Skip to content

Advertisement

  • Research article
  • Open Access

The relationship between the abundance of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) and its habitat: a conservation concern in Mbam-Djerem National Park, Cameroon

  • 1, 6, 9Email authorView ORCID ID profile,
  • 2,
  • 3, 4,
  • 5,
  • 6,
  • 7,
  • 8,
  • 8 and
  • 9
BMC Ecology201818:40

https://doi.org/10.1186/s12898-018-0199-3

  • Received: 10 May 2018
  • Accepted: 26 September 2018
  • Published:

Abstract

Background

Understanding the relationship between great apes and their habitat is essential for the development of successful conservation strategies. The chimpanzee Pan troglodytes ellioti is endemic to Nigeria and Cameroon, and occupies an ecologically diverse range of habitats from forests to forest-savannah mosaic in Mbam-Djerem National Park (MDNP) in Cameroon. The habitat variation in chimpanzees is poorly understood in MDNP which provides an excellent opportunity to assess ecological factors that shape the abundance and distribution patterns of P. t. ellioti over a small geographic scale.

Results

We counted 249 nests along 132 km of transects in total. Of these, 119 nests along 68 km occurred in dense forest and 130 nests along 64 km in forest-savannah mosaic. Chimpanzee density was 0.88 [95% CI (0.55–1.41)] individuals/km2 in the dense forest and 0.59 [95% CI (0.19–1.76)] in the forest-savannah mosaic. Nest abundance varied with vegetation type and was higher in areas with dense canopy cover, steeper slopes and relatively higher altitudes.

Conclusions

Our estimates of chimpanzee densities were lower than reported in other studied populations in the range of the Nigeria-Cameroon chimpanzee. However, we found that habitat features, slope and altitude likely play a role in shaping patterns of chimpanzee nesting ecology. Further studies need to be focused on nest decay rates and phenology of useful plants in order to model chimpanzee abundance and distribution in Mbam-Djerem National Park.

Keywords

  • Great apes
  • Mbam-Djerem National Park
  • Pan troglodytes ellioti
  • Habitat variation
  • Nest abundance
  • Distance sampling

Background

Great ape populations are currently threatened by hunting, habitat loss and infectious diseases [1, 2]. Understanding the relationship between each great ape species and its environment is therefore crucial for developing conservation policy [3]. For chimpanzees, key requirements such as food and nesting materials are sensitive to environmental variation, including climate change and other anthropogenic factors such as habitat conversion and poaching. However, monitoring chimpanzee population size is inherently difficult, and few studies have demonstrated clear links between habitat variation and conservation value [4, 5]. The Mbam-Djerem National Park (MDNP) in Cameroon offers an excellent opportunity to assess ecological factors shaping the abundance and distribution of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) over a small geographic extent in the core zone of the protected area, which includes both dense forest, colonizing forest and savannah ecosystems. Until now, the distribution pattern and abundance of the Nigeria-Cameroon chimpanzee has not been completely understood in MDNP which may hamper their long-term conservation. Our research highlights this issue by providing data on chimpanzee density and the environmental drivers affecting their distribution. Moreover, as the forest is currently expanding [6] and replacing savannah in MDNP [7], understanding how chimpanzees use different habitats can inform conservation efforts by providing key monitoring parameters on behalf of this species.

Studies of the subspecies P. t. ellioti in the dry and gallery forests of Nigeria in Gashaka-Gumti National Park [8], in Cameroon at Ebo Forest [9] and MDNP have so far failed to address the relationship between abundance and habitat characteristics. Differences between chimpanzee populations regarding ecology, social organisation and genetics [10, 11], population size [12], home range size [13], feeding habits [14, 15] and nesting behavior [16] have been described, and appear to be related to differences in habitat types [17, 18], but few studies have quantified how these factors impact local population sizes and habitat use [19]. Habitat assessment between Mahale Mountains and Gombe in Tanzania [20], at Lagoas de Cufada National Park in Guinea-Bissau [18], and between forests of Western Uganda [21] and Mount Assirik in Senegal [13, 14, 22] are examples of studies comparing chimpanzee ecological behavior across habitat types. Other studies have explored chimpanzee diet and habitat selection in the Democratic Republic of Congo [23] and in Uganda [15], and nesting ecology in Nigeria [24, 25] and Tanzania [16]. Little is known, however about the Nigeria-Cameroon chimpanzee in MDNP.

The Nigeria-Cameroon chimpanzee was recognized since 1997 as the fourth subspecies of chimpanzees [2628] and is the least studied among all subspecies of chimpanzees. Classified as Endangered by IUCN [29], with between 3500 and 9000 individuals remaining [25, 28, 29], their populations size is declining across their limited natural range [29]. As is the case for other subspecies of chimpanzees, landscape fragmentation, habitat loss, disease, commercial bushmeat hunting and climate change are all substantial threats to the conservation of the Nigeria-Cameroon chimpanzee [29]. The conservation status of this subspecies may also change rapidly in response to habitat change [29]. It is therefore important to explore how habitat variation impacts the density and distribution of local chimpanzee populations.

Emerging methods such as the use of infra-red camera [30], the use of drones [31] and genetic material are also appropriate to reliably estimate the density and distribution of chimpanzee communities [32], but these studies are currently limited to relatively small areas and are outside the budgetary capacities of most protected area management plans within the country. Studying the distribution of nests is currently the most efficient means to estimate the distribution and density of chimpanzee populations [12, 33]. Although evidence of presence such as direct sighting, feeding remains and footprints are still frequently used to derive densities of chimpanzees, the most robust method of estimating population density continues to be based on nest counts [34]. The main objective of this study was to estimate the density of the Nigeria-Cameroon chimpanzee in two main habitat types within the MNDP, namely forest-savannah mosaic and dense forest, and to study the nesting ecology of chimpanzees in these two main habitat types. We investigated how habitat variation in the forest-savannah mosaic and in the dense forests affects chimpanzee distribution in MNDP, and the importance of the availability of nesting materials, canopy cover, understory, slope and altitude. The results will help to design regular monitoring activities focusing on chimpanzee habitat suitability and to shape effective management practices in MDNP. Key activities might be focused on the phenology of useful plants for chimpanzees as well as human encroachment in their suitable habitats. Furthermore, the findings will be relevant to the update of the imminent revision of the 2011 IUCN Regional Conservation Action Plan for the subspecies [28].

