Seed dispersal patterns produced by white-faced

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Journal of
Ecology 2003
91, 677 – 685
Seed dispersal patterns produced by white-faced monkeys:
implications for the dispersal limitation of neotropical
tree species
Blackwell Publishing Ltd.
Departamento de Ecología Evolutiva, Universidad Nacional Autónoma de México, Apartado 70–275, México
DF 04510, México, †Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Republic of Panama,
‡Department of Botany, University of Georgia, Athens, GA 30602, USA, §Department of Botany, The Field Museum,
Chicago IL 60605, USA, and ¶Department of Plant Biology, University of Illinois, Champaign-Urbana, IL 61801,
1 Primate frugivores are important seed dispersers for a large fraction of tree species in
many tropical forests. The movement, diet preferences and defecation patterns produced by primates may therefore strongly influence seed dispersion patterns and seedling recruitment success. Here we examine the pattern of seed dispersal generated by
white-faced monkeys (Cebus capucinus) in relation to adult tree distribution in the
50-ha plot on Barro Colorado Island (BCI), Panamá.
2 Diet breadth of Cebus was remarkably wide. Over four months they consumed fruits
of 95 out of an estimated 240 species available. Seeds of 67 species passed intact through
the gut and 28 were spat out.
3 Dispersal effectiveness of Cebus was also high. Two Cebus groups on average
spent < 10 min feeding in individual trees, had large home ranges (> 150 ha), travelled
1–3 km day−1 and defecated seeds in small clumps throughout the day.
4 Mean dispersal distance of ingested seeds was 216 m (range 20–844 m), with the
highest probability of dispersal 100–200 m from the parent plant. For six of nine species
studied, the distance between defecation sites and nearest conspecific adults of seeds in
faeces was not significantly different from random expectations.
5 The scattered dispersal pattern produced by Cebus suggests that this species contributes relatively little to dispersal limitation (sensu Nathan & Muller-Landau 2000) compared to other dispersers in the community. Long-distance dispersal by Cebus resulted
in substantial movement of seeds in and out of the 50 ha plot, and suggests that inverse
modelling procedures to estimate dispersal functions from trap data may not adequately describe dispersal patterns generated by this primate.
Key-words: Cebus capucinus, dispersal effectiveness, primate dispersal, recruitment
limitation, seed dispersal.
Journal of Ecology (2003) 91, 677–685
Effective seed dispersal is critical to successful recruitment in tropical forests. Dispersal provides the opportunity to escape the neighbourhood of the parent
plant, and allows seeds to colonize new and potentially
© 2003 British
Ecological Society
*Correspondence: Elisabet Wehncke, Laboratorio de Interacciones Planta-Animal, Departamento de Ecología Evolutiva,
Apartado 70–275, Ciudad Universitaria, Circuito Exterior,
04510 México DF, México (fax +52 5 56161976, e-mail
[email protected]).
more favourable microsites for seedling establishment
(Howe & Smallwood 1982). Neighbourhood effects on
recruitment result from the increased risk of mortality
to seeds or seedlings from a range of sources including
pathogens (Burdon & Chilvers 1982; Augspurger 1983,
1984; Gilbert & De Steven 1996; Dalling et al. 1998;
Packer & Clay 2000), seed predators (Howe & Primack
1975; Janzen et al. 1976; Wright 1983; Clark & Clark 1984;
Ramírez & Arroyo 1987; Forget 1993) and herbivores
(Condit et al. 1992; Barone 1996; Coley & Barone 1996).
In one community, these mortality agents have been
shown collectively to exert negative density-dependent
E. V. Wehncke
et al.
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
effects on seedling recruitment for every one of 53 species examined in detail (Harms et al. 2000). Microsite
limitation is likely to be particularly important for
small-seeded and light-demanding species (Dalling &
Hubbell 2002), but may also be significant for larger
seeded, shade-tolerant species with topographically
determined habitat requirements (Webb & Peart 2000;
Harms et al. 2001).
Dispersal success, however, is constrained by the
level of resources available for investment in reproduction, and by the effectiveness of seed dispersal agents.
