ORIGINAL ARTICLE

New tools suggest local variation in tool use by a montanecommunity of the rare Nigeria–Cameroon chimpanzee,Pan troglodytes ellioti, in Nigeria

Paul Dutton • Hazel Chapman

Received: 9 July 2014 / Accepted: 2 October 2014

� Japan Monkey Centre and Springer Japan 2014

Abstract Regional variations in tool use among chim-

panzee subspecies and between populations within the

same subspecies can often be explained by ecological

constraints, although cultural variation also occurs. In this

study we provide data on tool use by a small, recently

isolated population of the endangered Nigeria–Cameroon

chimpanzee Pan troglodytes ellioti, thus demonstrating

regional variation in tool use in this rarely studied sub-

species. We found that the Ngel Nyaki chimpanzee com-

munity has its own unique tool kit consisting of five

different tool types. We describe a tool type that has rarely

been observed (ant-digging stick) and a tool type that has

never been recorded for this chimpanzee subspecies or in

West Central Africa (food pound/grate stone). Our results

suggest that there is fine- scale variation in tool use among

geographically close communities of P. t. ellioti, and that

these variations likely reflect both ecological constraints

and cultural variation.

Keywords Afromontane � Camponotus � Dorylus �Pan troglodytes ellioti � Stingless bees � Tool use

Introduction

Regional variation in tool use among chimpanzees is well

documented (McGrew 1992; Whiten et al. 1999; Humle

2003). For example, the use of wood or stones to crack

nuts has only been observed in West Africa (Boesch et al.

1994; Matsuzawa 1994; Humle 2003) and in Cameroon

(Morgan and Abwe 2006) and termite mound perforators

have only been observed in the Republic of Congo (Sanz

et al. 2004).

Chimpanzees use various tools and techniques to obtain

honey and brood from Apini (honey) and Meliponini

(stingless) bee nests. The use of clubs to pound into

arboreal bee nests appears limited to Central Africa (Fay

and Carroll 1994; Hicks et al. 2005; Sanz and Morgan

2009). Complex tool sets to extract honey from subterra-

nean nests have only been documented in Central Africa

(Boesch et al. 2009; Sanz and Morgan 2009) while West

African chimpanzees mainly use their hands (Boesch and

Boesch 1990).

Chimpanzees use tools to prey on a range of ant species

(Schoning et al. 2007) and these tools are usually designed

to provoke ants to attack and cling to them. ‘Ant dipping’

(McGrew 1974) for terrestrial ants involves the use of

modified sticks (wands), stems or blades of grass, while

‘fishing’ (Sanz et al. 2010) for arboreal ant species involves

the use of slender probes. Again, there is much regional

variation in ant tools (Tutin et al. 1995; Hicks et al. 2005;

Fowler and Sommer 2007; Sanz et al. 2010; Yamamoto

et al. 2011), some of which obviously reflects different

prey species or materials available for tool use. However,

some of the variation described above may be cultural and

most likely reflects complex interactions between ecolog-

ical constraints, genetic variation and culture (Humle

2010). Observing variation among geographically close

communities does, however, help to reduce the genetic and

ecological components of variation and therefore provide

evidence for cultural variation (Whiten et al. 1999; van

Schaik 2009).

Previous observations on tool use in the rare Nigeria–

Cameroon subspecies Pan troglodytes ellioti are from the

P. Dutton (&) � H. Chapman

School of Biological Sciences, University of Canterbury,

Private Bag 4800, Christchurch 8140, New Zealand

e-mail: duttonpe@hotmail.com

123

Primates

DOI 10.1007/s10329-014-0451-1

Ebo Forest, Cameroon (Morgan and Abwe 2006; Abwe

and Morgan 2008) and Gashaka Gumti National Park

(from here on in this paper referred to as Gashaka),

Nigeria (Fowler 2006; Fowler and Sommer 2007). In Ebo

Forest, there is evidence of the chimpanzees using ter-

mite fishing tools (Abwe and Morgan 2008) and four tool

combinations for cracking Coula edulis nuts (wooden

anvil and wooden hammer, stone hammer and wooden

anvil, stone hammer and stone anvil; stone hammer

without anvil; Morgan and Abwe 2006). In Gashaka,

chimpanzees use stingless bee digging and probing sticks

to access both arboreal and ground nests of the largest

type of stingless bees (Meliponula, Plebeina; Sommer

et al. 2012), Dorylus ant dipping wands (Schoning et al.

2007) and ant fishing rods for Camponotus arboreal nests

(Fowler and Sommer 2007).

The Gashaka population is only 25 km away in a

straight line from our study site, Ngel Nyaki Forest Reserve

and until recently the two populations will have been

connected to some extent genetically (Knight 2013). Here

we provide evidence of a unique tool assemblage used by

the small, nearly isolated Ngel Nyaki population. The aims

of our study were to add to what little is published about

tool use by P. t. ellioti by: (1) documenting tools and tool

use within Ngel Nyaki Forest Reserve, and (2) determining

if this population shows differences/similarities in tool use

with the lowland Gashaka population (Fowler and Sommer

2007). As outlined above, such information will contribute

towards understanding the interplay of ecology, genetics

and culture on tool use in P. t. ellioti.

Methods

Study site

A community of approximately 18 chimpanzees (P. t. ell-

ioti; Dutton et al. 2014) reside within the 46 km2 of Ngel

Nyaki forest reserve, on the Mambilla Plateau (N11�000–11�300, E6�300–7�150) in Taraba State, Nigeria (Fig. 1).

While much of the reserve is savannah scrubland, there is

approximately 7.5 km2 of montane/submontane forest

(Chapman and Chapman 2001) in two fragments: Ngel

Nyaki forest (5.3 km2) and Kurmin Danko (2.2 km2),

restricted mainly to steep slopes protected from fire and

cattle grazing (Chapman et al. 2004). The forest ranges in

altitude from 1,400 to 1,600 m in elevation. The climate

has a distinct wet (mid April–late October) and dry season

with an average annual rainfall of 1,800 mm (Nigerian

Montane Forest Project rainfall data). The Ngel Nyaki

chimpanzees are almost entirely isolated from other pop-

ulations (Knight 2013), are not habituated and are difficult

to follow; however, they are vocal and are sometimes heard

‘drumming’, pounding the buttresses of large trees with

their fists and feet (Nyanganji et al. 2011).

