Chimpanzee oil-palm use in southern Cantanhez National Park, Guinea-Bissau

American Journal of Primatology 73:485–497 (2011)

RESEARCH ARTICLE

Chimpanzee Oil-Palm Use in Southern Cantanhez National Park, Guinea-Bissau

JOANA SOUSA1– 3�, ANDRE V. BARATA2,4, CLAUDIA SOUSA3,5, CATARINA C.N. CASANOVA2,6, AND LUIS VICENTE2,7

1Oxford Brookes University, Oxford, United Kingdom2Centre for Environmental Biology (CBA), Lisbon, Portugal3Centre for Research in Anthropology (CRIA), Lisbon, Portugal4University of Stirling, Stirling, Scotland5Faculdade de Ciencias Sociais e Humanas (FCSH) da Universidade Nova de Lisboa, Lisboa, Portugal6CAPP, Instituto Superior de Ciencias Sociais e Polıticas da Universidade Tecnica de Lisboa, Lisboa, Portugal7Faculdade de Ciencias da Universidade de Lisboa (FCUL), Lisboa, Portugal

Cantanhez National Park in southern Guinea-Bissau is a mosaic of forest, mangrove, savanna, andagricultural fields, with a high prevalence of oil-palm trees (Elaeis guineensis). It hosts many differentanimal species, including the chimpanzee (Pan troglodytes verus). Very little is known about the ecologyof chimpanzees inhabiting this area. The main aims of this study were to evaluate chimpanzee nestingbehavior, define trends of habitat use, and estimate chimpanzee density in four separate forests byapplying the marked nest counts methodology. From the 287 new nests counted, 92% were built in oil-palm trees with a significantly higher frequency of nests in the forest edge than in forest cores.Differences in nest detection rates were observed in the four monitored forests, with two forests beingmore important for chimpanzee’s nesting demands. The number of nests documented in the forestsseemed to be correlated with the frequency of other signs of chimpanzee activity. Althoughchimpanzees selected nests on the forest edge, they were most frequently observed in forest coreareas. Constraints associated with estimating chimpanzee density through oil-palm nest counting arediscussed. Am. J. Primatol. 73:485–497, 2011. r 2011 Wiley-Liss, Inc.

Key words: chimpanzee; oil-palm; habitat selection; nesting ecology; Cantanhez National Park

INTRODUCTION

The preferred areas for chimpanzee nestingseem to reflect the general patterns of habitat use[Morgan et al., 2006]. Factors influencing thosepatterns include: (i) forest composition [Chapmanet al., 1995; Oates, 2006]; (ii) habitat structure[McGrew, 1992; Sept et al., 1992], (iii) food avail-ability [Plumptre & Cox, 2006; Sept et al., 1992],specifically, the occurrence of trees that are used as afood source [Basabose & Yamagiwa, 2002; Goodall,1986; Stanford & O’Malley, 2008], (iv) predation risk,and (v) human disturbance [Humle & Matsuzawa,2004]. Usually, nests are more abundant in lessdisturbed forests [Marchesi et al., 1995] or in areasthat offer a wider view over the surrounding land-scape [Kortlandt, 1992]. Additionally, chimpanzeenest height might be affected by habitat type [Fruth& Hohmann, 1996:230], predation [Kortlandt, 1992;Pruetz et al., 2008], and climatic conditions[Ham, 1998].

In Bossou (Guinea) [Yamakoshi, 1998], Gombe(Tanzania) [Goodall, 1962] and Kanfarande (north-west coast of Guinea) [Leciak et al., 2005] chimpan-zees are known to rely on oil-palm as a food source,especially during periods of food scarcity. Additionally,chimpanzee oil-palm nests have been described by

several authors [De Bournonville, 1967; Gippoliti &Dell’Omo, 1996; Goodall, 1962; Ham, 1998; Kortlandt,1996].

Oil-palms have spread through both naturaldispersion and human activities in the Holocene[Sowunmi, 1999] and grow in a wide variety ofhabitats, such as secondary, gallery, and dry forests,savanna, fresh water swamp forests, and on themargins of rainforests and savanna [Janick, 2002;Sowunmi, 1999]. In southern Guinea-Bissau, peopleare known to save this species, along with otherspecies like Ceiba pentandra, from forest vegetationclearing for upland farming [Temudo, 1998].

The northwestern coast of Guinea has a highconcentration of oil-palms [Leciak et al., 2005], andHam [1998] reported that 44% of chimpanzee nests

Published online 21 January 2011 in Wiley Online Library (wileyonlinelibrary.com).

DOI 10.1002/ajp.20926

Received 25 May 2010; revised 17 November 2010; revisionaccepted 20 December 2010

Contract grant sponsor: FCT (Fundac- ao para a Ciencia e aTecnologia, Portugal) and FEDER.

�Correspondence to: Joana Sousa, Rua de Santo Antonio 56,Sao Bernardino, 2525-763 Atouguia da Baleia, Portugal.E-mail: [email protected]

rr 2011 Wiley-Liss, Inc.

in Guinea were built by this species. However, in1967, De Bournonville reported just one oil-palmnest for the northwest coast of Guinea [1967],which might suggest that this preference for usingoil-palm trees for nesting can be a recent trait[Humle, 2003].

McGrew [1992] pointed out that oil-palm use canreflect patterns of material culture among chimpan-zee communities, where there is a considerablevariation in the extent to which different commu-nities use and consume different oil-palm parts[Humle & Matsuzawa, 2004]. Descriptions of aPortuguese Jesuit priest, Manuel Alvares, aboutSierra Leone chimpanzees in the 16th- and 17th-century, report the use of oil-palm for feeding, aswell as nut-cracking. Although he describes chim-panzee nests in trees, there is no reference tooil-palm nests [Sept & Brooks, 1994]. In Bossou(southern Guinea), chimpanzees have been con-firmed to use oil-palms for nesting and feeding since1976 [Humle & Matsuzawa, 2004; Yamakoshi, 1998].However, chimpanzees inhabiting the Nimba moun-tains, just 6 km from Bossou, never use oil-palm fornesting or feeding, even though it is available[Humle, 2003]. In Mt. Assirik (Senegal), there is noevidence that chimpanzees use the oil-palm fornesting, despite the tree’s presence in accessibleriverine corridors [McGrew, 1992]. In Kanfarande(Guinea), oil-palms grow in high densities in theforest-mangrove edge, in gallery forests, and inwoodland savanna, and they are the most commonlyused trees for nesting [Leciak et al., 2005].

