OIKOS 110: 435 /440, 2005
Influence of seed size on dispersal patterns of woolly monkeys
(Lagothrix lagothricha) at Tinigua Park, Colombia
P. R. Stevenson, M. Pineda and T. Samper
Stevenson, P. R., Pineda, M. and Samper, T. 2005. Influence of seed size on dispersal
patterns of woolly monkeys (Lagothrix lagothricha ) at Tinigua Park, Colombia.
/ Oikos 110: 435 /440.
Seed size in tropical forests is expected to vary in relation to dispersal mode,
recruitment requirements and the nature of seed enemies in each community. Some
studies have emphasized an advantage of large-seeded species in environments subject
to low rates of disturbance, but at the same time the number of dispersers tends to
decrease as seed size increases. In this paper we describe how seed size affects the
probabilities of seed dispersal by woolly monkeys at Tinigua National Park and we
compare dispersal patterns among age/sex classes. The results are based on 1236 fecal
samples recovered from focal individuals during two years. Woolly monkeys are able to
swallow wide seeds; however, there seems to be a limit imposed by anatomical
constraints that does not allow them to swallow seeds wider than 18 mm. Most of the
seed mass dispersed by the monkeys falls in the categories between 6 and 12 mm wide.
Seed selection in terms of mass was not observed for small-seeded species, but it was
observed for some of the medium sized species (without any clear size preference) and
there was a clear tendency to swallow relatively small seeds from the large-seeded
species. Although we did not observe a difference in the number of seeds dispersed by
deposition among age/sex classes, juveniles disperse a lower seed mass than adult
animals. These differences highlight that different age/sex categories play distinct
ecological roles in terms of seed dispersal processes. Seed selection by primates might
impose selection pressures in seed size traits, but more studies are necessary to ascertain
their potential evolutionary role.
P. R. Stevenson, Dept of Anthropology, SUNY at Stony Brook, Stony Brook, NY 117944364, USA. Present address for PRS, M. Pineda and T. Samper, Depto de Ciencias
Biológicas, Universidad de Los Andes, Cr. 1a No. 18A-10, Bogotá, Colombia
([email protected]).
Seed size in tropical forests is known to vary among
species depending on regeneration strategies, dispersal
mode, and other selection pressures that affect the
survival of the seeds, such as pathogens and herbivores
(Howe and Richter 1982, Foster and Janson 1985,
Westoby et al. 1996). There is a well established tradeoff
between seed size and the number of seeds a plant can
produce (Smith and Fretwell 1974, Leishman et al. 2000,
Westoby et al. 2002), because an individual plant can
produce a large number of small seeds or a few number
of large seeds (Shipley and Dion 1992, Greene and
Johnson 1994, Jakobsson and Eriksson 2000, Henery
and Westoby 2001). Large-seeded species usually have
considerable energy stored in the seed, that allows them
to start growing in conditions of low light availability
such as the ground under a forest with a closed canopy,
mineral nutrient shortage or soil drought, and to better
resist competition from established vegetation or other
seedlings, and/or defoliation (Salisbury 1974, Foster and
Janson 1985, Harms et al. 1997, Westoby et al. 2002). In
contrast, small-seeded plants need an abundance of light
for the first developmental stages. Thus, these kinds of
Accepted 23 January 2005
Copyright # OIKOS 2005
ISSN 0030-1299
OIKOS 110:3 (2005)
435
plants usually regenerate in canopy gaps. According to
parameters of recruitment success, in closed-canopy
forests there should be a selection pressure towards
increased seed size because large seeds could develop
well on the ground as well as in gaps, especially in stable
environments (Hammond and Brown 1995). However, it
is also known that the number of seed dispersers tend to
be negatively correlated with seed size (Wheelwright
1985), thus, seed size may influence dispersal probabilities. In other words, plants with large seeds have a lower
coterie of dispersers in contrast to small-seeded plants,
because there is a limit in the size of seed that an animal
can swallow, related to its size and anatomy (e.g. peak
gape or throat width; Janson 1983). Given that seed
dispersal in general increases plant fitness in tropical
forests (Wills et al. 1997, Wills and Condit 1999,
Terborgh et al. 2002), there should be a tradeoff between
seed size and dispersal probabilities.
