Black-and-white colobus monkey (Colobus vellerosus)

Mohamed bin Zayed Species project number 10251554

Background information

Two species of black-and-white colobus occur in Côte d'Ivoire: Colobus polykomos (Zimmerman, 1780), the king or western pied colobus, and C. vellerosus (I. Geoffroy, 1834), the ursine or Geoffroy's pied colobus (see Oates and Trocco 1983; Oates, 1994). Colobus vellerosus ranges from the Bandama River to western Nigeria (Oates et al., 1994; Kingdon, 1997). Colobus polykomos ranges from Guinea to the Sassandra River in western Côte d'Ivoire (Napier 1985; Oates et al., 1994; Groves 2001). Between the Sassandra and the Bandama Rivers, occurs in a narrow strip a population of black-and-white colobus whose taxonomic status is not yet clear. At least part of this population was originally described as the taxon dollmani (Booth, 1954), but recent accounts regard the "dollmani" specimens as hybrids, best referred to the species C. vellerosus (Groves, 2001; Grubb et al., 2003). It is still a matter of contention, however, whether "dollmani" might constitute a consistent morphotype or whether there are local populations that differ according to the degree of gene influx from C. polykomos or C. vellerosus.
During a survey of the forests between the Sassandra River and the Bandama River in Côte d'Ivoire, we were able to observe black-and-white colobus monkeys in only one forest reserve and we refer to this form as dollmani (Gonedelé Bi et al. 2006). However, Oates and McGraw (2009) are not yet convinced about whether these monkeys can be assigned to the taxon "dollmani" in the absence of a careful description of the monkeys observed there.
Because there is no consensus on the most appropriate classification of the form of black-and-white colobus occurring between the Sassandra River and the Bandama River, we refer to it in this proposal as "Colobus vellerosus".
In addition to the uncertainty as to the existence of a distinct form of colobus monkey that might be placed in the taxon dollmani, the continuous decline of Côte d'Ivoire forest due to forest encroachment and conversion to agriculture pose a particular threat to the remaining population of black-and-white colobus monkeys of the interfluvial region between Sassandra and Bandama rivers.

Methods 

Survey sites
From June 2011 to January 2013, we conducted surveys in forests at the interfluvial region between the Sassandra and Bandama Rivers (Figure 1). Based on information about the historical and recent distribution of the black-and-white colobus occurring at this region (Gonedelé Bi et al., 2006; 2008; Oates & McGraw, 2009), we conducted surveys in four forêts classées (forest reserves) (Dassioko Sud, Port Gauthier, Niégré, Bolo Ouest), one national park (Marahoué), two sacred groves (Grébouo 1, Bohico) and two rural community forest (Bakadou, Zahibré and Niapidou).

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Primate population survey
We interviewed people in villages close to the respective survey areas (particularly hunters/poachers, but also staff from the forestry service), asking them to describe the primates they know and to mimic their calls. We showed them photographs or drawings of the species afterwards to confirm their identifications. We gathered information about the presence of primates, particularly black-and-white colobus in the forests investigated.
During the actual survey in the areas, we walked slowly and quietly along old logging roads and existing paths at about 1-1.25 km/hour, for an average of 9 hours per day. We walked the paths back and forth, noted any visible or acoustic sign of the presence of primates, and determined their position with a GPS. We began early in the morning at 06:30 h and continued until 12:00 h. After two hours rest, we proceeded with the survey until 17:30 h. When a group of monkeys was detected, we stayed with the group and observed it for as long possible. Kingdon (1997) was used for the identification of species and subspecies.

Vocalization Recording

Vocalizations were recorded from black and white colobus in two forest groves : Dinaoudi forest grove in eastern Côte d'Ivoire and Grébouo 1 forest grove in central Côte d'Ivoire. Data were recorded between July 2012 and January 2013. Vocalizations of black-and-white colobus from Taï National Park were obtained from Karim Ouattara for comparison.
Calls were recorded with Sony TCD-D100 and TCD-D8 digital tape recorders, equipped with Sony EMS-907 microphones. To increase the number of recorded vocalizations, we used both all-occurrence and focal animal sampling methods (Altmann, 1974). We recorded all of the spontaneously occurring vocalizations without knowing the emitter identity and without the use of visual or acoustic playbacks.