Previous qualitative studies have described thewidespread presence of oil-palm nests in southernGuinea-Bissau [Casanova & Sousa, 2005; Gippoliti &Dell’Omo, 1996; Sousa, 2005], but systematic dataare lacking. The western chimpanzee (Pan troglo-dytes verus) occurs in Cantanhez and Cacine basin[Gippoliti & Dell’Omo, 2003; Sousa et al., 2005], inQuinara region (particularly in Cufada NaturalReserve, located 17 km northeast of CantanhezNational Park), and in Boe Region, spanning 70 kmto the east of Cantanhez National Park [Gippoliti &Dell’Omo, 2003; Gippoliti et al., 2003; Sousa et al.,2005]. Gippoliti et al. [2003] have roughly estimatedthe population at 600–1,000 individuals for theseregions. Recently, the presence of the species,previously unreported in the north of Corubal river,was described to extend up to the north margin ofthis river [Brugiere et al., 2009].

There is a lack of primatological studies forCantanhez National Park and very little is knownabout local hunting practices. Chimpanzees are nothunted for meat [Brugiere et al., 2009; Gippolitiet al., 2003], although there is an illegal tradenetwork from the southern region (Boe province,Quinara and Tombali Regions) to Bissau for pettrade [Casanova & Sousa, 2006]. This fact does not

make this species a target of human persecution,however, particularly in Cantanhez forests.

This study aims to evaluate chimpanzee nestingbehavior, characterize general patterns of habitatuse, estimate the density of weaned individualsnesting in four southern Cantanhez forests, anddescribe how nest count methods perform in ahabitat with a high density of oil-palms.

METHODS

Cantanhez National Park is located in TombaliRegion, in Southern Guinea-Bissau (northeast limit:1112205800N, 1414601200W; southwest limit: 111201800N,1511505800W), where the landscape is a patchy mosaicof rivers, forests, agricultural fields, savanna, andmangrove subjected to tidal flooding.

The rainy season usually starts in June and lastsuntil October/November. In Guinea-Bissau, theannual rainfall shows a considerable geographicvariation ranging from 2,400 mm in the southwestto 1,200–1,400 mm in the northwest. The relativehumidity varies between 69 and 79%, being higherfrom July to November and lower from December toFebruary. In Tombali region, the annual rainfall andhumidity indices are the highest in the country. Theclimate is classified as humid, and the aridity indexreveals great water deficiency due to the water deficitduring the dry season [Catarino et al., 2001].

Guinea-Bissau is included in the Guinea-Congo-lia/Sudania regional transitional zone, or zone XI,which leads to some heterogeneity in vegetation fromnorth to south and from coastal to inland areas[Catarino et al., 2001, 2008]. Cantanhez region isgenerally considered as a part of the sub-humidGuinean region [Martins, 1994] and contains thenorthernmost sub-humid Guinean forests of thecountry [Catarino et al., 2001; Silva, 1997], whichshow a species composition different from other typesof forest in Guinea-Bissau [Catarino, 2004]. Thedense forest present in Cantanhez National Parkis dominated by Hunteria umbellata, Malacanthaalnifolia, and Strombosia pustulata, but otherspecies may be present, including: Albizia dinklage,Anisophyllea laurina, Dialium guineense, Elaeisguineensis, Alstonia congolensis, Klainedoxa gabonen-sis, and Parinari excelsa [Catarino, 2004; p 231–236].

Patches of palm groves of Elaeis guineensis arefound in the borders of the inner lowlands or in thecoastal transition vegetation between the terrestrialand the halophytic communities in the coastalregions [Catarino et al., 2008]. The mixed oil-palmgroves are present in several regions of Guinea-Bissau and its dominant arboreal species is Elaeisguineensis, but other species are also present[Catarino, 2004; p 237–244]. Catarino also statesthat, regarding the floristic composition, the oil-palmgroves are not different from other communities ofnatural vegetation dominated by arboreal species.

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However, there are quantitative aspects that allowthis distinction, namely the abundance of oil-palmsand other floristic and ecological factors [Catarino,2004; p 241].

Data were collected during 4 months, fromFebruary to early June 2007 (dry season), in fourof the Cantanhez forests (Fig. 1): Caiquene, CibeCadique, Lautchande, and Madina, which altogethercomprise an area of 17.225 km2 [Silva, 1997].

Methods for Estimating Nesting Densities

Linear Transect Surveys are the most widelyused methods to estimate mammal densities[Chiarello, 2000; Devos et al., 2008b; Drummer &McDonald, 1987; Plumptre, 2000; Plumptre &Reynolds, 1996; Wanyama et al., 2010]. Thesemethods assume that there is a detection probabilitythat depends exclusively on the perpendicular dis-tance from the trail to the nest [Buckland et al.,2001]. Likewise, Marked Nest Counts using lineartransects surveys is a widely used method to estimatechimpanzee densities [Devos et al., 2008a; Furuichiet al., 2001; Hashimoto, 1995; Plumptre & Reynolds,1996]. This method consists of repeating samplingtransects using fixed time intervals and marking allnew nests. Although it is more time consuming than

the Standing Crop Nest Counts Method [Morganet al., 2006; Tutin & Fernandez, 1984], the MarkedNest Count avoids problems associated with nestdecay rate estimation [Kuhl et al., 2008; Plumptre,2000; Plumptre & Cox, 2006; Plumptre & Reynolds,1997], as long as the interval between samplings isshorter than the nest decay rate [Furuichi et al.,2001; Plumptre, 2000]. Furthermore, nest decayrates appear to vary between sites [Hall et al.,1998; Marchesi et al., 1995; Morgan et al., 2006;Tutin & Fernandez, 1984], and chimpanzee nests arehighly variable and cannot be considered as homo-geneous units [Brownlow et al., 2001].

