ORIGINAL ARTICLE

The effect of canopy closure on chimpanzee nest abundancein Lagoas de Cufada National Park, Guinea-Bissau

Joana Sousa • Catarina Casanova • Andre V. Barata •

Claudia Sousa

Received: 18 March 2013 / Accepted: 10 December 2013

� Japan Monkey Centre and Springer Japan 2014

Abstract The present study aimed to gather baseline

information about chimpanzee nesting and density in Lagoas

de Cufada Natural Park (LCNP), in Guinea-Bissau. Old and

narrow trails were followed to estimate chimpanzee density

through marked-nest counts and to test the effect of canopy

closure (woodland savannah, forest with a sparse canopy, and

forest with a dense canopy) on nest distribution. Chimpanzee

abundance was estimated at 0.79 nest builders/km2, the

lowest among the areas of Guinea-Bissau with currently

studied chimpanzee populations. Our data suggest that sub-

humid forest with a dense canopy accounts for significantly

higher chimpanzee nest abundance (1.50 nests/km of trail)

than sub-humid forest with a sparse canopy (0.49 nests/km of

trail) or woodland savannah (0.30 nests/km of trail). Dense-

canopy forests play an important role in chimpanzee nesting

in the patchy and highly humanized landscape of LCNP. The

tree species most frequently used for nesting are Dialium

guineense (46 %) and Elaeis guineensis (28 %). E. guine-

ensis contain nests built higher in the canopy, while

D. guineense contain nests built at lower heights. Nests

observed during baseline sampling and replications suggest

seasonal variations in the tree species used for nest building.

Keywords Chimpanzee � Marked-nest counts �Estimating density � Canopy closure � Lagoas de Cufada

Natural Park

Introduction

The western chimpanzee (Pan troglodytes verus) is reported

to exist in southern Guinea-Bissau (Gippoliti and Dell’Omo

1996; Casanova and Sousa 2005; Sousa et al. 2005), and the

species has been repeatedly reported in the Lagoas Cufada

Natural Park (LCNP) (Crawford-Cabral and Verıssimo 1997;

Gippoliti and Dell’Omo 2003; Gippoliti et al. 2003; Kar-

ibuhoye 2004; Sousa et al. 2005; Casanova and Sousa 2007b).

Lagoas de Cufada Natural Park is located in a patchy

landscape of mangrove, savannah, and forest affected by

humans, and chimpanzees have been described as making

differential use of these different habitats. In Cantanhez

National Park (CNP) in the south of Guinea-Bissau, chim-

panzees frequently nest in forest edges (Sousa et al. 2011).

Other chimpanzee populations, notably those in Haut Niger

National Park, Guinea-Conakry, have been described as nest-

ing frequently in gallery forests (Fleury-Brugiere and Brugiere

2010), and near fleshy-fruit trees in Kibale National Park,

J. Sousa � C. Sousa (&)

Departamento de Antropologia, Faculdade de Ciencias Sociais e

Humanas (FCSH), Universidade Nova de Lisboa, Av. Berna,

26-C, 1069-061 Lisbon, Portugal

e-mail: csousa@fcsh.unl.pt

J. Sousa

Oxford Brookes University, Oxford, UK

J. Sousa � C. Casanova

Centre for Environmental and Marine Studies (CESAM), Faculty

of Sciences of Lisbon University, Lisbon, Portugal

J. Sousa � C. Sousa

Centre for Research in Anthropology (CRIA), Lisbon, Portugal

C. Casanova

CAPP-Instituto Superior de Ciencias Sociais e Polıticas da

Universidade Tecnica de Lisboa, Lisbon, Portugal

C. Casanova

Unidade de Antropologia, Instituto Superior de Ciencias Sociais

e Polıticas (ISCSP) da Universidade Tecnica de Lisboa, Lisbon,

Portugal

A. V. Barata

University of Stirling, Stirling, UK

123

Primates

DOI 10.1007/s10329-013-0402-2

Uganda (Balcomb et al. 2000). On Mt. Assirik, Senegal,

chimpanzees nest in a wide array of environments, from gal-

lery forests to woodlands and grasslands (Baldwin et al. 1982).

