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INTRODUCTION
The importance of primates as agents of seed dis-persal has been widely noted, especially for tropi-cal forests (Howe 1980; Estrada & Coastes-Estrada1984, 1986; Gautier-Hion et al. 1985) and sometemperate forests (Yumoto et al. 1998). Primateshave a larger body size and range over a greaterarea than birds, which are generally considered tobe effective agents of seed dispersal in the forests(Terborgh 1986). However, little is known about
how primates contribute to the movements andfate of seeds.
Interpretations of the significance of seed dis-persal for plant populations have been framed interms of three hypotheses: the escape hypothesis,the colonization hypothesis and the directed dis-persal hypothesis (Howe & Smallwood 1982). Totest the validity of these three hypotheses, onemust measure the dispersal distance from themother plants, the location of seed deposition, andthe survival rate of seeds and seedlings after dis-persal. Some measurements of the distances seedsare carried by animals have been made for dis-persal by synzoochory (diaspores carried delib-erately, mostly in the mouth) in ants (Beattie & Culver 1981; Higashi et al. 1989; Gómez &Espadaler 1998), scatterhoarding animals (Sork1984; Miyaki 1987; Miyaki & Kikuzawa 1988)
Ecological Research (1999) 14, 179–191
Estimation of the retention times and distances of seed dispersed by two monkey species, Alouatta seniculus
and Lagothrix lagotricha, in a Colombian forestTakakazu Yumoto,1* Koshin Kimura2† and Akisato Nishimura3‡
1Center for Ecological Research, Kyoto University, Otsu 520-2113, Japan, 2Faculty of Economics,Nagoya Gakuin University, Seto, Aichi 480-1214, Japan and 3Biological Laboratory, Doshisha
University, Kyo-tanabe, Kyoto 610-0331, Japan
Isolated-bout method to estimate the retention times and dispersal distances was applied to the seeddispersal by red howler monkeys (Alouatta seniculus) and Humboldt’s woolly monkeys (Lagothrixlagotricha) in a lowland tropical forest at La Macarena, on the border of the Macarena and TiniguaNational Parks, the Department of Meta, Colombia. Continuous observations were made on thefeeding and ranging behavior of well-habituated troops of howler monkeys and woolly monkeys aswell as continuous collection of monkeys’ feces. We selected out the ‘isolated-bout’ as a feeding bouton the specific species that was only once recorded within 48 h before the seeds of that speciesappeared in the feces of monkeys. In that case, the seeds were strongly suggested to come from thatisolated bout. Then retention times, route seed dispersal distances and direct seed dispersal distanceswere estimated. Howler monkeys, which are regarded as generalist herbivores, showed longer reten-tion times and dispersal distances along monkeys’ route than did woolly monkeys, which are spe-cialist frugivores. However, the direct distances that seeds were carried from the mother tree werenot significantly greater for howler monkeys than for woolly monkeys. This shows that both reten-tion time and movement patterns by the monkeys, especially the total ranging area, influence thedirect distance that seeds are carried from the mother tree.
Key words: Alouatta seniculus; Colombia; isolated-bout method; Lagothrix lagotricha; seed dispersal;tropical forest.
*Email: <[email protected]>†Email: <[email protected]>‡Email: <[email protected]>Received 13 August 1998.Accepted 5 January 1999.
and monkeys using cheek pouches (Yumoto et al.1998); however, it is still very difficult to mea-sure these parameters in the field for seeds dis-persed by epizoochory (diaspores carried on the outside of animals by adhesion) or endo-zoochory (diaspores carried inside the animals).The best method is direct observation in the field of well-habituated animals, which have not been artificially fed, so that researchers canfollow the whole process from intake of seeds todispersal.
Recently, Julliot (1996) succeeded in directlyestimating retention times and dispersal distancesfor seeds dispersed by well-habituated red howlermonkeys (Alouatta seniculus) in French Guiana, bythe isolated-bout method’. In the isolated-boutmethod, continuous observations are made on thefeeding and ranging behaviour of well-habituatedtroops of animals as well as continuous collectionof animals’ feces. The seed source is estimated tothe one only when the feeding bout of that speciesis isolated (i.e. only once within a period longerthan estimated maximum retention time beforethe seeds of the species are found in the feces ofanimals). Then retention times, route seed disper-sal distances and direct seed dispersal distances are obtained, and the maximum retention timepresumed in the procedure is confirmed. Yumoto(1999) applied the same method to a terrestrialbird, Mitu salvini (Cracidae), and obtained theretention times and dispersal distances of seedscarried not only by endozoochory but also by epizoochory.
