American Journal of Primatology 00:1–10 (2012)
RESEARCH ARTICLE Newly Discovered Bale Monkey Populations in Forest Fragments in Southern Ethiopia: Evidence of Crop Raiding, Hybridization With Grivets, and Other Conservation Threats
ADDISU MEKONNEN1∗, AFEWORK BEKELE1, PETER J. FASHING2, JEAN-MARC LERNOULD3, ANAGAW ATICKEM4, AND NILS CHR. STENSETH4 1Zoological Sciences Program Unit, Faculty of Life Sciences, Addis Ababa University, Addis Ababa, Ethiopia 2Department of Anthropology and Environmental Studies Program, California State University Fullerton, Fullerton, California 3Conservation des Esp`eces et des Populations Animales (CEPA), Schlierbach, France 4Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biology, University of Oslo, Blindern, Oslo Norway Until recently, the Bale monkey (Chlorocebus djamdjamensis), an arboreal primate endemic to the southern Ethiopian highlands, remained virtually unstudied, and its distribution pattern inadequately documented. To broaden our knowledge of the species’ distribution and abundance, we carried out interviews with local people and total count surveys for Bale monkeys across 67 fragmented forest sites in human-dominated landscapes in the Oromia and Southern Nations, Nationalities, and People’s Regions, Ethiopia. From January 2010 to May 2011, we discovered 26 new Bale monkey populations inhabiting forest fragments at elevations ranging from 2,355 to 3,204 m asl. Across these populations, we recorded 37 groups ranging in size from 9 to 29 individuals (Mean = 19.5, SD = 4.5), for a total of 722 individuals. Black-and-white colobus monkeys (Colobus guereza) were sympatric with Bale monkeys at all sites, while grivet monkeys (Chlorocebus aethiops) were found only at sites where Bale monkeys did not occur. All of the newly discovered Bale monkey sites once contained bamboo forest, though at 35% of the sites bamboo forest had been eliminated during the past two decades. The persistence of Bale monkeys at fragmented sites lacking bamboo suggests greater habitat flexibility for the species than previously thought, though the long-term viability of populations both with and without bamboo remains uncertain. Human hunting in response to crop raiding, a behavior the monkeys engaged in at all sites, represents a major threat facing the newly discovered Bale monkey populations. Furthermore, despite their current lack of sympatry, apparently hybrid individuals between Bale monkeys and grivets were noted at three sites, posing yet another potential obstacle to Bale monkey conservation. Community conservation programs aimed at (1) protecting remaining habitat fragments, (2) planting bamboo and trees within and between fragments, and (3) reducing crop raiding represent the only hope for survival of the newly discovered Bale monkey populations. Am. J. Primatol. 00:1–10, 2012. C 2012 Wiley Periodicals, Inc.
Key words: Chlorocebus djamdjamensis; conservation; crop raiding; distribution; forest fragmen- tation; hybridization
INTRODUCTION for conflict between hungry primates and peo- Nonhuman primates face a variety of an- ple [Campbell-Smith et al., 2010; Cowlishaw and thropogenic threats including habitat destruction, Contract grant sponsor: Conservation des Especes` et des Pop- hunting, infectious disease, and climate change ulations Animals (CEPA); contract grant sponsor: Zoologis- [Chapman et al., 2006; IUCN, 2010]. The most se- che Gesellschaft fur¨ Arten- und Populationsschutz, Germany (ZGAP); contract grant sponsor: Le Conservatoire pour la Protec- rious immediate threat to the survival of many tion des Primates; contract grant sponsor: La Vallee´ des Singes primate species is habitat destruction for timber, Primate Park. ∗ agricultural land, and human settlement [Isabirye- Correspondence to: Addisu Mekonnen, Zoological Sciences Pro- Basuta & Lwanga, 2008; IUCN, 2010]. Habitat loss gram Unit, Faculty of Life Sciences, Addis Ababa University, PO has forced many primate populations to live in small Box 1176, Addis Ababa, Ethiopia. E-mail: [email protected] fragments isolated from one another by human- Received 25 August 2011; revised 17 November 2011; revision accepted 19 November 2011 dominated landscapes [Marsh, 2003]. Conversion of primate habitats into agricul- DOI 10.1002/ajp.21999 Published online xx XXXX xxxx in Wiley Online Library tural land, in particular, creates the potential (wileyonlinelibrary.com).
