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RESEARCH ARTICLE
Limited directed seed dispersal in the canopy
as one of the determinants of the low hemi-
epiphytic figs’ recruitments in Bornean
rainforests
Miyabi NakabayashiID
1¤
*, Yoichi Inoue
2
, Abdul Hamid Ahmad
3
, Masako Izawa
4
1Graduate School of Engineering and Science, University of the Ryukyus, Senbaru, Nishihara, Okinawa,
Japan, 2The School of Arts and Sciences, The University of Tokyo, Komaba, Tokyo, Japan, 3Institute for
Tropical Biology and Conservation, Universiti Malaysia Sabah, Jalan UMS, Kota Kinabalu, Sabah, Malaysia,
4Faculty of Science, University of the Ryukyus, Senbaru, Nishihara, Okinawa, Japan
¤Current address: Graduate School for International Development and Cooperation, Hiroshima University,
Kagamiyama, Higashi-Hiroshima, Hiroshima, Japan
*miyabi.nakabayashi@gmail.com
Abstract
Ficus species are keystone plants in tropical rainforests, and hemi-epiphytic figs play a nota-
bly important role in forest ecosystems. Because hemi-epiphytic figs have strict germination
requirements, germination and establishment stages regulate their populations. Despite the
ecological importance of hemi-epiphytic figs in the rainforests, seed dispersal systems by
fig-eating animals under natural conditions remain unknown because of the difficulty in trac-
ing the destiny of dispersed seeds in the canopy. Therefore, seed dispersal effectiveness
(SDE) has never been evaluated for hemi-epiphytic figs. We evaluated the SDE of hemi-epi-
phytic figs using qualitative and quantitative components by three relatively large-sized (>3
kg) arboreal and volant animals in Bornean rainforests that largely depend on fig fruits in
their diets: binturongs Arctictis binturong, Mueller’s gibbons Hylobates muelleri, and hel-
meted hornbills Rhinoplax vigil. The SDE values of binturongs was by far the highest among
the three study animals. Meanwhile, successful seed dispersal of hemi-epiphytic figs by gib-
bons and helmeted hornbills is aleatory and rare. Given that seed deposition determines the
fate of hemi-epiphytic figs, the defecatory habits of binturongs, depositing feces on specific
microsites in the canopy, is the most reliable dispersal method, compared to scattering
feces from the air or upper canopy. We showed that reliable directed dispersal of hemi-epi-
phytic figs occurs in high and uneven canopy of Bornean rainforests. This type of dispersal
is limited to specific animal species, and therefore it may become one of the main factors
regulating low-success hemi-epiphytic fig recruitment in Bornean rainforests.
PLOS ONE | https://doi.org/10.1371/journal.pone.0217590 June 13, 2019 1 / 17
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OPEN ACCESS
Citation: Nakabayashi M, Inoue Y, Ahmad AH,
Izawa M (2019) Limited directed seed dispersal in
the canopy as one of the determinants of the low
hemi-epiphytic figs’ recruitments in Bornean
rainforests. PLoS ONE 14(6): e0217590. https://
doi.org/10.1371/journal.pone.0217590
Editor: Kim R. McConkey, University of
Nottingham Malaysia Campus, MALAYSIA
Received: January 18, 2019
Accepted: May 14, 2019
Published: June 13, 2019
Copyright: ©2019 Nakabayashi et al. This is an
open access article distributed under the terms of
the Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This work was supported by JSPS Core-
to-Core Program A. Advanced Research Networks
to MN, JSPS Grants-in-Aid for JSPS Research
Fellow to MN (#25597, #201608680), Grants-in-
Aid of The Inui Memorial Trust for Research on
Animal Science to MN, and The Shikata Memorial
Trust for Nature Conservation to MN. The funders
had no role in study design, data collection and
Introduction
Ficus (Moraceae) is one of the world’s largest woody plant genera with approximately 750 spe-
cies of various growth forms: trees, shrubs, climbers, epiphytes, and hemi-epiphytes [1]. Ficus
species are distributed pantropically, but the majority are found in Malesia and Australia [2].