At the community level, dispersal success, measured as
the proportion of potential recruitment sites receiving
seeds of a given species, has been shown to be extremely
low for most species (Hubbell et al. 1999). As a consequence, dispersal limitation may be a potentially
important mechanism for the maintenance of diversity
by greatly slowing the local extinction rate of competitively inferior species (Tilman 1994; Hurtt & Pacala
1995; Wright 2002; but see Webb & Peart 2001).
In tropical forests, up to 90% of trees and understorey shrubs have fleshy fruits adapted to attract animals
as seed dispersers (Hladik & Hladik 1969; Van der Pijl
1969; McKey 1975; Howe 1977; Janson 1983; GautierHion et al. 1985). The foraging movements and behaviour of frugivorous animals therefore have profound
consequences on the spatial distribution of recruits
(e.g. Bleher & Bohning-Gaese 2001). Indeed, the deposition of seeds into favourable germination sites
depends exclusively on the foraging behaviour of the
dispersers, and is therefore largely outside the control
of the plant (Wheelwright & Orians 1982; Denslow
et al. 1986). In turn, foraging behaviour depends at
least in part upon abundance and availability of fluctuating food sources, competing species, intra-group
relationships and the activity of predators (Janson
Primates are important agents of seed dispersal for
a broad range of tropical tree species (e.g. Lieberman
et al. 1979; Estrada & Coates-Estrada 1984; GautierHion et al. 1985; Garber 1986; Janson et al. 1986; Tutin
et al. 1991; Chapman 1995). However, primate species
differ in their dispersal effectiveness depending upon their
behaviour, physiology and morphology (Lieberman &
Lieberman 1986; Levey 1987; Howe 1989; Zhang &
Wang 1995). Capuchin monkeys (Cebus spp.) are
considered especially effective seed dispersers because
of their short feeding bouts per tree, and removal of
most ingested seeds away from the source tree (Zhang
& Wang 1995). While several studies have examined
important aspects of the behaviour, ranging patterns,
resource use and seed dispersal by capuchin monkeys
(Janson 1985; Chapman 1989; Mitchell 1989), few have
analysed defecation patterns from the perspective of
the plant (Zhang & Wang 1995). Because capuchins
defecate seeds in smaller clumps than do most largerbodied primates (e.g. C. capucinus defecation mass: 7.6
± 4.8 g, n = 55; Alouatta palliata: 21.1 ± 16.9 g, n = 35;
E. V. Wehncke et al. unpublished data), survival of
capuchin-dispersed seeds is likely to be higher relative
to other primate species (Zhang & Wang 1995). As with
other frugivores, the seed shadows generated by primates may be estimated by combining information on
movements and gut passage rates of seeds (e.g. Murray
1988; Holbrook & Smith 2000). However, to characterize the biotic neighbourhood of dispersed seeds at
scales relevant to plant recruitment patterns requires
detailed information on the distribution of plant species.
These data are available from the 50-ha Forest Dynamics
Plot on Barro Colorado Island (BCI), Panamá.
Here we assess the seed dispersal pattern generated
by the white-faced capuchin, Cebus capucinus, and its
potential contribution to seedling recruitment on BCI.
Specifically, our objectives were to:
1 Determine the dietary preferences and feeding range
of Cebus groups that forage within the 50-ha Forest
Dynamics Plot.
2 Determine the distances and biotic neighbourhoods
to which seeds are dispersed.
3 Evaluate the contribution of Cebus to dispersal
limitation, defined as the reduction in dispersal success resulting from non-random deposition of seeds
(Nathan & Muller-Landau 2000).
Materials and methods
 
The study was carried out in a seasonally moist tropical
forest on Barro Colorado Island (BCI), Panamá
(9°10′ N, 79°51′ W). The island extends over 15.6 km2
and is covered with tropical moist, semi-deciduous
forest of several successional stages (Croat 1978; Foster
& Brokaw 1982). Rainfall averages 2600 mm year−1 with
a seasonal dry period from January until April (Windsor 1990). The annual temperature averages 27 °C, with
a diurnal variation of 9 °C. The main part of the study
was carried out in old growth forest in the 50-ha Forest
Dynamics Plot, on the central plateau of BCI. The plot
was established in 1982, and has been censused every
5 years since 1985. All trees > 1 cm d.b.h. have been
mapped, tagged and measured. The plot has been
described in detail by Condit (1998).
