the effect of canopy closure on chimpanzee nest abundance in lagoas de cufada national park,...
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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: [email protected]
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)
Primates
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
Primates
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
Primates
123
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)
Primates
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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123
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)
Primates
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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