Each individual produces ripe fig fruits asynchronously and aseasonally; therefore, each fig
population exhibits continual fruiting throughout the year [3]. This fruiting pattern enables
obligate pollination mutualism with wasps (Agaonidae) by maintaining the pollinating wasp
population [4]. Moreover, because of their year-round fruiting patterns, Ficus species are con-
sidered keystone food resources for animals in tropical rainforests, especially when the avail-
ability of preferred fruits is low [3,5–7]. Although this usually applies to whole Ficus
communities, Ficus species vary considerably in reproductive system, growth form, frugivore
guild (e.g. generalist and specialist), and habitat [6]. Among the Ficus species, hemi-epiphytes
include approximately 300 species [1] and occupy one-third to over one-half of the fig species
in the rainforest community [8]. They are a major component of canopy ecosystems across
tropical regions [9], and they increase population turnover and forest regeneration by causing
host tree-fall [10]. Therefore, hemi-epiphytic figs play a notably important role in forest
ecosystems.
Hemi-epiphytic figs germinate in the canopies of host trees as epiphytes [11]. After the
seedlings become established, they descend aerial roots to the forest floor to anchor themselves
around the host trees for additional physical support and to utilize soil water [12,13]. This is
the hemi-epiphytic stage, and some species called “strangler figs” kill their host trees by stran-
gling their trunk and finally, standing alone [11]. Thus, their seeds must be dispersed in the
canopies of host trees and only arboreal and volant animals can be their potential seed dispers-
ers. Seeds of hemi-epiphytic figs need to be dispersed in the host tree’s crown, but not every-
where in the crown. Several studies have indicated that a consistently moist condition is a
primary requisite for germination, rather than light level [14–16], and the water retention abil-
ity of substrates at germination sites is the most important germination factor [15]. Common
germination sites are tree forks, knotholes, axils of large branches, and broken or decomposed
parts of the host trees [13,15,17,18], where suitable substrates are usually found. Due to the
strict germination requirements, the epiphytic stage regulates hemi-epiphytic fig populations
[19]. Therefore, defecation habits and behavior of seed dispersers directly affect their seed
fates.
Ficus species are typical endozoochoric plants whose seeds are dispersed internally by frugi-
vores. The germination rates of these seeds usually increase after being passed through animal
digestive tracts, by separating pulp from fruits and seed scarification [20]. Additionally, fecal
materials fertilize seedlings [20]. Some animals eat, destroy, or drop seeds beneath the mater-
nal trees [21], but fig seed is too tiny to destroy, and most fig-eating animals can disperse its
seeds [6,22]. However, the density of hemi-epiphytic figs is extraordinarily low [8], and there
are many possible germination sites unsaturated in Bornean rainforests [8,23]. This indicates
that most fig-eating animals may not disperse hemi-epiphytic fig seeds effectively.
Seed dispersal effectiveness (SDE) is the number of new adult plants produced by the activi-
ties of each seed disperser, and it is evaluated by both qualitative and quantitative components
[24]. Quantity is the number of seeds dispersed, and quality is the probability that a dispersed
seed produces a recruit. Quality is usually affected by the treatment of seeds in the mouth and
gut and the seed deposition by the disperser [24]. Despite the ecological importance of hemi-
epiphytic figs in the rainforests, seed dispersal systems by fig-eating animals under natural
conditions remain unknown because of the difficulty in tracing the destiny of dispersed seeds
in the canopy. Therefore, SDE has never been evaluated for hemi-epiphytic figs. In this study,
Seed dispersal of hemi-epiphytic figs
PLOS ONE | https://doi.org/10.1371/journal.pone.0217590 June 13, 2019 2 / 17
analysis, decision to publish, or preparation of the
manuscript.
Competing interests: The authors have declared
that no competing interests exist.
we evaluated the SDE of potential seed dispersal agents of hemi-epiphytic figs on Borneo in
terms of both quantity and quality. For the evaluation of quantity, we used two Ficus species,
and for quality, we focused on several Ficus species. We also estimated seed dispersal distance
of animal species. We selected three relatively large-sized (>3 kg) arboreal and volant animals
with over 50% of their diets consisting of fig fruits, to reduce the bias of fig consumption.
Thus, we investigated binturongs Arctictis binturong, Mueller’s gibbons Hylobates muelleri,
and helmeted hornbills Rhinoplax vigil as seed dispersal agents of hemi-epiphytic figs in Bor-
nean lowland mixed dipterocarp forests.