Methods

Mbam and Djerem National Park

Created in 2000, MDNP covers 4165.2 km2 and lies between 5°30′N and 6°14′N, and 12°20′E and 13°15′E [35] (Fig. 1). The rainy season extends between mid-April and mid-October and a dry season between mid-October and mid-April. Average rainfall is 1900 mm/year, average annual temperature is 24 °C [35]. The area lies within the Guinea-Congolia/Sudania regional transition zone, between the Soudanian regional centre of endemism in the north and the Guinea-Congolian forest block in the south [36]. The vegetation of the MDNP grades from savannah in the northwest through forest-savannah mosaic to closed canopy humid forest in the south-west [7] (Fig. 1). The relief is relatively flat and the altitude ranges from 650 to 930 m above sea level (a.s.l.). Approximately 30,000 human inhabitants live in 74 villages at the periphery of the MDNP [35]. These people mostly depend on natural resources for their food, traditional medicine and income. The human population tends to be concentrated in the northern periphery where grazing lands are available and where the Mbakaou Dam was constructed in 1964, and in the eastern periphery of the MDNP where the Belabo-Ngaoudéré railway link is found as established in 1970 [35] (Fig. 1).
Fig. 1
Fig. 1

The study area with the 4165.2 km2 Mbam-Djerem National Park (MDNP). The 1662.34 km2 core zone in the middle of MDNP is delimited with rivers. The Mbakaou artificial lake in the northern periphery of the park is shown in blue. The inset represents the location of MDNP within Cameroon

Survey design

We used data from a transect survey for large mammals collected between 2009 and 2014 to design a sampling plan for the assessment of chimpanzee density at MDNP. We used the encounter rate of chimpanzee nests derived from these previous surveys as an indicator of the effort required to obtain a density estimate. The coefficient of variation of 15% for forest-savannah mosaic and 20% for dense forest were chosen to perform equation 7.3 [37].

Thus, given the encounter rates of 1.7 nest/km and 0.93 nest/km, we found that 80 km and 88 km of effort, respectively in forest-savannah mosaic and in dense forest, were required to assess the chimpanzee nest density with the defined target precision. The effort to reach the specific target coefficient of variation was calculated using the value of 3 as dispersion parameter (b) in equation 7.3. Using these results, we developed a population survey protocol that included 84 transects of 2 km each (Fig. 2). The core zones included two strata (based on the physiognomy and structural characteristics using satellite imagery Landsat TM of April 2011) within the forest-savannah mosaic in the north and the dense forest in the south.
Fig. 2
Fig. 2

Survey design of the assessment of chimpanzee abundance within the core zone of MDNP

Standing crop nest count

Chimpanzees are elusive, difficult to see and occur at relatively low densities [28, 3840], thus requiring an indirect method for density estimation. Nest counts are often used as all weaned chimpanzees from around 3 years of age generally build a night nest to sleep in [41]. We used the standing crop nest count (SCNC) method [42, 43] to estimate the density of chimpanzees by completing unrepeated transects to count nests from January to June 2016 at MDNP. Two survey teams of six persons each comprising one MDNP biologist team leader, two rangers and three local guides were established. The teams were trained on the use of CyberTracker to collect field data following the Wildlife Conservation Society protocol [44]. Along each transect, the coordinates of each nest were recorded as well as the age class of each nest. The age class of each nest was classified using the system developed by Tutin and Fernandez [41] as fresh (vegetation is still green, leaves are not yet wilted and urine and faeces may be present at the site); recent (nest contains leaves that are green but wilted); old (nest has leaves that are no longer green but remain intact); and rotting (nest has shed its leaves, leaving only bare branches).

Habitat assessment

Predicting the influence of habitat attributes on wildlife is useful for conservation and protected area management [4548]. While walking along transects, we examined a set of variables to assess the habitat used by chimpanzees. For each nest encountered, we recorded the distance along the transect with a topofil, the perpendicular distance to the transect line of each nest spotted from the transect (using tape measure), the type of nest, the height above ground, the tree height, the tree species, and the diameter at breast height (dbh) of the tree (i.e. at 1.3 m above ground), the slope of the site, the vegetation type, the canopy cover and the age class of each nest in the nesting site. Slope was defined according to the following scheme: 0 = flat, 1 = low, 2 = moderate and 3= steep. Nest type was defined according to [49] as (a) Minimum (terrestrial nest with one or two stems of herbaceous plants); (b) Mixed (terrestrial nest with herbaceous plants and woody vegetation); (c) Tree (nest made in tree). The canopy cover was assigned as open (0–25%), low closure (26–50%), moderate closure (51–75%) and high closure (> 75%).

Habitat type included seven categories [50]: (a) Colonising Forest (CF); (b) Gallery Forest (GF); (c) Liana Forest (LF); (d) Marantaceae Forest (MF); (e) Mixed Forest with Closed Understory and Marantaceae (MFCUM); (f) Mixed Forest with Closed Understory (MFCU); (g) Mixed Forest with Opened Understory (MFOU). These habitats are described in detail in Additional file 1. The plant species used for nesting were identified in the field. We used the Garoua Wildlife School herbarium to identify nesting plants from field samples. We assessed the relationship between habitat type and nest density using several parameters, including number of nests, nest height, dbh of the nesting tree, and encounter rates of nest sites registered for each strata and habitat type. We conducted non-parametric Kruskal–Wallis tests to compare dependent variables across habitat types and strata. We also used General Linear Models and contingency table [51] to explore the effects of habitat attributes (e.g. plant species, dbh of the nesting tree, slope, understory, canopy cover and altitude) on the nesting sites (e.g. nest abundance, nest height, nest encounter rate). We used the software program R for these analyses [51].

Estimating chimpanzee density, population size and distribution

Conversion parameters

Converting nest density into an estimate of chimpanzee density requires two parameters: a nest production rate and a nest decay rate [41, 42, 52]. Nest decay data were not available for MDNP. Therefore, similar to other studies where reliable nest production and decay data were unavailable, we used a range of possible nest decay rate values from previous studies [33, 52] to estimate the density of chimpanzees for this study. Nest production rates are estimated by averaging the number of nests built per day by a weaned chimpanzee from direct monitoring of habituated chimpanzees to then assess potential nest production rates in the given study site [42, 53]. Weaned chimpanzees generally make new sleeping nests every night [54] but they also sometimes build day nests in which to rest. Allowing for this, we used a value of 1.09 (± 0.5) nests per day reported in previous research [39, 42] for the present study.

Measuring nest decay rates is more challenging, as it involves monitoring a sufficient number of fresh nests from the time they are built to the time they disappear [39]. In addition, nest decay rates may vary considerably depending on the plant species used to build the nest and the local climatic parameters and therefore vary considerably between sites and vegetation type [33]; thus carrying an associated error which may affect the precision of density estimates [33, 53, 55]. Moreover, climate can affect the rate of re-use and building of nests as well as decay rates [21, 39, 54, 56]. Observations in Ebo Forest, Cameroon, which is close to the MDNP, suggest a nest decay rate of 88.2 (± 7.1) days. This is similar to the estimate from the Taï forests in the Ivory Coast (91.22 ± 5.8 days) [12]. Both MDNP and Ebo forest are found in the northern side of the Sanaga River and within the same climatic domain of Cameroon (2°–6° of northern latitude), with a similar amount of annual rainfall (2400 mm in the Ebo Forest and 1900 mm in the MDNP). Much uncertainty remains, however, in these estimates [43, 57]. A value of 221 days was previously used in the MDNP to convert nest density into chimpanzee density. To assess the sensitivity of the density estimate to nest decay rate, we also used 120 and 221 days.

Conversion of nest density to chimpanzee density

We used the Distance 7.0 Program to derive nest and chimpanzee density estimates [37, 58]. This program implements a series of detection function models with their expansion series acquired from the data set (Additional file 2) to estimate the chimpanzee density by inference from the nest density [37]. Different models are then compared based on the Akaike Information Criterion [58].

Single nests have been used to estimate chimpanzee nest density [12, 59]. Chimpanzee density was then derived from nest density using conversion parameters (nest production rate, nest decay rate and the proportion of nest builders).

