JoURNAL oF ThoprcAl- Bromcy A\D CoNsERvrroN, 2 (l ) : 65-70, 2006
Res€arch article
Seed
spitting and
seedswallowing by wild orang-utans
(pozgo pygmaeus monb) in Sabah,Malaysia
MartAN(RENAZ'r,IsabelhLACKI\{AN-ANCRENAZ$dHamirshELABAN
Ki
abatangan Orungutan Consenation Project, pO Box 3109, 90731 Sandakaa Sabah, MalaysiaConerpondcrce adbess: Austrul
Pait
Lorong 10, House 35 88300 Kora KiMbaIa Sabah, Matarsia6
ARSTRACT.
Wild
orang,utans (Pona,ptgnaeus moio) studied at
the"KirabatangarOrang-utan Conse ation project", Sabah, Malaysia, are mainly frugivorous. They are regularly observed ro swallow large seeds (length longer than five
rnm) ftom 37 different plant genera and to spit large seeds ftom 27 plant genera. For rkee
of
these genera, we compared the time to first
germination, the germination success, the 507, gemination time and s€€dling mortaliry
of
seeds that were spat out, swallowed or left unprocessed by orang-utans. Our results show that mean time from planting ro germination was shorter and seed germimrion rate was higher for seeds swallowed or spar than for seeds collecled f.om the parent tree for two tee species (D/ac ontomzlnn dao atld
Koo
ensinden&on ptundtn,
both sp€cies being part of the Anacardiaceae Family). For D .ddr, gemination success was better forseeds that were spat than swalowed, showing the potential inportance of seed-cleaning and seed-spitting by orang-utans for ce(ain rree species occuning within the natural orang- utan habitat.
INTRODUCTION
Seed swallowing has beer documented as rhe most colnmon way for seed dispersal by apgs
(Wrangham
et al.,
1994]. Chapman&
Orderdonl, 1998; Poulsen et a1.,2001).'the process
of
seed cleaningby
apes (i.e.consumption and rmoval of the exocarp and of the flesh of the fruit that is found around the endocarp) is also said to provide better gemination chances to the seeds (Lamberr, 2001). Seed spitting however is conmonly
seen as playing a minor rcle for seed dispersal.
At Kibale (Jganda), 82% of the tluit species eaten by chimpanzees were swallowed and defecated while seed spitting represented only 7% (Lambert & carber 1998).lnBomeo, Mcconkey (2000) reported se€ds of77 sp€cies in gibbon feces (i.e. 48% of fiuit species eaten) but only four types (or 2.5%) werc spat by this species. Orang-utans are described as
"gardeners o. culrivaro$ of much of their own povisions" in tlle forest (Rijkseen & Meijaard, 1999) since they have a large gut capaciry with variable gut passage time, consume targe quanrities of fruits from a wide variety
of
species, and can travel long distances in
nearly all E?es of habitats. Ar Tanjung Puring (Indonesia), nn}lalmed seeds of 23 species of plants were collected in 94% oforangutan Ke!
vo
s, Ponso Denaeus, seed spitling. seedddgub,
(crrdik^. le32) seed swalowinglhsiol*jd.lydnpesedbyo'h3.int
sNda
(gis@, b*.
sibboE hmbills,d)
o;ghbq
1901 j Ung,r, tg93rwuld.de, rgcr).'rhis
E!.n
inv*risares rh. pd$ibre rcle ot dmsrd sd
dispdsdh
$e r@ds of rheE@€lholosiel
dudi6 or*ild
hrbitoaedIn sabah o.,talaysiq Bom.o). acdholoeical
obsdaiios
oreild odtdd.
have ben codducrdsiG
193 d a 4 .q km inr.nsiv.sdy:iEGll3'l7 bll3'l3 r{'N532'2.r
io 5'33 30 ) esbhlished in sEood:ry nix€d
l
hnd diprero.rQ andt6h lab
swampleg.nerarion
(Ao euz ,, 4r.,
2004).a$isbob. Dah
nre couecred on diet@npsirim, sdvny budg.r Enging paften md
scill
b.hrvid.sp4i$
md planrpft
bmtrghr brck ro rhe KocP ndion for
tu!\q
i&tuiricrton by pnr*sional
bohlnr iion
rhg
"s.p
ok Foren Reserrchcenter'
rollo{r
Feca*eE
plaed in cleln plAticbags
nd
brcoghtb,.k
ro rhc(ocP
Fierdsciio,.
