termites vitrialatus Macrotermes Macrotermes lilljeborgi; M. lilljeborgi; Macrotermes ( M. lilljeborgi; M. M. lilljeborgi; M. M. lilljeborgi; muelleri; M. nobilis muelleri; M. nobilis muelleri; ) +/- mellifera
+/+/T +/+/T +/+/T +/+/T Honey BeesHoney Apis ( Note: We incorporate the Sonso, Busingiro and Kasongoire communities to the table (even though (even though the table to communities Kasongoire and Busingiro the Sonso, incorporate We Note: ) +/+/T +/+/T +/+/T +/+/T +/+/T +/+/T Trigona Trigona beccardi beccardi Meliponini ( gribodoi Mag (Hypotrigona) (Hypotrigona) Stingless BeesStingless Trigona gribodoi; gribodoi; Trigona Trigona (Meliplebia) Trigona Meliponula nebulata Meliponula Hypotrigona gribodoi; Hypotrigona Name of of Name Community Campo Dja Biosphere Reserve, La Belgique Ntale Bai Hokou Ndakan Ngotto Goualougo Lossi African Republic African Republic African Republic Republic Republic Country 1. Cameroon 2. Cameroon 3. Cameroon 4. Central 5. Central 6. Central 7. Congo 8. Congo Table 1. Presence or absence and type insectivory absence and insects of or products: +/+ their with 1. Presence chimpanzee gathering reports or of in communities use tool for Table ? unknown; consumed eaten; H consumed with T consumed with H? probably hands; tools; +/+?, present/probably eaten; +/− present/not present/eaten; its or presence/absence prey’s report of any we failed to find where thosesites for blank left consumed with Spaces were tools. with T? probably hands; Species provided are targeted when known.consumption. in the local insects) address variability to gathering for tools manufacture to known not they are Ant-fishing in Issa Chimpanzees / 3 . 1979 1996 . 1995; et al. al. et et al. al. et ., l. et al et al. et et al et a et al References Suzuki Kuroda Bermejo & Illera 1999 Boesch & Boesch 1990 Hicks data; unpublished C. pers. Hicks, comm. Hicks data; unpublished C. pers. Hicks, comm. Yamagiwa & 1988; Yamagiwa Basabose 2009 Takemoto 2005 1974; Pi Sabater McGrew
+/- +?/- ants +/+/T Camponotus
D. kohli ants . D +/+/T +/+/T +/+/T opacus +/+/H? +/+/H? with long long with short tools) D. wilverthi wilverthi D. D. terrificus; terrificus; D. D. nigricans; nigricans; D. Dorylus D. gerstaeckeri D. thin wand); thin wand); tools); tools); wilverthi (both D. terrificus; D. terrificus; D. consumed with with consumed (consumed with with (consumed (both consumed (both consumed ) +/- +/- +/- +/+/T +/+/T +/+/T +/+/T +/+/H muelleri Termites Termites M. muelleri M. lilljeborgi; M. lilljeborgi; Macrotermes Macrotermes Macrotermes ( ) mellifera +/-? +/-?
+/+/T +/+/H? Honey BeesHoney Apis ( ) + +/+/T +/+/T +/+/T +/+/T Meliponini ( consumption) Stingless BeesStingless (no evidence of evidence(no of Name of of Name Community Ndoki Ndoumbi Taї Forest Bili-Gagu Bili-Uele Bili-Uele Southern (Leguga Forests / Bambesa / Aketi) Kahuzi-Biega Mboete Okorobiko Republic d’Ivoire Guinea Guinea Republic Country 9. Congo 10. Congo 11. Côte Congo 12. DR 13. DR Congo 13. DR 14. DR. Congo 15. Equatorial 16. Equatorial Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table 4 / Wondra et al.
2009 et al al et 2013; 2015a et al. et et al. al. et et al. al. et et al. et et al. et al. et References & Rogers McGrew 1983 Boesch 1992; McGrew & Fernandez Tutin 1992; Tutin 1995 Nishimura & 2003; Wilfried 2014 Yamagiwa Sugiyama 1995; Humle & 1999; Humle 2002; Matsuzawa Yamamoto 2008; Sanz 2009 Koops Koops Koops
ants +/+/T +/+/T C. brutus C. brutus Camponotus +/- ants +/+/T +/+/T Dorylus D. kohli; D. D. mayri; mayri; D. D. emeryi; D. D. gribodoi D. D. lamottei; D. D. militaris; D. D. nigricans D. D. nigricans; nigricans; D. D. burmeisteri; burmeisteri; D. ) nobilis +/- +/- +/- +/+/T +/+/T . ? +/+?/T? Termites Termites M M. bellicosus Macrotermes ( ) +/- +/- mellifera
+/+/T +/+/T Honey BeesHoney Apis ( ) +/- +/+/T +/+/T +/+/T +/+/T Meliponula Meliponini ( Stingless BeesStingless Trigona, Meliponula Trigona, Meliponula lendiana Meliponula Meliplebeia nebulata;Meliplebeia Meliponula bocandei; bocandei; Meliponula Meliponula lendliana; Meliponula Name of of Name Community Belinga Loango Lope Moukalaba- Doudou Bossou Seringbara, Nimba Mountains Country 17. Gabon 18. Gabon 19. Gabon 20. Gabon 21. Guinea 22. Guinea Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table Ant-fishing in Issa Chimpanzees / 5 et 2013 . 2005; et al. al. et et al al. et et al. al. et 2012; O’Malley 2012; O’Malley References & Sommer Fowler 2007; Pascual- Garrido 2012; Dutton Dutton & Chapman 2015a, 2015b 2010 Easton McGrew McGrew Bogart & Pruetz 2008, 2011 McGrew 1988; McBeath 1992; & McGrew 1992 McGrew 1993 Alp 1974; McGrew Goodall 1986; Schoning 2008; O’Malley al. 2014; & Power R., pers. O’Malley, comm.
. sp. 1 . sp. ants +/+/T +/+/T +/+/T +/+/T C C. vividus; C. vividus; C. crhysurus C. nr. perrisi C. nr. C. chrysurus; C. chrysurus; Camponotus D. ants +/+/T +/+/T +/+/T +/+/T +/+/T +/+/T D. kohli Dorylus +/+/? D. rubellus burmeisteri D. anomma D. D. nigricans D. nigricans D. D. molestus;D. ) +/- +/- +/+/T +/+/T +/+/T Termites Termites with hands) M. bellicosus M. bellicosus Macrotermes M. subhyalinus M. subhyalinus ( M. subhyalinus; M. subhyalinus; M. subhyalinus; M. subhyalinus; this species eaten this species eaten spp. (only alates of of alates (only spp. Pseudacanthotermes ) +/+ mellifera
+/+/T +/+/T +/+/T +/+/H +/+/H? Honey BeesHoney pers. comm.) Apis ( (use of tools seen tools (use of rarely; O’Malley, R., O’Malley, rarely;
) +/+/T +/+/T +/+/H Meliponini pers. comm) ( Stingless BeesStingless (use of tools seen tools (use of Meliponula erythra Meliponula erythra rarely; O’Malley, R., O’Malley, rarely; Trigona; HypotrigonaTrigona; Hypotrigona gribodoi; Hypotrigona gribodoi; Hypotrigona Name of of Name Community Gashaka-Gumti Nyaki Ngel Nyungwe Fongoli Mt. Assirik Mt. Tenkere- Outamba- Kilimi Gombe (Kasekela) Leone Country 23. Nigeria 24. Nigeria 25. Rwanda 26. Senegal 27. Senegal 28. Sierra 29. Tanzania Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table 6 / Wondra et al. et
et al. al. et et al. et 2008; Sanz 2008; Sanz References et al. Schoning 2008; O’Malley 2011; O’Malley 2014; & Power pers. D., Mjunju, O’Malley, comm.; R. pers. comm. 2014 & Piel Stewart 1966; & Itani Izawa 1966 Suzuki 1982; Uehara & Collins McGrew 1985 & Hiraiwa Nishida 1982; 1982; Uehara & Uehara Nishida 1983; Schoning al. 2015; 2009; Kiyono M., Nakamura, pers. comm. & Uehara Nishida 1983; McGrew & Collins 1985; Schoning 2011; 2008; Nishie 2015; Kiyono M., Nakamura, pers. comm.
. sp. ? ants +/+/? +/+/T +/+/T +/+/T (maybe); C. brutus C. brutus C. vividus C. vividus C. chrysurus; C. chrysurus; C. chrysurus; Camponotus C. vividus; C. C. vividus; maculatus; C. maculatus; brutus; C. brutus; Current study Current ? +/- +/- +/- +/- ants +/+/T D. kohli Dorylus D. molestusD. molestusD. D. molestus;D. ) (tools are are (tools spp. (only (only spp. (tools were were (tools +/+T +/+/T +/+/T +/+/T +/+/T +/+/T hands) Termites Termites M. ?herus Macrotermes Pseudacantho- ( M. subhyalinus; M. subhyalinus; were eaten with with eaten were termes termes spiniger spiniger rarely used; alates used; alates rarely eaten with hands) with eaten spiniger spiniger alates of this species of alates Pseudacanthotermes Pseudacanthotermes rarely used, alates are are used, alates rarely are eaten with hands) with eaten are ) +/- +/- +/? mellifera
+/+/? +/+/? +/+/H comm.) Honey BeesHoney Apis rarely to widen to rarely ( entrance of nest, nest, of entrance Mjungu, D. pers. D. Mjungu, (use of tools only only tools (use of ) ? +/- +/+/T +/+/T +/+/T +/+/H Trigona Trigona Trigona comm.) Trigona?; Trigona?; Meliponini ( Hypotrigona? Stingless BeesStingless rarely to widen to rarely entrance of nest, nest, of entrance Mjungu, D. pers. D. Mjungu, (use of tools only only tools (use of Name of of Name Community Gombe (Mitumba) Issa Kasakati Mahale (B-Group) Mahale (K-Group; extinct) Mahale (M-Group) Country 30. Tanzania 31. Tanzania 32. Tanzania 33. Tanzania 34. Tanzania 35. Tanzania Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table Ant-fishing in Issa Chimpanzees / 7 ., in et al References Newton-Fisher 1999; Reynolds, pers. comm. V., pers. J., Wallis, comm. A., pers. Oxley, comm. & Hedges 2012 McGrew Mugisha Hobatier, press; C., pers. comm. 2011; McLennan 2014
. C ( found found ? +/- +/- ants +/+/H +/+/H +/+?/H reported) reported) (one single single (one observation observation brutus Camponotus (one possible possible (one C. vividus once in dung) once +/- +/- +/? ants (rare) +/+/T +/+/H Dorylus D. wilverthi wilverthi D.
)
and +/? +/? +/H rarely seen) rarely eaten) +/+/H +/+/H +/+?/H Termites Termites Macrotermes Macrotermes ( clearings, rarely rarely clearings, (present only in only (present Macrotermes (alates eaten only) eaten (alates Pseudocanthotermes spiniger Pseudocanthotermes ( ) +/- +/- +/? mellifera
+/+/H +/+/T? (use of tools tools (use of Honey BeesHoney primarily for for primarily Apis ( acquiring honey) acquiring ) +/- +/- +/? +/+/T +/+/H Meliponini ( Stingless BeesStingless Meliponula lendliana Meliponula Name of of Name Community Budongo (Busingiro) Budongo (Kasokwa) Budongo (Kasongoire) Budongo (Sonso) Budongo (Waibira) Bulindi Country 36. Uganda 37. Uganda 38. Uganda 39. Uganda 40. Uganda 41. Uganda Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table 8 / Wondra et al.
et et et
et al. et
. et al. al. et et al. et et al. et et al 2011; Nelson 2011; Nelson 2008; Sanz 2008; Sanz l. 2009; Potts 2009; Potts l. References Stanford 2000; Stanford & Nkurunungi & 2003; Kajobe 2006 Roubik Koops 2015b Koops 2015b Wrangham 1991; Schoning al. a al. 2013 2008; Watts 2014; McLennan *Bee taxa were in the listed not tool of reports Watts use by this (2008) but located is site 10km from Kanyawara Webster 2014
+/- +/- +/- ants Camponotus +/- +/- +/- ants +/+/T +/+/T +/+/H Dorylus D. wilverthi D. wilverthi D. D. terrificus; terrificus; D. terrificus; D. ) - = +/- +/- +/+/H Termites Termites Macrotermes ( ) mellifera
+/+/T +/+/T Honey BeesHoney Apis ( ) +/+/T +/+/T +/+/T +/+/T* Meliponini M. nebulata; M. nebulata; M. lendliana ( M. ferruginea; M. ferruginea; Stingless BeesStingless Meliponula bocandei, bocandei, Meliponula Name of of Name Community Bwindi Kalinzu (M-Group) Kalinzu (S-Group) Kibale (Kanyawara) Kibale (Ngogo) Toro-Semliki Country 42. Uganda 43. Uganda 44. Uganda 45. Uganda 46. Uganda 47. Uganda Table 1. Presence or absence and typeinsectivory and absence insectsof or (continued.) products their with 1. Presence chimpanzeegathering reports or of in communities use tool for Table Ant-fishing in Issa Chimpanzees / 9
Figure 1. Map of reported tool-use for insectivory by chimpanzees. Those communities with Camponotus consumption are underlined. The Issa Valley study area is denoted with a triangle. all ant genera across Africa (Wilson 1975; Nishida tools from various plant parts and exhibit multiple & Hiraiwa 1982; McGrew 1992). Their colonies of extraction techniques (Nishida & Hiraiwa 1982). For hundreds to thousands of soldier and worker ants example, in the Mahale Mountains National Park, are commonly found in nests made in the trunks Tanzania, Nishida (1973) discussed three different of trees, dry branches, or hollow grass stems from types of techniques (wiping handkerchief, expelling dispersed-open to dense-tropical forests (Nishida & stick, and poking rod) in his description of how Hiraiwa 1982). Direct observations of chimpanzees chimpanzees consumed Camponotus ants (see also preying on Camponotus have been described from Nishie 2011), as well as twenty-two different species Gashaka-Gumti National Park, Nigeria (Fowler & of plants used as raw material and six different types Sommer 2007), Bossou, Guinea (Yamamoto et al. of tools according to the physical characteristics and 2008), Lope Reserve, Gabon (Tutin & Fernandez technique used for each tool (Nishida & Hiraiwa 1992), Mahale, Tanzania (Nishida & Hiraiwa 1982; 1982). At Gombe, only 150 km north of Mahale, Nishie 2011) and Gombe, Tanzania (O’Malley et al. decades of intense research initially resulted in the 2012), while at Mt. Assirik (Senegal), also a dry, open, acceptance that Camponotus was never consumed mosaic habitat such as Issa, McGrew (1992) inferred (Nishida & Hiraiwa 1982), followed by the possibility their consumption from tool remains at a disturbed of their consumption (Goodall 1986), and more ant colony. Other sites where consumption has been recently, a detailed analysis of the dissemination inferred from tools left abandoned at targeted nests of the behavior across numerous members of the include Ngel Nyaki (Nigeria) and Taï National Park Kasekela community (O’Malley et al. 2012). About (Ivory Coast) (Boesch & Boesch 1990; Dutton 2012). halfway between Gombe and Mahale, in Kasakati, Similar to how researchers document Suzuki (1966) reported Camponotus consumption chimpanzee ant-dipping, researchers have noted through analysis of chimpanzee fecal remains, but the various techniques that chimpanzees employ ant-fishing was never confirmed with behavioral when fishing for carpenter ants, the reduction observations or through the indirect evidence of processes involved during tool manufacture, as well tools. as the diverse types of raw material used (Nishida & Here we report on the first direct observations Hiraiwa 1982). Tool structure is not only important of ant-fishing of Camponotus by chimpanzees in for efficiency, but also for avoiding the aggressive the Issa Valley, adding this type of tool use to the biting defenses of carpenter ants, which appear to repertoire of tool using behavior for this community discourage chimpanzees from predation (Nishida and describing a third occurrence of the behavior in & Hiraiwa 1982). Even within consumption of a western Tanzania. single prey species, chimpanzees may manufacture 10 / Wondra et al.
