(PDF) Watering holes: The use of arboreal sources of drinking water by Old World monkeys and apes

Behavioural

Processes

129

(2016)

18–26

Contents lists available at ScienceDirect

Behavioural

Processes

journal homepage: www.elsevier.com/locate/behavproc

Watering

holes:

The

use

of

arboreal

sources

of

drinking

water

by

Old

World

monkeys

and

apes

Narayan

Sharmaa,b,c,∗,

Michael

A.

Huffmand,∗∗,

Shreejata

Guptaa,

Himani

Nautiyala,

Renata

Mendonc¸

ae,

Luca

Morinof,

Anindya

Sinhaa,b

aSchool

of

Natural

Sciences

and

Engineering,

National

Institute

of

Advanced

Studies,

Indian

Institute

of

Science

Campus,

Bangalore

560012,

Karnataka,

India

bNature

Conservation

Foundation,

2076/5,

IV

Cross,

Gokulam

Park,

Mysore

570002,

Karnataka,

India

cDepartment

of

Environmental

Biology

and

Wildlife

Sciences,

Cotton

College

State

University,

Pan

Bazar,

Guwahati

781001,

Assam,

India

dSection

of

Social

Systems

Evolution,

Primate

Research

Institute,

Kyoto

University,

Inuyama,

Aichi

484-8506,

Japan

eSection

of

Language

and

Intelligence,

Primate

Research

Institute,

Kyoto

University,

Inuyama,

Aichi

484-8506,

Japan

fLaboratoire

de

Dynamique

de

l’Evolution

Humaine,

UPR

2147,

CNRS,

Paris,

France

a

r

t

i

c

l

e

i

n

f

o

Article

history:

Received

7

December

2015

Received

in

revised

form

20

April

2016

Accepted

23

May

2016

Available

online

24

May

2016

Keywords:

Primate

Tree-hole

Dipping-and-licking

Seasonal

water

Predator

avoidance

Self

medication

a

b

s

t

r

a

c

t

Water

is

one

of

the

most

important

components

of

an

animal’s

diet,

as

it

is

essential

for

life.

Primates,

as

do

most

animals,

procure

water

directly

from

standing

or

free-ﬂowing

sources

such

as

pools,

ponds

and

rivers,

or

indirectly

by

the

ingestion

of

certain

plant

parts.

The

latter

is

frequently

described

as

the

main

source

of

water

for

predominantly

arboreal

species.

However,

in

addition

to

these,

many

species

are

known

to

drink

water

accumulated

in

tree-holes.

This

has

been

commonly

observed

in

several

arbo-

real

New

World

primate

species,

but

rarely

reported

systematically

from

Old

World

primates.

Here,

we

report

observations

of

this

behaviour

from

eight

great

ape

and

Old

World

monkey

species,

namely

chim-

panzee,

orangutan,

siamang,

western

hoolock

gibbon,

northern

pig-tailed

macaque,

bonnet

macaque,

rhesus

macaque

and

the

central

Himalayan

langur.

We

hypothesise

three

possible

reasons

why

these

primates

drink

water

from

tree-holes:

(1)

coping

with

seasonal

or

habitat-speciﬁc

water

shortages,

(2)

predator/human

conﬂict

avoidance,

and

(3)

potential

medicinal

beneﬁts.

We

also

suggest

some

alter-

native

hypotheses

that

should

be

tested

in

future

studies.

This

behaviour

is

likely

to

be

more

prevalent

than

currently

thought,

and

may

have

signiﬁcant,

previously

unknown,

inﬂuences

on

primate

survival

and

health,

warranting

further

detailed

studies.

©

2016

Elsevier

B.V.

All

rights

reserved.

1.

Introduction

Water

is

essential

for

the

sustenance

of

life

and

therefore,

a

vital

component

of

an

animal’s

diet.

Primates,

like

most

animals,

procure

liquid

water

either

from

natural

ground

sources

such

as

pools,

puddles,

rivers,

springs,

and

streams,

from

occasional

anthro-

pogenic

sources

(e.g.,

Hillyer

et

al.,

2015),

or

as

pre-formed

water

(National

Research

Council,

2003),

by

consuming

tender

leaves,

leaf

petioles,

fruits,

ﬂowers,

stems,

roots

and

bark

(e.g.,

Poirier,

1970;

Angus,

1971;

Glander,

1978;

Nishida,

1980;

Chapman,

1988;

Ciani

et

al.,

2001).

The

consumption

of

water-containing

plant

parts

has

∗Corresponding

author

at:

Department

of

Environmental

Biology

and

Wildlife

Sciences,

Cotton

College

State

University,

Pan

Bazar,

Guwahati

781001,

Assam,

India.

∗∗ Corresponding

author

at:

Section

of

Social

Systems

Evolution,

Primate

Research

Institute,

Kyoto

University,

41-2

Kanrin,

Inuyama,

Aichi

484-8506,

Japan.

E-mail

addresses:

narayansharma77@gmail.com

(N.

Sharma),

huffman.michael.8n@kyoto-u.ac.jp

(M.A.

Huffman).

frequently

been

described

as

the

main

source

of

water

for

pre-

dominantly

arboreal

primate

species

or

for

those

living

in

arid

or

semi-arid

habitats,

with

little

or

no

opportunity

to

directly

access

ground

water.

Preformed

water

in

the

foods

of

free-ranging

non-

human

primates

has

been

reported

to

vary

from

less

than

5%

of

air-dried

seeds

in

hot

deserts

to

over

70%

of

the

fresh

weight

of

succulent

plant

parts

in

tropical

rainforests

(Baranga,

1982;

Calvert,

1985;

Rogers

et

al.,

1990;

Barton

et

al.,

1993;

Robbins,

1993;

Edwards,

1995).

Many

of

these

species,

thus,

often

lick

dew

and

rainwater

from

leaves

in

the

early

morning

or

after

rainfall,

only

rarely

descending

to

the

ground

to

drink

(e.g.,

Presbytis

[currently

Trachypithecus]

johnii,

Poirier,

1970;

Macaca

sinica,

Dittus,

1977;

Cebus

albifrons,

Deﬂer,

1979;

Procolobus

badius

temminckii,

Starin,

2002).

Another

source,

more

difﬁcult

to

observe

and

thus,

perhaps

less

frequently

reported,

is

the

drinking

of

rainwater

accumulated

in

the

holes

of

tree

trunks

(but

see

Dittus,

1977;

Glander,

1978;

Chapman,

1988;

Starin,

2002).

http://dx.doi.org/10.1016/j.beproc.2016.05.006

0376-6357/©

2016

Elsevier

B.V.

All

rights

reserved.

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

19

Fig.

1.

Location

of

study

areas

for

the

six

species

displaying

arboreal

drinking

behaviours

during

this

study.

The

species

have

been

listed

by

region.

In

general,

primates

have

two

ways

to

obtain

water

from

tree-

holes.