Similarly, in Kalinzu Forest, Uganda, chimpanzees use both

logged and unlogged forest and regularly nest very close to

human compounds (Hashimoto 1995). The present study was

performed with several aims in mind. First, we wished to

obtain quantitative information on chimpanzee density in an

area where no survey had been carried out before. Alongside

and similarly to the studies mentioned above, we also studied

the effect of habitat type (woodland savannah, sparse canopy

forest, dense canopy forest) on the distribution of chimpanzee

nests and the chimpanzees’ selection of tree species for nesting.

Methods

Study area

The LCNP is located in southwestern Guinea-Bissau, in

the Quinara region, and includes parts of the

administrative sectors of Buba and Fulacunda (Fig. 1).

These two cities are the main urban centers in the region,

and they mark the western and eastern limits of the park,

respectively. From Buba to Fulacunda, there is a wide

unpaved road that divides the park into northern and

southern parts. The LCNP covers an area of 700 km2

(Martins and Catarino 2001) and is located between the

latitudes 11�340N and 11�510N and the longitudes

14�490W and 15�160W (PNLC 2011). In 1994, there were

34 villages in LCNP (Araujo 1994), and the latest census

indicates that the park has a human population of 3,534

inhabitants (IBAP 2007).

The park’s climate, due to the marine influence, is

characterized by only small fluctuations in temperature

(both daily and seasonal) and an annual average tempera-

ture of 26 �C. The average rainfall measured for Buba

(within the limits of LCNP) from 1960 to 1999 was esti-

mated to be 1,797 mm/year (INEC cited in Sanches et al.

2003), with a very distinct rainy season spanning from June

to October (Catarino 2002). The altitude in the area of

LCNP does not exceed 40 m.

Fig. 1 Studied trails and land cover (INEP) for Lagoas de Cufada

Natural Park: subhumid forests and oil-palm groves; dry and semi-dry

forests; woodland savannas (based on the INEP classification; it

should be noted that a considerable area identified as subhumid forest

actually consists of cashew orchards)

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123

Sparse canopy forests are the dominant type of habitat,

and are characterized by species such as Parkia biglobosa,

Pterocarpus erinaceus, Erythrophleum spp., Parinari spp.,

Daniellia oliveri, Prosopis africana, Piliostigma thonnin-

gii, Lophyra alata, Khaya senegalensis, Borassus aethio-

pum, and Ficus spp. (Martins et al. 1998). Other types of

habitat in the park include: (1) riverine forests, where some

tree species present adaptations to flooding, such as sup-

porting roots; (2) savannahs that are periodically flooded

with fresh water; (3) mangroves populated with halophytic

species, such as Avicennia sp., Rhizophora sp., Terminalia

sp., Conocarpus sp.; (4) oil-palm groves, and; (5) aquatic

vegetation of lagoons (Martins et al. 1998). Although there

are recent cartographic data that include land-use infor-

mation (Catarino 2002), there are no recent estimates of the

areas occupied by the different habitats. Based on SCET

international land-cover images from 1978, Araujo (1994)

estimated that habitat cover was as follows: dense sub-

humid forests, 102 km2; sub-humid forest with sparse

canopy, 115 km2; and savannah with sparse tree cover,

160 km2; among others. In 1993, BISSASIG-Celula Sig/

INEP/GPC described approximately 135 km2 of dense sub-

humid forests (Salgado et al. 2009).

In 2009, a private enterprise began the construction of a

deepwater port that will occupy 70 km2 in an area of dense

sub-humid forest inside the park. According to the park

management plan (PNUD 2000), this area was designed to

be under ‘‘full protection.’’ Considering the total area

covered by sub-humid forests (135.46 km2), 51.7 % of this

area will potentially be deforested by the project (Salgado

et al. 2009). The deforestation that occurred in 2009, the

impact of constructing the port, and the changes resulting

from its operation will probably transform the social and

ecological environment. The present study, carried out in

2007, is important as a basis for future comparative studies

of chimpanzee distribution within LCNP and for making

inferences about the impact of these major habitat distur-

bances on wild populations.

Other primate species, such as Campbell’s monkey

(Cercopithecus campbelli), the green monkey (Chloroce-

bus sabaeus), the patas monkey (Erythrocebus patas), the

Guinea baboon (Papio papio), and the West African red

colobus (Procolobus badius), are also present in LCNP

(Karibuhoye 2004).

