Introduction
It is estimated that on average, 69% of the global wildlife population has been lost in just under 50 years (WWF Reference Almond, Grooten, Juffe Bignoli and Petersen2022), and 60% of all primate species are threatened with extinction as a result of human activities and behaviour (Estrada et al. Reference Estrada, Garber, Rylands, Roos, Fernandez-Duque, Di Fiore, Nekaris, Nijman, Heymann and Lambert2017). Numerous land-use practises lead to habitat degradation and the formation of forest fragments in the tropical forest regions of the world where primates live (Didham Reference Didham, Laurance and Bierregaard1997; Foley et al. Reference Foley, DeFries, Asner, Barford, Bonan, Carpenter, Chapin, Coe, Daily, Gibbs, Helkowski, Holloway, Howard, Kucharik, Monfreda, Patz, Prentice, Ramankutty and Snyder2005; Onderdonk & Chapman Reference Onderdonk and Chapman2000; WWF Reference Almond, Grooten, Juffe Bignoli and Petersen2022). Such anthropogenic activities affect plant species richness, and change the forest structure, diversity, and biomass (Arroyo-Rodríguez et al. Reference Arroyo-Rodríguez, Mandujano, Benítez-Malvido and Cuende-Fanton2007; Martin & Asibey Reference Martin and Asibey1979; Spracklen et al. Reference Spracklen, Kalamandeen, Galbraith, Gloor and Spracklen2015). As a result, primate food resources may be reduced, which has the potential to modify group size, group composition, and population size (Clarke et al. Reference Clarke, Crockett, Zucker and Zaldivar2002; Eppley et al. Reference Eppley, Verjans and Donati2011; Onderdonk & Chapman Reference Onderdonk and Chapman2000). When primate populations become completely isolated, especially in small fragments, they are likely to be threatened by localised extinctions (Benchimol & Peres Reference Benchimol and Peres2013; Lovejoy et al. Reference Lovejoy, Bierregaard, Rylands, Malcolm, Quintela, Harper, Brown, Powell, Powell, Schubart, Hays and Soulé1986).
The critically endangered white-thighed colobus (Colobus vellerosus) is resident only in Benin, Côte d’Ivoire, Togo, and Ghana (Matsuda et al. Reference Matsuda, Gonedelé Bi, Nobimè, Koné, Osei, Segniagbeto and Oates2020). In Boabeng-Fiema Monkey Sanctuary (BFMS), in Ghana, C. vellerosus population lives in fragmented habitats (Kankam Reference Kankam1997; Saj et al. Reference Saj, Teichroeb, Sicotte, Paterson and Wallis2005). Current evidence suggests that in addition to the Boabeng and Fiema communities, C. vellerosus also inhabits fragmented habitats within the forests of seven other communities (Kankam Reference Kankam1997; Kankam & Sicotte Reference Kankam and Sicotte2013).
The population of Colobus vellerosus at BFMS and the surrounding communities has increased over the years (Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010) from 128 individuals in 1990 (Fargey Reference Fargey1991) to 163 individuals in 1997 (Kankam Reference Kankam1997), excluding the small populations in the surrounding forest fragments. Furthermore, it increased from 200 individuals in 2005 (Saj et al. Reference Saj, Teichroeb, Sicotte, Paterson and Wallis2005) to 275 individuals in 2010 (Kankam & Sicotte Reference Kankam and Sicotte2013), making it possibly the only growing population of C. vellerosus in West Africa (Saj & Sicotte Reference Saj, Sicotte, Butynski, Kingdon, Happold and Kalina2013). However, there are fluctuations in the population trend in the surrounding communities (Kankam & Sicotte Reference Kankam and Sicotte2013). Monitoring the colobus population is critical to understanding the population dynamics of C. vellerosus at the BFMS and the surrounding forest fragments (Kankam & Sicotte Reference Kankam and Sicotte2013).