If

the

tree-hole

is

large,

the

animal

can

insert

its

head

inside

and

directly

drink

the

water

with

its

mouth

(Glander,

1978;

Nowak

2008).

If,

however,

the

hole

is

narrow,

the

individual

may

insert

its

forearm

inside,

dip

it

in

the

water

and

then

lick

the

adhering

water

from

it,

a

method

known

as

‘dipping-and-licking’

(Wrangham,

1981).

In

addition,

some

species

also

use

innovative

techniques

to

drink

water

from

tree-holes.

Chimpanzees

Pan

troglodytes

and

Sumatran

orangutans

Pongo

abelii,

at

some

sites,

for

example,

have

been

observed

to

use

their

hands

to

scoop

up

water

or

employ

leaves

as

a

tool

to

sponge

the

water

out

from

tree-holes

(e.g.,

Reynolds

and

Reynolds,

1965;

Sugiyama,

1995;

Tonooka,

2001;

van

Schaik

et

al.,

2003)

while

Zanzibar

red

colobus

Procolobus

kirkii

indi-

viduals,

in

a

mangrove

forest

refuge,

would

also

tilt

their

heads

up

and

scoop

water

into

their

open

mouths

with

their

hands

(Nowak,

2008).

The

‘dipping-and-licking’

method

is

well

documented,

partic-

ularly

in

New

World

primates

(Cebus

capucinus,

Freese,

1978;

Alouatta

palliata,

Glander,

1978;

Alouatta

caraya,

Bicca-Marques,

1992;

Giudice

and

Mudry,

2000;

Alouatta

guariba

clamitans,

Steinmetz,

2001;

Alouatta

pigra,

Dias

et

al.,

2014)

but

also

in

a

few

Old

World

species

(Erythrocebus

patas,

Struhsaker

and

Gartlan,

1970;

Lemur

catta,

Sussman,

1977;

Cercopithecus

aethiops,

Wrangham,

1981;

Presbytis

entellus,

Newton,

1992;

Macaca

silenus,

Fitch-Snyder

and

Carter,

1993)

and

in

certain

great

and

small

apes

(Hylobates

lar,

Carpenter,

1964;

Pan

troglodytes,

Reynolds

and

Reynolds,

1965;

Hylobates

spp.,

Chivers,

1977).

In

a

very

early

notable

study,

hoolock

gibbons

Hoolock

hoolock

were

observed

to

scoop

up

and

drink

water,

using

this

technique,

in

captivity

(Sanyal,

1892).

Here,

we

report

on

the

contexts

and

diverse

behaviours

involved

in

the

drinking

of

water

accumulated

in

tree-holes

by

eight

Old

World

primate

species—chimpanzee

Pan

troglodytes

schweinfurthii,

Bornean

orangutan

Pongo

pygmaeus

morio,

siamang

Symphalan-

gus

syndactylus,

western

hoolock

gibbon

Hoolock

hoolock,

northern

pig-tailed

macaque

Macaca

leonina,

bonnet

macaque

Macaca

radi-

ata,

rhesus

macaque

Macaca

mulatta

and

central

Himalayan

langur

Semnopithecus

schistaceus—inhabiting

a

wide

range

of

habitats

(Table

1).

We

also

propose

three

principal,

non-exclusive

hypotheses

to

argue

why

such

unusual

drinking

behaviour

may

be

far

more

widespread

than

originally

thought.

First,

drinking

of

water

from

tree-holes

may

have

evolved

and

been

maintained

in

response

to

habitat-speciﬁc

or

seasonal

shortages

in

water

from

other,

usu-

ally

more

prevalent,

sources.

Second,

this

strategy

of

drinking

from

arboreal

water

sources

could

be

a

possible

anti-predator

strategy

or

one

to

reduce

competition

with

and/or

minimise

aggression

from

conspeciﬁc

individuals,

or

even

avoid

conﬂict

with

other

species

such

as

humans.

Finally,

individual

primates

could

be

attracted

to

the

water

in

tree-holes

as

these

could

provide

medicinal

or

other

nutritional

beneﬁts

due

to

the

presence

of

leachates

in

them,

in

addition

to

being

possibly

less

contaminated

in

comparison

to

other

terrestrial

water

sources.

The

two

main

goals

of

this

paper

are,

therefore,

to

(1)

present

new

information

on

the

drinking

habits

of

20

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

Table

1

Characteristics

of

the

study

areas.

NoStudy

site

Area

(km2)

Latitude

Longitude

Elevation

(m

asl)

Annual

rainfall

(mm)

Maximum/minimum

temperature

(◦C)

Forest

type

Primate

community,

including

the

study

species

Reference

1

Hollongapar

Gibbon

Sanctuary

(HGS),

Assam,

India

20.98

26.691◦N

94.338◦E

110–120

2000

28/19

Dipterocarpus-Mesua-

Vatica

Bengal

slow

loris

Nycticebus

bengalensis,

capped

langur

Trachypithecus

pileatus,

western

hoolock

gibbon

Hoolock

hoolock,

northern

pig-tailed

macaque

Macaca

leonina,

rhesus

macaque

Macaca

mulatta,

stump-tailed

macaque

Macaca

arctoides

Sharma

et

al.

(2012)

2

Bandipur

National

Park,

(BNP)

Karnataka,

India

874

11.662◦N 76.627◦E 680–1454 141.4

33/11

Dry

deciduous,

moist

deciduous

and

dry

scrub

Bonnet

macaque

Macaca

radiata,

southern

plains

gray

langur

Semnopithecus

dussumieri

Chatterjee

(2012)

3

Kedarnath

Wildlife

Sanctuary,

(KWS)

Uttarakhand,

India

975

20.484◦N

79.280◦E

1558–2000

2044

16/6

Pine

and

oak,

temperate

oak-ﬁr

and

maple,

sub-alpine

oak-ﬁr

and

maple,

Rhododendron,

sub-alpine

ﬁr,

alpine

meadows

and

rocks

Central

Himalayan

langur

Semnopithecus

schistaceus,

rhesus

macaque

Macaca

mulatta

Kala

and

Gaur

(1982)

and

Gairola

(2010)

4

Danum

Valley

Conservation

Area,

(DVCA),

Sabah,

Malaysia

438

4.965

117.690

231–384

2881

22/32

Lowland

Dipterocarpus

Horsﬁeld’s

tarsier

Cephalopachus

bancanus,

Bornean

slow

loris

Nycticebus

menagensis,

long-tailed

macaque

Macaca

fascicularis,

pig-tailed

macaque

Macaca

nemestrina,

red

leaf

monkey

Presbytis

rubicunda,

silvered

leaf

monkey

Trachypithecus

cristatus,

Hose’s

leaf-monkey

Presbytis

hosei,

proboscis

monkey

Nasalis

larvatus,

Bornean

gibbon

Hylobates

muelleri,

Bornean

orangutan

Pongo

pygmaeus

Kanamori

et

al.

