Environmental and anthropogenic effects on the nesting patterns of Nigeria–Cameroon chimpanzees in North‐West Cameroon

Environmental conditions and human activity influence the selection of nest sites by chimpanzees and may have serious conservation implications. We examined the characteristics of nesting trees preferred by chimpanzees, investigated the effect of vegetation composition and topography on nest site locations and seasonality on nesting heights of chimpanzees, and verified the effect of predator occurrence and human activity on the nesting behavior of the Nigeria–Cameroon chimpanzee (Pan troglodytes ellioti) in Kom‐Wum Forest Reserve (KWFR) and surrounding unprotected forest in Cameroon. We recorded 923 nests, 502 signs of human activity, and 646 nesting trees along line transects and recces (reconnaissance) for two seasons. We found that chimpanzees constructed more arboreal nests on tall primary trees with high lowest branch height and large diameter at breast height. Moreover, they oriented their nests within trees in the slope direction when the nesting trees were located on slopes. Additionally, the occurrence of chimpanzee nests was positively related to increasing elevation and slope and decreased with distance to primary forest. In contrast, the number of nests increased with distance to secondary forest, open land, and villages, and nesting height was not influenced by seasons. While we recorded no signs of large nocturnal chimpanzee predators at nesting trees, we found signs of hunting activity at nesting locations. Nesting high in trees is likely a way of avoiding hunting, while nest orientation within trees in slope direction shortens escape routes from human hunters. Our findings suggest that chimpanzees select safe trees (tall trees with high lowest branch height) located in nesting areas (primary forest, high elevation, and steep slopes) that are not easily accessible by humans. Therefore, conservation efforts should focus on protecting primary forests at high elevation and steep slopes and reducing human impact.

