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Faculty Publications in the Biological Sciences Papers in the Biological Sciences
2004
Aggregated Seed Dispersal by Spider Monkeys Limits Aggregated Seed Dispersal by Spider Monkeys Limits
Recruitment to Clumped Patterns in Recruitment to Clumped Patterns in
Virola calophylla Virola calophylla
Sabrina E. Russo
University of Nebraska - Lincoln
, srusso2@unl.edu
Carol K. Augsperger
University of Illinois at Urbana-Champaign
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Russo, Sabrina E. and Augsperger, Carol K., "Aggregated Seed Dispersal by Spider Monkeys Limits
Recruitment to Clumped Patterns in
Virola calophylla
" (2004).
Faculty Publications in the Biological
Sciences
. 224.
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tion in seed density generated by dispersal agents, par-
ticularly in forest communities. An increasing number
of studies has revealed patterns of seed deposition in
forests either by using seed traps and inverse model-
ling or by developing mechanistic models of the be-
havior of dispersal agents to simulate seed dispersion
(Nathan & Muller-Landau 2000). These studies sug-
gest that seed deposition is often spatially aggregated,
particularly for vertebrate-dispersed tree species (Sch-
upp et al. 2002).
Second, the spatial pattern of seed deposition and the
recruitment consequences of that pattern affect the den-
sity and dispersion of plants in later life stages (Hubbell
1980; McCanny 1985). One mechanism that has gured
prominently in explaining tree dispersion, particular-
ly in tropical forests (Hubbell 1980; Augspurger 1983a;
Clark & Clark 1984; Condit et al. 1992), is survival that
depends upon the density of seeds, seedlings, and/
or saplings or their distance from a conspecic adult
(Janzen 1970; Connell 1971). Such non-random surviv-
al resulting from natural enemies, such as seed preda-
tors and seedling pathogens, can thin clumps of seeds
and seedlings and produce spatial patterns that dif-
fer from what would result simply from random thin-
INTRODUCTION
Seed dispersal results in colonization of potential re-
cruitment sites and establishes the initial template of
offspring dispersion. It therefore can strongly inu-
ence the spatial distribution of adult plants in a land-
scape (Howe & Smallwood 1982; Schupp & Fuentes
1995). The spatial distribution of individuals, in turn,
mediates intra-and interspecic interactions, such as
density-dependent mortality and competition, and the
balance of these interactions affects species coexistence
(Chesson 2000). Thus, understanding the role of seed
dispersal in the development of spatial pattern in plant
populations is critical to explanations of plant commu-
nity structure (Levin 1974; Hurtt & Pacala 1995; Ches-
son 2000).
The development of spatial pattern in plant popula-
tions results from a set of processes governing the pat-
tern of seed deposition and a set of post-dispersal pro-
cesses that modify that pattern during recruitment
(Schupp & Fuentes 1995; Schupp 1995). First, the spa-
tial extent of seed dispersal restricts the suite of poten-
tial sites for recruitment (Howe & Smallwood 1982).
However, there are few descriptions of seed dispersion
at spatial scales large enough to encompass the varia-
Published in Ecology Letters (2004) 7: 1,058-1,067. DOI: 10.1111/j.1461-0248.2004.00668.x. Copyright 2004, Wiley. Used by per-
mission.
Aggregated Seed Dispersal by Spider Monkeys Limits Recruitment to Clumped
Patterns in Virola calophylla
Sabrina E. Russo
1*
and Carol K. Augspurger
2
1
Department of Animal Biology, University of Illinois, Urbana, Illinois, U.S.A.
2
Department of Plant Biology, University of Illinois, Urbana, Illinois, U.S.A.