Monkeys of the Alouattinae, including Alouatta,and of the Atelinae including Lagostrix, Atheles andBrachyteles, consume a lot of fruits, and have beenregarded as major seed dispersers in the Neotrop-ics (Terborgh 1986). However, Alouatta dependsmuch more on leaves, whereas Lagostrix and Athelesfeed largely on fruits; their digestive organs arethus very different (Hladik 1967; Cramer 1968)and their digestive strategies are also different(Milton 1979, 1981, 1984; Milton & Nessimian1984; Stevenson et al. 1994). In this study, wecompare the retention times and the dispersal distances between two sympatric species of mon-keys, red howler monkeys (Alouatta seniculus) andHumboldt’s woolly monkeys (Lagothrix lagotricha),based on observations of well-habituated groups atLa Macarena, Colombia.
180 T. Yumoto et al.
METHODS
Study site
The study site at La Macarena (2°40¢N, 74°10¢W,350 m a.s.l.) is situated in a lowland tropical foreston the border of the Macarena and TiniguaNational Parks, the Department of Meta, Colom-bia. It lies on the bank of the Rio Duda, a tribu-tary of the Rio Guayavero. The site was establishedfor research on primates by Kosei Izawa in 1986,and is now known as CIEM (Centro de Investiga-ciones Ecológicas de La Macarena; Nishimura et al.1995). Seven species of cebid monkeys live sym-patrically in this area: Humboldt’s woolly monkey(Lagothrix lagotricha), black-capped capuchin(Cebus apella), long-haired spider monkey (Atelesbelzebuth), red howler monkey (Alouatta seniculus),common squirrel monkey (Saimiri sciureus), duskytiti (Callicebus moloch) and owl monkey (Aotustrivirgatus). Since 1986, several troops of monkeyshave been inhabitated without artificial feeding.Troops of red howler monkeys and Humboldt’swoolly monkeys are particularly well-habituated,and continuing socio-ecological research on themis in progress (Izawa 1988; Nishimura 1988,1990, 1994; Izawa & Lozano 1989, 1991, 1992,1994; Kimura 1992; Stevenson 1992; Stevenson et al. 1994).
The topography of the area is undulating, withrolling hills dissected by small brooks and with flooded areas near river margins. The vege-tation has been grouped into four formation types (Hirabuki 1990): (i) mature terra firme forest,localized on hill ridges with 20–25 m high trees and a continuous canopy with emergent trees reaching a maximum height of 30 m; (ii)open degraded forest, localized on erosion fronts,small valleys and brooks, and composed mostly of vines, lianas, bamboo and a few trees between20 and 25 m in height with a discontinuouscanopy and thick understory; (iii) seasonallyflooded varzea forest, in the flood plain and char-acterized by a discontinuous canopy dominated byInga spp. (Leguminosae), Ficus spp. and Cecropiaspp. (Moraceae) with an understory mostly of Heli-conia spp. (Musaceae); and (iv) riparian successionalvegetation, localized on recently formed sandshores and consisting mostly of graminoides, Tessaria integrifolia (Compositae) and youngCecropia trees.
The study area is characterized by highly sea-sonal rainfall. The dry period lasts from Decem-ber to March and the rest of the year is rainy (> 100 mm per month) (Kimura et al. 1994). Thestudy was conducted in the dry period in Febru-ary and March 1993.
Monkey troops and feeding observations
Observations on seed dispersal were carried out for 9 days between 22 February and 5 March forhowler monkeys, and for 12 days between 8 and 16March for woolly monkeys. We followed the well-habituated MN-2 troop of howler monkeys, andCR-1 troop of woolly monkeys, from sleeping siteto sleeping site, from approximately 06:00–17:00 h. The number of individuals was 14 inMN-2 troop and 24 in CR-1 troop. We observedthe process of seed dispersal from eating fruits atthe mother trees to excretion of seeds in the feces. The total observation time was 89 h 42 minfor howler monkeys and 123 h 32 min for woollymonkeys. The route of travel on each day wasrecorded on a map. The daily travel distance wascalculated from sleeping site to sleeping site bytracing the troops’ route on the map. The areaenclosing all of the routes taken by the monkeysduring the observation period is referred to as theranging area.
Times and locations of fruit-eating and defeca-tion were recorded. Feeding bouts were definedand timed from the first observation of a monkeyin the troop beginning to eat a particular fruit (orleaf, insect) on a tree, to the last observation of amonkey in the troop eating that kind of fruit (orleaf, insect) from the same tree. We collected asmany fecal samples as possible and washed themin sieves to identify the seeds contained withinthem.