by seasons. While we recorded no signs of large nocturnal chimpanzee predators at nesting trees, we found signs of hunting activity at nesting locations. Nesting high in trees is likely a way of avoiding hunting, while nest orientation within trees in slope direction shortens escape routes from human hunters. Our findings suggest that chimpanzees select safe trees (tall trees with high lowest branch height) located in nesting areas (primary forest, high elevation, and steep slopes) that are not easily accessible by humans. Therefore, conservation efforts should focus on protecting primary forests at high elevation and steep slopes and reducing human impact.
K E Y W O R D S ecological factors, human activity, nesting behavior, Nigeria-Cameroon chimpanzee, predation 1 | INTRODUCTION All weaned non-human great apes construct sleeping or resting platforms (hereafter "nests") by modifying branches and leaves of trees (Goodall, 1962;Tutin & Fernandez, 1984). This behavior is common for chimpanzees, bonobos, orangutans (Fruth & Hohmann, 1996), and gorillas (Iwata & Ando, 2007). Like other great apes, chimpanzees build a new nest every night or may re-use old nests after adding new material to reinforce them (Hernandez-Aguilar, 2006, 2009. Generally, their nests can be arboreal (Poulsen & Clark, 2004) or can be built on the ground (Abwe & Morgan, 2008;Furuichi & Hashimoto, 2000;. They can further be categorized as night or day nests (Brownlow et al., 2001;Koops et al., 2012). Usually, night nests are arboreal and more elaborate constructions (Fruth & Hohmann, 1996;Reynolds, 2005), while day nests tend to be terrestrial and the structure is less sophisticated (Brownlow et al., 2001;Koops et al., 2012). Day nests on the ground are constructed with leaves or consist of ferns which are used for resting during the day, whereas night nests on the ground consist of bent and broken branches (Furuichi & Hashimoto, 2000). Unlike day nests on the ground are mostly found without trees in their neighborhood, night nests on the ground usually occur in groups and are linked with arboreal nests in their surroundings (Koops et al., 2007).
Furthermore, day nests on the ground are used to protect chimpanzees from the cold soil surface (Boesch, 1995).
The selection of individual nesting trees by chimpanzees has been attributed to the morphological characteristics of trees, including the tree diameter, tree height, and lowest branch height (Hakizimana et al., 2015;Hernandez-Aguilar et al., 2013) as well as the species type (Brownlow et al., 2001;Sanz et al., 2007;Stanford & O'Malley, 2008). In addition to the selection of individual trees, chimpanzees also select nesting areas within forests, including a preference for primary forest cover (Bryson-Morrison et al., 2017;Koops et al., 2012), high elevation (Barca et al., 2018;Koops et al., 2012), steep slopes (Abwe, 2018;Dutton et al., 2016;Kamgang et al., 2018), and closed canopy (Abwe, 2018). Besides habitat and topographic factors, seasonality may affect nest construction in great apes. For example, Takemoto (2004) noted that chimpanzees tend to show arboreal behavior in the wet season to minimize the effect of heat loss and spend more time on the ground during the dry season due to an increase in surrounding temperatures. Similarly, Koops et al. (2012) demonstrated that nesting at elevated heights in the wet season is a strategy to avoid constructing nests in humid conditions closer to the ground.
Non-human primates select nesting sites in trees to reduce access or detection by predators (Anderson, 1984). For instance, Stewart and Pruetz (2013) showed that chimpanzees nest at high and peripheral nesting positions within trees in areas with potential terrestrial predators such as leopard (Panthera pardus) and lion (Panthera leo). Furthermore, human activity may also affect the selection of nesting locations by chimpanzees (Heinicke et al., 2019;. Particularly, the construction of night nests on the ground by chimpanzees is more frequently observed in areas with limited human activity (Hicks et al., 2010;Last & Muh, 2013).
Agricultural activity, illegal timber exploitation, uncontrolled burning, and illegal hunting are major anthropogenic threats to the Nigeria-Cameroon chimpanzee (Morgan et al., 2011). This chimpanzee subspecies has about 3500 individuals remaining in the wild, is the most threatened subspecies, and relatively unstudied. Since the recognition of the Nigeria-Cameroon chimpanzee subspecies in 1997 (Gonder et al., 1997), several studies have been conducted to improve our understanding of their nesting behavior at several sites, including the selection of nest trees and areas in relation to ecological conditions and human activity in Ngel Nyaki Forest Reserve (Dutton et al., 2016) and Gashaka-Gumti National Park (Fowler, 2006) in Nigeria. In Cameroon, recent studies focused on the selection of nest locations in relation to the availability of fruits in Ebo Forest Reserve (Abwe, 2018), the effects of preference for a particular habitat type and topography in Mbam-Djerem National Park (Kamgang et al., 2018), and in Ebo Forest Reserve (Abwe, 2018), the effect of human activity on arboreal and ground nest location in Lebialem-Mone Forest (Last & Muh, 2013), Tolafa Hill Wildlife Sanctuary (Njukang et al., 2019), Mone-Oku Forest (Wade, 2020), and Babanki-Finge Forest (Doumbé, 2014). However, information on nesting behavior of the Nigeria-Cameroon chimpanzee is still missing from priority conservation areas as outlined in the IUCN-endorsed regional conservation action plan (Morgan et al., 2011). The Kom-Wum Forest Reserve (KWFR) is considered a high priority conservation area for the Nigeria-Cameroon chimpanzee, and recommendations were made to conduct surveys on their abundance, behavior, and distribution (Morgan et al., 2011). Initial chimpanzee surveys in KWFR focused on confirming the presence of chimpanzees (Doumbé, 2015), estimating the population size (Chuo et al., 2017;Fotang et al., 2021), and indicating habitat preferences . Doumbé (2015) and Chuo et al. (2017) further suggested that chimpanzee predators are absent from KWFR, potentially resulting in specific nesting behavior. However, previous studies provided very little information about potential drivers of nesting behavior in this high-priority conservation area.
To improve our understanding of factors affecting nest building in chimpanzees in general, and to add to previous knowledge of nesting ecology of the Nigeria-Cameroon chimpanzee in particular, our study aims to analyze: (a) which traits of tree species are preferred for nesting (nesting tree selection); (b) the effects of environmental factors (vegetation, topography, seasonality) on nesting behavior (nesting area selection); and (c) if predator presence and human activity affect the selection of nest sites and nest distribution in trees (disturbance) in KWFR. We hypothesize that the selection of nesting trees by chimpanzees is driven by specific tree traits and that the selection of nesting areas further depends on the local vegetation composition, topography, and seasons (Koops et al., 2012). We predict that chimpanzees (i) construct more nests on tall primary trees (trees that provide the main support for nests), trees with larger diameter and high lowest branch height; (ii) orientate their nests in the direction of the decreasing slope, (iii) frequently nest in primary forests, at higher elevations, on steep slopes, and that (iv) nest higher in the wet season than the dry season. We further hypothesize that chimpanzees nest higher in trees if predators are present or when humans are active in the nesting location. We recommend conservation actions required to ensure the long-term survival of chimpanzees in the reserve. Nigeria (Kah, 2015). This reserve is home to seven diurnal and six nocturnal primate species (Chuo et al., 2017;Doumbé, 2015;Fotang, 2018). Among primates, chimpanzee population size estimates range from 10 (direct observation) to 83 individuals (distance sampling) based on the method used . In addition to primates, there are important timber species in the reserve, including forest products and hunting are the major threats to forest resources in KWFR Kah, 2015).