*Correspondence and present address: School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Ne-
braska, U.S.A.; srusso2@unl.edu
Abstract
The initial spatial pattern of seed deposition inuences plant population and community structure, particular-
ly when that pattern persists through recruitment. In a vertebrate-dispersed rain forest tree, Virola calophylla, we
found that spatially aggregated seed deposition strongly inuenced the spatial structure of later stages. Seed dis-
persion was clumped, and seed densities were highest underneath V. calophylla females and the sleeping sites of
spider monkeys (Ateles paniscus), the key dispersal agent. Although these site types had the lowest per capita seed-
to-seedling survival, they had the highest seedling/sapling densities. Conversely, seed and seedling/sapling den-
sities were lowest, and seed survival was highest, at sites of diurnal seed dispersal by spider monkeys. Negative
density-dependent and positive distance-dependent seed survival thinned seed clumps. Nonetheless, the clumped
dispersion at sleeping and parental sites persisted to the seedling/sapling stage because differences in seed depo-
sition were large enough to offset differences in seed survival among these site types.
Keywords: Ateles paniscus, Dispersion, Myristicaceae, Neotropical forest, Peru, Recruitment, Seed dispersal, Seed
survival, Seedlings, Virola calophylla.
Ag g r e g A t e d Se e d di S p e r S A l b y Sp i d e r Mo n k e y S li M i t S re c r u i t M e n t t o cl u M p e d pA t t e r n S i n Vi r o l a c a l o p h y l l a 1059
was consistent with the clumped dispersion of adults.
Thus, spatially aggregated seed dispersal had a strong,
persistent effect on the spatial structure of this popula-
tion of V. calophylla.
METHODS
St u d y S i t e
This study was conducted from August 1999 to De-
cember 2001 at Cocha Cashu Biological Station (CCBS)
in Manú National Park, Perú (18,812 km
2
, 11°54′ S,
71°18′ W, elevation c. 400 m). The average annual rain-
fall is c. 2,000 mm, with most precipitation falling be-
tween October and April (Terborgh 1983). This study
was conducted in c. 300 ha of mature oodplain forest
at CCBS. This site has been described in detail in previ-
ous publications (Terborgh 1983; Gentry 1990).
di S p e r S A l S y S t e M
Species of Virola have been a model system for study-
ing seed dispersal (e.g. Howe 1981; Howe et al. 1985;
Forget & Milleron 1991). Virola calophylla is a dioecious,
shade-tolerant, canopy tree in lowland moist forests of
South America (Rodrigues 1980). At CCBS V. calophyl-
la ripens fruit from early to mid-September to Decem-
ber. The fruit of V. calophylla is a bivalved, dark green
capsule that opens upon ripening to expose a single
seed with a bright red, oily aril. Most of the volume of
the diaspore is comprised of the seed (length: 17.0 ± 1.8
mm, n = 98; fresh mass: 1.4 ± 0.5 g, n = 108; ± SD).
At CCBS seeds of V. calophylla are dispersed by at
least 17 bird species and one primate, the spider mon-
key, Ateles paniscus (Russo 2003a). Based on 2 years of
observations quantifying visitation and seed disper-
sal rates, spider monkeys dispersed 92% of dispersed
seeds (Russo 2003a). They ingest up to 104 seeds in a
visit and defecate them intact after gut passage times
that range from c. 2.5 to 18 h (Milton 1981; S.E. Russo,
unpublished data). They are highly frugivorous, for-
age primarily in the canopy and subcanopy, and have
large home ranges (150–230 ha; Symington 1987). Sec-
ondary dispersal of V. calophylla by rodents (Russo, in
press) or dung beetles (Andresen 1994) appears to be
minimal at CCBS.
no n -d i S p e r S e d A n d n A t u r A l l y A n d e x p e r i M e n t A l l y d i S -
p e r S e d S e e d S
A combination of observational and experimental
methods was used to quantify seed deposition pat-
terns and to compare seed survival and germination of
non-dispersed seeds (seeds falling below the parent),
seeds dispersed by spider monkeys, and experimen-
tally dispersed seeds. To characterize seed production,
seed-fall below, and seed dispersal from V. calophylla
females, 10 female trees bearing fruit in the study area
in 2000 were randomly selected. The area of the crown
ning of the initial seed deposition pattern (Augspurger
1983a). Third, the availability and distribution of sites
suitable for establishment, combined with the interac-
tions between a plant’s regeneration requirements and
its environment and other species, can also inuence
the spatial pattern of seedling and sapling recruitment
(Grubb 1977).