To transform the number of detected sleepingplatforms into a number of individuals, it isnecessary to determine the nest production rate.For this, two parameters are used: a rate of nestreuse and a production rate of day nests. The formertakes place when some vegetal material is added to apre-existing structure that is then reused, and thelatter corresponds to day platforms used for shortdiurnal resting periods [Plumptre & Reynolds, 1997].

Since little is known about the hunting practices ofthe local community at Cantanhez, opening new trailswould possibly create new and easy opportunities forthe hunting of other primate species. Thus, as inprevious studies [Fashing & Cords, 2000; Hall et al.,1998; Ihobe, 1995], we used existing trails to assesschimpanzee nesting preferences and nest spatial pat-terns. We would like to add that, beyond the fact thatchimpanzees are not a species targeted for meat con-sumption, it is possible to find nests close to villages andpaths. This seems to be a reality in many parts of WestAfrica: (i) Sept and Brooks [1994] refer to chimpan-zees and people living in close proximity in Liberia in16th and 17th centuries; (ii) Hockings [2007] alsodescribes a similar scenario of close proximity betweenchimpanzees and humans for Bossou (Guinea); (iii) thefirst author of this paper is currently carrying outfieldwork in Cantanhez National Park about human–wildlife interaction and has testified to the sameproximity: chimpanzee nests close to villages, chimpan-zees crop raiding in people’s backyards, human–chimpanzee encounters in roads and paths. These,together with the fact that opening new transects wasreported to have an effect on the distribution ofchimpanzee nests [Plumptre & Reynolds, 1997], giverobustness to our assumption that chimpanzee nestingis probably not influenced by preexistent trails.

The trails used for nest counting were openedfor several reasons, and may or may not still be used:(i) old trails used during the independence war(1963–1974) to travel from one village to the other,(ii) trails used to search for oil-palm resources (fruitand sap) or Borassus aethiopum sap, (iii) trails thatwere used to lead to a cropland since the shiftingagriculture requires their installation. Although itwas not possible to know if or for what purpose thosetrails are used today (e.g. to hunt or collect forest

Fig. 1. The study area (black square) and the studied forests inCantanhez National Park (Guinea-Bissau): Caiquene, Cibe Cadique,Lautchande, and Madina forests.

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Nesting Ecology: Oil-Palms and Forest Edge / 487

fruits or plants), the trails that showed signs of beingregularly visited were discarded. The trails weregenerally narrow and marks had to be made in thetrees in order to repeat exactly the same path.

In this study, and as proposed by Morgan et al.[2006], a specific density was calculated for eachpotentially different ecological unit (stratum) and thegeneral density was a weighted average that tookinto account their representativeness in the studyarea. The four forests (Fig. 1) define one strata set.To avoid minus sampling, which would be character-ized by a low sampling effort in the limits of thestudy area [Thomas et al., 2006] the forest bound-aries were also considered. These, unlike forest coreareas, are often dominated by oil-palms [Cassama,2006; Catarino, 2004]. Owing to this particularfeature, and since the specific conditions of habitatedges influence the distribution of animal speciesthat may be attracted or repulsed by them [Herlin,2001], forest core areas and the forest edges wereconsidered as another strata set. Since we used trailsin this study, it was not possible to adopt a pre-determined definition of forest edge. Therefore, thisarea was qualitatively defined as a band within 100 mfrom the forest edge, which in certain areas shows ahigher occurrence of oil-palms. Such division couldnot be assumed for the Cibe Cadique fragment sincethe high degree of patchiness and forest fragmenta-tion did not allow a proper edge definition. Anexploratory qualitative description of each trail wasdeveloped and the following aspects were taken intoaccount: (i) the presence of oil-palm groves, and (ii)the presence of liana and tree species eaten bychimpanzees, which was based in a list of 20 speciesnamed by the local community as being used bychimpanzees as food source. There was no dbh cut-off; the transect width was not defined; every newspecies detected from the trail was registered.

Each trail was visited every 14 days, and duringeach sampling session all new nests were markedand described. The first two sampling sessionsworked as the baseline for the six replications(R1–R6), when new nests were counted. For eachnest, the tree species was identified, the nest heightwas measured using a range finder (Bushnell Yard-age Pro Sport 450), and the perpendicular distance tothe trail was measured with a meter tape. Treespecies were identified using the floral field guide toGuinea-Bissau [Catarino, 2006] and by using thelocal knowledge of skilled field assistants. The fieldassistants were adults (around 30–40 years old)recognized by the elders as being able to identifytree species in their local languages. Some of themhad previously worked with other researchers,including botanists. Moreover, the information wascross-checked using information from different fieldassistants using the Creole, Balanta, and Nalu namesfor the same species. A database with the correspon-dence between local names and scientific names in

the field guide of Catarino [2006] was consulted. Allsurveys were conducted with the first author presentand field assistants were trained on nest countmethods during baseline surveys.

During each sampling session, 22 transect trailswere followed (a total of 28.35 km) in the four forests(6.11 km in Caiquene; 4.74 km in Cibe Cadique;8.01 km in Lautchande; and 9.50 km in Madina), inboth core and boundary forest areas (14.28 km and14.07 km, respectively).