Each$npl.
wrs thcn{.ish.d,
OMNo-n^N
3D sl]Tc
$a
fiEm
loq) w6 rured,s lbsed,ft,
common, orubundmL
ks. sd. oo'gq
duo nve
m) *ft
exuaccd. cotrMdod
ideotih€n
h llnu
level *irh rhe asnbncefton borlihts lroi
rhcs.pnok Forc*
R*mh
c.drcio,iy
rrseEds wft
u$din rhis sddy (i... siz
lmsdrbdfr.m
lors) Dunng obsdnidd boub, weds
mllede!s..ds
ftmlnc
roEs trmi rh,r drtdl oms- ubs
spa',sd
dpeftlib
GdgimtinsrDr
In order ro
asss
n\eovm]l inpd
of Cutpft.e$iq Ydui onl presing
rrore ohclanctcrisi6,
we moduded a gem'imdderpa*n.d {irhlf c.
eds
(more rhrnfiE m
iD l.ngrh) orrhE 3F.i4
of nlir dta!wclrmody mumed
by
orhs,otms d
rheKocP
stody sne:pintatun
\ nacaii..ee),
an<tMincot .rasin*d (rili8ce). 1@
difiemr&€s ol lot *erc
considged:inlrl.ndo.,rp.
cndc.rps spar by
focll
oransurds, dd
0d6ve
iDd
endcarsdfoib
w.E pracd in pre$ic polybassrill.d
trpfrfi
ctan soil con.&d fDn a sinslelmnidi ii
ItefmsL
Tne ba$ weE *ept in
pdi,i
shrdeuidtr nxrrrr dry-r.i8rh
condliotrs 3ddw{.
w dd $ Bd.d
Dudng oitre monrhs,*e stc.es (cmd ie
numbtr ofeido$ipr
prcducine
sedringrnt b*
otend€rps
Dlanred) and the numberor s..dliias
pdtrd b, e iohiple
s.dedhde,Jps ot
D.d,o
rnd M. etussilotio.\N.
rtsDdebdined fie
50*
S.mimrionrire
(fmtMecANdEtr'.Is{ruf,aM-A\l]Nr sdtr^HF rrrN
(200r), lar.ncy
shouldb.
consid.redsicirlicddydif.Fmly'wofutimb
ilmi.sful
ForD ara, rh. s0%smimrid
dm. or s{,rrdwed seeds
ocs
at 33 drys,forspar$.ds
4t days md forfdib
!t3l
d!yr. shorinsr $cnifi.m
d.tay tor rruitgeminddempqEd6dft*oo1lragmtres'
nor rignificrndy iDnmc.d by rhe My
s.ds wft
plmssn by omg tr@r D d4a 03.14tor
Fd{piftiig; 36J*
ror s..narauo{ins:x,4.4!,
p>n.l):r.
phnotun156,3
d@ e%:
t
= D.52" p>n., M. crc
t atoti
d Q5.3.k md 2r.5%:f=
r.06,Pn3) Fcr/dd,f@
$edrings
w.r
prcduc.dbr iulli{eded
.ndocirys
sp
(12?.7%) rhm svalrowed (e4.6,6), bur lhis resoxws
3ignincaDdydi$erenr
p=0r
onty (11= 3.60,]xt.n
conbined bgerhe4 .ndoca?s or
t
&a &are@ pres.d
by onne&n pmduftdn@
k.dibgs .h.n fruia 00t.196 asainn 19.r%l t,= 24.1, p{.00D
cove
.1y,I@s.edtingr*c
prcduc.dwid n!i6
orM. narsiro,r,(rr04) Llln
wirb eDdeirys ploc*sed by{ms uM
(23gft): x?=72 %. p<o.00l).onr.ioed seed
fresfenh, showiig
rhe pornd,rhd
pEdarorbte oI dris speiesrd .everd
pradr5. However,onng
u&ns svlllowed whole s..ds oi a! l.a$ 37 senen yia}lcrdsmindion, n*iog $.fr
poleDrisl5..d
dispen$ l& nmy re.