Data collection

Data were collected from late September to December

2007. In LCNP, baboons and other monkeys are hunted

both for food and the pet trade (Casanova and Sousa 2005,

2006; Silva 2012), as well as for their skins, which are used

in traditional medicine (Sa et al. 2012), with their products

being both used locally and sent to urban markets in

Guinea-Bissau (Casanova and Sousa 2005, 2006; Silva

2012). Although chimpanzees are not a target species for

hunting, we chose to rely on methodological approaches

that guaranteed our study would neither enhance hunting

intensity nor the bushmeat trade. Therefore, like other

studies (Ihobe 1995; Hall et al. 1998; Fashing and Cords

2000), our study followed a non-ideal technique for esti-

mating chimpanzee densities.

Although, as a non-random sampling approach, the use

of paths to estimate densities represents poor sampling in

the majority of circumstances (Buckland et al. 2001; Kuhl

et al. 2008), other issues have to be considered when

making methodological choices. Fashing and Cords (2000)

used existing trails in their study area in order to follow the

local policy of avoiding opening of new paths in the forest,

and assumed that chimpanzees were at least partially

habituated to the trails and human presence.

Plumptre and Cox (2006) found that the encounter rates

per km walked on recces could be correlated with the

densities obtained from transects. It was also shown that

the use of new trails (as linear transects) may influence

spatial use and cause avoidance by chimpanzees (Plumptre

and Reynolds 1997). Moreover, if the trails are frequently

used by people, chimpanzees tend to avoid nesting nearby,

but if they are rarely used by people and not obviously

opened, the affect of the trail on chimpanzee nesting was

minimized (Plumptre and Reynolds 1997).

Our study relied on chimpanzee nest counting along

existing trails. Since people in the area practice shifting

agriculture, many trails are opened to provide access to

farms. These can be abandoned after harvest or they can be

used for different purposes (e.g., providing access to the

mangrove or small rivers, hunting and collection of wild

foods such as palm-oil sap, Borassus aethiopum sap).

Given that the chimpanzee is not a target species for

hunting (Gippoliti and Dell’Omo 2003; Casanova and

Sousa 2007a), we assumed this to have no effect on nest

distribution. These trails were followed as linearly as

possible in order to estimate chimpanzee density by nest

counting. In order to mitigate the effect of non-random-

ness, all known trails were used and there were no selection

criteria.

This study adopted the ‘‘marked nest counts’’ method to

collect data in order to (1) test the effect of canopy closure

on nest abundance and (2) estimate chimpanzee nest den-

sity. Prior to data collection, a baseline sampling marked

all standing nests along the studied trails and recces. This

was followed by four sampling replications carried out at

15-day intervals. The marked nest counts method assumes

that the objects located above the sampling line were

always detected (with a detection probability of 100 %),

while the others were detected with a probability that

depended on the perpendicular distance to the transect

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123

(Buckland et al. 2001; Plumptre and Cox 2006). Therefore,

for each detected nest, the perpendicular distance from the

nest to the trail was measured with a tape. Whenever

canopy density allowed it, nest heights were measured with

a rangefinder (Bushnell Yardage Pro Sport 450), and the

tree species bearing the nest was identified.

The density of chimpanzee nests was estimated using

the DISTANCE 5.0 software package (Thomas et al.

2010), as it has been used for estimating densities of pri-

mates in other studies (Plumptre 2000; Bennett et al. 2001;

Furuichi et al. 2001; Dupain et al. 2004; van Schaik et al.

2005; Morgan et al. 2006).

The advantage of the marked nest counts method is that

the nest decay rate is replaced by the period of time

between two consecutive replications (Plumptre and Rey-

nolds 1996), which was 15 days in our study. As the nest

production rate had not yet been estimated anywhere in

Guinea-Bissau, we used a nest production rate of 1.09 nests

built per individual per day, as estimated for Budongo

forest, Uganda (Plumptre and Reynolds 1997) and used in

other studies estimating densities of unhabituated chim-

panzees (Morgan et al. 2006; Plumptre and Cox 2006; Sanz

et al. 2007). Considering that there is no estimate for the

proportion of infants in the chimpanzee populations of

Guinea-Bissau, we will present our results in nest builders/

km2. The density estimation will be based on the formula

Dnest�builders ¼ D ¼ n=½2wLPPnI�; where D is the estimated

density of the individuals, n is the number of nests detec-

ted, 2w is the transect width, L is the length of the transect,

P is a function expressing the probability of detection at

different distances, Pn refers to the nest production rate

(1.09 nests/day/individual, adopted from Budongo), and

I refers to the number of days between samplings (15 days

for this study). Nest detection probability was determined

using nest distance data from all repetitions.