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Dunbar, 2000; Oates, 1996]. Crop raiding is an lion to 74 million. The resulting increasing human increasing source of human-wildlife conflict and demand for natural resources in Ethiopia has led many primate species living adjacent to agricul- to an alarming rate of deforestation. While initially tural land are known to engage in this behavior possessing 40% forest cover, the most recent esti- [Campbell-Smith et al., 2010; Hill, 1997; Lee & Pris- mates suggest that only 2.4% of Ethiopia remains ton, 2005; Marchal & Hill, 2009; Priston & Under- forested today [FDRE, 1998; Waktola, 1999]. Most down, 2009; Warren, 2008]. Local communities are of this forest clearance has been carried out to facil- likely to develop negative attitudes towards primate itate shifting agriculture, fuel wood collection, and species that crop raid, thereby further endanger- livestock production [FDRE, 1998; Waktola, 1999]. ing primates already at risk because of human en- From January 2010 to May 2011, we carried out croachment upon their habitat [Campbell-Smith et surveys to (1) improve our knowledge of the distri- al., 2010; Hill, 1997]. bution and abundance of Bale monkeys across the Habitat disturbance may also result in increased southern Ethiopian highlands and (2) document the chance of hybridization between taxa. For example, conservation threats the species faces because of the species previously separated by large tracts of for- degradation and loss of its habitat. Prior to our sur- est may encounter one another in agricultural areas veys, Bale monkeys were known primarily from sev- once forest has been cleared, leading to hybridization eral sites in and around Bale Mountains National [Chapman & Chapman, 1996; Detwiler et al., 2005]. Park in the Bale Mountains, Oromia Region (Fig. 1). Unfortunately, the conservation threats posed to pri- Here, we report the presence of newly discovered mate species by hybridization remain relatively lit- Bale monkey populations at 26 localities consisting tle studied [though see the excellent recent review of of forest fragments far to the W and SW of most pre- what is known on the topic by Detwiler et al., 2005]. viously known populations. At all 26 localities, Bale Species with limited distributions and narrow monkeys were directly observed or reported by lo- ecological niches are especially susceptible to extinc- cal people to engage in crop raiding. Furthermore, at tion caused by habitat disturbance [Yu & Dobson, three additional localities we recorded the presence 2000; Harcourt, 2006]. For example, the Bale mon- of likely hybrids between Bale monkeys (C. djamd- key (Chlorocebus djamdjamensis), an arboreal pri- jamensis) and grivet monkeys (C. aethiops). We sug- mate endemic to the southern Ethiopian highlands, gest strategies for conserving fragmented Bale mon- is at risk of extinction (IUCN classification: Vulner- key populations and expect that the new information able) because of rapid clearance of its bamboo for- on Bale monkey distribution, abundance, and con- est habitat [Butynski et al., 2008; Mekonnen et al., servation threats presented here will prove helpful 2010a]. While the full extent of the Bale monkey’s in updating the categorization of the species on the distribution remains unknown, its apparent dietary IUCN Red List. specialization on bamboo [Mekonnen et al., 2010a] suggests the species may lack the ecological flexi- bility to cope with disturbance to its habitat. Fur- METHODS thermore, Kingdon [1997] suggested that hybridiza- From January to June 2010 and December 2010 tion of Bale monkeys (C. djamdjamensis)withother to May 2011, Addisu Mekonnen and a team of more widespread and adaptable Chlorocebus spp. trained field assistants carried out surveys in 67 for- [e.g., grivets (Chlorocebus aethiops)orvervets(C. est fragments separated from one another by at least pygerythrus)] represents a potential threat facing 1 km of cultivated land and human settlement in two the species as its habitat is cleared for agricultural neighboring administrative regions, Oromia Region purposes. While the Bale monkey is unique among (West Arsi and Guji Zones) and Southern Nations, Chlorocebus spp. in its specialization on bamboo and Nationalities, and People’s (SNNP) Region (Sidama mostly arboreal lifestyle [Mekonnen et al., 2010a], and Gedeo Zones) (Fig. 1). We identified areas to sur- destruction of its habitat for agriculture could lead vey as those presently (or until recently) containing to crop raiding and spatial overlap and hybridiza- at least some bamboo and occurring at elevations tion with other more terrestrial Chlorocebus taxa. ranging from 2,000 to 3,300 m asl (i.e., the approxi- Indeed, J.-M. Lernould [pers. obs.] (who kept a tame mate range of elevations at which Bale monkeys are young male Bale monkey at home in Goba, Ethiopia known to occur). These areas generally consisted of at a time when the species was only known from some combination of bamboo-dominated forest, tree- the holotype) noted possible Bale monkey × grivet dominated forest, cultivated land, and human set- hybrids in Sidamo Province in 1969 though never tlement (Table I). The primary forms of human dis- published these observations. turbance in these areas included bamboo harvesting As for other primates, many of the anthropogenic and forest clearance for cattle ranching, cereal cul- threats faced by Bale monkeys can be linked to the tivation, and enset plantations [Ensete ventricosum high rate of human population growth in the coun- (Musaceae), the most important root crop and staple try where they occur. According to Ethiopia’s Central food for the Sidama people; Brandt et al., 1997]. Statistical Agency [2008], the population of Ethiopia During our surveys, we covered more than 4,300 nearly doubled between 1984 and 2007, from 40 mil- km by vehicle, motor bike, or horse to access the
Am.J.Primatol. Distribution and Conservation of the Bale Monkey / 3
Fig. 1. Map depicting portions of the Oromia Region (Bale, Guji, and West Arsi Zones) and SNNP Region (Gedeo and Sidama Zones), including the locations where Bale monkeys had been reported prior to our surveys (stars = extant populations; asterisks = extirpated populations).
