RESEARCH ARTICLE

Dietary Preferences of a Submontane Population of the RareNigerian‐Cameroon Chimpanzee (Pan troglodytes ellioti)in Ngel Nyaki Forest Reserve, Nigeria.

PAUL DUTTON* AND HAZEL CHAPMANSchool of Biological Sciences, University of Canterbury, Christchurch, New Zealand

We investigated the dietary preferences of chimpanzees residing in a Nigerian submontane forest usinga combination of fecal analysis, observations of feeding remains, evidence from feeding tools and fruitingphenological data between April 2010 and March 2011. A total of 495 fecal samples were collected inwhich 52 fruit taxa were identified as having being consumed by chimpanzees, including 22 identified tospecies level and two identified to genus level. Ficus (seven species) was the most common seed genusidentified, occurring in 61.2% of all fecal samples. Based on fecal analysis and phenological data, NgelNyaki chimpanzees do not solely consume fruits based on their availability within the habitat; while theproportion of fruit consumed did reflect the relative availability of fruit in the forest for some fruitspecies, Ficuswas a preferred fruit evenwhen scarce. In contrast, the proportion consumed of other fruitspecies was low relative to the abundance of their fruit available in the forest. Our results from the RankPreference Index (RPI) suggest that relative preferences in fruit are seasonal. We discuss the role ofFicus in the diet of chimpanzees in Ngel Nyaki Forest Reserve. Am. J. Primatol. © 2014Wiley Periodicals, Inc.

Key words: chimpanzee; food preference; food availability; Nigeria

INTRODUCTION

Chimpanzees are omnivorous and while fruit istheir preferred food [Wrangham, 1977] they consumea wide range of food types including seeds, bark,woody pith, flowers, tree gum, roots, tubers, andfoliage of tropical trees, mushrooms and algae,insects, other invertebrates, birds, and small mam-mals [Humle, 2011]. Different chimpanzee communi-ties incorporate different food items into their diet sothat some food types may be ignored in onecommunity but consumed in another [Fowler &Sommer, 2007; Goodall, 1986; McGrew, 1992]. Chim-panzees change their diet according to seasonal andannual variations in the abundance and diversity offruit species [Basabose, 2002; Humle, 2003; Yama-giwa&Basabose, 2006], which is thought to influencetheir technology in relation to tool‐use [Fowler &Sommer, 2007; Goodall, 1986; McGrew et al., 1979].They have been shown to prefer food items with highsugar content or caloric intake rate, regardless ofprotein content [Matsumoto‐Oda & Hayashi, 1999;Reynolds et al., 1998; Wrangham et al., 1991].

Thediet ofwild chimpanzees (Pan troglodytes) hasbeen well studied in a range of habitats from tropicalrain forests to savannah and woodland mosaic forest[McGrew, 1983; Newton‐Fisher, 1999; Nishida &Uehara, 1983; Sabater Pi, 1979; Sugiyama &Koman, 1992; Tutin & Fernandez, 1993; Wrangham,

1977; Yamagiwa & Basabose, 2006]. With foodavailability in tropical forests varying seasonally,annually and spatially, long‐term data on foodsconsumed by chimpanzees is essential for futurehabitat management and conservation initiatives.Expanding current knowledge on seed dispersal,predator/prey interactions, and the presence/absenceof key dietary itemsmayprovide essential informationabout the environment in which chimpanzees reside.

Research on the Nigerian‐Cameroon chimpanzee(P. t. ellioti) is summarized in the Regional ActionPlan [Morgan et al., 2011] which provides anoverview of its distribution and conservation.

Contract grant sponsor: North of England Zoological Society;contract grant sponsor: Nexen, Inc.; contract grant sponsor:A. G. Leventis Foundation; contract grant sponsor: PrimateConservation, Inc. (PCI)

Conflicts of interest: None.

�Correspondence to: Paul Dutton, University of Canterbury,Private Bag 4800, Christchurch 8140, New Zealand.E‐mail: duttonpe@hotmail.com

Received 23 December 2013; revised 5 June 2014; revisionaccepted 12 June 2014

DOI: 10.1002/ajp.22313Published online XX Month Year in Wiley Online Library(wileyonlinelibrary.com).

American Journal of Primatology

© 2014 Wiley Periodicals, Inc.

Significant study sites for the Nigerian‐Cameroonchimpanzee include Ngel Nyaki, Nigeria [Beck &Chapman, 2008; Dutton, 2013], Gashaka, Nigeria[Fowler, 2006; Sommer et al., 2004; Sommer & Ross,2010], and Ebo Forest & Mbam et Djerem NationalPark, Cameroon [Gonder et al., 2006; Morgan &Abwe, 2006].

Investigations into the diet of this rare subspe-cies of chimpanzee (P. t. ellioti) have been neglected.While vague reports are available on the diet ofchimpanzees within studies focused on tool‐use inEbo forest, Cameroon [Morgan & Abwe, 2006] andtool‐use and plant food ecology in Gashaka‐GumtiNational Park, Nigeria [Fowler, 2006] the availabili-ty of published data is limited.

The chimpanzees of Ngel Nyaki Forest Reserve,the focus of this study, are not at all habituated to thepresence of human observers [Beck & Chapman,2008; pers. obs.]. Thus, analysis of feces is the mostappropriate method to describe their diet [Basabose,2002]. Fecal analysis is useful in identifying fruitseaten by chimpanzees, as many swallowed seedspassed out in feces can be collected and identified tospecies level [Basabose, 2002; McGrew et al., 1988;Tutin&Fernandez, 1993]. Fecal analysis also revealsthe frequency of dietary constituents [Tutin &Fernandez, 1992] and allows quantification of sea-sonal and inter‐annual comparisons within sites[Basabose, 2002; Tutin & Fernandez, 1993].