Food resources commonly ([5 % of the diet/month)

consumed by the Ngel Nyaki chimpanzees include Ficus

spp. which occur in faeces during 9 months of the year

with an annual proportion of 32 % (Dutton and Chapman

2014). When Ficus spp. were not found in faecal samples

(during August, September and October), bark, grass,

leaves, Vitex doniana, Cordia millenii, Isolona deightonii,

Fig. 1 Ngel Nyaki Forest

Reserve (49 km2) showing the

reserve boundary (black line)

and the 7.5 km2 of forest split

into Ngel Nyaki forest and

Kurmin Danko

Primates

123

and Opilia amentacea were found (Dutton 2013). Dutton

and Chapman (2014) observed carpenter ants (Camponotus

nr. perrisii) in chimpanzee faeces during 3 months (March,

April and June), and stingless bees and beeswax during

1 month each of the year (April and August, respectively).

Data collection and analysis

Data on tool use were collected during reconnaissance and

transect walks over a 44-month period from April 2010 to

December 2013, for a total of 1,056 days in both dry

(October–March) and wet (April–September) seasons

during the course of a broader study on the ecology of P. t.

ellioti in Ngel Nyaki Forest Reserve (Dutton and Chapman

2014; Dutton et al. 2014). As the chimpanzees are not

habituated, we were never able to directly observe them

making or using tools. All our data are from objects found

at ‘tool sites’ accompanied by evidence of chimpanzee

presence, such as faeces, hair, dentition marks, foot/hand

prints, scent (from undiscovered faeces), nests, remaining

dietary items or any combinations of these. If suspected

tool sites did not have any evidence of chimpanzee pre-

sence they were discarded. We defined tools as being either

artefacts or naturefacts (sensu Fowler and Sommer 2007:

and references within); that is, they were either tools in the

sense that they had been fashioned by the chimpanzees, or

unaltered objects used by the chimpanzees to fulfil a par-

ticular purpose. We followed the tool nomenclature of

Fowler and Sommer (2007) to identify differences and/or

similarities of tool types because Gashaka, their study site,

is only 25 aerial km from Ngel Nyaki forest.

We measured the lengths and diameters of all stick tools

and their ends were categorised into proximal (the end

which was closer to the stem, branch or root of the plant

from which the tool was removed) and distal (the end

furthest from the stem, branch or root of the plant), based

on end diameter [wider proximal ends (Fowler and Som-

mer 2007)] and/or growing direction of (previously strip-

ped) side twigs, buds and/or leaves (directed away from the

proximal end). These ends were further placed into one of

five categories: sliced; blunt; frayed; pointed and split

(after Fowler and Sommer 2007) and measured from the tip

to the base of the end (defined as: the last part of the stick

to show structural alteration when measured from the tip),

running parallel with the stick. In addition we distinguished

between frayed ends of C30 mm and less than 30 mm in

length, because previous work (Sugiyama 1985) has made

this distinction and our doing so should allow for future

comparative studies. Animal ethics approval criteria

(University of Canterbury Animal Ethics Committee,

Approval # 2009/26R) disallowed the removal of any tools

from the forest, so measurements and evidence could only

be made/recorded at the time of discovery.

We compared dimensions (using t-tests) and character-

istics (using preliminary data) of tools made by chimpan-

zees from Ngel Nyaki with those made by chimpanzees

from neighbouring Gashaka (recorded by Fowler 2006).

All plant species were identified by consulting the lit-

erature (Keay 1990; Chapman and Chapman 2001; Haw-

thorne and Jongkind 2006), botanists from the Royal

Botanical Gardens, Kew, and the West African Plants

Facebook group. We were, however, unable to identify

several plant species. We made voucher specimens of all

species, which are kept at the Nigerian Montane Forest

Project herbarium.

Results

We found 113 individual tools belonging to five tool types

at 45 tool-sites over the 44 months (April 2010–December

2013) of opportunistic searches (Table 1). All tools we

observed were used for feeding, either on insects (n = 111;

four tool types) or fruit (n = 2; two tool types). We found

98 (86.7 %) tools associated with stingless bee (Melipo-

nini) nests (84 digging sticks and 14 probing sticks), 13

(11.5 %) tools associated with the procurement of subter-

ranean Camponotus ants (ten digging sticks and three

dipping wands) and two separate tools (1.8 %) associated

with the removal of exocarp from two fruit species

(Pseudospondias microcarpa and Symphonia globulifera).

Apparent tool assemblages (more than one tool type at the

Table 1 The dimensions of

vegetative tools used by

chimpanzees in Ngel Nyaki

Forest Reserve for insectivory

Tool dimensions Stingless bee

digging stick

Stingless bee

probing stick

Ant digging

stick

Ant dip

Number of tools 84 14 10 3

Number of tool sites 26 9 4 2

Mean tools/site (range) 3 (1–9) 2 (1–3) 2.5 (2–3) 1.5 (1–2)

Mean length ± SD (cm) 36.6 ± 15.3 35.4 ± 18.8 42.1 ± 27.8 57.7 ± 22.5

Range of lengths (cm) 6.0–75.5 11–73 10–102 32–74

Mean diameter ± SD (mm) 8.3 ± 2.7 8.8 ± 2.8 9.0 ± 2.0 6.3 ± 1.5

Range of diameters (mm) 3.0–19.1 4.0–13 6.1–13 5.0–8.0

Primates

123

same tool-site) were found at tool sites used to collect

stingless bee honey and brood, and on two occasions tool

assemblages were found at tool sites used to collect ants.

Table 2 illustrates the range of dimensions (whether

natural properties of the objects themselves (see Takemoto

et al. 2005) or fashioned by the chimpanzees) of the veg-

etative tools (n = 111) used in insectivory. In 97 %

(n = 110) of these tools it was the distal end (farthest away

from the plant body) which was used in digging, probing

and/or dipping. The proximal end was only used in 54 % of

these tools. Fifty-three percent of the tools were used at

both proximal and distal ends. All (n = 94) digging sticks

were used distally and were typically frayed (Table 2).