Location of deposition of feces was categorizedinto ‘under canopy’, ‘gap’, ‘bamboo/bush’ and‘brook’. The category ‘under canopy’ is subdividedinto ‘feeding trees’ (where monkeys were observedto eat fruits/leaves of a canopy tree at that time orjust before defecation) and ‘others’. ‘Gap’ wasdefined as a location where there were no over-hanging canopy trees nor dense cover of terrestrialvegetation.
For the fruits eaten by howling monkeys and woolly monkeys, the size and weight of the
heaviest fruit sample obtained, the number ofseeds contained in the fruit, sugar concentration(weight/weight, estimated by refractometer,Bellingham & Stanley Ltd, BS-R70, England), andthe size and weight of seeds were measured.
Estimation of retention times and dispersal distances
We estimated the sources of seeds found in fecalsamples using an isolated-bout method (Julliot1996). Bouts of fruit consumption were used in theanalysis only if they were isolated by at least 48 hfrom any other bout of feeding on fruit of the samespecies. We omitted any data for the estimation ofseed sources on the small-sized seeds, such as Ficusspp., Cecropia spp., which have been suggested to have longer retention times, sometimes up to100 h (Estrada & Coastes-Estrada 1986). For thecalculation of retention time, the mid-point offeeding time was taken as the mid-point betweenthe beginning and the end of a feeding bout. Thedifference between the mid-point of feeding timefor an isolated bout and the appearance of seeds infecal samples was taken as the retention time forthe seeds. Dispersal distances were estimated bothfrom the number of paces along the monkeys’route (the route distance), and by measuring theshortest distance between ingestion and depositionlocations on the map (the direct distance).
RESULTS
Daily travel distances and ranging area
The daily distance traveled by the howler troopranged from 560 m to 1660 m (mean = 980 m, SD = 410 m, n = 9), and that of the woolly troopranged from 830 m to 2380 m (mean = 1640 m,SD = 610 m, n = 12). The daily travel distances ofwoolly monkeys were significantly greater thanthose of howler monkeys (Wilcoxon’s rank sumtest, two-tailed, N1 = 9, N2 = 12, S = 61, P <0.05).
The ranging areas of howler monkeys andwoolly monkeys during the observation period was about 17.2 ha and 69.8 ha, respectively. Bothtroops mainly used mature forest on hill ridges andopen degraded forest, and seldom visited floodedforest or riparian forest during this period.
Seed dispersal by monkeys in Colombia 181
Feeding bouts and dispersed species
During the observation period, 118 bouts offeeding were observed for howler monkeys and 180 bouts for woolly monkeys. Table 1 shows thenumber of bouts and time spent feeding on fruits,leaves and insects by howler monkeys and woollymonkeys. Fruit-feeding accounted for 72.9% offeeding bouts for howler monkeys, and 86.7% forwoolly monkeys. For leaf-feeding, the values were27.4% and 8.9%, respectively. On average, howlermonkeys ate 5.22 species of fruits (SD = 1.39,range: 3–7, n = 9) in 9.56 bouts (SD = 3.32, range:5–14, n = 9) per day, while woolly monkeys ate8.08 species of fruits (SD = 3.68, range: 5–18, n =12) in 13.17 bouts (SD = 3.83, range: 9–20, n =12) per day. The number of daily fruit-feedingbouts was slightly higher for woolly monkeys thanfor howler monkeys (Wilcoxon’s rank sum test,two-tailed, N1 = 9, N2 = 12, S = 68, P < 0.05), andwoolly monkeys also ate a greater number of fruitspecies per day than howler monkeys (Wilcoxon’srank sum test, two-tailed, N1 = 9, N2 = 12, S = 73,P < 0.05). Howler monkeys spent 31.0% of allfeeding time eating leaves of the Leguminosae andBignoniaceae. Woolly monkeys spent only 4.4% oftotal feeding time on leaves. Almost all leaveseaten by Humboldt’s woolly monkeys were youngones of Dalbergia sp. (Leguminosae) and Himanan-thus articulatus (Apocynaceae).
182 T. Yumoto et al.
Insect-feeding by howler monkeys was notobserved, but 4.4% of feeding bouts by woollymonkeys involved insect-feeding. Woolly monkeysspent 14.1% of all feeding time on insects, espe-cially ants. They ate Crematogaster spp., which nestin dried twigs, and Eciton sp., which shelter tem-porarily in holes of trees. A single feeding bout wasobserved in which a female woolly monkey ate alizard of approximately 15 cm length.