(2010)

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

21

Table

1

(Continued)

NoStudy

site

Area

(km2)

Latitude

Longitude

Elevation

(m

asl)

Annual

rainfall

(mm)

Maximum/minimum

temperature

(◦C)

Forest

type

Primate

community,

including

the

study

species

Reference

5

Way

Canguk

ﬁeld

station,

Bukit

Barisan

Selatan

National

Park,

(BBSNP)

Sumatra,

Indonesia

9

5.650◦S

104.160◦E

30

3000–4000

35/27

Dipterocarpus

Siamang

Symphalangus

syndactylus,

agile

gibbon

Hylobates

agilis,

Sumatran

surili

Presbytis

melalophos,

silvered

leaf

monkey

Trachypithecus

cristatus,

long-tailed

macaque

Macaca

fascicularis,

southern

pig-tailed

macaque

Macaca

nemestrina,

Sunda

slow

loris

Nycticebus

coucang,

western

tarsier

Cephalopachus

bancanus

O’Brien

et

al.

(2003)

6

Mahale

Mountains

National

Park

(MMNP),

Kigoma,

Tanzania

1600

6.250◦S

29.917◦E

773–2462

1750

27/12

Highland

montane

savanna,

evergreen

montane

forest,

gallery

forest,

Miombo

Brachystegia

woodland,

Combretum

woodland

Chimpanzee

Pan

troglodytes,

yellow

baboon

Papio

cynocephalus,

blue

monkey

Cercopithecus

mitis,

red-tailed

monkey

Cercopithecus

ascanius,

red

colobus

Colobus

badius,

vervet

monkey

Cercopithecus

aethiops,

Angolan

black-and-white

colobus

Colobus

angolensis,

thick-tailed

greater

galago

Otolemur

crassicaudatus,

lesser

galago

Galago

senegalensis

Nishida

(1990),

Itoh

(2015)

and

Nakamura

and

Itoh

(2015)

22

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

several

Old

World

primates

from

arboreal

sources,

and

(2)

propose

potential

ecologically

relevant

functions

of

this

behaviour.

Given

that

there

are

only

limited

published

accounts

of

unusual

drinking

behaviour

displayed

by

Old

World

monkeys

and

apes,

we

wish

to

appeal

to

other

ﬁeld

primatologists

to

collect

and

col-

late

in

the

future,

particularly

to

document

the

innovation

capacities

of

nonhuman

primate

species

facing

environ-

mental

challenges

during

foraging

and

to

understand

the

selection

pressures

driving

such

adaptive

behaviours.

Indeed,

comparisons

with

species

outside

of

the

Order

Primates

would

provide

an

even

wider

perspective

from

which

to

consider

the

possible

ecologically

relevant

functions

of

this

behaviour.

2.

Methods

Three

of

our

study

areas

are

located

in

India,

and

one

each

in

Malaysia,

Indonesia,

and

Tanzania

(Fig.

1).

All

sites

are

different

in

terms

of

their

climate,

vegetation

types

and

primate

communities

(Table

1).

The

species

have

been

listed

and

discussed

by

region.

We

used

opportunistic

sightings

to

record

the

drinking

behaviours

of

the

study

species,

during

research

designed

for

other

purposes.

Given

this

constraint,

it

is

entirely

possible

that

the

fre-

quencies

of

the

reported

behaviours

have

been

underestimated.

3.

Observations

N.S.

observed

dipping-and-licking

behaviour

in

western

hoolock

gibbons

and

northern

pig-tailed

macaques

in

May

2009

during

a

ﬁeld

study

on

the

primate

communities

of

Hollongapar

Gibbon

Sanctuary

(HGS),

Assam

state,

northeastern

India.

On

3

May,

2009,

an

adult

male

hoolock

gibbon

was

observed

in

the

mid-canopy,

just

above

a

tree-hole,

to

repeatedly

dip

his

right

hand

inside

the

hole,

ﬁlled

with

rainwater,

and

then

lick

the

water

from

his

ﬁngers

by

positioning

the

hand

over

his

mouth

(Fig.

2A,

Supplementary

Mate-

rial

S1).

Another

record

was

made

on

12

May,

2009

in

the

same

locality,

when

a

northern

pig-tailed

macaque,

on

a

different

tree,

was

observed

to

drink

water

in

a

similar

fashion.

An

adult

macaque

dipped

its

hand

repeatedly

inside

a

tree-hole

and

licked

its

palm

covered

with

water

(Fig.

2B,

Supplementary

Material

S2).

S.G.

observed

the

dipping-and-licking

behaviour

in

six

individ-

ual

bonnet

macaques

in

Bandipur

National

Park

(BNP),

Karnataka

state,

southern

India,

on

three

occasions.

On

15

April,

2013,

a

juve-

nile

male

was

observed

to

dip

his

hands

inside

a

hole

on

the

trunk

of

a

Ficus

benghalensis

tree.

He

then

brought

out

his

palm,

soaked

in

rainwater

that

had

accumulated

in

the

hole,

and

licked

the

drip-

ping

water

off

it,

repeating

this

behaviour

multiple

times.

On

21

April,

2014,

three

juvenile

females

and

an

adult

female

(mother

of

one

of

the

juveniles),

belonging

to

the

same

troop

as

the

for-

mer

juvenile

male,

were

observed

to

perform

dipping-and-licking

in

the

same

F.

benghalensis

tree,

but

at

a

different

tree-hole

than

that

observed

earlier

(Fig.

2C,

Supplementary

Material

S3).

The

on

22

April,

2014,

another

juvenile

male

of

this

troop

was

observed

to

drink

from

the

same

tree-hole

using

the

dipping-and-licking

method.

In

her

study

on

central

Himalayan

langurs

in

Kedarnath

Wildlife

Sanctuary

(KWS),

Uttarakhand

state,

northern

India,

H.N.

observed

one

particular

semi-rural

troop

of

this

species

to

have

six

principal

feeding

sites,

all

of

which

had

mountain-fed

streams

or

other

stable

sources

of

drinking

water

in

their

vicinity;

these

sources

were

regu-

larly

used

by

the

langurs.

At

one

oak

forest

site,

however,

the

closest

perennial

water

source

was

located

adjacent

to

a

human

settlement

and

between

January

and

September

2015,

H.N.

observed

11

bouts

of

drinking

by

both

central

Himalayan

langurs

and

rhesus

macaques

at

a

particular

tree-hole

on

an

oak

Quercus

leucotrichophora

tree.

Individuals

of

both

species

were

able

to

insert

their

heads

inside

the

hole

to

drink

directly

with

their

mouths

but

occasionally

used

the

dipping-and-licking

technique

with

their

hands

(Fig.

2D,

Sup-

plementary

Material

S4).

On

11

September,

2015,

H.N.

observed

one

adult

female,

two

adult

males

and

one

juvenile

langur

using

both

techniques

to

drink

water

from

the

hole

(Supplementary

Material

S4)

while

two

adult

females,

three

juveniles

and

two

subadult

males

were

again

seen

drinking

there

on

13

September,

2015.

