Dispersal vacuum in the seedling recruitment of a primate

Biological Conservation xxx (2013) xxx–xxx
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Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
Dispersal vacuum in the seedling recruitment of a primate-dispersed
Amazonian tree
Taal Levi a,b, Carlos A. Peres c,⇑
a
Cary Institute of Ecosystem Studies, Millbrook, NY 12545, USA
University of Florida, Gainesville, Florida 32611, USA
c
School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich, Norfolk NR4 7TJ, United Kingdom
b
a r t i c l e
i n f o
Article history:
Received 1 October 2012
Received in revised form 27 January 2013
Accepted 8 March 2013
Available online xxxx
Keywords:
Atelinae
Amazonia
Brazil
Endozoochory
Frugivory
Sapotaceae
Seed cleaning
Seedling recruitment
Pathogens
Janzen–Connell
Seed fate
Tropical forest
a b s t r a c t
Unregulated hunting of large-bodied frugivores is ubiquitous in tropical forests. Due to their low fecundity and complex social organization, large primates are often the first tropical forest vertebrates to be
extirpated by hunting. Large primates are important seed dispersers and the only dispersal vectors of
many large-seeded plants, leading to concerns that primate-dispersed trees will succumb to large-scale
recruitment failure wherever they co-occur with overhunting. We used a field experiment in a remote,
nonhunted region of the western Brazilian Amazon to test how the seedling recruitment success of a primate-dispersed Sapotaceae tree (Manilkara bidentata) is affected by distance from parent trees, protection from vertebrate seed predators, and gastro-intestinal seed cleaning associated with passage
through frugivorous vertebrates. Only seed cleaning significantly increased the rate of seedling recruitment. Janzen–Connell effects have been widely purported as the central mechanism for recruitment failure, but our results suggest that for many tropical forest plant species Janzen–Connell effects are a
second-order effect that acts once seeds have been successfully cleaned of fruit pulp by gut treatment.
As an illustration of the relative importance of the sheer quantity of seeds ingested by woolly monkeys
(Lagothrix cana), we further estimate the density and dispersal services provided by a complete primate
assemblage to show that L. cana cleans and disperses nearly one million seeds per km2 per 24-day Manilkara fruiting season, amounting to over 71% of the seed dispersal services provided by the entire primate
assemblage. The disperser vacuum in the absence of L. cana greatly reduces the quantity of cleaned seeds
deposited on the forest floor. For similar fleshy-fruited species where gut passage greatly increases survival, a simple lack of redundancy in seed consumption may be the primary driver of recruitment failure
resulting from large-primate extirpation due to overhunting, with Janzen–Connell effects secondarily
influencing recruitment success as a function of either dispersal distance or seed density.
Ó 2013 Elsevier Ltd. All rights reserved.
1. Introduction
Many harvest-sensitive large-bodied vertebrates are extensively overhunted in tropical forests, resulting in marked population declines if not local extinctions (Milner-Gulland et al., 2003).
Although some harvest-tolerant game species can compensate
for elevated mortality via reproduction and immigration, largebodied primates, such as spider monkeys (Ateles spp.) and woolly
monkeys (Lagothrix spp.) in Amazonian forests, are easily overexploited due to very low fecundity and poor dispersal associated
with complex social structures (Peres, 1990; Peres and Palacios,
2007). These species are typically the first to become locally extirpated near subsistence communities that depend heavily on wild
meat. The local extinction radius away from a community depends
⇑ Corresponding author. Tel.: +44 1603 592549.
E-mail address: [email protected] (C.A. Peres).
on the hunting effort, weapon efficiency, and hunter selectivity
(Jerozolimski and Peres, 2003; Levi et al., 2009, 2011), but can exceed 15 km, corresponding to a circular area >700 km2. When
many communities are distributed over a large area, entire landscapes can become depleted of large-bodied primate populations
(Levi et al., 2011; Sirén et al., 2004).