The length of fruit-feeding bouts of howlermonkeys (10.20 min ± 11.28, n = 85) was greaterthan that of woolly monkeys (7.72 min ± 8.77, n =156) (t-test: t = 1.87, n = 238, P < 0.05), and thefruit menu of the two species differed (Table 2).Howler monkeys spent 46.1% of feeding time onsyconia of Ficus spp., while woolly monkeys werenot observed to eat syconia of Ficus spp. during theobservation period although a very small numberof fecal droppings contained the seeds of Ficus.Apart from Ficus spp., all species that wereobserved to be eaten by howler monkeys were alsoeaten by woolly monkeys. By contrast, fruits of sixspecies eaten by woolly monkeys were not observedto be eaten by howler monkeys.
Seeds of two species, Protium sagotianum andProtium robustum were not found in the feces ofhowler monkeys, although the fruits were observedto be eaten. Among plant species of which fruitswere observed to be eaten by woolly monkeys, seedsof Eugenia cribata, Perebea mollis and Pseudolmedialaevigata were not found in the feces. Table 3 showsthe number of fecal droppings that contained seeds,the total number of seeds found in feces and theaverage number of seeds per dropping for howlermonkeys and woolly monkeys for each plantspecies. Seeds of Ficus spp. were found in more than93% of all the feces of howler monkeys collected.Most seeds were whole, indicating that both speciesof monkeys seldom cracked them between theirteeth. Only young seeds of Pseudolmedia spp. wereobserved to be cracked by howler monkeys. One ortwo cracked seeds of Pseudolmedia spp. were foundin 44% of all the collected fecal droppings of redhowler monkeys. Monkeys always ate fruits on thetrees and never on the ground during the observa-tion period.
Figure 1(a, b) shows how many species of seedswere found in each fecal dropping of howlermonkeys and woolly monkeys, respectively. Forhowler monkeys, seeds of 3.04 species (SD = 1.11,
Table 1 Number and total duration of feeding boutsof howler monkeys and woolly monkeys
Howler monkeys Woolly monkeys
Fruit-feedingNo. bouts 85 (72.6%) 156 (86.7%)Time (min) 863 (69.0%) 1165 (81.5%)
Leaf-feedingNo. bouts 32 (27.4%) 16 (8.9%)Time (min) 388 (31.0%) 63 (4.4%)
Insect-feedingNo. bouts 0 8 (4.4%)Time (min) 0 201 (14.1%)
TotalNo. bouts 117 180Time (min) 1251 1429
ObservationTime (h, min) 89, 42 123, 32
Seed dispersal by monkeys in Colombia 183
Tab
le 2
Tota
l fe
edin
g ti
me
and
bout
len
gths
for
how
ler
mon
keys
and
woo
lly
mon
keys
fee
ding
on
diff
eren
t fr
uit
spec
ies
How
ler
mon
keys
Woo
lly
mon
keys
Feed
ing
Mea
n ti
me
Max
imum
Fe
edin
gM
ean
tim
eM
axim
um
tim
e N
o.of
bou
tti
me
of
tim
eN
o.of
bou
t ti
me
of
Spec
ies
(min
)%
bout
s%
(min
)SD
bout
(m
in)
(min
)%
bout
s%
(min
)SD
bout
(m
in)
Cla
risi
a ra
cem
osa
00
00
0—
065
5.6
53.
213
.08.
222
Eug
enia
cri
bata
00
00
0—
011
1.0
42.
62.
81.
54
Viro
la fl
exuo
sa0
00
00
—0
796.
811
7.1
7.0
12.1
43C
asti
lla
ulei
526.
03
3.5
14.7
8.6
2425
321
.728
17.9
9.0
11.9
54P
roti
um s
agot
ianu
m3
0.3
22.
41.
50.
72
665.
717
10.9
3.9
3.2
10St
rych
nos
schu
ltes
iana
00
00
0—
055
4.7
31.
918
.313
.734
Per
ebea
mol
lis
252.
94
4.7
6.3
5.1
1233
2.8
21.
316
.517
.729
Pou
roum
a pe
tiol
ulat
a0
00
00
—0
837.
19
5.8
8.8
8.2
23P
ouro
uma
bico
lor
111
12.9
1517
.67.
44.
215
494.
25
3.2
9.8
13.7
34C
repi
dosp
erm
um r
hoif
oliu
m0
00
00
—0
129
11.1
1610
.38.
17.
929
Pse
udol
med
ia l
aevi
gata
161.
94
4.7
4.0
0.8
512
1.0
31.
94.
02.