Awareness campaign
The project also makes an attempt to bring the local communities into the forefront of black-and-white colobus and their habitat conservation. Training provided under the project focused on providing local people with the skills and understanding to protect targeted species and to manage their habitat.
A meeting was held in the nearest village surrounding the surveyed forests in both formal and informal setting.

Members of local communities was organized as plant nursery volunteers for the propagation of native plants to support the revegetation of the forest grove where where a population of black-and-white colobus was found.

Data analysis

Survey data analysis
Data recorded for each primate observation included: date, time, species and location and group size. Since our survey method did not met transect line methods, we did not estimate the density of the populations. However, we estimated the relative abundance based on animal encounter rate, or "sightings" per km (National Research Council, 1981; Sutherland, 2002).

Acoustic Analysis

Recordings were digitalized at a sample rate of 44100 Hz (16-bit resolution, mono format) with Raven Pro 1.4. After a preliminary qualitative analysis of the entire recordings, we selected and saved into separate files all vocalizations whose recording quality allowed their subsequent quantitative descriptions.
The total sample of selected vocalizations comprised 24 black-and-white colobus long calls emitted belonging to 3 groups. Therefore we measured inspiration duration (IR) and expiration duration (ET) of the whole vocal emission for each defined group.
Statistical analyses were performed with Statistica 6.1 for Windows (StatSoft, Tulsa, Oklahoma). Using univariate statistics, we calculated the median for each measured acoustic parameter per subject. Using these medians, we applied Student's t-test for each parameter to test whether there were any significant differences among the 3 populations.

Results

Distribution and relative abundance of primates between the Sassandra and Bandama Rivers

Our survey efforts encompass 10 most conserved forest fragments extending between the Sassandra and Bandaman Rivers.
Between the Sassandra and Bandama Rivers, no population of black-and-white colobus actually survived, except for a population occurring in a forest grove in the village of Grébouo 1 (UTM coordinates: N 0793849; W 0626724). Grébouo 1 is a small remote village in Soubré Department in the South-western Côte d'Ivoire around 45 kilometers from Soubré and 100 kilometers from Gagnoa (Figure 1). This region is referred to as Guinean zone, covered by a dense evergreen rain forest. In Grébouo 1, primates live in close proximity to people, although they often stay out of sight in the neighboring forest. The forest serves as a retreat for the monkeys, and is about 16 ha in size and contiguous to the village. The Grébouo 1 forest grove owes its existence directly to the beliefs, culture and history of the local people, consisting of Bété ethnic group. Community elders acted as the guardians of the sacred site and cutting of trees or destruction of vegetation around it is "prohibited".
The facial fringe of the black-and-white colobus inhabiting Grébouo 1 forest grove is pure or creamy white, bushy and restricted to the circumfacial region with a white stripe on the thigh. In all these defined aspect, this population is similar to Colobus vellerosus. However the black-and-white colobus of Grébouo 1 has a tail relatively long and untufted, in that aspect similar to Colobus polykomos.
Images of the form of black-and-white colobus found in the forest grove of Grébouo 1 are shown in Figure 2.

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Of the 8 diurnal primate taxa that were expected in each of the 7 forests surveyed, we found 0 to 6 taxa per forest (Table 1). Niégré FR, Bolo Ouest FR and Marahoué NP are the forests were we could find any presence of primates. Dassioko Sud forest reserve presents the highest number of primate taxa relative to the other forest. Three primate taxa (Cercopithecus diana, Cercocebus atys lunulatus, Pan troglodytes) inhabiting this forest are among the most threatened primates in West Africa.
Black-and-white colobus was encountered at 0.19 groups/km (Table 1) in Grébouo 1. Cercopithecus campbelli and Cercopithecus petaurista were the most common taxa observed. They were observed in 7 out of the 10 forests surveyed with respectively the highest encounter rate in each of the forest surveyed, except for Grébouo 1 forest grove where Colobus vellerosus was more observed than C. petaurista.