Study species
Cebus capucinus (white-faced monkeys) are relatively
small primates weighing on average 3 kg (Milton 1984)
and ranging from Honduras to Ecuador (Wolfheim
1983). Previous work on C. capucinus on BCI has
shown that the bulk of its diet (65%) is made up of fruit
and that group movements are related to the location of
fruit sources (Hladik & Hladik 1969; Mitchell 1989).
Cebus live in permanent social groups ranging from 5
to 24 individuals (Oppenheimer 1968; Mitchell 1989).
According to Mitchell (1989) at least 16 groups live on
BCI, with an estimated total population of between
278 and 313 individuals. Home ranges average
Seed dispersal
by white-faced
90 ± 13.2 ha, n = 4 (Mitchell 1989). In addition to C.
capucinus, howler monkeys (Alouatta palliata), tamarins
(Saguinus geoffroyi), night monkeys (Aotus trivirgatus)
and a single, re-introduced group of spider monkeys
(Ateles geoffroyi) are present on BCI.
    
Two groups of Cebus capucinus (hereafter Cebus) were
followed around the central plateau of mostly oldgrowth forest on BCI. The groups contained 15–17
individuals, and their home ranges overlapped in and
near the 50 ha plot. The study was carried out over four
months (March–July 1999) at the end of the dry season
and the transition to the wet season, when most plant
species fruit (Foster & Brokaw 1982). The groups were
observed during a total of 180 h. Observations were
more or less evenly distributed across all hours of the
day (from 6:00 to 18:00 h). Identifying marks on individual faces allowed us easily to track the same groups.
Each group was followed separately, and its location
was recorded every 10 min, or when abrupt changes in
the direction of travel occurred. Locations within the
plot were determined by recording the tag number of
the closest tree. Outside the plot, locations from either
trails or the plot edge were estimated using a compass
and pedometer. Although Cebus individuals commonly move together as a group, intra-group spatial
positions tend to differ according to individual social
status (Janson 1990a,b). Therefore for calculations of
feeding bouts per tree, peripheral subordinate individuals were not considered members of the group. We
estimated the time of entry/exit from feeding trees as
those times when the first non-peripheral individual
monkey of the group started and the time when the last
non-peripheral individual finished feeding in each tree.
We used the program TM (Version 1.1, Solna,
Sweden) to calculate the home range (area traversed by
a group during a given period) and feeding area (locations where the monkeys search for and eat fruits) of
each Cebus group. The Minimum Convex Polygon
method was used to calculate the size of the home
range. This method is frequently used in home range
studies (e.g. Mohr 1947; Thies 1998; Holbrook &
Smith 2000), and works particularly well for animals
that move together in groups. Using this method, isopleths are generated that connect the outermost coordinates in the range with the same estimated density of
observations. The technique provides a non-parametric
mapping method that can be applied to autocorrelated
points (the most common case for tracking data).
   
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
Diet was characterized from observations of feeding
events and from analysis of faecal material. We
recorded the location and time spent feeding by the
group (as defined above) in each fruiting tree, and collected a sample of the fruit, seed or other plant part
eaten for later identification. In addition, we recorded
how seeds were handled (seeds spat out, seeds damaged
and seeds swallowed) by classifying how the majority
of seeds per species were treated by the monkeys.
We used the Kernel method within  to
define feeding areas (Worton 1989; Seaman & Powell
1996). With this method, a feeding probability density
function is fitted around each mapped feeding observation. Isopleths of equal estimated feeding probability are generated by superimposing a grid over the
observed data and estimating feeding probability densities at each grid intersection. The kernel density estimator has the desirable qualities of directly producing
a density estimate, and being uninfluenced by effects
of grid size and placement (Silverman 1986). Using
, isopleths can be generated enclosing any percentage of feeding events. For this study we used isopleths enclosing 95% of feeding observations. We chose
a time interval of 10 min between feeding observations
to define feeding areas. Finally, we measured the areas
enclosed by the isopleths selected.