Several studies have reported selection on seed size for
avian-dispersed plants (Howe and Vander Kerckhove
1980, Wheelwright 1993). If dispersal is a process that
increases plant fitness and seed size is a heritable trait, an
evolutionary change should be expected. On the other
hand, comparative analyses and other evidence have
suggested that there are several constraints limiting the
evolution of fruit and seed morphology (Herrera 1985,
Jordano 1995), though, changes do occur (Janson 1992).
Seeds should be swallowed only if the process offers
some foraging benefits to the dispersers, presumably
from the nutrients and water present in the fleshy parts
of the fruit (Pijl 1972). A large load of small seeds or
some very large seeds may increase body weight and
unbalance travel energetics (Janzen et al. 1976). Therefore, large seeds should be swallowed when the reward is
high enough to counterbalance the foraging cost, and
this may happen when there is a positive correlation
between seed size and reward (e.g. pulp energy, Wheelwright 1993, Garber and Kitron 1997, Pineda 2004).
Furthermore, the final outcome depends on the relative
size of the disperser (a large palm seed might be
impossible to carry for an ant, a considerable weight
for a spider monkey, but insignificant to a tapir).
Generally it is difficult for frugivores to separate the
seeds from the pulp, either because they are small and
immersed in the pulp and/or because the pulp is firmly
attached to the seed. Thus, it might be too costly for
frugivores to spend time separating seeds from pulp,
because that time could be used to ingest more fruits, a
resource that could be limited in time (a fixed number of
ripe fruits during a particular visit time). For example,
Old World monkeys are known to disperse fewer seeds in
their guts than New World primates (Chapman 1995,
Lambert 2002), and this difference has been associated
with the fact that the Old World cercopithecines have
cheek pouches where the monkeys store many fruits that
are later processed to discard the seeds. This example
436
also stresses that morphological adaptations and handling abilities differ among frugivores. Since handling
time usually is important determining foraging efficiency, these factors must also affect the chance of
endozoochorous seed dispersal. For instance, the handling time necessary to open a protected fruit or to ingest
a large drupe should not be as limiting for a primate
than for a bird.
In addition to the potential foraging benefits discussed
above, only one hypothesis has been postulated to
explain direct benefits of swallowing large seeds (Garber
and Kitron 1997). According to this theory, which is
based on observations of relatively huge seeds dispersed
by small tamarins, the monkeys use these kinds of seeds
to remove parasites attached to the digestive tube.
The aim of this paper is to describe how woolly
monkeys disperse seeds of plants with different seed size.
In particular we answer the following questions: 1) is
there a limit in the width of seeds dispersed by woolly
monkeys? 2) Is the ratio between the mass of dispersed
seeds and the mass of manipulated seeds negatively
correlated with seed size? 3) Do different age/sex classes
disperse seeds of different size? 4) Do they prefer to
swallow small rather than large seeds from the same
plant species? 5) Are internal parasites found less often
in feces when the monkeys are swallowing large seeds?
The results are discussed in relation with the potential
role of the woolly monkeys in imposing selection
pressures on plants for a particular seed size.
Methods
We recovered dispersed seeds from focal woolly monkeys
during five days per month for two years at Tinigua
National Park (Stevenson 2002). In about 19% of the
1527 collected depositions we were uncertain if the focal
animal was indeed the origin of the fecal material,
because other monkeys were in close proximity to the
focal animal. Such depositions were not included in the
analyses, in order to assure that the seed size corresponded to the age/sex class of the focal animal.
We assessed seed size in different ways for the analyses
in an effort to avoid manipulation of defecated seeds. For
the majority of the analyses, we used the average or the
midrange value of the largest seed width presented for
each plant species (Stevenson et al. 2000b, Stevenson
2002). This value is the minimum dimension that the
gape has to open to allow a seed to be swallowed. We
compared the frequency of seeds dispersed in different
seed width classes among (1) the weight of seeds
dispersed by the focal animals, (2) the estimated mass
of seeds manipulated by the monkeys, and (3) the mass
of seeds available in the forest. The last estimate was
based on the number of seeds produced by different
species in 5.6 km of phenological transects during two
OIKOS 110:3 (2005)
study years and the average seed weight per seed of each
species (Stevenson 2002).