| Study area
F I G U R E 1 Maps of (a) Cameroon and the study location Kom-Wum Forest Reserve (KWFR) in North-West Cameroon (redpoint), (b) map of KWFR including major villages with transects for surveys (1-23) and location of camera traps

| Ethics statement
We conducted this study respecting the principles for research on non-human primates outlined in the American Society of Primatologists manual for primates' ethical handling. We obtained authorization from the Ministry of Scientific Research and Innovation in Cameroon and respected the protocols of the 1994 forestry and wildlife law governing research on chimpanzees.

| Chimpanzee nest surveys and description of nesting trees
We generated a 2 × 2 km grid across the study area (100 km 2 ) to place line transects (each 2 km in length) equally spaced (1000 m) following a systematic design (Buckland et al., 2001). Additionally, we considered the reconnaissance (recce) method to identify hotspots of chimpanzee activity since they are unhabituated (Kühl et al., 2008).  et al. (1981). We also marked nesting tree locations using a GARMIN GPSMAP 64 s device and recorded the nest height, tree height, and lowest branch height using a hypsometer (Nikon Forestry Pro 6x216x21\11-55YD). Furthermore, we noted the number of nests per tree and the number of trees per nest (integrated nest), and measured the diameter at breast height (DBH) and the horizontal distance of the nest from the tree trunk using a 30-m tape. For each nest, we recorded the nest type following Furuichi and Hashimoto (2000). Additionally, we defined the nest age classes per tree as fresh-when all leaves in the nest were green; recent-drying leaves of distinct colors; old-nest structure is unbroken with most of the leaves being brown; and very old-nest with holes displaying little or no leaves, but still be distinguished by bent twigs following Tutin and Fernandez (1984). Simultaneously, we calculated the vertical position of a nest within the crown following Hernandez-Aguilar et al. (2013).
We recorded the slope direction for nests and the nest orientation within a tree using a Gearmax® Professional military clinometer following Hernandez-Aguilar et al. (2013). For nesting trees located on slopes, we classified nests as oriented to the east (>22.5°and and south (between >167.5°and ≤202.5°). Nesting trees in the field were identified by a PhD botanist student (Nkemnkeng Francoline, Jong) from the University of Dscang, Cameroon. Samples and pictures of unidentified plants were taken to the Cameroon National Herbarium for identification by experts. We conducted a Bivariate Spearman's rank correlation analyses to test the relationship between tree height and nest height, DBH, and lowest branch height. The χ 2 tests were used to analyze whether chimpanzee nest orientation depended on slope direction and the Wilcoxon rank-sum tests to compare mean nest heights between wet and dry seasons.

| Environmental determinants of nesting sites
We described vegetation at nesting sites following White and Edwards (2000): primary forests-mixed forest with many large trees, unbroken canopy, and scanty vegetation cover on the ground, and mixed forest with dense vegetation cover on the ground dominated by lianas and Marantaceae; old secondary forest included-sections of forest with large trees, but showing indicators of previous disturbance by humans, with no grown crops, but occasionally with old palm or mango trees still present; and grassland-grazing land depicted by short-grass mixed with arable fields and cattle paths. Following Koops et al. (2012), we classified canopy cover as: no cover (0%)-nests with no branches with leaves over a nest; little cover-when 1%-25% of nests were covered by branches with leaves; light cover-when 26%-50% of nests were covered; moderate cover-when 51%-75% of nests were covered; and complete coverwhen 76%-100% of nests were covered. The slope for each nest was In addition to field surveys, we acquired land cover from remote sensing data (Landsat 8, 30 m pixel, on September 02, 2017). The imagery was classified into primary forest, secondary forest, bare lands, and water bodies using supervised image classification and the maximum likelihood algorithm (Ganasri & Dwarakish, 2015).
We obtained the elevation from a Shuttle Radar Topography Mission 30 m resolution Digital Elevation Model (Jarvis, 2008).
To assess whether nests are distributed randomly regarding the environmental variables or not, we created 2000 random points for each variable; that is, 2000 points for elevation, slope, primary forest, secondary forest, bare land, villages, aspects, rivers, and signs of human activities (Figure 2). We used the whole KWFR Reserve and surrounding forest with chimpanzee nests to define the limits of the random points. We then created layers representing distances to the random points generated to each environmental variable by calculating Euclidean distances and extracted these distances to nest locations following Enoguanbhor et al. (2020).
We first checked collinearity among environmental variables by calculating the variance inflation factor (VIF) using the package usdm (Naimi et al., 2014). We excluded all environmental variables with a VIF >5 (Table 1). We then performed a Pearson correlation test to calculate the collinearity among pairs of environmental variables. For each pair of significantly correlated environmental variables (slope vs. aspect and elevation vs. rivers), we eliminated one of the environmental variables (i.e., aspect and rivers). Our final model considered seven environmental variables, including elevation, slope, distance to primary forest, distance to secondary forest, distance to bare land, distance to villages, and distance to signs of human activities (Table 1). We used the package car (John Fox; Sanford Weisberg, 2019) and a linear model function to perform a multiple regression analysis of the relationship between the dependent variable (chimpanzee nest locations) and independent variable, including ecological (distance to primary forest, distance to secondary forest, elevation, slope, aspect, distance to rivers) and human factors (distance to villages, distance to bare land, distance to signs of human activity). All spatial analyses were conducted in ArcGIS 10.6.1 (ESRI, 2018) and hypothesis testing in R (R core team, 2016) version 3.5.1 (Venables et al., 2009).

