Study site

The Kikélé Sacred Forest (13 ha) is in the Bassila administrative region near the village of Kikélé in central Benin, West Africa (Fig. 1). This forest is occupied by a single, multi-male/multi-female group of Colobus vellerosus of 18 individuals that has been protected by traditional beliefs for decades (Djègo-Djossou et al. 2012). The Sacred Forest is extended by a gallery forest that surrounds the entire village and is fragmented by agricultural clearings and access roads.

The climate of Kikélé is of the Sudanian dry type, characterized by a dry season from mid-October to mid-April, alternating with a rainy season from mid-April to mid-October. Although the climate is dry, yearly rainfall (1300 mm) is higher compared to other regions in Benin (950–1200 mm). The vegetation of this Sacred Forest contains tall trees that are typical of semi-deciduous forests. There are several vegetation types: dense forest, woodland, and savanna. The most common species in this region are similar to those of the Boabeng-Fiema Monkey Sanctuary, Ghana. They include Cola gigantea (Sterculiaceae), Celtis zenkeri and C. toka (Ulmaceae), Antiaris toxicaria (Moraceae), Holoptelea grandis (Ulmaceae), Erylhrophleum suaveolens (Leguminosae - Caesalpinioideae), and Khaya grandifoliola (Meliaceae) (Adomou 2005). Besides C. vellerosus, the mammal fauna of the Kikélé Sacred Forest comprises a few individuals of Cercopithecus mona and various rodents, including the rare Beecroft's flying squirrel Anomalurus beecrofti.

Data collection: Activity budget and food resources

Data were collected using instantaneous scan sampling (Altmann 1974) during an annual cycle from February 2010 to January 2011. In optimal conditions, the scans were made every 30 minutes from 6:30 am to 6:30–7:00 pm when the monkeys would retire to a sleeping tree. Observations were made twice a month during three consecutive days with an interval of at least seven days between each observation period. During each scan, data were registered for five minutes on the first five adult or sub-adult monkeys seen clearly (Arroyo-Rodriguez et al. 2007). A total of 1,772 scans were made over 886 hours of observations. Activities recorded were grouped into five categories: social interactions, resting, moving, feeding and other (auto-grooming, vocalization, scratching, urination). When feeding, the plant species and parts eaten were recorded.

Data collection: Habitat characteristics

Vegetation structure was determined in two forest patches—Patch 1 in the Kikélé Sacred Forest and Patch 2 a connected gallery forest—through plot surveys following Braun-Blanquet (1932). Patch 2 was visited by the monkeys only occasionally. A total of 16 plots were set up at random in four locations over the home range of the C. vellerosus group: 10 square plots of 30 × 30 m in Patch 1 (six in the dense forest, two in the woodland, and two in the savanna); and six rectangular plots of 25 × 20 m in Patch 2 (gallery forest). Plants with a diameter at breast height (DBH) of 10 cm or more were identified in each plot (Chapman et al. 1992). The height and the location of each sleeping tree were also recorded.

Figure 1.

Map of the study site showing the location of the Kikélé Sacred Forest, Benin.

Data analysis: Activity budget, diet and foods resources

The time spent on each activity was estimated indirectly by calculating the percentage between the number of records of the activity and the total number of records. Data were computed using Statistica 10.0 and the significance level was set for analyses α = 0.05. The three-day observation period is the unit of analysis (N = 24). An analysis of variance was performed to compare the times spent in each activity in the dry season and the wet season. The proportions of the items consumed were estimated indirectly by calculating the percentage of feeding records for each item against the total number of feeding records records.

Data analysis: habitat structure and computation of ecological indexes

Three indices were computed to assess the habitats occupied by the colobus monkeys. The Shannon-Wiener Index of Diversity was used to estimate plant species diversity. Sorensen's Coefficient (S) was calculated to compare similarity between the two forest patches: S = 2C/A+B, where C is the number of species shared in both patches; A and B the number of species specific to each patch. If S ≤0.5 the communities compared are dissimilar; if S > 0.5, the communities compared are similar. The Evenness Index of Pielou was used to examine how evenly the species recorded are represented in each habitat.

We also calculated the patch attendance rate through the ratio between the number of days where the colobus used Patch 1 and/or Patch 2, and the total number of observation days. We calculated the average diameter and height of sleeping trees and all the trees in each plot.

Activity budgets

The time the C. vellerosus group spent resting was more than twice the time it spent feeding (56.6% vs. 26.3%), and more than four times the time allocated to moving (56.6% vs. 13.0%) (Fig. 2). Social interactions and other activities accounted for only 3.3% and 0.7% of the activity budget, respectively.