To evaluate whether the estimated feeding range of
Cebus corresponded to an area of high abundance
of preferred fruit trees, we compared the abundance of
preferred adult (reproductive-sized) trees per ha inside
the feeding range and outside the feeding range but
within the plot, and between the overlap and nonoverlap areas of the feeding ranges of the two groups.
Preferred fruit species were defined as those that
contributed > 5% of the total time Cebus spent feeding
(n = 6 species).
   
Where possible, defecations were collected while following the monkeys. The samples were taken to the
laboratory and all seeds found were counted and identified. The number of seeds < 1 mm long was estimated
from counts made of weighed subsamples of faecal
material. We mapped every location where faeces were
dropped, and recorded the tag number of the nearestneighbour plant for defecations inside the 50-ha plot.
With Cebus it is practically impossible to follow the
same individual for prolonged periods. Therefore, to
obtain valid seed dispersal distances, we first needed
to measure the monkey’s seed retention time. We did
this by feeding five captive Cebus at the Summit Zoo,
Panamá, with four different cultivated fruit species varying in seed mass (melon, papaya, cucumber and tomato;
range in fresh seed mass: 0.002–0.13 g, length: 3.3–
17.1 mm, width: 2.4 –6.3 mm), on five consecutive days.
The average time for > 75% of seeds to appear in faeces
was 105 ± SD 38 min (n = 36) (E. V. Wehncke unpublished data). There were no significant effects of individual Cebus or seed type on gut retention time
(F7,33 = 1.58, P = 0.17). To verify whether gut passage
times from captive monkeys are representative of wild
monkeys, we also directly calculated gut passage times
from our records of feeding events on infrequently
E. V. Wehncke
et al.
consumed species and from the subsequent collection
of faecal samples in the field. These passage times for
wild monkeys corresponded closely to our data from
the captive population (mean = 94 ± 43 min, n = 33).
We therefore selected 100 min for all calculations of
seed dispersal distances as it represents an intermediate
value between seed passage times of captive and wild
Cebus. This estimated passage time of 100 min was also
found in a study of captive Cebus apella in Brazil (E. V.
Wehncke unpublished data).
Data on gut passage time, the location and time of
departure from feeding trees, and subsequent movement patterns were used to calculate seed dispersal distances. Trees considered for analysis were those in
which monkeys spent more than 5 min feeding on
fruits and which had seed sizes that fall in the range of
swallowed seeds. From information on the location of
groups and on the time spent feeding per tree visited we
calculated the probability of movement away from the
food tree prior to defecation. The time of exit from
feeding trees was estimated as the time when the last
individual of a group left each tree. To evaluate the
probability with which Cebus defecated seeds beneath
conspecifics we used 26 days of tracking data and a
sample of 428 trees to estimate the probability of visiting a conspecific tree after the mean time of seed transit
through the gut (100 min). To estimate the proportion
of feeding events resulting in seed movement inside and
outside the plot, we used data of the position of feeding
trees and of the estimated position of the group at defecation and counted the events occurring inside and
outside the plot.
Finally, we evaluate whether Cebus preferences for
particular fruits results in shorter than expected dispersal distances. For the nine species most abundant in
faeces we compared the mean distance between seed
defecation sites and the nearest adult conspecifics with
the mean distance between 100 sites within the plot
chosen at random and nearest adult conspecifics. As
distances between trees and random plot locations
were not normally distributed we used the one-tailed
Mann–Whitney U-test for the comparison of each species. Seeds in defecations and random points found
nearer a plot boundary than an adult conspecific have
been excluded from the analyses.