Dassioko Sud and Port Gauthier FR are actually facing severe threats from logging, intensive forest clearance for agriculture purpose and intensive poaching.
We estimated forest clearance to around 90% of the forest zone covered by our foot survey in Dassioko Sud and Port Gauthier FC.
Evidence of poaching in Dassioko Sud FC and in Port-Gauthier FC was noted with the presence of poachers in the forest, logging and the observation of used gunshot shells and several poaching paths throughout the forest (Figure 3).
For Bolo Ouest and Niégré FR, no forest fragment remained; these two reserves have been completely transformed into cocoa plantations (Figure 3).

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Awareness campaign

Meetings have been held among local population in the localities visited in both formal and informal setting, with a special focus in Grébouo 1 where a population black-and-white colobus was observed. One meeting has been held every month (from December 2011 to January 2013) in each of the six villages surrounding the forest grove in both formal and informal setting. These meetings have been attended by prominent leaders and others in each community (Figure 3). Educational materials (posters, flyers) have also been produced and distributed in different villages in addition of the Primate field Guide by John Oates (Oates, 2011). Four signs indicating the presence of the forest grove and reminding the public of the protected status of the forests and warning people not to cause damage have been placed around the forest (Figure 3).
As part of the awareness building efforts, the Project leader met different administrative authorities (Deputy, Mayor, Prefect, Subprefect), Forest Department Personnel and inform then about the importance of Grébouo 1 forest groves ant its threatened black-and-white colobus.
All interviewees claimed that the Project‘s public awareness and education activities have helped to generate greater interest in the conservation of the sacred grove and its colobus. This is illustrated by the numbers of members of local communities that served as plant nursery volunteers (Figure 3). The nursery propagates native plants to support the revegetation of the forest grove.

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Evaluation of threats to Grébouo 1 forest groves

Before starting awareness campaign around Grébouo 1 forest grove, several cases of desecration were observed in the forest, namely hunting, smashing bundle, cutting of trees for house building (Figure 4). If tree felling, burning and fagots cutting was practiced by native peoples (Bété ethnic group), hunting was practiced by non-native (Baoulé ethnic group) and foreigners (population from Mali and Burkina Faso) that have their plantations around the forest. During that period, at least two gun shots were heard per day around or inside the sacred forest. The forest was also severely degraded with a mean number of 1.68 (±1.27) cut trees / m2. After the awareness campaign among communities living around Grébouo 1 sacred grove, hunting ceased in the forest as well as faggot cracking and trees cutting and burning.

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Statistical comparisons between subsets of vocal data

Student's t-Test was used to test differences between different populations of black-and-white colobus in single acoustic parameters.
The parameters of 24 analyzed calls are summarized in Table 2. When considering the number of expiration per second, no significant difference was observed between the population of Colobus vellerosus of Grébouo 1 FG and the population of Colobus polykomos of Taï NP (N=8, t=-0.139, p=0.89), whereas significant differences were observed between the populations of Grébouo 1 and Dinaoudi (N=8, t=4.47, p<0.001) and between Dinaoudi vs Taï (N=8, t=-4.88, p<0.001).
No significant difference was observed between the three groups when considering Inspiration Duration (P > 0.05) (Grébouo 1 vs Dinaoudi : N=8, t=0.113, p=0.91; Grébouo 1 vs Taï : N=8, t=-1.71, p=0.11; Dinaoudi vs Taï : N=8, t=-0.91, p=0.38).
For the Expiration Duration no significant difference was observed between the population Grébouo 1 vs Dinaoudi (N=8, t=0.57, p=0.58), whereas significant differences were observed between the populations of Grébouo 1 vs Taï (N=8, t=-5.69, p<0.001) and between Dinaoudi vs Taï (N=8, t=-2.98, p<0.001).

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Students involvement

Three undergraduate students: one in the Department of Zoology (http://www.csrs.ch/fichiers_csrs/recrutement_dea_pcbd.pdf), another one in the Department of Botany and the third one in the Department of Anthropology at the University Félix Houphouet Boigny in Abidjan received training in field survey techniques (Figure 5). They gained experience in the use of field equipment and methodologies, and new insights to biodiversity conservation that will enhance their work as conservation scientists.