The population trend in the sanctuary and the surrounding communities has not been monitored for over a decade to determine its current status. Regular monitoring and provision of information on the population status are very important to assess the success of primate conservation programmes (Kankam Reference Kankam2010). Therefore, the objective of the research was to examine current population trends of Colobus vellerosus in the BFMS and surrounding forest fragments. Specifically, we undertook a complete count of the population of C. vellerosus in the BFMS and the surrounding fragments in 2020, and this data was compared with previously conducted counts from 1990 to 2014.
Study site
The study was carried out at BMFS and surrounded forest fragments (7o 43’ N, 1o 42’ W). It is a 1.9 km2 area within a 4.5 km2 sacred grove, situated around the twin villages of Boabeng and Fiema in the Nkoranza District in Ghana (Wong & Sicotte Reference Wong and Sicotte2007). The sanctuary is surrounded by communities that have pockets of forest owned by the communities (Kankam Reference Kankam1997; Kankam & Sicotte Reference Kankam and Sicotte2013; Wong & Sicotte Reference Wong and Sicotte2006). The area lies within the southern rainforest–dry northern grassland transition zone, with a mean annual temperature and rainfall of 26oC and 1,250 mm, respectively (Kankam & Sicotte Reference Kankam and Sicotte2013). The sanctuary is home to the endangered white-thighed colobus (Colobus vellerosus), which is endemic to the Upper Guinean Forest, and Lowe’s monkeys (Cercopithecus campbelli lowei) (Fargey Reference Fargey1991). The vegetation comprises a mosaic of original forest, degraded forest, woodland, and savannah (Kankam Reference Kankam2010).
Materials and methods
To determine the current population of C. vellerosus in BFMS and the surrounding fragments (n = 11), the complete count method (Jarman et al. Reference Jarman, Smith, Southwell, Wilson, Cole, Nicols, Rudran and Foster1996; Onderdonk & Chapman Reference Onderdonk and Chapman2000) was adopted for consistency and comparability with the methods previously used by other researchers at the site (Fargey Reference Fargey1992; Kankam Reference Kankam1997; Kankam & Sicotte Reference Kankam and Sicotte2013; Saj et al. Reference Saj, Teichroeb, Sicotte, Paterson and Wallis2005; Wong & Sicotte Reference Wong and Sicotte2006). It is perhaps the most accurate primate census technique to assess group size and population size (Plumptre & Cox Reference Plumptre and Cox2006), although it cannot be generalised (Ross & Reeve Reference Ross, Reeve, Setchell and Curtis2003). In the pre-census period, the colobus groups were identified and their general location was assessed by trained research assistants (n = 42) for two weeks. This exercise was very important to identify all groups and where they could possibly be found. To gain access to various parts of their ranges to locate the groups of C. vellerosus, several transects were cut, and existing trails, footpaths, and roads were also used (estimated total distance covered: 88.2 km). The length of transects was averaged at 0.05 km (range: 0.02–0.1 km). The population survey was conducted over three days in October 2020. On each census day, research assistants located a group assigned to them in the morning before the census began at 10:00 h. The censuses were carried out on the same day and at the same time (from 10:00 h to 15:00 h) to avoid counting moving individuals or groups that may be moving between fragments during the census period. Research assistants were rotated to get an independent count for each group and also minimise biases in the counts. For each census, a ‘good count’ was used. A ‘good’ count was characterised by the fact that the group either crossed an opened area during counting, which made the monkeys more visible and easier to count, or when they were in a tree with good visibility (Baker et al. Reference Baker, Tanimola, Olubode and Garshelis2009, Kankam & Sicotte Reference Kankam and Sicotte2013). The absence of groups in a fragment was also recorded. For each group encountered, we recorded the total number of individuals by sex and age-class. The age-class was classified into adults (this category included sub-adults), immature, and infants (Kankam & Sicotte Reference Kankam and Sicotte2013; Wong & Sicotte Reference Wong and Sicotte2006). Estimation of age-class was based on the relative size of the monkeys and our knowledge of each group’s history (Kankam Reference Kankam2010).