We assume that non-linearity does not signi-ficantly interfere with the detection function, sincetrails had a smooth sinuosity and the shortestdistance from the trail to each detected nest wasmeasured. In spite of the limitations described, weassumed that in these field conditions this option wasthe most adequate one. DISTANCE 5.0 software[Thomas et al., 2010] was used. Though the samplingtechniques employed do not always meet all assump-tions, such software is broadly used because of itsrobustness [Bennett et al., 2001; Blom et al., 2001;Hall et al., 1998; Morgan et al., 2006; Plumptre, 2000;Plumptre & Cox, 2006], and it has frequently beenchosen as an operational tool to estimate densities.The detectability curve was calculated using thissoftware, and the criteria to choose the best modelwere: Aikaike’s Information Criterion (AIC), indicatorof simplicity and parsimony; the GOF/w2 to estimatethe model adjustment; and variation coefficient (CV),although it is known that it is not a very powerfulestimator of the precision level [Sokal & Rohlf, 1995].

Chimpanzee nests are clustered, so it is impor-tant to truncate the sampling data in order todecrease the correlation between detection probabil-ity and cluster size and consequently improve theindependence between observations [Buckland et al.,2001]. The distance adopted for data truncation wasdefined according to the nest detectability curve, andthe most appropriate cutline was considered to be at32 m (see the results section). The nests consideredfor the analysis were the ones not excluded by thistruncation procedure that excludes the extreme andless probable observations [Buckland et al., 2001].No distance intervals were adopted, because thedistance measurements were accurate.

As there was no quantitative data on chimpanzeesin Cantanhez forests, we decided to use the nestproduction rate estimated for Budongo forest (Uganda)[Plumptre & Reynolds, 1997], which could be a sourceof error to our study [Kuhl et al., 2008]. In Cantanhez,the chimpanzees are not habituated to researchers;therefore, we were not able to estimate the local-specific nest production rate. Therefore, similar toother studies of unhabituated chimpanzees [Morganet al., 2006; Plumptre & Cox, 2006; Sanz et al., 2007],we used Plumptre and Reynolds’ value. This estimateaverages that 1.09 nests are built per individual pernight [Plumptre & Reynolds, 1997].

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In spite of the fact that direct observations oflarge mammals can be constrained by the lowvisibility in the forest, resulting in inadequatesample sizes, all clusters of chimpanzee feces andsightings (groups or lone individuals) were docu-mented. Only those detectable from the trail wereconsidered. Feces were removed from the trail afterdocumentation to ensure that no double countingoccurred.

As the data are non-normally distributed (testedwith Shapiro–-Wilk normality test), nonparametricMann–Whitney and Kruskal–Wallis tests were per-formed to check differences between samples. A leastsquares regression analysis was used to adjustvariations in nest detection rates along samplingsessions. The Chi-square test and the Wilcoxon ranktest were used to evaluate nesting preferences. Ana-level of 0.05 was adopted as the cut-off forsignificance or a/N, where N is the number of com-parisons. This last cut-off results from Bonferonnicorrections [Abdi, 2007].

Morgan et al. [2006] defined a nest-site as ‘‘allnests created by the same ape species and of thesame age class created r50 m of each other.’’ Wetried to identify nest-sites by applying this concept tonests detected in each replication through the hot-spot analysis of CrimeStat v3.0 software (Ned Levineand Associates, Houston, TX and the NationalInstitute of Justice, Washington, DC) [Levine,2004]. Therefore, the nearest neighbor hierarchicalspatial clustering (Nnh) was used to group pointstogether on the basis of spatial proximity. Thethreshold distance was 50 m and two nests was theminimum number of nests defining a cluster (nest-site). In order to determine the preferred nestingareas, this analysis was repeated on trail sections of250 m where a minimum of two nest-sites occur.

This research was conducted in compliance withthe American Society of Primatologists’ Principlesfor the Ethical Treatment of Primates. This studyused exclusively noninvasive methods and was basedon indirect evidence of presence, principally chim-

panzee nests. Therefore, the potential risks forchimpanzees or other primate species were minimal.Moreover, as stated before, the conservation andanimal welfare aims were prioritized rather than theadoption of most adequate sampling strategy.Additionally, we state that all protocols reported inthis manuscript were approved by the governmentalagency that regulates research in protected areas inGuinea-Bissau and the legal requirements of thiscountry were fulfilled.

RESULTS

During data collection, a total of 718 nests weredetected, marked, and described; 431 nests weresampled during the baseline period and 287 nestswere detected during the six following samplingsessions. Sampling sessions were separated by14-day intervals.

Detection Probability

As the distance from the trail increased, thenumber of nests sighted decreased for N(D) 5

�1.67D157.09, N being the number of nestsdetected at each distance D (R2 5 94.0, Po0.01;Fig. 2A). The half-normal detection probabilitymodel with cosine adjustments fitted the data best(AIC 5 932.16, CV 5 9.35%, w2 5 0.94) with datatruncation at 32 m, which corresponds to a detectionprobability of 0.10 (Fig. 2B). Of the 287 new nestsregistered during the six replications (R1–R6), 250were considered for analysis after truncation (13% ofthe nests were discarded).

There were significant differences in the detec-tion distances for the four studied forest fragments(H 5 15.530; Po0.01; N 5 113, N 5 29, N 5 134,N 5 11). However, when Madina is not consideredin the analysis this difference disappears (H 5 0.450;p 5 0.979; N 5 113, N 5 29, N 5 134). Moreover,there are only significant differences in the detectiondistances when each forest is compared with Madina;

Fig. 2. Number of new nests detected at each distance interval during the six replications: (A) linear regression; (B) detectability curve(half-normal model performed with DISTANCE 5.0 software).

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when Bonferonni corrections (a/N 5 0.05/6) areapplied these remain significant (Po0.01; Table I).The new nests registered in Madina forest (N 5 11)were detected at the following distances: 4, 22, 25,35, 46, 46, 71, 77, 77, and 80 m, which means thatafter truncation seven were discarded.