While more than 20 plant species were used to make

tools, there does not appear to be any consistency in which

species were used. Stems of Psychotria peduncularis (a

small shrub) showed the highest proportion of use as a tool

(23.6 %, n = 26), while stems of the tree Strombosia

scheffleri were used 12.7 % (n = 14) as well as the leaf

rachis of the tree Carapa oreophila 8.2 % (n = 9).

Tool types

Subterranean stingless bees (Meliponini), species

unidentified

Prey species While stingless bees are common across

Africa, species from the Cameroon Highlands remain

poorly described (Njoya 2010). The subterranean species

found at Ngel Nyaki forest store honey in an underground

nest into which lead several entrances concealed under leaf

litter (Fig. 2). The entrance tubes are made of wax

approximately 8 mm in diameter with 1- to 2-mm-thick

walls. The tubes always project upwards directly above the

underground nest. Such nests are common (38 nests were

discovered in the 44 months of this study) within Ngel

Nyaki forest.

Digging sticks (used to dig, perforate and enlarge nest

entrances) We found 26 tool sites with a total number of

84 digging sticks associated with stingless bee subterranean

nests (Fig. 3), with up to nine abandoned sticks

(mean = 3) of between 6 and 75.5 cm in length

(mean = 36.6, SD = 15.3) and 3.0–19.1 mm in diameter

(mean = 8.3, SD = 2.7; Table 1). All tools used proxi-

mally were also used distally, with all (n = 84) tools used

Table 2 Dimensions of tools used by chimpanzees for insectivory and frugivory in Ngel Nyaki Forest Reserve

Stingless bee digging

stick N = 84

Stingless bee probing

stick N = 14

Ant digging

stick N = 10

Ant dip

N = 3

Number of tools with proximal end use 51 5 2 1

Number of tools with distal end use 84 14 10 2

Number of tools used at both ends 51 5 2 0

Mean proximal end length ± SD (mm) 19.9 ± 25.6 29.5 ± 20 10.3 ± 2.83 5.1

Mean distal end length ± SD (mm) 12.1 ± 11.8 27.6 ± 29.7 24.1 ± 31.0 4.7 ± 2.12

Tools proximally stripped of bark (%) 10.7 0 10 0

Tools distally stripped of bark (%) 25.0 0 10 0

Tools stripped completely of bark (%) 19.0 28.6 10 33.3

Frays \30 mm (%) 89.3 0 60.0 0

Frays 30 mm and above (%) 10.7 0 40.0 0

Frayed ends (%) 97.7 0 100 0

Pointed ends (%) 0 0 0 66.6

Blunt ends (%) 2.38 64.30 0 33.3

Sliced ends (%) 17.9 35.70 0 0

Split ends (%) 2.38 0 0 0

Fig. 2 Exposed stingless bee entrance/exit tubes found under leaf

litter

Primates

123

distally and 61 % (n = 51) used proximally. The mean

proximal end length (19.9 mm, SD = 25.6) was signifi-

cantly longer than the distal end length (12.1 mm,

SD = 11.8; n (proximal) = 51, n (distal) = 83, U = 1410,

z = -3.2352, p = 0.0012). These tools were almost

exclusively frayed (97.7 %), with 10.7 % (n = 9) frayed

above 30 mm in length, 17.9 % (n = 15) sliced, 2.4 %

(n = 2) blunt and 2.4 % (n = 2) split. All tools were

stripped of leaves/twigs, most displaying soil contamina-

tion, along with 19.0 % (n = 16) completely stripped of

bark, 25 % (n = 21) distally stripped and 10.7 % (n = 9)

proximally stripped (Table 2). Of the 20 identified plant

species used by chimpanzees to construct tools, 16 were

used for stingless bee digging sticks (Table 3).

Probing sticks (used to probe nests and extract honey/

brood) Again associated with stingless bee subterranean

nests, we found nine tool sites with a total number of 14

probing sticks. We found up to three probing sticks per site

(mean = 2, n = 14) ranging from 11 to 73 cm in length

(mean = 35.4, SD = 18.8; Fig. 4; Table 1) and 4–13 mm in

diameter (mean = 8.8, SD = 2.8; Table 1). Distal ends of

tools (n = 14) were always used; however, only 35.7 %

(n = 5) of tools showed proximal use. When the proximal

end of a tool was used, the distal end was also used. There was

no significant difference between the mean proximal end

length (29.5 mm) and the mean distal end length (27.6 mm,

n (proximal) = 5, n (distal) = 14; U = 32.5, z = -0.1852,

p = 0.8493). Although we cannot be certain that these two

subterranean stingless bee tool types (digging and probing

sticks) had a different function, the differences in wear pattern

and their proximity to extracted honey or wax strongly sug-

gest that they differed from the digging sticks. In contrast to

the digging sticks, these tools were never frayed but their ends

were either sliced (35.7 %, n = 5) or blunt (64.3 %, n = 9;

Table 2). They always had all leaves and twigs removed, and

28.6 % (n = 4) were completely stripped of bark. They

showed little evidence of soil contamination, often (n = 11)

exhibited traces of honey, and/or its odour and on two occa-

sions beeswax. Probing tools were frequently (n = 5) found

together with chewed beeswax, which sometimes exhibited

chimpanzee dentition (Fig. 3). Seven of the nine tool sites

that were discovered also contained two to five digging sticks

(mean = 2.3, SD = 1.1). Two tool sites solely contained

probing sticks (one probing stick at the first site and two

probing sticks at the second site). Seven plant species were

used to construct stingless bee probing sticks (Table 3).

Stingless bee tool analysis The distal and proximal end

lengths of stingless bee probing sticks were significantly

longer than stingless bee digging sticks (U = 908,

z = 3.357, p \ 0.0003; U = 199, z = 2.054, p = 0.0399,

respectively). There was no significant difference between

the diameter (U = 677, z = 0.9036, p = 0.3662), or length

(U = 647.5, z = 0.6041, p = 0.5458) of tools used to

procure stingless bees.