Activity budgets varied seasonally and monthly (Fig. 3). Seasonal fluctuations in feeding (df = 23, F = 5.02, p = 0.03) and moving (df = 23, F = 12.6, p = 0.01) were statistically significant, while those for resting, social interactions and other activities showed no difference (df = 23, F<4.28 and p >0.05 in each case). Regardless of the month, the time spent on resting was always more than 50% of the total activities.

Daily activity pattern

The monkeys were very active in the early morning; activities were dominated by moving and feeding. Activities could be broadly categorized into three periods: (i) in the morning, between 7:00 am and 10:00 am; (ii) in the afternoon, between 12:00 am and 2:00 pm, activities were dominated by resting and social interactions (grooming, physical contacts, playing, and scratching); whereas (iii) in the afternoon and early evening, between 3:30 pm and 5:30 pm, feeding, moving and social were the predominant activities. The large majority of social interactions were affiliative (94% were grooming and playing).

Habitat characteristics

Sixty species of 28 families were recorded in Patches 1 and 2. Most of the trees were of the families Moraceae (18% of the species) and Leguminosae (13%). Although the number of food plants was similar in the two patches, the monkey troop used the forest of Patch 1 every day and entered the gallery forest of Patch 2 on only 57% of the days. Sorensen's Index (0.33) showed a significant difference between the patches. The Evenness Index of Pielou had similar value for both patches (0.97) indicating an even distribution of recorded species (Table 1). The Shannon-Wiener Index of Diversity was also high in both patches, with its value being slightly higher in Patch 2 (H = 5.19) than in Patch 1 (H = 4.87) (Table 1).

Figure 2.

Activity budget of Colobus vellerosus in the Kikélé Sacred Forest, Benin.

Figure 3.

Seasonal variations in the activity budget of Colobus vellerosus in the Kikélé Sacred Forest, Benin.

Food plants and items consumed

The colobus monkeys ate 60 items; 59 plant parts (leaves 53.1%, fruits 33.3%, seeds 2.5%, stems 1.3%, bark 1.4%, buds 3.1%, flowers 2.45%, and petioles 2.8%) and one prey (ants). The plant parts came from 35 species belonging to 16 families (Table 2). The best represented families in the diet were the Leguminosae (29% of species) and Moraceae (23%). Leaves and fruits contributed more than 90% of the diet (Fig. 4).

Characteristics of sleeping trees

Over 72 nights, C. vellerosus used 13 trees of three species as sleeping sites in Patch 1. The species were Celtis integrifolia, Cola cordifolia, and Holoplelea grandis. The troop's favorite species was C. integrifolia; six trees (DBH = 90–125 cm) were used on 86% of the 72 nights. Five H. grandis (DBH = 100–135 cm) were used on 10%, and two C. cordifolia trees (DBH =110–120 cm) were used on 4%. The frequency of use of different trees in each species varied. Two Celtis integrifolia trees were used more than the other four individuals. The average diameter at breast height (DBH) and mean height of the 13 sleeping trees were 112.07 ± SD 14.23 cm and 22.53 ± SD 13.76 m, respectively, while the averages for all trees measured were 53.72 ± SD 38.26 cm for mean DBH, and 17.23 ± SD 9.81 m for mean height. Of note is that a sleeping tree could be used for several consecutive nights. One sleeping tree was used for two consecutive nights on twelve occasions, three consecutive nights on two occasions, and once for four consecutive nights.

Figure 4.

Annual diet of Colobus vellerosus in the Kikélé Sacred Forest, Benin.

Table 1.

Habitat characteristics in the Kikélé Sacred Forest, Benin.

Activity budget

Colobus vellerosus of the Kikélé Sacred Forest showed an activity pattern similar to that of most colobines, with time spent on resting much greater than that spent on feeding. Table 3 shows the activity budgets of several species of black-and-white colobus monkeys and that of C. vellerosus in the Kikélé Sacred Forest recorded in this study. With the exception of Colobus guereza in Ituri, Democratic Republic of Congo, and C. angolensis ruwenzorii in Nyungwe, Rwanda, with 44% and 32% of the time spent on resting, respectively, all studies show that black-and-white colobus monkeys spend more than 50% of the time resting. Long resting time among colobines has been explained in a number of ways. Some authors have linked it to the need to ferment leaves for their digestion or to the quality of the habitat (Marsh 1981; Oates 1988; Korsjtens et al. 2010). It has also been considered a strategy of behavioral thermoregulation for Colobus polykomos, as it may limit energy losses (Dasilva 1992, 1994).