Chimpanzee distribution

We calculated encounter rates of nest sites for each transect and used this information to develop Inverse Distance Weighting-IDW interpolation using 30 neighbors and a power of 2 in ArcGIS 10.1 software [60, 61]. The corresponding raster layer was extracted by mask and exported as PNG file.

Results

Detection models

The model fits for the nest counts were as follows: hazard-rate simple polynomial truncated at 20 m of perpendicular distane for all data (Fig. 3a), Hazard-rate simple polynomial truncated at 25 m in the forest-savannah mosaic (Fig. 3b) and Hazard-rate cosine truncated at 20 m in the dense forest (Fig. 3c).
Fig. 3
Fig. 3

a Global detection function curve of all nests combined (Hazard-rate simple polynomial) truncated at 20 m of perpendicular distance. b Global detection function curve of nests from the forest-savannah mosaic (Hazard-rate simple polynomial) truncated at 25 m of perpendicular distance. c Global detection function curve of nests from the dense forest (Hazard-rate cosine) truncated at 20 m of perpendicular distance

Chimpanzee density at Mbam-Djerem National Park

A total of 32 transects were surveyed in the forest-savannah mosaic and 34 transects in the dense forest. We observed 249 nests from these transects, of which 119 nests occurred in dense forest and 130 nests in forest-savannah mosaic. The nest detection probability was 0.58 (± 0.05) and 0.52 (± 0.06), respectively, in the forest-savannah mosaic and the dense forest. The effective strip width was 14.62 (± 1.37) m in the forest-savannah mosaic and 10.46 (± 1.30) m in the dense forest. Table 1 shows nest density estimates while Table 2 shows chimpanzee density estimates.
Table 1

Estimated nest density (per km2) in the forest-savannah mosaic, the dense forest and all nests combined

 

Number of Nestsa

ESW (SD)

Pa (SD)

Nest density

CV

Models

All data

249

12.95 (1.07)

0.51 (0.04)

80.75 (51.32–127.04)

23.06

Hazard-rate simple polynomial + 20 m truncation

Forest-savannah mosaic

130

14.62 (1.37)

0.58 (0.05)

77.20 (36.06–165.29)

38.69

Hazard-rate simple polynomial + 25 m truncation

Dense forest

119

10.46 (1.30)

0.52 (0.06)

84.80 (52.97–135.74)

23.80

Hazard-rate cosine + 20 m truncation

ESW effective strip width (m), SD standard deviation; Pa probability of detection; CI 95% confidence interval, CV percentage coefficient of variation

aSample size after truncation

Table 2

Estimated chimpanzee density and population size based on a range of estimated nest decay rate

Decay rate

88 days

120 days

221 days

Area (km2)

Estimates

Chimpanzees/km2 (CI)

Population size (CI)

Chimpanzees/km2 (CI)

Population size (CI)

Chimpanzees/km2 (CI)

Population size

All data

0.83 (0.32–2.11)

1396 (535–3643)

0.61 (0.23–1.59)

1026 (397–2650)

0.33 (0.12–0.86)

557 (216–1439)

1662.34

Forest-savannah mosaic

0.80 (0.26–2.41)

612 (203–1842)

0.59 (0.19–1.76)

449 (150–1343)

0.32 (0.10–0.95)

244 (82–729)

900.84

Dense forest

0.88 (0.55–1.41)

795 (496–1272)

0.64 (0.24–1.68)

584 (225–1517)

0.35 (0.13–0.91)

317 (122–824)

761.5

CI 95% confidence interval. Estimates derived from decays rate considered to be the most suitable for each habitat type are given in italics

The density varies considerably depending on the nest decay rate used. The nest decay rate is inversely proportional to the nest density. Considering the same nest decay rate, chimpanzee densities were similar across strata although with different confidence interval.

Habitat assessment

Surveyed effort was assessed as well as the proportion of nests in each habitat type (Table 3).
Table 3

Total effort and proportion of nests per habitat type

Vegetation types

Effort (km)

Percent

Proportion of nests

CF

48

36.36

40.56

GF

46

34.85

37.75

LF

24

18.18

14.05

MFOU

6

4.55

4.41

MFCU

4

3.03

1.60

MF

2

1.52

0.80

MFCUM

2

1.52

0.80

Total

132

100.00

100.00

CF colonising forest, GF gallery forest, LF liana forest, MF Marantaceae forest; MFCUM mixed forest with closed understory and Marantaceae, MFCU mixed forest with closed understory, MFOU mixed forest with opened understory

A total distance of 48 km (36.36%) was covered in colonising forest and 46 km (34.85%) in gallery forest. These are the two main vegetation types where chimpanzee nests were recorded. The proportion of nests varies with habitat types (F6, 284 = 9.54, P < 0.001). The number of nests found in colonizing forest was 101 nests (40.56%) and 94 nests (37.75%) in gallery forest (Fig. 4).
Fig. 4
Fig. 4

The percentage of nests per vegetation type in dense forest and in forest-savannah mosaic: CF colonising forest, GF gallery forest, LF liana forest, MF Marantaceae forest; MFCUM mixed forest with closed understory and Marantaceae, MFCU mixed forest with closed understory, MFOU mixed forest with opened understory

We identified a total of 31 plant species used as nesting material. Species commonly used to build nests were Berlina sp. (Caesalpiniaceae) (18.84%), Diospyros sp. (Ebenaceae) (15.36%) and Uapaca guineensis (Euphorbiaceae) (14.78%) (Additional file 3) (Fig. 5).
Fig. 5
Fig. 5

Nesting choice in different habitat types

No evidence for difference was found on the number of plant species used for nesting between the dense forest and the forest-savannah mosaic (Kruskal–Wallis X2 = 1.1, df = 1, P = 0.293) or between habitat types (Kruskal–Wallis X2 = 6, df = 6, P = 0.423).

There was no evidence for difference in nest density and chimpanzee density between the dense forest and the forest-savannah mosaic (Kruskal–Wallis X2 = 1, df = 1, P = 0.31). Similarly, there was no difference in nest encounter rates (Kruskal–Wallis X2 = 0.13, df = 1, P = 0.71) between the dense forest and forest-savannah mosaic.

The nest type frequency differed between dense forest and forest-savannah mosaic (Pearson’s X2 = 9.19, P = 0.046) and between habitat types (Pearson’s X2 = 14.84, P = 0.05). However, 98.88% of all nests (N = 249) were tree nests with 52.20% (N = 130) and 46.58% (N = 116) found, respectively in forest-savannah mosaic and in dense forest. Among all the nests registered (n = 249), only three (1.20%) were ground nests although there was no evidence as to whether chimpanzees slept in them over night or used them to rest during day. These nests were found in the dense forest and built with Marantaceae leaves (Additional file 4) (Table 4).
Table 4

Nest types per sector with the mean nest height and the mean dbh of the nesting tree

Sector

Area (km2)

Tree nests

Ground nests

Mean nest height (m)

Mean dbh of the nesting tree

Overall dataset

1662.34

246

3

11.59 ± 7.83

10.3 ± 8.42

Dense forest

900.84

116

3

10.61 ± 6.05

9.84 ± 5.72

Forest-savannah mosaic

761.5

130

0

12.42 ± 6.56

10.68 ± 6.10

Nest encounter rates varied significantly with altitude (F1, 197 = 55.24, P < 0.001). A total of 189 nests (75.9%) was observed between 650 m and 800 m a.s.l

There was a strong evidence of the influence of canopy cover (F3, 284 = 31.75, P < 0.001) and slope (F3, 284 = 10.22, P < 0.001) on the nesting site. In forest-savannah mosaic, 38.99% of the nests where found under high closure canopy (> 75%) while in dense forest, 37.03 of the nests were found under moderate closure canopy (51–75%). As for the slope, 53.45% of the nests recorded in forest-savannah mosaic and 60% in dense forest were found in low slope, although 31.44% of the nests were found in steep slope in forest-savannah mosaic. Low slope may offer comfortable nesting conditions to chimpanzee in MDNP.