METHODS well, while the other three chimpanzees remained close by, including two adult males and one adult Study Site female. We observed them directly consuming ants The Issa Valley is located about 100km east of directly by their mouths or by using their hands, Lake Tanganyika, almost halfway between Gombe sweeping them across the surface of the tree. After and Mahale Mountains National Parks (Figure a few minutes, the young female reached down and 2). The region is one of the driest, most open and broke off a piece from a liana, before inserting it into seasonally extreme habitats in which chimpanzees a tree-hole (Figure 3; see supplementary video1). live (Moore 1992), with the landscape characterized She repeated this process multiple times, making by miombo woodland (dominated by Brachystegia numerous new tools, using them briefly, and then and Julbernardia), interspersed with grasslands, changing tools until approximately 11:30 when she swamps and steep gallery forest ravines (Piel et al. left the tree, after over two hours of fishing. Given 2015). Annual temperature and precipitation ranges our obscured visibility of the ant-fishers, details of from 11° to 35°C, and 900-1400mm, respectively. the manufacturing process, technique used and The Ugalla Primate Project established a whether the new tools were taken from the same permanent research presence at Issa in 2008, but liana, or a stem or branch could not be seen. shorter-term (temporary) studies have occurred In a second observation on July 8, 2015, AVC in the area since 2001. As of May 2016, the Issa observed an adult female (possibly the same as community was partially habituated: fourteen previously observed) ant-fishing. On this occasion chimpanzees were individually identifiable and the individual was alone, fishing in the same the community size was estimated to be at least location of the same tree, and also fishing with her 67 individuals based on genetic analyses, with a right hand. Fishing occurred between 10:00 and minimum estimated home range of 85km2 (Rudicell 11:00, lasting almost one hour. Despite visiting the et al. 2011). tree on subsequent days, we observed no further fishing bouts. Data Collection Subsequent tool collection and botanical Research teams consisting of two people identification revealed all tools to be manufactured searched for chimpanzees on a near-daily basis. from Dichapetalum crassifolium chodat (Table 2) Usually, we relied on known feeding trees, and the host tree of the ant colony to be Ficus lutea preferred nesting sites, and dawn vocalizations to vahl. Tool types (Figure 4) most closely resembled locate chimpanzee parties. When we encountered Type B, described in Nishida and Hiraiwa (1982) as chimpanzees, we recorded data on party size, a tool made from the bark fiber of a liana, peeled location, habitat, demography, and behavior. For off and often divided into thin strips used for small the current observations, chimpanzees were found nest entrances. One other tool that we recovered in a tree that was already being monitored because suggested a similarity to Type BBr - made of a branch its fruit had recently ripened and we had observed of a liana that has had its bark partially or completely chimpanzees feeding there for several days. All removed, to facilitate it fitting into a small ant hole, research complied with protocols approved by the and with its distal end showing evidence of wear with Tanzania Wildlife Research Institute and adhered to a slightly split end. Two additional plant remains the legal requirements of Tanzania and the American were also collected from the same area that may Society of Primatologists Principles for the Ethical have been tool fragments that had detached from Treatment of Non-Human Primates. the tool during the course of its use or manufacture. However, their small size makes validity or tool type RESULTS classification unreliable, although they seem to be of similar age based on color and condition (Figure 4). Observation On July 2, 2015, researchers encountered five chimpanzees feeding in a Ficus lutea vahl tree in DISCUSSION the core study area. At 09:15, EW and field assistant MR observed one young adult female perched on Whereas tool use for insectivory is nearly a tree with a vine for balance 19 meters above the pervasive across chimpanzee communities, ant- ground, using a tool with her right hand to fish ants from the crux of the tree, before the four others later 1 Supplementary video may be viewed at: https://youtu.be/ joined her. Only an estrous female then fished as ejGiYbEljrs. Ant-fishing in Issa Chimpanzees / 11
Figure 2. Map of western Tanzania with the Issa study site highlighted in the center. The two closest study sites where ant-fishing has also been recorded, Gombe and Mahale National Park, to the north and south, respectively, are also highlighted. Vegetation, river and roads that may act as barriers between these populations and could influence cultural transmission are indicated. Map credit: L. Pintea, Jane Goodall Institute. fishing has been reported in only 10 communities Camponotus chrysurus in the Issa chimpanzees of (Figure 1), surprising given the widespread western Tanzania, making it the third description distribution of Camponotus across Africa (although for the region. Given the previous reports of this possibly under-represented due to the elusiveness behavior, where chimpanzees were preying on the of the tools [Bolton 1995]). We have now added same species of arboreal ants at nearby Mahale to this list with two observations of ant-fishing of (Nishida & Hiraiwa 1982; Nishie 2011) and further 12 / Wondra et al.
Table 2. Dimensions and types of tools found at site of fishing. Type B = strip of bark removed from a liana; Type BBr = branch of liana with some or all bark removed.
Tool Length Width Match to Nishida and Hiraiwa Material number (mm) (mm) (Nishida & Hiraiwa 1982) 1 214 < 1 Dichapetalum Type Ba crassifolium chodat 2 109.48 < 1 D. c. chodat Type B 3 88.34 1.48 D. c. chodat Type BBrb 4 97.78 1.38 D. c. chodat Type B 5 99.80 1.82 D. c. chodat Type B Types are taken from Nishida and Hiraiwa’s (1982) descriptions of the variations of ant-fishing tools made by chimpanzees. a Type B = a tool made from the bark fiber of a liana, pealed off and divided into thin strips used for small nest entrances. b Type BBr = a tool made of a branch that has had its bark partially or completely removed to facilitate it fitting an ant hole.
Figure 3. Picture of Camponotus chrysurus and the area where ants were observed on the Ficus tree where fishing occurred. Photograph by A. van Casteren. Ant-fishing in Issa Chimpanzees / 13
Figure 4. All five tools made from the bark of Dichapetalum crassifolium chodat, and additional fragments that we collected from the fork of the Ficus tree where ant-fishing was observed. Photograph by E. Wondra. 14 / Wondra et al.
north, Gombe (O’Malley et al. 2012), this could be thorough comparative study. More information on a case of diffusion of the habit, where the behavior the abundance of carpenter ants in Issa, their range spread from one or both of the other study sites east in habitat and altitude will be essential to addressing to Issa, by social learning (Whiten et al. 2001, 2007; this. This is both a rare and important occasion to McGrew 2004). However, an independent invention document and pursue for it may help to increase our in similar ecological contexts cannot be ruled understanding of tool use, cultural transmission and out: ant-fishing has been recognized as habitual insect foraging in chimpanzees, which is a viable in chimpanzees from the Mitumba community approach to anthropology and cultural evolution living in the northern parts of Gombe for decades, (McGrew 2004, O’Malley & Power 2014). while remaining absent from neighboring Kasekela community. It was only relatively recent that ant- fishing became a customary behavior in Kasekela, ACKNOWLEDGMENTS practiced exclusively by younger individuals and immigrant females (O’Malley et al. 2012). This We thank the Tanzanian Wildlife Research suggests that a possibility of ant-fishing traditions, Institute (TAWIRI) and the Commission for Science even if having a common origin, going extinct and and Technology (COSTECH) for permission to subsequently becoming re-established might exist. conduct research in the Issa valley. We greatly Only further observations of the behavior will appreciate the help of Msigwa Rashid, Busoti allow for more detailed comparisons of tools and Juma, and Shedrack Lukas for field assistance. extraction techniques between communities. APG is grateful to The Leverhulme Trust / UK for Regardless of whether techniques overlap across providing an Early Career Fellowship during the communities, Ficus appears not to be a commonly production and revision stage of this manuscript used tool source anywhere. In his summary analysis and AVC thanks the Max Plank Society for partially of over a half-century of Camponotus fishing in funding this work. We would also like to thank Mahale, Nishie (2011) described chimpanzee Caspar Schöning for ant-prey identification and use of 92 different trees to ant fish representing Yayha Abeid for botanical identification of tools. 24 different tree species, of which only one was Our special thanks to Paul Dutton, Cleve Hicks, Ficus (exasperata). Also at Gombe, O’Malley et al. Catherine Hobaiter, Kathelijne Koops, Bill McGrew, (2012) reported eighteen different observations Matthew McLennan, Deus Mjungu, Tweheyo that occurred over two years in seven different tree Mnason, Michio Nakamura, Rob O’Malley, Aimee species (three sources were unidentified) and again, Oxley, Vernon Reynolds and Janette Wallis for only one was Ficus sp. Continued monitoring at Issa providing information on chimpanzee insectivory will reveal whether a similar pattern holds. at field sites, and to reviewers for their constructive At Issa, fruit availability peaks in the late dry feedback. The UCSD/Salk Center for Academic season when Parinari curatellifolia and Strychnos Research and Training in Anthropogeny (CARTA) spp. comprise a large proportion of chimpanzee provides support to the Ugalla Primate Project. diet (Piel et al. unpublished data), whereas termite fishing is most frequent at the onset of the rains, in October-November (Stewart & Piel 2014). O’Malley LITERATURE CITED et al. (2012) do not discuss seasonal differences of ant-fishing at Gombe, and Nishida’s (2011) data Alp, R. 1993. Meat eating and ant dipping by wild suggest a bimodal distribution, of peak fishing chimpanzees in Sierra Leone. Primates 34(4): in the late dry (August-September) and mid wet 463–468. (December-January) seasons, when 62/99 (62.6%) Bermejo, M. & G. Illera. 1999. Tool-set for termite- sessions were observed. It is worth noting that these fishing and honey extraction by wild chimpanzees observed encounters do not control for search effort, in the Lossi Forest, Congo. Primates 40(4): 619– which may bias the results. At Issa, we do not yet 627. have sufficient data to assess seasonal patterns, but Boesch, C. & H. Boesch. 1990. Tool use and tool we predict that consumption rate will be similar to making in wild chimpanzees. 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An Evaluation of the Oral Microbiome and Potential Zoonoses of the Southern Thick-Tailed or Greater Galago (Otolemur crassicaudatus)
Antoinette Kotze1,2, Desire L. Dalton1,2*, Michael Strinden3, Michelle L. Sauther4, Frank P. Cuozzo5 and Anne C. Stone6
1National Zoological Gardens of South Africa, Pretoria, South Africa; 2Genetics Department, University of the Free State, Bloemfontein, South Africa; 3University of North Dakota School of Medicine and Health Sciences, Grand Forks, North Dakota, USA; 4Department of Anthropology, University of Colorado, Boulder, Colorado, USA; 5Department of Anthropology, University of North Dakota, Grand Forks, North Dakota, USA; 6School of Human Evolution and Social Change and Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, USA
Abstract: As the southern thick-tailed or greater galago (Otolemur crassicaudatus) is ubiquitous throughout parts of southern Africa they are thought to be of little conservation risk. As such, this species is seldom studied and relatively little is known of their behavior and biology. This research partially addresses this lack of knowledge by investigating the oral microbiome for potential zoonoses. Real-time PCR was used for the detection of Mycobacterium tuberculosis and M. leprae whereas next generation MiSeq Illumina sequencing was conducted on the 16S ribosomal RNA gene (16S rRNA) with a universal primer set which amplified the variable V3 and V4 regions to quantify the amount of different bacterial taxa. Major bacterial taxa of each tested oral microbiome were isolated, and those with potential for causing disease in humans and domestic animals were identified. The results illustrated a potential core microbiome for all O. crassicaudatus consisting of three separate bacterial taxa: Mannheimia caviae, Porphyromonas catoniae and Gemella cunicula that were present in all samples. The qPCR analysis did not detect the presence of mycobacteria. Several potentially pathogenic bacterial strains were observed that are known to result in disease in human and domestic animals. These findings thus form an important basis for several future avenues of potential research to assess any real zoonotic risks associated with O. crassicaudatus either to or from human and/or domestic animal populations of southern Africa.
Key words: Otolemur crassicaudatus, microbiome, 16s, zoonoses, next-generation sequencing
INTRODUCTION
The greater galago (Otolemur crassicaudatus) has the north; and O. c. monteiri, which is found in the a large distribution over most of southern Africa. Brachystegia miombo woodland zone from Angola A total of three subspecies of O. crassicaudatus in the west, to Zambia, Malawi and northern has been described: O. c. crassicaudatus, which is Mozambique in the east and north to Rwanda. reported only in the KwaZulu-Natal region; O. c. However, Grubb et al. (2003) reported that O. c. kirkii Gray, 1863, which ranges from Massangena, monteiri can further be divided into two groups: the Mozambique, in the south to southern Malawi in monteiri group, which is found from Angola through
Correspondence to: Desire Lee Dalton, National Zoological Gardens of South Africa, Box 254, Pretoria 0001, South Africa; Phone: +27 12 328 3265, Fax: +27 12 323 4540; E-mail: [email protected]. 20 / Kotze et al.
the southern Democratic Republic of the Congo, to the presence of both hard tissue surfaces and Zambia, Zimbabwe, northern Mozambique, Malawi mucosal surfaces (Zaura et al. 2009). However, use and southern Tanzania (Tabora), and the argentatus of the oral microbiome as a predictor of zoonoses group, which has an unknown distribution, although is a new and potentially important research reported in Rwanda, Kenya and Tanzania (Bearder approach, and has been applied to few nonhuman 2008). O. crassicaudatus is found in coastal forest primate taxa (Venezia et al. 2012, Mugisha et al. and riparian bushland in the southern parts of its 2014). Information on the oral microbiome of O. range and in bushland and open woodland in the crassicaudatus has not been noted previously. This northern parts of its range (Skinner & Chimimba species has not been reported to be linked with 2005). pathogen transmission and was selected as it is very The greater, or thick-tailed, galago O.( distantly related to humans and can live in close crassicaudatus), which averages a weight of proximity with humans. Thus, this study provides approximately 1,384 g (Nekaris & Bearder 2011), baseline knowledge in order to understand the type feeds primarily on gums and fruits and supplements and diversity of bacterial groups found within an its diet with insects (Nekaris & Bearder 2011). This isolated population of wild O. crassicaudatus as well species is found primarily in rural areas where they as to identify any known pathogens. have been found in small family groups (Clark 1985), often in larger vegetation such as tall trees routinely surrounded by lower scrub foliage and acacia trees MATERIALS AND METHODS (Nekaris & Bearder 2011). Zoonotic transmission represents a major Sample collection source of novel and emerging pathogenic infections Wild O. crassicaudatus individuals were sampled worldwide (Wolfe et al. 1998). It has thus become at the Lajuma Research Centre, which forms part of increasingly important to investigate potential the Luvhondo Nature Reserve within the UNESCO reservoirs of zoonotic disease for novel pathogenic Vhembe Biosphere Reserve in Limpopo Province, involvement in addition to those that are already South Africa, during the months of June and July, known to harm humans and livestock. Nonhuman 2013. This site consists of a mosaic of habitats that primates are important reservoirs of zoonoses. They includes marshland, thicket and riverine forest are taxonomically and genetically close to humans (Willems 2007). The areas adjacent to the reserve, and as such their parasites and pathogens are more however, have been altered by humans, with a likely to cross the species boundary than are those ranch along one border and a tourist lodge along from other taxonomic groups (Guerrera et al. 2003). another. Additionally, one area of the reserve was Rising human populations and anthropogenic formerly used as a fruit plantation. HavahartTM live pressures are resulting in humans and nonhuman traps and custom-made Chardonneret traps were primates being more frequently in close proximity zip-tied into trees and were baited with a mixture creating increasing opportunities for pathogenic of bananas and honey. Once secured in a trap, transfer (Chapman et al. 2005; Engel & Jones- individuals were anesthetised by a certified wildlife Engel 2012). In addition, nonhuman primates are veterinarian as prescribed in Larsen et al. (2011). frequently relocated from wild populations (De The oral microbiome was sampled in two ways: with Thoisy et al. 2001) and are kept in zoos, homes, and a Thermo Scientific AssayAssureTM kit and using a research centers that increase the amount of contact cheek swab (Epicenter) that was then placed in 700 with humans (Guerrera et al. 2003). This is often ul of buffer containing 50 mM Tris (pH 8.0, 50 mM done as a result of habitat loss, which is also one of EDTA, 50 mM sucrose, 100 mM NaCl and 1% SDS the major causes of zoonotic transfer and emergence (for collection of salivary mycobacterial samples, see of novel pathogens (De Thoisy et al. 2001). Abusleme et al. 2014). Both sides of the cheek were A key way to understand what pathogens a swabbed as well as under the pseudo-tongue, which given species harbors is through investigation of is where the majority of saliva pooled (Figure 1). their microbiomes. Studies have been conducted on both Homo and Pan salivary and oral microbiomes in order to understand bacterial diversity and 16 S DNA extraction and detection individual health (Li et al. 2013). The oral cavity is DNA extraction was conducted using the ZR usually selected both for ease of sampling - as it is Genomic DNATM Tissue MiniPrep kit from Zymo minimally invasive - as well as for the propensity Research following the protocol as outlined by the of different bacteria to colonize the oral cavity due manufacturer. Each sample was screened for the Oral Microbiome of Southern Thick-Tailed Galagos / 21
Figure 1. Oral swab of wild Otolemur crassicaudatus at Lajuma Research Centre. Photograph by M. Sauther. presence of bacteria by analyzing the prokaryotic 16S was added in order to lyse cells. Samples were then ribosomal RNA gene (16S rRNA) with a universal placed into a rotisserie incubator at 55 - 65°C for primer set which amplified the variable V3 and V4 a period of one hour to catalyze the lysis process. regions of the 16S rRNA gene in single amplicon Extraction was performed using the Phenol- of 460 bp (Frank et al. 2008). Samples (n=8) were Chloroform method. The TaqMan qPCR tests submitted to the Agricultural Research Center were conducted at Arizona State University using (ARC, South Africa) for analysis using an Illumina protocols described in Harkins et al. (2015). Four MiSeq high-throughput sequencing platform. separate qPCR tests were run, two for M. tuberculosis Analysis was conducted on BaseSpace, a MiSeq DNA and two for M. leprae DNA. Of the two M. Reporter Metagenomics workflow which performs tuberculosis qPCRs, one targeted the single-copy a taxonomic classification using an Illumina- rpoB gene (the rpoB2 qPCR) and one targeted the curated version of the Greengenes 16S rRNA gene M. tuberculosis complex-specific multi-copy IS6110 database providing information on genus or species insertion element (Klaus et al. 2010; Harkins et al. level classification. In addition, samples were 2015). To detect the presence of M. leprae DNA, analysed in Genomics Workbench where primer qPCRs targeting the 85B single-copy gene and the sequences were removed and reads were grouped rlep multi-copy gene were used (Martinez et al. into operational taxonomic units (OTUs). In order 2006; Truman et al. 2008). The four primer sets used to compare OTU prevalence and to identify the top are listed in Appendix 1. Each qPCR reagent set eight contributions, the percentage abundance was consisted of varying concentrations of primer, probe, determined (# of reads for strain/total # of reads), in Rat Serum Albumin and Taq Master Mix. Standards all of the O. crassicaudatus samples. were included in duplicate with concentrations varying from 5e-1 – 5e-5 ng/µL. Two non-template Mycobacterium tuberculosis and M. leprae controls were also included to test for contamination detection and samples were run in triplicate. The qPCR Prior to the extraction of DNA, each sample thermocycling conditions for the ABI7900 consisted (n=24) was incubated at 80°C for a period of one of one cycle of two min at 50°C, one cycle of 10 min hour to kill any remaining harmful viable bacteria. at 95°C followed by 50 cycles at 95°C for 15 sec and After incubation, 25 µL of Proteinase K (10 mg.mL) 60°C for one min. 22 / Kotze et al.