66
Pro
tium
rob
ustu
m2
0.2
22.
41.
00.
01
776.
610
6.4
7.7
6.9
19C
occo
loba
den
sifr
ons
576.
66
7.1
9.5
5.0
1813
1.1
21.
36.
56.
411
Per
ebea
xan
thoc
hym
a11
1.3
22.
45.
50.
76
131.
14
2.6
3.3
3.2
8P
seud
olm
edia
lae
vis
161
18.7
1821
.28.
97.
832
222
19.1
3321
.26.
76.
327
Cec
ropi
asp
.27
3.1
78.
53.
82.
68
70.
64
2.6
1.8
1.5
4F
icus
spp
.39
846
.122
25.9
18.1
17.6
700
00
00
—0
Tota
l86
385
1165
156
184 T. Yumoto et al.
Tab
le 3
Seed
con
tent
of
feca
l dr
oppi
ngs
in r
elat
ion
to f
eedi
ng t
ime
for
each
foo
d sp
ecie
s
How
ler
mon
keys
Woo
lly
mon
keys
Feed
ing
No.
fec
al
No.
see
dsFe
edin
g N
o. f
ecal
N
o. s
eeds
tim
edr
oppi
ngs
in f
ecal
M
ean
tim
edr
oppi
ngs
in f
ecal
M
ean
Spec
ies
(min
)co
ntai
ning
see
ds%
drop
ping
snu
mbe
r(m
in)
cont
aini
ng s
eeds
%dr
oppi
ngs
num
ber
Cla
risi
a ra
cem
osa
00
00
065
52.
86
1.20
Eug
enia
cri
bata
00
00
011
00
00
Viro
la fl
exuo
sa0
00
00
7918
10.2
331.
83C
asti
lla
ulei
5240
26.1
281
7.03
253
3922
.212
93.
31P
roti
um s
agot
ianu
m3
00
00
6643
24.4
132
3.07
Stry
chno
s sc
hult
esia
na0
00
00
555
2.8
142.
80P
ereb
ea m
olli
s25
1811
.742
2.33
330
00
0P
ouro
uma
peti
olul
ata
00
00
083
4324
.413
83.
21P
ouro
uma
bico
lor
111
110
71.9
871
7.92
4910
6.2
373.
36C
repi
dosp
erm
um r
hoif
oliu
m0
00
00
129
158.
536
2.40
Pse
udol
med
ia l
aevi
gata
166
4.3
91.
5012
00
00
Pro
tium
rob
ustu
m2
00
00
7724
13.6
512.
13C
occo
loba
den
sifr
ons
5746
32.4
191
4.24
131
0.6
11.
00P
ereb
ea x
anth
ochy
ma
1137
24.2
144
3.89
1310
5.7
333.
30P
seud
olm
edia
lae
vis
161
95.
926
2.89
222
6134
.627
34.
48C
ecro
pia
sp.
2766
43.1
6843
103.
687
169.
138
624
.13
Fic
us s
pp.
398
143
93.5
7046
749
2.77
04
2.3
9223
.00
Tota
l86
315
378
874
1165
176
1361
n = 153) were found in a fecal dropping on average.For woolly monkeys, the mode of species numberwas 1, and the average was 1.78 species (SD = 0.98,n = 176). The number of species found in a fecaldropping of howler monkeys was significantlygreater than that for woolly monkeys (t-test, t =10.93, n = 327, P < 0.005).
Characteristics of fruits and diaspores consumedby the monkeys are shown in Table 4. Sizes of fruitseaten ranged from the smallest Pseudolmedia laevis(12.7 mm in length, 0.9 g in wet weight) to thelargest Strychnos schultesiana (60.2 mm in length,135.6 g in wet weight). The largest seed was thatof Clarisia racemosa. The larger-sized seeds, C. race-mosa and Virola flexuosa were excreted only bywoolly monkeys. All fruits consumed by bothspecies of monkeys were very sweet, except for
those of C. racemosa which contained no sugar, butseemed to be rich in lipids.
Retention time and dispersal distance
The estimated retention times and dispersal dis-tances based on combined data during the obser-vation period are shown in Tables 5 and 6 forhowler monkeys and woolly monkeys, respectively.Castilla ulei was the only plant species for whichdata were obtained for both howler monkeys andwoolly monkeys. For this species the retentiontime was significantly longer when dispersed byhowler monkeys (t-test, t = 5.11, n = 323, P <0.005), and the same tendencies were detected forthe route distance (t = 3.44, P < 0.005) and thedirect distance (t = 2.09, 0.01 < P < 0.025). Basedon the average value for each plant species, theretention times of howler monkeys were signifi-cantly longer than those of woolly monkeys(Wilcoxon’s rank sum test, two-tailed, N1 = 5, N2 = 8, S = 15, P < 0.025). The route distances dispersed by howler monkeys were significantlygreater than those by woolly monkeys (Wilcoxon’srank sum test, two-tailed, N1 = 5, N2 = 8, S = 23,P < 0.05), however, there was no significant differ-ence between the direct distances dispersed byhowler and woolly monkeys (S = 40.5).