Subterranean ants, Camponotus nr. perrisii

Prey species Camponotus nr. perrisii (formerly identified

by K.P. Yoriyo, Gombe State University, Nigeria), most

commonly subterranean, is the most common ant species

evident at Ngel Nyaki Forest Reserve (P. Dutton, pers. obs) and

was identified in chimpanzee faecal samples during March,

April and June (Dutton and Chapman 2014). Army ants,

Dorylus, are also present at Ngel Nyaki; they are epigaeic,

organizing conspicuous swarm raids on the ground surface

(Schoning et al. 2007) and have not been reported in the diet of

chimpanzees (Dutton 2013). Nests of C. nr. perrisii appear to

be either completely subterranean with only holes in the

Fig. 3 Subterranean stingless

bee nest dug out by

chimpanzees in Ngel Nyaki

forest. Inset shows chimpanzee

dentition marks in wax found at

the site

Primates

123

ground with multiple entrances/exits; or slight mounds (about

30 cm in height and 1 m in diameter) on the ground with one

major entrance/exit at the top of the mound. Differences in

substrate (e.g. compaction, moisture content, particle size)

may determine nest variations (P. Dutton, pers. obs.).

Ant-digging sticks [used to dig and enlarge nest entrances

and possibly stir (aggravate) ants] We assume chim-

panzees used ant digging sticks because on two occasions

we disturbed chimpanzees, which immediately fled, leav-

ing behind disturbed ant nests with abandoned tools. Some

of the tools showed fresh soil contamination and the ant

nests showed disturbance which appeared to be the result

of digging with the soil-contaminated tools. We found four

tool sites with a total number of ten ant-digging sticks

associated with C. nr. perrisii ant nests. We found up to

three digging sticks per site (mean = 2, n = 10, Fig. 5),

ranging from 10 to 102 cm in length (mean = 42.1,

SD = 27.8, n = 10) and 6.1–13 mm in diameter

(mean = 9.0, SD = 2.0). Distal ends of tools were always

(n = 10) used, while only 20 % (n = 2) of tools showed

proximal use. The proximal sample size was too small

(n = 2) to identify any significant difference between

proximal (mean = 10.3 cm, SD = 2.83) and distal end

lengths (mean = 24.1 cm, SD = 31.0). All ant digging

sticks (n = 10) had frayed ends, were stripped of leaves

and twigs, displayed soil contamination, and 30 % were

either completely stripped of bark (n = 1), distally stripped

of bark (n = 1) or proximally stripped of bark (n = 1). Six

plant species were used to construct ant digging sticks

(Table 3).

Ant dips (used to procure ants and transport to mouth)

We found two tool sites with two and one ant dips

Table 3 Plant species used by

chimpanzees at Ngel Nyaki to

construct different tool types.

Numbers indicate how many

tools were made from each plant

species

Plant species used Stingless bee Camponotus nr. perrisii n

Digging Probe Digging Dip

Aframomum angustifolium 1 1

Anthonotha noldeae 4 2 6

Carapa oreophila 4 3 2 9

Diospyros monbuttensis 1 1

Garcinia smeathmannii 6 1 7

Guarea sp. 1 1

Harungana madagascariensis 1 1

Keetia venosa 1 1 2 4

Leptaulus subscorpoidea 3 3

Leea guineensis 1 1

Newtonia buchananii 1 1

Pleiocarpa pycnantha 4 4

Psorospermum aurantiacum 2 2

Psychotria peduncularis 20 6 26

Strombosia scheffleri 11 2 1 14

Synsepalum aubrevillei 1 1

Tabernaemontana contorta 2 1 1 4

Tragia preussii 6 6

Unidentified 15 15

Xymalos monospora 3 3

Zanthoxylum leprieurii 1 1

n 84 14 10 3

Fig. 4 Stingless bee probing stick found at a disturbed stingless bee

nest

Primates

123

(respectively) associated with C. nr. perrisii ant nests. Ant

dips ranged from 32 to 74 cm in length (mean = 57.7,

SD = 22.5) and 5–8 mm in diameter (mean = 6.3,

SD = 1.5; Fig. 6). Two tools were used only at the distal end

and one tool was used only at the proximal end. Proximal and

distal end length was similar among the three tools (proxi-

mal = 5.1 mm, distal = 3.2 and 6.2 mm). Ant dips differed

from ant digging sticks in that they never showed soil-con-

tamination and their ends were either pointed or blunt. Ant

dips were always stripped of leaves and side twigs and were

either completely stripped of bark (n = 1) or had no bark

stripping (n = 2). At one tool site, two ant dips were dis-

covered with three digging sticks, and at the other one ant dip

was found with two digging sticks. Two plant species were

used to construct ant dips (Table 3).

Ant tool analysis Ant digging sticks had a significantly

wider diameter than ant probing sticks (U = 27,

z = 2.0284, p = 0.0425), however, there was no signifi-

cant difference in length (U = 21, z = 1.0142, p =

0.3105), or tool end length (proximal ? distal; U = 30,

z = 1.7321, p = 0.0833) between tools used to procure

ants.

Food-pound/grate against stone

These tools were observed twice, with a different fruit

species on each occasion. On the first occasion, on 04 April

2010, we discovered bunches (approximately ten) and

individual immature P. microcarpa fruits (individual fruit

dimension: 1 cm width 9 2 cm length) scattered along a

chimpanzee trail and observed chimpanzee foot and hand

prints in disturbed soil. The trail crossed a dried-up stream

bed, in which was a boulder (1 m in height, 0.75 m in

width, light grey in colour and rough, full of indentations)

covered with smashed, scraped, rasped exocarp, mesocarp,

juice and resins of P. microcarpa (equivalent to approxi-

mately 40 fruits). The ground around the boulder was also

littered in mashed fruit. The closest P. microcarpa fruiting

tree was at least 100 m away from the boulder and thus

circumstantial evidence suggests that the fruit had been

carried this distance along the chimpanzee trail before

being pressed and scrubbed/rolled/scraped against the

boulder to clean the seed of the bitter (senior author, pers.

obs.) exocarp and mesocarp before swallowing the seeds.

No seeds remained on or around the boulder and after a

thorough search (approximately 5 min) no hammers were

found with evidence of exocarp or resins/juices, even

though appropriate sized stones were readily available.

Seeds of P. microcarpa are common in the chimpanzees&faeces at Ngel Nyaki (Dutton 2013).