Transects’ Description

Along the 23 trails, the plant species reported tobe used as a food source by the chimpanzees weredetected as follows (within brackets are the numberof trails where each species was detected): (i) the treespecies: Dialium guineense (18), Ceiba pentandra(17), Parinari excelsa (15), Treculia Africana (14),Borassus aethiopum (13), Spondias mombin (13),Vitex sp. (11), Parkia biglobosa (11), Ficus sp. (11),Antiaris toxicara (10), Anisophyllea laurina (9),Neocarya macrophylla (9), Sarcocephalus latifolius(4), Adansonia digitata (3), Mangifera indica (3),Anacardium occidentale (2); and (ii) liana species:Saba senegalensis (14), Landolphia sp. (14), Uvariachamae (10), Anthostema senegalense (7).

In the trails in Madina forest, seven of thesespecies were identified, in Caiquene we detected18 species, while in Cibe Cadique and Lautchande 19species were observed. Oil-palm groves appeared inforest edges, since they occur in lower altitudes,which in Cantanhez forests correspond to savanna(that could be flooded in the rainy season) ormangrove boundaries. In both Caiquene and Madina,the edge trails corresponded to areas where theforest is surrounded by mangrove, while in Lautch-ande savanna is the boundary ecosystem of the trails’edges. From this exploratory approach, there are nospecies specific to forest core areas or forest edge.

Habitat Heterogeneity Among Forests

Considering the new nests detected within thetruncation distance, Lautchande forest had the highestnest detection rate (2.54 nests km�1), followed by

Caiquene (1.85 nests km�1), while Cibe Cadique andMadina displayed the lowest values (Fig. 3; 0.78 and0.07 nests km�1, respectively). Significant differencesin the detection rate of new nests existed for thefour forests (H 5 14.68; Po0.01, N 5 6). However,the forest pairs Lautchande/Caiquene and CibeCadique/Madina did not reveal significant differ-ences in terms of nest detection rates (Table I). WhenBonferroni corrections were applied to the cutline,the pairs Caiquene/Cibe Cadique and Lautchande/Cibe Cadique lost significance as well (Table I).

The forests with a higher number of nestsaccounted for more sightings (R 5 0.95; Po0.05)and feces (R 5 0.95; P 5 0.05). The relationshipbetween nests and feces among the four forests wasnot significant (R 5 0.80; P 5 0.20; Table II).

Habitat Heterogeneity in Forest Edge andCore Areas

The new nests found within the truncationdistance did not exhibit a homogenous distributionbetween forest core areas and forest edge: 54 newnests (24%) were recorded in forest core areas and171 (76%) in the forest edge. The nest detectionprobability is not significantly different for forestcore areas and forest edge (U 5 8,412.5; P 5 0.352;N 5 192, N 5 94) and there are significant differencesof nest detection rates between these (U 5 0.00,Po0.01, N 5 6).

Chimpanzee sightings and feces were mostlyrecorded inside the forest fragments, whereas nestswere mostly distributed on forest boundaries(Table II). Moreover, considering forest boundaryand forest core areas, the nest frequencies differsignificantly from the occurrence of sightings(w22 5 18.71, Po0.01) and from the occurrence offeces (w2 5 10.30, Po0.01). In the nonpaved roads,two fecal samples were found, and one sighting ofchimpanzees crossing the road was recorded.

TABLE I. Mann–Whitney Tests for the Number of Nest Detected (day�1 km�1) vs. the Detection Distances in theFour Forests

Detection rate of new nests (new nests day�1 km�1)

Caiquene Cibe Cadique Lautchande Madina

Detection distance (m) Caiquene U 5 6.00 U 5 13.00 U 5 0.00P 5 0.05a P 5 0.423 Po0.01��

Cibe Cadique U 5 1561 U 5 3.00 U 5 10.00P 5 0.695 Po0.05�a P 5 0.184

Lautchande U 5 7337.5 U 5 1804.5 U 5 0.00P 5 0.675 P 5 0.548 Po0.01��

Madina U 5 212.5 U 5 64.0 U 5 194.5Po0.01�� Po0.01�� Po0.01��

�Significantly different with Po0.05.��Significantly different with Po0.01.aNonsignificant if Bonferroni corrections are applied.

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Use of Oil-Palms for Nesting

In the study area, 92% of the nests were in oil-palms. The remaining 8% were built in Dialiumguineense, Parinari excelsa, Anisophyllea laurina,Xylopia aethiopica, Treculia africana, Parkia biglo-bosa, Trichilia prieuriana, and Malacantha alnifolia.However, if only baseline sampling nests are con-sidered, the percentage of oil-palm nests increases to99.54%, which is, most probably, due to the longertime required for this nest type to decay. During datacollection, new leaves of oil-palm were found on thefloor nearby the oil-palms and the pith had beeneaten by chimpanzees.

Considering all nests, the average nest heightwas 19.7272.94 m, very similar to the average heightof oil-palm nests (19.7872.76 m) and to the averageheight of nests built in other tree species(18.8076.05 m). The nest height varied from 5 to30 m, the first corresponding to Malacantha alnifoliaand the latter to Parinari excelsa, this speciescorresponds to the nests built at heights greaterthan oil-palms (from 24–30 m).

A higher frequency of oil-palm nests wasreported, not only for forest edge (w2 5 838.17,Po0.01; Table II) but also for forest core areas,where the oil-palm is not dominant (w2 5 133.79,Po0.01; Table III). Only one of a total of 15 newnon-oil-palm nests was located on the forest edge.However, forest core areas and forest boundarieswere not significantly different regarding the fre-quencies of nests built in the several tree species(P 5 0.345, Table III).

Oil-Palm Specificity: Implications forChimpanzee Census

During fieldwork, two kinds of oil-palm nestswere identified. Their differences appear as a con-sequence of leaf handling that can lead to ‘‘nests ofbroken leaves’’ (Fig. 3a) or ‘‘nests of bent leaves’’(Fig. 3b). Although in the former type nutrient flowto the leaves is inhibited and, consequently, thestructure starts to present decay signs such as colorchange from green to brownish, the latter allows forthe oil-palm leaves to unfold and recover, with nocoloration change (Fig. 3).