spei.s.fte
hishly prchsile, iobile sd nusnt'rtip3 or
oms uds
feilihre fmdF@sing,
npidlruir
rreshids. ion
and...d{piting
(cddiks,
1932) md hav. b.cn rumrioi.uy comparddro rhe
chaeckpouch.sof ca!.pitEim
(*hl*ei 19?9).of dpsilmr
sho*€n
$ spi(iis
rnds*axoviig
had asimilretrdons.ed
gmiBdm
iift eprsr
uhDs in !h.
loy.r Ki'sb
rngm. Anhoqhrhc
6bl
nunbnofg.mid".d erdc,rpsisc
TrNccr & Verd!, 20ot).ud
c.urenceof
{ecdi.dour lrachi
sqoesr
(ssPs).RESUTNANDDISC'IJSSION
we observ.d thai oniq-uhns ii
xin,b@cd
conmen ftnib ot 30 seD.m or pr,n60d sp,b.dr
o1 27 planrscie6 (33J*olgeD
consnftd r& deirtuib),
whi.n n
d.
high4rnc
everdeu@nrd turap€ sp.ci.s.
D!n'g
dresm
p€do4se
iidividurls riv,ns at rh. KocP $udy sihEas{db
of#rd! (}usr, sddsJp, *ocalp)3?
dfi.firgd@ olitrh s.d!
('u i@r!d.d inilc
30 g.n.m) w.€ idcnri{iedil ,it r..6
(46s orgeoen coisuncd for den finib), 22
cdqa
win\s.ds
lonserrhs oe cn
Eschtdl
$nprc conbioe!l ned (!
sEndirdDeviadod)
afoe (!
r.02)qus
ofinbr &rd
FisuE
l
shows rh. geminarionsre$
.ordiff{d
$b or *.ds.D
d@ and,(prM'r@
pdu..
multi sedcd.ndo.!qs (*id
n\eionb*
oIs.ds nududins lrcn oic 1orbE
pcGineb anit) Thn Eobsic?r
hit
dptrinswhy n
posibr.b
ob6in more cedrdg!rhri
the numberot
endo.dps rhar wasTt. erreft
row geftimriod tuorded ror con.cbdd
rh? lored smund suffrr.niion
eed pfdarion or amgus adrck, or weEfdirid
byrcr
ponindiod.ftey w
e not in ou sbrisricar snrysis. rh$e Hulrssho'
inr
n i. rrways 1 Fobl.m ro coledconftt
sds 6d
rh.!iderlu
rhey sho d onsimb tumtu
rrdi6 collece!djdrly
in rh.k
o6;;;::
lb)
K@d.riadadon
phnoton:e9€e3
AAA;;A
r
etu oc.rps sprr mt (!=71) E swllowed endocarps (n=37)r
endeaDs fiom 6uirs(n+3)
I ddoceps
spar out(nd5)
o
swslowed endocarps (n=31)!
endoca,Ffton
nuiis {n=20)figln
1'C.mindio
sllEgsfd s.ds
M^rcArcMq b}llu LcM
Axsn ckhins
is oorcr.rry
hdecrood, nh6 be..