Data analyses
The population density (number of individuals/km2) was calculated by dividing the total number of monkeys in each forest fragment by the size of the fragment. A good count of the number of individuals in each fragment was used to estimate the colobus population density in each community (Kankam & Sicotte Reference Kankam and Sicotte2013; Wong & Sicotte Reference Wong and Sicotte2006). The population growth rate from one period to another (Table 2) was calculated from the formula PR = [(Vpresent –Vpast)/Vpast × 100]/N, where PR is the percentage growth rate, Vpresent is the present population, Vpast is the past population, and N is the number of years (Organization for Economic Cooperation and Development 1997).
The size of the fragments was obtained by traversing the defined pillared boundaries of some communities. Other communities have planted trees with fire resistant characteristics, such as teak (Tectona grandis), to demarcate the forest boundaries. For communities with no defined boundaries, the elders and chiefs elected some community members who had knowledge of the proposed boundaries of the areas to accompany the first author to take the Global Positioning System points. A map was generated from this data, which allowed documentation of the fragment sizes (Kankam Reference Kankam2010).
Results
Thirty-six white-thighed colobus monkey groups with a total of 581 individuals inhabited the BFMS and the surrounding forest fragments, for a population density of 148.6 ind/km2 and group density of 9.0 groups/km2 (Tables 1 and 2). In BFMS alone, the population was 451 individuals (density: 234.9 ind/km2) in 27 groups (density: 14.1 ind/km2). The colobus population of the surrounding forest fragments was composed of 130 individuals (density: 65.3 ind/ km2), divided into nine groups (density: 4.5 groups/km2) (Table 2). Overall, the total population growth rate of colobus monkeys at BFMS and the surrounding forest fragments was 353.9% in the 30 years between the 1990 and 2020 censuses (at a rate of 11.8% annually). In the BFMS alone, the total population growth rate was 252.3% between 1990 and 2020 (i.e., at a rate of 8.4% annually). The population growth rate from 1990 to 2000, 2000 to 2010, and 2010 to 2020 was 5.6%, 3.8%, and 6.4%, respectively, in the BFMS. The total population growth rate in the surrounding forest fragments was 97.0% in the 23 years between the first census years of 1997 and the 2020 census (i.e., at a rate of 4.2% annually). However, the population growth rate from 1997 to 2010 and 2010 to 2020 was 7.5% and 3.8%, respectively, in the surrounding forest fragments. The mean group size of colobus in BFMS was 16.7 individuals (SD = 4.0; range = 9–25), while that of the surrounding forest fragments was 14.4 individuals (SD = 4.6; range = 9–23). The overall mean group size was 16.1 individuals (SD = 4.3; range = 9–25) in BFMS and surrounding forest fragments (Table 1). There was an approximate ratio of one adult male to three adult females in both BFMS and in the surrounding fragments, as deduced from Table 1. However, the ratio of adult individuals (adult females and adult males) to immature individuals, including infants, was skewed towards immature individuals at BFMS (1:0.7) and the surrounding forest fragments (1:0.8). On average, there was a ratio of one adult female to one immature individual (1:1.2).
Table 1. C. vellerosus population characteristics and density in the BFMS and surrounding forest fragments in 2020
Table 2. C. vellerosus population trends in the BFMS and surrounding fragments between 1990 and 2020. The numbers of monkey groups are shown in brackets
Source: Fargey (Reference Fargey1991)a; Kankam (Reference Kankam1997)b; Saj et al. (Reference Saj, Teichroeb, Sicotte, Paterson and Wallis2005)c; Wong and Sicotte (Reference Wong and Sicotte2006)d; Kankam et al. (Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010)e; Sicotte and Kankam (Reference Sicotte and Kankamunpublished report)f; this survey*, (-) means census was conducted only in BFMS.
Discussion
We detected an impressive growth of colobus monkeys at BFMS and the surrounding fragments, about 354% in a 20-year period (1990–2020; at a rate of 11.8% annually). In the BFMS alone, the total population growth rate was 252.3% between 1990 and 2020 (i.e., at a rate of 8.4% annually).