Dispersion of vertebrate-dispersed tree species, then,
can be viewed in terms of the balance between disper-
sal processes that aggregate seeds and post-dispersal
processes that alter the initial offspring dispersion pat-
tern through non-random survival (Schupp & Fuent-
es 1995; Schupp 1995). However, the recruitment con-
sequences of natural seed deposition patterns remain
unquantied for all but a handful of the wide variety
of plant–animal disperser systems (e.g. birds, Herrera
et al. 1994; Wenny 2000; tapirs, Fragoso 1997; howler
monkeys, Julliot 1997; rodents, Forget 1990, 1994, For-
get et al. 1999). Despite recent advances (Houle 1992;
Herrera et al. 1994; Nathan et al. 2000; Balcomb & Chap-
man 2003), the extent to which the spatial patterns of
recruitment are determined by the initial seed deposi-
tion pattern remains a fundamental unanswered ques-
tion in plant ecology. Thus, in order to understand
the importance of seed dispersal for plant communi-
ty ecology, we must describe its consequences for later
life stages and link patterns of dispersion among mul-
tiple life stages (Levine & Murrell 2003).
The objectives of this study were to investigate the
development of spatial structure of a vertebrate-dis-
persed, neotropical nutmeg tree, Virola calophylla
(Myristicaceae), and to determine whether dispersion
shifts through time as individuals age. We evaluated
how the spatial pattern of recruitment from the seed
to the adult stage was modied from the initial tem-
plate of seed deposition in V. calophylla growing in ma-
ture oodplain forest in Amazonian Peru. First, obser-
vations documented the spatial pattern of seed depo-
sition. Second, natural and manipulative experiments
quantied spatial variation in post-dispersal seed sur-
vival to the seedling stage. In particular, the strength
of density- and distance-dependent mortality was esti-
mated. Third, patterns of seed deposition and survival
were related to densities of V. calophylla seedlings and
saplings. Finally, the dispersion of juvenile and adult
V. calophylla individuals was quantied and interpret-
ed in light of the spatial structure of earlier life stages
and the strength of density- and distance-dependent
survival.
Our results indicate that a clumped pattern of seed
deposition was generated by the key dispersal agent,
the spider monkey, Ateles paniscus (Platyrrhini). This
clumped pattern was largely maintained through re-
cruitment to the sapling stage, despite substantial
density- and distance-dependent seed mortality, and
1060 ru S S o & Au g S p e r g e r i n Ec o l o g y lE t t E r s (2004) 7
recorded. The distance of each quadrat to the nearest
adult female V. calophylla tree was calculated based on
mapped locations of quadrats and trees.
po S t -d i S p e r S A l S e e d S u r v i v A l A n d S e e d l i n g e S t A b l i S h M e n t
Non-dispersed and naturally and experimentally dis-
persed seeds were censused every 2 wk for 15 months
from September 2000 to December 2001 to estimate
seed survival and germination rates. Preliminary stud-
ies indicated that V. calophylla seeds can germinate and
establish seedlings with two leaves in 13 months. Seeds
were categorized as (1) intact, but not germinated, (2)
removed (seed not found in quadrat), (3) seed present,
but preyed upon, and (4) germinated.
Se e d l i n g , S A p l i n g , A n d A d u l t d e n S i t i e S A n d d i S p e r S i o n
Under each female crown and at each site of naturally
dispersed seeds, seedlings and saplings < 10 cm diam-
eter at breast height (d.b.h.) were censused and their
heights (or d.b.h. for saplings > 2 m tall) measured.
Density of seedlings and saplings was calculated using
the estimated areas of each site (crown projection or
dispersal site). To quantify dispersion of seedlings and
saplings, 13 parallel belt transects 334–419 m in length
were placed in a stratied random design through a
30-ha plot. Twelve transects were 6-m wide, and one
transect was 3-m wide due to proximity of a trail. In
each transect, each V. calophylla seedling and sapling <
10 cm d.b.h. was mapped to the nearest 10 cm and its
height or d.b.h. measured. For each individual, its light
environment (gap or understorey) was assessed qual-
itatively. Gaps were considered areas > c. 20 m
2
with
a canopy height averaging < c. 3 m, as judged by eye.