On the second occasion, on 20 May 2010, we discov-

ered, approximately 150 m off the transect, a group of 16

newly made chimpanzee nests with fresh (\24 h) faecal

matter littering the ground. On the ground and directly

beneath the nests we discovered a large, partly submerged

stone (greatest exposed dimension: 25 cm height 9 45 cm

width) covered in fresh (\24 h) S. globulifera fruit exocarp

(equivalent to approximately 12 fruits; Fig. 7). The sides of

Fig. 5 Digging sticks found at a disturbed nest of Camponotus nr.

perrisii

Fig. 6 Ant dipping wand found at a disturbed nest of Camponotus nr.

perrisii

Fig. 7 Stone used by chimpanzees to remove Symphonia globulifera

exocarp

Primates

123

the stone were covered in a thick layer of moss, with the

arch in the stone showing evidence of disturbance; moss

was disturbed and had been rubbed off from the arch in the

stone as though it had been used as an anvil on which to

pound the S. globulifera (fruit dimensions: 4 cm

width 9 6 cm length) to release the seeds from the

mesocarp which contains bitter latex. Most of the larger

pieces of exocarp were damaged (bruising and cracking)

and appeared consistent with impact blows with the arch of

the rock. There was no evidence in the vicinity (5 m

radius) to suggest hammers were used. Fruiting S. globu-

lifera trees were located within a 50-m radius of the stone.

Further analyses of tool measurements

There was no significant difference in the mean length of

tools among stingless bee digging sticks (mean = 36.6 cm,

SD = 15.3), stingless bee probing sticks (mean = 35.4 cm,

SD = 18.8), ant digging sticks [mean = 42.1 cm,

SD = 27.8; Kruskal–Wallis: H (adjusted) = 0.843, df = 2,

p = 0.6562] and ant dips [mean = 57.7 cm, SD = 22.5;

Kruskal–Wallis: H (adjusted) = 3.74, df = 3, p = 0.291,

imperfect approximation due to small sample size].

There was no significant difference in the mean diameter

of tools among stingless bee digging sticks (mean = 8.3 mm,

SD = 2.7), stingless bee probing sticks (mean = 8.8 mm,

SD = 2.8), ant digging sticks (mean = 9.0 mm, SD = 2.0;

Kruskal–Wallis: H = 1.65, df = 2, p = 0.4382) and ant dips

(mean = 6.3 mm, SD = 1.5; Kruskal–Wallis: H = 4.26,

df = 3, p = 0.3296, imperfect approximation due to small

sample sizes).

Comparison of Ngel Nyaki and Gashaka tool

dimensions

We found no significant differences in stingless bee dig-

ging stick length (n1 = 84, n2 = 9, t = 2.98, df–t = 48.1,

p = 0.9976) and diameter (n1 = 84, n2 = 9, t = -0.274,

df–t = 10.9, p = 0.3915) and stingless bee probing stick

length (n1 = 171, n2 = 14, t = -0.019, df–t = 14.7,

p = 0.4923) between Ngel Nyaki and Gashaka. However,

Ngel Nyaki stingless bee probing sticks were significantly

wider (n1 = 172, n2 = 14, t = -3.094, df–t = 17.1,

p = 0.0029) than those at Gashaka. There were no sig-

nificant differences in ant dipping wand length (n1 = 72,

n2 = 3, t = 1.95, df–t = 1.8, p = 0.1039) or diameter

(n1 = 71, n2 = 3, t = 0.063, df–t = 1.6, p = 0.5216)

between populations. There was also no difference in

length between Ngel Nyaki dipping wands (used for subter-

ranean Camponotus) and Gashaka’s fishing rods (used for

arboreal Camponotus; n1 = 38, n2 = 3, t = -2.925, df–

t = 1.5, p = 0.0508). However, the diameter of Camponotus

dipping wands found at Ngel Nyaki were significantly wider

than Gashaka’s Camponotus fishing rods (n1 = 38 n2 = 3,

t = -3.222, df–t = 1.5, p = 0.0428).

Discussion

The small, isolated population of approximately 18 P. t.

ellioti individuals in Ngel Nyaki Forest Reserve has its own

unique tool assemblage with an observed five tool types.

Four of these tool types may be part of tool sets, one set for

digging and extracting honey and brood from stingless bee

subterranean nests (stingless bee digging stick and stingless

bee probe) and the other set for the extraction of ants from

subterranean nests (ant digging stick and ant dip).

While we did not directly observe the chimpanzees using

these tools, we found strong evidence for their use. For

example, digging tools that we recovered from sites where

chimpanzees had obtained honey from subterranean stingless

bee nests had their ends caked in soil, most of them were

frayed at one or both ends, their bark was stripped to varying

extents and they had no odour of honey. This evidence sug-

gests that these sticks had been used to dig through the soil

and enlarge nest entrances (Tutin et al. 1995; Fowler and

Sommer 2007). The wax and dentition marks we observed

alongside the probes is indicative of these tools being used to

determine the presence of honey and brood in the nest, veri-

fying access into the hive, testing the structural integrity of the

nest (Sanz and Morgan 2009) and possibly to pry out the

honey itself. Tool sites that only contained stingless bee

probes (without digging sticks) suggest that either these nests

did not require digging because they were easy to access (e.g.

nests were not built at great depths, loose soils, thin or soft

batumen walls), chimpanzees used their hands to dig, or

possibly they removed the digging tools from the site to re-use

elsewhere (e.g. Sanz et al. 2010).

The ant digging stick is notable in that tools used for

digging after ants have only been reported a few times for

catching Dorylus army ants in Bossou, Guinea and in the

Goualougo Triangle, Republic of Congo (Sugiyama 1995;

Sanz et al. 2010; respectively). At Ngel Nyaki the ants

were Camponotus nr. perrisii. Moreover, Camponotus spp.

at Ngel Nyaki are subterranean, which differs from studies

elsewhere where they are arboreal (Nishida and Hiraiwa

1982; Fowler and Sommer 2007; Yamamoto et al. 2011).

Ant dips are most probably used to transport ants from

the nest into the mouth (Sugiyamaet al. 1988; Alp 1993).

The term ‘ant dipping wand’ has previously been reserved

for use with harvesting Dorylus species (see Whiten et al.

2001); however, as described here this term needs to be

expanded in its meaning to include Camponotus species, as

to our knowledge, they have not been recorded elsewhere.

Alternatively a new tool type must be defined such as

‘‘Camponotus dip’’ to distinguish between ant genera.