On

one

of

these

occasions,

the

white

chin

hairs

of

a

langur

became

stained

with

a

yellow

colouration

after

it

had

drunk

directly

from

the

tree-

hole.

On

another

occasion,

a

rhesus

macaque

individual

was,

in

fact,

subsequently

observed

to

remove

and

discard

material

resembling

decomposed

plant

tissues

from

the

same

hole,

prior

to

drinking

water

from

it.

On

12

September,

2015,

two

rhesus

macaques

(a

subadult

and

an

adult

male)

were

observed

to

supplant

langurs

from

the

same

hole

and

use

it

to

drink,

employing

the

same

tech-

nique

as

the

langurs.

R.M.

recorded

33

events

of

water-drinking

behaviour

by

wild

Bornean

orangutans

in

Danum

Valley

Conservation

Area

(DVCA),

Sabah,

Malaysia

between

May–July

and

September–December

2013

and

between

February–December

2014.

Of

these

33

events,

22

acts

were

performed

by

adult

females

carrying

offspring

(n

=

6

individuals),

four

by

adolescents

(n

=

3)

and

seven

by

immature

individuals

(n

=

4).

In

31

of

these

33

events,

individuals

accessed

water

from

inside

tree-holes

by

dipping

their

hands

in

the

water.

There

were,

however,

two

different

ways

that

the

water

was

then

consumed.

One

consisted

of

cupping

the

ﬁngers

to

collect

the

water,

bringing

the

hands

to

the

mouth

and

then

either

drinking

from

the

cupped

hands

or

pouring

the

water

into

the

mouth

(Supplemen-

tary

Material

S7).

The

other

way

consisted

of

dipping

the

ﬁngers

into

the

water

and

transferring

water

to

the

mouth,

without

cup-

ping

the

ﬁngers,

but

in

a

rapid

grabbing-like

movement

(Fig.

2G,

Supplementary

Material

S8).

The

differences

in

the

two

methods

by

which

orangutans

obtained

water

from

the

tree-holes

may

have

been

due

to

dif-

ferences

in

the

size

and

depth

of

the

tree-holes,

or

possibly,

even

a

matter

of

individual

preference.

Less

frequently,

when

the

opening

was

large

enough,

they

were

observed

to

drink

from

tree-holes

directly

with

their

mouths.

In

the

two

other

drinking

events

observed,

an

adult

female

carrying

her

infant

was

observed

climbing

down

through

the

liana

and

drinking

from

the

stream,

immersing

her

mouth

directly

in

the

water

(Supplementary

Mate-

rial

S9).

Adult

female

orangutans

in

DVCA

were

rarely

observed

on

the

ground

and

this

was

the

only

context

in

which

they

were

seen,

other

than

short-distance

travel

from

one

tree

to

another.

The

immatures

followed

their

mothers’

behaviour

and

were

often

observed

to

drink

water

at

tree-holes

after

their

mothers

ﬁnished

drinking,

with

the

exception

of

a

seven-year-old

juvenile,

which

drank

before

his

mother.

Adult

male

orangutans

were

never

seen

to

drink

water

from

tree-holes

during

the

study

period

although

there

were

casual

observations

of

them

obtaining

water

from

both

tree-holes

and

streams

in

the

area

at

other

times.

Between

October

2007

and

April

2009,

L.M.

observed

541

drink-

ing

events

among

11

groups

of

wild

siamangs

in

the

Way

Canguk

locality

of

the

Bukit

Barisan

Selatan

National

Park

(BBSNP)

in

Suma-

tra,

Indonesia.

Adult

males

(n

=

20),

adult

females

(n

=

11),

large

juveniles

(n

=

8)

and

small

juveniles

(n

=

5)

were

observed

drinking

water

with

the

use

of

their

hands

233,

141,

115

and

52

times

respec-

tively

during

the

study

period.

In

12

other

instances,

siamangs

collected

water

directly

using

their

mouths.

Individual

siamangs

collected

rainwater

from

holes

in

tree

trunks

by

a

typical

sequence

of

hand

motions

and

postural

modiﬁcations

that

allowed

them

to

efﬁciently

extract

the

liquid

with

cupped

ﬁngers

and

bring

it

to

their

mouths

(Fig.

2F,

Supplementary

Material

S5).

Evidence

that

this

was

an

important

activity

for

the

population

came

from

the

alterna-

tive

observation

that

there

were

at

least

four

occasions

at

the

peak

of

the

dry

season

when

the

siamangs,

which

typically

remained

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

23

Fig.

2.

The

six

species

displaying

arboreal

drinking

behaviours,

described

in

this

study.

(A)

Western

hoolock

gibbon,

(B)

Northern

pig-tailed

macaque,

(C)

Bonnet

macaque,

(D)

Central

Himalayan

langur,

(E)

Chimpanzee,

(F)

Siamang,

and

(G)

Bornean

orangutan.

in

the

high

layers

of

the

canopy

and

virtually

never

descended

to

the

ground,

climbed

down

along

lianas

and

drank

directly

from

a

nearby

river

(Supplementary

Material

S6).

Access

to

a

water

source

in

tree-holes,

thus,

appeared

to

be

of

importance

to

the

siamangs.

This

hypothesis

was

further

supported

by

observation

of

social

ten-

sions

that

were

generated

in

the

groups

when

they

accessed

these

holes,

with

adult

females

initially

monopolising

the

water

source.

They

were

typically

followed

by

adult

males

and

then

by

subadults,

while

juveniles

were

generally

tolerated

during

drinking

episodes.

At

Mahale

Mountains

National

Park

(MMNP)

in

Kigoma

state,

Tanzania,

on

13

December,

1991,

M.A.H.

observed

three

chim-

panzees

(two

immature

males

and

a

mature

male)

approach

a

Monates

elegans

tree.

The

tree

had

a

small

natural

opening

about

1.5

m

above

the

ground

(Fig.

2E).

The

cavity

extended

down

into

the

central

part

of

the

trunk

to

a

depth

of

approximately

30

cm.

A

thickened

layer

of

bark

formed

a

small

over-hanging

lip

and

created

a

small

recess

above

and

around

the

natural

opening.

There

was,

in

this

recess,

a

dark,

resinous

material-covered

nest

of

a

ﬂying

insect,

tentatively

identiﬁed

to

be

a

species

of

the

sweat

bee

Megalopta.

Dark

stains

from

the

nest

streaked

down

into

the

hole,

suggest-

ing

that

a

rainwater-leached

substance

from

the

nest

may

have

been

deposited

in

the

hole.

The

chimpanzees

lined

up,

in

accor-

24

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

dance

to

their

relative

age,

with

the

younger

individuals

behind,

patiently

waiting

for

a

chance

to

access

the

tree-hole.