RESULTS crassicaudatus may be able to do so elsewhere, i.e., in closer proximity to human populations or where In this study, the overall number of bacterial taxa, human populations utilizing bushmeat. Thus, we both indefinable and non-identifiable, in randomly cannot discount the possibility of O. crassicaudatus selected oral microbiomes was parsed from the acting as a reservoir for these two pathogens samples. Both the MiSeq Reporter results as well elsewhere (Deredec & Courchamp 2003). as analysis on Genomics Workbench used to group As humans could also be at risk from galago- OTUs with at least 97% identity provided similar borne diseases, especially in the context of keeping results. In addition, the top eight bacterial taxa were galagos as pets, consuming them as bushmeat, or identified (Table 1) and abundance of each bacterial other documented contact (Linden 2015, Tshikudo taxon per sample was determined (Table 2). The 2015), the investigation of the oral microbiome highest bacterial taxon in each sample was unknown revealed many bacterial strains (Table 3) that are and could not be identified to genus or species level opportunistically pathogenic to humans, primarily (Table 1.). A total of four bacterial strains that were those which cause endocarditis, a potentially fatal identified have been reported to have pathogenic inflammation of cardiac tissues due to injury or implication in humans and/or livestock (Table severe illness (Mayo Clinic 2014). Another key 3). Amplification of M. leprae and M. tuberculosis result is the suspected interplay in bacterial ecology DNA via qPCR was not detected in any of the tested between O. crassicaudatus, domesticated ungulates, samples. However, qPCR was considered successful and humans. One potential bacterial microbiome as amplification occurred for the standards and was species, discovered in 40% of tested samples, was absent in the non-template control. Streptococcus bovis, a bacterium that is commonly found in the alimentary tract of ruminants and causes neonatal septicemia and meningitis in DISCUSSION humans (Russell & Hino 1985). The source of this bacterium is unknown, but there were several The identifiable oral microbiome of wildO. free ranging horses at the research centre during crassicaudatus was found to consist of three bacterial the research period and there are also farms with species: Mannheimia caviae, Gemella cunicula, and cattle around the surrounding area. There is thus a Porphyromonas catoniae. This finding is similar potential of pathogen transmission to humans and to previous studies of human populations where domestic animals, but this would require further they found a core microbiome in unrelated healthy research. humans. A study on the oral microbiome of humans The large number of previously unidentified conducted by Zaura et al. (2009) in three healthy bacterial strains is also an important finding. It individuals found that the individuals shared is because of this gap in our knowledge that we 1660 of 6315 unique sequences of which the core are unable to say if those strains are potentially microbiome was observed in 66% of the reads. A hazardous or benign in this population. This study core microbiome in five healthy individuals has thus offers important baseline data to provide a also been reported by Lazarevic et al. (2010). These greater understanding of how susceptible nonhuman three bacterial taxa observed in our study can primates are to human pathogens and vice versa, thus potentially be considered the “universal core”, something of great concern to conservationists, meaning all O. crassicaudatus will exhibit these wildlife biologists, and zoo health officials (De bacteria in addition to their individually diverse Thoisyet al. 2001; Engel & Jones-Engel 2012). loads. However, microbiome studies are in their infancy and larger scale projects would be required ACKNOWLEDGMENTS in order to both identify core and individual microbiomes. Thus, the results reported here may We would like to thank A. Tordiffe, H. only pertain to animals sampled from the Lajuma Brettschneider and Ms G. Hausman for their study site and further larger scale analysis could expertise and guidance. In addition, we would like elucidate whether this proves to be true in other to thank Dr. I. Gaigher for his support of the project regions as well. at Lajuma. Funding for the project was provided by No mycobacterium loads were detected. While the University of Colorado, the University of North this means that this particular population of sampled Dakota, and the National Zoological Gardens of individuals is not harboring these mycobacteria, South Africa. it does not preclude the possibility that O. Oral Microbiome of Southern Thick-Tailed Galagos / 23 8th Highest aeria Rothia Planococcus maritimus Streptococcus peroris Fusobacterium naviforme Leptotrichia goodfellowi Aggregatibacter aphrophilus Lautropia mirabilis Gemella cunicula Avibacterium avium 7th Highest Butyrivibrio proteoclasticus Sneathia sanguinegens Moraxella caviae Ureaplasma gallorale Streptococcus peroris Aggregatbacter aphrophilus Sneathia sanguinegens Moraxella caviae Streptococcus peroris Veillonella dispar 6th Highest Streptococcus bovis Butyrivibrio proteoclasticus Lautropia mirabilis Sneathia sanguinegens Butyrivibrio proteoclasticus Fusobacterium naviforme Fusobacterium naviforme Streptococcus bovis aeria Rothia Aggregatibacter aphrophilus 5th Highest Porphyromonas catonaie Streptococcus bovis Streptococcus bovis Fusobacterium navidorme Ureaplasma gallorale cunicula Gemella cunicula Gemella Butyrivibrio proteoclasticus Streptococcus sanguinis Corynebacterium durum 4th Highest Moraxella caviae Gemella cunicula Porphyromonas catoniae Porphyromonas catoniae Porphyromonas catoniae Porphyromonas catoniae Butyrivibrio proteoclasticus Gemella cunicula Aggregatbacter aphrophilus Streptocaucus peroris 3rd Highest 3rd Gemella cunicula Porphyromonas catoniae Gemella cunicula Gemella cunicula Gemella cunicula Butyrivibrio proteoclasticus Porphyromonas catoniae Porphyromonas catoniae Neisseria lactamica Gemella cunicula 2nd Highest Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae 1st Highest 1st at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level at Unspecified Species Level 703 790 682 652 554 684 792 901 887 883 tributors # of Con- # of Sample C35F 3C15 5F87 58A3 98C7 2979 5010 8123 Cap1 Cap3 Table 1. Top eight contributors of distinct bacterial taxa for each oral microbiome sample. each oral microbiome bacterial distinct taxa for of contributors eight 1. Top Table 24 / Kotze et al. 9 7 9 % 10 10 12 10 19 10 12 4th Highest Other Other Other Other Other Other Other Other Other Other % 6 13 7 11 5 5 13 5 3rd Highest 3rd cunicula Gemella Porphyromonas catoniae cunicula Gemella cunicula Gemella Butyrivibrio proteoclasticus Porphyromonas catoniae Porphyromonas catoniae cunicula Gemella % 19 26 16 14 32 20 10 16 6 21 2nd Highest caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia caviae Mannheimia % 66 51 70 76 45 65 74 52 84 62 1st Highest 1st Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified Species at Level Unspecified 703 790 682 652 554 684 792 901 887 883 tributors # of Con- # of Sample C35F 3C15 5F87 58A3 98C7 2979 5010 8123 Cap1 Cap3 Table 2. Abundance (number of reads identified/total number of reads) of reads)species. bacterial of number reads identified/total of (number 2. Abundance Table Oral Microbiome of Southern Thick-Tailed Galagos / 25
Table 3. Identified bacterial pathogens and their known effects. Bacterial Strain Human pathogenic involvement Livestock pathogenic involvement Gemella cunicula Endocarditis, Meningitis, Arthritis and No known pathogenic effects Pneumonia Streptococcus bovis Colorectal Cancer, Endocarditis, Meningitis Ruminal Acidosis and Feedlot Bloat and Neonatal Septicemia Fusobacterium Lemierre Syndrome and Generalized No known pathogenic effects naviforme Inflammation Mannheimia No known pathogenic effects Conjunctivitis caviae
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Appendix 1: Primers and TaqMan probes used for mycobacterial qPCR.
Primer /probe name Sequence RpoB2_F 5’- CAA CGT CGA GGT GCT ATC G -3’
RpoB2_R 5’- CTC CAG GTC CTC GTC CTC A -3’
RpoB-Probe 5’- 6FAM-TCG CCG CAC CGT CAC T-MGBNFQ-3’
Rlep_F 5’-GCA GTA TCG TGT TAG TGA A-3’
Rlep_R 5’-CGC TAG AGG GTT GCC GTA TG-3’
Rlep_Probe 5’- 6FAM-TCG ATG ATC CGG CCG TCG GCG-MGBNFQ-3’
IS6110-F 5’-GGG TAG CAG ACC TCA CCT ATG TG-3’
IS6110-R 5’-CGG TGA CAA AGG CCA CGT A-3’
IS6110-Probe 5’- 6FAM-ACC TGG GCA GGG TT-MGBNFQ-3’
85B-F 5’-GTG GTC GGC CTC TCG AT-3’
85B-R 5’-CGA GCC AGC ATA GAT GAA CTG ATC-3’
85B-Probe 5’- 6FAM-CTC GGC CCT AAT ACT-MGBNFQ-3’ African Primates 11(1): 27-36 (2016)/ 27
Observation of an Encounter between African Wild Dogs (Lycaon pictus) and a Chimpanzee (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania
Edward McLester1,2, Fiona A. Stewart1,3 and Alexander K. Piel1,2
1Ugalla Primate Project, Uvinza, Tanzania; 2School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK; 3Department of Archaeology, University of Cambridge, Cambridge, UK
Abstract: There has been considerable discussion of chimpanzees Pan( troglodytes) as predators, most commonly of red colobus monkeys (Procolobus spp.). Far more infrequent are published descriptions of chimpanzees as prey. The paucity of direct observations of chimpanzee-predator encounters is an obstacle in situating chimpanzees in both predator and prey roles. For the first time, we describe an observation of an encounter between African wild dogs (Lycaon pictus) and a chimpanzee in the Issa Valley, Tanzania, one of the driest and most open chimpanzee habitats. Whilst the initiation of the encounter was missed, here we nonetheless interpret the data that we did record. Our observations of behavior in both parties suggest the possibility of an investigatory rather than predatory encounter on the part of the wild dogs.
Key words: wild dog, chimpanzee, Pan troglodytes, predation, carnivore, prey
INTRODUCTION
The role of predation as a selection pressure on from anecdotal observations and playback studies great ape evolution remains unclear; however, this (Crockford et al. 2012). can in part be attributed to an absence of records Reports of direct observation of carnivore describing primate-predator interactions (Cheney predation on chimpanzees are rare in the literature & Wrangham 1987). Historically, researchers have (Table 1). First, most chimpanzees live in dense, identified four potential mammalian predators of tropical forests, which lack many of the large wild chimpanzees (Pan troglodytes): lions (Panthera carnivore species that live in savanna mosaics (eg., leo), leopards (P. p ardu s ), spotted hyenas (Crocuta lion, cheetah – Mills & Funston 2011). Second, the crocuta) and African wild dogs (Lycaon pictus) (Tutin only fully habituated savanna-dwelling chimpanzee et al. 1981; Boesch 1991; Stewart & Pruetz 2013). community, Fongoli, in Senegal, lives in an area Outside of Zuberbühler & Jenny’s (2002) study of where almost all of the natural predators no longer leopard predation in the Taï Forest, Côte d’Ivoire, range due to human population expansion (Stewart none of these carnivore species have been studied & Pruetz 2013). Finally, given the selective pressure in detail in areas of sympatry with chimpanzees. on anti-predatory behaviors, actual predation Consequently, substantiation of chimpanzee events are themselves rare, even in the most pristine predators, and in turn our understanding of landscapes. Apes generally rely more on predator chimpanzee antipredator strategies, is derived avoidance and vigilance than defensive counter-
Correspondence to: Edward McLester, School of Natural Sciences and Psychology, Liverpool John Moores University, James Parsons Buildinng, Byrom Street, Liverpool, L3 3AF, UK; E-mail: [email protected]. 28 / McLester et al.
et al. et . 2013 2005 Source et al . 1981 1996 et al. et et al et al. et Gandini & Baldwin 1978 Gandini Tutin Hiraiwa-Hasegawa 1986 Nakazawa 1968 Nishida 2006 Kutsukake Lawick-Goodallvan 1968 “ “ 2009 Pierce 1966 & Itani Izawa Boesch 1991 2002 & Jenny Zuberbühler Henschel 2000 Furuichi Rahm 1967 Hart 1998 Ososky . 2012). et al (modified Klailovafrom Notes tree of chased out Chimpanzees or vocalizing, hiding chimpanzees of instances Multiple by leopard to detection response in fleeing den, killed cub leopard raided Chimpanzees corpse chimpanzee near prints and feces Leopard leopard at threw branches Chimpanzees to in response alarm vocalizations gave Chimpanzees vocalizations leopard below leopard vocalized in tree at infant Chimpanzee vocalizing in vicinity leopard to in response reaction No leopard at threw branch Chimpanzees vocalized leopard mobbed Chimpanzees and vocalized of and in direction branches shook Chimpanzees in vicinity leopard and mobbing chimpanzees including interactions, Multiple attributed mortalities chimpanzee 39% of leopards; chasing predation leopard to in some leopard; by scavenged juveniles Dead chimpanzee drumming chimpanzee to response fled in cases, leopards vocalizations and remains chimpanzee contained feces Leopard remain chimpanzee containing feces and prints Leopard corpse a chimpanzee near found killed infant and attacked chimpanzees Female remains chimpanzee contained feces Leopard remains chimpanzee contained feces Leopard Pan troglodytes Pan X X X X X X X X X X X X X X Indirect Indirect Evidence
X X X X Direct Evidence
Park Idambo Ituri Forest Ituri Population Petit Loango Loango Petit National Park National Park National Kasakati Basin Kasakati Gombe National National Gombe Taї National Park National Taї Mahale Mountains Mountains Mahale Koba National Park National Koba Lopé National Park Lopé National Mt. Assirik, Niokolo Niokolo Assirik, Mt. Ndoki National Park National Ndoki Mbeli Bai, Nouabalé- Mbeli Bai,
DRC Congo Gabon Senegal Country Tanzania Republic of of Republic Ivory Coast ) Panthera pardus Predator Leopard ( Table 1 Summary of evidence describing carnivore interactions on 1 Summary on evidence of interactions carnivore describing Table Encounter between African Wild Dogs and a Chimpanzee / 29 et al. al. et Source . 1981 . 1981 . 1981 et al et al et al Tutin Tutin in (pers. obs.) M. Mbrisho Goodall 1986 Hiraiwa-Hasegawa 1986 1993 Tsukahara 1993 & Tsukahara Inagaki 1979 1972; Itani Kano Tutin Tutin Zamma 2011 Lawick-Goodallvan 1968 Lawick-Goodallvan 1968 Lawick-Goodallvan 1968 . 2012) (continued). et al (modified Klailovafrom Notes or vocalizing, hiding chimpanzees of instances Multiple lion by detection to in response reaction no showing flee to forced lion until threw branches Chimpanzee killed and cub lioness adult an mobbed Chimpanzees hair, (bones, remains chimpanzee contained feces Lion teeth) remains chimpanzee contained feces Lion to vocalized response and in up trees fled Chimpanzees lion hiding reaction No wild to dog vocalizedChimpanzees in response presence and vocalizations to response in retreated vocalized and first Chimpanzees python for waited and then tracked python, discovering area it left after to in response branches vocalized shook Chimpanzees and python dying which after escaped, it adder until night hit Chimpanzees follow did not chimpanzees throwing once chasing, chimpanzees of instances Multiple to in response reaction no showing once and at, rocks lizards monitor nearby Pan troglodytes Pan X X X X X X X X X X X X Indirect Indirect Evidence Direct Evidence Park Park Park Ugalla Kigoma Population National Park National Park National Gombe National National Gombe National Gombe National Gombe Mahale Mountains Mountains Mahale Mountains Mahale Koba National Park National Koba Park National Koba Park National Koba Mt. Assirik, Niokolo Niokolo Assirik, Mt. Niokolo Assirik, Mt. Niokolo Assirik, Mt. Senegal Senegal Senegal Country Tanzania Tanzania Tanzania Tanzania
) ) pictus ) Crocuta
) species) Panthera Panthera ) Lycaon Causus Varanus Predator ( Lion leo ( Hyena crocuta Dog Wild ( Python (unk. Python Adder Night ( rhombeatus Monitor Nile ( niloticus Table 1 Summary of evidence describing carnivore interactions on 1 Summary on evidence of interactions carnivore describing Table 30 / McLester et al.
Figure 1. L. pictus and P. troglodytes ranges across sub-Saharan Africa (Oates et al. 2008; Woodroffe & Sillero- Zubiri 2015). Areas of range overlap are indicated by circles.
attacking (Treves & Palmqvist 2007). For example, an encounter between wild dogs and a group of chimpanzees produce alarm calls (“waa barks” - chimpanzees at the same site; however, only limited Schel et al. 2013) in response to terrestrial predators details were provided with no reference to the and adjust their sleeping behavior to predator behavior of either party except for the vocalizations presence, nesting higher in the canopy and on more issued by the chimpanzees. peripheral branches when they co-exist with large Aside from the single interaction reported in carnivores (Pruetz et al. 2008; Stewart & Pruetz brief by Tutin et al. (1981), to date there have been 2013). no prior observations of chimpanzees encountering Indirect evidence of carnivore predation on apes African wild dogs. Wild dogs have both extremely and especially chimpanzees is more common than large home ranges (mean = 537km2, range: 357- direct evidence, yet still infrequent (Table 1). Of the 930km2 - Mills & Gorman 1997) and live at very four mammalian species identified as chimpanzee low densities (16.7 individuals per 1000km2 - predators, only six cases have been inferred for Maddock & Mills 1994), a similar pattern to savanna lion predation, none of which involved direct chimpanzees (reviewed in Moyer et al. 2006). At the observation. Numerous reports have described Issa Valley in Tanzania, reports on chimpanzee and leopards as a primary threat to wild chimpanzees, sympatric wildlife date to the 1950s (Kano 1971, but only four direct encounters have been described. 1972), and yet we describe here only the fourth Tutin et al. (1981) observed the sole chimpanzee- researcher-encounter with wild dogs. Despite both hyena encounter, in which chimpanzees in Mt. species being widely distributed across Africa, Assirik (Senegal) did not exhibit any anti-predatory current chimpanzee and wild dog ranges overlap in or unusual behavior in response to wild spotted only three areas (Figure 1). Such a small degree of hyenas. Tutin et al. (1981) also briefly recorded overlap also existed in historic distributions, largely Encounter between African Wild Dogs and a Chimpanzee / 31
Figure 2. Map of western Tanzania, indicating location of Issa Valley study site in relation to Gombe and Mahale Mountains National Parks. Vegetation index shows woodland and forest cover; predicted chimpanzee distribution shows suitable nesting habitat (Pintea 2007). due to the restriction of wild dog populations to METHODS dry, savanna landscapes (Creel & Creel 1998; Oates et al. 2008). Furthermore, given their population The Issa Valley research station in western densities, it is extremely unlikely that these two Tanzania is an “open area” with no formal species encounter each other frequently. Here, we protection status, situated in the north of the Greater report on only the second observation of such an Mahale Ecosystem (Figure 2). The entire region is encounter. characterized as a savanna-mosaic, with deep valleys 32 / McLester et al.