TABLE I. Description of Habitat Types in Southern Ethiopia
Habitat type Description
Tree-dominated forest Habitat type composed primarily of indigenous trees Degraded tree-dominated Habitat type composed of mostly indigenous trees though at reduced densities because of forest deforestation by humans Bamboo forest Habitat type dominated by indigenous bamboo, A. alpina (Poaceae), interspersed with relatively few trees and shrubs Degraded bamboo forest Habitat type dominated by indigenous bamboo and some trees though at reduced densities because of harvesting by humans Bushland Habitat type dominated by woody shrubs and herbaceous plant species Human settlement Habitat type dominated by human settlement areas like villages Cultivated land Cultivated areas including agricultural fields and land being prepared for raising crops Protected habitat A legally protected area where cattle grazing and tree and bamboo harvesting are prohibited by the local government
67 survey sites. Upon arriving in a new area, we Chlorocebus spp., we stopped to record Global Po- carried out informal interviews with local people sitioning System (GPS) location (using a Garmin [e.g., Baker & Olubode, 2007; Davenport et al., GPS 12), altitude, habitat type(s) occupied, group 2008], asking them if bamboo forest currently (or size, instances of crop raiding, and morphological ev- previously) occurred nearby and showing them pho- idence of hybridization with other Chlorocebus spp. tographs of the three Chlorocebus spp. that occur in We also noted the presence of additional diurnal pri- Ethiopia: Bale monkeys, grivets, and vervets. During mate species, eastern black-and-white colobus mon- these interviews, we also asked whether Bale mon- keys (Colobus guereza), and baboons (Papio anubis), keys at a site (1) engaged in crop raiding, (2) were in forest fragments containing Bale monkeys. hunted, or (3) had been extirpated by humans. We recorded habitat types as bamboo-dominated If people reported the existence of Chlorocebus forest, tree-dominated forest, bushland, cultivated in an area, we then surveyed nearby forested sites land, or human settlements (see Table I for defini- by walking along existing paths or newly cut trails. tions of habitat types). We also noted when forested We conducted surveys in the early morning or late sites were heavily disturbed. We identified possible afternoon, when monkeys were most likely to be ac- hybrid individuals based on phenotypic features, in- tive [Struhsaker, 1981], at an average speed of 1.5– cluding coat color, facial hair (including moustache) 2.0 km/hr. Upon sighting Bale monkeys or other pattern, and tail length and color that appeared to
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be intermediate between C. djamdjamensis and C. boons were present at three of these sites as well aethiops [Aguiar et al., 2007; Bicca-Marques et al., (Table II). Grivet monkeys were never found in sym- 2008; Detwiler et al., 2005]. patry with Bale monkeys, but were observed at 13 Because forest patches surveyed were small (es- sites to the N and W of Bale monkey populations timated fragment sizes ranged from <1to10km2), (Fig. 2). Most (85%) grivet monkey populations oc- we attempted to identify and count all Bale mon- curred below the minimum elevation for Bale mon- key groups inhabiting them. This total count method keys (2,300 m asl), though at two localities (Arsi [Davenport et al., 2008; Plumptre & Cox, 2006] was Negele and Bowicha) they were found at ∼2,500 m used to estimate the population size of Bale monkeys asl. in each forest patch. Most monkey populations were All 26 new Bale monkey sites consisted of frag- partially habituated to human observers given the mented forest in human-dominated landscapes out- fragmented and human-dominated habitats they oc- side officially protected areas (Table II). At most cupied. Multiple individuals (Addisu Mekonnen and sites where Bale monkeys occurred, the bamboo for- local assistants) simultaneously counted the number est had either been degraded or, in several cases, of individuals in the groups encountered, though we eliminated and converted into human use areas for acknowledge that some group sizes may have been settlement, agriculture, or livestock grazing. Most at least slightly underestimated. We can be confi- sites containing Bale monkeys occurred on public dent, though, that