The landscape-scale loss of large primates has led to concerns
over widespread recruitment failure of the many primate-dispersed trees in tropical forests (Nuñez-Iturri and Howe, 2007; Terborgh et al., 2008). This argument has thus far rested primarily on
the Janzen–Connell model (Connell, 1971; Janzen, 1970), which
states that the per-capita recruitment success of a seed depends
strongly on escape from pathogens and seed predators associated
with conspecific neighborhoods. Without large primates many
large-seeded plants are expected to go undispersed, or dispersed
only a short distance by poor dispersers (Chapman, 1989), which
is expected to lower per-capita seed and seedling survival. This
0006-3207/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.biocon.2013.03.016
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
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T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
effect has been proposed to explain the widely observed paradox of
dense aggregations of fruits and seeds underneath parent trees
that fail to produce seedlings. Recent research supports the important role of Janzen–Connell effects in seedling recruitment (Swamy
et al., 2011; Swamy and Terborgh, 2010), but a previous meta-analysis covering 40 studies failed to detect a general effect of distance
on enhancing seed survival (Hyatt et al., 2003). Other research has
found that the effect of seedling density is equally or more important than the effect of distance from a conspecific in driving seedling recruitment patterns (Clark and Clark, 1984), but recent work
suggests that the seed-rain density of most tropical forest tree species is so low that density dependence is inconsequential to seedling recruitment dynamics except in the immediate vicinity of
conspecific adults (Terborgh et al., 2011). However, many seeds
may be deposited at high density under sleeping or congregating
sites, which may lead to higher mortality if density dependent processes are important (Russo and Augspurger, 2004).
Importantly, Terborgh et al. (2011) sampled the rain of propagules over 6 years at a southwestern Amazonian forest site, but
classified propagules as intact seeds, damaged seeds, seeds with
adhered pulp, ripe fruit, and immature or damaged fruit. They suggested that ‘net’ fecundity, which considers only intact dispersed
seeds, was more biologically relevant to recruitment dynamics
than gross fecundity, which considers all propagules, because virtually no saplings arise from undispersed seeds. Dispersed seeds
were well mixed and randomly distributed at low density throughout the forest. Nearly 90% of seed traps failed to capture intact
seeds each year, suggesting extreme seed limitation. This was further reinforced by a strong positive correlation across species between the spatial distribution of dispersed seeds and the spatial
distribution of saplings.
These results suggest that recruitment outside the immediate
vicinity of a parent tree is most limited by the quantity of dispersed
seeds, rather than post-dispersal forces acting on density or distance (Terborgh et al., 2011). Moreover, survival rates from the seed
to seedling stage (i.e. seedling recruitment) is very low in tropical
forests, representing a critical bottleneck in tree recruitment
(Chambers and MacMahon, 1994). We thus hypothesized that the
effect of distance from maternal trees on seedling recruitment
would be swamped by the effect of seed treatment in the disperser’s
digestive tract. This effect is plausible because mildly abrasive gut
passage removes the perishable exocarp from intact seeds and
cleans the seed testa of the tightly adhered edible fleshy fruit pulp
that can attract agents of mortality, including both pathogens (e.g.
fungi and bacteria) and seed predators (e.g. bruchid beetles and rodents). There is a rich literature in diverse systems suggesting that
germination success is reduced or prevented if seeds remain associated with pulp (Barnea et al., 1991; Izhaki and Safriel, 1990; Rick
and Bowman, 1961; Temple, 1977; Traveset et al., 2001), but this
has received little attention in tropical ecosystems (Dinerstein and
Wemmer, 1988; but see Fragoso et al., 2003) and to our knowledge
no attention in the recruitment failure literature associated with
defaunation. This hypothesis asserts that fruiting plants rely on
the quantitative effect of removal and benign gut passage of many
thousands of seeds on a daily basis by co-occurring populations of
relatively abundant endozoochores. The implication is that intact
seeds trapped inside uneaten fruits falling below fruiting crowns fail
to germinate primarily because they have not been removed from
other fruit parts and cleaned by adequate gut passage rather than
reduced per-capita survival due to proximity to parent plants. For
fruits that require seed cleaning by gut passage for germination,
the conservation implication is that plant recruitment success will
decline more than suggested by Janzen–Connell experiments if
seeds remain unprocessed regardless of dispersal distance.
To test whether large-primate extirpation could lead to seedling
recruitment failure by creating a seed dispersal vacuum, we first
estimated the seed dispersal services provided by a diverse primate guild in a remote and completely undisturbed terra firme forest of western Brazilian Amazonia, and the fraction of those seeds
dispersed by a locally abundant large-primate, the gray woolly
monkey (Lagothrix cana). In this low-productivity interfluvial forest
region, black spider monkeys (Ateles chamek) are restricted to relatively productive seasonally-flooded riparian areas but are absent
from the wider matrix of unflooded (terra firme) forest. We then
used a large field experiment to test how seedling recruitment of
Manilkara bidentata, a fleshy-fruited primate-dispersed canopy tree
in the family Sapotaceae, is impacted by distance from the parent
tree, seed cleaning associated with gut passage, and physical exclusion of vertebrate seed predators. Finally, we used the results of
our experiment to project the seedling density in our study area
with and without the seed dispersal services provided by L. cana,
the dominant endozoochore in this system.