Material and methods
Permission to conduct the research was granted by the Sabah Biodiversity Centre of Sabah
State Government. We were granted permission to capture and attach radio-collars to bintur-
ongs by the Sabah Biodiversity Council and the Sabah Wildlife Department (permission num-
ber: JKM/MBS.1000-2/2 JLD.4 (170), JKM/MBS.1000-2/2 JLD.5 (137), JKM/MBS.1000-2/2
JLD.7 (64)). Trapping and handling of the animals conformed to guidelines of the American
Society of Mammalogists [25]. Research on gibbons and helmeted hornbills was non-invasive
and involved direct observations. We kept certain distance from the animals so as not to dis-
turb their behaviors.
Study sites
We conducted this study at Danum Valley Conservation Area (Danum) and Maliau Basin
Conservation Area (Maliau) in Sabah, north-eastern Borneo, from January 2013 to May 2014,
and from February 2016 to June 2018, respectively. Danum (4˚57´N, 117˚48´E) is a 438 km
2
protected zone, and 90% of this area consists of mature lowland evergreen dipterocarp forest
[26]. Maliau (4˚490N, 116˚540E) is a 588 km
2
protected zone. The study area was outside the
basin in a selectively logged dipterocarp forest [27].
Study animal species
Binturongs are the largest arboreal frugivorous carnivorans on Borneo. They weigh 6–10 kg
[28] and fig fruits constitute nearly 90% of their diet [29]. Mueller’s gibbons are highly arboreal
primates weighing 5–6.4 kg [28]. Fig fruits account for 1–56% of their diet, depending on the
availability of other foods [30]. Helmeted hornbills are the largest hornbill species on Borneo;
they weigh 2.6–3.1 kg [31] and nearly 100% of their diet constitutes fig fruits [32].
Seed dispersal effectiveness
We calculated the SDE values of the three species and visualized them by SDE landscape [24].
The SDE landscape is a two-dimensional representation of the quantity and quality compo-
nents. Because fig fruits include tiny and numerous seeds, we estimated number of fig seeds
ingested by each species per day as the quantitative component. We assessed qualitative effec-
tiveness based on germination rate and defecation microsite. Because we could not trace the
post-germination destiny of dispersed seeds by the study animals, we used only defecation
microsite data to estimate the one-year seedling survival rate as the qualitative component. To
calculate the SDE value, we multiplied the estimated number of ingested fig seeds by each ani-
mal species by the estimated one-year survival probability.
Seed dispersal of hemi-epiphytic figs
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Quantitative component
First, we estimated the number of consumed fig fruits by observing the study animals feeding
on hemi-epiphytic Ficus species (Ficus benjamina in Danum and F.kerkhovenii in Maliau) fol-
lowing the method of [33]. The relative fruit abundance in both periods was low. Visitation
length was defined as the time interval between entry and exit for each individual of the three
animal species during each visit, and feeding speed was recorded as the time spent to eat a fig
fruit while the focal animal continuously consumed more than five fruits on the same branch
with a precision of 0.1 s. We divided the mean visitation length by the mean feeding speed
(time spent to eat a fig fruit) to estimate the total number of fig fruits eaten by each species per
day. Then we estimated the ingested seed number by multiplying the mean seed number
included in a fig fruit by the estimated total number of consumed fig fruits. These values were
used as the quantitative component for evaluation of the total SDE.
At the Maliau site, we recorded only visitation length for binturongs because of the diffi-
culty in observing feeding speed at night. The sample size for feeding speed and visitation
length at each patch was too small for statistical analysis; thus, we pooled data from the two
sites to estimate the probability of fig fruits consumed by each species after we confirmed that
there were no significant differences in feeding speeds between the two sites (no data for bin-
turongs at Maliau, Mueller’s gibbon p = 0.80, and helmeted hornbill p = 0.97). The crop and
fig fruit sizes of these patches were similar; therefore, the effect of pooling the data was small.
Then, for the quantity component, we multiplied the mean seed number per fruit of the
two hemi-epiphytic species, 148.7 [34], by the estimated number of consumed fig fruits by
each animal species.