Each trail was classified in accordance with the predom-

inant habitat that it crosses, following the categories pro-

posed by Catarino (2002): forest with dense canopy, forest

with sparse canopy, or woodland savannah. The categories of

forest with dense and sparse canopies were distinguished by

the structure of the strata (herbaceous, shrub-like, and tree-

like). A total of 192.95 km of trails were sampled during one

baseline sampling and four replications. The sampled trails

were distributed across different habitats, but the ratios do

not express the proportions in which they occur within

LCNP. Excluding the km followed during the baseline

sampling, and considering exclusively the four repetitions

conducted when sampling new nests, we followed 37.20 km

in woodland savannah, 78.04 km in forest with dense canopy

cover, and 39.12 km in forest with sparse canopy cover, or a

total of 154.36 km.

The model of detection probability produced from the

detection distances with the DISTANCE software was

chosen using different criteria: Akaike’s information cri-

terion (AIC), an indicator of simplicity and parsimony;

GOF/w2, to estimate the model adjustment; and the coef-

ficient of variation (CV) (Sokal and Rohlf 1995). Another

criterion is the visual appreciation of the detection proba-

bility curve, which should have a plateau at low distances

from the sampling line where the derivative of the proba-

bility at distance 0 m is g(0)0 = 0; here, g is the detection

probability (Buckland et al. 2001).

Data normality was tested with the Shapiro–Wilk test

(Hill and Lewicki 2006). As in similar previous studies

(Brownlow et al. 2001; Furuichi and Hashimoto 2004;

Matthews and Matthews 2004), the fact that the data are

non-normally distributed demanded the use of nonpara-

metric methods: the Kruskal–Wallis test was used to check

for significant differences between the three habitats

regarding nest detection rate and detection distances (Hill

and Lewicki 2006). The nonparametric Tukey HSD test

was used as a post hoc test for multiple comparisons.

The number of detected nests per km was used to

compare the different habitats and replications. The chi-

square test was used to evaluate the effect of canopy clo-

sure categories on nest frequency. Since the sampling effort

was not the same for each category of canopy closure, the

data were transformed as follows: F0WS ¼ ðFWS=LWSÞ=LT; F0DF ¼ ðFDF=LDFÞ=LT; F0SF ¼ ðFSF=LSFÞ=LT; where F0

refers to the transformed frequency of nests, F refers to the

original frequency of nests, and L refers to the length of the

trails in meters (LT refers to the overall length of trails). As

for the indices, they are WS for woodland savannah, DF for

forest with dense canopy cover, and SF for forest with

sparse canopy cover.

The overall density of chimpanzees was estimated taking

into account the heterogeneity of the nest detection rate

across the different habitat strata, and was calculated as

follows: D ¼ DWSðAWS=ATÞ þ DDFðADF=ATÞ þ DSFðASF=

ATÞ; where D refers to chimpanzee density (individuals/

km2); A refers to area (km2); and AT is the total area. The

same estimates for land use proposed by Araujo (1994) were

also used to estimate chimpanzee density, considering the

proportion of area occupied by each habitat within LCNP.

All statistical analyses were performed using the

STATISTICA 6.0 software package (StatSoft 2003),

assuming a significance level of 0.05.

We also registered other evidence of chimpanzees’ pre-

sence—such as footprints, vocalizations, and sightings—

which were descriptively considered against habitat type.

The scientific names of tree species bearing nests were

translated from the local languages (Creole, Balanta, and

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Beafada) using the floral field guide to Guinea-Bissau

(Catarino 2006). Identification of tree species was based on

the knowledge of skilled field assistants together with the

experience of the first and third authors in previous field

work of this kind. The field assistants were adults (around

30–50 years old), all with some previous experience in

assisting animal and plant ecology studies. This research

was conducted in compliance with Primate Society of

Japan guidelines for ethical treatment of primates. The

study used exclusively noninvasive methods and was based

on indirect evidence of presence—principally chimpanzee

nests. Therefore, the potential risks to chimpanzees or other

primate species were minimal. Moreover, as stated before,

conservation and animal welfare aims were prioritized over

the adoption of the most adequate sampling strategy.