    
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
Two Cebus groups, and on a few occasions some solitary individuals (that could have been members of
these groups), were seen feeding inside the plot. Both
groups of monkeys moved approximately 1.5–3.5 km
each day. Group 1 was followed inside and outside
the plot, whereas Group 2 was followed only inside the
plot, although its range extended beyond the plot. The
home range of group 1 occupied c. 150 ha (inside plot:
41 ha, n = 437 points; outside plot: 109 ha, n = 522
points). The 50-ha plot therefore comprised 27% of the
total home range of this group. Group 2 used an area of
33 ha inside the plot (n = 249 points). Therefore, group
1 used 81% and group 2 used 67% of the plot. Considering that their estimated home-range overlap inside the
plot is 31 ha (n = 17 points), we calculated that both
groups together used 86% of the plot (43 ha).
Considering both groups together, a total of 39 ha
inside the plot were used for feeding (78%). Separately,
group 1 used 29 ha and group 2 used 32 ha of the plot
for feeding. The overlap in their feeding area was of
22 ha (44% of the plot, n = 172 points). We found no
clear evidence to suggest that the within-plot feeding
range of Cebus was determined by a higher availability
of preferred tree species. Considering only the six most
frequently consumed species, we found a greater density of adult trees outside (71.9 trees ha−1) rather than
inside this feeding area (45.5 trees ha−1). However, the
density of adult trees where feeding ranges overlapped
was higher (53.9 trees ha−1) than in the rest of their
feeding area (21 trees ha−1).
Cebus monkeys spent 53% of the total observation time
feeding on fruits (5652 of 10630 min) and on average
spent 9.1 ± 6.8 min (range 1–52 min; n = 624) feeding
per fruiting tree. Over the 4 months of the study the two
groups manipulated fruits of 105 species, and ate all but
10 of them (Appendix 1). These 10 species were opened
and seeds removed while looking for insects. Of the 95
species eaten, the seeds of 67 of them were swallowed
and passed intact through the gut, and 28 were spat
out. Seeds eaten by Cebus ranged from 0.1 to 7 cm
long, and seed sizes swallowed were between 0.1 and
3 cm long (Appendix 1). From several sources of information we estimated that 240 species of trees, shrubs
and lianas fruited within the study area (J. Wright,
R. Perez, R. Foster, unpublished data). Therefore, we
estimate that 40% and 28% of species in fruit were
consumed and swallowed, respectively.
We estimated that a Cebus individual produces 8–10
defecations per day. On average, fresh faeces weighed
7.6 ± 3.2 g (n = 9). Ninety three percent (161 of 174)
of faecal samples collected contained seeds, which in
total represented 67 species. Each dropping contained
on average 2 ± 1.3 (range 0–8) different seed species.
Small-seeded (< 3 mm length) species were present in
most of the faecal samples collected (seeds of Cecropia
and Ficus were present in 90% of the seed containing
faeces). Faeces that contained only C. insignis seeds
contained on average 1430 ± 700 seeds (n = 9). By
contrast the top six species (those representing the
most abundant species in faeces, with seeds > 3 mm
length) occurred in droppings at densities of 7–57
seeds per dropping (average numbers of seeds per
droppings: Havetiopsis flexilis = 56.9 ± 155.5, n = 21;
Laetia procera = 29 ± 16.6, n = 11; Randia armata =
11.2 ± 12.8, n = 13; Cordia bicolor = 4.3 ± 4.7, n = 26;
Seed dispersal
by white-faced
Fig. 1 Probability of seed dispersal by Cebus away from a
parent plant. Estimates are based on individuals inside and
outside the 50-ha plot.
C. lasiocalyx = 4.4 ± 2.9, and n = 20; Hasseltia floribunda
= 6.9 ± 9.3, n = 7).
    
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
In general, the distance travelled by Cebus was also
a good predictor of the dispersal distance, because
the routes from one tree to the other tended to follow
straight lines. The two groups visited 624 trees, at a
rate of 3.1 ± 1.3 trees h−1 and 1.6 ± 0.9 species h−1.