Seasonal fluctuations in tree fruit availabilityhave been documented at numerous chimpanzeestudy sites, including Kahuzi, DRC [Basabose, 2002],Kalinzu Forest, Uganda [Furuichi et al., 2001], andBossou, Guinea [Yamakoshi, 1998]. Based on thechimpanzees’ strong dietary preference for ripefruits, environments with less seasonality in fruitavailability, or with the availability of high‐qualityfallback foods, may reduce levels of food competitionand allow chimpanzees to maintain a high‐qualitydiet year round [Moscovice et al., 2007]. Therefore, inorder to understand dietary preferences of chimpan-zees it is necessary to study tree fruiting phenologywithin the geographical range of the study popula-tion. Tool use and feeding remains can also provideimportant information on the diet of chimpanzees,particularly for foods that are consumed but that arenot evident or are unidentifiable in feces, such as softbodied invertebrates, fruit pulp, soft seeds, andhoney.

The aims of this studywere to add to what little ispublished about the dietary preferences of P. t. elliotiby (i) documenting the seasonal diet of a smallsubmontane population and (ii) determining if thispopulation showed preferences for particular fruitspecies. Such knowledge has implications for seeddispersal in the small isolated fragment of Nigeriansubmontane forest.

METHODS

Study Site

Ngel Nyaki Forest Reserve (46 km2) is locatedtoward the western escarpment of the MambillaPlateau (N11° 000–11° 300, E6° 300–7° 150) in TarabaState, Nigeria (Fig. 1). The forested area of thereserve totals 7.5 km2 and comprises submontaneforest at 1,400–1,600m elevation [Chapman &Chapman, 2001]. The total population size of P. t.ellioti in Ngel Nyaki Forest Reserve has beenobserved and estimated at 16 weaned individuals[Dutton, 2013]. This methods used in this projectwere approved by the University of CanterburyAnimal Ethics Committee, Approval # 2009/26R;and the research adhered to the American Society ofPrimatologists principles for the ethical treatment ofprimates and was in compliance with the lawsgoverning animal research in Nigeria.

Data Collection

In order to determine the annual diet of the NgelNyaki forest chimpanzee population, we collectedfresh feces opportunistically but with equal samplingeffort, from approximately 8 am to 4 pm, 24 days/month, fromApril 2010 toMarch 2011. This samplingprotocol was approved by the University of Canter-bury Animal Ethics Committee, Approval # 2009/26R; and the research adhered to the AmericanSociety of Primatologists principles for the ethicaltreatment of primates and was in compliance withthe laws governing animal research in Nigeria. Onlyfresh chimpanzee feces (up to 24hr old) werecollected; age was judged from scent, moisturecontent, collection under fresh nests, and/or followingchimpanzee vocalizations. Fecal samples weresluiced in 1mm mesh sieves following approachesby Basabose [2002] and Yamagiwa and Basabose[2006]. We noted and/or photographed any non‐identifiable vegetative remnants in the fresh fecesto allow us to more efficiently locate parent trees foridentification. The samples were then placed intoreferenced paper envelopes and dried in a dryingoven, amodified 44 gallon drumwith a kerosene stoveserving as a heat source, to a constant mass (OhausSP202 lab balance) between two readings takenmorethan 20min apart. The dried samples were thenstored in plastic bags. We examined any undigestedparticles remaining in the feces and the contents ofeach sample were divided into (i) fruits (seeds, fruitfiber, and fruit exocarp), (ii) foliage (leaf fiber andundigested fragments of leaves), (iii) bark, (iv) frag-ments of insects or other animal matter, and (v) otheritems such as moss, roots, stones and internalparasites. (ii–v are provided in SupplementaryInformation due to low presence in fecal samples).

We counted and weighed all constituents tonearest 0.01 g and the proportional percentage of

Am. J. Primatol.

2 / Dutton and Chapman

each of the contents was established based on driedmass. All contents that were counted were identifiedto species level whenever possible, and measuredagainst total driedmass of the fecal sample.Measure-ments of the focal fecal remnants are provided inTable 1. Representative samples of all items identi-fied in chimpanzee feces are kept in the herbarium attheNigerianMontane Forest Projectfield station.Weattempted to identify fecal remnants by locatingparent trees, germinating unidentified seeds (to littleeffect, either seeds did not germinate, were predated,or did not grow at a rate allowing the authors toidentify the species over the course of the study) andconsulting literature [Chapman & Chapman, 2001;

Hawthorne and Jongkind, 2006; Keay, 1990]. Morerecently theWest African Plants Facebook group hashelped. There is also a progressive checklist of plantsfrom Ngel Nyaki at http://www.afromontane.canter-bury.ac.nz/checklist.shtml.

To further contribute to the assessment of thechimpanzee diet, we analyzed their tools to establishreasons for use. Artifacts as well as objects usedwithoutmodificationwere assigned to particular foodsources based on evidence such as traces of foods suchas honey or dead insects on the end of a tool, sticktools found close to a bee hive or ant nest, andmodifications to objects made by the chimpanzeessuch as fraying of stick ends.

Fig. 1. Ngel Nyaki forest (5.3 km2 Southern forest) andDanko forest (2.2 km2Northern forest) showing the transects used for collection ofphenology data (white lines) and the ranging area of the chimpanzees (black line; based on fecal and nesting data waypoints [black dots]).

Am. J. Primatol.