Additionally, we state that all legal requirements of the

governmental agency that regulates research in protected

areas in Guinea-Bissau were fulfilled.

Results

During this study, 312 chimpanzee nests were encountered,

151 of which were detected during the baseline sampling,

with the remaining 161 registered from the first to the

fourth replications. Nests counted during the baseline

sampling were referred to as standing nests, and those

counted during replications were thereby designated new

nests.

The numbers of new nests detected in the four replica-

tions were not significantly different (Kruskal–Wallis:

H = 0.55, P = 0.91). In the first replication, the average

new nest detection rate was 0.69 nests/km of trail, in the

second it was 1.08 nests/km, in the third it was 0.73 nests/

km, and in the fourth it was 1.58 nests/km.

Regarding the trails studied, while the chimpanzee nests

seemed to be widely distributed in LCNP, nests were more

frequently encountered along certain trails. Considering the

overall number of nests found per repetition, the nest

detection rate was the highest for trails crossing sub-humid

forest with a dense canopy (1.50 nests/km), lower in forest

with a sparse canopy (0.49 nests/km), and lowest in

woodland savannah (0.30 nests/km). The categories of

canopy closure had a significant effect on nest abundances.

The nest detection rates were different for the three habitats

(Kruskal–Wallis; H = 6.04, P \ 0.05). The nonparametric

post-hoc Tukey HSD (for P \ 0.05) revealed significantly

different nest detection rates for savannah and dense-can-

opy forests (Fig. 2).

The distances at which nests were detected were not

normally distributed for woodland savannah and forest

with a dense canopy (Shapiro–Wilk: woodland savannah

W = 0.88, P \ 0.05; dense forest W = 0.92, P \ 0.05);

while, in forest with a sparse canopy, nest detection

distances were normally distributed (W = 0.94,

P = 0.105). The Kruskal–Wallis revealed significant

differences in nest detection distance among the three

categories (Kruskal–Wallis; H = 36.96, P \ 0.01). The

nonparametric post-hoc Tukey HSD (for P \ 0.05)

revealed significantly different nest detection distances

when either of the other two habitats was compared to

savannah (Fig. 2).

The model that best fit the data for the three habitats was

the hazard-rate/cosine with distances grouped in 5 m

intervals. This model presented the best output for the three

criteria: AIC (584.24), coefficient of variation

(CV = 13.40 %), and v2 (P = 0.24). Data were truncated

at 45 m (w), the distance at which the detection probability

curve reached a plateau tending to zero, which excluded 14

nests, the largest distance of which was 111.85 m.

Fig. 2 Distributions of nest detection distance (N = 266, on the left) and the average number of nests detected per km per repetition (N = 12, on

the right). Nonparametric post hoc tests results are shown, and points labeled with the same letter are not significantly different (P \ 0.05)

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123

The estimated chimpanzee density in woodland savan-

nah was 0.29 nest builders/km2. In forest with a sparse

canopy, it was 0.64 nest builders/km2, while in dense-

canopy forest it was 1.77 nest builders/km2. The weighted

average of chimpanzee density for the three habitats was

0.79 (0.61–1.04; c.i. 95 %) nest builders/km2 or a total of

300 (230–390 c.i. 95 %) individuals that were able to build

nests, considering both the significantly different distribu-

tions of nests in the studied habitats and the areas occupied

by each habitat type (according to Araujo 1994).

The species of trees used for nesting observed during the

baseline sampling and repetitions were different. During

baseline sampling, the nests were most frequently built in

Elaeis guineense, while the Dialium guineense was the

most frequently used species during the repetitions

(Table 1).

The nest heights varied between 4 m in Newbouldia

laevis and 38 m in Ceiba pentandra. The average nest

height was 16.08 ± 5.21 m (N = 164). The nests in Dia-

lium guineense were built at considerably lower heights

than in other species, corresponding to an average height of

12.80 ± 3.86 m (N = 73 nests). On the other hand, nests

in oil palm (Elaeis guineensis) were built at an average of

20.11 ± 3.33 m (N = 49) and those in Azfelia africana at

18.55 ± 2.74 m (N = 25; Fig. 3). Ground nests were

never encountered.