| Antipredator/human avoidance
To investigate the effect of predator or human activity on the nesting behavior, we searched for signs of chimpanzee predators or human activity along transects and recces. We further attached ten camera traps to trees at a height between 30 and 80 cm along frequently used chimpanzee routes leading to nesting sites to increase the probability of detecting chimpanzee predators .
We recorded human signs (farms, spent cartridges, snares, nontimber forest product collection, timber extraction, grazing activities) within a 50 m radius of each nesting site following White and Edwards (2000).  We calculated the Kilometric Count Index for human signs (encounter rates of human signs) as the total number of human signs encountered (N) during the survey divided by the total length of the transect (L) in km (Mathot & Doucet, 2005).

| Physical characteristics of nesting trees
We found arboreal, ground, and liana nests in descending order during our survey (Table 2). Most nests were recorded in the wet season. Consequently, more trees were used for nesting in the wet season (Table 2) There was a significant relationship between nest orientation within the tree and slope direction (χ 2 test = 40.675, p < 0.010). Most nests located on the west slope were oriented in western direction (χ 2 test = 79.752, p < 0.001). Of the 72 ground nests recorded, 57 were night nests and 15-day nests. All ground nests were located on precipitous slopes (>26.6°) and were found under high canopy cover (75%-100%). A majority of the ground nests were further supported either by a tree trunk, tree roots, fallen wood, a stone, or liana from different plants.

| The environmental determinants of the selection of nesting locations
The multiple linear regression model indicates that the locations of chimpanzee nests decreased with distance to primary forest and increases with slope and elevation (Table 1; df = 1992, R² = 0.69, F = 628.8, p < 0.001; Figure 2b,f,c). In contrast, the number of T A B L E 2 Number of nests and trees recorded per season (wet and dry), in total and percentage of each nest category

| Physical characteristics of nesting trees
Our results support previous work showing that tree height is the most preferred tree trait by chimpanzee for nesting than the lowest branch height and tree diameter (Hernandez-Aguilar & Reitan, 2020).
Most tall trees had a high lowest branch height and large diameters confirming that nesting tree selection primarily depends on tree height. These results further support previous work that chimpanzees prefer tall trees with high lowest branch height for nesting (Hakizimana et al., 2015;Hernandez-Aguilar et al., 2013). At Mon-Oku Forest in Cameroon, tall and large trees were also selected trees to build multiple nests (Wade, 2020). Fowler (2006) reported that nesting trees' mean height and diameter were higher than those of surrounding non-nesting trees at Gashaka-Gumti-National Park in Nigeria. Our results also support previous work that chimpanzees prefer some tree species for nesting over others (Brownlow et al., 2001;Furuichi & Hashimoto, 2004;Hakizimana et al., 2015;Sanz et al., 2007;Stanford & O'Malley, 2008). Overall, four species Babanki-Finge (Doumbé, 2014), Mone-Oku Forest Reserve (Wade, 2020), and Ngel Nyaki Forest Reserve (Dutton et al., 2016). At Albert Lake escarpment, in the Democratic Republic of the Congo, M. myristica, followed by Strombosia sp. were the most used tree species for nesting by chimpanzees (Laudisoit et al., 2021). Although two of the most important nesting trees P. macrocarpa and M. myristica, are also important fruit species in the chimpanzees' diet in KWFR (Fotang, 2018), further studies on tree phenology are required to fully understand if the observed preferences for nesting by chimpanzees is based on fruit availability. Our results suggest that preferences for some tree species are related to physical tree characteristics.
The average nest height of chimpanzees at most previous study sites was between 10 and 20 m, and the average nest height of chimpanzees in KWFR was at the upper end of this range (Table 4).
The higher arboreal nesting height of the Nigeria-Cameroon chimpanzees in KWFR and some sites across its distribution range (e.g.,