The C. vellerosus density in BFMS was higher (density: 14.1 groups/km2) for a small fragment than that of Colobus guereza in Kakamega Forest in Kenya (estimate of 11.5 groups/km2), which was described as high for a rainforest site (Fashing & Cords Reference Fashing and Cords2000). Also, the smaller fragments of the surrounding communities support a relatively higher population density (Irwin Reference Irwin2008). The average ratio of one adult female to one immature (1:1.2) is an indication that the population in the fragments is growing with births (Emmel Reference Emmel1976; Kankam Reference Kankam2010).
The colobus population in BFMS continues to increase, as seen in successful stories of primate conservation in fragments (e.g., the golden lion tamarin Leontopithecus rosalia in Brazil: Kierulff et al. Reference Kierulff, Ruiz-Miranda, Oliveira, Beck, Martins, Dietz, Rambaldi and Baker2012; the howler monkey populations in Mexico: Estrada et al. Reference Estrada, Mendoza, Castellanos, Pacheco, Belle, Garcia and Munoz2002; and the black-and-white colobus Colobus guereza in Kibale National Park: Chapman et al. Reference Chapman, Bortolamiol, Matsuda, Omeja, Paim, Reyna-Hurtado, Sengupta and Valenta2018). Conversely, the population of the black-and-white colobus Colobus guereza and the red colobus Procolobus pennantii decreased in Western Uganda due to habitat loss and forest degradation in small and unprotected forest fragments (Chapman et al. Reference Chapman, Naughton-Treves, Lawes, Wasserman and Gillespie2007). The construction of large infrastructures affected the population of the black howler monkey Alouatta pigra in Mexico (Pozo-Montuy & Bonilla-Sánchez Reference Pozo-Montuy and Bonilla-Sánchez2022). Moreover, primate habitat fragmentation also decreased the population of the black-fronted titi monkey Callicebus nigrifrons in Brazil (Berthet et al. Reference Berthet, Mesbahi, Duvot, Zuberbühler, Cäsar and Bicca-Marques2021); and in India, of the western hoolock gibbon Hoolock hoolock: ICIMOD 2021; Sharma et al. Reference Sharma, Madhusudan and Sinha2014).
We do not completely understand the causes of this population increase in BFMS; however, it suggests some degree of success for the community-based primate conservation programme (Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010). Although we did not specifically investigate the cause of the increase in population over the past thirty years, it is likely that, first, the success of protecting the monkeys using traditional systems or cultural beliefs infused with the biological conservation management goal of the Wildlife Division of Ghana to assist communities in managing natural resources is a contributing factor (Saj et al. Reference Saj, Mather and Sicotte2006). At BFMS, the monkeys are revered by the communities as the ‘children of the gods’ and protected as such (Fargey Reference Fargey1992). Second, improved stakeholder inclusion through the formation of a monkey sanctuary management committee comprised of representatives from Boabeng-Fiema and the surrounding communities with fragments occupied by colobus monkeys could be another factor. This committee includes a wildlife officer-in-charge of the sanctuary who is tasked with assisting in educating the communities about primate conservation, protecting biodiversity, and enhancing the site’s tourism potential. The participating communities get financial support from monies accrued from the eco-tourism project (Kankam Reference Kankam2010). Third, the monkey’s ability to cope well in smaller fragments (at least for the time being) may be due to their ability to broaden their diet to include low-quality plants when limited food resources are available (Kankam & Sicotte Reference Kankam and Sicotte2013; Marsh et al. Reference Marsh, John, Ayres, Marsh and Mittermeier1987; Saj & Sicotte Reference Saj and Sicotte2007; Saj et al. Reference Saj, Teichroeb, Sicotte, Paterson and Wallis2005; Tutin Reference Tutin1999), as seen in other colobus species (Colobus polykomos: Davies et al. Reference Davies, Oates and Dasilva1999, Colobus guereza: Fashing Reference Fashing2001, Procolobus badius, Procolobus verus, and Colobus satanas: McKey et al. Reference McKey, Gartlan, Waterman and Choo1981). For example, in 2007, the colobus monkeys at the BFMS were found eating the leaves and green pods of an exotic and invasive species (Leucaena leucocephala) for which we have no records at the site as colobus food trees (Bright O. Kankam, pers. obs.). A similar behaviour is reported for black howler monkeys (Alouatta caraya) and brown howler monkeys (Alouatta guariba clamitans) in Rio Grande do Sul State, southern Brazil (Bicca-Marques & Calegaro-Marques Reference Bicca-Marques and Calegaro-Marques1994; Chaves & Bicca-Marques Reference Chaves and Bicca-Marques2016). We argue that the conservation of the monkeys at the site should include planting food trees for the monkeys to increase the fragment size and food resources of the monkeys (Anderson et al. Reference Anderson, Cowlishaw and Rowcliffe2007; Chapman et al. Reference Chapman, Bicca-Marques, Dunham, Fan, Fashing, Gogarten, Guo, Huffman, Kalbitzer, Li, Ma, Matsuda, Omeja, Sarkar, Sengupta, Serio-Silva, Tsuji and Stenseth2020).