Seeds < 3 cm in length were typically swallowed along
with the attached fruit pulp. Fruits with seeds too large
to be swallowed and most unripe fruits (8.6% of the
species handled) were dropped under the tree or up to
20 m from the source. Cebus moved swallowed seeds
from 10 m to 844 m away from parent plants, with the
highest probability of seed dispersal ranging between
100 m and 200 m (Fig. 1), and a mean distance of seed
travel of 216 ± 121 m (n = 323). For seeds consumed
inside the plot, where locations could be more accurately
determined, we found an average dispersal distance of
swallowed seeds of 208 ± 113 m (range: 20–844 m, n =
170). Although we found that seed size did not affect
gut passage time for captive Cebus, variation in the spatial location of fruit trees and in the time spent feeding
and manipulating fruits might result in differences in
dispersal distances among species. We found the highest estimated distance for Pterocarpus rohrii (843.8 m),
followed by Capparis frondosa (334.7 m) and Paullinia
bracteosa (334.7 m), and the lowest for Apeiba membranacea (61.6 m).
Dispersal by Cebus resulted in a high flux of seeds
in and out of the plot. Overall, 26% of feeding events
inside the plot resulted in dispersal beyond its perimeter
(n = 223). As expected, fewer feeding events recorded
outside the plot resulted in dispersal into it (8%, n =
153). All of the tree species dispersed into the plot were
already represented there as recruits > 1 cm d.b.h.
Fig. 2 Probability of movement of Cebus away from fruiting
trees after starting feeding.
    
 
Once feeding bouts started in a tree, the highest probability of group movement away from that tree was
within the following 10 min (Fig. 2). Therefore, Cebus
monkeys almost always moved seeds that they swallowed away from the crown of the maternal tree.
Sequential selective foraging on favoured species, however, could result in dispersal back below or near conspecifics. We evaluated this possibility in several ways.
Firstly, we compared the identity of trees where defecations occurred with their seed contents. Only 7 of 138
defecations examined were deposited beneath conspecifics. Secondly, we used tracking data to calculate the
probability that Cebus would visit a conspecific after
the mean time of seed transit through the gut. For a
sample of 428 trees this probability was only 0.093.
Thirdly, we compared the mean distance between defecation sites and nearest adult conspecifics with the
mean distance to nearest adult conspecifics if seeds
were deposited at random through the plot. We found
that for six of nine species present in 161 defecations,
mean distances from random points and from defecation sites were not significantly different (Table 1). For
the remaining three species, distance to conspecifics
from defecation sites was significantly shorter than
expected. Two of these species, Cecropia insignis and
Cordia bicolor, were among the most frequently visited
by Cebus (Appendix 1), yet differences in mean distance were rather small (< 10 m). The remaining species, Ficus costaricana is represented by only seven
adults in the plot, only one of which was visited by
Cebus and may have been the only individual that was
reproductive during the study period.
Our results indicate that Cebus capucinus monkeys on
BCI are effective seed dispersers that are likely to
strongly influence the recruitment success of trees
E. V. Wehncke
et al.
Table 1 Average minimum distances within the plot between (i) 100 randomly selected points and the nearest reproductive-sized
tree of each species listed, and (ii) defecation locations and the nearest reproductive-sized conspecific tree. Differences in distance
distributions are tested with the Mann–Whitney U-test
Minimum distance
(random points)
Minimum distance
(defecation sites)
Mean (m)
Mean (m)
trees (N)
sites (N)
Cecropia insignis
Cordia bicolor
Desmopsis panamensis
Ficus costaricana
Ficus yoponensis
Hasseltia floribunda
Laetia procera
Miconia argentea
Randia armata
< 0.01
whose seeds they swallow. High dispersal effectiveness
results from the following attributes: (i) long-distance
and near-continuous daily movement patterns; (ii) a
highly frugivorous diet encompassing many species;
(iii) scattered deposition of seeds through frequent defecations; (iv) inferred low rates of post-dispersal seed
predation relative to other primate species. Below we
discuss these attributes of dispersal effectiveness in
more detail.
    
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
We recorded daily movement patterns of up to 3.5 km
by the two groups of Cebus studied on BCI. This is
comparable with observations made by Zhang & Wang
(1995) of C. apella in French Guiana (about 2 km day−1).