Figures 2(a, b) and 3(a, b) show the relationshipsbetween retention times and dispersal distances ofhowler monkeys and woolly monkeys, respectively.For howler monkeys, the route distance leveled off,and the direct distance decreased when the reten-tion times exceeded 20 h. For woolly monkeys,both the route and direct distances peaked whenthe retention time was 6 h and increased againwhen the retention times exceeded 14 h. Seeds thatwere retained for more than 14 h during sleepingtime were excreted in the morning after monkeyshad eaten fruits in the late afternoon of the previ-ous day, and almost all seeds seemed to be excretedwithin 10 h before sleeping; so that, it is assumedthat the data corresponding to the retention timesbetween 10 h and 14 h were not available.
Location of deposition
Locations of seeds dispersed by howler monkeysand woolly monkeys are shown in Table 7. Forhowler monkeys, only 5.9% of seeds were dis-
Seed dispersal by monkeys in Colombia 185
Fig. 1. Number of seed species that were found ineach fecal dropping of (a) red howler monkeys (Alouattaseniculus) and (b) Humboldt’s woolly monkeys(Lagothrix lagotricha).
186 T. Yumoto et al.
Tab
le 4
Col
or,
size
and
wet
wei
ght
of a
fru
it,
wet
wei
ght
of t
he o
uter
par
t an
d th
e ed
ible
par
t, s
ugar
con
cent
rati
on (
wei
ght/
wei
ght)
, nu
mbe
r of
dia
spor
espe
r fr
uit,
and
siz
es a
nd w
et w
eigh
t of
dia
spor
e fo
r ea
ch p
lant
spe
cies
con
sum
ed b
y m
onke
ys
Frui
tO
uter
par
tE
dibl
e pa
rtD
iasp
ore
Wet
W
etW
etN
o.W
etSi
zew
eigh
tw
eigh
tw
eigh
tSu
gar
dias
pore
s/Si
zew
eigh
tSp
ecie
sFa
mil
yC
olor
(mm
¥m
m¥
mm
)(g
)(g
)(g
)(%
)fr
uit
(mm
¥m
m¥
mm
)(g
)
Cla
risi
a ra
cem
osa
Mor
acea
eO
rang
e22
.0¥
22.0
¥31
.08.
6—
4.3
181
15.0
¥14
.8¥
21.3
4.32
Eug
enia
cri
bata
Myr
tace
aeR
ed31
.0¥
37.4
¥41
.224
.4—
22.6
81
14.2
¥14
.2¥
10.6
1.82
Viro
la fl
exuo
saM
yris
tica
ceae
Gre
en20
.7¥
20.7
¥21
.64.
42.
50.
4—
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Seed dispersal by monkeys in Colombia 187
Fig. 2. Relationship between retention time and (a)route dispersal distance, and (b) direct dispersal dis-tance of red howler monkeys (Alouatta seniculus).
Table 5 Estimated retention times and dispersal distances via fecal droppings of howler monkeys
Retention time (h) Route distance (m) Direct distance (m)Species n Mean SD Maximum Mean SD Maximum Mean SD Maximum
Castilla ulei 298 19.1 4.6 41.2 719 434 1875 347 183 575Perebea mollis 28 18.8 2.4 20.8 858 189 1019 218 82 288Pourouma bicolor 198 21.3 2.4 32.0 1114 310 1630 440 179 637Coccoloba densifrons 118 20.0 2.1 23.3 819 375 1395 231 96 365Perebea xanthochyma 72 19.7 6.8 41.4 562 258 1000 310 62 375Pseudolmedia laevis 3 19.1 0.9 19.6 1000 444 1256 354 199 469
Dispersal distances are shown in the route and the direct distances.