Dietary Preferences of Chimpanzees / 3

TABLE

1.The26

PlantSpec

iesId

entified

Fro

mSee

dsof

495Chim

pan

zeeFec

alSam

plesin

Nge

lNya

kiFor

estRes

erve

Spe

cies

Fam

ily

Lifeform

Sam

ple

See

ddimen

sion

sFecal

mea

sures

Ave

rage

leng

th(m

m)

Ave

rage

width

(mm)

Ave

rage

height

(mm)

Ave

rage

driedmas

s(g)

Num

ber

offeces

Ave

rage

numbe

rof

seed

s/feces

Max

numbe

rof

seed

s/feces

Min

numbe

rof

seed

s/feces

Ave

rage

dried

mas

s(g)

Max

dried

mas

s(g)

Min

dried

mas

s(g)

Total

numbe

rof

seed

s

Afram

omum

angu

stifolium

Zing

iberacea

eGeo

phyte

See

d/Fiber

3.5

33

0.01

207.68

251

0.17

0.61

0.01

146

Beilsch

miedia

man

nii

Lau

raceae

Tree

See

d—

——

—2

58

212

.06

19.28

4.84

10Celtisgo

mph

ophylla

Can

naba

ceae

Tree

See

d—

——

—3

37

10.17

0.32

0.05

9Chionan

thusafrica

nus

Oleacea

eTree

See

d15

117

1.31

94.33

71

1.22

2.55

0.03

39Cordia

millenii

Borag

inacea

eTree

See

d/Bark

3313

132.43

108.9

132

25.29

41.69

6.3

89Deinbo

llia

pinnata

Sap

inda

ceae

Shr

ub‐Tree

See

d—

——

—1

4747

4738

.02

38.02

38.02

47Diosp

yros

mon

butten

sis

Ebe

naceae

Tree

See

d5.5

3.5

2.5

0.06

11

11

0.01

0.01

0.01

1Ficussp

p.Moracea

eTree

See

d/Foliage

——

——

302

——

—7.58

69.17

0.01

—

Guar

easp

.Meliaceae

Tree

See

d9

75

0.21

21.5

21

0.14

0.14

0.14

3Isolon

adeigh

tonii

Ann

onacea

eTree

See

d28

.512

111.62

165.5

161

7.01

20.94

0.49

88Pseudospo

ndiasmicroca

rpa

Ana

card

iaceae

Shr

ub‐climbe

rSee

d15

1111

0.78

3412

.53

801

5.91

40.26

0.28

426

Lan

dolph

ialandolph

ioides

Apo

cyna

ceae

Liana

See

d/Bark

1810

.57.5

1.23

122

17.73

136

112

.75

74.03

0.53

2,14

5Mae

salanceolata

Myrsina

ceae

Shr

ub‐Tree

See

d—

——

—1

11

10.8

0.8

0.8

1Opiliaam

entacea

Opiliacea

eShr

ub‐climbe

rSee

d20

11.5

11.5

1.09

293.11

81

4.95

13.82

0.14

82Oxy

anthussp

eciosu

sRub

iaceae

Tree

See

d27

12.5

9.5

0.71

45

161

3.31

10.88

0.09

20Par

kiafilicoidea

Leg

uminosae

Tree

See

d17

134

0.4

36

161

4.63

13.08

0.37

18Pou

teriaaltissim

aSap

otacea

eTree

See

d25

15.5

15.5

2.45

41

11

1.1

1.95

0.64

4Psych

otriape

duncu

laris

Rub

iaceae

Shr

ubSee

d6

42

<0.01

11

11

0.03

0.03

0.03

1Psych

otriasu

cculenta

Rub

iaceae

Shr

ub‐Tree

See

d6

4.5

40.02

22

22

0.03

0.04

0.01

4San

tiriatrim

era

Bur

seraceae

Tree

See

d24

1510

2.23

62.33

81

3.42

13.44

0.25

14Syzigium

guineense

Myrtaceae

Tree

See

d/Foliage

1210

100.36

6024

.52

105

112

.57

65.03

0.11

1,42

2Trilepisium

mad

agas

carien

seMoracea

eTree

See

d14

1212

0.91

199.53

291

0.65

2.31

0.03

181

Vitex

don

iana

Lam

iaceae

Tree

See

d23

1610

2.11

338.75

281

10.71

31.07

0.25

210

Xylop

iaac

utiflora

Ann

onacea

eTree

See

d11

.55.5

2.5

0.04

11

11

0.1

0.1

0.1

1Unide

ntifiedref#13

——

See

d13

5.1

4.6

0.44

226.27

751

2.74

33.2

0.2

138

Unide

ntifiedref#37

——

See

d13

.55.3

4.3

0.51

157.07

541

2.66

23.96

0.1

106

The

tablepr

esen

tsthesp

eciesna

me,familyna

me,life

form

,sam

plefoun

dwithinfecalsam

ple,seed

dimen

sion

s,an

ddr

iedfecalm

easu

res.The

dimen

sion

sof

each

seed

werecalculatedfrom

theav

erag

eof

20dr

yseed

scollectedfrom

withinNge

lNya

kiForestReserve

.Ada

sh(—

)de

notesda

tade

ficien

cy.

Am. J. Primatol.

4 / Dutton and Chapman

Phenology

In order to investigate possible relationshipsbetween seeds collected from feces and fruit avail-ability, we collated fruiting phenology data from overthe entire period during which fecal samples werecollected. These data (from 1,053 trees) were collectedover 18.8 km (4.0m wide¼ 75,200m2) of regularlywalked transects located so as to include as repre-sentative a sample of the forest as possible. Six of theeight transects (we established two new transects in2010 to incorporate a larger representative of theforest) were established in 2006 using a systematicdesign (500m apart; Beck & Chapman, 2008] andsince then have been walked on a monthly basis fortree phenology sampling. As chimpanzees seldomventure outside of the forested areas in Ngel Nyaki[Dutton, 2013] the transects used were all locatedwithin the 7.5 km2 forested area.