Primates

123

Our discovery of the food-pound/grate against stone

used to remove the skin and pulp from fruits of P. micro-

carpa and S. globulifera is especially interesting in that this

is the first record of this tool type being used in West

Central Africa. This technology differs from percussive

extractive foraging (such as nut-cracking, baobab-smash-

ing, Strychnos-smashing and pestle-pounding; Koops et al.

2010) in that the food item does not have a hard layer

which requires smashing/cracking, but instead has an

undesirable exocarp which requires removal. Other exam-

ples of non-extractive technology are stone and wooden

cleavers, and stone anvils, used by chimpanzees in the

Nimba Mountains (Guinea) to fracture large fruits of Tre-

culiaa africana into manageable pieces (Koops et al.

2010). Other records of food being pounded onto stones

come from Mahale, Tanzania (Nishida and Uehara 1983);

Gombe, Tanzania; the Tai‹ forest, Cote d’Ivoire; Assirik,

Senegal (Whiten et al. 2001) and Bili, D.R.C. (Hicks

2010). Of relevance to this study is that food-pound/grate

stones have not been found in P. t. ellioti populations in

Cameroon or neighbouring Gashaka. S. globulifera is rel-

atively common in Gashaka (Dishan et al. 2010) and very

likely to be present in Ebo Forest (M. Cheek, pers. comm.

2012) The use of the food pound/grate stones by chim-

panzees in Ngel Nyaki most resembles reported behaviour

in capuchin monkeys (Sapajus libidinosus) from Fazenda

Boa Vista, Brazil. There, the capuchins use two processing

techniques (rubbing/piercing and stone tool use) to avoid

the caustic chemicals protecting the nutritious kernel of

cashew nuts (Sirianni and Visalberghi 2013).

Differences and similarities in tool use between Ngel

Nyaki and Gashaka

Of note is that we found both similarities and differences in

tools and tool use between the Ngel Nyaki population and

the nearby Gashaka population of P. t. ellioti (Fowler

2006), only 25 aerial km away. Similarities included the

presence of stingless bee digging and probing sticks, ant

dipping wands, absence of termite procuring tools and

preferential use of distal ends. Differences included the

absence of food pound/grate stones at Gashaka and absence

of honeybee tools and ant fish rods (for arboreal Camp-

onotus ants) at Ngel Nyaki.

While analysis of the raw data is necessary for detailed

comparisons between the studies, there is a high likelihood

that ecological factors contribute to the difference in tools

and tool use between these two neighbouring populations.

For example, the difference in the selection and con-

sumption of ant species using ant dips is likely a result of

species availability (Dorylus at Gashaka versus Campon-

otus at Ngel Nyaki), likewise the use of ant fishing rods at

Gashaka and their absence at Ngel Nyaki may reflect the

arboreal nature of Camponotus chrysurus ants at Gashaka

(Sommer et al. 2012) and the apparent scarcity of arboreal

ants at Ngel Nyaki.

The fact that we found no significant differences in some

tool dimensions between Ngel Nyaki and Gashaka

(Table 4) but significant differences in others may also

have ecological explanations. For example, the fact that the

length of stingless bee digging sticks and stingless bee

probing sticks were the same in both sites but that stingless

bee probing sticks were significantly wider in Ngel Nyaki

than in Gashaka might reflect the different structure of

stingless bee nest types between the two sites. In Gashaka

they are arboreal and subterranean, while at Ngel Nyaki

only subterranean nests were observed. Arboreal nests

likely require thinner probing tools compared to subterra-

nean nests, as nest entrances are immersed within the tree

bark and as a result tend to be thinner. In contrast, digging

sticks are used to access subterranean nests at both sites.

Despite the fact that the chimpanzees in each population

were eating different ant genera (Ngel Nyaki Camponotus

versus Gashaka Dorylus) with different defence strategies

[Dorylus (aggressive) and Camponotus (subtle)] we found

no significant differences in ant dipping wand length or

diameter, presumably because both dipping wands are used

on subterranean ant nests; we had predicted that the dif-

ference in defence behaviours would select for significantly

longer dipping wands used for Dorylus than those used for

Camponotus.

There was also no difference in length between Ngel

Nyaki dipping wands (used for subterranean Camponotus)

and Gashaka’s fishing rods (used for arboreal Campono-

tus). However, the diameter of Camponotus dipping wands

found at Ngel Nyaki were significantly wider than Ga-

shaka’s Camponotus fishing rods which may result from

the difference between accessing a subterranean Campon-

otus nest (Ngel Nyaki) and accessing an arboreal Camp-

onotus nest (Gashaka). Thinner tools may be required to

access arboreal ant nests as nest entrances are immersed

within the tree bark and as a result tend to be thinner or

more restricted than subterranean nests.

The fact that Dorylus ants are present at Ngel Nyaki but

the chimpanzees appear to be ignoring them (i.e. no evi-

dence of tool use or remains in their faeces; Dutton 2013)

and that Dorylus ants are consumed in great proportions at

Gashaka (Pascual-Garrido et al. 2013), may reflect cultural

variation. However, these comparisons are speculative as

the sample size from Ngel Nyaki is small (Table 4).

Morgan and Abwe (2006) found that P. t. ellioti in Ebo

Forest, Cameroon, used hammers and anvils to crack open

Coula edulis nuts with combinations of four tools: wooden

anvil and wooden hammer, stone hammer and wooden

anvil, stone hammer and stone anvil and stone hammer

without anvil. None of these behaviours were recorded in

Primates

123

either the Gashaka or Ngel Nyaki populations, despite the

presence of Elaeis guineensis and Detarium microcarpum

nuts in Gashaka (Fowler and Sommer 2007). There have

not been any nuts identified at Ngel Nyaki; however, seeds

of Carapa ereophila do have similar characteristics (hard

outer shell; P. Dutton, pers. obs.) but these have not been

identified in the diet of the chimpanzees (Dutton and

Chapman 2014). The Ebo Forest population also differs

from the Nigerian populations in the use of termite fishing

tools. The fact that termite mounds (Macrotermes) are

present within both Ngel Nyaki and Gashaka, but no evi-

dence of tools are associated with them may reflect com-

mon ecological constraints (such as low abundance of

mounds, suitable materials to manufacture tools and ter-

mite responsiveness to provocation; Fowler 2006) or a

cultural variant (see Fowler and Sommer 2007). Addi-

tionally, small termite mounds (about 30 cm high; P.