Beyond nests, other evidence of presence (vocalizations,

sightings, and footprints) also revealed a higher frequency

of chimpanzee presence in dense-canopy forest than in the

other two habitat types. Hunting shells were found in both

dense- and sparse-canopy forests (Table 2), with a mini-

mum of 0 to a maximum of 3 shells per trail. In the four

trails where we counted the majority of nests, we found 0–3

shells per trail.

Discussion

Different habitats show different nest detection rates, and it

is essential to stratify the data to avoid bias. Differences in

nest detection in different habitats within the same land-

scape have also been reported in other studies (Hashimoto

1995; Ogawa et al. 2007; Hernandez-Aguilar 2009; Fleury-

Brugiere and Brugiere 2010; Sousa et al. 2011), and the

need to stratify according to the representativeness of dif-

ferent habitats has also been highlighted by others (Stokes

et al. 2010; Sousa et al. 2011).

The density estimated in our study included different

types of habitat, and the overall estimate was slightly lower

than that described by Sousa (2009) in the east of the

Table 1 Frequency (%) of the species used by chimpanzees for nest

building, as observed during the baseline sampling (standing nests)

and repetitions (new nests)

Species Baseline sampling

(standing nests)

Frequency (%)

Repetitions

(new nests)

Frequency (%)

Elaeis guineensis 45.21 28.57

Dialium guineense 19.86 46.58

Parinari excelsa 8.91 0.62

Spondias mombin 6.16 0.62

Afzelia africana 5.48 15.53

Newbouldia laevis 5.48 3.74

Parkia biglobosa 3.42 0.00

Detarium senegalense 1.38 1.86

Khaya senegalensis 1.38 0.62

Anisophyllea laurina 0.68 0.00

Ceiba pentandra 0.68 0.00

Milicia regia 0.68 0.00

Pterocarpus erinaceus 0.68 0.00

Xylopia aethiopica 0.00 0.62

Antiaris toxicaria 0.00 0.62

Albyzia zygia 0.00 0.62Table 2 Evidence of chimpanzees and of human hunting activity in

the habitat types studied

WS FSC FDC

Hunting shells 0 10 13

Footprints 0 1 2

Vocalizations 1 1 8

Sightings 1 0 3

WS woodland savannah; FSC forest with a sparse canopy, FDC forest

with a dense canopy

Fig. 3 Heights of chimpanzee nests built in Dialium guineense,

Elaeis guineensis, and Azfelia africana

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Tombali region (Guinea-Bissau), an area that also contains

different types of habitat. Our chimpanzee density estimate

for LCNP is also lower than the density estimates for

southern CNP in the same region (Sousa et al. 2011;

Hockings and Sousa 2013). The fact that chimpanzee

density is lower in LCNP than at these other sites in Gui-

nea-Bissau is probably associated with the composition of

tree species or forest cover, since chimpanzees are not

hunted for food at either site. Commercial chimpanzee

hunting has been described as having an important effect

on chimpanzee populations, such as in Gabon (Walsh et al.

2003), but this is not the case in LCNP or CNP.

The population estimate for forest with a dense canopy

in LCNP is unusually high (1.77 nest builders/m2) when

compared to other studies carried out in dense forests

(Marchesi et al. 1995; Blom et al. 2001; Beck and Chap-

man 2008), although lower than some extremely high

density sites (Fleury-Brugiere and Brugiere 2010; Sousa

et al. 2011; Hockings and Sousa 2013) (see Table 3).

However, our estimate of the chimpanzee population in

dense forests is within the range estimate of chimpanzees/

km2 that Morgan et al. (2006) describe for undisturbed

forests. Our estimate for woodland savannah (0.29 nest

builders/km2) is similar to densities estimated elsewhere

for the same kind of habitat (Pruetz et al. 2002; Fleury-

Brugiere and Brugiere 2010), which are generally smaller

than those for forested environments (see Table 3).

Encroached forests and mosaic habitats (Marchesi et al.