As an indicator of monthly fruit availability, weestimated the proportion of crown occupied bymature fruit in a given tree and gave scores betweenzero and four (0¼ 0%, 1¼ 1–25%, 2¼ 26–50%, 3¼ 51–75%, 4¼ 76–100%) following methodology by Sunet al. [1996]. Only trees >10 cm diameter wererecorded. The basal area of each fruiting tree wasused as a proxy for canopy volume [Strier, 1989]. Wechose this method because it is relatively quick andeasy and has been used successfully in severalstudies to estimate canopy volume in relation to fruitabundance [Anderson et al., 2000; Chapmanet al., 1994; Stevenson et al., 1998; Worman &Chapman, 2006].

We calculated the density and basal area of eachidentified tree species (Table 2) using the followingformula:

ð1=2DBHÞ2 � p

where DBH represents Diameter at Breast Height[1.4m; Sun et al., 1996].

We multiplied the basal area of each tree by theproportion of crown occupied by mature fruit obtain-ing an index of the total mature fruit load on eachtree.

In Ngel Nyaki Forest Reserve, at least seven treespecies of Ficus have been identified. Five have beennamed: F. chlamydocarpa, F. lutea, F. polita, F.sansibarica, and F. sur. (http://www.biol.canterbury.ac.nz/nmf_project/plant‐checklist.shtml). While somespecies such as F. lutea and F. sur are certainly eatenby the chimpanzees (pers obs) we are not sure that allthe species are chimpanzee foods. However, as theirseeds are difficult to differentiate from one another,for the purpose of this studywe refer to allFicus seedsas the genus. When calculating the basal area forFicus as a genus, only established trees and notepiphytes where used as this may of conflicted withbasal area versus canopy volume.

Seasonal Fruit Availability and Consumption

As fruit availability fluctuates annually andseasonally at Ngel Nyaki [unpublished data], wemeasured fruit availability monthly and then com-bined months to form two seasons (i.e., the rainyseason from April through October and the dryseason from November through March). Thesemonths were chosen to represent seasons based ondata downloaded from weather stations located atNgel Nyaki Forest Reserve (http://www2.phys.canterbury.ac.nz/�seg50/nigerian_data.html).

We calculated fruit availability index (Fm)monthly using the following formula:

Fm ¼X

Pkm � Bk

where Pkm denotes the proportion of trees withmature fruit for species k in monthm, andBk denotesthe total basal area per hectare for species k[Basabose, 2002].

Rank Preference Index

To calculate the Rank Preference Index, weselected 17 fruit species based on the availability ofphenological data (required life form must have beena tree) and the proportions discovered in chimpanzeefeces. We ranked the availability of each of the seedspecies from the total basal area of each tree speciesexhibiting mature fruit per month. Likewise, weranked the consumption of each seed species from themass percentage of seeds discovered in feces permonth. We then used the difference in these ranks(availability versus consumption) tomeasure relativepreference per month. We averaged the rank differ-ences across all months to give an order of relativepreference for the species in the diet using thefollowing formula:

ti ¼ ri � si

where ti is the rank difference (measure of relativepreference), ri is the rank of consumption of speciestype i (i¼ 1, 2, 3,…,m), and si is the rank ofavailability of species type i [Strauss, 1979].

Seeds that were found in feces but not present inthe phenological data, either did not show anymature fruiting along transects during this study(such as Xylopia acutiflora), were not trees (such asAframomum angustifolium) or were not identified.Twenty‐six seed species discovered in feces duringthis study remain to be identified.

Seasonal Variations—Consumption VersusAvailability

We used a multi‐way ANOVA to determinewhether: (i) there was a significant difference in

Am. J. Primatol.

Dietary Preferences of Chimpanzees / 5

TABLE

2.Tot

alBas

alAre

a(cm

2/ha)

Rep

rese

ntingMat

ure

Fru

itCan

opyVolumean

dTre

esWithMat

ure

Fru

it(%

)per

Mon

thof

the17

Mat

ure

Fru

itin

gTre

eSpec

iesCon

sumed

byChim

pan

zees

inNge

lNya

kiFor

estRes

erve

Spe

cies

Janu

ary

Feb

ruary

March

Apr

ilMay

June

July

Aug

ust

Sep

tembe

rOctob

erNov

embe

rDecem

ber

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

BA

(cm

2)

MF

(%)