Seedlings and saplings in these transects provided an
estimate of seedling and sapling density in random lo-
cations. To quantify adult dispersion, all V. calophylla
trees ‡ 10 cm d.b.h. were mapped in the 30-ha plot.
St A t i S t i c A l A n A l y S e S
Statistical analyses focused on seed survival through
seedling establishment. It was not possible to analyse
separately survival of the seed vs. the seedling because
too few seeds survived to germination. Seeds were
considered alive if they were intact or germinating
(categories 1 and 4 above); otherwise, seeds were con-
sidered dead. Because few seeds survived to the end
of the study (see Results), probabilities based on as-
ymptotic tests may be biased. We therefore used exact
methods in two sets of analyses. First, variation in per
capita seed survival among dispersal site types (non-
dispersed, dispersed and experimental site types) was
analyzed using a Fisher’s exact test using SAS PROC
FREQ (The SAS Institute 2000). Differences in surviv-
al probabilities between pairs of site types were esti-
mated using odds ratios, which compare whether the
projection of each tree was estimated based on the area
of an ellipse by measuring four radii of the crown. Be-
neath each tree, 1-m
2
fruit traps (3–12 traps per tree)
were located randomly using methods described in
Russo (2003a). Seed production and dispersal were es-
timated from fruit- and seed-fall into traps as in Rus-
so (2003a). Next to each trap, a quadrat (0.5 × 0.5 m)
was delineated on the ground. At each weekly empty-
ing of traps, no more than 10 seeds from the trap were
coded individually using colored paint and placed in
the quadrat. One seed naturally fallen into the quadrat
and not part of the study was removed for each coded
seed added, which maintained the natural density of
seeds and timing of seed-fall in the quadrat.
Individual spider monkeys that fed in V. calophyl-
la were followed to describe movements and behav-
iors that inuence seed dispersal patterns and to char-
acterize and map the locations where spider monkeys
defecated V. calophylla seeds. When spider monkeys
defecated V. calophylla seeds, the polygon describing
the area receiving freshly defecated seeds was delin-
eated, mapped, and its area estimated using ArcView
geographical information systems software. Within
this boundary, quadrats (0.5 × 0.5 m), were aligned so
that each seed was contained within one quadrat, but
quadrats could contain more than one seed. All fresh-
ly defecated seeds of V. calophylla were counted and
uniquely coded as above.
Seeds were experimentally dispersed to randomly
selected locations in the study area in order to mimic
seed dispersal by birds (hereafter, experimental sites).
Freshly fallen seeds were collected from underneath
multiple fruiting V. calophylla trees distant from the
study area. The arils were manually removed from the
seeds, and damaged seeds were discarded. The intact
seeds from the multiple source trees were bulked, and
those to be experimentally dispersed were selected at
random from the bulked seeds. A random location was
selected for placement of paired quadrats (0.5 × 0.5 m),
each 15-m apart in opposite directions from the ran-
dom location. Into each quadrat, either six seeds (high
density) or one seed (low density) was placed, simulat-
ing locations of seeds regurgitated by birds, for a total
of 132 quadrats. Seeds were uniquely coded as above.
The seeds in quadrats in one pair were all placed on
the same day, but pairs were placed at temporally stag-
gered intervals according to the availability of V. calo-
phylla seeds, mimicking natural dispersal.
For all quadrats, the date that each seed fell, was nat-
urally dispersed, or was placed into a quadrat ranged
from early to late in the V. calophylla population’s
fruiting season (c. 4 months). In each quadrat, the to-
tal numbers of V. calophylla seeds (including both cod-
ed seeds part of the study and uncoded seeds) and of
seeds of other species that were 5 mm or longer were
Ag g r e g A t e d Se e d di S p e r S A l b y Sp i d e r Mo n k e y S li M i t S re c r u i t M e n t t o cl u M p e d pA t t e r n S i n Vi r o l a c a l o p h y l l a 1061
er than the distance to the nearest edge and 1 other-
wise. Condence envelopes (95%) for K(d) were con-
structed by simulating 99 realizations of a complete-
ly spatially random process on the area (or line) con-
taining the original point pattern. Observed values ex-
ceeding the upper envelope indicate clustering, where-
as those falling below the lower envelope indicate reg-
ularity (Ripley 2003).