Differences in group activity budgets may be explained by differences in group size as social activities are more frequent in larger troops (Teichroeb et al. 2003), as well as by other factors such as predation risk, the social structure of troops, seasonality, and the availability and distribution of food resources (Kinnaird and O'Brien 2000). The time that C. vellerosus spent resting in Kikélé Sacred Forest was lower than that recorded for the same species in Ghana. This could be explained by the small size of the Kikélé group and the relatively poor quality of the habitat (Wong and Sicotte 2007). Our results contrast with the theory that indicates that time spent resting increases when it is hotter (Chaves et al. 2011). We found no difference in time spent resting by colobus in dry and rainy seasons. This is probably a consequence of the degraded habitat; Kikélé Sacred Forest is a small fragmented forest.

Feeding

Fifty eight percent of the plant species occurring in the study area contribute to the diet of Colobus vellerosus. Our findings are congruent with previous works that suggest that the Leguminosae provides the main food sources for colobus monkeys (Davies et al. 1988). Consumption of Erythrophleum suaveolens leaves by C. vellerosus was also confirmed despite their toxicity (see Kay and Davies 1994).

Feeding generally ranks after resting in the activity budget of colobines, unlike other primates where feeding is the primary activity (for example, Cercopithecus ascanius: Cords 1987; Lagothrix lagothricha: Defler 1996). The diet of the C. vellerosus group was dominated by leaves, as has been reported elsewhere for this species. However, when compared to other sites, leaves are much less dominant (i.e., 53% vs. 74% in Ghana, Saj et al. 2005; Tan 2006; Wong et al. 2006). Foods such as fruits, seeds and ants also seem to be important components. This could result either from a locally higher diversity of food resources or a shortage in the preferred food (i.e., leaves); leading to exploration and inclusion of alternative foods in the diet.

Table 2.

Food plants consumed by Colobus vellerosus in the Kikélé Sacred Forest, Benin.

Sleeping sites and their characteristics

The monkeys of the Kikélé Sacred Forest chose the Patch 1 forest for their sleeping sites and never slept in Patch 2, the gallery forest. This may be an anti-predation strategy because gallery forest used to be exploited by people from the surrounding villages (i.e., Manigri, Bassila), and colobus monkeys were hunted there over many years. Although there is currently no hunting in the Kikélé Sacred Forest, this finding may support the hypothesis of predator avoidance in the selection of sleeping sites, as indicated in studies of other primates (for example, Saguinus mystax and S. fuscicollis: Heymann 1995; Macaca leonina: Albert et al. 2011) and for C. vellerosus by Teichroeb et al. (2012). Although there is no predation, in Patch 1 the colobus monkeys chose sleeping trees to rest. Predator avoidance behaviors could also be associated with hunting in the vicinity of the study area, as mentioned above. However, other factors such as reducing time and energy needed for foraging could also determine sleeping tree selection (Anderson 1998).

Table 3.

Comparison of the activity budget of the white-thighed colobus, Colobus vellerosus, at Kikélé with those of other Colobus species.

The physical characteristics of the sleeping sites also support the idea that C. vellerosus at Kikélé selects sleeping sites to avoid predators. The sleeping trees were generally the largest and tallest trees, undoubtedly reducing the chances of predators climbing them. Some large and tall trees, however, were not used as sleeping sites. This was the case for a Ficus sp., Albizia zygia, and Blighia sapida (Sapindaceae); the first two being food species for the colobus monkeys. Selection of sleeping trees is probably also linked to other physical characteristics of the trees. Celtis integrifolia was the species the monkeys slept in most. Compared to the other trees, Celtis integrifolia has very rigid stems and its branches are well spread, which allows for a better distribution of colobus monkeys through the crown and, it could well be more comfortable. However, the monkeys seemed to prefer certain individual trees of the same species despite their similar physical characteristics. This may be a question of habit, or may be linked to their position, which may, for example, allow for better views of their surroundings (Bovy 2010; Maslarov 2012).

Use of the same sleeping tree on consecutive nights may be due to the lack of predators. In high-risk environments, primates often avoid consecutive use of the same sleeping sites so as to reduce detection by predators (Li et al. 2006; Phoonjampa et al. 2010). The selection of sleeping trees appears to be a compromise between several factors—species, diameter and height, and location—and the preference of C. vellerosus for C. integrifolia in Kikélé may also be explained by the fact that it is also used for feeding and resting during the day, with monkeys spending up to eight hours a day on its branches.