The analyses presented in the previous paragraphs
were done using the average seed width for the species,
calculated from non-dispersed seeds. Thus there is some
possibility that the monkeys can select to swallow seeds
of a particular size, which could be different from the
estimated average for the community. In order to
estimate selection of individual seeds within the same
plant species, we compared the dry weight of dispersed
seeds with seeds collected from fruits in good condition
below the parental tree (using TS tests).
Results
We found that woolly monkeys do swallow very wide
seeds. The largest seeds can be as wide as 18 mm and as
long as 33 mm, from species such as Spondias mombin
(28/17 mm), Garcinia macrophylla (30/18 mm and
33 /13 mm), Talisia intermedia (22 /14 mm) and Endlicheria sericea (27 /17 mm). However, there is a sharp
drop in the mass of dispersed seeds of species that have
an average of more than 18 mm width, even though they
consume fleshy fruits from plants with seeds at least 23
mm wide (Fig. 1). The majority of the seeds swallowed
by the monkeys are small, but the majority of the seed
mass dispersed by woolly monkeys corresponded to seed
widths between 6 and 12 mm (Fig. 1). The apparent
Fig. 1. Size width comparison among the mass of seeds
dispersed and manipulated by woolly monkeys and those
available in the forests at Tinigua National Park. The estimated
proportion of weight of seeds dispersed comes form the number
of seeds recovered from the feces and their average weight. The
mass of manipulated seeds was estimated from the total
duration of feeding times by focal animals to each fruiting
species and feeding rates (total number of seeds manipulated in
periods of 30 s). The value of available seed weight comes from
estimate of the number of seeds produced by all species in 5.6
km of phenological transects.
OIKOS 110:3 (2005)
bimodal distribution of seed mass along the seed width
continuum is related to the distribution of seed mass of
manipulated seeds and seed availability, except for the
large mass fraction of large seeds (/18 mm wide) that
are not swallowed by the monkeys.
The ratio between the number of dispersed seeds and
manipulated seeds for different plant species was negatively correlated with seed width. A linear regression
model to explain that ratio, which describes the probability of ingestion, resulted in a significantly negative
slope (F /7.8, p/0.006, n/139). However, the explanatory power of the model was very low (r2 /0.05)
because the ratio was quite variable for small and
medium seeds. In fact, the negative relationship is caused
mainly by very low ratios for large seeded species
(Fig. 1), which are usually dropped under the parental
tree after a few bites (e.g. Spondias spp).
In the analysis of seed size including eleven species for
which we measured the weight of dispersed and undispersed seeds, we found evidence of seed selection for
five of them (Table 1). It is interesting to note that
selection was not observed for either of the two smallseeded species analyzed. Seed selection was found for
two out of the six species with medium sized seeds, and
the monkeys preferred to swallow small seeds in one case
and large seeds in the other. In the latter case we found a
positive relationship between seed and pulp mass
(Pineda 2004). For all three large-seeded species, the
woolly monkeys showed a very consistent pattern to
prefer to swallow smaller seeds than the average.
We found no differences in the average number
of seeds dispersed by different age/sex classes (adult
males /70, adult females /77 and juveniles/65). The
large variations in the number of seeds per deposition
were mainly due to the temporal availability of small
seeded species. In contrast, there were marked differences among age/sex classes in the mass of seeds
dispersed in each deposition because small immature
monkeys carried less mass (adult males /4.3, adult
females /4.4, and juveniles/2.5). In Fig. 2, this tendency is apparent for a wide variety of seed sizes and it is
accentuated in the largest size category, for which the
juveniles disperse less than one-seventh of the seed mass
dispersed by adult animals.
For small seeded species we did not detect differences
in the mass of seeds swallowed by different age/sex
classes. Some differences were apparent for medium
sized species, but selection of small or large seeds was
not consistent among age/sex classes (Table 2). Few
differences were found for large-seeded species, but this
result is due to the fact that juveniles were not included
in the analyses because they seldom disperse large seeds
(Fig. 2).
