Endangered West African Chimpanzees Pan troglodytes verus (Schwarz, 1934) (Primates: Hominidae) in Senegal prefer Pterocarpus erinaceus, a threatened tree species, to build their nests: implications for their conservation

1 UCAD, Université Cheikh Anta Diop, Département de Biologie animale, B.P 5005, Dakar-Fann, Senegal 2,3 UCAD IRD, Université Cheikh Anta Diop Institut de Recherche pour le Développement, Département Ressources vivantes, and IUCN Species Survival Commission, Route des Pères Maristes, Dakar, Senegal 4 IRD, Institut de Recherche pour le Développement, UMR 211 Bioemco, 5 rue du Carbone, 45072 Orléans cedex 2, France 1 ibnou.ndiaye@ucad.edu.sn (corrosponding author), 2 anh.luong@ird.fr, 3 gerard.galat@ird.fr, 4 georges.nizinski@ird.fr

The West African chimpanzee (Image 1) is listed as Endangered (A4cd ver 3.1) by IUCN (Humle et al. 2008).In Senegal, the main threats are habitat fragmentation/ destruction (Galat-Luong et al. 1999-2000;Carter et al. 2003;Humle et al. 2008) and competition with humans (Pruetz 2002).Additionally, some tree species used for woodworking, such as Pterocarpus erinaceus, are becoming hard to find outside of national parks (Brunken et al. 2008;author pers. obs.).Galat-Luong et al. (1999-2000, 2009), Pruetz (2002), Pruetz et al. (2002), Carter et al. (2003) and Ndiaye et al. (2013) showed that chimpanzees still roam outside of their main refuge in Senegal, Niokolo Koba National Park.In this study we went outside of protected areas to gather and analyse the first qualitative and quantitative data on the West African Chimpanzee's tree species preferences for nest building in Senegal.Furthermore, we related these preferences to the availability of suitable trees in their habitat and to the features of preferred trees.These data are needed to provide conservation managers with information on the extent of habitat dependency of this ape in Senegal and what consequences it may have in the anthropogenic setting currently characterizing this country.

Methods
Study Area: This study was carried out in Kédougou Region (12 0 33'N & 12 0 11W) in southeastern Senegal (Fig. 1), in West Africa.See Pruetz et al. (2002Pruetz et al. ( , 2008) ) and Stewart & Pruetz (2013) for detailed descriptions of the habitat vegetation types.We surveyed the entire region for chimpanzee habitats based on the presence of their nests.Annual rainfall in Kedougou over the 1995-1998 period ranged from 1000-1600 mm, with one dry season from October to May and one rainy season from June to September (Baldensperger 1965), which is typical of a Sudano-Guinean climate as defined by Aubreville (1949).The mean annual temperature was around 28.6 0 C (21.9-35.2 0C) (Galat et al. 2009).Further details on the climate and its changes during this period and the impact on large fauna including chimpanzee behaviour were reported by Galat et al. (2009) and Galat-Luong et al. (2009).
Sudano-Guinean wooded savanna vegetation, as described by Aubreville (1949), prevails in this area.The tree densities vary, and open dry forests are sometimes found.Typically, Guinean tree species grow in gallery forests, which could be relicts of a former denser forest cover that diminished as a result of increasing dryness (Mühlenberg et al. 1990).Almost all trees shed their leaves during the long dry season, except for evergreens in gallery forests.The leaves usually re-emerge just prior to the first rains.
Nest trees: In a previous study (Galat-Luong et al. 1999-2000), in a 15,000km survey carried out in a vehicle, we first identified chimpanzee nesting sites in southeastern Senegal.The present study spanned over 80 days between March 1998 and February 2000, and we covered about 380km outside protected zones on foot and recorded the number of chimpanzee nests on different species.
Abundance of available trees in the habitat: We also sampled the availability in the habitat of tree species (and attached vines) that could potentially host chimpanzee nests by recording them along 927 sampling transects set up perpendicularly to the gallery forests along five rivers where chimpanzee nests had been recorded (Diaguiri River: 598 transects; Dimboli River: 130; Dialabatama River: 37; Djigoumato River: 56; and Linguékoto River: 106).
Species preferences for nest building: In order to assess tree species preferences for nest building, we compared the number of nests hosted by the different tree species to the abundance of the trees in the habitat using Fisher's exact test (two tailed).

Results
Nest trees: We sampled chimpanzee nests (N=1794) and found that only four had been built on the ground, while 1790 were built in trees.We identified the tree species bearing the nests (Table 1).Chimpanzees had built nests for resting in 34 different tree species.
Abundance of available trees in the habitat: We identified 834 trees and vines belonging to 44 different species (Table 1).
Species preferences for nest building: Some species were chosen proportionally to their abundance, whereas others were preferred or less preferred (Fisher's exact test p-value significant to extremely significant; Table 1).Pterocarpus erinaceus, Parkia biglobosa, Anogeissus leiocarpus, Cola cordifolia, Erythrophylum guineensis, Ficus gnaphalocarpa, Lannea acida, Piliostigma reticulatum, and Dalbergia sissoo were used to a greater extent than their availability in the habitat would suggest.