2. Methods
2.1. Study site
The study was conducted in an entirely undisturbed terra firme
forest landscape in the headwaters of the Tefé River (hereafter, Alto
Tefé), State of Amazonas, Brazil (5°200 2800 S, 66°400 3400 W, Fig. 1).
This remote site was isolated by a fluvial distance of 682 km from
the nearest town (Tefé), and had long been depopulated of native
Amazonians and subsequently rarely visited by post-Conquest
hunters and Couma latex tappers since at least the 1850s. The
study area was bounded by a 16-km2 trail grid containing five parallel 4-km transects spaced apart by 1 km. This grid consisted of
mildly dissected terra firme forest (83–138 m asl) where soils are
typically heavily leached and nutrient poor. The study area has a
wet, tropical climate with a mean annual temperature of 27.1 °C
and rainfall—based on daily records over three consecutive years
(2008–2010) at the Bauana Ecological Station (65 km west of the
trail grid)—averaging 3679 mm/yr, with only 4.1% of annual rainfall available in the three driest months (July–September). Due to
low productivity in this interfluvial region, the white-lipped peccary (Tayassu pecari), an important seed predator, was conspicuously absent from this site, but collared peccaries (Pecari tajacu)
were present.
2.2. Line transect census
Forest vertebrate surveys of diurnal primates and other medium and large-bodied vertebrates were conducted over a 3-week
period during the rainy season (January 2012) by a small team of
six previously trained observers, followed by a second visit to the
site during the subsequent dry season (July 2012). Following
line-transect census guidelines of Peres and Cunha (2011),
straight-line transects were cut along a compass bearing, measured with both a Hip-ChainÓ and a Garmin CSx60 GPS, and
marked using brightly colored flagging at 50-m intervals to ensure
adequate mapping resolution of all vertebrate sightings. Preparation of each transect was usually completed within 1 day, and surveys were not conducted within 2 weeks of line cutting. Each of the
five 4-km transects was surveyed at least eight times, resulting in
an aggregate census effort of 301.3 km walked. Analogous linetransect surveys in French Guiana showed that even 40–90 km of
census walks can be sufficient to reliably assess the population
abundance of a similar set of vertebrate species (Thoisy et al.,
2008). Transects were walked in the morning (0630–1000 h) and
in the afternoon (1330–1700 h), when animals are most active.
Surveys were typically conducted by two observers who walked
slowly (1250 m/h) along the transect line, pausing at regular
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
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Fig. 1. (A) Location of the study area in the State of Amazonas, Brazil, showing (B) the position of the 16-km2 trail grid within an entirely undisturbed terra firme forest in the
headwaters of the Tefé River (Alto Tefé; white square). Access to this remote field site was facilitated by helicopter flights. Red polygon in (A) indicates the phytogeographic
boundaries of Amazonia; yellow circle in (B) indicates the market town of Tefé at a downriver fluvial distance of 682 km from the grid. (C) Detail of elevational gradient in the
Alto Tefé region from lower terrain (blue) along igapó forests to higher terrain (red) dominated by moderately dissected terra firme terraces. (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of this article.)
intervals to scan the forest with minimum background noise. Upon
detection of any target species, the location along the transect and
perpendicular distance to the animal sighted were determined,
spending no longer than 10 min per sighting. In case of social species, we also noted the number of animals that were visible near
the transect line, and counted the group size and estimated perpendicular distances to the approximate geometric centers of both
the visible party near the transect and, whenever possible, the entire group. Distances were estimated by highly trained observers
who had worked with CAP for at least 3 years and were very familiar with the forest wildlife in this region.
2.3. Estimation of dispersal services
As an illustration of relative seed dispersal capabilities of the
primate community, we estimated the number of seeds potentially
dispersed by L. cana and other sympatric primates for a primatedispersed canopy tree species, M. bidentata, that is widespread in
central-western Brazilian Amazonia. Individual M. bidentata
typically produces super-abundant fruit crops, each with a single
seed (rarely two seeds), of several thousand fruits during the wet
season every year; globose fruits and their seeds average
21.6 ± 4.3 mm and 15.5 ± 3.2 mm in length and 22.3 ± 4.1 mm
and 10.2 ± 2.3 mm in width, respectively. At our study site, the
population density of adult M. bidentata was estimated at 0.349
trees/ha on the basis of 62.9 ha of forest censused along transects,
assuming a reliable effective detection strip-width of 15 m along
which all adults >35 cm in DBH (which could be clearly distinguished on the basis of bark characters) were identified.