Each

indi-

vidual

then

climbed

up

to

the

hole,

in

turn,

inserted

their

hands

inside,

withdrew

liquid-dripping

ﬁngers

and

licked

them,

this

pro-

cess

being

repeated

several

times

by

each

individual.

When

the

group

left,

M.A.H.

smelled

and

tasted

a

few

drops

of

the

same

liquid.

It

was

salty

and

had

a

strong

smell

of

human

sweat.

This

behaviour

was

observed

only

once

at

this

location.

During

the

same

season,

however,

at

another

site,

M.A.H.

periodically

observed

chimpanzees

using

similar

techniques

to

drink

water

from

a

tree

of

another

species

Parinari

curatellifolia

(dates

not

recorded).

In

this

case,

the

chimpanzees

used

a

sponge

made

of

softened

woody

material

scraped

from

the

interior

of

the

tree-hole

by

hand.

A

later

visual

inspection

of

the

hole

revealed

the

water

inside

to

be

brown-

ish

in

colour

but

with

no

evidence

of

any

insect

nest

in

the

hole,

as

in

the

Chimpanzees

have

occasionally

been

observed

to

drink

water

from

holes

in

trees

in

MMNP

but

the

frequency

has

never

been

too

high,

possibly

due

to

their

having

ample

year-round

access

to

streams

throughout

their

home

ranges.

4.

Discussion

We

have

documented

and

systematically

collated

the

‘dipping-

and-licking’

method

of

drinking

of

water

(Wrangham,

1981)

in

several

wild

populations

of

Old

World

primate

species,

including

the

Bornean

orangutan,

siamang,

western

hoolock

gibbon,

northern

pig-tailed

macaque,

bonnet

macaque

and

the

central

Himalayan

langur,

and

provided

further

evidence

for

its

presence

among

chim-

panzees.

It

is

noteworthy,

in

this

context,

that

there

are

species

or

their

particular

populations,

which

have

never

been

reported

to

use

this

method

to

drink

water

in

spite

of

prolonged

observations

(e.g.,

Trachypithecus

johnii,

Poirier,

1970).

Whether

this

reﬂects

a

species-typical

failure

or

simply

a

lack

of

opportunity

or

need

for

some

populations

of

an

otherwise

capable

species

to

simply

employ

this

method

during

their

foraging

for

water,

however,

remains

to

be

discovered.

It

may

be

expected

that

arboreal

primates

would

be,

in

general,

more

likely

to

drink

water

from

tree-holes

than

would

largely

ter-

restrial

species.

The

arboreal

species

that

we

studied,

indeed,

did

display

relatively

higher

frequencies

of

drinking

from

tree-holes

than

did

the

terrestrial

monkeys

and

apes.

It

is,

nevertheless,

impor-

tant

to

understand

why

largely

terrestrial

primates

occasionally

also

do

drink

water

from

tree-holes.

First,

in

response

to

our

hypothesis

that

seasonal

water

short-

ages

could

play

a

role

in

primates

switching

to

alternative

water

sources,

we

expected

that

drinking

from

tree-holes

would

be

more

prevalent

during

dry

seasons,

provided,

of

course,

these

holes

did

have

adequate

water

in

them.

However,

contrary

to

our

expecta-

tions,

this

behavioural

strategy

was

observed

particularly

during

the

wet

season

in

not

only

the

arboreal

hoolock

gibbon

but

also

in

the

relatively

terrestrial

species

like

the

pig-tailed

macaque,

rhesus

macaque

and

the

central

Himalayan

langur,

and

in

habi-

tats

that

had

abundant

fruits

or

tender

leaves

at

the

time

and

when

water

was

available

from

multiple

free-ﬂowing

sources.

In

the

Bandipur

National

Park

in

southern

India,

however,

there

were

three

instances

of

bonnet

macaques

using

tree-holes

in

a

relatively

dry

period,

but

when

afternoon

showers

had

ﬁlled

up

the

holes

with

water.

It

must

also

be

recognised

that

certain

trees

in

some

habi-

tats

may

be

particularly

suitable

for

the

accumulation

of

water

in

their

tree-holes

and

thus

facilitate

drinking

behaviour

more

often

than

from

other

sources

in

the

same

habitat.

In

the

Bandipur

National

Park,

for

example,

other

troops

of

bonnet

macaques

did

not

display

such

drinking

behaviour,

even

after

rains.

They

had

instead

been

observed

to

lick

rainwater

from

leaves

or

acquire

drinking

water

from

other

sources

by

lapping

up

water

from

the

ground,

kitchen-pipes,

buckets,

bottles

or

other

opportunis-

tic

anthropogenic

sources.

Although

the

individuals

in

the

study

troop,

in

which

dipping-and-licking

behaviour

was

observed,

had

also

utilised

other

water

sources,

the

presence

of

a

particular

tree

with

a

hole

that

accumulated

rainwater

may

have

afforded

a

conve-

nient

opportunity

for

the

display

of

the

observed

behaviour

by

this

troop.

In

this

context,

it

is

noteworthy

that

the

water-hole

was

used

mostly

by

juvenile

individuals

of

this

troop,

a

possible

outcome

of

the

curiosity-driven

behaviour

of

immature

individuals.

Alterna-

tively,

it

is

possible

that

the

acquisition

of

water

from

sources

other

than

those

used

by

the

adults

of

the

group

is

a

juvenile

strategy

to

avoid

confrontation

with

or

aggression

from

the

adults

of

the

group.

Our

results

and

arguments

thus

suggest

that

certain

habitats

and

suitable

trees

may

facilitate

the

drinking

of

water

from

tree-

holes

by

individual

primates.

Wet

seasons

are

also

likely

to

be

the

most

suitable

times

when

tree-holes

contain

water,

which

can

be

proﬁtably

exploited

by

primates,

although

this

begs

the

question

of

why

these

species

do

not

invariably

drink

from

free-ﬂowing

water

sources,

which

are

also

easily

available

during

these

seasons.

A

possible

response

to

this

question

could

be

represented

by

our

second

hypothesis

that

arboreal

primates

may

take

recourse

to

drinking

water

from

tree-holes

at

certain

times

and

in

spe-

ciﬁc

localities

in

order

to

avoid

terrestrial

predators

(e.g.,

Starin,

2002).

Gibbons,

siamangs

and

orangutans

are

strongly

adapted

to

arboreal

life

and

are,

thus,

usually

not

motivated

to

descend

to

the

ground

in

search

of

water,

except

perhaps

under

exceptional

circumstances.

This

reluctance

to

be

terrestrial

could

perhaps

be

ascribed

to

increasing

risks

of

predation

when

on

the

ground.

This

possibility

appeared

to

be

supported

during

our

studies

when

we

observed

siamangs

in

Sumatra

and

Bornean

orangutans

in

Sabah,

both

extremely

arboreal

species,

to

descend

to

the

ground

rather

rarely,

and

that

too

only

in

search

of

water.