Beilsch

miedia

man

nii

0.0

0.0

99.3

7.7

0.0

0.0

0.0

0.0

99.3

0.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Celtisgo

mph

ophylla

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

164.8

0.2

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

117.8

14.3

0.0

0.0

Chionan

thus

africa

nus

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

13.0

1.0

13.0

1.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Cordia

millenii

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

363.7

0.2

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Deinbo

llia

pinna

ta0.0

0.0

144.0

7.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Diosp

yros

mon

butten

sis

157.6

11.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

472.7

33.3

315.1

22.2

315.1

22.2

157.6

11.1

157.6

11.1

Ficusexas

pera

ta0.0

0.0

0.0

0.0

0.0

0.0

122.1

33.3

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Ficuslutea

0.0

0.0

0.0

0.0

0.0

0.0

4,71

9.9

14.3

6,60

7.8

20.0

4,40

5.2

13.3

2,20

2.6

6.7

2,20

2.6

6.7

4,40

5.2

13.3

2,20

2.6

6.7

2,20

2.6

6.7

0.0

0.0

Ficussu

r51

0.4

12.0

1,36

1.1

32.0

850.7

20.0

966.7

22.7

1,93

3.4

45.5

1,24

0.6

29.2

0.0

0.0

580.0

13.6

0.0

0.0

0.0

0.0

580.0

13.6

0.0

0.0

Ficustype

A0.0

0.0

1,14

7.1

100.0

1,14

7.1

100.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Ficustype

B0.0

0.0

1,33

6.8

25.0

1,33

6.8

25.0

0.0

0.0

0.0

0.0

0.0

0.0

668.4

12.5

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

FicusUnide

ntified

298.9

12.5

298.9

12.5

298.9

12.5

0.0

0.0

341.6

14.3

797.0

33.3

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

341.6

14.3

683.1

28.6

Guar

easp

.94

.550

.094

.550

.00.0

0.0

0.0

0.0

0.0

0.0

189.0

1.0

0.0

0.0

0.0

0.0

189.0

100.0

189.0

100.0

0.0

0.0

189.0

100.0

Isolon

adeigh

tonii

0.0

0.0

0.0

0.0

0.0

0.0

675.6

0.1

6,08

0.5

0.6

5,40

4.8

0.5

675.6

0.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Oxy

anthussp

eciosu

s0.0

0.0

0.0

0.0

194.1

0.1

0.0

0.0

582.5

0.2

1,94

1.2

0.8

776.5

0.3

194.1

7.7

194.1

7.7

0.0

0.0

0.0

0.0

0.0

0.0

Par

kiafilicoidea

0.0

0.0

0.0

0.0

0.0

0.0

223.8

0.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Pou

teriaaltissim

a1,15

7.9

6.3

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

3,47

3.6

0.2

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Psych

otriasu

cculenta

307.4

83.3

0.0

0.0

0.0

0.0

0.0

0.0

52.7

0.1

0.0

0.0

105.4

0.3

105.4

28.6

263.5

71.5

263.5

71.4

263.5

71.4

210.8

57.1

San

tiriatrim

era

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

1,12

2.6

0.1

2,24

5.2

0.2

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Syzigium

guineense

0.0

0.0

0.0

0.0

186.7

0.1

186.7

0.1

1,68

0.7

0.7

747.2

0.3

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Trilepisium

mad

agas

carien

se0.0

0.0

0.0

0.0

358.1

0.2

119.3

0.1

358.1

0.2

119.3

0.1

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

Vitex

don

iana

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

793.9

0.3

0.0

0.0

0.0

0.0

2,38

2.0

100.0

1,58

7.8

66.7

0.0

0.0

Total

2,52

6.6

4,48

1.7

4,37

2.4

7,01

4.0

17,749

.419

,982

.17,46

7.7

3,55

4.8

5,36

6.9

5,35

2.2

5,25

0.8

1,24

0.5

Note:

Ficustype

Aan

dB

have

been

distingu

ishe

dfrom

othe

rFicusbu

tthesp

eciesarestillto

beclarified

.BA,total

basa

larea

/haof

treeswithmatur

efruit;MF,p

ropo

rtionof

totalba

salarea

(/ha)

withmatur

efruit.

Am. J. Primatol.

6 / Dutton and Chapman

availability and consumption ofmature fruit betweenthe wet (April—October) and dry (November—March) seasons and (ii) there was a significantdifference between the availability and the consump-tion ofmature fruit species. Amulti‐wayANOVAwasused to account for the two factors (season andpreference), each with multiple levels (season¼wetvs. dry and preference¼ consumption vs. availability).We used Wilcoxon rank sum tests to: (i) identify anydifferences between the relative seasonal availabilityfor each consumed species, (ii) identify any differ-ences between the seasonal consumption for eachspecies, and (iii) identify if the seasonal availabilityreflected seasonal consumption for each species.Wilcoxon rank sum tests were appropriate becausethe data were not normally distributed when usingthe Shapiro–Wilk normality test. All analyses werecarried out in R v2.13 software package [R Develop-ment Core Team, 2011].

ResultsA total of 495 fresh fecal samples were collected

over the 12‐month period from April 2010 toMarch 2011. The collection of fecal samples permonth ranged from 1 in November to 96 in March.Fresh fecal samples ranged from 1.51 to 304.79 g(mean¼ 42.51 g; s.e.¼ 1.6) with dried fecal samplesranging from 0.06 to 96.11 g (mean 12.0 g; s.e.¼ 0.61).

Seventy‐five food items were distinguished inchimpanzee feces. Of the 495 fecal samples, 58.4%(n¼ 289) solely contained fruit (seeds and/or exo-carp). As a percentage of total dried mass of the fecalsamples, fruit made up 91% (n¼ 495), foliage 5%(n¼ 156), and the last 4% comprised of bark (n¼ 57),animals (n¼ 116) and other items (n¼ 33). Fifty‐twofruit taxa were identified and of these, two wereidentified to genus level and 22 were identified tospecies level. Of the 495 fecal samples, only 1.2%(n¼ 6) contained no traces of fruit. Of these six feces,three contained only foliage, one contained foliageand ants (Camponotus nr. perrisii), one containedfoliage, ants, and bark and one contained only theremains of a freshwater crab.Ficus spp. was themostcommon genus identified in the fecal samples,occurring in 61.2% (n¼ 303) of all samples.