Discussion
Our results showed that chimpanzees in Senegal were highly selective when choosing trees in the environment to build their nests.Pterocarpus erinaceus was the most used by far: 25.42% of the nests were built in this species.This is four times more than expected by chance, given its relative abundance among trees in the habitat (6.35%, p<0.0001).In Issa, Ugalla, western Tanzania, chimpanzees also built their nests in a Pterocarpus species (P.tinctorius Welw.) more often (184 of 1504 nests = 12%) than would be expected considering the availability of this species in transect samples (8 of 211 trees = 4%; Hernandez 2006).The second most used species, Diospyros mespiliformis, was chosen proportionally to its abundance.Chimpanzees feed on fruits of this tree, but ripe fruits were not always available (Ndiaye et al. unpub. data).Together with P. erinaceus, more than a third (36.82%) of all nests were built in one of these two species.The three other species used most frequently, i.e., Parkia biglobosa (11.17% of the nests), Anogeissus leiocarpus (9.22%), and Cola cordifolia (7.60%), were all highly selected (p<0.0001).Nearly half (47.99%) of all nests were recorded in the Different authors have described selection of some tree species for nest building by chimpanzees, including Wrogemann (1992), Brownlow et al. (2001), Basabose & Yamagiwa (2002), Hernandez (2006), Stewart et al. (2007) and Ogawa et al. (2007).According to Stanford & O'Malley (2008), out of 163 tree species present in Bwindi National Park, Uganda, only four harboured 72.1% of all sampled chimpanzee nests.These authors noted the type of nest tree is influenced especially by the extent of food availability, safety and comfort (Stanford & O'Malley 2008).Furnichi & Hashimoto (2004) analysed different factors influencing nesting-site selection by chimpanzees in Kalinzu Forest, Uganda, where only four of seven preferred species provided edible fruit, and one of four less preferred species provided both edible fruit and leaves, the preference for certain species may not be explained by the availability of edible fruit or leaves in the preferred trees.Table 2 describes the physiognomic features common to the six most used tree species, which hosted 70% of all nests.These features, especially the wood hardness (which explains why they are regularly used by woodworkers), seemed to be associated with the chimpanzees' preferences.The sixth species, Syzygium guineense, though also hard, may have been less preferred (5.36% of the nests versus 9.35% in the habitat, p=0.0002) because it was the smallest species.
Two other large tree species, which could be considered as being good 'nest hosts' due to their height, i.e., Butyrospermum parkii (syn.Vitellaria paradoxa, "Karité", "Shea") and Adansonia digitata, were not used more than expected (0.06% and 0.34%, respectively) given their abundance in the new habitat (0.36% and 0.12%, respectively, with no statistical significance).The common feature between these two tree species is their very soft and relatively poor quality wood.This also suggests that wood quality may be a chimpanzee nest tree selection criterion.
In this study, we noted a chimpanzee nest in an Elaeis guineensis Jacq tree on the edge of a gallery forest.Neither preference nor avoidance was significant (p=0.0977).The nest was made of a single E. guineensis palm leaf even though several other tall trees, including Diospyros mespiliformis, were growing nearby.Gippoliti & Dell'Omo (1995) also reported observing chimpanzee nests in E. guineensis trees in Guinea-Bissau.Moreover, Barnett et al. (1994) and Prangley & Barnett (1994) observed a similar phenomenon on Mount Nimba in Guinea.Kortlandt (1996) reported observing chimpanzee nests in this species since 1965 in Guinea.All of these authors considered that nest building in E. guineensis trees is a typical behaviour of chimpanzees inhabiting West African degraded savanna forests, where the canopy is generally not closed.Two authors (A.G.L. & G.G.) also observed that in Senegal E. guineensis trees were used as sleeping trees by Guinea baboons (Papio papio Desmarest 1820) along the Gambia River.
The high extent to which Pterocarpus erinaceus trees were used by chimpanzees for nest building should be emphasized.In West Africa and Senegal, this tree species is commonly used for fuel, woodworking and medicinal purposes (Lykke 2000;Karon et al. 2003;Brunken et al. 2008).As it is a highly valued fodder tree, pruning is a serious threat (Bonkoungou et al. 2001), and the species is declining and disappearing (Diallo 1997;Koita 1998) offshoots, regrowth is low and therefore regression is accelerated (Fournier et al. 2001).In addition, fallow shortening will lead to its extinction (Camara 1997).
In Senegal, the species became so rare that logging, sawmills and woodworking companies had to stop exploiting this resource (P.I.N., pers.obs.and pers.com. of sawmill and woodworking company owners).As a result, though P. erinaceus is not registered on the IUCN Red List (but quantitative scientific data are lacking) as are the closely related species P. angolensis D.C. and P. brenanii L. Barb.& Torre, (IUCN 2010), it is apparently threatened in Senegal.
In conclusion, chimpanzees were found to show preferences when choosing trees to build their nests.Pterocarpus erinaceus, a tree that is threatened in Senegal outside national parks due to abusive cutting and pruning, was found to be the tree species that chimpanzees most preferred for nest building, though its numbers have been drastically decreased.This choice is likely related to the hardness of its wood.There is a high risk that abusive cutting of P. erinaceus could endanger chimpanzees outside of protected areas where most of the population of Senegal's chimpanzees live.Consequently, chimpanzee conservation outside of such areas seems to be partly dependent on the preservation of this tree species.Moreover, in the habitat destruction and global climate change setting, chimpanzees will have to cope with increased flora changes.The results of the present work will provide conservation managers with information on how to protect the species' natural environment and to make appropriate management decisions.
. Furthermore, as the stumps generate few Number of nests recorded on a same tree species; Nt -Number of trees of each species sampled in the habitat; % -Percentage; p-value -Fisher's exact test p-value.Bold figures: significant to extremely significant.