The total stomach content mass of four adult and one subadult
L. cana killed by hunters (mean weight = 8706 ± 1174 g, range =
7400–10,200 g) has been measured at 499 ± 128 g (range = 455–
620 g), and the mean volumetric content of intact seeds in their
digesta represents 58 ± 17% of the total stomach content (Peres,
1994). This leads to an estimate of mean seed mass per digesta
of 289.42 g, which is equivalent to 1158 Manilkara seeds (mean
wet weight of 0.25 g per seed). Based on an intensive 11-month
observational study of L. cana at an undisturbed terra firme forest
site 170-km east of our study area (including L. cana–Manilkara
interactions: Peres, 1996; C.A. Peres, unpubl. data), we assume that
(1) on average three feeding bouts are allocated each day to Manilkara trees during their fruiting season by each L. cana group and
(2) that on average only one third of the satiation-point stomach
capacity of any given individual is allocated to Manilkara fruits during each feeding bout. We estimated the potential per-capita daily
seed removal by L. cana and other primates based on estimates of
population density and allometric body mass scaling (i.e. seed consumption by other primates relative to L. cana scales with body
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
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T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
mass). In sum, the seed consumption estimate for each primate
species is the ratio of body mass to that of L. cana multiplied by
the number of feeding bouts per day, divided by the fraction of
stomach capacity allocated to Manilkara, multiplied by the total
number of Manilkara seeds that can fit into one L. cana digesta.
Our estimates of seed dispersal by L. cana are conservative because we assume that (1) interspecific exploitative and interference competition for fruit resources within Manilkara crowns
play a negligible role when in fact large-group living large-bodied
primates typically dominate fruit patches; (2) on average individual Manilkara trees are equally available to all primate groups
throughout the study area including A. chamek, when in fact this
large-bodied species at this site was largely restricted to seasonally-flooded riparian (igapó) forest where Manilkara trees were absent; (3) all primate species consume Manilkara fruits when
fruiting trees are available; and (4) all primate species ingest all
Manilkara seeds from consumed fruits, and that seeds are passed
intact through their digestive tracts. This assumption overestimates the rate of seed dispersal by some medium and all smallbodied species that are known to spit out (rather than ingest) a
variable proportion of the seeds processed in their mouths (Peres
and Roosmalen, 2002). For example, Ratiarison and Forget (2011)
found that while large primates swallow nearly all Manilkara seeds
in French Guiana, both small-bodied (Saguinus midas) and medium-bodied (Cebus spp.) primates spit out most seeds. To estimate
dispersal services of other sympatric primate species, we additionally assume that their per-capita seed removal rate scales to that of
L. cana based on allometric body mass ratios.
2.4. Seed dispersal experiment
In January 2012, we collected 5280 whole M. bidentata fruits,
each with a single seed, from our study area during the early to
mid fruiting period of this Sapotaceae species. Fruits were collected
before deployment of the experiment and randomized such that
seeds and fruits were not preferentially planted near the parent
tree. We hand-cleaned half of the seeds from those fruits by
extracting all other fruit parts and rinsing the seeds to remove
any residual fruit debris, whereas the other half of whole fruits
were left intact. We planted both hand-cleaned seeds and whole
fruits in a nested design at the neighborhoods of eleven M. bidentata trees that were widely distributed on three 4 km transects
(i.e. proximity to conspecifics was rare and was not detected for
our focal trees). Along each of the four cardinal directions we
established four near sites (i.e. 5 m from the parent tree) and four
far sites (i.e. 30 m from the parent tree). Semi-permeable exclosures of 30 cm in diameter and 50 cm in height were constructed
with 20-gauge chicken wire (1-in. hex mesh) pegged to 70-cm
poles with industrial staples, and subsequently firmly staked to
the ground. These exclosures did not deter invertebrate seed predators but effectively excluded most small and all medium-sized
and large vertebrate seed predators including spiny rats (Proechimys spp.), although small murid rodents may have been able to
breach the exclosure. Within each site we placed four plots, each
with 15 seeds, with the four possible combinations of vertebrate
exclosure and seed cleaning treatments. Thus, within each tree
neighborhood we had a manipulative factorial design consisting
of 480 seeds arranged within the North, South, East, and West replicates, each of which with near/far, protected/unprotected, and
hand-cleaned seed/whole fruit treatments (Fig. 2). We then returned to the site in July 2012 to monitor the seedling recruitment
success of the experimental sites, and counted the number of seeds
and early seedlings surviving after a period of 6 months from
planting.