Fig. 3. Relationship between retention time and (a)route dispersal distance, and (b) direct dispersal distanceof Humboldt’s woolly monkeys (Lagothrix lagotricha).
persed in ‘gap’ where no canopy tree was foundnearby nor dense terrestrial vegetation covered,and 41.2% of seeds were found under ‘feedingtrees’ where monkeys were observed to eatfruits/leaves at that time or just before defecation.The howler monkeys rested for long periods in thefeeding trees after feeding, and defecation was synchronized, with all individuals in the troopsexcreting within a short period. In contrast, forwoolly monkeys 25% of seeds were dispersed in‘gap’. This difference in the locations of seed dispersal between howler monkeys and woollymonkeys was significant (c2-test, n = 4, c2 =89.46, P < 0.005).
DISCUSSION
Retention time in the guts of folivorousand frugivorous primates
Red howler monkeys and Humboldt’s woollymonkeys differ in the basic composition of theirdiets. Howler monkeys are regarded as the mostfolivorous of the New World primates (Milton1979; Eisenberg 1989; Julliot & Sabatier 1993),whereas woolly monkeys are mostly frugivores
188 T. Yumoto et al.
(Kavanagh & Dresdale 1975; Delfer 1987; Steven-son et al. 1994), although they also take some ver-tebrate and invertebrate prey (Milton & Nessimian1984; Stevenson 1992). The digestive tract ofhowler monkeys, although capacious, lacks thespecializations found in the guts of Old Worldleaf-eating primates, such as extensive enlarge-ment and sacculation (Fooden 1964; Hladik1967). The howler monkey’s stomach is simpleand not remarkably large (Cramer 1968), and thececum and colon are not outstanding in size, especially when compared with those of indriids(Hladik 1967). Howler monkeys should, therefore,be less efficient than specialized Old World leaf-eaters at digesting foods high in fiber (Milton1979).
Using an artificial dye, Estrada and Coates-Estrada (1986) showed that captive howlermonkeys fed a diet of fruits and leaves had foodpassage rates averaging about 18 h (range 16–25 h). Using a method similar to the current study,Julliot (1996) showed the retention time of seedsfrom 17.5 to over 62 h for red howler monkeys intheir natural habitat. Milton (1981) compared thepassage time of caged mantled howler monkeys(Alouatta palliata), black-handed spider monkeys(Ateles geoffroyi) and black spider monkeys (Ateles
Table 6 Estimated retention times and dispersal distances via fecal droppings of woolly monkeys
Retention time (h) Route distance (m) Direct distance (m)Species n Mean SD Maximum Mean SD Maximum Mean SD Maximum
Clarisia racemosa 2 2.0 0 2.0 126 0 126 126 0 126Virola flexuosa 26 6.1 4.5 17.2 677 301 1681 435 177 1106Strychnos schultesiana 14 4.1 2.2 9.2 442 84 701 349 15 362Castilla ulei 27 14.5 2.6 16.2 426 381 1034 271 161 644Pourouma petiolulata 29 4.6 1.1 7.2 760 191 1273 454 101 731
Dispersal distances are shown in the route and the direct distances.
Table 7 Locations of seed deposition by howler monkeys and woolly monkeys
Under canopyFeeding trees Others Gap Bamboo/Bush Brook Sum
Howler monkeys 63 (41.2%) 24 (15.7%) 9 (5.9%) 27 (17.6%) 30 (19.6%) 153Woolly monkeys 23 (13.1%) 83 (47.2%) 44 (25.0%) 21 (11.9%) 5 (2.8%) 176
Locations are categorized into ‘under canopy’, ‘gap’, ‘bamboo/bush’, and ‘brook’. The category ‘under canopy’ is subdividedinto ‘feeding trees’ (where monkeys were observed to eat fruits/leaves at that time or just before defecation) and ‘others’.
paniscus) using colored markers in the food. Sheshowed that the passage times for food in howlermonkeys and spider monkeys were 20.4 ± 3.50 hand 4.38 ± 1.53 h, respectively. Spider monkeysare regarded as frugivores and committed to astrategy of rapid food passage (Milton 1981). Evi-dently they can process a considerable volume offruit which is generally rich in non-structural car-bohydrates but low in protein. In this study, weobtained the retention times of 18.8–21.3 h for redhowler monkeys based on the data of six species ofseeds, and 2.0–6.1 h (with an exceptional value of14.5 h) for Humboldt’s woolly monkeys. Althoughretention time can never be certain without‘marking’ the seeds, the howler monkeys and thewoolly monkeys in this study showed very similarretention times to those reported for the howlermonkeys and spider monkeys by Milton (1981),respectively.
