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

Authors:
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
26.691N
94.338E
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
11.662N 76.627E 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
20.484N
79.280E
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
5.650S
104.160E
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
6.250S
29.917E
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
related
information
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
next
day,
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
previous
case.
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.
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