1995), young regenerating forests (Anderson et al. 1983),

and highly fragmented forests (McLennan 2008) all

correspond to lower chimpanzee densities, while dense

forests account for comparatively high chimpanzee density

estimates (Marchesi et al. 1995; Morgan et al. 2006)

(Table 3). Gallery forests and dry forests have been found

to be relevant to chimpanzee densities in environments

dominated by savannah (Fleury-Brugiere and Brugiere

2010), and this is similar to the role dense forests play in

chimpanzee density in LCNP. The presence of these forests

in LCNP allows for considerable chimpanzee density in a

landscape that includes different types of habitats. Logging

has been shown to have negative consequences for the

number of chimpanzees (Hicks et al. 2009), and therefore

the recent logging in the forests of LCNP, apparently for

the construction of the deep-water harbor, may have had a

considerable impact on the chimpanzee population.

Contrary to the situation described for the southern part

of CNP, where the oil palm is used more frequently for nest

construction, in LCNP, Dialium guineense appears to be

the tree species most frequently used for nesting; or at least

this was the case during the study period (September to

December), which corresponded to the end of the rainy

season and beginning of the dry season. As already high-

lighted by Sousa et al. (2011), care should be taken when

comparing the frequency of standing and new nests built in

different tree species, because different nest decay rates

affect the proportion of nests present in the sample of

standing nests. This does not allow for reliable compari-

sons, as tree species with the slowest nest decay rates are

overrepresented in the baseline sampling. Knowing the

decay rates of nests built in oil palms and in other tree

Table 3 Estimates of chimpanzee density in different types of habitat in West and Central Africa

Name and field site Vegetation type Density

(chimps/km2)

Source

Cantanhez National Park, Guinea-Bissau Cadique-Caiquene forest fragments 3.00 Hockings and Sousa (2013)

Northest of Tombali region, Guinea-Bissau Heterogeneous forests 0.90 Sousa (2009)

Assirik area of Niokolo Koba National Park and

vicinities of the park

Woodland savannah 0.13 Pruetz et al. (2002)

Haut Niger National Park, Republic of Guinea Dry forests and gallery forests 2.16; 5.97 Fleury-Brugiere and

Brugiere (2010)Woodland savannah 0.29

Sapo Forest, Liberia Primary and regenerating forests 0.24 Anderson et al. (1983)

Taı National Park, Cote d’Ivoire Human-encroached forests and

mosaic habitat

0.09 Marchesi et al. (1995)

Degraded forests 0.40

Intact primary forests 1.64

Forest of Ngel Byaki Forest Reserve, Nigeria Dense forests 1.67 Beck and Chapman (2008)

Tschego, southwestern Congo Evergreen forests with different

hunting pressures

0.27 Ihobe (1995)

Goualougo Triangle, Republic of Congo Undisturbed forests 1.53–2.23 Morgan et al. (2006)

Dzanga-Ndoki National Park, Central African

Republic

Dense forests 0.16 Blom et al. (2001)

Bulindi, Hoima District, Uganda Small forest fragments 0.66 McLennan (2008)

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123

species would allow the use of the standing crop method in

Guinea-Bissau for the estimation of chimpanzee densities.

Moreover, particularly in contexts such as LCNP, where

oil-palm nests are well represented, site-specific estimates

of nest decay rates are important. Nest decay rates vary

considerably and are influenced by tree species, shade,

moisture (Ihobe 2005), seasonality, and vegetation type

(Zamma and Makelele 2012). Considering only the

standing nests, the Elaeis guineensis (oil palm) is more

frequently used than Dialium guineense. However, as

mentioned above, this could be a consequence of a slower

decay rate for nests in oil palms. New nests were mainly

found in Dialium guineense, Elaeis guineensis, and Afzelia

africana.

Standing nests were exclusively found in three species

(Spondias mombin, Parkia biglobosa, Khaya senegalensis),

and new nests were exclusively found in seven others

(Xylopia aethiopica, Anisophyllea laurina, Antiaris toxi-

caria, Pterocarpus erinaceus, Ceiba pentandra, Albizia

zygia, Milicia regia). These differences could be related to

seasonal variation, as the nests observed during baseline

sampling had been built during the rainy season, and the

new nests were built in the dry season. There is not, as yet,

an ecological or behavioural explanation for the species

used for nest building.