TABLE II. Number of New Nests, Dung Clusters and Sightings Registered During the Eight Sampling Surveys, inEach Studied Forest (Caiquene, Cibe Cadique, Lautchande and Madina), in Both Forest Edge and Forest Core Area

Signs Caiquene Cibe Cadique Lautchande Madina Corea Boundary

Nests (truncation 32 m) 9839.2%

2510.0%

12449.6%

31.2%

5424.0%

17176.0%

Dung findingsb 621.4%

932.1%

1346.4%

27.1%

1152.4%

838.1%

Sightingsc 216.7%

216.7%

758.3%

18.3%

880.0%

110.0%

aThe nests in Cibe Cadique forest were not taken into account since this forest does not have a defined edge; thus the total number of nests, dung, andsightings for all forests is not equal to the total of core, boundary and road.bRefers to clusters of droppings.cA group of individuals constitutes one sighting; the same individual may have been seen on different days.

Fig. 3. Types of chimpanzee nests on oil-palms: (a) ‘‘nest of broken leaves’’; (b) ‘‘nest of bent leaves’’; (c) recovery of a bent oil-palm nestthrough leaves unfolding.

Am. J. Primatol.


The existence of two types of nests was noticedwhile monitoring 15 oil-palm trees that wereobserved over time to have an overview of the decayprocess. These were monitored each time the trailwas visited and were always photographed from thesame place to prevent different perspectives of thenest from leading to different interpretations oftemporal changes. Three nests did not undergounfolding, and 12 went through leaves unfolding.In a few cases, it was difficult to distinguish the nesttypes because some leaves were broken and othersonly bent. Regarding this, an oil-palm nest was onlyclassified as a ‘‘broken leaves nest’’ if all leaves werebroken, making unfolding unlikely. Although it waspossible to observe leaves unfolding within thelength of the period, the complete decay process ofthe ‘‘broken leaves nest’’ was too long to be followed.Leaf unfolding seemed to occur at different speeds.A nest built without using all leaves, or the unfoldingof bent leaves could increase the probability of oil-palm nest reuse (Fig. 4).

The spatial pattern of new nests exhibited aclustered distribution (nearest neighbor index 5 1.32,Z 5 9.70, Po0.01, N 5 250) and, considering eachreplication separately, nests also revealed a signifi-cant clustered pattern (Po0.01 for each of the sixreplications, R1–R6). Thirty-four nest clusters (nest-sites) were detected: ten in R1, nine in R2, three inR3, seven in R4, three in R5, and another two in R6.These nest clusters also showed a clustered distribu-tion (nearest neighbor index 5 1.48, Z 5 5.39, two-tailed Po0.01, N 5 34). Moreover, the clusteranalysis (Nnh) of the 34 nest-sites led to four nest-site ‘‘hotspots’’ (defined as a minimum of two nest-sites less than 250 m to each other), of which threewere in the trails containing oil-palm groves.

The replications accounted for a nest detectionrate ranging from 2.39 nests km�1 in the firstreplication to 1.08 nests km�1 in the sixth replica-tion. During these six replications, the averagenumber of new nests detected decreased at a rateof N(R)’ 5 0.24 nests km�1 (Fig. 5).

At each of the six replications, an average of48 new nests were registered and marked. Thisincrement of marked nests caused the number of

Fig. 4. Reused nest not considered as a new nest due to previousmarking (on the 15th of March the nest was monitored and theoil-palm nest had not yet been reused).

TABLE III. Species Preference for Nesting in ForestCore Areas and Forest Edge Considering the NewNests Found Within the Truncation Distance (w)

Number of nests (w 5 32 m)

Species % nestsForest

core areasForestedge

Elaeis guineensis 93.33 41 169Parinari excelsa 2.23 4 1Anisophyllea laurina 1.78 4 0Dialium guineense 1.78 4 0Trichilia prieuriana 0.44 1 0Treculia africana 0.44 1 0Total 55 170w2 test w2 5 133.79,

Po0.01�w2 5 838.17,

Po0.01�

Wilcoxon matchedpairs test

Z 5 0.943, P 5 0.345

Cibe Cadique nests were not considered in the analysis.�Significantly different with Po0.05.

Fig. 5. Number of nests detected per kilometer in the eightsamplings (two baseline samplings plus six replications). �pregards to parameters b1 and b2 estimated for the exponentialmodel, N(R)5 b1� exp(b2R). All samplings N(B) 58.55exp(�0.28R);R2 5 0.70, Po0.01. Discarding baseline samplings: N(R)53.02–0.24R; R2 50.84, Po0.01.

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492 / Sousa et al.

undetectable nests to increase at a rate of0.242 nests km�1 (see Fig. 5); this resulted in anaverage of 6.86 nests not being detected in eachreplication (0.242� 28.345 km of trails length). The6.86 nests undetected on samplingx each time 48 newnests are marked in samplingx�1 allows us toestimate the effect of each sampling on the subse-quent sampling. Therefore, the first baselinesampling led to 36 nests being undetectable in thesecond baseline sampling, and so on. This wouldforce us to recalculate and correct the new nests foreach replication taking into account this cumulativeeffect, which lead us to an average of 129 new nestsdetected in each replication, value that is 2.7 timeshigher if the correction is not adopted (Table IV).