Figure 3. Adult male chimpanzee feeding on Brachystegia spiciformis in miombo woodland in the Issa Valley. Photograph by E. McLester.
containing evergreen, riverine forest and separated (hyena, leopard, lion, and wild dog). Although there by steep slopes and expansive, flat plateaus of are no permanent settlements in the study area, miombo (Brachystegia and Julbernardia) woodland, illegal logging, poaching, and herding do account rocky outcrops and grassland swamps (Piel et al. for human traffic throughout the region (Pielet al. 2015). From 2009-2014, annual rainfall averaged 2015). 1240mm and temperatures ranged from 11-35°C At least one two-person research team tracked (Piel et al. 2015). chimpanzee parties daily by listening for loud Ugalla chimpanzees were first studied by Kano calls and monitoring important feeding trees, as over a half-century ago (Kano 1971, 1972), with brief well as conducting reconnaissance walks around surveys conducted subsequently (Nishida 1989), the study area. In collaboration with the Pan and a project ongoing in Nguye, south of Uvinza Africa Programme of the Max Plank Institute for (Ogawa et al. 2007; Iida et al. 2012; Yoshikawa & Evolutionary Primatology, Leipzig (Germany), we Ogawa 2015). Issa Valley chimpanzees (Figure 3) also deployed twenty-six motion-triggered cameras were first studied in 2001 by Hernandez-Aguilar (Bushnell HD) on known wildlife paths, with the aim (2009) for two years, and since 2008 have been of monitoring biodiversity, especially chimpanzees under continuous study, with habituation efforts and cryptic species. beginning in 2012. As of December 2015, fourteen chimpanzees were individually recognizable to researchers, and genetic analyses suggested a single RESULTS community of at least 67 individuals (Rudicell et al. 2011), which may range over 150km2 based on At 14:04 on 7 July 2015 EM and a field assistant population density (0.25 individuals/km2 - Piel et al. heard two simultaneous vocalizations – the first 2015). In addition to chimpanzees, the region has chimpanzee “waa barks” (Schel et al. 2013), the other a rich faunal community, including eight species dog barks – approximately 25 meters away from of primate and four species of large carnivores a clearing in a patch of evergreen forest, bordered Encounter between African Wild Dogs and a Chimpanzee / 33 by a river on one side and a woodland slope on the other side. On approaching the sounds, we observed an adult chimpanzee (sex unknown) approximately 20 meters away and 15 meters high in a tree (Vitex doniana) and a pack of nine wild dogs moving around the base of the tree, looking up and barking at the chimpanzee. We never observed more than nine dogs at a single time during the encounter. For over a minute, both the chimpanzee and dogs barked continuously. Whilst issuing these vocalizations, the chimpanzee jumped up and down, and paced back and forth about ten meters along a single branch, raising and lowering its arms in a rapid motion. It was not observed whether the Figure 4. Image of a wild dog captured on a motion hair of the chimpanzee was erect. Eventually, the triggered camera in the Issaa Valley on 21 August, 2015. chimpanzee’s vocalizations became more regular, Photograph courtesy UPP/MPI-EVA. being produced approximately every two minutes. The dogs in our view fixed their attention on the captured wild dogs (Figure 4; see supplementary chimpanzee, tracking it from the ground as the video1), including one of dogs chasing a blue chimpanzee continued to pace on the branch. As duiker (Philantomba monticola). This is the first bark and growl vocalizations continued to be heard, camera encounter with wild dogs in five years of the dense undergrowth and rapid movement of the monitoring wildlife with 20-25 motion-triggered dogs prevented us from identifying whether all dogs cameras (>20,000 photos and videos). The camera in the party were vocalizing. was located approximately 1.61km from the wild After approximately six minutes, four dogs dog encounter described above. The spatiotemporal looked at and began to approach us, stopping about information of each encounter, combined with what 20 meters from us. These dogs, moving toward us we know of wild dog ranging behavior (see below), in stagger, eventually reached about 15 meters from means it is extremely likely these observations us. The dogs looked directly at us, but remained represent the same pack. silent. They appeared to be investigating us, and did not adopt a stalking posture (see Estes & Goddard 1967). For example, the ears of each individual DISCUSSION remained clearly upright versus flattened down against the head. This shift in attention lasted almost Whereas numerous characteristics ultimately three minutes. determine prey preference, a comparison of weight After approximately eight minutes without preference, for example, in fourteen wild dog vocalizing, the chimpanzee descended in the tree to populations by Hayward et al. (2006) found that wild about ten meters from the ground, and out of our dogs prefer animals between 16-32kg and 120-140kg sight. We were unable to see its position. At this (Hayward et al. 2006). The mean weight of small point, the activity of all of the dogs’ activity changed, adult and juvenile chimpanzees (males: 28-56kg; resulting in more dog vocalizations and movement females: 20-46kg - Foley et al. 2014) suggests that of the entire pack toward the last location of the chimpanzees would fit wild dog prey preferences; chimpanzee (and, consequently, out of our sight). however, prey of this smaller size would probably As we attempted to gain a better view, we continued only be targeted opportunistically or during times to hear dog vocalizations approximately 30 meters of food scarcity (Schaller 1972). Numerous other away for a further minute, but we could see neither species found in the study area, including common pack members nor the chimpanzee. When we (Sylvicapra grimmia) and blue (P. monticola) attempted to follow both parties at approximately duikers, klipspringers (Oreotragus oreotragus), 14:13, we saw a single wild dog moving out of the and roan antelope (Hippotragus equinus), provide forest and into the woodland approximately 20-30 wild dogs with targets that are more vulnerable meters away from the encounter site. We did not see or hear the dogs again. On 21 June, two weeks after the encounter, 1 Supplementary video may be viewed at: https://www. two sequential videos on the same camera trap youtube.com/watch?v=lP1gDqnjw50. 34 / McLester et al.
to exhaustion after a sustained chase (Tayloret al. established between other predators (e.g., leopards 1971), versus those that can escape into the canopy – Zuberbühler & Jenny 2002) and chimpanzees like chimpanzees and other primates. Arboreal prey indicate that predation from African wild dogs provide a different stimulus to prey fleeing along the is similarly unlikely to have acted as a significant ground and are less likely to elicit a chase reflex in selection pressure. Even when these species do wild dogs, which is critical to prey selection (Estes & encounter each other, the circumstances suiting Goddard 1967). opportunistic predation – such as in times of food Our observation suggests the possibility of scarcity or when encountering an ill, old, or weak investigatory behavior by the dogs. The wild dogs chimpanzee – are limited and depend on both an produced alarm barks, indicating alertness (Estes appropriate trigger that will provoke a chase reflex, & Goddard 1967), rather than the “twittering” and the prospect of the prey being caught through typically issued during a hunt. The chimpanzee pursuit; however, we are confident that in encounters also issued alarm calls and only attempted to move with such suitable conditions wild dogs would be away from the wild dogs at least eight minutes into capable of predating chimpanzees. the encounter, despite access to the tree canopy Savanna chimpanzees are known to exhibit throughout. This is consistent with the use of alarm behaviors not observed in forest-dwelling calls as a deterrent in primates (Zuberbühler et al. populations (e.g., using tools to hunt bushbabies – 1999). On the part of the chimpanzee, the agitation Pruetz & Bertolani 2007), suggesting that behavior seen suggests aversion or threatening behavior in predator-ape interactions is also likely different toward the wild dogs rather than curiosity. Curiosity given such contrasting environments. Although typically involves soft “huu” vocalizations and we cannot conclude from our observation that persistent observation without agitation (Schel et al. African wild dogs actively hunt chimpanzees, our 2013). description provides the first direct evidence of the The behavior exhibited by the dogs toward the behavior of both predator and potential prey in a research team (curiosity) can also not be compared wild dog-ape encounter. directly with their behavior toward the chimpanzee (excitement). This may be because the density of ACKNOWLEDGMENTS chimpanzees in the area and the large range of the wild dogs has resulted in the dogs being more We thank the Tanzanian Wildlife Research familiar with chimpanzees than with humans. Given Institute (TAWIRI) and the Commission for Science the presence of poachers and herders in the area and Technology (COSTECH) for permission to who are known to react antagonistically to predators conduct research in the Issa Valley, and to the (AKP personal observation), we suspect that any UCSD/Salk Center for Academic Research and previous wild dog encounters with humans would Training in Anthropogeny (CARTA) for support to likely have been persecution and, therefore, our the Ugalla Primate Project. The Max Plank Institute quiet and motionless presence was probably novel for Evolutionary Anthropology, Leipzig, provided for them. This behavior from the dogs is consistent the camera used in this study and also partial with what has been described previously for wild financial support. We thank Mlela Juma for helping dog investigation of sympatric, non-prey species to record and recount events and Adrian Treves (Darnell et al. 2014). and three anonymous reviewers for providing Previous observations of wild dogs in the extremely helpful feedback on an earlier version of Issa Valley study area are limited. Aside from the this manuscript. sole camera encounter following this interaction, Hernandez-Aguilar (2006) observed indirect evidence of wild dogs approximately every three LITERATURE CITED months, with two direct observations in 21 months. Likewise, Stewart & Pruetz (2013) observed wild Boesch, C. 1991. The effects of leopard predation dogs only once in twelve months. The consistently on grouping patterns in forest chimpanzees. low number of wild dog observations over a ten- Behaviour 117: 220–242. year period at Issa suggests that wild dog presence, Cheney, D.L. & R.W. Wrangham. 1987. Predation. and in turn wild dog-chimpanzee encounters, In Primate Societies. B.B. Smuts, D.L. Cheney, do not occur frequently enough for wild dogs to R.M. Seyfarth, R.W. Wrangham, T.T. Struhsaker, have played a significant role on chimpanzee anti- eds. University of Chicago Press, Chicago. Pp. predatory behavioral evolution. Relationships 227–239. Encounter between African Wild Dogs and a Chimpanzee / 35
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An Infanticide Attempt After Male Takeover in Diana Monkeys (Cercopithecus diana diana) in Taï, Côte d’Ivoire
Erin E. Kane1,2 and Frederic Gnépa2
1Department of Anthropology, The Ohio State University, USA; 2Taï Monkey Project, Taï, Côte d’Ivoire
INTRODUCTION
The killing of infants by conspecific males has been directly observed in 35 species of wild primates and its occurrence has been inferred in an additional 16 species (Palombit 2012). A meta- analysis of observed and suspected infanticide revealed that: infanticidal males tended to be related distantly, if at all, to infants they attacked; females who lost infants to infanticide tended to resume ovarian cycling quickly after the infant loss; and males who attempted infanticide were more likely to have sexual access to females than males who do not (van Schaik 2000). Several competing hypotheses attempt to explain the occurrence of infanticide in primate taxa. Sarah Blaffer Hrdy (1974, 1994) proposed that infanticide is an adaptive, sexually selected strategy for infanticidal males. By killing the unweaned offspring of rival males, infanticidal males bring about the premature end of lactational Figure 1. An adult female Diana monkey in Taï National Park. Photograph by E. Kane. amenorrhea and resumption females’ estrous cycles. Other researchers contend that infanticide is an unnatural behavior, a social pathology resulting (Cercopithecus diana) in Taï National Park (Figure from overcrowding and anthropogenic habitat 1), Côte d’Ivoire and assess which hypothesis best disturbance (Curtin & Dolhinow 1978). A third explains this observation. hypothesis suggests that infanticide is a byproduct of generalized aggression following male transfer and/or male acquisition of higher dominance status: METHODS infant death in these cases is a side effect of male aggression (Bartlett et al. 1993; Sussman et al. 1994). The incident occurred in the study grid of the Here, we report an attempted infanticide Taï Monkey Project, an approximately 1 km2 area of following the replacement of the resident adult evergreen rain forest on the western border of Taï male in a group of free ranging Diana monkeys National Park. Taï National Park in Southwestern
Correspondence to: Erin E. Kane, Department of Anthropology, 4034 Smith Laboratory, 174 W. 18th Street, The Ohio State University, Columbus, OH USA 43210; E-mail: [email protected]. 38 / Kane and Gnépa
Côte d’Ivoire is the largest remaining intact segment with the group prior to October 13. At 07:35, the of the Upper Guinea Forest in West Africa. It is group began vocalizing with females emitting high- primarily composed of 330,000 ha of protected pitched alarm calls. At 07:38, an adult male in the primary moist evergreen rainforest, with a 20,000 ha upper canopy chased several adult females (including buffer zone surrounding the park’s boundary. At the Melo), and a subadult female. At 07:41, the male study site of the Taï Monkey Project, seven species of lunged at Melo, and the infant fell from her ventrum monkey are habituated and have been under regular about 15 m to the ground. The infant immediately observation since 1989, including Diana monkeys, started screaming, and most of the adult females who live in single male groups and exhibit female in the group gathered in the canopy directly above philopatry (Buzzard & Eckardt 2007). The primate the infant, staring down at it and making contact community in Taï also includes several prosimians, calls. Melo attempted to climb down to the ground an additional monkey species rarely found in the at 07:46 and 07:54, but on both occasions, the adult study grid (spot-nosed monkey, C. nictitans), and the male chased her into the upper canopy. At this point, Western subspecies of chimpanzee (Pan troglodytes we recognized that this was not the resident male verus) (McGraw et al. 2007). (Fred), but a different male whose tail was bleeding Observations reported here were made by the and broken at the tip. authors using ad libitum notes (Altmann 1974) in At 08:06, an adult female who is frequently in the course of all-day follows of habituated Diana proximity to Melo climbed down towards the baby, monkey (Cercopithecus diana diana) groups during but the new male lunged at her with bared teeth which routine feeding data were being collected. and she climbed back up to the understory. She This group has been under regular study since descended to the ground a second time at 08:14 and 1989, and all adults are individually recognized. briefly touched the baby with her hand, but almost F. Gnépa has been the primary observer of this immediately climbed back up to the main canopy. group since January 2010; E. Kane began following Adult females who had been vocalizing with contact this study group in June 2013. At the time of these calls stopped calling and climbed up to the main observations, the group consisted of one adult male canopy. The infant, still on the ground, continued (Fred), eight adult females, two subadult females, screaming. and several juveniles of unknown sex. Following At 08:16, a solitary adult male chimpanzee these observations, Fred disappeared and the new appeared about 5 meters from the infant. He was male whose behavior is reported here remained in not calling or buttress drumming, and the Diana the group as the resident male. monkeys made no alarm calls before his approach. He approached the infant and picked it up by the ankle, running and dragging it behind him for RESULTS about 40 meters before throwing it against the trunk of a Piptadenastrium africanum tree and running We began our week of daily follows on October away from the group. At 08:25, the infant started 13, 2013, and that day recorded the presence of screaming again. At 8:29, Melo descended to the the group’s resident male, Fred, all adult females, ground and picked up the baby, who immediately subadults, and juveniles. We observed no infants in started nursing. Melo was peripheral to the group the group on October 13 or on any day prior. Our for the rest of the day, and we did not observe her final scan sample at 18:00 on the evening of October interacting with the strange adult male. Several 13 is the last time we observed Fred in the group. other adult females chased this new adult male twice Heavy rainfall on October 14, 2013, prevented during the day but we observed no further physical data collection during that day. On October 15, we contact. We left the group at 18:05. arrived at the group’s sleeping tree at 07:00 and found Our next contact with the group was at 06:45 group members either resting or foraging on insects the morning of October 16. Our first observation of in the upper canopy. The group was in a polyspecific Melo was at 07:30, and we did not observe her, or any association with three other taxa: Piliocolobus badius, other female, carrying an infant. We did not see the Procolobus verus, and Cercopithecus campbelli. infant after October 15. No other infants were born At approximately 07:15, we observed that an in this group in 2013, although two infants were born adult female (Melo) had an infant clinging to her in an adjacent group during October 2013, both of ventrum; we suspect this infant was born between whom survived at least through August 2015. Melo October 14 and 15 since no infants were observed gave birth to an infant in October 2014 who was still alive as of January 2016. As of this writing, the adult Infanticide Attempt After Male Takeover in Diana Monkeys / 39 male first seen in the study group on October 15 is takeover by a new male, and the infant who died was the sole adult male in the group, and Fred has not almost certainly the offspring of the former resident been observed in this or any adjacent Diana monkey male. group. Although we did not observe Melo mating with the new male over the next five months, she gave birth to an infant the following year (2014) who was still DISCUSSION alive as of January 2016. Diana monkeys, like most guenons, are seasonal breeders, and typically have an We attribute the disappearance of Melo’s infant approximately two-year interbirth interval (Butynski to death from the combined effects of (1) the new 1988; Cords 1988; Kane, unpublished data). Melo’s male’s attack, (2) the subsequent fall to the forest interbirth interval was shortened by the loss of her floor, and (3) injuries sustained after the chimpanzee infant, which ended lactational amenorrhea and threw it against a tree. Although it is not clear restarted her estrous cycles. Consequently, she