Dutton, pers. obs.) are present outside of the forest but are

rare within the forest at Ngel Nyaki (Chapman pers.

comm.) with the chimpanzee population seldom venturing

outside (P. Dutton pers. obs.) this may reflect both eco-

logical constraints and cultural variation. Tools used by

chimpanzees to procure honey from African honeybees

(Apis mellifera) have been observed in Gashaka but we

found no evidence of such tools at Ngel Nyaki, despite

eight encounters with honeybee nests during this study.

Table 4 Comparison of the tools discovered at Ngel Nyaki (NN) with tools discovered by Fowler (2006) at Gashaka (Ga). There was no

evidence of ant digging sticks in Gashaka or likewise ant fishing rods and honey bee probes at Ngel Nyaki

Tool Stingless-bee

digging stick

Stingless-bee

probing stick

Ant dipping

wandaCamponotus

fishing rod

Study site NN Ga NN Ga NN Ga Gac

Tool sites n 26 4 9 15 2 17 3

Tools n 84 15 14 178 3 73 38

Tools/site Mean 3 3.8 2 11.9 1.5 4.3 12.7

Min 1 1 1 1 1 1 4

Max 9 5 3 48 2 16 20

Tool length (cm) n 84 9 14 171 3 72 38

Mean 36.6 29.6 35.4 35.3 57.7 83.8 19.5

Median 36.1 30 37.5 33 17.9 81 17

SD 15.3 6.4 18.8 19.3 22.5 27.4 8.4

Min 6 20 11 7 32 28 5

Max 75.5 37 73 105 74 160 44

Tool diameter at midpoint (mm) n 84 9 14 172 3 71 38

Mean 8.3 8.1 8.8 6.3 6.3 6.4 1.2

Median 8.4 9 8.25 6 8 6 1

SD 2.58 2 2.8 4 2.73 2.1 0.9

Min 3 5 4 2 5 3 0

Max 19.1 11 13 50 8 12 6

Distal end length (mm): length of fray n 82 7 14b 81 2b 30 6

Mean 12.1 31.7 29.5 32.3 4.7 28.2 4.9

Median 8.25 23 23 27 4.7 20 6

SD 11.9 18.4 21.6 26.9 2.12 23.7 3.2

Min 2 14 5 3 3.2 3 0

Max 73 58 71 160 6.2 95 8

Proximal end length (mm): length of fray n 30 2 5b 38 1b 15 8

Mean 13.75 67.5 27.6 30.7 5.1 43.9 19.2

Median 10.15 68 18 26 5.1 29 6

SD 9.05 38.9 24 16.8 0 39.9 23.4

Min 5.4 40 12 3 5.1 15 3

Max 40 95 70 86 5.1 150 61

a Differences in prey species between NN (Camponotus) and Ga (Dorylus)b No fray to tool ends was observed in NN tools, therefore the length of the other end (i.e. sliced, pointed, etc.) is providedc Arboreal ant species Camponotus chrysurus

Primates

123

Although more research is clearly needed to understand

the details of behavioural diversity amongst this population

of P. t. ellioti, the current study has made it clear that even

nearby populations of the subspecies can differ dramati-

cally in their material culture.

Acknowledgments Thanks to Taraba State Forestry for logistical

support and the Nigerian Montane Forest Project for field facilities

and field assistance, especially to Alfred Moses and Suleiman A. Idi.

Funding was from the North of England Zoological Society (Chester

Zoo), Nexen Inc., A. G. Leventis Foundation and Primate Conser-

vation Inc. (PCI).

The sampling protocol used in this study complied with the ethical

standards in the treatment of animals with the guidelines laid down by

the Primate Society of Japan, NIH (US), EC Guide for animal

experiments, was approved by the University of Canterbury Animal

Ethics Committee, Approval # 2009/26R and was in compliance with

the laws governing animal research in Nigeria.

References

Abwe EE, Morgan BJ (2008) The Ebo Forest: four years of

preliminary research and conservation of the Nigeria–Cameroon

chimpanzee (Pan troglodytes vellerosus). Pan Africa News

15:26–29

Alp R (1993) Meat eating and ant dipping by wild chimpanzees in

Sierra Leone. Primates 34:463–468

Boesch C, Boesch H (1990) Tool use and tool making in wild

chimpanzees. Folia Primatol 54:86–99

Boesch C, Marchesi P, Marchesi N, Frut B, Joulian F (1994) Is nut

cracking in wild chimpanzees a cultural behaviour? J Hum Evol

26:325–338

Boesch C, Head H, Robbins MM (2009) Complex tool sets for honey

extraction among chimpanzees in Loango National Park, Gabon.

J Hum Evol 56:560–569

Chapman JD, Chapman HM (2001) The forests of Taraba and

Adamawa States, Nigeria. An ecological account and plant

species checklist. University of Canterbury, Christchurch

Chapman HM, Olsen SM, Trumm D (2004) An assessment of

changes in the montane forests of Taraba State, Nigeria, over the

past 30 years. Oryx 38:282–290

Dishan EE, Agishi R, Akosim C (2010) Women’s involvement in non

timber forest products utilization in support zones of Gashaka

Gumti National park. J Res For Wildl Environ 2:73–84

Dutton P (2013) Chimpanzee (Pan troglodytes ellioti) ecology in a

Nigerian montane forest. Ph.D. thesis. University of Canterbury

Dutton P, Chapman H (2014) Dietary preferences of a submontane

population of the rare Nigerian-Cameroon chimpanzee (Pan

troglodytes ellioti) in Ngel Nyaki Forest Reserve, Nigeria. Am J

Primatol. doi:10.1002/ajp.22313

Dutton P, Chapman H, Moltchanova E (2014) Secondary removal of

seeds dispersed by chimpanzees in a Nigerian montane forest.