There was a significant positive correlation between nest height and dbh of the nesting trees (Additional file 5) (r = 0.365, t292 = 6.717, p < 0.001) (Fig. 6). The mean dbh of nesting tree was 10.03 (± 8.42) cm, while the mean nest height was 11.59 (± 7.83) m.
Fig. 6
Fig. 6

Correlation between the nest height and the diameter at breast height (dbh) of the nesting trees

Chimpanzee distribution

The spatial interpolation of the encounter rates of chimpanzee nests is shown in Fig. 7. Chimpanzee nests were found between the Djerem and the Mekié Rivers. Nests were most frequently encountered in the dense forest and especially in the middle, south and north-west of the core zone, and few nests were found in the north.
Fig. 7
Fig. 7

Spatial distribution of chimpanzee nest densities in the core zone of MDNP

Discussion

Chimpanzee densities

Our findings suggest that gallery forest and colonizing forests are preferred habitats for chimpanzees in the MDNP. The forest-savannah mosaic with associated gallery forests provide suitable habitat for the Nigeria-Cameroon chimpanzee. The nest density estimates varied with strata and the chimpanzee density was similar to the density previously reported in the area, although with a relatively high coefficient of variation. The larger error associated with the chimpanzee density estimate might be explained by the use of a non-site specific nest decay rate as the later depends on the environmental variables of the study site [12] and the intrinsic limitations attributed to the survey method. On 25 of these transects (34% of the total) we found no chimpanzee nests. However, compared to the Ebo Forest in Cameroon where a nest decay rate of 88 days was used to obtain a chimpanzee density estimate of 0.67 animals/km2, our density estimate is lower than those from other Nigeria-Cameroon chimpanzee sites (Table 5).
Table 5

Population density estimates of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti) at the Mbam-Djerem National Park compared to other surveys

Site

Decay rate (days)

Chimpanzee/km2 (CI)

References

MDNP (dense forest stratum), Cameroon

88

0.88 (0.55–1.41)

This study

MDNP (forest-savannah stratum), Cameroon

120

0.55 (0.19–1.76)

MDNP (all data combined), Cameroon

221

0.33 (0.12–0.88)

Ngel Nyaki Forest Reserve, Nigeria

162.8

1.5

[63]

Ngel Nyaki Forest Reserve, Nigeria

 

1.67

[25]

Taï National Park, Ivory Coast

91.22

0.89

[12]

CI 95% confidence interval when available

Although chimpanzee density appears to be low in MDNP, the population may be more stable compared to other sites where hunting is considered to be a major threat [62]. Our density estimate should be considered with caution because specific nest decay rates for MDNP are unavailable. We recommend the MNC method for future surveys because it does not require decay rate and direct observations, even though they are more costly and time-consuming.

Habitat assessment

We found no evidence that different types of plant species were used for nesting in the dense forest compared with the forest-savannah mosaic, even though considerably more plant species were found in the latter habitat type. Landolphia sp. and Diospyros sp. were also used by chimpanzees for nesting in Nigeria and Democratic Republic of Congo [23, 63]. The abundance of plant species found in nests in the forest-savannah mosaic might be explained by the high frequency of gallery forests and colonising forests. Both these contain food trees such as Uapaca guineensis and are relatively more diverse than dense forest. Thus, chimpanzees may not need to range so far as in dense forest for food, water and nesting materials.

Our results show that most nests occurred in trees, which is consistent with several other field studies of chimpanzee communities in other regions of Africa (i.e. Nigeria [63], Tanzania [16] and Kahuzi Biega National Park [64]). In our study, only 1.20% of nests were on the ground. This was the first time that ground nests have been recorded in the MDNP, and further monitoring is required to understand this behaviour: does it indicate the absence of predators or some aspect of social behaviour? In general, the construction of sleeping nests which are usually more elaborate than the day nests, and ground nesting is rarely observed in unhabituated chimpanzees [65]. Ground nesting has been reported in Senegal in habitats with no or few predators [66] although predators were abundant at the ground nesting site of Bili [23]. In south-east Cameroon, ground nests (3.47% of 1008 nests) were probably the consequence of a lack of nesting trees, or a reaction to hunting with guns or the abundance of terrestrial herbaceous vegetation [67]. It could also indicate that the nest builders were sick [65]. Previous reports of relatively high rates of ground nesting (6.1% of 994 nests) in the Nimba Mountains in Guinea [65] and (3.7% of 37 nests) at Yealé in Ivory Coast [68], have been hypothesized to result either from a male mating strategy, or a regional or seasonal fluctuation in the availability of ground nesting material [68]. Disturbance by humans and seasonal effects may both affect whether chimpanzees construct their nests on the ground or in trees [23]. While Pruetz et al. speculates arboreal nesting as anti-predator adaptation for chimpanzee, there is no evidence that in the absence of predators, chimpanzees switch to ground nesting [64, 69, 70]. Koops et al. suggested that the tendency to build ground nests may be genetically determined in the Nimba Mountains at Seringbara in Guinea. Males may also nest on the ground to guard an oestrous female in a tree above [71].

Over half of the nests were found in gallery forests, highlighting the importance of this habitat type for chimpanzee conservation. At the Ngel Nyaki Forest Reserve in Nigeria, chimpanzees most frequently built nests in gallery forests [72]. Habitat attributes such as elevation also affect nest abundance. Nest encounter rates were higher with increasing elevation between 650 and 800 m a.s.l. in our study, still relatively lower than those of Budongo Forest in Uganda, where they were more likely to be found above 2000 m a.s.l. [21]. Chimpanzee abundance was highly correlated with food availability in the Kibale National Park in Uganda [17] and in the Budongo Forest [21]. In Kahuzi Biega National Park, in Ngel Nyaki Forest Reserve and in Kibale National Park chimpanzees preferred nesting in trees with ripe fruits [64]. Canopy cover was also found to influence the choice of nesting site. Chimpanzees in MDNP appeared to prefer habitat with closed canopy for nesting. Previous studies in Senegal reported that chimpanzees also preferentially chose habitat with closed canopy for nesting [23, 66].

We also found that the nest height was related to the height and dbh of trees (R2 = 0.13), as has been described in previous studies [72]. The average dbh of nesting trees at our site was c. 10.30 ± 8.42 cm compared to 54 cm in the Bili-Uele forest in Democratic Republic of Congo [23]. While the average nest height (11.59 ± 7.83 m) was greater compared to 8 m found in Senegal [66] but lower than 20 m found in Nigeria [63]. In the Nigerian study nest height were positively correlated to tree height.