and whether the infant would have died from the initial the new male reproduced sooner than they would attack and fall without the additional trauma caused have if the infant had survived. by the chimpanzee, we strongly suspect that this To our knowledge, this is the first description was the result of attempted infanticide rather than of attempted infanticide in Cercopithecus diana. a chimpanzee hunt. Chimpanzees at Taï very rarely With these observations, we add to the list of successfully hunt Diana monkeys (2% of hunts, species known to, or strongly suspected to, commit 4% of successful captures) and when they do hunt, infanticide in the wild, including three other forest it is generally a social activity; in this case, the guenons (Cercopithecus ascanius: Struhsaker 1977; chimpanzee was solitary and did not eat the infant Cercopithecus campbelli: Galat-Luong & Galat 1979; (Boesch & Boesch 1989). Cercopithecus mitis: Butynski 1982, Fairgrieve 1995, These observations are inconsistent with the social Cords & Fuller 2010). Our observations provide pathology hypothesis, which attributes aggression limited support for the assertion that infanticide and infanticide to artificially high population may be an adaptive strategy for male primates densities and the effects of anthropogenic disturbance even in seasonally breeding taxa, who increase (Curtin & Dolhinow 1978). The study group’s home their reproductive success by shortening females’ range is in an undisturbed patch of primary forest interbirth intervals. While we can reject the social with no signs of anthropogenic disturbance, and no pathology hypothesis, our observations support behaviors indicative of poaching pressure (Koné & both the generalized aggression and sexual selection Refisch 2007). Population density in this area is low, hypotheses for infanticide. with 2-3 groups per square kilometer (Buzzard & Eckardt 2007; Kane, unpublished data), and inter- ACKNOWLEDGEMENTS and intragroup aggression are rare: 1 aggressive intergroup encounter occurs approximately every We thank the Ministere de l’Enseignement 9 days, and 1.4% of behaviors recorded during scan Superieur et de la Recherche Scientifique, Direction samples were aggressive intergroup interactions Generale de l’Innovation Technologie, and the (Buzzard & Eckardt 2007; Kane, unpublished data). Ministere de l’Environment, des Eaux et Forets, Our observations are consistent with both Office Ivorien de Parcs et Reserves for their the generalized aggression and sexual selection permission to conduct fieldwork in the Taï Forest. hypotheses. The generalized aggression hypothesis The Centre Suisse de Recherche Scientifique predicts that infanticide occurs as a byproduct of provided logistical support for our research, and Dr. generally elevated rates of aggression coincident with Anderson Bitty directed the project from the field. All male takeovers or shifts in the dominance hierarchy research described here complied with institutional (Bartlett et al. 1993), and indeed this infant death and government regulations regarding the ethical occurred in the context of aggression towards several treatment of animals. This research was supported by females immediately following a male takeover. The funds from The Ohio State University Department sexual selection hypothesis suggests that infanticide of Anthropology, The Ohio State University chapter is an adaptive behavior for males who kill unweaned of Sigma Xi, and NSF BCS 0921770 and 0922429. infants and bring their mothers into estrus earlier Finally, we thank Noah Dunham, Scott McGraw, than if the babies had survived. This attempted Janette Wallis, and three anonymous reviewers for infanticide occurred – at most – within 24 hours of their helpful comments on an earlier version of this the disappearance of the resident male and group manuscript. 40 / Kane and Gnépa
LITERATURE CITED Galat-Luong, A. & G. Galat. 1979. Conséquences comportementales des perturbations sociales Altmann, J.A. 1974. Observational study of behavior: repetées sur un troupe de Mones de Lowe, sampling methods. Behaviour 49(3): 227-267. Cercopithecus campbelli lowei, de Cote d’Ivoire. Bartlett, T.Q., R. W. Sussman & J.M. Cheverud. 1993. Terre et Vie 33(1): 4-57. Infant killing in primates: a review of observed Hrdy, S.B. 1974. Male-male competition and cases with specific reference to the sexual infanticide among the langurs (Presbytis entellus) selection hypothesis. American Anthropologist of Abu, Rajasthan. Folia Primatologica 22(1): 19- 95(4): 958-990. 58. Boesch, C. & H. Boesch. 1989. Hunting behavior Hrdy, S.B. 1994. Infanticide: Let’s not throw out of wild chimpanzees in the Taï National Park. the baby with the bath water. Evolutionary American Journal of Physical Anthropology 78(4): Anthropology 3(5): 151-154. 547-573. Koné, I. & J. Refisch. 2007. Can monkey behavior Butynski, T.M. 1982. Harem-male replacement and be used as an indicator for poaching pressure? A infanticide in the blue monkey (Cercopithecus case study of the Western red colobus (Procolobus mitis stuhlmanni) in the Kibale Forest, Uganda. badius) and the Diana guenon (Cercopithecus American Journal of Primatology 3(1-4): 1-22. diana) in Taï National Park. In Monkeys of the Butynski, T.M. 1988. Guenon birth seasons and Taï Forest: An African Primate Community. correlates with rainfall and food. In A Primate W.S. McGraw, K. Zuberbühler & R. Noë, eds. Radiation: Evolutionary Biology of the African Cambridge, Cambridge University Press. Pp. Guenons. A. Gautier-Hion, F. Bourlière & J.P. 257-289. Gautier, eds. Cambridge, Cambridge University McGraw W.S., K. Zuberbühler & R. Noë. eds. 2007. Press. Pp. 284-322. Monkeys of the Taï Forest: An African Primate Buzzard, P.J. & W. Eckardt. 2007. Social systems of Community. Cambridge, Cambridge University the Taï guenons (Cercopithecus spp.). In Monkeys Press. of the Taï Forest: An African Primate Community. Palombit, R.A. 2012. Infanticide: male strategies W.S. McGraw, K. Zuberbühler & R. Noë, eds. and female counterstrategies. In The Evolution Cambridge: Cambridge University Press. Pp. 51- of Primate Societies. J.C. Mitani, J. Call, P.M. 71. Kappeler, R.A. Palombit & J.B. Silk, eds. Chicago, Cords, M. 1988. Mating system of forest guenons: The University of Chicago Press. Pp. 432-468. a preliminary review. In A Primate Radiation: Struhsaker, T.T. 1977. Infanticide and social Evolutionary Biology of the African Guenons. A. organization in the redtail monkey (Cercopithecus Gautier-Hion, F. Bourlière, & J.P. Gautier, eds. ascanius schmidti) in the Kibale forest, Uganda. Cambridge, Cambridge University Press. Pp. Zeitschrift für Tierpsychologie45(1): 75-84. 323-339. Sussman, R.W., J.M. Cheverud & T.Q. Bartlett. 1994. Cords, M. & J.L. Fuller. 2010. Infanticide in Infant killing as an evolutionary strategy: Reality Cercopithecus mitis stuhlmanni in the Kakamega or myth? Evolutionary Anthropology 3(5): 149- Forest, Kenya: variation in the occurrence of 151. an adaptive behavior. International Journal of van Schaik, C.P. 2000. Infanticide by male primates: Primatology 31(3): 409-431. The sexual selection hypothesis revisited. In Curtin, R. & P. Dolhinow. 1978. Primate social Infanticide by Males and its Implications. C.P. behavior in a changing world: human alteration van Schaik & C.H. Janson, eds. Cambridge, of the environment may be pushing the gray Cambridge University Press. Pp. 27-60. langur monkey of India beyond the limits of its adaptability. American Scientist 66(4): 468-475. Fairgrieve, C. 1995. Infanticide and infant eating in the blue monkey (Cercopithecus mitis stuhlmanni) Received: 14 February 2016 in the Budongo Forest Reserve, Uganda. Folia Accepted: 5 April 2016 Primatologica 64(1-2): 69-72. African Primates 11(1): 41-44 (2016)/ 41 Brief Communication:
Preliminary Report on Bonobo (Pan paniscus) Feeding Ecology in a Forest-Savanna Habitat at Bolobo, Democratic Republic of Congo
Ulrich Maloueki, Mpaka Lutonadio, Kumugo Ndimbo, and Nseu Bekeli Mbomba
University of Kinshasa, Faculty of Sciences, Department of Biology, Kinshasa, Democratic Republic of Congo
INTRODUCTION
We present a preliminary report on foods unpublished data) due to the ongoing habituation consumed by unhabituated bonobos (Pan paniscus) effort. During such encounters we noted that in a forest-savanna habitat during the period 07-29 bonobos fed on fruits, leaves, stems and shoots of September 2008. Although limited in scope, our data terrestrial herbs, possibly coinciding with a seasonal reveal some novel foods that had not been reported scarcity of arboreal ripe fruits (Maloueki, personal as food items from other bonobo study sites. This observation). We recorded frequency of food items study was conducted 300 km northwest of Kinshasa as one count per observation in a discrete feeding- along the Congo River, near the villages of Nkala, patch. Mbou-Mon-Tour, and Embirima, Bolobo Territory, District of Plateaux de Batéké, in Bandundu province RESULTS in D.R. Congo (for more details, see Maloueki et al. 2013). Terrestrial herbaceous vegetation (THV) was a We tracked the bonobos using noninvasive major part of the bonobos’ diet even in the presence methods by following along transect lines located of arboreal ripe fruits. The bonobos consumed the by random selection (Maloueki et al. 2013) and soft parts of the plants such as seedlings, stems, leaves, bonobo traveling paths. Direct observation of pith, and fruit pulp. We noted 24 species of plants bonobo feeding behaviour was not feasible as the consumed by bonobos, belonging to 18 genera from animals were not fully habituated and moved rapidly 11 families (Table 1). The most frequently represented through the trees. Low visibility in the forest and the families were Marantaceae (25%, N = 6), followed by dense undergrowth further hindered systematic Zingiberaceae (16.7 %, N = 4), Apocynaceae (12.5 behavioral observations. The majority of our ad- %, N = 3), Commelinaceae, Connaraceae, Poaceae libitum observations were recorded indirectly by (8.33 %, N = 2), and Annonaceae, Dioscoreaceae, identifying food remains around sleeping sites and Loganiaceae, Piperaceae, Sapindaceae (4.17 %, N = identifying discarded food items along bonobo 1). paths or trails where bonobo footprints were seen. Some species recorded during this study Additionally, trackers employed to follow the were absent and/or not previously reported as bonobos for habituation, provided information food resources for wild bonobos in other studies. about plant foods consumed by the bonobos. During The novel species include Annonaceae Annona the study period, the bonobos were more terrestrial senegalensis, Apocynacae Landolphia lanceolata, than in previous encounters between the periods Clitandra cymulosa, Connaraceae Rourea coccinea from December 2007 to March 2008 (Ndimbo et al. var. viridis, Dioscoreaceae Dioscorea smilacifolia,
Correspondence to: Ulrich Maloueki, University of Kinshasa, Faculty of Sciences, Department of Biology, P.O Box 190, Kinshasa XI, Democratic Republic of Congo; Phone: (+243) 820 445 407; E-mail: [email protected]. 42 / Maloueki et al. b 1, 2 1, 2, 3, 4 1, 2 2 5 1, 2, 3, 4 1 1, 2, 3, 4 1, 2, 3, 4, 5 References Tree Vine Vine Vine Vine Vine Vine Herb Herb Herb Herb Herb Herb Herb Herb Shrub Life Life Form Part ) in the forest-savanna at Bolobo. at ) in the forest-savanna Pulp Pulp Pulp Pulp Pith Pith Leaf Pulp, Leaf Pulp, Stem Pulp Pith Pith Pith Pith Pith Pith Consumed paniscus
Pan Téké Name Téké Elolo Manyau Bempuri Mayaon Matilatili Matilatili Unknown Unknown Esalatina Bikilikio Nteele Nkuwanseyi Ekanu Makanu Nkuwangowu Mpumpolo plants consumed by bonobos consumed by ( plants a Le Thomas (Kuntze) Milne-Redh. (Benth.) Milne-Redh. oulotricha (Gilg) Jongkind (K. Schum.) J. Leonard & Mull. (De Wild. & T. Durand) J. Léonard T. & Wild. (De De Wild. Eurard & Bamps P. Beauv. Beauv. P. Baker (K. Schum.) Pichon viridis subsp. (Lam.) Baill. Benth. (P. Beauv.) C.B. Clarke Beauv.) (P. var. var. (Thunb.) K. Schum. sp. Clitandra cymulosa Landolphia lanceolata Landolphia owariensis Palisota ambigua Palisota hirsuta Agelaea pentagyna coccinea Rourea smilacifolia Dioscorea Strychnos cocculoides Haumania leonardiana Haumania liebrechtsiana Haumania Marantochloa congensis schweinfurthianum Sarcophrynium Annona senegalensis
Family Species Family Annonaceae Apocynaceae Commelinaceae Connaraceae Dioscoreaceae Loganiaceae Marantaceae Megaphrynium macrostachyum Table 1. THV (which can also include small woody shrubs) Table Bonobo Feeding Ecology at Bolobo, DRC / 43 b 1, 4 2 1, 2, 3, 4, 5 1, 2, 3, 4 References Tree Vine Herb Herb Herb Herb Herb Herb Life Life Form Part ) in the forest-savanna at Bolobo. (Continued.) Bolobo. at ) in the forest-savanna Stem Stem Pulp Pulp Pulp Pith, Pulp Pith, Pulp Pith, Pith Consumed paniscus
Pan Téké Name Téké Makawu Koko Bankere Unknown Montuna Ntuna ababebubu Ntondolo Montuna plants consumed by bonobos consumed by ( plants a 2001. (Ridley) K. Schum. (Sonn.) K. Schum. et al. et (A. Chev.) Hauman (A. Chev.) L. Benth. ex Hook. f. (L.) Raeusch 1981. Schumach. & Thonn. Schumach. & . 1994. et al. et sp. et al Imperata cylindrica Saccharum officinarum Piper guineense Ganophyllum giganteum Aframomum alboviolaceum Aframomum Aframomum angustifolium Renealmia africana Data comparing the list known as food resources with those from other bonobo study sites. study bonobo other those with from food as resources known the list comparing Data Definition given by Conklin-Brittain by Conklin-Brittain given Definition Family Species Family Poaceae Piperaceae Sapindaceae Zingiberaceae a b Idani 1. Wamba: data). (unpublished Maloueki 2. Iyondje: Badrian 3. Lomako: 2009. & Matungila Inogwabini 4. Lake Tumba: 1991. & Stiles Malenky 5. Lomako: Table 1. THV (which can also include small woody shrubs) Table 44 / Maloueki et al.
Loganiaceae Strychnos cocculoides (this tree grows In: The Apes: Challenges for the 21st Century, in woodlands that are burnt annually), Piperaceae Conference Proceedings of Brookfield Zoo. Piper guineense, Poaceae Imperata cylindrica (grass), May 10-13, 2000. Chicago Zoological Society, and Sapindaceae Ganophyllum giganteum. The lack Chicago. Pp. 167-174. of consumption of these food items in other bonobo Harrison, M.E. & A.J. Marshall. 2011. Strategies populations may be due to cultural difference or food for use of fallback foods in apes. International preference (Hohmann & Fruth 2003; Harrison & Journal of Primatology 32: 531-565. Marshall 2011). Additionally, some dietary variation Hohmann, G. & B. Fruth. 2003. Culture in bonobos? across sites may be the influence of habitat types for Between-species and within-species variation in the presence or absence of plant species. behavior. Current Anthropology 44: 563-571. Idani, G., S. Kuroda, T. Kano & R. Asato. 1994. Flora ACKNOWLEDGMENTS and vegetation of Wamba forest, Central Zaire with reference to bonobo (Pan paniscus) foods. The authors wish to thank all the villagers and Tropics 3: 309-332. local assistants for facilitating this research. We Inogwabini, B.I. & B. Matungila. 2009. Bonobo food express our gratitude to Mr. Jean Christophe Bokika items, food availability and bonobo distribution from NGO Mbou-Mon-Tour at Bolobo for his in the Lake Tumba swampy forest, Democratic help and support during this research. We convey Republic of Congo. The Open Conservation our sincere gratitude to the late Prof. Timothée Biology Journal 3: 14-23. Maloueki from the Marien Ngouabi University Malenky, R.K. & E.W. Stiles. 1991. Distribution in Congo-Brazzaville for funding this work. We of terrestrial herbaceous vegetation and its would like to thank the anonymous reviewers and consumption by Pan paniscus in the Lomako Dr. Jo Thompson for their very constructive and forest, Zaire. American Journal of Primatology useful comments on the manuscript and also for 23: 153-169. improvements to our writing in English. We are Maloueki, U., K. Ndimbo, M.J. Malekani & N.B. grateful to Dr. Janette Wallis for her assistance. Mbomba. 2013. Estimation de la densité par comptage des nids des bonobos (Pan paniscus) dans la région de Bolobo des localités de Nkala et LITERATURE CITED Embirima, République Démocratique du Congo: résultats préliminaires. Revue de Primatologie, Badrian, N., A. Badrian & R. Susman. 1981. Vol. 5. http://primatologie.revues.org/1660; doi: Preliminary observations on the feeding behavior 10.4000/primatologie.1660. of Pan paniscus in the Lomako forest of Central Zaire. Primates 22: 173-181. Conklin-Brittain, N.L., C.D. Knott & R.W. Received: 20 January 2016 Wrangham. 2001. The feeding ecology of Apes. Accepted: 2 June 2016 African Primates 11(1): 45-48 (2016)/ 45 Brief Communication:
Documentation of Plant Consumption by Galago moholi in South Africa
Ian Ray1,2,3*, Brandi T. Wren2,4, and Evelyn J. Bowers1
1Department of Anthropology, Ball State University, Muncie Indiana USA; 2Applied Behavioural Ecology and Ecosystem Research Unit, University of South Africa; 3Science Department, Heritage High School, Littleton Public School District, Littleton Colorado USA 4Department of Anthropology, Purdue University, West Lafayette, Indiana USA
BACKGROUND
Galagos, or bushbabies, are small nocturnal (Harcourt 1986). This was not surprising given primates found exclusively in sub-Saharan Africa. that galagos in general possess morphological Three species are known to inhabit the Southern specializations for feeding on gum, including African sub-region, including Galago moholi, specialized dentition, an additional pseudo-tongue Galagoides granti, and Otolemur crassicaudatus for cleaning dentition, and a specialized digestive (Nash et al. 1989; Yokwana et al. 2014). Galago system (Caton et al. 2000; Gebo 2014). Despite moholi (the southern lesser bushbaby) averages these studies, captive G. moholi populations have 158g and 438mm in total length, including the traditionally been fed a diet of fruits and vegetables, tail (Nash et al. 1989). Bearder and Doyle (1974) supplemented by available insects (Doyle & Bekker reported population densities ranging from a low 1967). of 95 animals/km2 in escarpment riparian bush and scrub habitat to a high of 500 animals/km2 in Acacia Recent Findings karoo thickets, though later studies, including Bearder (1987) and Ray et al. (unpublished data), Scheun et al. (2014) documented the first found significantly lower densities, suggesting that published account of G. moholi consuming vegetative the early studies overestimated population density. matter. G. moholi was found to consume the fruit of Pappea capensis (the jacket-plum) during a study Diet conducted in the Buffelsdrift Conservation Area, approximately 125km west of Loskop Dam Nature Galago moholi’s diet has been documented in Reserve, Mpumalanga Province, South Africa several studies. Bearder and Martin (1980) studied (Scheun et al. 2014). The fruits ofP. capensis are G. moholi by radio-tracking over a two year period bright red, around 15mm in diameter, and surround from 1975 to 1977. At no point during that study did black seeds (Schmidt et al. 2002). any individuals of the species attempt to consume any available fruit, pods, or seeds (Bearder & Martin We observed G. moholi emerge from a building 1980). Harcourt (1986) conducted a study on the in the University of South Africa research camp seasonal diets of G. moholi and O. crassicaudatus. at Loskop Dam Nature Reserve (Figure 1), during The results indicated that G. moholi consumed a winter in which daily temperatures ranged from exclusively insect prey and tree gums, with no 7oC to 21oC (National Center for Environmental evidence of the consumption of any fruiting bodies Information 2016). Several G. moholi were
Correspondence to: Ian Ray, Department of Anthropology, Ball State University, 2000 W. University Ave., Muncie, Indiana 47306 USA; Phone: +1 (303) 974-8160; E-mail: [email protected]. 46 / Ray et al.