Qualitative components
Germination rates. To test the effect of gut passage on seed germination, we planted defe-
cated and control seeds derived from the same trees, as inferred from the average gut passage
time. Because of the difficulties in determining the mother trees of ingested seeds, we included
other growth forms besides hemi-epiphytes for analyses. We could not determine the mother
trees of ingested seeds in gibbon feces, so we used data from a previous study [35] on hybrid
Mueller’s gibbons (Hylobates muelleri ×agilis). We planted fig seeds of three species collected
from binturong feces (hemi-epiphytes F.forstenii (two individuals) and F.stupenda, and
climber F.punctata) and two species collected from helmeted hornbill feces (hemi-epiphyte F.
benjamina and climber F.trichocarpa). For hybrid Mueller’s gibbons, we referred to data for
four hemi-epiphytes (F.crassiramea,F.kerkhovenii,F.sumatrana,F.stupenda) and a climber
(F.sinuata) from the previous study [35]. It was not practicable to collect feces from all three
study animals that fed in the same trees. We extracted 100 seeds from the feces or figs and
placed them in plastic nursery bags filled with forest soil within six hours of collection. We
recorded germination weekly for eight weeks. We assessed the effect of gut passage on germi-
nation rates using Fisher’s exact test.
Seed dispersal microsites. We located the microsites where we found feces of the study
animals by individually tracking them after they left the feeding patches or when we found
them by chance. Because of the nocturnality of binturongs, we radio-tagged three [29] and
recorded their seed dispersal microsites at their feeding and sleeping sites by following them.
We also recorded defecation microsites of non-radio-tagged binturongs at their feeding and
sleeping sites. We used the single-rope technique to access the defecation sites in the canopy
[36]. The microsites were classified into five categories: tree fork, branch, epiphytic mat,
foliage, and forest floor. We attempted to record survival of the dispersed seeds at each site,
but all died out or became inaccessible during the study period. Therefore, we used seedling
Seed dispersal of hemi-epiphytic figs
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survival rates per microsite after one year, based on [15]. The one-year seedling survival rates
in tree forks, epiphyte clumps, branches, and knotholes were 3.7, 7.6, 4.7, and 13.9%, respec-
tively [15]. We assumed that not all seeds deposited on the forest floor and foliage would sur-
vive because the germination conditions were unsuitable, or rains washed the seeds away to
the forest floor [23]. The zero value for the survival rate was substituted with 0.03% to mini-
mize the Type I error [37]. We calculated the frequency of finding feces at each microsite and
estimated the seedling survival rate per study animal by multiplying the one-year seedling sur-
vival rate at each microsite. These values were used as the qualitative component for the evalu-
ation of SDE.
We recorded establishment microsites of hemi-epiphytic fig saplings to evaluate resem-
blance between sapling position and seed dispersal microsite per study animal. We calculated
the Bray-Curtis dissimilarity index among microsites. Then, we used these indices to ordinate
the units by non-metric multidimensional scaling (NMDS) using package “vegan” in R version
3.4.3 [38].
Dispersal distance
We estimated the seed dispersal kernels [39] per study animal by combining the distance of
animals from the origin at each hour and seed deposition time. The moving distance of ani-
mals at each hour was based on direct following of binturongs by radio-tracking (see [29])
and gibbons (S1 Table) in the study areas. Because of the small number of successful follow-
ings of helmeted hornbills from the feeding to defecation sites, we used hourly movement
data of a similarly sized hornbill, great hornbill Buceros bicornis, in a mosaic of seasonally
evergreen forest and grassland in Thailand (S1 Table) [40]. We fitted the seed deposition
times with the Gamma distribution, which was based on the mean and variance of empirical
gut retention time data of a hybrid Mueller’s gibbon (Hylobates muelleri × agilis) [35] and
binturongs [41] (S1 Table). For helmeted hornbills, we used data of a similarly sized Sulaw-
esi’s hornbill species, knobbed hornbill Rhyticeros cassidix [42] (S1 Table). We randomly
drew moving distance and seed deposition times for 1000 repetitions to estimate dispersal
kernels.