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Discussion

The presence of the form of black-and-white colobus in Grébouo 1 (Soubré region) that has a similar coat pattern like Colobus vellerosus, confirm the thoughts of Oates & McGraw (2009) who argued that the populations of black-and-white colobus monkey in the Bolo-Dassiéko-Niégré complex are members of Colobus vellerosus. Since this forest complex is in the vicinity of Grébouo 1, the same population should have been expected there. Our data also concord with the map drawn by Booth (1954) showing the presence of vellerosus to the west of the lower Bandama River, including one in the approximate vicinity of Gagnoa (6°08'N, 5°57'W). Gagnoa is about 100 km from Grébouo 1 and 90 km from the northern limits of the Bolo- Niégré forest complex (see Fig. 1). Based on Booth's map, it might be expected that the form of black-and-white colobus monkey inhabiting this forest complex is Colobus vellerosus rather than dollmani.
Since 2000, no population of black-and-white colobus has been observed around and in Marahoué National park. With the actual transformation of this park and its adjacent forest fragment into cocoa plantations, there is no doubt that the population of black-and-white colobus that has been called dollmani is already extinct.
The other population of black-and-white colobus that extend between the Sassandra and Bandama rivers would have faced the same fate if the actual population found in the Grébouo 1 did not get a refuge in the forest grove of this village. This pinpoints the importance of forest groves in preserving threatened species. The key role played by local communities believes in preserving population of black-and-white colobus has been recognized elsewhere in Côte d'Ivoire and in West Africa (Gonedelé Bi et al., 2010; Baker et al., 2009).
As respect for traditional values and ancestral beliefs declines, the threat to the few remaining individuals of black-and-white colobus will continue to increase. The erosion of traditional values, especially among the youth, has rendered the Grébouo 1 forest grove vulnerable to encroachment, overexploitation and desecration. This coupled with growing human needs for forest products and land for agriculture, will lead to the illegal appropriation and destruction of the forest groves, resulting in decline or the complete disappearance of the population of black-and-white colobus inhabiting this forest.
The forest reserves in Côte d'Ivoire are on continuous decline in the absence of control, threatening their global biodiversity. Several of the threatened taxa that previously inhabit these forests have gone locally extincted. Primates have been encountered in the other forest at a very lower rate. This indicates how vulnerable the global biodiversity of Côte d'Ivoire is and highlights that urgent and strong conservation actions are needed to protect the remaining forests.
Hour vocalization data based on the number of expiration per second indicate that the form of black-and-white colobus found in Grébouo 1 forest grove is more similar to Colobus polykomos than to Colobus vellerosus and contrast with the similarity found between the population of Grébouo 1 and Colobus vellerosus in their feature pattern. However vocalization data based on Expiration Duration indicates that the population of black-and-white colobus found in Grébouo 1 is more similar to Colobus vellerosus. Our data seem very limited to shed firm conclusion. Continued study and collection of more accurate and large vocalization data including the vocalization context, could offer insights on the similarities between these populations. Molecular data analyses are on way and could also help to clarify the affinity of the population of black-and-white colobus that survived in Grébouo 1 forest grove.
Further intensification of poaching or a continued conversion of sacred groves into agriculture would lead to the extirpation of this unique population for which urgent conservation actions are needed.