Moreover,

the

impor-

tance

of

tree-holes

as

sources

of

water

for

the

siamangs

was

clearly

evidenced

when

we

observed

intra-group

inter-sexual

scramble

competition

for

these

sources

of

water.

A

noteworthy

variation

of

such

decision-making

was

encoun-

tered

during

H.N.’s

studies

on

the

central

Himalayan

langur

in

northern

India.

The

semi-rural

troop

of

this

species,

which

extracted

water

exclusively

from

a

tree-hole,

when

ranging

in

this

particular

area

(but

drank

from

ground

water

sources

in

other

areas),

possibly

did

so

in

order

to

avoid

the

risk

of

encounter-

ing

humans,

which

appeared

inevitable

had

they

used

the

only

perennial

water

source

available.

Additionally,

it

is

perhaps

illu-

minating

that

the

largely

terrestrial

rhesus

macaques

at

this

site

also

employed

this

particular

tree-hole

to

extract

water

and

were

even

observed

to

compete

with

the

langurs

for

this

resource.

Our

predation-avoidance

hypothesis

could

also

potentially

explain

the

unusual

cases

of

bonnet

macaques

in

the

Bandipur

National

Park,

which

employed

particular

tree-holes

as

sources

of

rainwater

even

though

the

observed

troop

was

largely

terrestrial

and

usu-

ally

obtained

water

from

perennial

ground

sources

across

its

home

range.

Our

third

hypothesis

was

that,

regardless

of

an

arboreal

or

largely

terrestrial

habit,

certain

primate

populations

may

obtain

potentially

medicinal

or

other

nutritional

beneﬁts

from

substances

that

may

leach

into

the

rainwater,

which

accumulates

in

holes,

from

the

tree

or

from

other

materials

deposited

on

the

tree.

During

the

period

of

observation

at

Mahale

in

Tanzania,

for

example,

many

of

the

chimpanzees,

which

were

followed,

exhibited

signs

of

gastroin-

testinal

disorder

(diarrhoea),

parasitosis

(oesophagostomiasis)

and

simultaneously

exhibited

one

or

both

of

two

self-medicative

behaviours—leaf-swallowing,

which

is

known

to

physically

expel

adult

Oesophagostomum

stephanostomum

worms,

or

ingest

the

pharmacologically

active,

bitter

pith

of

Vernonia

amygdalina,

which

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

25

is

known

to

reduce

symptoms

of

O.

stephanostomum

infection

(Huffman

et

al.,

1996,

1997;

Huffman

and

Caton,

2001).

In

the

case

of

the

semi-rural

troop

of

central

Himalayan

lan-

gurs,

the

observed

yellow

staining

of

the

chin

hairs

of

an

individual

after

it

had

drunk

water

from

a

tree-hole

suggested

that

the

water

could

have

contained

materials

leached

into

it,

most

likely

from

the

wood

itself

or

possibly

from

the

oak

leaves

that

had

accumu-

lated

inside

the

water-ﬁlled

hole.

Oak

leaves

are

characteristically

high

in

condensed

tannins,

a

group

of

compounds

known

for

their

signiﬁcant

anti-parasitic

activity

(e.g.,

Hoste

et

al.,

2009;

Williams

et

al.,

2014).

It

is

tempting

to

speculate

that

the

langurs

could

have

sought

out

the

water

from

this

particular

tree-hole

for

its

particular

anti-parasitic

properties

but

this

hypothesis

remains

to

be

tested.

In

the

case

of

the

chimpanzees

of

Mahale

too,

it

is

unlikely

that

they

used

the

tree-hole

simply

for

water,

as

there

were

many

free

ﬂowing

streams

in

the

area.

One

must,

therefore,

consider

the

pos-

sibility

that

there

was

some

added

appeal

from

the

extracts

of

wood

and

the

sweat

bee

nest,

which

attracted

the

individuals

to

this

water.

Elsewhere,

in

the

habitat,

chimpanzees

have

also

been

observed

to

lick

the

material

that

had

accumulated

below

sweat

bee

nests

on

rocks.

Additionally,

there

are

a

few

possibilities,

currently

beyond

the

scope

of

our

observations,

which

could

constitute

productive

avenues

of

future

research.

Commonly

explored

relationships

in

folivorous-frugivorous

New

World

primates,

for

example,

are

those

between

the

degree

of

folivory

and

the

frequency

and

timing

of

drinking

behaviour

in

certain

species

populations

or

the

possible

inﬂuence

of

relative

humidity

and

diet

composition

on

the

time

of

drinking

of

water

(Norconk

et

al.,

1996;

National

Research

Council,

2003;

and

references

therein);

our

knowledge

of

Old

World

mon-

keys

and

apes

would

clearly

beneﬁt

from

such

explorations.

Finally,

although

we

do

not

have

any

information

yet

regarding

the

origins

and

spread

of

this

unusual

behaviour

in

the

study

species

and

populations,

it

is

possible

that

certain

individuals

may

have

independently

acquired

such

behavioural

strategies

by

accident

or

trial-and-error

learning

and

that

these

strategies

may

have

then

spread

in

the

groups,

to

which

these

individuals

belong,

by

social

learning

(reviewed

in

Avital

and

Jablonka

2000).

More

detailed

observations

need

to

be

conducted

on

these

and

other

neighbouring

groups

within

each

population

to

discern

whether

such

behaviours

of

cultural

origin

display

rapid-spread,

parent-offspring

or

group-

speciﬁc

patterns

(Cavalli-Sforza

and

Feldman,

1981;

reviewed

in

Huffman

and

Sinha,

2011).

It

may

also

be

pertinent

to

note

here

that,

amongst

our

study

species,

cultural

traditions

in

food

acquisi-

tion

and

handling

as

well

as

other

foraging-related

strategies

have

been

well

documented

in

chimpanzees

(Tomasello,

1990;

McGrew,

1992;

Whiten,

2000;

Matsusaka

et

al.,

2006;

Huffman

and

Sinha,

2011),

orangutans

(van

Schaik

et

al.,

2003)

and

in

bonnet

macaques

(Sinha,

2005;

Huffman

and

Sinha,

2011).

In

conclusion,

our

observations,

we

believe,

are

useful

in

further-

ing

a

more

comprehensive

understanding

of

how

primates

procure

water,

an

essential

component

of

their

diet.

We

have

suggested

a

number

of

possible

reasons

why

certain

unusual

forms

of

water

acquisition

strategies

may

be

prevalent

in

certain

primate

species

and

populations,

and

the

beneﬁts

that

may

accrue

to

the

practition-

ers

of

these

behaviours.

We

believe

that

the

drinking

water

from

holes

in

trees

might

be

more

prevalent

than

previously

thought,

given

the

wide

range

of

species

and

habitats

represented

in

this

preliminary

investigation.