We modeled the number of seedling recruits counted at each
plot as both (1) independent replicates with a Poisson distributed
generalized linear model using exclosure treatment, distance from
maternal trees, and seed cleaning treatment as main predictors
and (2) with a Poisson distributed mixed effects model (‘nlme’
package in R version 2.15.1) using the tree identity replicate as a
random effect to account for the spatially nested design. We tested
for an effect of exclosure, distance from tree, and seed cleaning
treatment in both regression models.
3. Results
3.1. Disperser abundance
A total of 11 diurnal primate species were observed in the 16km2 study plot during both field campaigns. Night monkeys (Aotus
nigriceps) were also detected in the plot but nocturnal surveys
were not systematically conducted. Woolly monkeys (L. cana) were
the largest and most numerically abundant primate species occurring throughout the entire plot, with an estimated mean density of
35 individuals per km2. This species alone accounted for approximately 71% of total diurnal primate biomass density at this nonhunted forest site (Table 1). The moderately abundant and
medium-bodied brown capuchin monkey (Cebus apella; recently
renamed Sapajus apella (Alfaro et al., 2012)) had the next highest
biomass density on the plot, followed by A. chamek, whose spatial
distribution did not coincide with that of M. bidentata, and then Cebus albifrons. Together, these four taxa accounted for over 90% of
the diurnal primate biomass, even though tamarins (Saguinus mystax and S. fuscicollis) were the second and fourth most abundant
species. Night monkeys at a structurally comparable terra firme
forest in the same interfluvial region had a population density of
9 ind./km2 (Urucu forest: Peres, 1999), and this species was unlikely to occur at much higher densities in the study plot.
3.2. Estimation of seed dispersal services
Using the population density of L. cana at our study site, we estimated the number of seeds potentially dispersed by L. cana alone
per km2 of forest per day to be approximately 40,662. This
amounts to nearly 1 million Manilkara seeds scattered throughout the forest per km2 during the 24-day fruiting season of this
Sapotaceae tree.
L. cana is the second largest-bodied primate, after Ateles, at our
study site. We estimated the potential per-capita daily seed removal of other primates based on allometric body mass scaling.
Using the local densities of diurnal primates and their respective
seed removal rates, we estimated that 71.3% of Manilkara seeds
at our study site are removed by L. cana alone (Fig. 3A). This is a
minimum estimate of the dispersal services provided by L. cana because it does not account for interference and/or exploitative competition excluding smaller-bodied primates, or for the fraction of
partially clean seeds processed by smaller bodied species that
would be spat out close to or underneath fruiting crowns (Peres
and Roosmalen, 2002), or for the more varied diets of smaller-bodied species, which can consume substantial amounts of animal
protein and can destroy seed embryos (Mittermeier and Roosmalen, 1981). While L. cana dominated the quantitative effect of seed
dispersal at this site, in general large-bodied taxa consumed more
seeds per km2 (based on their density and body mass) than did
smaller-bodied species (p = 0.02 on log–log scale, Fig. 3B).
3.3. Seed dispersal experiment
Over the entire experiment, emergent Manilkara seedlings were
recorded in 21 (6%) of the 352 seedling plots. Some plots (each
with 15 fruits or seeds planted) had more than 1 seedling, leading
to a total of 25 seedlings from the 5280 seeds planted (0.47%). All
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
5
Fig. 2. Experimental design of our seed and fruit plots around 11 adult Manilkara trees. The factorial design includes both protected (within exclosures) and unprotected
(exposed) treatments and cleaned seed and whole ripe fruit treatments placed at both near (5 m) and far sites (30 m) from the bole of each focal tree. A total of 15 seeds were
placed at each plot, thereby amounting to 480 seeds per tree.
other seeds that had failed to germinate within 6 months of planting had perished. Near and far plots averaged 0.073 and 0.068
seedling recruits per plot, respectively, which did not amount to
a significant effect in either simple (p = 0.863) or multiple regression models (p = 0.842). Protected and unprotected plots had an
average of 0.08 and 0.06 seedlings, respectively, which was also
not a significant effect in simple (p = 0.599) or multiple regression
models (p = 0.549). In contrast, cleaning of the seed coat significantly increased seedling recruitment in both simple (p = 0.006)
and multiple regression models (p = 0.006), with cleaned seed
treatment plots averaging 0.11 seedlings per plot and whole-fruit
plots averaging only 0.03 seedlings per plot (Fig. 4A). There were
no significant interaction terms, so we present the results of multiple regressions without interaction effects. Detailed physical
examination of residual fruit parts consistently revealed rotten
seeds, suggesting that fungal pathogens had destroyed the embryos, precluding germination of seeds that had not been removed
from their fruits. A total of four of the 176 exclosure plots had been
partially trampled, indicating that large mammals may have been
responsible for some of the seed removal of missing fruits and
seeds. Finally, these effects were consistent with the results from
a mixed-effects model in which tree was treated as a random effect
in the spatially hierarchical design of the dispersal experiment
(Cleaning: p = 0.009; Distance: p = 0.861; Exclosure: p = 0.599 in a
multiple regression). The standard deviation of the random intercept term for the ‘tree’ level was estimated to be 0.038.