Both groups on BCI used the 50-ha plot during the
study, feeding in 67–86% of the total plot area. The
groups overlapped in their feeding area over almost
half of the plot. Assuming that Cebus monkeys move in
relation to the location of preferred available fruit
sources (Hladik & Hladik 1969; Mitchell 1989), such a
strong overlap of feeding areas may suggest a high concentration of preferred species in that area. We found
no evidence for increased densities of preferred fruit
trees inside the feeding area compared with the rest of
the plot, although a larger proportion of trees may have
been in fruit in the feeding range, or may have produced
larger fruit crops.
However we would expect the distribution of reproductive trees to have only a relatively diffuse effect on
foraging locations during the dry–wet season transition, given the tremendous diet breadth of this primate
species, which consumed 40% of all species in fruit
available during the study. Rather than tracking the
distribution of fruiting trees, Cebus movement patterns
may be a consequence of other factors, including
intraspecific competition, predation pressure (if existent in the study site) and the distribution of food
resources other than fruit (e.g. invertebrate and vertebrate prey and water holes).
   
Despite the short duration of the study, the two Cebus
groups manipulated and consumed 105 species of fruit
from inside and outside the 50-ha plot. In addition, the
seeds of a majority of them (64% of 95 fruit species consumed) were found intact in their faeces. Three factors
may help explain the diversity of the Cebus diet. First,
the study was carried out at the dry–wet season transition when most of tree species on the island fruit (Foster 1982). Second, the social organization of the Cebus
group influences feeding behaviour because members
with low dominance rank avoid entering trees with low
fruit production until after the rest of the group has left
(Janson 1985; E. V. Wehncke pers. obs.). In the meantime, they remain in surrounding trees exploring for
new food items. Third, Milton (1984) suggested that
food choice might be dictated as much by internal constraints intrinsic to the digestive physiology of the
feeder as by extrinsic factors such as nutrient content or
relative availability. Cebus turned over gut contents
very rapidly, and this fast food passage permits them to
rid the gut rapidly of indigestible seeds present in fruit.
Consequently, Cebus are able to compensate for the
low protein content of some foods by turning over a
large volume of fruit each day (Milton 1984).
 
 
Characteristics related to morphology and physiology
of Cebus also explain the effectiveness with which these
seeds were dispersed. Dispersal effectiveness is defined
as the contribution a disperser makes to the reproductive success of a plant, and is determined by the quantity of dispersed seeds and the quality by which seeds
are dispersed (Schupp 1993, 2002). In turn, the quality
of seed dispersal can be characterized by the treatment
that seeds receive by the disperser and the spatial
pattern in which they are deposited (Schupp 1993, 2002).
We show here that the gut retention times for Cebus
(100 min) is much shorter than for other sympatric
Seed dispersal
by white-faced
primate species (Alouatta palliata: 20.4 h, Ateles geoffroyi:
4.4 h, Milton 1984), resulting in more defecation events
per day and fewer seeds per dung pile. Furthermore,
individual Cebus faeces were small and were produced
asynchronously by members of the group. Scattered
dispersal of small numbers of seeds may strongly influence post-dispersal seed fate for Cebus relative to other
primates (Howe 1989). Zhang & Wang (1995) showed
that in Guyana seeds dispersed by spider monkeys
(Ateles paniscus) were more than twice as likely to be
subsequently removed as seeds dispersed by Cebus apella.
Similarly, in a tropical dry forest (E. V. Wehncke et al.
unpublished data) have shown that seed removal by
rodents in Alouatta palliata (howler monkey) faeces
was higher than from Cebus capucinus faeces. Because
most seed removal is likely to result in seed predation
(Janzen 1971), the amount of faecal mass likely has a
direct effect on post-dispersal seed survival.
The second component of dispersal effectiveness is
the biotic and abiotic neighbourhood into which seeds
are dispersed. Dispersal below or close to conspecific
crowns is likely to result in lowered probabilities of
recruitment due to increased seed and seedling predation (Janzen et al. 1976; Augspurger 1983, 1984; Condit
et al. 1992; Forget 1993; Coley & Barone 1996). Although
short seed retention times might be expected to result in
defecation of seeds below or close to parent trees, this
did not occur. Cebus spent a maximum of 50 min foraging in a single tree and most frequently left within
10 min of starting to feed. This resulted in a high rate of
trees visited and dispersal distances averaging 216 m.