While

such

behavioural

strategies

may

be

of

relatively

rare

occurrence

in

most

primate

populations,

more

systematic

observations

are

required

to

accurately

ascertain

the

frequency

and

signiﬁcance

of

these

strategies

for

particular

pop-

ulations

or

individuals

(see,

for

example,

Dittus,

1977).

We

hope

that

this

report

will

stimulate

similar

research

in

other

primate

species

and

further

discussions

on

the

possible

functions

of

these

unusual

behaviours

for

the

health

and

general

survival

of

primate

populations

and

their

individual

members.

Acknowledgements

N.S.

and

A.S.

are

grateful

to

the

Assam

Forest

Department

for

permission

to

work

in

the

Hollongapar

Gibbon

Sanctuary,

and

Dilip

Boruah

and

Noren

Bhuyan

for

their

help

during

the

ﬁeldwork.

S.G.

and

A.S.

thank

H.C.

Kantharaju

of

the

Karnataka

Forest

Depart-

ment

for

his

support

during

their

research

at

the

Bandipur

National

Park.

S.G.

is

also

grateful

to

Jagadish

M

and

Sharmi

Sen

for

assis-

tance

during

ﬁeldwork.

The

ﬁeld

study

in

Bandipur

National

Park

was

partially

funded

by

the

Department

of

Science

and

Technol-

ogy,

Government

of

India

(Cognitive

Science

Research

Initiative

Grant

SR/CSI/44/2008).

N.S.

and

H.N.

were

supported

by

Rufford

Small

Grants

(Grants

62-09-08

and

16805

respectively)

during

their

respective

studies.

H.N.

would

like

to

thank

Akash

Verma,

Divisional

Forest

Ofﬁcer,

Kedarnath

Wildlife

Sanctuary

for

grant-

ing

the

required

permits,

and

her

ﬁeld

assistants,

Abhi,

Alissa,

Nitin,

Rimung

and

Munib.

L.M.

thanks

his

research

assistants

Laji,

Tarmin,

Usman,

Maryadi,

Mislan,

and

Budi

for

their

collaboration

in

data

collection.

His

research

was

supported

by

grants

from

the

National

Science

Foundation

(Grant

ID

0726022),

Wenner-Gren

Foundation

(Grant

7766),

and

research

clearance

from

the

State

Ministry

of

Research

and

Technology

and

Forestry

Department

of

Indonesia.

M.A.H.

thanks

his

ﬁeld

assistant,

the

late

Mohamedi

Seifu

Kalunde

(Tanzanian

National

Parks)

for

sharing

his

knowl-

edge

of

jungle

lore

and

his

crucial

assistance

in

the

ﬁeld.

He

also

thanks

COSTECH,

TAWIRI

and

TANAPA,

the

administrative

bod-

ies

that

grant

research

clearance

in

Tanzania.

R.M.

thanks

Tetsuro

Matsuzawa

for

supporting

her

research,

her

collaborators,

Tomoko

Kanamori

and

Noko

Kuze,

and

her

research

assistants

Eddy

Boy,

Poleh

Bin

Inging

and

Kirmizi

Bin

Rosliu

for

the

help

during

her

ﬁeldwork.

She

is

also

grateful

to

the

Sabah

Biodiversity

Centre

and

Danum

Valley

Management

Committee

for

granting

permis-

sion

to

conduct

her

research

and

to

the

Royal

Society

SE

Rainforest

Research

Programme

for

providing

climate

data.

R.M.

was

sup-

ported

by

a

Grant-in-Aid

for

Specially

Promoted

Research,

No.

24000001

(PI:

Tetsuro

Matsuzawa)

by

the

Ministry

of

Education,

Science,

Sports

and

Culture,

Japan

and

by

ITP-HOPE

Program

to

Tetsuro

Matsuzawa.

Appendix

A.

Supplementary

data

Supplementary

data

associated

with

this

article

can

be

found,

in

the

online

version,

at

http://dx.doi.org/10.1016/j.beproc.2016.

05.006.

References

Angus,

S.,

1971.

Water

contact

behavior

of

chimpanzees.

Folia

Primatol.

14,

51–58.

Avital,

E.,

Jablonka,

E.,

2000.

Animal

Traditions:

Behavioural

Inheritance

in

Evolution.

Cambridge

University

Press,

Cambridge.

Baranga,

D.,

1982.

Nutrient

composition

and

food

preferences

of

colobus

monkeys

in

Kibale

Forest,

Uganda.

Afr.

J.

Ecol.

20,

113–121.

Barton,

R.A.,

Whiten,

A.,

Byrne,

R.W.,

English,

M.,

1993.

Chemical

composition

of

baboon

plant

foods:

implications

for

the

interpretation

of

intra-

and

interspeciﬁc

differences

in

diet.

Folia

Primatol.

61,

1–20.

Bicca-Marques,

J.C.,

1992.

Drinking

behavior

in

the

black

howler

monkey

(Alouatta

caraya).

Folia

Primatol.

58,

107–111.

Calvert,

J.J.,

1985.

Food

selection

by

western

gorillas

(G.

g.

gorilla)

in

relation

to

food

chemistry.

Oecologia

65,

236–246.

Carpenter,

C.R.,

1964.

A

ﬁeld

study

in

Siam

of

the

behavior

and

social

relations

of

the

gibbon.

In:

Carpenter,

C.R.

(Ed.),

Naturalistic

Behavior

of

Nonhuman

Primates.

Pennsylvania

State

University

Press,

University

Park,

Pennsylvania,

pp.

145–271.

Cavalli-Sforza,

L.L.,

Feldman,

M.W.,

1981.

Cultural

Transmission

and

Evolution:

A

Quantitative

Approach.

Princeton

University

Press,

Princeton.

Chapman,

C.,

1988.

Patterns

of

foraging

and

range

use

by

three

species

of

neotropical

primates.

Primates

29,

177–194.

26

N.

Sharma

et

al.

/

Behavioural

Processes

129

(2016)

18–26

Chatterjee,

M.,

2012.

An

Uncommon

Performing

Monkey:

Behavioural

Flexibility

and

Social

Diversity

in

the

Northern

Bonnet

Macaques

Macaca

radiata

radiata.

Doctoral

Thesis.

National

Institute

of

Advanced

Studies,

Bangalore

and

Manipal

University,

Manipal,

India.

Chivers,

D.J.,

1977.

The

feeding

behaviour

of

siamang

(Symphalangus

syndactylus).

In:

Clutton-Brock,

T.H.

(Ed.),

Primate

Ecology:

Studies

of

Feeding

and

Ranging

Behaviour

in

Lemurs,

Monkeys

and

Apes.

Academic

Press,

London,

pp.

355–382.

Ciani,

A.C.,

Martinoli,

L.,

Capiluppi,

C.,

Arahou,

M.,

Mouna,

M.,

2001.

Effects

of

water

availability

and

habitat

quality

on

bark-stripping

behavior

in

Barbary

macaques.

Conserv.

Biol.

15,

259–265.