Evidence of Diet From Non‐Fecal Sources

We observed evidence of the chimpanzees con-suming items which were not identified in thecollected fecal samples. Honey consumption wasassociated with beeswax observed in feces in Augustand stingless‐bee remains observed in feces in April,but tools suggest that chimpanzees at Ngel Nyakiexcavate hives in March, April, May, July, August,September, and October [Dutton, 2013]. Evidence ofSymphonia globulifera fruit consumption was ob-served from a food pound stone [Dutton, 2013]. Ants

(C. nr. perrisii) were only observed in feces duringthree months of the year (March, April, and June),however, tool sites suggest that chimpanzees werealso excavating ant nests during February, October,and November [Dutton, 2013].

Seasonal Availability

A multi‐way ANOVA on phenological datashowed that there was no significant difference ofseason on fruit availability (F¼ 1.830, df¼ 214,P¼ 0.178) when based on the basal areas of 17consumed mature fruiting species (Table 2). Howev-er, there was a significant species effect, with morespecies available in the wet season than in the dryseason (F¼ 10.264, df¼ 198, P< 0.001).

The results of the Wilcoxon rank sum testsshowed that there were no significant differences inmature fruit availability between seasons (W¼ 5,065,P¼ 0.113).

Seasonal ConsumptionA multi‐way ANOVA showed that there was no

significant difference between the quantity of fruit inthe feces between seasons (F¼ 1.740, P¼ 0.190).However, there was a significant species� seasoninteraction with more species consumed in the wetseason than in the dry season (F¼ 2.464, P¼ 0.03).

Wilcoxon rank sum tests showed that there weresignificantly more small mammals and birds eatenduring the dry season than during the wet season(W¼ 28, P¼ 0.033). Wilcoxon rank sum tests showedthat therewere no significant differences between thewet and dry seasons in the consumption of inverte-brates (W¼ 23.5, P¼ 0.363), bark (W¼ 9, P¼ 0.202),roots (W¼ 24.5, P¼ 0.105), grass (W¼ 15, P¼ 0.744),and leaves (W¼ 13, P¼ 0.501).

Wilcoxon rank sum tests also showed that therewere no significant differences in the consumption ofmost fruit species between seasons. However, I.deightonii (W¼ 7.5, P¼ 0.066) and T. madagascar-iense (W¼ 7.5, P¼ 0.066) showed a trend to beconsumed more in the wet season. Opilia amentacea(W¼ 5, P¼ 0.030) and unidentified species ref#13(W¼ 5, P¼ 0.030), and ref#37 (W¼ 5, P¼ 0.030) wereall consumed significantly more in the wet season.

Rank Preference Indices

Rank preference indices were calculated for 17fruit seed species identified in the chimpanzee fecalsamples. The relative availability of each fruitingspecies was determined from the contribution of eachfruiting tree species to total basal area of maturefruiting trees during each month (April 2010–March 2011). The consumption of each species wasdetermined from the mass percentage of all driedfecal samples combined during each month. Across

Am. J. Primatol.

Dietary Preferences of Chimpanzees / 7

the entire year, the rank preference index showedthat P. altissima was the most preferred fruit of the17 species, with D. monbuttensis the least preferredandFicus spp. also one of the least preferred (Table 3).P. altissimawas also highly preferred in both seasonswith D. monbuttensis least preferred in both seasons(Table 3). Interestingly, Ficus was less preferred inthe wet season than the dry season.

Consumption Versus Availability

Wilcoxon rank sum tests calculated for theproportion of fruit consumed per month versus theproportion of trees bearing mature fruit per monthshowed that there was significantly more Ficus spp.consumed than expected based on the proportion oftotal fruit available that were Ficus spp. (W¼ 36,P¼ 0.040). Wilcoxon rank sum tests also showed thatthere was proportionately more availability thanfruit consumed of D. monbuttensis (W¼ 105,P¼ 0.019), Guarea sp. (W¼ 105, P¼ 0.019), M.lanceolata (W¼ 111.5, P¼ 0.007), O. speciosus(W¼ 105, P¼ 0.019), and P. succulenta (W¼ 116,P¼ 0.005). Wilcoxon rank sum tests also revealedthat the proportion of fruit consumed was about asexpected based on what was available in theenvironment for many fruit species (SupplementaryInformation).

Items Consumed Regularly

There were only 14 items that constituted>5% ofthe chimpanzee diet per month and together these 14items accounted for over 80% of the total fecal massduring each month and over 94% of the annual diet(Table 4). Ficus spp. occurred in feces during nine

months of the year; its proportion throughout the yearvaried from 0% to 87%, with an annual proportion of32%.When Ficus spp. were not found in fecal samples(during August, September and October) bark, grass,leaves, V. doniana, C. millenii, I. deightonii, andOpilia amentacea were found (Table 4). The propor-tional mass of Ficus spp., L. landolphioides, andS. guineense contributed to >70% of the annual diet.There was a large difference in the number of fecalsamples discovered during each month, from one inNovember to 96 in March (Table 4).

Discussion

Seasonal AvailabilityOur study has shown that there is no seasonal

difference in fruit availability for P. t. ellioti at NgelNyaki forest despite their being more speciesavailable and therefore fruit choice during the wetseason. Interestingly, no correlation between fruitavailability and rainfall was reported in Kahuzi,Democratic Republic of Congo [Yamagiwa &Basabose, 2006] and in Kibale, Uganda [Mitaniet al., 2002]. Contrastingly, higher fruit abundancewas observed in the dry season in the montane forestof Kahuzi [Basabose, 2002] and lower fruit abun-dance in the dry season in the lowland forests of LopéReserve, Gabon [Tutin and Fernandez, 1993], NdokiForest, Congo [Kuroda et al., 1996], and Taï forest,Ivory Coast [Doran, 1997].