we are reporting at least mini- lands (e.g., Bodie Mountain, Felada Mountain, Ger- mum group sizes. amba Mountain, and Sucha Mountain), though sev- Furthermore, though we treated each forest eral of the sites with the best protected remaining fragment containing Bale monkeys as a separate bamboo (and Bale monkeys) occurred on privately population in this study, we should note that the owned land (e.g., Guticha, Womma Shella). distance Bale monkeys are capable of dispersing be- During our surveys, local people reported the re- tween fragments through a matrix of human set- cent extinction of Bale monkeys at two sites near tlements and croplands is unknown. Despite our Hagere Selam (H.S.) town—Abera (10 km SW of ignorance about the dispersal capabilities of Bale H.S.) and Selassie Church (2 km N of H.S.)—in monkeys, it seems possible, or even likely, that some Sidama Zone (Table II). Indeed, the past presence of of the populations found in this study belong to a Bale monkeys at Abera can be confirmed from pub- larger metapopulation given that some fragments lished reports stating that the species occurred at containing Bale monkeys were located as little as this site 40 years ago [Carpaneto & Gippoliti, 1994; 1 km apart [e.g., Swart and Lawes, 1996; Anderson Dandelot & Prevost,´ 1972]. The extinctions at Abera et al., 2007a]. and Selassie Church were reputedly because of a We incorporated GPS locations of Bale monkey combination of habitat loss and hunting in response populations recorded during the current surveys, to crop raiding [Mulushewa Belachew, pers. comm.]. along with the locations of previously known pop- ulations [Butynski et al., in press; Mekonnen et al., 2010b], into geographic information system (ArcMap Crop Raiding v. 9.1) to create a distribution map for Bale monkeys. Across the newly discovered populations of Bale The research described here complied with the monkeys, conflict with humans was widespread. Lo- ASP Principles for the Ethical Treatment of Nonhu- cal people reported that Bale monkeys were crop man Primates and adhered to the legal requirements pests at all 26 sites. We were able to confirm these of Ethiopia. reports at five sites where we directly observed Bale monkeys engaging in crop raiding. Local people re- ported using dogs, spears, or traps to kill Bale mon- RESULTS keys at many sites. Distribution and Population Status Bale monkeys were observed at 26 of the 67 Hybridization With Grivets sites surveyed (Table II; Fig. 2). Local people re- Throughout the areas surveyed for Bale mon- ported the existence of Bale monkeys at an additional keys, we found no evidence of current sympatry five sites where their presence was not confirmed with grivets, though populations of the two species through direct observation. At sites where they were were found separated by as little as 12 km. Despite observed, Bale monkey populations occurred at ele- their apparent lack of sympatry, we observed pu- vations ranging from 2,355 to 3,204 m asl. A total of tative hybrid populations of C. djamdjamensis × 37 Bale monkey groups containing 722 individuals C. aethiops at three localities in Oromia Region: were recorded with groups ranging in size from 9 to Ekuma Mountain, Kulla Mountain, Wotiye. Mon- 29 individuals (Mean = 19.5, SD = 4.5). keys at these sites were morphologically different Black-and-white colobus monkeys were observed from Bale monkeys elsewhere (Fig. 3). In particu- at all sites where Bale monkeys occurred and ba- lar, all monkeys observed exhibited coat colors, tail
Am.J.Primatol. Distribution and Conservation of the Bale Monkey / 5 C. × C. djamdjamensis ) or Bale Monkey–Grivet ( Number of Number of Crop Other . C. djamdjamensis C. guereza 0467688 07509620464613 0750144 2,754 2,900 Sighting Sighting 2 2 31, 38 25, 34 Degraded TDF, no bamboo Degraded TDF, no bamboo Yes Yes CM 0465236 0694038 CM 2,632 Sighting 1 16 Degraded TDF, HS Yes CM a a a . ; CM, Eastern black-and-white colobus monkeys: C. aethiops and Papio anubis Location C. djamdjamensis Name of Woreda/zone/ Bale GPS location Method of groups individuals Habitat raiding primates ) Hybrids Were Sighted (1–29), Were Reported to Occur by Local People (30–34), or Had Recently Gone Extinct (35–36) in Southern Ethiopia Putative hybrid between Habitat type: BF, bamboo forest;Other BL, primates bushland; seen: CL, AB, cultivated Anubis land, baboons: HS, human settlement; TDF, tree-dominated forest. TABLE II. Description ofaethiops Survey Localities Where Populations of Bale Monkeys ( a 56 Kulla Mountain7 Shambel Kedir8 Ashena Forest9 Gorte Forest10 Kokossa/ West Ududa Arsi/ Oromia11 Afursa Mountain Nenesebo /West12 Arsi/Oromia Geramba Mountain Dodola/West13 Arsi/Oromia Bodie Mountain Hybrid 14 Sadisa Present Arbegona/Sidama/SNNPR Kedado Arbegona/Sidama/SNNPR Kokosa/West Forest Arsi/Oromia15 Felada Mountain Chire/Sidama/SNNPR16 Sucha 0506032 Mountain Present Bensa/Sidama/SNNPR17 0736328 Melke Dintu Gorche/Sidama/SNNPR Present Present18 Present Kankicha Chire/Sidama/SNNPR 0517175 2,72319 Keransa 0747695 Village 0468685 Chire/Sidama/SNNPR 046141220 0480669 Abaye 0741162 Kutre 0745412 Present Village 075225221 Loga 2,790 Present Forest Sighting Present22 Aroressa/Sidama/SNNPR Gelesho 2,681 3,204 Forest Bore/Guji/Oromia 0497602 2,740 Bore/Guji/Oromia23 Present Womma 0719694 0491434 Shella village 0460530 Sighting24 Hula/Sidama/SNNPR 0724153 Wotiye Present 0753015 Ana Sora/Guji/Oromia Sighting Sighting 125 0497610 Bubie 2,620 Kersa Sighting Present 0717408 2,77326 Guticha Ana 0503277 2,833 Area Ana Sora/Guji/Oromia Sora/Guji/Oromia27 0726091 2 Heto Dadi 0493681 2,805 Sighting28 1 Bondie 2 0700793 Forest Sighting 1 Present 2,637 Present Sighting29 Wolena Present Forest Present 2430 Kedida Ana 2,355 Sighting Forest Sora/Guji/Oromia 23, Damma/Guji/Oromia 0460635 17 045219931 Ana 2 Gerbicho Present 0459413 Sora/Guji/Oromia Present Kila 0464434 Degraded Sighting 0702232 0718249 23, BF, 2 18 070486832 CL Edume 1 0694705 Forest Uraga/Guji/Oromia BF Sighting &33 Damma/Guji/Oromia 21 TDF Buke 0467327 0470580 Forest Uraga/Guji/Oromia 2,674 2,676 18 2 Protected 2,670 0691184 BF,34 0681652 Siba BL, 2,628 Forest TDF Uraga/Guji/Oromia 29, Protected 21 235 TDF Sakaro Present Degraded village 20, TDF 25 Aleta and 2,693 Wondo/Sidama/SNNPR Hybrid 2,39036 BF Present Sighting 1 Abera Sighting Sighting Hula BF Not /Sidama/SNNPR Sighting and confirmed TDF 0471293 Selassie 16 Yes 24,14 BF Church, Yes and Abela 0443184 TDF 0678239 0448519 Gorche/Sidama/SNNPR Present Hula/Sidama/SNNPR 0727080 Sighting Present 13,19 Sighting 0698350 Degraded BF TDF, Yes Present and HS 1 Ana 1 Bule/Sidama/SNNPR TDF Sora/Guji/Oromia 2,360 1 CM CM 2 0444845 Not 2,468 BF Present 0443001 confirmed and 2,775 TDF Yes 0693351 15 Not 0689863 0444081 0441434 Yes confirmed 1 CM 1 0686949 0721820 Local 0450475 0449431 people Sighting CM, Degraded 2,846 AB 0754630 TDF 2,835 0681745 Not and Sighting Extinct Hula/Sidama/SNNPR confirmed Not HS 17, confirmed CM 23 2,711 2,628 Yes 0488673 Yes 11 0433547 23 2,407 0661329 Yes ? 2,563 0687789 9 0447542 Sighting Private 1 Sighting Local BF people and HS Degraded 0718587 HS BF CM Sighting 2 and Yes 21 Yes Local CM 18 2,205 TDF, HS people 2,987 HS CM Sighting Yes 2,693 TDF Extinct HS ? Yes Local and 1 people Local TDF 1 people CM CM ? ? 2 18, 23 0441508 CM 19 Sighting Yes 2 CM 0712177 ? ? Private BF BF Degraded and and TDF, HS HS HS 2,890 ? 27, CM 19 13 16 0 ? 16, 23 Private Degraded BF Degraded BF, Sighting TDF BF HS Yes ? and ? degraded Degraded BF BF, Yes TDF TDF HS Yes Yes Yes 0 Yes CM Degraded TDF, Degraded 0 HS BF CM CM Yes CM CM Yes Yes CM Yes BF and HS CM Yes CM CM Yes 0 CM Yes CM CM Yes CL CM Yes CM CM, AB Yes CM Yes CM No.12 Woge Abeyu3 locality Gata Forest4 Kokossa Forest Ekuma Mountain Kofele/West Arsi/Oromia Kokossa/West Kokossa/ Arsi Kokossa/West West Oromia Arsi/Oromia Arsi/Oromia region Present Hybrid Present Present 0469957 0478173 0485508 0765101 0774996 0744400 2,664 2,643 2,716 monkey Sighting Sighting Sighting X 2 1 1 Y 18, 24 Altitude, m 26 18 Degraded TDF, detection BF, HS Degraded Degraded TDF, BF bushland observed per Yes group Yes CM, AB CM Yes type(s) CM, AB (yes/no) present
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tal, we discovered 722 Bale monkeys belonging to 37 groups distributed across 26 new fragmented for- est sites, all occurring outside protected areas. Bale monkeys in the Oromia and SNNP Regions face ma- jor conservation challenges because of (1) degrada- tion of their habitats, (2) backlash against their crop raiding behavior, and, at some sites, (3) apparent hybridization with the more widespread and adapt- able grivet monkey (C aethiops). We hope that by having identified new Bale monkey populations and the threats they face, we have helped to further clar- ify the distribution and conservation status of Bale monkeys in southern Ethiopia.