prdposed ro Educe se.dnonaliry
L!rcqh rhed€*sa
ot fons'rar
k in rh"c4e opilhaus
ossniu'
l'-anb.R, 2oot).Mos pmbrbry, rhe
No
rr?e! ofcogod
sd-hindring Ge.d{e3rb*ins
d sed-rpiniig)
incl64
rhc rmge or@Fnuniri*
ror
se&
ro b. dcpGird in a nicGhabibrrhe orrd .dfplex idtracriotr
b.r*ei
biodcd &bioric
fabn
iniiiridg smimrid
strc.c*
dd
renciesj.quiar
rhrt rbe.fied
ol sch sed dispss.r sp.ci.s n cdi3idercd
$pdddy
toi.fb
ptdt speies(cwoo4
r93r). Tsrins rh. r,r. of 3.:nr
*dtow.d
or sendt
by om8-dms*s
beymdtu sop.
of
omg ftdi b f(mr
regenemrioh.loL\esabah\l,ildlftD.plfuolmdlo rhe(ocPG!{ch sish$ r\t
woutd also like ro rhmk rhesrM Fdctrr D.ptuo.
fdr
simrifrc
conebontion,L sh.em,
Rcdl.r|J.
s&h.rl,c
Kmgse,M schn$ui&i mdrhoiyfous
eviewas for6ei. n:.fnl
suppon
vs miv.d ftm
ApeDh.ut. Bush PalmyE, Lincohrrl.
Pnabugh zoor,Dkn.y
coisewarioDFuid, Au raliri
orssubn
Prcjec',Abrdm
Foundariod, lVrVW, Sh,ftdEdh
Fouodzriod, us Fish&
Mldrife
swie, wwF
(uK-usAHoll'd.
Mrlr$i!),
d other piva6$un.s.
Anci.naz- {2004). o6n3-trsd /poisa (srbih,
Md.$;)
IiEpftlriois .d n$i
ce@ihkturN0una ttutuku cr.!iu,
c_^. &Di. ondsdo*, oe3).
cndcpc\det.' Anunan Jak.,4l
aJk co
.y, K,R,(mr. Fi:ry sd
srnovcrrdilii,
B.oe3r). oQ4uk s
Ecddilp.eB
arratrjlr Ptriis. cotrd Gt). rh. a.oryrhr: n, bbks,
ard@a.fu''@n"ksue'ld
Giq4d,
N, Oeeo.scd3.miidoi!6od bt
d roEnhhEhr:
ac(,IDlrirysdy L'!bed, J.r.
(r00r),R.d.b
cd sDeiotrsdsP{3zi hEnab@t r'qnot ol
P n n d o t
4r,
22 t2)t t3q2o IP,!. crrbri
oee3).Ewdudo!4ed(dogi4linoltldoBd Pfuc
&cd dbFfu]'i'?n:4 Jw'rl ,l
krsbb4
M. (lt9]), Mderi4dn'4 sLdviry
*hdion. ltt o aact hvrd ot
Ibr4Jr,
cJ,cftk
& T.B.sdd (rdl).
scddiFdbyadlndFfu€@mm'ly
h
,r'. DjrtusFq
cmcrc@ rolhdr o/Rjbd, LD,
&r, M.ird. oeel o!.
w&4ttui|.. tu,tu ot||iaoN|.
vtu de cbc oItu tuM ctuD.
h!.i.t
^.&rlr.\!rnr,@x)1}^o!b{!td 3mj'dio'InlAq,DJ.wR.su{aM,
cl]F
i
l.nr.r- s..daw$d
onatuerwryUqra
ns.09rat Fx lcrdtua
ot fours@tin!@iLtlndi .ttun t4
wr&q Pr oeetTdedrInreslllincled nwjtt:tnaulj'. nuautua r*ta a w'.!!hu, r.w- cI cL.pDro & LJ.
cil!@! o99.l
s..ddirrl
byrM
o!ji{.'B
ta!?piL rd
nat oI Dapba!lvudabrrr.lll. ntl€nLoldidd
'.!gmdmdd$d.dd!0igll!,dsllod
k'|ogairfu'e'9:2,32x5'