We did not achieve a unique robust chimpanzeedensity estimation for the four forests of southernCantanhez National Park. Nevertheless, we presentthe possible estimates for these forested areas,considering the extreme cases: (1) If we assume thattwo exhaustive baseline samplings were sufficient toensure that all standing nests were marked beforethe replications and that reuse of already marked oil-palm in nests is an important factor causing thenumber of the detected nests to decrease, the bestestimate would be 6.18 weaned individuals per km2

of forest. This corresponds to 106 weaned individualsin these four forests (this estimate takes into accountthe correction for new nests detected—see Table IV);(2) On the other hand, if we assume that the effect ofoil-palm nest reuse is not important and that thebaseline sampling was not successful, then some oldnests were probably marked as new nests and thefirst replications are likely to be overestimations. Inthis case, the density would be lower than 2.64weaned individuals per km2, estimated exclusivelyfrom the first replication (R1), and higher than 1.10weaned individuals per km2, estimated exclusivelyfrom the sixth replication (R6, that is likely to beunderestimated due to oil-palm reuse), which corre-spond, respectively, to 45 and 17 weaned individualsinhabiting these forests.

DISCUSSION

There were significant differences in the fre-quency of chimpanzee nests among the four forestsof Cantanhez, as well as differences in nest detectionrates between forest edges and core areas. As nestdetection differences were not influenced by canopycover, we can assume that they reflect a preferencefor nesting. Lautchande and Caiquene appear to bethe most important forests for nesting, showing ahigher nest detection rate than Madina or CibeCadique. Although the amount of feces found wasnot large, the forests with a higher number of nestsalso showed a higher number of fecal samples andsightings. Madina forest appears to be the leastimportant for both chimpanzee nesting and foraging.Morgan et al. [2006] stated that the spatial distribu-tion of nests reflects the general pattern of habitatuse for the chimpanzees in the Republic of Congo.Although this seems to be the case in the four studiedforests, where forests with a greater number of nestsalso exhibited a higher occurrence of fecal observa-tions and direct observations, the opposite occurswhen comparing forest edge and forest core areas.Most nests were recorded in the forest edge, whiledirect observations and feces were mainly recordedin the forest core areas, which may suggest that thespatial distribution of nests may not correspond tothe pattern of habitat use in terms of forest edge andforest core areas.

Chimpanzees are thought to show a preferencefor nest-building in less disturbed forests [Marchesiet al., 1995]; however, in the south CantanhezNational Park nests appear mainly in forest edge.These areas are characterized by more open habitattypes than those where the local community extractsoil-palm fruit for oil production, or sap from oil-palmand Borassus aethiopum for wine production. Thissuggests that in this area of Southern Guinea-Bissauchimpanzees are still not directly persecuted byhumans and do not avoid areas of human use. Inaddition, the nonpaved roads in this region do notseem to act as barriers to chimpanzee movement,as they are quite narrow and have vegetation along

TABLE IV. The Effect of the Previously Marked Nests on Nest Counting in Each Replication

Samplings Marked nestsPreviously

marked nestsUndetectable

nestsActual number

of new nests

Baseline (phase 1) 250 0 0 n.aBaseline (phase 2) 181 250 35.7 n.aR1 68 431 61.6 130R2 57 499 71.3 129R3 43 556 79.5 122R4 53 599 85.7 138R5 36 652 93.2 129R6 31 687 98.3 129Average number of

new nests (R1–R6 samplings)48 (N 5 287) n.a. n.a. 129 (N 5 782)

Am. J. Primatol.


the verges [personal observation; Hockings, unpub-lished data].

These results confirm that the tree speciesprimarily used by chimpanzees for nest-building inthe studied area is, by far, the oil-palm (Elaeisguineensis). The nesting behavior by chimpanzees inCantanhez shows many parallels with that ofchimpanzees in Karanfarande, Guinea, where themajority of nests are also built in oil-palm trees andthe second and third most important species areDialium guineense and Parinari excelsa. However,absolute levels of oil-palm nesting in this region areunknown and it is still not possible to define if thepresence of oil-palm nests in Kanfarande region is asdominant as in the four studied forests of Cantanhez.More research is needed to address the similaritiesand differences among chimpanzee communitiesregarding the factor(s) responsible for oil-palmnesting preference. The clumped distribution ofnests along forest edge may either be a simpleconsequence of oil-palm distribution, or it could havea more complex behavioral or ecological cause, suchas food trees being more abundant in the forest edge.The higher number of nests in oil-palms was reportedeven in forest core areas, where the availability of oil-palm is not as high as in forest fringes [Catarino,2004; Janick, 2002]. Chimpanzees still use thisspecies more frequently than others. This mightindicate a preference for nesting in oil-palms evenwhen their availability is lower than other species.However, a study such as the one developed byFuruichi and Hashimoto [2004] in Kalinzu forest(Uganda) would help to understand nesting prefer-ences as well as the extent of oil-palm preference.

Chimpanzees in Cantanhez nested at an averageheight of 19.72 m. This is similar to reports of17.65 m from northern and coastal Guinea[Ham, 1998] and 20 m in the Ivory Coast [Fruth &Hohmann, 1994], but higher than reports from othersites (8.33 m in Senegal [Pruetz et al., 2008]); 11 m[Baldwin et al., 1981] and 13.55 m [Pruetz et al.,2008] in Mt. Assirik in Senegal; 8.7 m for Gabon[Tutin & Fernandez, 1984]; 12 m in Liberia [Andersonet al., 1983] and 5–15 m in Budongo Forest, Uganda[Plumptre & Reynolds, 1997]). In the fourCantanhez forests studied, there were no groundnests as described at other sites [Humle, 2003;Koops et al., 2007; Matsuzawa & Yamakoshi, 1996;Nkurunungi & Stanford, 2006; Pruetz et al., 2008].

The places where chimpanzee nests accumulateare described as areas with high fruit availability[Baldwin et al., 1981; Furuichi & Hashimoto, 2004;Groves & Sabater Pi, 1985; Kortlandt, 1992; Septet al., 1992]. However, this may not explain thepreference for oil-palms, unless this species repre-sents an extremely important food resource inGuinea-Bissau. In other sites, despite being de-scribed as a fallback food [Humle & Matsuzawa,2004; Yamakoshi, 1998] the preference for nesting in

oil-palm is not evident. In fact, Leciak et al. [2005]state that the possible oil-palm preference atKanfarande could be due to the high density of thistree species and the potential importance of oil-palmfruits as food source from November to May whenother forest fruits are less available.