Bale Monkey Distribution and Abundance Despite substantially widening the known dis- tribution of Bale monkeys (Fig. 2), our study failed to identify any populations that are large in size. In- deed, the largest population we found contained only 50 individuals. Even if the total counts conducted during our preliminary surveys slightly underesti- mated the number of individuals in these popula- tions [Baker et al., 2009; Plumptre & Cox, 2006], the sizes of these populations still fall far below the the- oretical threshold for population viability [Harcourt, 2002]. Although dispersal between at least some of the forest fragments is probably possible [e.g., An- derson et al., 2007b], the long-term prognosis for the Fig. 2. Map of Bale monkey and grivet monkey localities in small Bale monkey populations in these fragments southern Ethiopia discovered during our current research, in- is poor, even without considering the other conser- cluding localities of presumed hybridization. Letters A-–K rep- resent different Woredas (administrative districts): A, Kofele; vation threats facing these monkeys (see below). B, Dodola; C, Nenesebo; D, Aroresa; E, Bensa; F, Kokosa; G, Arebegona; H, Hula; J, Bore and K, Uraga. Asterisks indicate grivet monkey localities, circles indicate Bale monkey localities, and triangles indicate possible hybrid populations. Sympatry With Other Primates We found that throughout the southern range of Bale monkeys, the species lives in sympatry lengths, and whisker lengths that were intermedi- with eastern black-and-white colobus monkeys (C. ate between Bale and grivet monkeys. Furthermore, guereza). Indeed, the two species were often observed the putative hybrids had white tail tips and white in proximity to one another during our surveys [Ad- browbands that are larger in grivets and absent in disu Mekonnen, pers. obs.], a phenomenon warrant- Bale monkeys. Photos of examples of putative hy- ing further study. These apparent associations may brids from Wotiye and Ekuma Mountains are pro- arise because of the small sizes of the forest frag- vided in Figure 3c and d, respectively, along with ex- ments they occupy, dietary overlap among fellow amples of pure Bale monkeys (Fig. 3a,b) and grivets folivores [Fashing, 2001; Mekonnen et al., 2010a], (Fig. 3e,f) from other sites for comparative purposes. or predator avoidance benefits [e.g., Bshary & Noe,¨ Curiously, none of the three sites with putative hy- 1997] resulting from colobus monkeys appearing to brids contained bamboo forest, yet group sizes of hy- prefer the top canopy and Bale monkeys the middle brids were larger on average (Mean = 28.8; n = 5 and lower canopies [Addisu Mekonnen, pers. obs.]. groups) than those of pure Bale monkeys at other On the other hand, we found no evidence for cur- sites (Mean = 19.5; n = 37 groups). rent sympatry between Bale monkeys and grivets or vervets in the areas surveyed. This lack of over- lap appears to result from differences in altitudinal DISCUSSION range and habitat preferences between Bale mon- Our study extends the distribution of the Bale keys and their congeners. While grivets and vervets monkey (C. djamdjamensis) to Guji and West Arsi tend to prefer lower elevations and drier woodland Zones of Oromia Region and to Sidama Zone of SNNP habitats [Jaffe & Isbell, 2011; Zinner et al., 2002], Region in the southern Ethiopian highlands. In to- Bale monkeys tend to occupy high elevation sites
Am.J.Primatol. Distribution and Conservation of the Bale Monkey / 7
Fig. 3. Comparison of appearance of pure C. djamdjamensis, C. aethiops, and their putative hybrids. (a, b) Adult male pure C. djamdjamensis from Odobullu Forest. Note that the pelage is relatively brown, a white browband is absent, the whiskers are short, and the tail is short with no tuft. (c) Adult male putative hybrid C. djamdjamensis × C. aethiops at Wotiye, Ana Sora Woreda possessing an intermediate coat color that is grayer than that of a pure Bale monkey but less gray than that of a pure grivet. The animal possesses a white browband, though it is smaller than that of a pure grivet. (d) Subadult male putative hybrid C. djamdjamensis × C. aethiops at Ekuma Mountain, Kokossa Woreda exhibiting a coat color intermediate between that of a Bale monkey and a grivet, a tail of