Figure 1. The location of Loskop Dam Nature Reserve within Mpumalanga.
seen leaving a known nest site in the camp at more use of other food sources, like P. capensis approximately 16:40h on 5 July 2011. As they passed and D. cinerea fruits. This is possible in areas of through the bush surrounding the common area of Loskop where D. cinerea is common due to prior the camp, one individual stopped and consumed cattle grazing (Filmalter 2010). Additional research approximately one-half of a fruit, ingesting both is being conducted to better understand G. moholi seed and pod (Figure 2). This tree was later identified dietary ecology in southern Africa. as a Dichrostachys cinerea (the sicklebush), which produces fruits in curled clusters of green to brown pods from May to September (Schmidt et al. 2002). ACKNOWLEDGMENTS
Implications We are grateful for the aid provided by Jannie Coetzee and the staff of the Applied Behavioural We agree with Scheun et al. (2014) that the Ecology and Ecosystem Research Unit (ABEERU) consumption of plant matter by G. moholi is of the University of South Africa (UNISA), and unsurprising, given the species’ extensive geographic for being allowed to work at Loskop Dam Nature range and known reliance on fruits in captivity. Reserve. There are a number of possible explanations for this behavior only recently being documented. LITERATURE CITED It is possible that G. moholi has been studied so rarely that the consumption of fruits was simply Bearder, S.K. 1987. Lorises, Bushbabies, and not observed. Also, lesser bushbabies most likely Tarsiers: diverse societies in solitary foragers. In display more behavioural and dietary plasticity than Primate Societies. B.B. Smuts, D.L. Cheney, R.M. previously acknowledged, as Scheun et al. (2014) Seyfarth, R.W. Wrangham, & T.T. Struhsaker, note. In addition, anthropogenic habitat alteration eds. University of Chicago Press, Chicago. Pp 11- may lead to altered dietary ecology, resulting in 24. Plant Consumption in Galago moholi / 47
Figure 2. An individual of G. moholi spotted at approximately 16:40h in Loskop Dam Nature Reserve, South Africa. Photograph by I.S. Ray. 48 / Ray et al.
Bearder, S.K. & G.A. Doyle. 1974. Ecology of Nash, L.T., S.K. Bearder, & T.R. Olson. 1989. Synopsis bushbabies Galago senegalensis and Galago of galago species characteristics. International crassicaudatus. In Prosimian Biology. R.D. Journal of Primatology 10(1): 57-80. Martin, G.A. Doyle, & A.C. Walker, eds. National Center for Environmental Information. Duckworth Publishers, London. Pp 109-130. 2016. Land Surface Station Oudestad. NOAA. Bearder, S.K. & R.D. Martin. 1980. Acacia gum Accessed 28 Jul 2016. Retrieved from http://www. and its use by bushbabies, Galago senegalensis. ncdc.noaa.gov/orders/isd/9172557095940dat.txt International Journal of Primatology 1(2): 103- Scheun, J., N.C. Bennett, A. Ganswindt, & J. Nowack. 128. 2014. Spicing up the menu: evidence of fruit Caton, J.M., M. Lawes, & C. Cunningham. 2000. feeding in Galago moholi. Primates 55: 359-363. Digestive strategy of the south-east African Schmidt, E., M. Lotter, & W. McCleland. 2002. Trees lesser bushbaby, Galago moholi. Comparative and Shrubs of Mpumalanga and Kruger National Biochemistry and Physiology Part A: Molecular & Park. Jacana Media, Johannesburg. Integrative Physiology 127: 39-48. Yokwana, A. 2014. Comparing the preferred habitats Doyle, G.A. & T. Bekker. 1967. A facility for of South Africa’s two lesser galago species naturalistic studies of the lesser bushbaby (Galagoides granti and Galago moloti [sic]). The (Galago senegalensis moholi). Folia primatologica 12th Annual Conference of the South African, 7: 161-168. Primate Ecology and Genetics Group, University Filmalter, N. 2010. A Vegetation Classification and of South Africa, Cradle of Humankind, South Management Plan for the Honderkraal Section Africa. of the Loskopdam Nature Reserve. MTEch dissertation, University of South Africa. Gebo, D.L. 2014. Primate Comparative Anatomy. Received: 9 April 2016 Johns Hopkins University Press, Baltimore. Accepted: 28 July 2016 Harcourt, C. 1986. Seasonal variation in the diet of South African galagos. International Journal of Primatology 7(5): 491-506. African Primates 11(1): 49-50 (2016)/ 49 Brief Communication:
Birth of the African Primatological Society for the Future of African Primates
Inaoyom Imong1, Rachel Ikemeh2, Inza Kone3, and Denis Ndeloh4
1Wildlife Conservation Society, Nigeria Programme, Calabar, Nigeria; 2Southwest/Niger Delta Forest Project, Nigeria; 3Centre Suisse de Recherches Scientifiques en Côte d’Ivoire; 4Wildlife Research Division, Nunavut Department of Environment, Igloolik, NU, X0A 0L0”
At the IUCN / SSC Primate place within Africa. There is the Specialist Group African Primate need, therefore, for Africans to Red List Assessment Workshop get more actively involved in and in Rome in April 2016 experts lead efforts to better understand assessed the conservation status and protect African primates of African primates based on and their habitats. a set of criteria which includes For too long, Africans hunting pressure and habitat loss have taken a back seat in and fragmentation. A hundred African primate research and out of 179 taxa were classified conservation efforts at local as threatened including 35 and international levels. For endangered and 15 critically example, few primate research endangered. More than ever and conservation projects in before, these assessments Africa are led by nationals revealed the dire situation facing African primates of range countries; and until the Rome meeting and drew attention to the imminent catastrophic this year only a few, if any, Africans were able to loss of the continent’s rich heritage if concrete participate in the Red List Assessment of African steps are not taken urgently to reverse the current primates, which assigns defined threat categories to trend. A clear take home from these assessments the different taxa and therefore sets the agenda for is that current efforts are simply not enough to conservation interventions. The situation is similar safeguard the future of African primates. Moving for other international primatological fora such as forward, there must be greater commitment from the International Primatological Society Congresses, all stakeholders – international and local. National convened to share information about research and governments, international organizations, donor conservation efforts and to assess the state of the agencies, research institutions, local communities, world’s primates, including African Primates. groups and individuals must reassess their levels One of the factors that have been identified for of commitment and intervention strategies, and this low level of involvement of Africans in such reposition themselves to be more effective in their international efforts is the lack of coordination efforts to save Africa’s primate diversity. among African primatologists and conservationists. In particular, Africans must step up to the In contrast to other regions of the world, there is challenge of saving their natural heritage. Many have no established platform for information sharing, argued that in the long term, effective conservation coordination of research and conservation of African primates lies principally in the hands of efforts, promotion of greater and more effective Africans and requires that significant changes take representation at international fora, and networking
Correspondence to: Steering Committee E-mail: [email protected] or [email protected]; Web site: www.africanprimatologicalsociety.org; Facebook: https://www.facebook.com/African.Primatological.Society/; Twitter: @AfricanPS. 50 / Imong et al.
Participants at the 2016 IUCN SSC Primate Specialist Group’s African Primate Red List Assessment Workshop, Rome, Italy.
among African primatologists to promote research of the Society. We are proud and most pleased to and improve conservation efforts. announce the birth of the APS! The lack of coordination has also limited the The steering committee is working towards ability of African primatologists to influence organizing an inaugural congress of the APS in policies that impact on African primates and their 2017. Among other things the congress will agree ability to lend support as a regional group where on the structure and operational framework of needed. While there is still a dearth of Africans with the APS, adopt a constitution for the Society and expertise in primate research and conservation on elect officers to lead and coordinate the affairs of the continent, such expertise is undeniably growing the Society. The steering committee is developing and needs to be harnessed for the benefit of African a membership form that will be circulated widely primates. and also working towards creating a website and a It is against this backdrop that the idea of database of members with contact and other relevant forming an African primate group was conceived. information. It is hoped that everyone will help This idea was discussed at a number of meetings and contact primate researchers and conservationists via email leading to the formation in 2013, of the in their countries and sub-regions to gather “African Primatologists Working Group” (APWG), information for the database. We are also working which was essentially an email correspondence towards identifying potential partner institutions, group coordinated by an ad hoc steering committee. donors, and a host institution (where the Society At the 2016 IUCN /SSC Primate Specialist Group is to be headquartered). We encourage all African African Primate Red List Assessment Workshop in primatologists to join the APS and help to safeguard Rome, the African representatives continued these the future of African primates. discussions and officially adopted the name “African Primatological Society (APS)” with a new steering (The African Primatological Society thanks Conservation committee constituted to coordinate the activities International’s Stephen Nash for logo design). African Primates 11(1) (2016) / 51 News
IPS Grants and Awards for Primate Work The International Primatological A Message from the Africa Section Society (IPS) has several grant of the Society for Conservation and award programs. See the Biology - for AFRICANS who are IPS web site for details about members of SCB. conservation, research, captive care, and education grants (be Access to scientific publications is sure you submit applications a major challenge for conservation to the grant program that fits your goal to students, scientists and managers maximize chances for funding). See http://www. internationalprimatologicalsociety.org. The next in Africa, due to the paywall many deadline for grant submissions: March 1, 2017. publishers have placed on their journals.
More Funding Opportunities In order to assist African SCB members to overcome this The British Ecological Society is offering up to eight challenge, some SCB members in thousand pounds research grants for ecologists in North America have offered to assist Africa. Deadline is September 16. See: http://www. you all in providing literature for your britishecologicalsociety.org/funding/ecologists-in- work. africa/ This is how it works: send the Film4Climate Global Video competition invites citation (authors' names, paper title, filmmakers worldwide between 14 and 35 years old to create and submit an advertisement or short film year of publication, journal name, about climate change. Best films will be awarded volume, series and page range) to cash prizes up to $8,000. Deadline for submission me (SEE BELOW). I will either help is September 15. See: https://www.film4climate.net/ you search for the paper, or send it to other North American SCB Elsevier Foundation, in collaboration with members to help you download the Organization for Women in Science for the paper and I will send it back to you. Developing World and The World Academy of Sciences offers award for early career women If the publication size is more than scientsts. This award carries a $5000 prize and 25 MB, you may have to give me a grant to attend AAAS 2017 meeting. Deadline for nominations is September 1. See: http://owsd. Dropbox or Google Drive account to ictp.it/resources/news-events/call-opens-2017- which I can upload it for you. awards-early-career-women-scientists-engineering- innovation This offer begins NOW!!
Do not forget also, that as SCB Visit the Primate Info Network member, you have access to SCB for the latest news on primate journal publications: Conservation jobs, meetings, and educational Biology and Conservation Letters. opportunities. Israel Borokini http://pin.primate.wisc.edu Section Information Officer 52 / News Job Opportunities
Sanctuary Manager, Libassa Wildlife CAP employs a range of conservation strategies to Sanctuary increase knowledge of and mitigate threats to great We are seeking a Sanctuary Manager for a new apes and their habitats. For details, see http://www. sanctuary in Liberia - the Libassa Wildlife Sanctuary janegoodall.org/wp-content/uploads/CAP-PM-Job- Liberia (LWS). The Sanctuary Manager is expected Advert.pdf to manage the care of the animals at the sanctuary, as well as the care staff, and any interns and volunteers. Tuungane Program Director Duties include general husbandry for over Location: Kigoma, Tanzania Libassa Wildlife Sanctuary animal residents, The Nature Conservancy is seeking a Project Director including monkeys, pottos, Duikers, parrots, etc... to provide strategic leadership in integrated planning, For the safety of sanctuary residents and co- project cycle management, annual work plans and workers, we do not accept applicants who smoke. budgets development, staff management, results You will have to have all necessary vaccinations, monitoring and reporting. We are therefore looking including for Rabies and yellow fever. You must also for an individual who is experienced in project sign up for medical evacuation insurance. management in remote settings, organizational Salary/funding: $200/month, Round-trip airfare capacity building expertise, innovative problem plus accommodation. Term of Appointment: 12 solver, effective team coordinator, proven networker months. Contact Information: Jim and Jenny and self-starter. The Greater Mahale Ecosystem is Desmond; Phone Number:+231 776147565; Email: remote, with limited transport and communication [email protected]; Skype ID: jim.desmond; networks, making it a very challenging living and Website: http://www.libassa.com/ working environment. See more details here.