Seasonal Consumption

Fruit dominated the diet of P. t. ellioti withinNgel Nyaki Forest reserve. The number of fruit

TABLE 3. Seasonal and Annual Rank Preference Index for 17 Plant Species Identified From Seeds of 495Chimpanzee Fecal Samples From Ngel Nyaki

SpeciesWet

season�Preferenceindex rank

Dryseason�

Preferenceindex rank

Annualaverage�

Preferenceindex rank

Cordia millenii �2.79 1 1.00 11 �1.21 4Pouteria altissima �2.21 2 �2.60 1 �2.38 1Trilepisium madagascariense �2.14 3 0.90 10 �0.88 6Deinbollia pinnata �2.07 4 0.70 8 �0.92 5Chionanthus africanus �1.71 5 �0.90 4 �1.38 3Syzigium guineense �1.57 6 0.50 7 �0.71 8Isolona deightonii �0.57 7 �0.90 4 �0.71 8Santiria trimera �0.57 7 0.80 9 0.00 11Vitex doniana �0.57 7 �2.60 1 �1.42 2Beilschmiedia mannii �0.21 8 �1.00 3 �0.54 9Parkia filicoidea �0.21 8 �0.90 4 �0.50 10Celtis gomphophylla 0.43 9 �2.50 2 �0.79 7Guarea sp. 1.00 10 3.20 12 1.92 12Diospyros monbuttensis 2.36 11 3.50 13 2.83 16Oxyanthus speciosus 3.29 12 0.70 8 2.21 14Ficus spp. 3.36 13 0.20 6 2.04 13Psychotria succulenta 4.21 14 �0.10 5 2.42 15

�The higher the score the less that species was preferred.

Am. J. Primatol.

8 / Dutton and Chapman

species consumed (n¼ 52) is similar to the findings ofother studies from similar altitudinal habitats.Basabose [2002], recorded 66 fruit species consumedby chimpanzees at Kahuzi, DRC (altitude >2,050mabove sea level); Wrangham et al. [1991], recorded 68fruit species consumed at Kibale, Uganda (altitude�1,500m a.s.l.), and Stanford & Nkurunungi [2003],who recorded 46 fruit species consumed by chimpan-zees at Bwindi, Uganda (altitude >2,000m a.s.l.).The number of recorded fruit species in the diet of thechimpanzees at all these study sites may be areflection of altitude (>1,500m a.s.l.). Lower diversi-ty of vascular plants has been attributed to higheraltitude [Gautier‐Hion, 1983; Odland & Birks, 1999;Ohlemüller & Wilson, 2000; Rahbek, 1995]. There-fore, proportionately fewer seed species are dispersedby chimpanzees in montane forests than in otherforests [Gross‐Camp et al., 2009].

Species discovered in feces but not available inthe phenological data means that either the treespecies were below 10 cm in diameter, were not trees(i.e. liana) and/or that certain species were not evenlydistributed throughout the forest and may requireinvestigation into tree species distribution patterns.

Fruit Preference Relative to Availability

While the same quantity of fruit was availablethroughout the year, the species contributing towardtotal fruit mass varied between the wet and dryseasons. Correspondingly, chimpanzee fecal analysisshowed no difference in the quantities of fruitremaining in the feces between seasons, but didshow differences in the seed composition. Thissuperficial comparison between fruit availability

and fecal content suggests that P. t. ellioti consumefruit in the same proportion as the fruit is available inthe environment.

However, the results of the Rank PreferenceIndex (RPI) show that fruit preference byP. t. ellioti isnot always based on relative availability. Mostly,relative preferences for fruit species are seasonal,although a few fruit species are preferred across boththe wet and the dry seasons. For example, P.altissima, which ranked first in the overall RPI,was ranked second during the wet season when it isreadily available and first during the dry seasonwhen it is scarce. Other preferred fruit species (thoseare consumed when their availability is low) includeC. millenii, T. madagascariense, D. pinnata, C.africanus, and S. guineense. In contrast, Guarea sp.and D. monbuttensis had a consistently low RPIacross both seasons, irrespective of abundance whichindicates these species are tolerated but notpreferred.

This lack of correlations between the fruitavailability index and the proportional mass of fruitseeds remaining in feces described above suggeststhat Ngel Nyaki chimpanzees may be selective intheir fruit diet. This conclusion is supported byBasabose [2002; 2004] and Gross‐Camp et al. [2009]who both report that chimpanzees seem to activelyseek a fruit species rather than simply consume itopportunistically.

Fruits of Ficus spp. were unusual in that theywere equally abundant in both the wet and dryseasons. However, their RPI varied with season witha RPI rank of thirteenth in the annual RPI,thirteenth in the wet season RPI when there is alarger choice of fruiting species and sixth in the dry

TABLE 4. Items Consumed Regularly by Chimpanzees at Ngel Nyaki Forest Reserve, Showing Number of FecesCollected Each Month and Species Identified That Contributed to Over 5% of the Proportional Dried Mass perMonth

Category SpeciesJanuary,n¼ 20

February,n¼28

March,n¼ 96

April,n¼82

May,n¼ 93

June,n¼51

July,n¼31

August,n¼25

September,n¼ 20

October,n¼ 27

November,n¼1

December,n¼21 Annual %

Fruit (seedand skin)