Chimpanzee distribution

In this study, we found that chimpanzee nests were concentrated in the middle of the core zone and relatively rare in the north and north-east. However, this may vary depending on season and food availability. Using only nests may fail to consider the seasonality of chimpanzees ranging, and should not imply that only areas where nests are observed are valuable for conservation [53, 73]. Further exploration of the effects of human pressure and the density of fruiting trees are required for a better understanding of chimpanzee distribution in the MDNP [17, 74]. Chimpanzees were most abundant in the middle and southern sections of the core zone which are the least accessible to park rangers, and consequently are relatively undisturbed.

The MDNP is the stronghold of Nigeria-Cameroon chimpanzee, noted for its exceptional conservation value [28] and the genetic distinctiveness of its population [10, 75]. Monitoring chimpanzee nesting and feeding sites will continue to be important for efficient conservation planning for this subspecies of great apes. More efforts are therefore needed to assess the chimpanzee nest decay rate to improve the reliability of density estimates. Regular monitoring and patrols should be focused in those areas to sustain this critical chimpanzee population and their habitat into future.

Conclusions

This study provides the first systematic assessment of the effect of habitat variability on the density of chimpanzees in the MDNP, revealing that gallery forest and colonising forest are preferred by chimpanzees in the core area, while highlighting characteristics of habitat that are positively associated with nest abundance and therefore high conservation importance. Our study indicates that as long as these habitat types are protected, current management practices to maintain savannahs are compatible with chimpanzee conservation. Well-designed surveys are required to assess the sustainability of chimpanzee populations [41, 76]. Currently chimpanzees in the MDNP are becoming increasingly tolerant of humans (Additional file 6). The MDNP offers an excellent opportunity for long-term research on the Nigeria-Cameroon chimpanzee, the least studied great ape subspecies [75] and aimed at understanding and dealing with its potential threats there and elsewhere. To safeguard this area from anthropogenic threats, we recommend that intensive patrols and biomonitoring activities should be focused on the pattern of chimpanzee nesting ecology to prevent threats that could led to almost complete depletion of chimpanzee and other wildlife as has occurred in the Gashaka Gumti National Park and Ngel Nyaki Forest Reserve in Nigeria [63, 7779]. Further studies need to be focused on nest decay rates and phenology of useful plants (Berlina sp., Diospyros sp., Uapaca guineensis, Xylopia aethiopica and Landolphia sp.) in order to model chimpanzee abundance and distribution in MDNP. Base on the field observations, human population and chimpanzee both make use of Xylopia aethiopica and awareness activities need to be developed to protect this tree species. Our findings were transferred to the park authorities to update the biomonitoring database and measure the progress of chimpanzee conservation in MDNP.

Declarations

Authors’ contributions

SAK, KSB, MKG and BS designed the research and SAK, RDDA and DEAO implemented the research. SAK, JM and PJ performed data analysis. SAK, KSB, PJ and JM wrote the paper. FM helped the design of the study, advised the data analysis. All authors read and approved the final manuscript.

Acknowledgements

This research was implemented with the generous support of the Rufford Foundation, the World Wide Fund for Nature (WWF) Russell E. Train Education for Nature and the Garoua Wildlife School via its US Fish and Wildlife Service capacity-building program to which we are grateful. We thank the Director of the Wildlife Conservation Society Project in Mbakaou Mr. Fosso Bernard and park manager Mr. Mounga Albert for their collaboration and logistical support during fieldwork. We also thank all of the survey teams and biomonitoring unit staff, for their help with data collection. We thank the Central African Biodiversity Alliance for the logistic support and to Dr. Zacharie Nzooh Dongmo of the WWF Cameroon for his technical advice on the research proposal and survey design. We are grateful to the Wildlife Conservation Research Unit of the University of Oxford, and to Dr. Christos Astaras, for providing the opportunity to participate in the Postgraduate International Diploma on Wildlife Conservation Practice and to analyse the data as part of my training. Finally, we acknowledge Professor Robert Weladji of the University of Concordia in Canada and the anonymous reviewers for their helpful comments on the revised manuscript of this paper.

Competing interests

There are no competing interests. Our connection with World Wide Fund for Nature and Rufford Foundation is simply a donor/grantee relation. This does not hinder our commitment to the editorial policies of BMC Ecology on publishing findings, data and materials.

Availability of data and materials

Data analysed during this study are included in this published article.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Funding

This research was funded by grants awarded to Serge Alexis Kamgang from World Wide Fund for Nature (ST68) and the Rufford Foundation (13184_1, 20258_2). The funders had no role in study design, data collection and analysis or the decision to publish the findings.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Garoua Wildlife School, Face aéroport international de Garoua, P.O. Box 271, Garoua, Cameroon
(2)
Department of Forestry, Faculty of Agronomy and Agricultural Sciences, University of Dschang, P.O. Box 222, Dschang, Cameroon
(3)
Global Conservation Program, Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, New York, NY 10460, USA
(4)
Faculty of Natural Sciences, University of Stirling, Stirling, FK9 4LA, Scotland, UK
(5)
Cameroon Biodiversity Programme, Wildlife Conservation Society, P.O. Box 3035, Yaoundé, Cameroon
(6)
Ministry of Forestry and Wildlife, Yaounde, Cameroon
(7)
Department of Biology, Drexel University, Philadelphia, PA 19104, USA
(8)
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Recanati-Kaplan Centre, Tubney, Oxford, UK
(9)
Laboratory of Applied Ecology, Faculty of Agronomic Sciences, University of Abomey-Calavi, 01 P.O.Box 526, Cotonou, Benin