intermediate length, a very small white tail tuft, and a small white browband and moustache. Pure adult grivet monkeys from Awash National Park (e) and Wondo Genet (f) with grayish-gold fur, thick white browbands, long, white, and slightly curved whiskers, black faces with white moustaches, and long tails whose bases contain tufts of white hairs on both sides. containing some bamboo forest [Mekonnen et al., in Oromia and SNNP Regions. Of the 26 new local- 2010a,b; this study]. ities where Bale monkeys were discovered, only 17 contained bamboo. It should be noted, however, that the nine sites lacking bamboo held the species until Evidence of Habitat Flexibility recently (i.e., within the past ∼20 years) according Previous surveys across the Bale Mountains to local people. At most of these sites, humans are area (in Bale Zone, Oromia Region; Fig. 1) suggested presumed to have eliminated the bamboo through that Bale monkeys occurred only in bamboo forest overexploitation, though at Kulla and Ekuma Moun- [Mekonnen et al., 2010b]. Indeed, a detailed ecolog- tains (Kokossa area) people reported that bamboo ical study of Bale monkeys undertaken at Odobullu disappeared naturally after last producing seeds ∼20 Forest (Fig. 1) in Bale Zone found that 77% of their years ago. diet consisted of a single species of bamboo, Arundi- The persistence of populations of Bale monkeys naria alpina (Poaceae) [Mekonnen et al., 2010a]. We for over a decade in heavily disturbed forest frag- were therefore surprised to find Bale monkeys living ments lacking bamboo suggests the species is ca- in forests lacking bamboo during our recent surveys pable of greater habitat flexibility than previously
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believed [e.g., Mekonnen et al., 2010a,b]. Unlike ex- A third threat to Bale monkeys for which treme bamboo specialists such as bamboo lemurs we found evidence is hybridization with other (Hapalemur spp.) [Tan, 1999], for example, Bale more widespread and adaptable Chlorocebus species monkeys are able to subsist on other food sources in [Kingdon, 1997]. Since the three sites (Ekuma Moun- bamboo-less forest fragments. More intensive study tain, Kulla Mountain, and Wotiye) at which proba- is needed, however, to determine exactly how Bale ble hybrids were found are at elevations well above monkeys manage to survive in suboptimal habitat. where grivets occurred in our surveys, and even Incidentally, the captive Bale monkey kept by J.-M. adult individuals at the three sites appeared to be Lernould [pers. obs.] in Goba in 1969 subsisted on hybrids, the hybridization must have occurred long grass and insects as well as a variety of provisioned ago. As Detwiler et al. [2005] noted, hybridization fruits and vegetables though the long-term ability of between closely related taxa is often facilitated by captive Bale monkeys to survive on such unnatural anthropogenic habitat modification. Given the dif- diets is unknown. ferences in habitat preferences between grivets and Bale monkeys [Mekonnen et al., 2010a,b; Jaffe & Isbell, 2011; Zinner et al., 2002], it seems probable Conservation Threats that past (and potentially future) zones of contact While the evidence for ecological lability un- were in agricultural areas to which the two taxa covered by our study is encouraging, the long-term were attracted for crop raiding. Further research prospects for the small Bale monkey populations in on the population genetics and molecular phylogeny fragments both with and without bamboo remain of the “phenotypically hybrid” monkeys observed in grim. As for many primates [Chapman et al., 2006; our surveys is recommended to confirm that the pre- IUCN, 2010], habitat loss is the greatest threat fac- sumed hybridization hypothesized in our study did ing Bale monkeys in southern Ethiopia. All 26 for- indeed occur. Because the remaining numbers of est fragments where Bale monkeys were found dur- Bale monkeys appear to be small [Mekonnen et al., ing our surveys occurred amidst a matrix of human 2010b; this study], we concur with previous sugges- settlements and cultivation and were undergoing ex- tions that the potential for genetic swamping by the tensive habitat modification. Unfortunately, a recent more abundant grivet must be considered a real long- study of a far more flexible species, C. guereza in term risk for Bale monkeys [Kingdon, 