Cordia millenii 42.16 18.37 2.16

Ficus spp. 33.17 86.72 27.36 27.91 15.99 75.06 84.50 90.23 75.20 32.48Isolona deightonii 6.95 40.94 1.92Pseudospondias

microcarpa8.64 3.43

Landolphialandolphioides

64.11 45.36 14.86 26.58

Opilia amentacea 5.43 5.53 24.11 2.68Syzigium guineense 7.66 48.61 12.24Vitex doniana 43.38 60.49 13.49 5.30

Foliage Unidentified 6.71 40.54 2.88Grass 6.90 7.25 16.87 2.02

Bark Cordia millenii 10.78 1.54Unidentified 8.11 1.46

Vertebrates Mammal furand bones

8.77 9.52 0.96

Invertebrates Unidentified 9.77 0.043Total 90.17 95.49 91.48 89.57 84.88 87.85 91.45 81.92 90.81 89.64 100.00 98.22

The annual percentage over all fecal samples and the proportion that these items contributed to the monthly total is also provided.

Am. J. Primatol.

Dietary Preferences of Chimpanzees / 9

seasonRPIwhen choice of fruit species is limited. Thefact that chimpanzee preference for Ficus variesaccording to the availability and/or quantity of otherspecies may indicate that Ficus is a fallback food forchimpanzees in Ngel Nyaki Forest.

FicusFigs are an important component of chimpanzees

diets and have been variously described as “fallbackfoods” and preferred species. The term “fallback food”is used to describe food of relatively poor nutritionalquality that becomes a particularly important part ofthe diet during periods when preferred foods arescarce [Marshall et al., 2009]. Ficus fruits have beendescribed as a main fallback food for chimpanzees byWrangham et al. [1991], Kuroda et al. [1996], andWrangham et al. [1996]. However, in other studiesfigs have been found to be a valuable and preferredfood resource for chimpanzees [Basabose, 2002;Conklin & Wrangham, 1994; Kagoro‐Rugunda &Baranga, 2009; Wrangham et al., 1994; Yamagiwa &Basabose, 2009]. In this study, we found evidence forFicus being a preferred food for P. t. ellioti at NgelNyaki forest reserve. Fruits were produced all yearround, as has been recorded elsewhere for Ficus[Basabose, 2002; Newton‐Fisher, 1999; Wranghamet al., 1996; Yamagiwa et al., 1996]. They wereequally abundant in the wet and dry seasons andconsumed in almost every month of the year.Although the Ficus RPI varied with season, it wasalways relatively high, being 13th out of 17 in the wetseasonwhen there is a larger choice of fruiting speciesavailable and sixth in the dry season when choice offruit species is limited. Only in September andOctober, when Ficus fruits were least abundant(Table 4), was Ficus substituted for C. millenii, V.doniana, and an unknown variety of leaves (Table 4).When other fruit species were available in highquantities and were ordered higher in the rankpreference index (e.g., P. altissima in January, I.deightonii in May and June, O. speciosus and S.trimera in June, and S. trimera in July, Tables 2and 3), Ficus fruits were still consumed in highquantities.

Non‐Fruit Foods

Evidence of birds, eggs, small mammals, milli-pedes, and grasshoppers was only found in fecesduring October to February, effectively the dryseason when fruit choice was lowest. Other chimpan-zee populations have also been shown to prey onmammals. At Kahuzi (DRC) the chimpanzees prey onCercopithecus monkeys, although in contrast to ourstudy this only occurred when the diversity ofsucculent ripe fruits was highest [Basabose &Yamagiwa, 1997; Basabose, 2002]. Seasonality ofhunting has been explained by the coincidence with

formation of larger foraging groups [Stanfordet al., 1994; Takahata et al., 1984], which mayexplain the absence of highly mobile prey items (suchas monkeys) in the Ngel Nyaki chimpanzee dietbecause the population is small, comprising approxi-mately 16 weaned individuals [Dutton, 2013]. Scav-enging events may be a more plausible explanationfor the occurrence of mammal remains in Ngel Nyakichimpanzee feces.

While ants (C. nr. perrisii) were only observed infeces during three months of the year (March, Apriland June), tool sites suggest that chimpanzees werealso excavating ant nests during February, October,and November. The consumption of bees and/or honeywas evident in chimpanzee feces at Ngel Nyaki. Beeswaxwas observed in feces only inAugust and stinglessbees were observed in feces in April, but tools suggestthat chimpanzees at Ngel Nyaki excavate hives inMarch, April, May, July, August, September, andOctober, which corresponds somewhat to the wetseason. Grass and leaves were consumed all yearround. However, one interesting piece of data was thehigh consumption (>40%) of leaves during September,corresponding to fresh leaf flush.

In conclusion, a low variety, fruit‐dominated dietwas observed in the P. t. ellioti population in NgelNyaki Forest Reserve. Chimpanzees at Ngel NyakiForest Reserve do not solely consume fruits based ontheir availability within the environment but ratherare selective in their fruit diet. Evidence from theRank Preference Index shows that Ficus spp. was nota fallback food for the chimpanzees at Ngel Nyaki butrather a preferred and important food.

There were seasonal changes in the type of fruitsavailable and preferred by chimpanzees, but noseasonal differences in the quantity of fruit availableor consumed. When there is a low variety of fruitavailable during the dry season at Ngel Nyaki ForestReserve, P. t. ellioti consumed more small mammals,birds, and selective invertebrates. The use of toolsand feeding remains contributed to a better under-standing of the chimpanzee diet in Ngel Nyaki ForestReserve.

ACKNOWLEDGMENTS

Thanks to Taraba State Forestry for logisticalsupport and Nigerian Montane Forest Project forfield facilities and field assistance, especially toAlfred Moses and Suleiman A. Idi.

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