References

  1. Williamson EA, Maisel F, Groves CP. Family hominid (Great Apes). In: Intermediary RA, Irelands AB, Wilson DE, editors. Handbook of the mammals of the world. 3rd ed. Barcelona: Lynx Dictions; 2013. p. 792–843.Google Scholar
  2. IUCN. IUCN red list of threatened species 2017-3. Cambridge: IUCN; 2017.Google Scholar
  3. Junker J, Blake S, Boesch C, Campbell G, du Toit L, Duvall C, Ekobo A, Etoga G, Galat-Luong A, Gamys J, Ganas-Swaray J, Gatti S, Ghiurghi A, Granier N, Hart J, Head J, Herbinger I, Hicks TC, Huijbregts B, Imong IS, Kuempel N, Lahm S, Lindsell J, Maisels F, McLennan M, Martinez L, Morgan B, Morgan D, Mulindahabi F, Mundry R, N’Goran KP, Normand E, Ntongho A, Okon DT, Petre C-A, Plumptre A, Rainey H, Regnaut S, Sanz C, Stokes E, Tondossama A, Tranquilli S, Sunderland-Groves J, Walsh P, Warren Y, Williamson EA, Kuehl HS. Recent decline in suitable environmental conditions for African great apes. Divers Distrib. 2012;18:1077–91. https://doi.org/10.1111/ddi.12005.View ArticleGoogle Scholar
  4. Torres J, Brito J, Vasconcelos M, Catarino L, Gonçalves J, Honrado J. Ensemble models of habitat suitability relate chimpanzee (Pan troglodytes) conservation to forest and landscape dynamics in Western Africa. Biol Conserv. 2010;143(2):416–25. https://doi.org/10.1016/j.biocon.2009.11.007.View ArticleGoogle Scholar
  5. Pintea L, Bauer ME, Bolstad PV, Pusey A. Matching multiscale remote sensing data to inter-disciplinary conservation needs: the case of chimpanzees in Western Tanzania. In: Remote Sensing Symposium/Land Satellite Information IV Conference and the ISPRS Commission: 2003. Citeseer.Google Scholar
  6. Ernst C, Verhegghen A, Mayaux P, Hansen M, Defourny P, Kondjo K, Makak J-S, Biang J-DM, Musampa C, Motogo RN. Cartographie du couvert forestier et des changements du couvert forestier en Afrique centrale. Les forêts du Bassin du Congo: état des forêts. Commission of Central African Forest; 2010. p. 23–42.Google Scholar
  7. Mitchard ETA, Saatchi SS, Gerard FF, Lewis SL, Meir P. Measuring woody encroachment along a forest-savanna boundary in Central Africa. Earth Interact. 2009;13(8):1–29. https://doi.org/10.1175/2009EI278.1.View ArticleGoogle Scholar
  8. Knight A, Chapman HM, Hale M. Habitat fragmentation and its implications for Endangered chimpanzee Pan troglodytes conservation. Oryx. 2015. https://doi.org/10.1017/S0030605315000332.View ArticleGoogle Scholar
  9. Morgan BJ, Abwe EE. Chimpanzees use stone hammers in Cameroon. Curr Biol. 2006;16(16):R632–3. https://doi.org/10.1016/j.cub.2006.07.045.View ArticlePubMedPubMed CentralGoogle Scholar
  10. Mitchell MW, Locatelli S, Ghobrial L, Pokempner AA, Clee PRS, Abwe EE, Nicholas A, Nkembi L, Anthony NM, Morgan BJ. The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies. BMC Evol Biol. 2015;15(3):1. https://doi.org/10.1186/s12862-014-0276-y.View ArticlePubMedPubMed CentralGoogle Scholar
  11. Sesink-Clee PR, Abwe EE, Ambahe R, Anthony NM, Fotso R, Locatelli S, Maisels F, Mitchell MW, Morgan BJ, Pokempner A. Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change. BMC Evol Biol. 2015;15:2. https://doi.org/10.1186/s12862-014-0275-z.View ArticlePubMedPubMed CentralGoogle Scholar
  12. Kouakou CY, Boesch C, Kuehl H. Estimating chimpanzee population size with nest counts: validating methods in Taï National Park. Am J Primatol. 2009;71(6):447–57. https://doi.org/10.1002/ajp.20673.View ArticlePubMedPubMed CentralGoogle Scholar
  13. Baldwin PJ, McGrew WC, Tutin CE. Wide-ranging chimpanzees at Mt. Assirik, Senegal. Int J Primatol. 1982;3(4):367–85. https://doi.org/10.1007/BF02693739.View ArticleGoogle Scholar
  14. McGrew W, Baldwin P, Tutin C. Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal: I. Composition. Am J Primatol. 1988;16(3):213–26. https://doi.org/10.1002/ajp.1350160304.View ArticleGoogle Scholar
  15. Tweheyo M, Lye KA, Weladji RB. Chimpanzee diet and habitat selection in the Budongo Forest Reserve, Uganda. Forest Ecol Manag. 2004;188(1):267–78. https://doi.org/10.1016/j.foreco.2003.07.028.View ArticleGoogle Scholar
  16. Hernandez-Aguilar RA, Moore J, Stanford CB. Chimpanzee nesting patterns in savanna habitat: environmental influences and preferences. Am J Primatol. 2013;75(10):979–94. https://doi.org/10.1002/ajp.22163.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Balcomb SR, Chapman CA, Wrangham RW. Relationship between chimpanzee (Pan troglodytes) density and large, fleshy-fruit tree density: conservation implications. Am J Primatol. 2000;51(3):197–203. https://doi.org/10.1002/1098-2345(200007)51:3%3c197:AID-AJP4%3e3.0.CO;2-C.View ArticlePubMedPubMed CentralGoogle Scholar
  18. Carvalho JS, Meyer CF, Vicente L, Marques TA. Where to nest? Ecological determinants of chimpanzee nest abundance and distribution at the habitat and tree species scale. Am J Primatol. 2015;77(2):186–99. https://doi.org/10.1002/ajp.22321.View ArticlePubMedPubMed CentralGoogle Scholar
  19. Morgan D, Mundry R, Sanz C, Ayina CE, Strindberg S, Lonsdorf E, Kühl HS. African apes coexisting with logging: comparing chimpanzee (Pan troglodytes troglodytes) and gorilla (Gorilla gorilla gorilla) resource needs and responses to forestry activities. Biol Conserv. 2017. https://doi.org/10.1016/j.biocon.2017.10.026.View ArticleGoogle Scholar
  20. Collins DA, McGrew WC. Habitats of three groups of chimpanzees (Pan troglodytes) in western Tanzania compared. J Hum Evol. 1988;17(6):553–74. https://doi.org/10.1016/0047-2484(88)90084-X.View ArticleGoogle Scholar
  21. Plumptre AJ, Cox D. Counting primates for conservation: primate surveys in Uganda. Primates. 2006;47(1):65–73. https://doi.org/10.1007/s10329-005-0146-8.View ArticlePubMedGoogle Scholar
  22. McGrew WC, Baldwin PJ, Tutin CE. Chimpanzees in a hot, dry and open habitat: Mt. Assirik, Senegal, West Africa. J Hum Evol. 1981;10(3):227–44. https://doi.org/10.1016/S0047-2484(81)80061-9.View ArticleGoogle Scholar
  23. Hicks TC, Tranquilli S, Swinkels J, Faustin L, Roessingh P. Morphology, distribution, nesting, and diet of the Bili apes. A Chimpanzee Mega Culture 2010.Google Scholar
  24. Sommer V, Adanu J, Faucher I, Fowler A. Nigerian chimpanzees (Pan troglodytes vellerosus) at Gashaka: two years of habituation efforts. Folia Primatol. 2004;75(5):295–316. https://doi.org/10.1159/000080208.View ArticlePubMedGoogle Scholar