Even though we do not yet know the reason whynesting in oil-palms is so prevalent among thechimpanzee community in the south of CantanhezNational Park, we offer the following hypotheses,which were mainly based on a review of theliterature: (1) As suggested by Kortlandt [1992],Ham [1998], and Brownlow et al. [2001] predation isan important factor in determining the heightchosen for nesting. In fact, the height of oil-palmcrowns and the oil-palm morphology ensures that nopredator (like Panthera pardus, which is described toexist in the area [Gippoliti & Dell’Omo, 1996]) is ableto reach the nesting place; (2) the height of oil-palmcrowns and nesting at the forest boundary enables awider view of the surrounding landscape [Kortlandt,1992], especially when the groves of oil-palms arelocated in the forest edge or in regeneration forests;(3) the similar heights of oil-palms make commu-nication easier among group members, especiallywhen the groves of oil-palms are located in the forestedge or in regeneration forests; (4) oil-palms areassociated with areas of lower altitudes and/or forestedge with savanna or mangrove, and it might be thatthese environments offer some specific resource(s) tothe chimpanzees.

Nesting in oil-palms implies a set of behaviorsand technical skills that have to be perfectly adaptedto the specific morphology of oil-palms, which is verydifferent from the other tree species. Oil-palm nestshave been described before [De Bournonville, 1967;Gippoliti & Dell’Omo, 1996; Goodall, 1962; Ham,1998; Kortlandt, 1996] but never with quantitativedata that illustrate such a marked frequency of oil-nests in comparison with other nest types.

This study highlights the idea of Brownlow et al.[2001] that chimpanzee nests should no longer beconsidered a homogenous concept. Moreover, in thesouth of Cantanhez National Park, we distinguishedtwo types of oil-palm nests: the ‘‘broken leaves nest’’that follows a typical decay process, and the ‘‘foldedleaves nest’’ that loses its shape within an unknowntime period without decaying and, after a sponta-neous and slow unfolding, free leaves becomeavailable for nesting. The difficulty with describingnest decay has been discussed extensively [Blomet al., 2001; Morgan et al., 2006; Tutin & Fernandez,1984], but we highlight that oil-palm nests often donot follow the usual decay process described in theliterature. Moreover, they seem to take longer todecay, since the percentage of oil-palm nests markedin the baseline sampling is higher than in thesubsequent samplings, although it may be the casethat this resulted from a seasonal change in the

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habitat that interferes with nesting preferences. Ifnest decay rate is going to be estimated for thisregion, it should follow the method described byBlom et al. [2001] in order to take into account theoil-palm nest as a different type.

Besides the effect of non-linearity, anotherpotential limitation of estimating chimpanzee den-sity during this study was that we adopted a nestproduction rate of 1.09 nests per day/individual fromBudongo Forest, Uganda [Plumptre & Reynolds,1997]. The southern areas of Cantanhez NationalPark present a quite different scenario from othersites in terms of chimpanzee nesting. The highfrequency of oil-palm nests and its clustered patternmake oil-palm reuse very likely since chimpanzeesquite often visit the same oil-palm areas. Moreover,nest unfolding is another factor that may tend toincrease nest reuse probability, which would conse-quently give rise to a lower nest production rate.Hence, as was stated in Kuhl et al. [2008], andespecially for this region, it becomes imperative toestimate appropriate and site-specific parameters, ifchimpanzees are to be censused using nest counting.Regarding chimpanzee densities, oil-palm nests in-troduce new challenges to census methods for twomain reasons: (1) the spatial arrangement of oil-palmnests is clustered and the nests are built very close toeach other. This makes nest counting a verydemanding task, and if the old nests are not allmarked in baseline sampling, the later replicationscan be overestimated; and (2) leaf unfolding maypromote nest reuse, and if a certain tree has alreadybeen marked, the second nest will not be detected. Ifwe assume that the movement of chimpanzees doesnot induce a significant effect on nest distributionand that the baseline sampling successfully markedall nests, oil-palm reuse will be the only factoraffecting the decrease on nest detection rates. Sincethe number of marked oil-palms increases at eachreplication, the increasing number of replicationsalso increases the probability of underestimation.Thus, in contrast to the majority of ecologicalsurveys where a higher number of replicationsincreases the sampling accuracy, in this context itmay adversely affect the probability of detecting newstructures, leading to an underestimation. Fromthese surveys, we estimate that between 17 and106 weaned chimpanzees are present in the fourforests. In summary, despite the constraints ofestimating chimpanzee densities in Cantanhez, wewere able to identify important ecological nestingfeatures such as the frequent use of oil-palm trees fornesting, particularly those on the forest edge.

ACKNOWLEDGMENTS

The authors thank the following field assistants:Zeca Dju, Queba Indjai, Djibi Indjai, Iaia Camara,Braima Vieira, Braima Camara, and Saidu Kuiate,

and all human and non-human primates of Cantanhez.A special thanks to Tiago Marques for his usefuladvice; to Matt McLennan for his comments andliterature suggestions; to Kimberley Hockings andAna Luisa Luz for their important commentsand review. Acknowledgments are also due toGuinean governmental institutions such as IBAP(Instituto da Biodiversidade e das Areas Protegidas)and DGFF (Direcc- ao Geral das Florestas e Fauna).Finally, thanks are due to the Guinean NGO AD (Acc-ao para o Desenvolvimento). This study was con-ducted within a wider project (POCI/ANT/57434/2004) and was financially supported by the FCT(Fundac- ao para a Ciencia e a Tecnologia, Portugal)and FEDER, through the Research and DevelopmentProgram POCI 2010.

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Documents

Chimpanzee oil-palm use in southern Cantanhez National Park, Guinea-Bissau