4. Discussion
We have proposed that the extirpation of large primates leaves
a disperser vacuum that smaller-bodied species are unable to fill.
In defaunated forests this may operate as the primary demographic
filter prior to seedling recruitment for fleshy fruits that require gut
passage to clean seeds and leave them unapparent on the forest
floor prior to germination. Angiosperms produce seeds that are often encased inside a nutritional reward to incentivize endozoochorous seed dispersal. In a faunally intact forest where largebodied primates (e.g. Lagothrix and Ateles throughout most Amazonian forests) are able to function as primary seed dispersers, a large
fraction of the overall fruit production is consumed and large numbers of seeds are cleaned and repeatedly deposited on the forest
floor. These large-bodied prehensile-tailed primates are high-quality seed vectors for several reasons, as illustrated by an intensive
study of a population of L. cana 170 km east of our study site
(Peres, 1994, 1996). First, the year-round diet of this species includes mostly fleshy fruits from at least 193 tree and liana species,
the mature seeds of which are rarely destroyed in their digestive
tracts (Stevenson, 2011). Second, the germination success of Lagothrix-dispersed seeds range from 72% to 100% for 15 fleshy fruit
species tested, including five Sapotaceae species. Third, a single
moderate-sized group of 44–49 individuals can scatter
23.2 ± 6.8 kg of intact seeds per day across the forest floor. Fourth,
highly elastic groups of up to 70 individuals can be very uncohesive, often dispersed over a mean group diameter of >900 m,
increasing both the number of fruit patches visited and the overall
spatial spread of defecation events. Finally, individual fecal deposits are highly diffuse, with a seed spatial scatter on the ground per
defecation event of 292 ± 149 cm in diameter, usually resulting in
deposition of isolated (rather than clumped) seeds which have an
opportunity to survive at a much larger number of microsites (Bueno et al., 2013).
Any parent tree overcomes dispersal limitation whenever one of
these many viable seeds successfully survives the seedling and
sapling stages and recruits as juveniles into the subcanopy, thereby
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
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T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
Table 1
Population and biomass density of primate species at Alto Tefé, and estimates of the seed dispersal services provided by each species in the primate assemblage for a primatedispersed, fleshy-fruited canopy tree species, Manilkara bidentata.
Primate
species
Body mass
(kg)
Lagothrix cana
Cebus apella
Ateles chamek
Cebus albifrons
Pithecia albicans
Saguinus mystax
Saimiri ustus
Saguinus fuscicollis
Callicebus torquatus
Callicebus cupreus
Alouatta seniculus
6.968
2.328
7.216
2.16
1.76
0.408
0.752
0.312
0.96
0.84
5.23
Total
Biomass density
(kg/km2)
Per-capita seed
removal (seeds/day)
Seeds removed per km2
35.12
12.48
3.80
7.31
4.10
17.51
9.08
12.39
0.75
0.75
0.00
244.74
29.06
27.40
15.79
7.22
7.15
6.83
3.86
0.72
0.63
0.00
1157.68
386.78
1198.88
358.87
292.41
67.79
124.94
51.84
159.50
139.56
868.92
40662.40
4828.24
4552.72
2623.41
1199.17
1187.13
1134.65
642.01
119.32
104.56
0.00
975897.5
115877.9
109265.3
62961.8
28780.1
28491.1
27231.5
15408.3
2863.8
2509.4
0.0
71.27
8.46
7.98
4.60
2.10
2.08
1.99
1.13
0.21
0.18
0.00
103.29
343.40
4807.16
57053.61
1369286.6
100.00
Density
(ind./km2)
evading the heavy mortality filters typical of the early stages of a
plant life cycle (Chambers and MacMahon, 1994). For an unknown
number of taxa, successful gut passage is a first step to survivorship, followed by subsequent drivers of post-dispersal seed and
seedling survival that differ among species (Terborgh et al.,
1993). When large primates are driven to ecological extinction
by overhunting, a disperser vacuum causes most seeds to not only
fail to be dispersed, but to also fail to be adequately cleaned by gut
passage, which for many tree species may be the primary mortality
filter resulting in seedling recruitment failure in defaunated forests. This may occur whenever there is low redundancy in primate
seed dispersal services (Peres and Roosmalen, 2002; Poulsen et al.,
2002). At our study site, we estimated that L. cana alone consumed
and passed intact nearly one million seeds of a single Sapotaceae
tree species per km2 per 24-day fruiting season. This dominant
endozoochore alone conservatively contributed some three-quarters of the overall seed dispersal services provided by any frugivorous vertebrate for this canopy tree species.