The existing threats in the area run counter the success of increasing populations of the monkeys, thus questioning the long-term conservation of the monkeys in the fragments at the BFMS (Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010). Habitat disturbance (e.g., bushfire, farming activities, cutting of fuelwood, burning of charcoal in the fragments, and settlement expansion) has occurred and still occurs in the small fragments and the patches in between the fragments (Amankwah et al. Reference Amankwah, Quaye-Ballard, Koomson, Amankwah, Awotwi, Kankam, Opuni-Frimpong, Baah and Adu-Bredu2021; Kankam Reference Kankam2010; Yeboah Reference Yeboah2020). The colobus habitat is consistently becoming smaller due to the high level of anthropogenic disturbance (Amankwah et al. Reference Amankwah, Quaye-Ballard, Koomson, Amankwah, Awotwi, Kankam, Opuni-Frimpong, Baah and Adu-Bredu2021; Kankam & Sicotte Reference Kankam and Sicotte2013; Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010). For example, some large trees in the Busunya community have been removed to pave way for infrastructure expansion because it has been elevated to the district capital status of the Nkoranza South Municipal (Robert Koranteng, pers. comm.). Also, part of the core forest of BFMS was gutted by fire, which led to the death of 49 C. vellerosus in early 2020 (Samuel Amponsah, pers. comm.). The long-term persistence of the colobus species is at risk because of the shrinkage of forest fragments (Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010; Yeboah Reference Yeboah2020). Given that active farming activities and the burning of charcoal are still going on in the agricultural lands in-between fragments, the long-term conservation of C. vellerosus at BFMS is at risk because the removal of trees will reduce the food resources (Medley Reference Medley1993), destroy the forest structure (Chapman & Chapman Reference Chapman and Chapman1999), and reduce the possibility of arboreal movements for colobus in small fragmented landscapes (McGraw et al. Reference McGraw, Zuberbühler and Noë2007; Medley Reference Medley1993). Revenue sharing from the conservation effort is also motivating the stakeholders to protect the monkeys and the forest fragments (Samuel Amponsah, pers. comm.). We believe that the lack of collaborative effort from stakeholders (e.g., the chiefs and leaders of all communities and the Ghana Wildlife Division), as a result of any non-transparent revenue-sharing and accountability plan (Kankam et al. Reference Kankam, Saj, Sicotte, Puplampu and Tettey2010), would become one of the future potential threats to the protection and better management of the ecotourism programme at BFMS.
We suggest that C. vellerosus populations have the potential to increase further in small, suitable fragments if habitat destruction and settlement expansion are managed with primate conservation intentions.
Acknowledgements
We thank the chiefs and elders of all the fragments and the Wildlife Division officer-in-charge of BFMS (Samuel Amponsah) for granting permission to conduct this research at BFMS. Thanks to all the research assistants, especially Robert Koranteng and Charles Kodom, for training research assistants and helping in the censusing of the monkeys.
Financial support
This research received no specific grant from any funding agency or not-for-profit sector.
Competing interests
The authors declare none.