Executive Director, African Wildlife Capital Congo Basin Communications Coordinator Location: Washington, DC, or flexible Location: Kinshasa, Democratic Republic of globally the Congo, DRC The Executive Director, African Wildlife Capital The World Resources Institute (WRI) seeks a Congo (AWC), will work in partnership with African Basin Communications Coordinator to support Wildlife Foundation (AWF), AWC's Chief WRI's Forest Program's mission by developing Investment Officer, and the appointed fund and implementing communications strategies, and administrator of AWC to scale up Africa's first supporting multiple communications channels impact investing vehicle for conservation enterprise. (such as web, social media, blog, publications, Established in 2011, AWC utilizes private sector media relations, and events). The Communications capital to promote commercial ventures that support Coordinator will proactively collaborate with WRI's the conservation of threatened landscapes in Congo Basin and Forest Program's communications Africa. AWC has already raised and allocated US$7 teams on all aspects of work. See WRI web site for million across nine investments, and now aims to more details: www.wri.org significantly scale up operations. AWC was founded and is backed by AWF. For details, see: http://www. Project Communications Specialist, awf.org/about/careers/executive-director-african- TRAFFIC wildlife-capital. Location: Washington, DC World Wildlife Fund (WWF) seeks a Project Conservation Action Plan Project Manager Communications Specialist, TRAFFIC at our Location: Democratic Republic of the Congo Washington, DC office. In close collaboration with The Project Manager will apply strong project TRAFFIC leadership, the job holder plans, manages, management skills, experience and a track record communicates, and implements project priorities of successfully managing conservation programs and activities in the area of communications. in challenging developing country contexts to Develops and plans communications strategies for support the implementation of the Conservation two USAID-funded wildlife trafficking projects. Action Plan for Great Apes in Eastern DRC. The Details at www.worldwildlife.org. African Primates 11(1) 2016 / 53 Volunteer Opportunities
Engagement Intern applicants with a degree in biology, anthropology or Location: Washington, DC environmental sciences, although we can consider African Biodiversity Collabortive Group, via applicants with different backgrounds depending its host organization the Wildlife Conservation on their experience. Experience in field work with Society, seeks a motivated part-time Engagement international teams, experience in Africa and Intern to support this consortium of seven U.S. experience in similar projects will be major assets. based non-governmental organizations NGOs. The Volunteer must be able to endure simple living Engagement Intern will have the opportunity to conditions in the middle of the wilderness, camping learn about communicating key messages, building and staying away from civilization for long periods brand awareness, and deepening stakeholder in a multicultural environment. The volunteer engagement that will protect wildlife and natural should be able to walk long distances across savanna resources across the African continent, and learn and forest in harsh climatic conditions and work about the environmental communications and during long periods. conservation landscape in Washington. S/he will This is a volunteer non funded position. work closely with the ABCG Coordinator to support Volunteers will need to pay for their travel and ABCG’s efforts to explore emerging and high priority expenses during their stay. Volunteers will get all themes affecting biodiversity conservation in Africa. the needed vaccination before travelling, including See the ABCG web site for details: www.abcg.org or at least yellow fever and hepatitis, antimalarial go here: http://www.idealist.org/view/internship/ treatment and a visa covering their stay. A minimum kDSNCxDNjMJd/ of 3 months of commitment is mandatory, but we accept longer stays. Contact: Juan Lapuente, Volunteer Field Assistant for Study of Wild [email protected] Chimpanzees in Comoé National Park, Ivory Construction/ Builder’s Volunteer at Coast We are looking for volunteers to help with the the Limbe Wildlife Centre, Pandrillus field work, local teams' coordination, data and Foundation samples collection and data entry in our project to The Limbe Wildlife Centre (LWC) is seeking study and protect the wild chimpanzees of Comoé a construction/building professional to provide National Park, in Ivory Coast. Comoé National Park assistance and advise to a conservation programme. is one of the largest in the World, with 11,500 km2 The builder will be appointed on a voluntary basis. of savanna-woodland mosaic. Chimpanzees were The volunteer is required to show strong skills, supposed to be extinct in the park until our project and knowledge in building (including masonry, rediscovered them in October 2014. Presently, we carpentry), electricity and plumbing, but also are working to know the status and distribution of in welding, painting, etc., and must be willing wild chimpanzees across the whole park, but we to participate and help a wildlife conservation mainly focus in the study of 3 neighboring groups programme. He/she should be aware of the general around the Comoé Research Station that German context of the project, and demonstrate inter- University of Würzburg has in the park. personal skills for evolving in a multi-cultural These are non-habituated chimpanzees, so we environment. As a volunteer at Limbe Wildlife study them using camera traps, transects and etho- Centre, you will be able to play an active role in archaeological methods, avoiding close contact. We conservation by assisting in the care of 300 animals are working in collaboration with local managers of who have been orphaned by the bushmeat trade. The the park to improve the conditions for conservation volunteer will assist the LWC Head of Construction, of chimpanzees and their hábitats, with the provide technical advises and assistance. perspective of a long term project. We provide basic accommodation with security We are looking for responsible mature guard, house cleaner and lunch on workdays. volunteers able to work in small teams with people We need a CV, 2 recommendation letter. Contact of very different culture. At least basic knowledge of Information: Peggy Motsch, P.O. Box 878, Limbe, French is mandatory. We will consider preferently South West Region, Cameroon; Website: http:// www.limbewildlife.org, [email protected]. 54 / News Volunteer Opportunities
Short and Long term Volunteer at the Limbe with individual time frames negotiated separately, Wildlife Centre, Pandrillus Foundation though we prefer a minimum commitment of four As a volunteer at Limbe Wildlife Centre, you months. Responsibilities include all-day follows of will be able to play an active role in conservation by baboons (5-15 km/day), daily census of the study assisting in the care of 300 animals who have been group, collection of behavioral and reproductive orphaned by the bushmeat trade. Volunteers take data, and collection and field laboratory processing part in the day to day activities of the sanctuary, of fecal samples for genetic and hormone analyses. including cleaning cages, preparing food and Volunteers would be accompanied in the field by our feeding animals, creating enrichment, and doing current field manager, our local field assistant, and/ daily observations. or a local park scout. Depending on the time and current activities, you Depending on length of stay, amount and quality may also have the opportunity to observe surgeries of data collected, and intellectual contributions to in our veterinary clinic, assist in an education the project, a field assistant position at Filoha could lesson in local schools or work on your own project potentially lead to co-authorship on a publication. depending of your skills (for the long term position). A position at Filoha provides excellent field Currently Limbe Wildlife Centre cares for experience for those interested in pursuing graduate Western Lowland Gorillas, Central and Nigeria- studies in anthropology or biology. Successful Cameroon Chimpanzees, drills, mandrills, baboons volunteers learn a variety of field techniques in several species of guenons and mangabeys, as well as behavioral biology and hormone/genetic sample various non-primates. processing. For the short term volunteer (1 week to 3 Volunteers need to be physically fit (the baboons months) no experience is needed. No interview often travel quickly over rough terrain) and able to is needed. For the long term volunteer (at least 6 collect data under the conditions described above. month), experience with wildlife is recommended; A Due to the remoteness of the field site and the lack of minimum of bachelor degree; There is an interview communication infrastructure, volunteers must also before the final decision. For short term volunteers: be of sound physical and mental health without any A donation of 250 euro/week or 750 euro/month for pre-existing conditions that might require immediate the project and for lunch, lodging, house security, medical attention. Volunteers must also be able and and cleaning is requested. All of the funds raised in willing to maintain professional relationships with this program go directly towards the animals under people of varied cultural backgrounds and cope our care and to pay for volunteer costs (housing, with disruptions to fieldwork due to possible ethnic etc.). conflict and other factors out of one’s control. Volunteers are provided with accommodation This is a volunteer position, so unfortunately in our volunteer house, which has a basic room as no salary is available. Volunteers would need to well as shared bathrooms and a kitchen. Lunch is cover their own travel expenses and pay a US$1000 provided on working days. research fee to the Ethiopian Wildlife Conservation Contact Information: Peggy Motsch, P.O. Box Authority (that could potentially be reimbursed 878, Limbe, South West Region, Cameroon, Website: by the project after successful completion of six http://www.limbewildlife.org, peggy@limbewildlife. months of fieldwork; see below). In addition, each org. person should allow $100-200 per month for living expenses while in Ethiopia. Volunteer Field Assistants for Filoha We require a minimum 4-month commitment Hamadryas Project in Awash National Park, and prefer longer, but individual time frames are negotiated separately. Ethiopia, Filoha Hamadryas Project, Queens Contact: Larissa Swedell, Anthropology, Queens College, City University of New York College, 65-30 Kissena Blvd, Flushing, NY 11367- We are seeking volunteer field assistants for a 1597, USA; Telephone: 718-997-2897; Fax: 718- study of hamadryas baboons at the Filoha study 997-2885; Website: http://larissaswedell.org/filoha; site in the lowlands of central Ethiopia. Volunteer [email protected] positions at Filoha can be short-term or long term, African Primates 11(1) 2016 / 55 Bioko Island Study Abroad For over 13 years, the Bioko Study Primate Field Abroad program (Drexel University) Schools in has taken students to Bioko, Equatorial Africa Guinea, as part of an immersive experience with the Bioko Biodiversity Protection Program (BBPP) that focuses on hands-on experiential learning and training in biodiversity • Study tropical biodiversity and its research. This unique program includes conservation, with an emphasis on individual field research projects at the field work that takes advantage of Moka Wildlife Center in the highlands Bioko Island's pristine rainforests, its of Bioko, academically rigorous 7 species of rare monkeys, and its 4 coursework at the National University species of nesting sea turtles. of Equatorial Guinea in the capital city • Work in collaboration with of Malabo, expeditions into Bioko's experienced African field biologists tropical forests, and cultural excursions on an individual research project, to explore Bioko's diverse and storied and thus adding to the biodiversity past. Students have come from a wide database being created for Bioko array of backgrounds, but they have Island. all left transformed, with a broadened • Participate in the activities of an worldview and a depth of experience established conservation program that can only result from study of on the political, economic and complex environmental challenges in a ecological issues involved in global context. biodiversity conservation, thereby To maintain this high level of building personal credentials and individualized study, the program is contacts. offered twice a year (September - • Explore the linguistic and cultural December and January - March) to a diversity of Equatorial Guinea, class of eight students. Africa’s only Spanish-speaking The program offers a unique country, by collaborating with local opportunity for undergraduates and university students on research recent graduates to: projects and on Spanish language skills.
For more information, visit www.drexel. edu/studyabroad or contact either Study Abroad at Drexel University (Daniela Ascarelli; [email protected]; 215- 895-6280) or Dr. Mary Katherine Gonder ([email protected]; 215- 571-4638). For more information on the BBPP and its activities, please visit www.bioko.org. 56 / Field Schools & News
Primate Field Schools in Africa
Sepela Field Programs offers a variety of field experiences, including a Field Primatology course and Primate Health Care Program.
All field experiences include Wilderness First Aid training and certification by one of Sepela’s accredited American Health and Safety Institute Instructors. More information is available at www.sepela. org or [email protected].
IUCN SSC Primate Specialist Group’s
“Primates in Peril: The World’s Most Endangered Primates - 2014-2016”
Now available!
Pick up a hard copy at the Conservation International table at IPS/ASP in Chicago.
Or visit the Primate Specialist Group web site for a digital copy. African Primates 11(1) 2016 / 57 Recent Publications*
Bădescu, I., E.C. Wikberg, L.J. Macdonald, disturbance factors in density estimation. S.A. Fox, J.V. Vayro, A. Crotty & P. Sicotte. PloS ONE 11(2): pp.e0148289. 2016. Infanticide pressure accelerates infant Cronin, D.T., C. Riaco, J.M. Linder, R.A. Bergl, development in a wild primate. Animal M.K. Gonder, M.P. O'Connor & G.W. Behaviour 114: 231-239. Hearn. 2016. Impact of gun-hunting on Barale, C.L., D.I. Rubenstein & J.C. Beehner. monkey species and implications for primate 2015. Juvenile social relationships reflect conservation on Bioko Island, Equatorial adult patterns of behavior in wild geladas. Guinea. Biological Conservation 197: 180- American Journal of Primatology 77(10): 189. 1086–1096. Cronin, D. T., S. Woloszynek, W. A. Morra, S. Borgeaud C., S. Sosa, R. Bshary, C. Sueur & Honarvar, J. M. Linder, M. K. Gonder, M. P. E. van de Waal. 2016. Intergroup variation O'Connor, & G. W. Hearn. 2015. Long-term of social relationships in wild vervet urban market dynamics reveal increased monkeys: a dynamic network approach. bushmeat carcass volume despite economic Frontiers in Psychology 7:915. doi: 10.3389/ growth and proactive environmental fpsyg.2016.00915. legislation on Bioko Island, Equatorial Barrett, L., P. Henzi & L.R. Brown. 2016. Guinea. PLoS ONE 10(7): e0134464. Resource selection on woody plant species by doi:10.1371/journal.pone.0134464. vervet monkeys (Chlorocebus pygerythrus) Dunham, N. & P. Opere. 2016. A unique case of in mixed-broad leaf savanna. South African extra-group infant adoption in free-ranging Journal of Wildlife Research 46(1): 14-21. Angola black and white colobus monkeys Bortolamiol, S., M. Cohen, F. Jiguet, F. Pennec, (Colobus angolensis palliatus). Primates A. Seguya & S. Krief. 2016. Chimpanzee non‐ 57(2): 187-194. avoidance of hyper‐proximity to humans. Eckardt, W., K. Fawcett & A. Fletcher. 2016. The Journal of Wildlife Management 80(5): Weaned age variation in the Virunga 924-934. mountain gorillas (Gorilla beringei beringei): Breuer, T., A. Robbins & M. Robbins. 2016. influential factors.Behavioral Ecology and Sexual coercion and courtship by male Sociobiology 70(4): 493-507. western gorillas. Primates 57(1): 29-38. Freeman, N.J., C. Young, L. Barrett & S.P. Henzi. Brockmeyer, T., P.M. Kappeler, E. Willaume, L. 2016. Coalition formation by male vervet Benoit, S. Mboumba & M.J.E. Charpentier. monkeys (Chlorocebus pygerythrus) in South 2015. Social organization and space use of Africa. Ethology 122(1): 45-52. a wild mandrill (Mandrillus sphinx) group. Fröhlich, M., R. Wittig & S. Pika. 2016. Should American Journal of Primatology 77(10): I stay or should I go? Initiation of joint travel 1036–1048. in mother–infant dyads of two chimpanzee Bronikowski, A.M., M. Cords, S.C. Alberts, J. communities in the wild. Animal Cognition Altmann, D.K. Brockman, L.M. Fedigan, A. 19(3): 483-500. Pusey, T. Stoinski, K.B. Strier & W.F. Morris. 2016. Female and male life tables for seven wild primate species. Scientific Data 3: pp.160006. * This is not an exhaustive list and focuses mostly Cavada, N., C. Barelli, M. Ciolli & F. Rovero. on publications from peer-reviewed journals. To 2016. Primates in human-modified and have your new publications listed in this section fragmented landscapes: the conservation of future African Primates, please send an e-mail relevance of modelling habitat and notice to [email protected]. 58 / Recent Publications Recent Publications