Both adult females and males swallow large seeds and
differences between these adult classes were only found
437
Table 1. Difference in seed mass between the seeds dispersed by woolly monkeys at Tinigua National Park and seeds collected
directly from parental plants (available seeds). The type of difference in relation to seed size between dispersed and available seeds is
noted in the last column.
Species
Seed size
Width (mm)
Apeiba aspera
Laetia corymbulosa
Pseudolmedia laevigata
Protium glabrescens
Protium sagotianum
Inga cylindrica
Castilla ulei
Gustavia hexapetala
Garcinia macrophylla
Spondias mombin
Spondias venulosa
2
2
5
6
7
8
8
11
13
16
18
ANOVA and t-test statistics
Weight (g)
0.02
0.01
0.25
0.37
0.43
0.76
0.62
1.09
5.96
3.13
3.06
F
3.4
1.4
1.4
0.3
26.1
1.0
22.8
0.3
16.4
23.7
18.2
Fig. 2. Comparison of the seed mass dispersed by three
different age/sex classes of woolly monkeys at Tinigua National
Park, in relation to seed width.
for the species with the widest seeds analyzed, for which
the adult males disperse larger seeds than adult females.
Finally, in spite of the careful inspection and washing
of the fecal samples, we were unable to recognize any
type of macroscopic parasites such as the spiny-headed
worms (Ancanthocephala).
Discussion
Several lines of evidence described in this study suggest
that woolly monkeys are selective in the kind of seeds
that they swallow, the most consistent pattern being that
they preferentially disperse the smallest seeds available
from the very large seeded species. In spite of the fact
that they consume fruits from species larger than 18 mm
wide, this width seems to be the size limit that they are
able to swallow (Dew 2001). This limit seems to be
imposed by morphological restrictions associated with
body size (e.g. esophagus size), in accordance with the
438
P
0.08
0.24
0.24
0.56
B/0.0001
0.31
B/0.0001
0.60
0.0001
B/0.0001
B/0.0001
Type of difference
N
26
72
139
80
327
197
135
231
69
431
240
dispersed/available
dispersedB/available
dispersedB/available
dispersedB/available
dispersedB/available
different role that the small juvenile individuals play in
contrast to adult animals that carry a larger proportional mass of seeds. This difference is highly accentuated in the largest width category that they swallow and
suggests that conservation programs must consider that
different age classes play different ecological roles in
processes of forest regeneration.
The size preference might impose a selection pressure
for the plant species if several conditions are met. First,
woolly monkeys should be important dispersers for
those plant species by being the main seed dispersers
or by producing better dispersal efficiency than other
fruigivores, a point that will remain obscure until similar
quantitative data are obtained for other animal species.
Second, the morphological traits should have a high
heritable component, which is a point that we do not
know for the species analyzed, although heritability in
seed morphology traits has been found in other studies
(Harper et al. 1970, Hulme 1971, Burly and Styles 1976,
Harper 1977, Wheelwright 1993, but see Obeso 1993). In
relation to the set of dispersers, we found a trend for the
large-seeded plants to have a smaller number of seed
dispersers (Stevenson 2002), a result that suggests that
woolly monkeys could be playing important roles in the
demography of these species. However, in this community we did not find any case in which a particular
plant species could be entirely dependent on woolly
monkeys for dispersal. In general the fruit diet of woolly
and spider monkeys is very similar in the study site
(Stevenson et al. 2000a). For example, Spondias spp. are
dispersed by other ateline monkeys and the fruits
dropped below the parental trees are consumed by a
variety of animals, including tapirs, who during the
fruiting time of these species defecate up to 70 seeds in
each deposition (P. R. Stevenson, unpubl.). In general,
the patterns of germination rates of seeds dispersed by
different primates are not very different (Stevenson et al.
2002). However, more studies quantifying seed dispersal
by other vectors will be necessary to assess the potential
for selection in the evolution of morphological traits.
OIKOS 110:3 (2005)
Table 2. Difference in the seed mass dispersed by three different age/sex classes of woolly monkeys (fe /adult females, ma /adult
males, and juv/juveniles) at Tinigua National Park. The main type of difference in relation to seed size between dispersed and
available seeds is noted in the last column.