1997; Detwiler small, heavily disturbed Ugandan forest fragments et al., 2005]. found that their numbers declined by 55% over just an 8-year period during which they experienced ex- tensive habitat degradation and loss of the sort re- Conservation Status and Recommendations ported in our study of Bale monkeys [Chapman Bale monkey populations in southern Ethiopia et al., 2007]. are under immense anthropogenic pressure because Another threat placing the newly discovered of rapid habitat loss and hunting, and may also be Bale monkey populations in Oromia and SNNP Re- threatened via hybridization with grivets. Consider- gions at risk of extirpation is hunting by local peo- ing these threats along with their narrow geographic ple in response to crop raiding by the monkeys. Bale distribution and generally small remaining popula- monkeys were observed or reported to be crop raiders tion sizes, Bale monkeys appear to face a high risk at all sites where they were found during our sur- of extinction. We fear that most extant Bale monkey veys. At Felada Mountain and Melke Dintu, for ex- populations will not be sustainable over the long- ample, we watched Bale monkeys feeding on barley term without immediate conservation action. As a planted near the edge of the forest [Mekonnen, pers. result, we suggest that the species be given serious obs.]. Elsewhere, they entered agricultural areas to consideration by IUCN for elevation to “Endangered” feed on other cereals, vegetables, fruits, and enset. status from their current designation of “Vulnera- Like other crop raiding primates [Campbell-Smith ble” [Butynski et al., 2008]. In the meantime, further et al., 2010; Hill, 1997; Lee & Priston, 2005; Marchal surveys are needed to determine the remaining num- & Hill, 2009; Warren, 2008], having lost their pri- bers of Bale monkeys in the Bale Mountains range mary food item (bamboo) to human disturbance, Bale as well as the conservation threats the monkeys face monkeys have extended their diet to include agri- in that area [Mekonnen et al., 2010b]. cultural products, resulting in conflict with nearby The newly discovered Bale monkey populations human populations [Cowlishaw & Dunbar, 2000]. In occurring outside formally protected areas in the response, humans have turned to hunting Bale mon- Oromia and SNNP Regions of southern Ethiopia keys as crop pests, though taboos prevent local peo- provide opportunities for community-based conser- ple from consuming the monkeys after killing them vation. Indeed, sustainable resource management [Mekonnen, pers. obs.]. As long as the monkeys con- projects were recently initiated by the Agriculture tinue to intensively raid crops, efforts to convince Offices of the Chire, Kokossa, and Arbegona Woredas local people to conserve them are probably doomed (i.e., administrative districts). These projects may in to fail. the future generate income by attracting ecotourism
Am.J.Primatol. Distribution and Conservation of the Bale Monkey / 9
which would provide funds for the local community The “tree against hunger”: enset-based agricultural systems [Wearing & Neil, 2009]. These activities would, in in Ethiopia. Report to the American Association for the Ad- turn, presumably help promote conservation of the vancement of Science, Awassa Agricultural Research Cen- ter, Kyoto University Center for African Area studies, and monkeys and their habitats [Wearing & Neil, 2009]. University of Florida. 56 p. In addition to the protection of existing habitats, Bshary R, Noe¨ R. 1997. Red colobus and diana monkeys restoration of bamboo forest within and between for- provide mutual protection against predators. Anim Behav est fragments must be a primary goal of Bale mon- 54:1461–1474. Butynski TM, Atickem A, De Jong YA. In press. Bale monkey key conservation efforts. Lastly, solutions must be (Chlorocebus djamdjamensis). In: Butynski TM, Kingdon found to reduce crop raiding which will help to in- JS, Kalina J, editors. The mammals of Africa. Vol. 2. Ams- crease support for Bale monkey conservation efforts terdam, The Netherlands: Primates Academic Press. among the local community and may even help to Butynski TM, Gippoliti S, Kingdon J, De Jong Y. 2008. Chloro- prevent future hybridization between Bale monkeys cebus djamdjamensis. In: IUCN Red List of Threatened Species Version 2010.4.
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