Mone-Oku [Cameroon], Lebialem-Mone [Cameroon], and Ngel Nyaki
[Nigeria]) can be explained by the more common human disturbance FOTANG ET AL.  (Doumbé, 2014). The observed orientation of nests towards the slope direction could reduce the escape route through neighboring trees or increase the functional nest height and thereby minimize contact with predators (Goodall, 1968;Koops et al., 2012). Hernandez-Aguilar et al.
(2013) reported that chimpanzees orientate nests in the slope direction to maximize exposure to sunlight during sunrise for nests orientated eastwards and during sunset for nests oriented westwards.

| Environmental determinants of the selection of nesting locations
Our results suggest that distance to primary forest, distance to secondary forest, and human activities are the most important determinants for selecting nesting sites by the chimpanzees. Additional local nest site conditions like elevation and slope are important too (Table 1). Most primary forest patches remaining in the study area are found at a higher elevation and on steep slopes that are rarely used by humans and harbor tall and mature trees that are important for nesting. Our results support previous findings that primary forest vegetation and high elevation areas are preferred for nesting over secondary forest and lowland areas (Carvalho et al., 2021;Granier et al., 2014;Koops et al., 2012;Njukang et al., 2019). The positive association between primary forest and nest locations reported in this and previous studies may also be due to the presence of a high density of large  Hunt and McGrew (2002) fleshy fruits trees (Balcomb et al., 2000;Chitayat et al., 2021;Potts et al., 2011), and low impact of human activities (Strindberg et al., 2018). Although secondary forests may provide important food resources for chimpanzees (Basabose, 2005), our results strongly suggest that chimpanzees rarely nest in this vegetation type because of poaching and harvesting of timber and non-timber plant products . Chimpanzees avoided low elevations areas in this study because these habitats are made up of rich soils suitable for farming, especially along the banks of three rivers that flow through the reserve (Chuo et al., 2017;Fotang et al., 2021;Kah, 2015). While riparian forest provides suitable nesting habitat for chimpanzee in the Greater Mahale Ecosystem in Tanzania (Chitayat et al., 2021;Dickson et al., 2020), this forest type is not suitable for chimpanzees nesting in

| Antipredator/human avoidance hypothesis
Although the selection of tall trees for nesting by chimpanzees is related to the presence of chimpanzee predators such as leopard at some study sites (Hernandez-Aguilar et al., 2013;Pruetz et al., 2008;Stewart & Pruetz, 2013), the preference for tall trees for nesting in KWFR may be also related to human activities such as poaching and harvesting of timber and non-timber forest products . In fact, chimpanzee predators such as leopard were not found in KWFR in the current and past surveys (Chuo et al., 2017;Doumbé, 2015

| Conclusion and conservation implications
We show that chimpanzees prefer locating nests in primary forest vegetation, at higher elevations with slopes and away from villages and bare land exposed to cattle grazing and farming activities. They further selected tall trees with a high lowest branch height and large DBH for nest construction and orientated their nests in the slope direction for security reasons. We recorded no large nocturnal predators, but observed signs of human activity within nesting locations and evidence of chimpanzee hunting. Chimpanzees may escape human activities by nesting high in trees and constructing ground nests exclusively on steeper slopes. Our results suggest that primary forests at higher elevations and steep slopes are crucial for the conservation of chimpanzees as they are preferred habitats for nesting.
We recommend protecting such habitats because they contain preferred nesting trees and a topography that is anyway not ideal for human use (e.g., as agricultural production areas). We also recommend regular law enforcement patrols to curb poaching and the implementation of sustainable land-use practices to prevent forest conversion into agricultural fields in the reserve. We propose that chimpanzee nesting locations in the surrounding forests should be included in the reserve's management plan.

CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are not publicly available to protect the species in the study area. However, these can be made available on reasonable request from the corresponding author.