Species
Seed width
(mm)
Fresh weight
(g)
ANOVA statistics
F
Jacaratia digitata
Trichilia tuberculata
Inga edulis
Pseudolmedia laevis
Protium glabrescens
Protium sagotianum
Brosimum lactescens
Crepidospermum rhoifolium
Inga alba
Pourouma bicolor
Inga cylindrica
Castilla ulei
Alibertia cf. hadrantha
Inga stenoptera
Paullinia faginea
Gustavia hexapetala
Hymenaea oblongifolia
Bursera inversa
Spondias mombin
Spondias venulosa
4
4
5
5
6
7
7
7
7
7
8
8
9
9
9
11
11
12
16
18
0.05
0.18
0.50
0.21
0.37
0.43
0.41
0.34
0.23
0.49
0.76
0.62
0.17
0.82
0.26
1.09
2.42
0.82
3.13
3.06
Preliminary results in this community showed that seed
dispersal is important for many plant species, especially
to colonize appropriate places for development, and to
avoid negative density-dependent effects in sapling
recruitment (Stevenson 2002).
The woolly monkeys preferences of large seeds in
some medium-sized species suggest that there are
benefits associated with the ingestion of such seeds,
such as a positive correlation between the amount of
pulp ingested and seed size. Some preferences among
age/sex classes do not seem to show particular patterns
(e.g. juveniles preferring relatively small seeds), and in
some cases it may be that the differences are superfluous,
because it was impossible to assure statistical independence in the measurements. In particular, it is possible
that many of the recovered seeds belonged to a single
parental plant and those seeds were taken as independent sample points in the analyses. In this scenario, the
differences between age/sex classes could represent
differences in seed size of two different trees, from which
seeds were consumed during two distinct sampling
bouts. Given the long retention times in the gut
(Stevenson 2000) and without any molecular tool to
infer plant maternity, it is impossible to know how
frequently this effect could have happened. We suggest
that a better analysis could be done including the average
seed size of each sampling session as an independent
data point (a procedure that we were unable to do in the
reorganized data sets).
The inspection of more than 1500 fecal samples
without recognizing any macro-parasite suggests that
the curative theory to explain the swallowing of large
seeds does not play a role in woolly monkeys. Therefore,
there was no correlation between the occurrence of large
OIKOS 110:3 (2005)
0.20
0.66
2.37
5.57
9.70
4.50
8.86
0.85
2.85
37.90
9.00
7.00
0.64
2.18
2.01
0.30
2.10
1.70
0.44
7.80
p
0.890
0.510
0.050
0.006
0.004
0.004
B/0.001
0.470
0.060
B/0.001
B/0.001
0.000
0.640
0.110
0.160
0.900
0.100
0.160
0.440
0.002
Type of difference
n
60
108
185
68
39
295
160
37
166
682
181
106
43
32
41
125
79
76
54
30
fe/others
fe/ma
ma /others
fe/others
fe/juv/ma
juv /others
ma /others
ma /fe
seeds in the droppings and the appearance of macroparasites, and there was no support for the hypothesis
that large seeds are used to scour out parasites. We
suggest that there may be foraging advantages in
swallowing seeds, given that visit time seems to be
limited by factors like competition and group cohesion
constraints, which allow the individual monkeys to
acquire more total energy by ingesting the pulp together
with the seeds. Separation of seeds from pulp might
require time or morphological adaptations such as cheek
pouches that Neotropical primates lack.
Acknowledgements / We would like to thank the field assistants
who helped in gathering information, especially MaClara
Castellanos, Alicia Medina, Carolina Garcı́a and Andrés
Link. We thank Drs. Charles Janson, Patricia Wright, John G.
Fleagle and Anthony DiFiore for their comments. This study
was possible thanks to the help of different institutions such as
La Fundación para la Promoción de la Investigación y
la Tecnologı́a (Banco de la República), Margot Marsh
Foundation, Lincoln Park Zoo, Primate Conservation Inc.,
IdeaWild, Colciencias, Universidad de Los Andes and CIEM
(Centro de Investigaciones Ecológicas La Macarena).
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