Results
Quantitative component
We conducted comprehensive field observations at two hemi-epiphytic fig patches: F.benja-
mina at Danum for six continuous days, totaling 108 hours [33] and F.kerkhovenii at Maliau
for four continuous days, totaling 56 hours. In both patches, binturongs, Mueller’s gibbons,
and helmeted hornbills fed on whole fig fruits, while several consumers, such as long-tailed
macaques, pigeons, squirrels, and barbets often partially consumed fig fruits. The mean visita-
tion length (minutes ±standard deviation) per day for binturongs, gibbons, and helmeted
hornbills was 207.2 ±71.6 (n = 9), 47.5 ±12.7 (n = 4), and 6.0 ±3.4 (n = 5), respectively. The
mean feeding speed (seconds/fig fruit) of binturongs, gibbons, and helmeted hornbills was
11.69 ±10.91 (n = 5), 9.21 ±4.64 (n = 8), and 6.19 ±2.81 (n = 5), respectively; the estimated
number of fig fruits consumed in a fig patch per day was 1063.47, 309.45, and 58.16, respec-
tively; and the estimated ingested seed number in a fig patch per day was 132640.4, 31554.1,
and 8713.8, respectively (Fig 1). Binturongs ingested substantially more fig seeds in the same
trees than gibbons and helmeted hornbills.
Seed dispersal of hemi-epiphytic figs
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Qualitative component
Germination rates. The germination rates of all species except F.stupenda were signifi-
cantly higher after being defecated by binturongs (all p <0.01, Table 1). Ficus benjamina seeds
showed a reduced germination rate after being defecated by a helmeted hornbill (p <0.01),
but that of F.trichocarpa was higher than the control (p <0.01). All the fig species germinated
significantly faster after being defecated by both animals (Table 1).
Fig 1. Estimated number of ingested fig seeds per day (1a), visitation length (1b), and feeding speed (1c) of binturongs, Mueller’s gibbons, and helmeted
hornbills.
https://doi.org/10.1371/journal.pone.0217590.g001
Seed dispersal of hemi-epiphytic figs
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Seed dispersal microsites. We located 37, 56, and 17 seed dispersal microsites for bintur-
ongs, Mueller’s gibbons, and helmeted hornbills, respectively. Binturongs disproportionally
defecated in the canopy: tree forks (47.2%), branches (30.6%), epiphytic mats (19.4%), and for-
est floor (2.8%). The estimated one-year seedling survival rates (%) at each microsite were
0.017, 0.014, 0.015, and 0.0003, respectively. Most gibbon feces were found on the forest floor
(96.4%) and on foliage in the understory (3.6%). The estimated one-year seedling survival rate
of both sites was 0.0003. Helmeted hornbill feces were deposited on the forest floor (58.8%),
understory foliage (29.4%), and branches (11.8%). The estimated one-year seedling survival
rates at each site were 0.0003, 0.0003, 0.014, respectively. All three study animals defecated in
the canopy level, but only binturongs deposited their feces on microsites in the canopy. They
defecated on relatively flat tree surfaces, such as tree forks, large epiphytes, and large branches;
and they often rubbed their feces onto the surface of the defecation sites. Gibbons and hel-
meted hornbills let the feces drop down from the canopy.
Most hemi-epiphytic fig saplings (n = 45) were encountered on tree forks (73.3%), followed
by branches (22.2%), knotholes (2.3%), and epiphytic mats (2.3%). The NMDS ordination
showed that binturong dispersal microsites coincided with fig establishment sites; and gibbon
and hornbill dispersal microsites were neither similar to fig establishment sites nor to each
other (Fig 2). The stress value of the NMDS ordination was <0.01.
Seed dispersal effectiveness
The SDE values of binturongs at each dispersal microsite—tree fork, branch, epiphytic mat,
and forest floor—were 2317.5, 1904.9, 1960.1, and 3.9, respectively. Those of Mueller’s gibbons
at foliage and forest floor were 0.9 and 0.9, respectively, and those of helmeted hornbills at
branch, foliage, and forest floor were 120.5, 0.3, and 0.3, respectively. The total SDE values dif-
fered considerably per study animal and seed dispersal microsite (Fig 3). The binturongs’ effec-
tiveness was the highest among the study animals when they defecated at tree forks, branches,
and epiphytic mats. Although the SDE values of helmeted hornbills were low, the qualitative
effectiveness was high when their feces stuck to branches. The SDE of the three species showed
the same value when they dispersed seeds on the forest floor and foliage.
Table 1. Germination tests for the ingested and control seeds.