Recommendations

• Threats to the sacred forest of Grébouo 1 still exist, due to the presence of a large community of allochtones in the villages that surround the forest grove. These populations are not always respectful of local tradition. There is therefore the risk for hunting, cutting of trees to build houses that could destroy their habitat and leaving it open to predation. This threat can be mitigated by offering the local communities with alternative sustainable livelihoods like eco-tourism so that they can see the value of forest grove and the primates it inhabits.
• There is need for more vocalization data collection and a genetic analysis of the population of black-and-white colobus that survided in Grébouo 1 to firmely highlight their affinity with Colobus vellerosus and Colobus polykomos.
• The level of awareness among the local community, governmental and non-governmental organisations working in the area was surprisingly low. It is only by creating awareness among all the stakeholders both locally and nationally that the form of black-and-white colobus that survived in Grébouo 1 will be accorded formal protection to save it from the threat of global extinction.
• A local conservation initiative by the people living around Grébouo 1 forest grove should be formed with the aim of protecting their rich biodiversity resources through sustainable management and advocating for sustainable livelihoods. This noble initiative currently requires external support especially on organizational capacity building, alternative livelihood generation, tourism infrastructure development and marketing of the area for sustainable tourism.

References
Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49: 227-67.
Baker, L. R., Tanimola, A. A., Olubode, O. S., Garshelis, D. L. 2009. Distribution and abundance of sacred monkeys in Igboland, southern Nigeria. American Journal of Primatology, 71: 574-586.
Booth, A. H. 1954. A note on the colobus monkeys of the Gold and Ivory Coasts. Ann. Mag. Nat. Hist., 12th series. 7: 857-860.
Gonedelé Bi S, Koné I, Bené JC, Bitty A, Akpatou B, Goné Bi Z, Outtara K, Koffi A. 2008. Tanoé forest (south-eastern Côte d'Ivoire), a community area identified as a high priority site for the conservation of critically endangered primates in West Africa. Tropical Conservation Science 3: 262-276.
Gonedelé Bi, S., Bitty A., Gnangbé, F., Bené, J. C., Koné, I., Sangaré, A., Zinner, D. 2010. Conservation status of geoffroy's pied colobus monkey (Colobus vellerosus, Geoffroy 1834) has dramatically declined in Côte d'Ivoire. African Primates 7: 19-26.
Gonedelé Bi, S., Zinner, D., Koné, I., Goné Bi, Z., Akpatou B., Koffi Bené J. C., Sangaré, A., Boesch, C. 2006. A West African black-and-white colobus monkey, Colobus polykomos dollmani Schwarz, 1927, facing extinction. Primate Conservation 21: 55-61.
Groves, C. P. 2001. Primate Taxonomy. Smithsonian Institution Press, Washington, DC.
Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. P., Struhsaker, T. T. 2003. Assessment of the diversity of African primates. International Journal of Primatology 24: 1301-1357.
Kingdon, J. 1997. The Kindon Field Guide of African Mammals. Academic Press, London. Oates, J. F. and T. F. Trocco. 1983. Taxonomy and phylogeny of black-and-white colobus monkeys: inferences from an analysis of loud call variation. Folia Primatol. 40: 83-113.
Napier, P. H. 1985. Catalogue of primates in the British Museum (Natural History) and elsewhere in the British Isles. Part III: Family Cercopithecidae, subfamily Colobinae. London: British Museum (Natural History). 58p.
National Research Council. 1981. Techniques for the study of primate population ecology. National Academy Press: Washington.
Oates J. F., Davies A. G. and Delson E. 1994. The diversity of living colobines. In Colobine monkeys: their ecology, behaviour and evolution (ed. A. G. Davies and J. F. Oates) pp. 45-73. Cambridge University Press, Cambridge, UK.
Oates J.F., Trocco T.F. 1983. Taxonomy and phylogeny of black-and-white colobus monkeys: inferences from an analysis of loud call variation. Folia Primatol.: 40, 83-113.
Oates, J. F. 1994. The natural history of African colobines. In: Colobine Monkeys: Their Ecology,Behaviour and Evolution, A. G. Davies and J. F. Oates (eds.), pp.75-128. Cambridge University Press, Cambridge.
Oates, J. F. 2011. Primates of West Africa. A Field Guide and Natural History. Arlington, Conservation International.
Oates, J. F., McGraw, W. S. 2009. A comment on the status of "Colobus polykomos dollmani" in Côte d'Ivoire. Primate Conservation. 24: 73-76.
Sutherland, W.J. 2002. Mammals. In Ecological Census Techniques (ed. W.J. Sutherland), pp. 260-278. Cambridge University Press, Cambridge, United Kingdom.