Deﬂer,

T.R.,

1979.

On

the

ecology

and

behavior

of

Cebus

albifrons

in

eastern

Colombia:

I.

Ecology.

Primates

20,

475–490.

Dias,

P.A.D.,

Rangel-Negrín,

A.,

Coyohua-Fuentes,

A.,

Canales-Espinosa,

D.,

2014.

Factors

affecting

the

drinking

behavior

of

black

howler

monkeys

(Alouatta

pigra).

Primates

55,

1–5.

Dittus,

W.P.J.,

Rainier

III,

H.S.H.P.,

1977.

The

socioecological

basis

for

the

conservation

of

the

toque

monkey

(Macaca

sinica)of

Sri

Lanka

(Ceylon).

In:

Bourne,

G.H.

(Ed.),

Primate

Conservation.

Academic

Press,

New

York,

pp.

237–265.

Edwards,

M.S.,

1995.

Comparative

Adaptations

to

Folivory

in

Primates.

Doctoral

Thesis.

Michigan

State

University,

East

Lansing,

Michigan,

USA.

Fitch-Snyder,

H.,

Carter,

J.,

1993.

Tool

use

to

acquire

drinking

water

by

free-ranging

lion-tailed

macaques

(Macaca

silenus).

Lab.

Primate

Newsl.

32,

1–3.

Freese,

C.H.,

1978.

The

behavior

of

white-faced

capuchins

(Cebus

capucinus)

at

a

dry-season

waterhole.

Primates

19,

275–286.

Gairola,

S.,

2010.

Phytodiversity,

Forest

Composition,

Growing

Stock

Variation

and

Regeneration

Status

in

the

Mandal-Chopta

Forest

of

Garhwal

Himalaya.

Doctoral

Thesis.

Garhwal

University,

Garhwal,

Uttarakhand,

India.

Giudice,

A.M.,

Mudry,

M.D.,

2000.

Drinking

behavior

in

the

black

howler

monkey

(Alouatta

caraya).

Zoocriaderos

3,

11–19.

Glander,

K.E.,

1978.

Drinking

from

arboreal

water

sources

by

mantled

howling

monkeys

(Alouatta

palliata

Gray).

Folia

Primatol.

29,

206–217.

Hillyer,

A.P.,

Armstrong,

R.,

Korstjens,

A.H.,

2015.

Dry

season

drinking

from

terrestrial

man-made

watering

holes

in

arboreal

wild

Temminck’s

red

colobus,

The

Gambia.

Primate

Biol.

2,

21–24.

Hoste,

H.,

Brunet,

S.,

Paolini,

V.,

Bahuaud,

D.,

Chauveau,

S.,

Fouraste,

I.,

Lefrileux,

Y.,

2009.

Compared

in

vitro

anthelmintic

effects

of

eight

tannin-rich

plants

browsed

by

goats

in

the

southern

part

of

France.

In:

Papachristou,

T.G.,

Parissi,

Z.M.,

Ben

Salem,

H.,

Morand-Fehr,

P.

(Eds.),

Nutritional

and

Foraging

Ecology

of

Sheep

and

Goats.

CIHEAM/FAO/NAGREF

Options

Méditerranéennes:

Série

A.

Séminaires

Méditerranéens,

No.

85,

431–436.

Huffman,

M.A.,

Caton,

J.M.,

2001.

Self-induced

increase

of

gut

motility

and

the

control

of

parasitic

infections

in

wild

chimpanzees.

Int.

J.

Primatol.

22,

329–346.

Huffman,

M.A.,

Sinha,

A.,

2011.

Nature

and

culture.

In:

Narasimha,

R.,

Menon,

S.

(Eds.),

Project

of

History

of

Indian

Science,

vol.

XIV.

Philosophy

and

Culture

Centre

for

Studies

in

Civilizations,

New

Delhi,

pp.

367–389

(Part

1).

Huffman,

M.A.,

Koshimizu,

K.,

Ohigashi,

H.,

1996.

Ethnobotany

and

zoopharmacognosy

of

Vernonia

amygdalina,

a

medicinal

plant

used

by

humans

and

chimpanzees.

In:

Hind,

T.J.N.

(Ed.),

Compositae,

Proceedings

of

the

Compositae

Conference,

Kew,

1994,

Vol.

2,

Biology

and

Utilization.

Royal

Botanic

Gardens

Kew,

UK,

pp.

351–360.

Huffman,

M.A.,

Gotoh,

S.,

Turner,

L.A.,

Hamai,

M.,

Yoshida,

K.,

1997.

Seasonal

trends

in

intestinal

nematode

infection

and

medicinal

plant

use

among

chimpanzees

in

the

Mahale

Mountains,

Tanzania.

Primates

38,

111–125.

Itoh,

N.,

2015.

Climate

and

climatological

trends

in

the

Kasoje

Forest.

In:

Michio,

N.,

Kazuhiko,

H.,

Noriko,

I.,

Koichiro,

Z.

(Eds.),

Mahale

Chimpanzees:

50

Years

of

Research.

Cambridge

University

Press,

Cambridge,

pp.

143–149.

Kala,

S.P.,

Gaur,

R.D.,

1982.

A

contribution

to

the

ﬂora

of

Gopeshwar

(Chamoli-

Garhwal).

In:

Paliwal,

G.S.

(Ed.),

The

Vegetation

Wealth

of

Himalayas.

Puja

Publishers,

New

Delhi,

pp.

347–413.

Kanamori,

T.,

Kuze,

N.,

Bernard,

H.,

Malim,

T.P.,

Kohshima,

S.,

2010.

Feeding

ecology

of

Bornean

orangutans

(Pongo

pygmaeus

morio)

in

Danum

Valley,

Sabah,

Malaysia:

a

3-year

record

including

two

mast

fruitings.

Am.

J.

Primatol.

72,

820–840.

Matsusaka,

T.,

Nishie,

H.,

Shimada,

M.,

Kutsukake,

N.,

Zamma,

K.,

Nakamura,

M.,

Nishida,

T.,

2006.

Tool-use

for

drinking

water

by

immature

chimpanzees

of

Mahale:

prevalence

of

an

unessential

behavior.

Primates

47,

113–122.

McGrew,

W.C.,

1992.

Chimpanzee

Material

Culture:

Implications

for

Human

Evolution.

University

of

Cambridge,

Cambridge.

Nakamura,

M.,

Itoh,

N.,

2015.

Overview

of

the

ﬁeld

site:

Mahale

Mountains

and

their

surroundings.

In:

Michio,

N.,

Kazuhiko,

H.,

Noriko,

I.,

Koichiro,

Z.

(Eds.),

Mahale

Chimpanzees:

50

Years

of

Research.

Cambridge

University

Press,

Cambridge,

pp.

7–20.

National

Research

Council,

2003.

Nutrient

Requirements

Watering holes: The use of arboreal sources of drinking water by Old World monkeys and apes

Figures