Dispersal distances by narrow- and wide-ranging monkeys
The home range of MN-1 troop of red howlermonkeys was about 25 ha in 1986 (Izawa &Nishimura 1988), and the size and location of fivetroops of red howler monkeys have shown no greatchanges since then. The home range of CR-1 troopof Humboldt’s woolly monkey troops was 260 hafor CR-1 in 1993. Thus, the troop of Humboldt’swoolly monkeys uses a much larger area than thoseof red howler monkeys. The ranging area duringthe study period represented 68.8% (17.2 ha) ofthe howler monkeys troop’s total range recorded sofar, and 26.8% (69.8 ha) of that of the woollymonkeys. These differences in ranging areabetween howler monkeys and woolly monkeysapparently affected the direct dispersal distances,because the upper limit of the direct dispersal dis-tances by howler monkeys was no more thanapproximately 650 m which was the widest lengthin the ranging area of the troop observed duringthis period, and because the fast travel speed ofwoolly monkeys seems not to be able to compen-sate the very fast passage speed of seeds in theintestine for the contribution of seed dispersal dis-tances. In spite of a longer retention time in thegut, seeds eaten by howler monkeys were dispersedover a smaller area than those eaten by woollymonkeys.
Can monkeys be effective seed dispersers?
Concerning the direct dispersal distances, therewas no significant difference between seeds carriedby howler monkeys and those by woolly monkeys,and the dispersal distances were long enough toescape the effect of the mother trees. As for theeffect on dispersal distances, which is one of themost important for colonization and escape frommother trees, these two species of monkeys wouldbe the same.
Tokuda (1988) found the distance between indi-vidual red howler monkeys during feeding andresting time was less than that for Humboldt’swoolly monkeys. From our observations, redhowler monkeys showed a remarkable degree ofaggregation, with many individuals simultane-ously using the same food patch, whereas Hum-boldt’s woolly monkeys tended to use small foodpatches individually. The howler monkeys had a tendency to excrete in a particular place. Asreported in a previous study (Tokuda 1988),during their feeding periods the monkeys come inturn to discharge from a specific branch of a treeand the feces drop to the ground below. Conse-quently, seeds are dispersed under feeding trees ofhowler monkeys after the feeding. These tenden-cies lead to the directed dispersal, but it is not onewhich favors the plants. From our observations, itappeared that many feces were deposited underlarge trees of Ficus sp., which would not be suit-able for the recruitment of seedlings.
By contrast, Humboldt’s woolly monkeysshowed some tendency of directed dispersal intogaps, which provide good condition for plants,because the survival ratio of both seeds andseedlings would be high. Humboldt’s woollymonkeys can, therefore, be regarded as better seeddispersers than red howler monkeys, as theycarried seeds as far as howler monkeys did, and dis-persed them in gaps although retention times weremuch shorter.
At La Macarena, mammal fauna is extremelyrich. For most fruits consumed by monkeys duringobservation periods, however, monkeys (includingblack-capped capuchins, long-haired spider mon-keys and common squirrel monkeys) were themain consumers. Most of the fruits mentioned inthis paper were consumed and dispersed only bymonkeys. All of the available data that were
Seed dispersal by monkeys in Colombia 189
obtained during a 10-year study in La Macarenasuggest that monkeys are the most important dis-perser for these plants. As for Ficus species, notonly monkeys, but also coati (Nasua nasua), kinka-jou (Potos flavus), collared peccary (Tayassu tajacu)and common tapir (Tapirus terrestris) and somebirds, including Salvin’s curassows (Mitu salvini),were observed to eat the fruits, either from the treeor fallen fruits from the ground. Some of the smallcarnivores were observed to excrete seeds intact intheir feces, but Salvin’s curassows are mainly seedpredators (Yumoto 1999). The relative importanceof monkeys as seed dispersers seems to beextremely high in the forest at La Macarenabecause of the combination of the largest biomassof monkeys, and their dependency on fruits.
ACKNOWLEDGEMENTS
We are greatly indebted to Prof. Carlos Mejia (Uni-versidad de Los Andes) for kind permission forwork at CIEM and to Prof. Kosei Izawa (MiyagiUniversity of Education) for his kind arrangementand guidance of the fieldwork. We appreciate DrCeser Barbosa (UNIFEM-INDERENA) for infor-mation on the flora in the study site. We also thankMr Henry Lozano (CIEM project) for help withfieldwork. We thank Dr David A. Hill and DrHiroyuki Takahashi for their critical reading.Fieldwork was supported by a Japan Ministry ofEducation, Science and Culture (Monbusho)Grant-in-Aid for International Scientific ResearchProgram: Field Research, FY1990–92 (Leader: K.Izawa, 02041009) ‘Field studies on the chrono-logical social structure of New World monkeys, thedynamics of Neotropical forests as their habitats’.
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