Galbany, J., O. Imanizabayo, A. Romero, V. Journal of Primatology 77(11): 1193–1206. Vecellio, H. Glowacka, M.R. Cranfield, T.G. Herzog, N.M., E.R. Keefe, C.H. Parker & K. Bromage, A. Mudakikwa, T.S. Stoinski & Hawkes. 2016. What's burning got to do S.C. Mcfarlin. 2016. Tooth wear and feeding with it? Primate foraging opportunities in ecology in mountain gorillas from Volcanoes fire-modified landscapes. American Journal National Park, Rwanda. American Journal of of Physical Anthropology 159(3): 432-441. Physical Anthropology 159(3): 457-465. Humle, T. 2016. Franco-Japanese and other Galbany, J., T.S. Stoinski, D. Abavandimwe, collaborative contributions to understanding T. Breuer, W. Rutkowski, N.V. Batista, chimpanzee culture at Bossou and the F. Ndagijimana & S.C. McFarlin. Nimba Mountains. Primates 57(3): 339-348. 2016. Validation of two independent Imong, I., H.S. Kühl, M.M. Robbins & R. photogrammetric techniques for Mundry. 2016. Evaluating the potential determining body measurements of gorillas. effectiveness of alternative management American Journal of Primatology 78(4): scenarios in ape habitat. Environmental 418–431. Conservation 43(2): 161-171. Goldstone, L., V. Sommer, N. Nurmi, C. Isbell, L.A. & L.R. Bidner. 2016. Vervet monkey Stephens & B. Fruth. 2016. Food begging (Chlorocebus pygerythrus) alarm calls to and sharing in wild bonobos (Pan paniscus): leopards (Panthera pardus) function as a assessing relationship quality? Primates predator deterrent. Behaviour 153(5): 591- 57(3): 367-376. 606. Granier, N. 2016. Chimpanzee research and Ito, A., W. Eckardt, T.S. Stoinski, T.R. Gillespie conservation in Bossou and the Nimba & T. Tokiwa. 2016. Prototapirella ciliates Mountains: a long-term international from wild habituated Virunga mountain collaborative effort in West Africa.Primates gorillas (Gorilla beringei beringei) in Rwanda 57(3): 349-357. with the descriptions of two new species. Gross, M. Chimpanzees, our cultured cousins. European Journal of Protistology 54: 47-58. 2016. Current Biology 26(3): R83-R85. Janmaat, K.R.L., C. Boesch, R. Byrne, C.A. Haurez, B., N. Tagg, C.-A. Petre, C. Vermeulen Chapman, B. Goné, B. Zoro, J.S. Head, M.M. & J.-L. Doucet. 2016. Short term impact of Robbins, R.W. Wrangham & L. Polansky. selective logging on a western lowland gorilla 2016. Spatio‐temporal complexity of population. Forest Ecology and Management chimpanzee food: how cognitive adaptations 364: 46-51. can counteract the ephemeral nature of ripe Habumuremyi, S., C. Stephens, K.A. Fawcett, T. fruit. American Journal of Primatology 78(6): Deschner & M.M. Robbins. 2016. Endocrine 626-645. assessment of ovarian cycle activity in wild Jantz, S., L. Pintea, J. Nackoney & M. Hansen. female mountain gorillas (Gorilla beringei 2016. Landsat ETM+ and SRTM data provide beringei). Physiology & Behavior 157: 185- near real-time monitoring of chimpanzee 195. (Pan troglodytes) habitats in Africa. Remote Hans, J.B., A. Haubner, M. Arandjelovic, R.A. Sensing 8(5): 427. Bergl, T. Fünfstück, M. Gray, D.B. Morgan, Kalousová, B., H. Hasegawa, K.J. Petrželková, T. M.M. Robbins, C. Sanz & L. Vigilant. Sakamaki, T. Kooriyma & D. Modrý. 2016. 2015. Characterization of MHC class II B Adult hookworms (Necator spp.) collected polymorphism in multiple populations of from researchers working with wild western wild gorillas using non-invasive samples lowland gorillas. Parasites & Vectors 9: pp.75. and next-generation sequencing. American Klass, K. & M. Cords. 2015. Agonism and African Primates 11(1) 2016 / 59 Recent Publications
dominance in female blue monkeys. associated calling in gorillas (Gorilla American Journal of Primatology 77(12): g. gorilla) in the wild. PloS ONE 11(2): 1299–1315. pp.e0144197. Knight, A., H.M. Chapman & M. Hale. 2016. Matsumoto, T., I. Noriko, S. Inoue & M. Habitat fragmentation and its implications Nakamura. 2016. An observation of a for endangered chimpanzee (Pan troglodytes) severely disabled infant chimpanzee in the conservation. Oryx 50(3): 533-536. wild and her interactions with her mother. Kühl, H.S., A.K. Kalan, M. Arandjelovic, F. Primates 57(1): 3-7. Aubert, L. D'Auvergne, A. Goedmakers, S. McLennan, M. & C. Asiimwe. 2016. Cars Jones, L. Kehoe, S. Regnaut, A. Tickle, E. kill chimpanzees: case report of a wild Ton, J. Van Schijndel, E. Abwe, S. Angedakin, chimpanzee killed on a road at Bulindi, A. Agbor, E.A. Ayimisin, E. Bailey, M. Uganda. Primates 57(3): 377-388. Bessone, M. Bonnet, G. Brazolla, V E. Buh, Minhós, T., L. Chikhi, C. Sousa, L.M. R. Chancellor, C. Cipoletta, H. Cohen, Vicente, M. Ferreira Da Silva, R. Heller, C. K. Corogenes, C. Coupland, B. Curran, Casanova & M.W. Bruford. 2016. Genetic T. Deschner, K. Dierks, P. Dieguez, E. consequences of human forest exploitation Dilambaka, O. Diotoh, D. Dowd, A. Dunn, in two colobus monkeys in Guinea Bissau. H. Eshuis, R. Fernandez, Y. Ginath, H. Biological Conservation 194: 194-208. Hart, D. Hedwig, M.T. Heegde, T.C. Hicks, Mjungu, D., M.L. Wilson, S. Foerster & A.E. I. Imong, K.J. Jeffery, J. Junker, P. Kadam, Pusey. 2016. Fighting back: population M. Kambi, I. Kienast, D. Kujirakwinja, recovery and expansion of the range size K. Langergraber, V. Lapeyre, J. Lapuente, of the Mitumba chimpanzee community K. Lee, V. Leinert, A. Meier, G. Maretti, S. in Gombe National Park, Tanzania. PeerJ Marrocoli, T.J. Mbi, V. Mihindou, Y. Moebius, Preprints. http://dx.doi.org/10.7287/PEERJ. D. Morgan, B. Morgan, F. Mulindahabi, M. PREPRINTS.1806V1. Murai, P. Niyigabae, E. Normand, N. Ntare, Moeller, A.H., S. Foerster, M.L. Wilson, A.E. L.J. Ormsby, A. Piel, J. Pruetz, A. Rundus, Pusey, B.H. Hahn & H. Ochman. 2016. C. Sanz, V. Sommer, F. Stewart, N. Tagg, Social behavior shapes the chimpanzee pan- H. Vanleeuwe, V. Vergnes, J. Willie, R.M. microbiome. Science Advances Vol.2(1): Wittig, K. Zuberbuehler & C. Boesch. 2016. pp.e1500997. Chimpanzee accumulative stone throwing. Motsch, P., C. Dilger, B. Ngoubangoye, J.-P. Scientific Reports 6: pp.22219 Gonzalez & G. Le Flohic. 2016. The sun‐ Leblan, V. 2016. Territorial and land-use tailed monkey (Cercopithecus solatus): first rights perspectives on human-chimpanzee- report of mother‐infant dorsal carrying elephant coexistence in West Africa (Guinea, behaviour in a forest guenon, Gabon. African Guinea-Bissau, Senegal, nineteenth to Journal of Ecology 54(2): 252-255. twenty-first centuries).Primates 57(3): 359- Motsch, P., G. Le Flohic, C. Dilger, A. Delahaye, 366. C. Chateau-Smith & S. Couette. 2015. Lu, A., T.J. Bergman, C. McCann, A. Stinespring- Degree of terrestrial activity of the elusive Harris & J.C. Beehner. 2016. Growth sun-tailed monkey (Cercopithecus solatus) in trajectories in wild geladas (Theropithecus Gabon: Comparative study of behavior and gelada). American Journal of Primatology postcranial morphometric data. American 78(7): 707–719. Journal of Primatology 77(10): 1060–1074. Luef, E.M., T. Breuer & S. Pika. 2016. Food- Nahoko Tokuyama, N. & T. Furuichi. 2016. Do 60 / Recent Publications Recent Publications
friends help each other? Patterns of female mountain gorillas (Gorilla beringei beringei). coalition formation in wild bonobos at Primates 57(1): 17-28. Wamba. Animal Behaviour 119: 27-35. Roth, A.M. & M. Cords. 2016. Effects of group Owens, J.R., S. Honarvar, M. Nessel & G.W. size and contest location on the outcome Hearn. 2015. From frugivore to folivore: and intensity of intergroup contests in wild Altitudinal variations in the diet and feeding blue monkeys. Animal Behaviour 113: 49-58. ecology of the Bioko Island drill (Mandrillus Ruiz-Lopez, M.J., C. Barelli, F. Rovero, K. leucophaeus poensis). American Journal of Hodges, C. Roos, W.E. Peterman N. Ting. Primatology 77(12): 1263–1275. 2016. A novel landscape genetic approach Qureshi, A. & O. Saeed. 2016. Ebola Virus demonstrates the effects of human Disease: From Origin to Outbreak. Elsevier disturbance on the Udzungwa red colobus Inc. monkey (Procolobus gordonorum). Heredity Patterson, L., R. Kalle & C. Downs. 2016. 116(2): 167-76. Predation of artificial bird nests in suburban Salmi, R., U. Rahman & D. Doran-Sheehy. gardens of KwaZulu-Natal, South Africa. 2016. Hand preference for a novel bimanual Urban Ecosystems 19(2): 615-630. coordinated task during termite feeding in Piel, A.K., N. Cohen, S. Kamenya, S.A. wild western gorillas (Gorilla gorilla gorilla). Ndimuligo, L. Pintea & F.A. Stewart. International Journal of Primatology 37(2): 2015. Population status of chimpanzees in 200-212. the Masito-Ugalla Ecosystem, Tanzania. Schlenker, P., E. Chemla, K. Arnold & K. American Journal of Primatology 77(10): Zuberbühler. 2016. Pyow-hack revisited: 1027–1035. two analyses of putty-nosed monkey alarm Plumptre, A. & S. Nixon. 2016. New survey calls. Lingua 171: 1-23. reveals dramatic decline of Grauer's gorilla. Schwitzer, C., R.A. Mittermeier, A.B. Rylands, Oryx 50(2): 203-203. F. Chiozza, E.A. Williamson, J. Wallis & A. Potts, K.B., E. Baken, A. Levang & D.P. Watts. Cotton. (eds.). 2015. Primates in Peril: The 2016. Ecological factors influencing habitat World’s 25 Most Endangered Primates 2014– use by chimpanzees at Ngogo, Kibale 2016. IUCN SSC Primate Specialist Group National Park, Uganda. American Journal of (PSG), International Primatological Society Primatology 78(4): 432–440. (IPS), Conservation International (CI), and Rosenbaum, S., J.P. Hirwa, J.B. Silk & T.S. Bristol Zoological Society, Arlington, VA. Stoinski. 2016. Relationships between iv+93pp. http://static1.1.sqspcdn.com/sta adult male and maturing mountain gorillas tic/f/1200343/26892107/1456949943947/ (Gorilla beringei beringei) persist across PrimatesInPeril2014-2016.pdf?token=wR1 developmental stages and social upheaval. 2v06E8FSElET0KkfCl3fiqDQ%3D Ethology 122(2): 134-150. Seiler, N. & M.M. Robbins. 2016. Factors Rosenbaum, S., J.P. Hirwa, J.B. Silk, L. Vigilant influencing ranging on community land and & T.S. Stoinski. 2016. Infant mortality risk crop raiding by mountain gorillas. Animal and paternity certainty are associated with Conservation 19(2): 176-188. postnatal maternal behavior toward adult Sakamaki, T., U. Maloueki, B. Bakaa, L. Bongoli, male mountain gorillas (Gorilla beringei P. Kasalevo, S. Terada & T. Furuichi. 2016. beringei). PloS ONE 11(2): pp.e0147441. Mammals consumed by bonobos (Pan Rosenbaum, S., A. Maldonado-Chaparro & paniscus): new data from the Iyondji forest, T. Stoinski. 2016. Group structure predicts Tshuapa, Democratic Republic of the Congo. variation in proximity relationships between Primates 57(3): 295-301. male–female and male–infant pairs of African Primates 11(1) 2016 / 61 Recent Publications
Stephan, C. & K. Zuberbühler. 2016. Turner, T.R., W.G. Coetzer, C.A. Schmitt, J.G. Social familiarity affects Diana monkey Lorenz, N.B. Freimer & J.P. Grobler. 2016. (Cercopithecus diana diana) alarm call Localized population divergence of vervet responses in habitat-specific ways.Royal monkeys (Chlorocebus spp.) in South Africa: Society Open Science 3(2): pp.150639. evidence from mt DNA. American Journal of Stone, O., A. Herries, J. Brink & S. Laffan. 2016. Physical Anthropology 159(1): 17-30. The chacma baboon (Papio ursinus) through Van Andel, A.C., S.A. Wich, C. Boesch, L.P. Koh, time: a model of potential core habitat M.M. Robbins, J. Kelly & H.S. Kuehl. 2015. regions during a glacial–interglacial cycle. Locating chimpanzee nests and identifying Evolutionary Ecology 30(4): 755-782. fruiting trees with an unmanned aerial Teichroeb, J.A. & W.D. Aguado. 2016. Foraging vehicle. American Journal of Primatology vervet monkeys optimize travel distance 77(10): 1122–1134. when alone but prioritize high-reward food Waters, S., A. El Harrad, Z. Amaouch & B. sites when in competition. Animal Behaviour Kubanova. 2016. Releasing confiscated 115: 1-10. Barbary macaques to improve awareness Tocheri, M.W., R. Dommain, S.C. Mcfarlin, of the illegal pet trade in Morocco. Global S.E. Burnett, C.D. Troy, C.M. Orr, N.T. Reintroduction News 216-220. Roach, B. Villmoare, A.B. Eriksen, D.C. Wiafe, E.D. 2016. Population studies of Kalthoff, S. Senck, Z. Assefa, C.P. Groves, Lowe’s Monkey (Mammalia: Primates: W.L. Jungers. 2016. The evolutionary origin Cercopithecidae: Cercopithecus lowei and population history of the Grauer gorilla. Thomas, 1923) in Kakum Conservation American Journal of Physical Anthropology Area, Ghana. Journal of Threatened Taxa 159: 4-18. 8(2): 8434–8442.
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Connections: E-News, Web Sites, and Social Media
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 Centre for Education, Research and Conservation African Wildlife Foundation of Primates and Nature (CERCOPAN) • Website: www.awf.org • Website: www.cercopan.org • Facebook: https://www.facebook.com/ • Facebook: www.facebook.com/CERCOPAN AfricanWildlifeFoundation • E-newsletter contact: webmaster@cercopan. • Twitter: http://twitter.com/AWF_Official org • Twitter: http://twitter.com/CERCOPANHQ Amboseli Baboons • Website: www.amboselibaboons.nd.edu Chimp Eden (JGI Sanctuary, South Africa) • Twitter: https://twitter.com/ • Website: http://www.chimpeden.com/ AmboseliBaboons • Twitter: https://twitter.com/jgisachimpeden
Barbary Macaque Awareness and Conservation Chimpanzee Sanctuary & Wildlife Conservation • Website: www.barbarymacaque.org Trust (Ngamba Island) • Newsletter: Contact sian@barbarymacaque. • Website: www.ngambaisland.com/ org • E-newsletter contact: info@ngambaisland. • Facebook: www.facebook.com/ org BarbaryMacaqueAwarenessandConservation • Facebook: www.facebook.com/ngambaisland • Twitter: https://twitter.com/Barbarymacaque • Instagram: https://www.instagram.com/ Colobus Conservation barbary_macaque/ • Website: www.colobusconservation.org • Facebook: www.facebook.com/pages/ The Bioko Biodiversity Protection Program Colobus-Conservation/137445029669543 (BBPP) • Twitter: http://twitter.com/ColobusConserva • Website: www.bioko.org • Facebook: English - www.facebook.com/ Conservation through Public Health pages/Bioko-Biodiversity-Protection- • E-newsletter contact: [email protected] Program/107673299261496; Spanish - www. • Facebook: Conservation Through Public facebook.com/BiokoBiodiversidad Health https://www.facebook.com/ • Twitter: http://twitter.com/Bioko_BBPP pages/Conservation-Through-Public- • Instagram: https://www.instagram.com/ Health/115176086614; CTPH Gorilla bioko_BBPP/ Conservation Camp: https://www.facebook. com/pages/CTPH-Gorilla-Conservation- Camp/239975179417714 • Twitter: http://twitter.com/CTPHuganda African Primates 11(1) 2016 / 63 Connections: E-News, Web Sites, and Social Media
Comoe Chimpanzee Guenon Conservation Community • Facebook: www.facebook.com/ • Facebook: www.facebook.com/pages/ comoechimpanzeecp/ Guenon-Conservation-Community/2031800 09723143?ref=stream The Drill Project • Website: thedrillproject.org/ HELP Congo (Chimpanzee Sanctuary) • Facebook: https://www.facebook.com/The- • Website: www.help-primates.org/ Drill-Project-258035237544233/ • Facebook: https://www.facebook.com/ HELP-Congo-29693148237/ East Africa Primate Diversity and Conservation Program Imfene Education and Conservation (Baboons) • Website: http://www.wildsolutions.nl/ • Website: www.imfene.org/ • Twitter: https://twitter.com/WildSolutions • Facebook: https://www.facebook.com/ ImfeneOutreach Ebo Forest Research Project • Website: www.eboforest.org International Gorilla Conservation Programme • E-Newletter contact: [email protected] • Website: www.igcp.org • Twitter: http://twitter.com/IGCP Falémé Chimpanzees • Twitter: http://twitter.com/FalemeChimps International Primate Protection League • Website: www.ippl.org Filoha Hamadryas Project • Facebook: www.facebook.com/ • Website: http://larissaswedell.org/filoha InternationalPrimateProtectionLeague • Facebook: https://www.facebook.com/filoha • Twitter: http://twitter.com/ipplprimate
Fossey Gorilla Fund International Primatological Society – • Website: https://gorillafund.org/ Conservation • Twitter: https://twitter.com/SavingGorillas • Website: www. internationalprimatologicalsociety.org GAIA – Great Ape Institute for Awareness • Twitter: http://twitter.com/ipsconservation • Website: www.gaiasanctuary.org/ • Facebook: https://www.facebook.com/ Jane Goodall Institute ProtectApes • 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 • Twitter: http://twitter.com/graspunep 64 / Connections: E-news, Web Sites, and Social Media
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Kyambura Gorge Chimpanzee Community Red-bellied Guenon • Facebook: https://www.facebook. • Facebook: www.facebook.com/ com/Kyambura-Gorge-Chimpanzee- Cercopithecuserythrogastererythrogaster Community-119478481457652/ Samango Monkey Project Le Projet Gorille Fernan-Vaz (Gabon) • Facebook: www.facebook.com/groups/ • Website: www.gorillasgabon.org/ samango/ • Facebook: https://www.facebook.com/pgfv. fvgp Save the Abandoned Chimps (Liberia) • Facebook: https://www.facebook.com/ LimbeWildlifeCentre abandonedchimps • Facebook: www.facebook.com/pages/Limbe- Wildlife-Centre/504832002861894 Society for Conservation Biology – Africa Section • Twitter: http://twitter.com/LimbeWildlife • E-mail list contact: Beth Kaplin bkaplin@ anticho.edu Lukuru Foundation • Website: www.lukuru.org Tacugama Chimpanzee Sanctuary • Facebook: https://www.facebook.com/ • Website: www.tacugama.com/ LukuruFoundation?fref=ts • Facebook: https://www.facebook.com/ Tacugama Lwiro Sanctuary • Twitter: http://twitter.com/Tacugama • Website: www.lwiroprimates.org • Facebook: www.facebook.com/lwiro Tai Chimp Project • Twitter: https://twitter.com/lwirosanctuary • Website: www.taichimps.org • Twitter: http://twitter.com/TaiChimpProject Mbeli Bai Study • Website: www.mbelibaistudy.org Uaso Ngiro Baboon Project • Facebook: https://www.facebook.com/Mbeli- • Website: http://www.baboonsrus.com/6.html Bai-Study-137426999658859/ • Twitter: https://twitter.com/mbelibai Ugalla Primate Project • Website: www.ugallaprimateproject.com Ngogo Chimp Project • Website: www.ngogochimpanzeeproject.org/ Vervet Monkey Foundation • Facebook: https://www.facebook.com/ • Facebook: www.facebook.com/groups/vervet NgogoChimps/ • Twitter: http://twitter.com/VervetMonkeys • Twitter: https://twitter.com/ngogochimps West African Primate Conservation Action Pan African Sanctuary Alliance (WAPCA) • Website: www.pasaprimates.org • WAPCA News contact: • E-newsletter contact: [email protected] [email protected] • Facebook: www.facebook.com/pages/PASA- • Facebook: www.facebook.com/pages/ Primates/150322194563 West-African-Primate-Conservation- • Twitter: http://twitter.com/pasaprimates Action/427913537273055
Pandrillus (Primate Sanctuary, Nigeria) Wild Chimpanzee Foundation • Website: www.pandrillus.org/ • Website: www.wildchimps.org/ • Facebook: https://www.facebook.com/ • Facebook: https://www.facebook.com/ Pandrillus-379304355421353/ wildchimps
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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 11, Issue 1 2016
Research Articles
A New Report of Chimpanzee Ant-fishing from the Issa Valley, Tanzania...... 1 Eden M. Wondra, Adam van Casteren, Alejandra Pascual-Garrido, Fiona Stewart, and Alexander K Piel
An Evaluation of the Oral Microbiome and Potential Zoonoses of the Southern Thick-Tailed or Greater Galago Otolemur( crassicaudatus) ...... 19 Antoinette Kotze, Desire L. Dalton, Michael Strinden, Michelle L. Sauther, Frank P. Cuozzo, and Anne C. Stone
Observation of an Encounter between African Wild Dogs (Lycaon pictus) and a Chimpanzee (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania ...... 27 Edward McLester, Fiona A. Stewart, and Alexander K. Piel
Brief Communications
An Infanticide Attempt After Male Takeover in Diana Monkeys (Cercopithecus diana diana) in Taї, Côte d’Ivoire ...... 37 Erin E. Kane and Frederic Gnépa
Preliminary Report on Bonobo (Pan paniscus) Feeding Ecology in a Forest-Savanna Habitat at Bolobo, Democratic Republic of Congo ...... 41 Ulrich Maloueki Mpaka Lutonadio, Kumugo Ndimbo, and Nseu Bekeli Mbomba
Documentation of Plant Consumption by Galago moholi in South Africa ...... 45 Ian Ray, Brandi T. Wren, and Evelyn J. Bowers
Birth of the African Primatological Society for the Future of African Primates ...... 49 Inaoyom Imong, Rachel Ikemeh, Inza Kone, and Denis Ndeloh
News ...... 51
Primatology Field Schools ...... 55
Recent Publications ...... 57
Connections: E-News, Web Sites, and Social Media ...... 62