  25. Beck J, Chapman H. A population estimate of the Endangered chimpanzee Pan troglodytes vellerosus in a Nigerian montane forest: implications for conservation. Oryx. 2008;42(03):448–51. https://doi.org/10.1017/S0030605308001397.View ArticleGoogle Scholar
  26. Gonder MK, Oates JF, Disotell TR, Forstner MR, Morales JC, Melnick DJ. A new west African chimpanzee subspecies? Nature. 1997;388(6640):337. https://doi.org/10.1038/41005.View ArticlePubMedGoogle Scholar
  27. Oates JF, Groves CP, Jenkins PD. The type locality of Pan troglodytes vellerosus (Gray, 1862), and implications for the nomenclature of West African chimpanzees. Primates. 2009;50(1):78–80. https://doi.org/10.1007/s10329-008-0116-z.View ArticlePubMedGoogle Scholar
  28. Morgan BJ, Adeleke A, Bassey T, Bergl R, Dunn A, Fotso R, Gadsby E, Gonder MK, Greengrass E, Koulagna DK. Regional action plan for the conservation of the Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti). San Diego: IUCN/SSC Primate Specialist Group and Zoological Society of San Diego; 2011.Google Scholar
  29. Oates JF, Doumbe O, Dunn A, Gonder MK, Ikemeh R, Imong I, Morgan BJ, Ogunjemite B, Sommer V. Pan troglodytes ssp. ellioti. The IUCN red list of Threatened Species 2016: e.T40014A17990330. Downloaded on 20 October 2016. 2016.Google Scholar
  30. Després-Einspenner M-L. Utilisation des caméras de piégeage et des modèles de capture-recapture pour l’estimation des densités de chimpanzés d’Afrique occidentale (Pan troglodytes verus) en Côte d’Ivoire. 2016.Google Scholar
  31. Bonnin N, van Andel S, Kerby J, Piel AK, Pintea L, Wich SA. Assessment of chimpanzee nests detectability on drone-acquired images. Drones. 2018;2(2):17. https://doi.org/10.3390/drones2020017.View ArticleGoogle Scholar
  32. Arandjelovic MHJ, Rabanal LI, Schubert G, Mettke E, et al. Non-invasive genetic monitoring of wild Central chimpanzees. PLoS ONE. 2011;6(3):e14761. https://doi.org/10.1371/journal.pone.0014761.View ArticlePubMedPubMed CentralGoogle Scholar
  33. Laing S, Buckland S, Burn R, Lambie D, Amphlett A. Dung and nest surveys: estimating decay rates. J Appl Ecol. 2003;40(6):1102–11. https://doi.org/10.1111/j.1365-2664.2003.00861.x.View ArticleGoogle Scholar
  34. Kühl H. Best practice guidelines for the surveys and monitoring of great ape populations. Gland: IUCN; 2008.View ArticleGoogle Scholar
  35. MINFOF. Plan d’aménagement du Parc National de Mbam et Djerem et sa zone périphérique 2007–2011. Yaounde: MINFOF; 2007.Google Scholar
  36. White F. The vegetation of Africa, a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa (3 Plates, Northwestern Africa, Northeastern Africa, and Southern Africa, 1: 5,000,000). Paris: UNESCO; 1983.Google Scholar
  37. Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers D, Thomas L. Introduction to distance sampling estimating abundance of biological populations. Oxford: Oxford University Press; 2001.Google Scholar
  38. Marques TA, Thomas L, Martin SW, Mellinger DK, Ward JA, Moretti DJ, Harris D, Tyack PL. Estimating animal population density using passive acoustics. Biol Rev. 2013;88(2):287–309. https://doi.org/10.1111/brv.12001.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Plumptre A, Reynolds V. Censusing chimpanzees in the Budongo forest, Uganda. Int J Primatol. 1996;17(1):85–99. https://doi.org/10.1007/BF02696160.View ArticleGoogle Scholar
  40. Guschanski K, Vigilant L, McNeilage A, Gray M, Kagoda E, Robbins MM. Counting elusive animals: comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol Conserv. 2009;142(2):290–300. https://doi.org/10.1016/j.biocon.2008.10.024.View ArticleGoogle Scholar
  41. Tutin CE, Fernandez M. Nationwide census of gorilla (Gorilla g. gorilla) and chimpanzee (Pan t. troglodytes) populations in Gabon. Am J Primatol. 1984;6(4):313–36. https://doi.org/10.1002/ajp.1350060403.View ArticleGoogle Scholar
  42. Morgan D, Sanz C, Onononga JR, Strindberg S. Ape abundance and habitat use in the Goualougo Triangle, Republic of Congo. Int J Primatol. 2006;27(1):147–79. https://doi.org/10.1007/s10764-005-9013-0.View ArticleGoogle Scholar
  43. Fleury-Brugiere M-C, Brugiere D. High population density of Pan troglodytes verus in the Haut Niger National Park, Republic of Guinea: implications for local and regional conservation. Int J Primatol. 2010;31(3):383–92.View ArticleGoogle Scholar
  44. Kühl H, Maisels F, Ancrenaz M, Williamson EA. Lignes Directrices pour de Meilleures Pratiques en Matière d’Inventaire et de suivi des Populations de Grands Singes. Gland: IUCN; 2009.Google Scholar
  45. Dormann C, McPherson JM, Araújo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Daniel Kissling W. Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography. 2007;30(5):609–28. https://doi.org/10.1111/j.2007.0906-7590.05171.x.View ArticleGoogle Scholar
  46. Burgess ND, Balmford A, Cordeiro NJ, Fjeldsa J, Kueper W, Rahbek C, Sanderson EW, Scharlemann JPW, Sommer JH, Williams PH. Correlations among species distributions, human density and human infrastructure across the high biodiversity tropical mountains of Africa. Biol Conserv. 2007;134(2):164–77. https://doi.org/10.1016/j.biocon.2006.08.024.View ArticleGoogle Scholar
  47. Hedley SL, Buckland ST. Spatial models for line transect sampling. J Agric Biol Environ Stat. 2004;9(2):181–99. https://doi.org/10.1198/1085711043578.View ArticleGoogle Scholar
  48. Guisan A, Zimmermann NE. Predictive habitat distribution models in ecology. Ecol Model. 2000;135(2):147–86. https://doi.org/10.1016/S0304-3800(00)00354-9.View ArticleGoogle Scholar
  49. Tutin CE, Parnell RJ, White LJ, Fernandez M. Nest building by lowland gorillas in the Lopé Reserve, Gabon: environmental influences and implications for censusing. Int J Primatol. 1995;16(1):53–76. https://doi.org/10.1007/BF02700153.View ArticleGoogle Scholar
  50. White L, Edwards A. Conservation research in the African rain forests: a technical handbook. New York: Wildlife Conservation Society; 2000. p. 444.Google Scholar
  51. Team. RDC. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www-project.org/. 2016. Accessed 22 Sept 2016.
  52. Hicks TC, Tranquilli S, Kuehl H, Campbell G, Swinkels J, Darby L, Boesch C, Hart J, Menken SB. Absence of evidence is not evidence of absence: discovery of a large, continuous population of Pan troglodytes schweinfurthii in the Central Uele region of northern DRC. Biol Conserv. 2014;171:107–13. https://doi.org/10.1016/j.biocon.2014.01.002.View ArticleGoogle Scholar