Previous research has largely invoked Janzen–Connell effects as
the main driver of recruitment failure in primate-dispersed trees in
overexploited forests (Chapman and Russo, 2006; Swamy et al.,
2011; Terborgh et al., 2008). However, our results suggest that Janzen–Connell effects are not necessary to derive widespread recruitment failure once abundant large primates are extirpated. The
most important factor driving recruitment failure may simply be
that (1) other smaller primate species are unable to fill the quantitative seed consumption vacuum left unattended when high-biomass consumers are extirpated and (2) the vast majority of seeds
are doomed when trapped inside the uneaten parent fruit. However, the importance of seed cleaning by gut passage across taxa
and fruit morphology is still poorly understood.
Our estimates of Manilkara seed dispersal are illustrative of the
seed consumption vacuum remaining when large primates such as
L. cana are extirpated. These estimates relied on several assumptions. First, we assumed that seed consumption by species other
than primates is minimal. This assumption is supported by recent
research showing that primates accounted for all arboreal dispersal
activity in two species of Manilkara, but trumpeters (Psophia crepitans) and coatis (Nasua narica) were also observed eating fallen
fruit under trees (Ratiarison and Forget, 2011). Moreover,
Amazonian Sapotaceae trees are known to be primarily or exclusively primate-dispersed (Juliot, 1996; Simmen and Sabatier,
1996; Spironello, 1999), and Manilkara spp. are no exception.
Second, we conservatively assumed three feeding bouts per day
and that one-third of seed mass in the digesta is allocated to Manilkara (Peres, 1996; C.A. Peres unpubl. data). Actual levels of seed
consumption are variable, but this assumption was applied equally
to all primates, which we argue underestimates the relative impor-
Seeds removed
per km2 per season
Percent
removed
tance of L. cana seed consumption because smaller primates spit
rather than defecate seeds and can be excluded from mast-fruiting
Manilkara trees by larger primates. Additionally, in our experiment
we cleaned seeds of fleshy fruit parts to simulate defecation, but
this does not account for the possibility of any residual fecal material as a subsequent attractant of seed predators. However, fruits of
Manilkara and several other Sapotaceae become available during
the peak rainy season, so that dispersed seeds are rapidly washed
of any fecal residues following deposition. Moreover, an intensive
small-mammal trapping campaign at another 16-km2 forest grid
within 80 km of our study site indicates that echimyid and murid
rodent densities at these low-productivity terra firme forests are
extremely low (M. Santos-Filho and C.A. Peres, unpubl. data), again
suggesting that agents of seed mortality are overwhelmingly
pathogens, rather than seed predators. Given these assumptions,
these results should be seen as illustrative of the seed dispersal
vacuum and the failure of seedling recruitment when fleshy fruit
parts are not removed by gut passage.
Manilkara is a relatively small-seeded genus within the family
Sapotaceae that can also be dispersed by smaller species in the primate assemblages of Amazonia (Peres and Roosmalen, 2002) and
Mesoamerica (Estrada and Coates-Estrada, 1985). Accordingly,
fruits of this species have a relatively soft exocarp to allow smaller
primates to access the fruit and relatively small seeds that can be
ingested intact by smaller primates at our study site. However, tree
taxa that specialize on large primates have large seeds and tough,
indehiscent exocarps. In the absence of large primates, these seeds
can only be released once the exocarp has deteriorated, at which
point the seed may already be doomed to inoculation by microbial
pathogens or predation by granivores. Irrespective of Janzen–Connell effects, plants that require large primate seed dispersal are
likely to succumb to greater recruitment failure simply by the disperser vacuum if mature seeds are not cleaned of their fruit parts
and deposited unapparent on the forest floor. Following this process, the secondary density or distance-dependent Janzen–Connell
effects may further enhance average survival and recruitment rates
of those seeds deposited in much rarified numbers and/or farther
away from conspecifics.