RESULTS
The 10 focal V. calophylla trees produced a total of 35
835 seeds and dispersed an average of 54% of their
seed crops (range 24–77%). Densities of non-dispersed
V. calophylla seeds under females were high (Figure 1a,
Table 1). Few seeds of species other than V. calophyl-
la were found below females, making the total seed
density there similar to the seed density of V. calophyl-
la (Table 1).
Figure 1. Densities (mean + 1 standard error) of seeds (a) and seed-
lings and saplings (b) of V. calophylla under V. calophylla crowns [n =
10 in (a), n = 14 in (b)], under spider monkeys. sleeping (n = 14) and
in-transit (n = 14) sites, and at experimental [n = 132 in (a)] and ran-
domly located sites [n = 13 in (b)]. In-transit sites refer to seeds dis-
persed diurnally. In (a), density is based onexperimental sites, which
were randomly placed. In (b), density in random sites is based on
random transects. See text for details. Lower-case letters indicate sig-
nicant differences based on the Tukey–Kramer method after a sig-
nicant Kruskal–Wallis test.
probability of an event (in this case survival of a seed)
is the same (not signicantly different from one) for
two groups (Agresti 1990). Odds ratios > 1 indicate
signicantly greater survival in the rst, relative to the
second, group.
The second analysis tested the effects of conspecic
seed density and distance from the nearest V. calophyl-
la female tree on per capita seed survival. For this set,
analysis of deviance using likelihood ratio tests (SAS
PROC GENMOD; The SAS Institute 2000) was used to
determine the best-t main-effects model. Odds ratios
estimated the strength of the effects of density and dis-
tance on survival, corresponding to a unit increase in
the predictor variables. We veried probabilities using
exact logistic regression by Monte Carlo simulation
with 100 replicates, as implemented in LogXact-5 soft-
ware (LogXact-5 for Windows 2002).
The dispersion of adults in the 30-ha plot and of seed-
lings and saplings within the 13 randomly placed
transects was tested for deviations from complete spa-
tial randomness. For adults, we used the standard K
function, which describes the extent to which there is
spatial dependence in the arrangement of events. It is
dened by the relationship λK(d) = E (number of(events
≤ radius d of an arbitrary event)), where E() denotes the
expectation, and λ is the intensity, which is estimated
by the mean number of events per unit area (Ripley
2003). We used an edge-corrected estimator of K(d):
where n is the number of points in region A with area
|A|, d
i,j
is the distance between the ith and jth points,
w
i,j
is the proportion of the circle with the center at i
and passing through j, which lies within A, and Id(d
i,j
)
is an indicator function that is 1 if d
i,j
is ≤ d. Estimates of
K(d) were adjusted using a variance-stabilizing trans-
formation:
For transects, the K-function modied for the one-di-
mensional case was used. The area A was instead a line
L, and λ in this case was estimated by the mean num-
ber of events per unit length. Positions of seedlings and
saplings in transects were collapsed to fall along a line,
and dispersion of seedlings and saplings combined in
each transect was thus analyzed with respect to one-
dimension using the edge-corrected estimator:
where all variables are as above, except c
ij
is 2 when
the distance between the ith and the jth points is great-
![Figure 1. Densities (mean + 1 standard error) of seeds (a) and seedlings and saplings (b) of V. calophylla under V. calophylla crowns [n = 10 in (a), n = 14 in (b)], under spider monkeys. sleeping (n = 14) and in-transit (n = 14) sites, and at experimental [n = 132 in (a)] and randomly located sites [n = 13 in (b)]. In-transit sites refer to seeds dispersed diurnally. In (a), density is based onexperimental sites, which were randomly placed. In (b), density in random sites is based on random transects. See text for details. Lower-case letters indicate significant differences based on the Tukey–Kramer method after a significant Kruskal–Wallis test.](/figures/figure-1-densities-mean-1-standard-error-of-seeds-a-and-3j6i5flc.webp)