  53. Mathewson P, Spehar S, Meijaard E, Sasmirul A, Marshall AJ. Evaluating orangutan census techniques using nest decay rates: implications for population estimates. Ecol Appl. 2008;18(1):208–21. https://doi.org/10.1890/07-0385.1.View ArticlePubMedGoogle Scholar
  54. Plumptre AJ, Reynolds V. Nesting behavior of chimpanzees: implications for censuses. Int J Primatol. 1997;18(4):475–85. https://doi.org/10.1023/A:1026302920674.View ArticleGoogle Scholar
  55. Plumptre AJ. Monitoring mammal populations with line transect techniques in African forests. J Appl Ecol. 2000;37(2):356–68. https://doi.org/10.1046/j.1365-2664.2000.00499.x.View ArticleGoogle Scholar
  56. Stewart FA. The evolution of shelter: ecology and ethology of chimpanzee nest building. University of Cambridge; 2011. https://doi.org/10.17863/CAM.13968.
  57. Wrogemann D. Wild chimpanzees in Lope, Gabon: Census method and habitat use. Univ. Zugl.: Bremen; 1992. http://hdl.handle.net/11858/00-001M-0000-0012-72D1-8.
  58. Thomas L, Buckland ST, Rexstad EA, Laake JL, Strindberg S, Hedley SL, Bishop JR, Marques TA, Burnham KP. Distance software: design and analysis of distance sampling surveys for estimating population size. J Appl Ecol. 2010;47(1):5–14. https://doi.org/10.1111/j.1365-2664.2009.01737.x.View ArticlePubMedPubMed CentralGoogle Scholar
  59. Grossmann F, Hart JA, Vosper A, Ilambu O. Range occupation and population estimates of bonobos in the Salonga National Park: application to large-scale surveys of bonobos in the Democratic Republic of Congo. In: The Bonobos. Springer; 2008. p. 189–216. https://doi.org/10.1007/978-0-387-74787-3_11.
  60. McCoy J, Johnston K, institute Esr. Using ArcGIS spatial analyst: GIS by ESRI. Redlands: Environmental Systems Research Institute; 2001.Google Scholar
  61. Ling F, Du Y, Li X, Li W, Xiao F, Zhang Y. Interpolation-based super-resolution land cover mapping. Remote Sens Lett. 2013;4(7):629–38. https://doi.org/10.1080/2150704X.2013.781284.View ArticleGoogle Scholar
  62. Dutton PE. Chimpanzee (Pan troglodytes ellioti) ecology in a Nigerian montane forest. University of Canterburyy. 2012; 221.Google Scholar
  63. Dutton PE. Chimpanzee (Pan troglodytes ellioti) ecology in a Nigerian montane forest. 2012.Google Scholar
  64. Basabose AK, Yamagiwa J. Factors affecting nesting site choice in chimpanzees at Tshibati, Kahuzi-Biega National Park: influence of sympatric gorillas. Int J Primatol. 2002;23(2):263–82. https://doi.org/10.1023/A:1013879427335.View ArticleGoogle Scholar
  65. Koops K, Humle T, Sterck EH, Matsuzawa T. Ground-nesting by the chimpanzees of the Nimba Mountains, Guinea: environmentally or socially determined? Am J Primatol. 2007;69(4):407–19. https://doi.org/10.1002/ajp.20358.View ArticlePubMedGoogle Scholar
  66. Pruetz JD, Fulton S, Marchant LF, McGrew WC, Schiel M, Waller M. Arboreal nesting as anti-predator adaptation by savanna chimpanzees (Pan troglodytes verus) in southeastern Senegal. Am J Primatol. 2008;70(4):393. https://doi.org/10.1002/ajp.20508.View ArticlePubMedGoogle Scholar
  67. Tagg N, Willie J, Petre C-A, Haggis O. Ground night nesting in chimpanzees: new insights from central chimpanzees (Pan troglodytes troglodytes) in South-East Cameroon. Folia Primatol. 2013;84(6):362–83. https://doi.org/10.1159/000353172.View ArticlePubMedGoogle Scholar
  68. Humle T. Culture and variation in wild chimpanzee behaviour: a study of three communities in West Africa. University of Stirling; 2003.Google Scholar
  69. Blom A, Almaši A, Heitkönig I, Kpanou JB, Prins H. A survey of the apes in the Dzanga-Ndoki National Park, Central African Republic: a comparison between the census and survey methods of estimating the gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes) nest group density. Afr J Ecol. 2001;39(1):98–105. https://doi.org/10.1046/j.0141-6707.2000.00280.x.View ArticleGoogle Scholar
  70. Yamagiwa J. Factors influencing the formation of ground nests by eastern lowland gorillas in Kahuzi-Biega National Park: some evolutionary implications of nesting behavior. J Hum Evol. 2001;40(2):99–109. https://doi.org/10.1006/jhev.2000.0444.View ArticlePubMedPubMed CentralGoogle Scholar
  71. Koops K, McGrew WC, Matsuzawa T, Knapp LA. Terrestrial nest-building by wild chimpanzees (Pan troglodytes): implications for the tree-to-ground sleep transition in early hominins. Am J Phys Anthropol. 2012;148(3):351–61. https://doi.org/10.1002/ajpa.22056.View ArticlePubMedPubMed CentralGoogle Scholar
  72. Dutton P, Chapman H. Dietary preferences of a submontane population of the rare Nigerian-Cameroon chimpanzee (Pan troglodytes ellioti) in Ngel Nyaki Forest Reserve, Nigeria. Am J Primatol. 2015;77(1):86–97. https://doi.org/10.1002/ajp.22313.View ArticlePubMedPubMed CentralGoogle Scholar
  73. Ban SD, Boesch C, N’Guessan A, N’Goran EK, Tako A, Janmaat KR. Taï chimpanzees change their travel direction for rare feeding trees providing fatty fruits. Anim Behav. 2016;118:135–47. https://doi.org/10.1016/j.anbehav.2016.05.014.View ArticleGoogle Scholar
  74. Hohmann G, Potts K, N’Guessan A, Fowler A, Mundry R, Ganzhorn JU, Ortmann S. Plant foods consumed by Pan: exploring the variation of nutritional ecology across Africa. Am J Phys Anthropol. 2010;141(3):476–85. https://doi.org/10.1002/ajpa.21168.View ArticlePubMedPubMed CentralGoogle Scholar
  75. Mitchell MW, Locatelli S, Clee PRS, Thomassen HA, Gonder MK. Environmental variation and rivers govern the structure of chimpanzee genetic diversity in a biodiversity hotspot. BMC Evol Biol. 2015;15(1):1. https://doi.org/10.1186/s12862-014-0274-0.View ArticlePubMedPubMed CentralGoogle Scholar
  76. Plumptre AJ. Eastern chimpanzee (Pan troglodytes schweinfurthii): status survey and conservation action plan, 2010–2020. Gland: IUCN; 2010. https://doi.org/10.1007/s10980-008-9231-x.View ArticleGoogle Scholar
  77. Duvall CS. Human settlement ecology and chimpanzee habitat selection in Mali. Landsc Ecol. 2008;23(6):699–716. https://doi.org/10.1007/s10980-008-9231-x.View ArticleGoogle Scholar
  78. Junker J, Blake S, Boesch C, Campbell G, Toit LD, Duvall C, Ekobo A, Etoga G, Galat-Luong A, Gamys J. Recent decline in suitable environmental conditions for African great apes. Divers Distrib. 2012;18(11):1077–91. https://doi.org/10.1111/ddi.12005.View ArticleGoogle Scholar
  79. Eniang E, Ijeomah H, Okeyoyin G, Uwatt A. Assessment of human–wildlife conflicts in Filinga range of Gashaka Gumti National Park, Nigeria. Prod Agric Technol J. 2011;1:15–35.Google Scholar

Copyright

© The Author(s) 2018

Advertisement