Small changes in seed demography may be very important to
forest dynamics when operating on millions of viable seeds, but
may nevertheless be difficult to detect in experimental manipulations operating on thousands of seeds. Most previous research on
Janzen–Connell effects has been indirect and correlative, but recent
experimental work using a different species of Manilkara in an African forest of the northern Republic of Congo found that successful
seedling recruitment depended more on seed density than on distance from the parent tree (Poulsen et al., 2012). We did not
manipulate seed density, but instead manipulated the cleaning
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
7
Fig. 3. Illustration of the relative dispersal services offered by the primate community. (A) Estimates of the percentage of total seeds removed by each primate disperser at
Alto Tefé for the local Manilkara bidentata population showing the disproportionate importance of Lagothrix cana. (B) The relationship between primate body mass and
relative amount of seed dispersal services as estimated by the density of each primate and allometric scaling of seed consumption based on body mass.
Fig. 4. (A) Seedling recruitment rate per plot from hand-cleaned seeds and seeds left in whole fruits; from seeds near (5 m) and far (30 m) from the maternal tree; and from
seeds in protected (within exclosures) and unprotected (exposed) plots. Dark gray bars indicate treatments expected to yield a higher recruitment rate. Only seed cleaning
significantly increased seedling recruitment rates (p = 0.006). (B) Extrapolated number of seedling recruits associated with gastrointestinal seed cleaning across our 16-km2
study site including (dark gray) and excluding (light gray) fruit consumption services provided by each co-occurring primate species. Loss of fruit consumption and gut
treatment by woolly monkeys (Lagothrix cana) alone is projected to produce nearly 90,000 fewer Manilkara bidentata seedlings per fruiting season over the entire study area.
treatment of the seed testa to simulate gut passage. There is a large
difference in the magnitude of the effect identified in our two studies. Poulsen et al. (2012) found that ‘‘good seed dispersal’’ increased seed survival by 26%, while in our experimental study
four times as many cleaned seeds survived to the seedling stage
than did seeds still embedded within the fruit (Fig. 4A; seedling
recruitment rate of 0.76% for cleaned seeds and 0.19% for seeds
within fruits). We estimate that this would amount to 7448 seedling recruits from the 975,897 seeds cleaned by gut passage and
dispersed by L. cana alone per km2 per fruiting season. Without
the service of gut passage offered by L. cana, this number falls to
only 1862 seedling recruits. Over our 16 km2 study area this
amounts to 89,378 fewer seedlings (or 55.9 fewer seedlings per
ha) resulting from the loss of the gut treatment provided by a single species of large-bodied endozoochore (Fig. 4B).
Plants produce nutritional rewards such as high sugar content
to entice mutualists, but paradoxically those same rewards can
also attract lethal natural enemies to the otherwise viable seed embryo. If mutualists fail to consume edible fruit parts, these same
attractive fruit parts become a net cost to the seed because ripe
fruit attracts natural enemies such as fungal pathogens, bruchid
beetles, and vertebrate seed predators. The large expected decline
in the seedling abundance of primate-dispersed plants in the absence of L. cana arises principally because a lack of adequate gut
treatment fails to remove the fruit pulp from the seed testa, subsequently attracting agents of mortality regardless of where seeds
Please cite this article in press as: Levi, T., Peres, C.A. Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree. Biol. Conserv.
(2013), http://dx.doi.org/10.1016/j.biocon.2013.03.016
8
T. Levi, C.A. Peres / Biological Conservation xxx (2013) xxx–xxx
are deposited. This simple mechanism clearly swamped the effect
of semi-permeable exclosures and of distance from the parent tree
and is considerably larger in magnitude than the seed density effect quantified in Poulsen et al.’s (2012) seed augmentation experiment. While more complex dynamics are important to understand
the maintenance of tropical forest plant diversity and structure, the
recruitment failure of primate-dispersed trees in defaunated areas
may be primarily due to massive seed mortality associated with
the absence of seed cleaning services induced by gut passage when
keystone frugivores are extirpated.
Acknowledgements
Logistical and material support for the field work, including
helicopter flights to the remote Alto Tefé forest site was provided
by HRT Oil and Gas under a cooperative agreement with CAP. We
wish to thank Ricardo Mello and Felipe Ramos for their competent
assistance. Additional funding was provided by NSF GRF, NSF PRFB,
and Cota-Robles fellowships to TL, and a Brazilian Ministry of Education (CAPES) grant to CAP. Earlier versions of this manuscript
benefited from comments from J. Terborgh, M. Galetti and four
anonymous reviewers.
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