Afr J Ecol. doi:10.1111/aje.12138

Fay JM, Carroll RW (1994) Chimpanzee tool use for honey and

termite extraction in central Africa. Am J Primatol 33:309–317

Fowler A (2006) Behavioural ecology of chimpanzees (Pan troglo-

dytes vellerosus) at Gashaka, Nigeria. Ph.D. thesis. University

College London

Fowler A, Sommer V (2007) Subsistence technology in Nigerian

chimpanzees. Int J Primatol 28:997–1023

Hawthorne WD, Jongkind CCH (2006) Woody plants of western

African forests, a guide to the forest trees, shrubs and lianas from

Senegal to Ghana. Kew Publishing, Kew

Hicks TC. 2010 A chimpanzee mega-culture? Exploring behavioral

continuity in Pan troglodytes schweinfurthii across northern DR

Congo. Dissertation, University of Amsterdam, Netherlands

Hicks TC, Fouts RS, Fouts DH (2005) Chimpanzee (Pan troglodytes

troglodytes) tool use in the Ngotto Forest, Central African

Republic. Am J Primatol 65:221–237

Humle T (2003) Behaviour and ecology of chimpanzees in West

Africa. In: Kormos R, Boesch C, Bakarr MI, Butynski TM (eds)

Status survey and conservation action plan: West African

chimpanzees. IUCN, Gland, pp 13–19

Humle T (2010) How are army ants shedding new light on culture in

chimpanzees. In: Lonsdorf EV, Ross SR, Matsuzawa T (eds) The

mind of the chimpanzee: ecological and experimental perspec-

tives. University of Chicago Press, Chicago, pp 116–126

Keay RWJ (1990) Trees of Nigeria. Clarendon Press, New York

p 486

Knight A (2013) The genetic structure and dispersal patterns of the

Nigeria-Cameroon Chimpanzee (Pan troglodytes ellioti). MSc

thesis. University of Canterbury, New Zealand

Koops K, McGrew WC, Matsuzawa T (2010) Do chimpanzees (Pan

troglodytes) use cleavers and anvils to fracture Treculia africana

fruits? Preliminary data on a new form of percussive technology.

Primates 51:175–178

Matsuzawa T (1994) Field experiments on use of stone tools by

chimpanzees in the wild. In: Wrangham RW, McGrew WC, de

Wall FBM, Heltne P (eds) Chimpanzee cultures. Harvard

University Press, Cambridge, pp 351–370

McGrew WC (1974) Tool use by wild chimpanzees in feeding upon

driver ants. J Hum Evol 3:501–508

McGrew WC (1992) Chimpanzee material culture. Implications for

human evolution. Cambridge University Press, Cambridge

Morgan BJ, Abwe EE (2006) Chimpanzees use stone hammers in

Cameroon. Curr Biol 16:R632–R633

Nishida T, Hiraiwa M (1982) Natural history of a tool-using behavior

by wild chimpanzees in feeding upon wood-boring ants. J Hum

Evol 11:73–99

Nishida T, Uehara S (1983) Natural diet of chimpanzees (Pan

troglodytes schweinfurthii): long-term record from the Mahale

Mountains, Tanzania. Afr Stud Monogr 3:109–130

Njoya MTM (2010) Diversity of stingless bees in Bamenda Afromon-

tane Forests—Cameroon: nest architecture, behaviour and labour

calendar. Dissertation, Hohen Landwirtschaftlichen Fakultat der

Rheinischen Friedrich-Wilhelms-Universitat zu Bonn

Nyanganji G, Fowler A, McNamara A, Sommer V (2011) Monkeys

and apes as animals and humans: ethno-primatology in Nigeria&sTaraba Region. In: Sommer V, Ross C (eds) Primates of

Gashaka. Springer, Heidelberg, pp 101–134

Pascual-Garrido A, Umaru B, Allon O, Sommer V (2013) Apes

finding ants: predator–prey dynamics in a chimpanzee habitat in

Nigeria. Am J Primatol 75:1231–1244

Sanz C, Morgan D (2009) Flexible and persistent tool-using strategies in

honey gathering by wild chimpanzees. Int J Primatol 30:411–427

Sanz CM, Morgan D, Gulick S (2004) New insights into chimpan-

zees, tools, and termites from the Congo Basin. Am Nat

164:567–581

Sanz CM, Schoning C, Morgan DB (2010) Chimpanzees prey on

army ants with specialized tool set. Am J Primatol 72:17–24

Schoning C, Ellis D, Fowler A, Sommer V (2007) Army ant prey

availability and consumption by Chimpanzees at Gashaka

(Nigeria). J Zool 271:125–133

Sirianni G, Visalberghi E (2013) Wild bearded capuchins process

cashew nuts without contacting caustic compounds. Am J

Primatol 75:387–393

Sommer V, Buba U, Jesus G, Pascual-Garrido A (2012) Till the last

drop. Honey gathering in Nigerian chimpanzees. Ecotropica

18:55–64

Primates

123

Sugiyama Y (1985) The brush-stick of chimpanzees found in south-

west Cameroon and their cultural characteristics. Primates

26:361–374

Sugiyama Y (1995) Tool-use for catching ants by chimpanzees at

Bossou and Monts Nimba, West Africa. Primates 36:193–205

Sugiyama Y, Koman J, Bhoye Sow M (1988) Ant-catching wands of

wild chimpanzees at Bossou, Guinea. Folia Primatol 51:56–60

Takemoto H, Hirata S, Sugiyama Y (2005) The formation of the

brush-sticks: modification of chimpanzees or the by-product of

folding? Primates 46:183–189

Tutin CEG, Ham R, Wrogemann D (1995) Tool use by chimpanzees

(Pan t. troglodytes) in the Lope Reserve, Gabon. Primates

36:181–192

van Schaik CP (2009) Geographical variation in the behavior of wild

great apes: is it really cultural? In: Laland KN, Galef BG (eds)

The question of animal culture. Harvard University Press,

Cambridge, Massachusetts, pp 70–98

Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,

Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (1999)

Cultures in chimpanzees. Nature 399:682–685

Whiten A, Goodall J, McGrew WC, Nishida T, Reynolds V,

Sugiyama Y, Tutin CEG, Wrangham RW, Boesch C (2001)

Charting cultural variation in chimpanzees. Behaviour

138:1481–1516

Yamamoto S, Yamakoshi G, Humle T, Matsuzawa T (2011) Ant

fishing in trees: invention and modification of a new tool-use

behavior. In: Matsuzawa T, Humle T, Sugiyama Y (eds) The

Chimpanzees of Bossou and Nimba. Springer, Japan,

pp 123–130

Primates

123