Study Animals Ficus species Life form
a
Germination rate (%) Effect
(p-value)
b
Days to germination
ingested control ingested control
Binturong F.forstenii1 H 70 47 + (<0.01) 5 6
F.forstenii2 H 43 15 + (<0.01) – –
F.punctata C 53 2 + (<0.01) 4 17
F.stupenda H 19 30 n.s. 3 5
Gibbon (Hylobates muelleri ×agilis)
data from [35]
F.crassiramea H 0 0.3 n.s. – –
F.kerkhoevenii H 22 0 + 1 –
F.sinuata C 93 17 + 5 13
F.sumatrana H 47 0 + 3 –
F.stupenda H 43 11 + 4 4
Helmeted hornbill F.benjamina H 11 46 - (<0.01) 8 10
F.trichocarpa C 14 2 + (<0.01) 9 21
a
H: hemi-epiphyte, C: climber
b
whether animals enhance (+) or hinder (–) germination of each Ficus species
https://doi.org/10.1371/journal.pone.0217590.t001
Seed dispersal of hemi-epiphytic figs
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Dispersal distance
Seed dispersal kernels generated by binturongs ranged from 0 to 6105.3 m, with a mean dis-
tance of 342.7 ±505.5 m (mean ±standard deviation). Approximately 16.3% of ingested seeds
will be dispersed within 10 m of the parent trees, and 44.1% and 9.1% of the seeds would be
dispersed within 100 m and more than 1 km, respectively (Fig 4). Seed dispersal kernels gener-
ated by Mueller’s gibbons ranged from 20.3 to 1893.2 m, with a mean distance of 338.8 ±197.2
m. They would disperse all ingested seeds more than 10 m from the parent trees, and 5.6% and
0.8% of seeds would be dispersed within 100 m and more than 1 km, respectively (Fig 4). That
of helmeted hornbills ranged from 0.9 to 10,707.6 m, with a mean distance of 1611.8 ±1569.1
m. They would disperse 0.44% of the ingested seeds within 10 m from the parent trees, and
5.4% and 53.3% of the seeds would be dispersed within 100 m and more than 1 km, respec-
tively (Fig 4).
Fig 2. Non-metric multidimensional scaling (NMDS) ordination of microsites generated by binturongs, Mueller’s gibbons, helmeted
hornbills, and hemi-epiphytic fig saplings.
https://doi.org/10.1371/journal.pone.0217590.g002
Seed dispersal of hemi-epiphytic figs
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Discussion
Quantity
The number of fig seeds ingested in the same patch differed considerably among the three fru-
givorous species. Binturongs consumed by far the largest number of fig fruits in the feeding
patch followed by Mueller’s gibbons and helmeted hornbills. However, this does not indicate
that a binturong is a quantitatively effective seed disperser at the population level of Ficus
Fig 3. The total seed dispersal effectiveness (SDE) of binturongs, Mueller’s gibbons, and helmeted hornbills across their defecation microsites, per
quantitative (estimated number of ingested seeds per day) and qualitative (estimated one-year seedling survival rate based on defecation microsite data)
components. The elevational contours depict the isoclines of SDE. The numbers on the apex of each isocline indicate SDE values. SDE values to the right and
above have greater effectiveness.
https://doi.org/10.1371/journal.pone.0217590.g003
Seed dispersal of hemi-epiphytic figs
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species because it tends to stay for a long time at a single feeding patch [29]. At the individual
fig level, binturongs had more opportunities than the other two species to disperse hemi-epi-
phytic fig seeds. At the fig population level, animals feeding at several fig patches in a day, such
as gibbons and hornbills (M Nakabayashi, pers. obs. and [42]) would contribute more than
those, such as binturongs, that visited a few patches in a day.