  C E B U S  
 
© 2003 British
Ecological Society,
Journal of Ecology,
91, 677–685
One of the major factors thought to contribute to tree
species coexistence is the failure of seeds to arrive at
potential recruitment sites (Tilman 1994; Hurtt & Pacala 1995; Pacala & Levin 1997; Zobel et al. 2000). This
phenomenon, called seed limitation, reduces population growth rates and provides a mechanism by which
competitively inferior species can be maintained in a
community for prolonged periods (Crawley 1990;
Turnbull et al. 2000; Muller-Landau et al. 2002). Seed
trapping in tropical forests indicates that some degree
of seed limitation, determined either by limited reproductive output (source limitation, sensu Nathan &
Muller-Landau 2000), or clumped patterns of seed distribution (dispersal limitation, senso stricto Nathan &
Muller-Landau 2000; Schupp et al. 2002) operates for
almost all species in the community. This includes very
common species and small-seeded species dependent
upon the availability of particular microsites (Silman
1996; Hubbell et al. 1999; Dalling et al. 2002).
Our observations of Cebus indicate a tendency of
this dispersal agent to contribute relatively little to the
overall dispersal limitation of species whose seeds it
swallows. The combination of short feeding bouts, a
broad diet, rapid movement and asynchronous defeca-
tion within the group meant that the locations of seed
deposition sites were widely spaced, and were not significantly different from random with respect to distance to nearest adult conspecifics, at least for most
species. This contrasts with many other vertebrate frugivores capable of equally long-distance seed dispersal.
Important alternate dispersers of species consumed by
Cebus on BCI include bats, tapirs, and howler and
spider monkeys. These frugivores are also capable of
moving seeds several hundred metres but are likely to
contribute more strongly to dispersal limitation than
Cebus because seeds are primarily deposited in large
clumps at feeding roosts, latrines and sleep trees (Julliot
1986; Zhang & Wang 1995; Fragoso 1997; Thies 1998;
Schupp et al. 2002).
   
Vertebrate frugivores generate dispersal patterns that
have proven difficult to describe with current models.
Recently, inverse modelling procedures have been
developed that use data on the location of adult trees
and seed collections in traps to characterize seed dispersal patterns (Ribbens et al. 1994; Clark et al. 1999).
These models hold much promise for characterizing
landscape-level seed limitation and for providing an
integrated measure of the net activity of all dispersal
agents against which the relative effectiveness of particular dispersers could be evaluated (Nathan &
Muller-Landau 2000).
The application of inverse modelling on BCI has
shown good fits between actual and predicted seed
capture to mesh traps arrayed on the 50-ha plot for winddispersed species, but rather poorer fits for vertebratedispersed species (Dalling et al. 2002). Our results
indicate that a limitation to applying this technique for
primate-dispersed species is that the mean dispersal
distance of > 200 m for Cebus greatly exceeds the mean
distance between reproductive sized conspecifics for
most tree species on the plot. A future generation of
dispersal predictors will therefore likely require much
larger mapped forest stands and more parameter-rich
models that can account for the complex movement
patterns of vertebrate frugivores.
This research was funded by the Smithsonian Tropical
Research Institute (STRI) through a Short-Term Fellowship to E.W. We especially thank Osvaldo Calderón
for identification of the plant and seed samples. We
thank STRI for logistic support, Joseph Wright and
Rolando Perez for access to unpublished data, and Juan
José Rodríguez and Javier Ballesteros for help in the
field. Hugh Drummond, César Domínguez, Gerardo
Ceballos, Sabrina Russo, Helene Muller-Landau and
Carol Augspurger provided helpful comments on the
E. V. Wehncke
et al.
Supplementary material
The following material is available from http://
Appendix S1 List of plant species manipulated by
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Received 19 September 2002;
revision accepted 7 April 2003.

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