In the forested areas of both CNP and LCNP, all of the

trees species mentioned above are present (Catarino 2004),

and Dialium guineense and Elaeis guineensis were most

frequently selected for nesting (Sousa et al. 2011). These

species are also important as food for chimpanzees: Dia-

lium guineense is described as a chimpanzee food in

Bossou (Republic of Guinea) (Sugiyama and Koman 1987)

and in CNP (Guinea-Bissau) (Hockings and Sousa 2013),

and Elaeis guineensis has been so described in Bossou. The

local people in CNP also describe chimpanzees feeding on

flowers, fruit, and the petioles of the leaves of Elaeis

guineensis (Sousa et al. 2013). Chimpanzee nesting pref-

erences in Kibale (Uganda) have been described as being

associated with fruit availability (Balcomb et al. 2000).

Upon studying several tree species in West Africa (Cote

d’Ivoire), Polansky and Boesch (2013, p 438) found that,

except for Dialium guineense and Elaeis guineensis, all

species ‘‘show a significant intra-annual smooth term

describing either regular or biannual fluctuations in fruiting

presence.’’ A study of fructification by Polansky and Bo-

esch (2013) allows us to suggest that chimpanzees could be

paying special attention to Dialium guineense and Elaeis

guineensis because of their unpredictable fructification.

Therefore, the high frequency of nest building in these tree

species could be a consequence of frequent monitoring of

fruit availability. However, other factors have been pre-

sented as explanations of nesting preferences, such the high

density of foliage on branches, which provides a good

substrate for nest building (Brownlow et al. 2001).

Therefore, a study of forest species fructification and

foliage characteristics, among other features, as well as of

chimpanzee diet in both LCNP and CNP, could shed light

on the leading factors that influence nesting choices. We

also suggest that the higher frequency of nests found in

Elaeis guineensis in CNP than in LCNP may be linked to

the greater availability of that species; but again quantita-

tive and comparative studies on tree availability are

missing.

Evidence of human hunting practices was identified in

both sparse- and dense-canopy forests. It is not possible to

infer the presence of hunting practices in the savannah

woodland without more information on hunting techniques

(such as those using fire). The four transects where we

counted high frequencies of chimpanzee nests corre-

sponded to trails where we found either no shells or the

maximum number of shells per trail. Although more

research is needed to be able to discuss the influence of

using pre-existing trails to estimate distance, our data do

not contradict the hypothesis that chimpanzees are

accustomed to the trails followed in this study, and pos-

sibly to hunting activities that do not impact on

chimpanzees.

As a final note, taking into account the chimpanzees’

preference for forested areas, it is important to highlight the

need to avoid permanent deforestation of the densely for-

ested areas associated with the construction of the deep-

water port in order to maintain chimpanzee population

densities in the LCNP.

Acknowledgments This study was developed within the project

‘‘Chimpanzee distribution and relation with local human communities

in coastal area of Guinea-Bissau’’ PPCDT/ANT/57434/2004, funded

by the Foundation for Science and Technology, Portugal, and was

conducted within the framework of the Dari Project. The authors

would like to thank IBAP (Institute of Biodiversity and Protected

Areas of Guinea-Bissau) for the logistical and administrative support,

to Honorio Fernandes Pereira, the Director of the LCNP, and to INEP

(National Institute of Studies and Research). We are also grateful to

Jeremy Huet and Joana Silva for their support with GIS information.

Thanks are also due to Musa Mane, Umaru Cande, Bacari Sanha,

Agostinho N’fanda, Bafode Mane, Abu Dabo, and Benjamim Indec

for helping the first and third authors during data collection. Many

thanks to Joost van Schijndel for carefully commenting on this paper

and for his patience as a reviewer, to Joana Carvalho for her insights

on this draft, and to Diana Alcantara for performing a final revision of

the first version. Thanks are due too to Cristina Santos and Ricardo

Ramos for insights concerning some of the statistical analysis. Great

thanks go to Justo Nadum for his great capacity to mobilize and

organize people and work, and to Idrissa Camara for his support.

Further thanks are due to Duana Namfe, Maria and Alfredo Naw-

guale, comrades in everyday life, to Marina Correia for her care, and

to Cristina Silva for her organizational efforts and conversations.

Finally, we acknowledge Yan Overfield Shaw for proofreading the

final version of the manuscript.

Primates

123

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