Quality
Germination rate. Given that all three animal species ejected viable seeds to an extent,
gut passage by the three animal species did not adversely affect seed germination. A previous
study reported rapid and high germination of a hemi-epiphytic species Ficus benghalensis after
passing through the bird digestive tract [43]. However, the benefit of gut passage for hemi-epi-
phytic figs in our results was variable among the Ficus species and probably individuals, and it
is unclear compared to that for climber species (Table 1). This study used relatively large
Fig 4. Seed dispersal kernels of binturongs, Mueller’s gibbons, and helmeted hornbills. Asterisks represent the mean values.
https://doi.org/10.1371/journal.pone.0217590.g004
Seed dispersal of hemi-epiphytic figs
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animals, so gut passage may have a different effect than with smaller birds. The obvious posi-
tive effect of gut passage on climbers might be attributed to their growth pattern. Generally,
tested climber figs germinate and establish on the forest floor [44], and they need to climb tall
trees and get to the high-light canopy rapidly [45]. Therefore, the rapid and high germination
of ingested seeds are beneficial for their survival and growth. However, these benefits might
not be useful for hemi-epiphytic figs if ingested seeds hit unsuitable sites. Therefore, the most
beneficial point of ingestion for the seeds of hemi-epiphytic figs could be the existence of viable
seeds, rather than high and rapid germination. Ingestion by all three animal species fulfils this
requirement.
Dispersal microsite. This is the most decisive component of survival for hemi-epiphytic
figs [19]. Of the dispersed microsites generated by the three animal species, only tree forks, epi-
phyte clumps, and branches are potential establishment microsites [15]. Our results show that
binturongs disperse fig seeds into suitable establishment sites for hemi-epiphytic figs. Bintur-
ongs have difficulty in digesting fruits efficiently because of their morpho-physiological con-
straints [41,46]: their feces are watery, making it easier to stick to tree bark. The reason for the
binturongs’ defecatory habits is unclear; however, given that seed deposition determines the
fate of hemi-epiphytic figs, these habits are notably beneficial for fig survival. Binturongs feed
at various heights, from the understory to upper canopy strata [47], distributing seeds to all
canopy layers. Moreover, they frequently rest on large and relatively horizontal branches of
dipterocarps (M Nakabayashi, pers. obs. and [48]), which are the major host plants of hemi-
epiphytic figs on Borneo [8]. These behaviors largely contribute to an increased probability of
establishment success.
To date, reliable directed dispersal of hemi-epiphytic figs has not been thought to occur in
Bornean rainforests [23], but the present study shows that it occurs via binturongs. Despite
their high reproductivity and many potential seed dispersal agents [6], only 0.01% of seeds are
dispersed in suitable sites [23] and 1.3% of seedlings will survive to one year [15]. This rate is
strikingly lower than that of non-hemi-epiphytic figs [49], even though hemi-epiphytic figs are
tolerant to severe conditions, such as water shortage, compared to non-hemi-epiphytic figs
[50]. One of the reasons for its low successful dispersal could be the difficulty in seed dispersal
in mature Bornean rainforests with developed forest strata [51]. The opportunity of seeds to
reach specific microsites for establishment in vertically stratified forests is likely much lower
than in forests with less developed canopy structures. In the uneven canopy of Bornean rain-
forests, defecating directly at the establishment sites is the most reliable dispersal method,
compared to scattering feces from the air or upper canopy. Hemi-epiphytic fig species account
for over 70% of the Ficus species that binturongs feed on in Bornean rainforests [29]. There-
fore, eventually binturong behaviors lead to directed seed dispersal [52] of hemi-epiphytic figs.
Total SDE
In the present study, only three large frugivorous animals were assessed for their effectiveness
as seed dispersers of hemi-epiphytic figs. Among them, binturongs were the most effective dis-
perser in both quality and quantity. We focused on different hemi-epiphytic Ficus species for
quantity and quality evaluations, but these species are in the same subsection of the same sub-
genus [1] and have almost same seed sizes [M Nakabayashi unpubl. data]. Therefore, the effect
of gut treatment on germination for different Ficus species would be small. Although bintur-
ongs and Mueller’s gibbons were more quantitatively effective than helmeted hornbills, the
total SDE was the same when they defecated at unsuitable sites. Although helmeted hornbills
were not quantitatively effective when compared to the other two species, the total SDE
increased when the ingested seeds hit suitable microsites. These results indicate that quality is
Seed dispersal of hemi-epiphytic figs
PLOS ONE | https://doi.org/10.1371/journal.pone.0217590 June 13, 2019 11 / 17
more critical than quantity for hemi-epiphytic figs. The degree of effects of quality and quan-
tity components on total SDE differs with seed dispersers, plants, environment, and also meth-
odology [53,54]. In other areas and other plants, dispersers usually have higher effectiveness
either quantitatively or qualitatively [53,54], whereas binturongs showed high values in both
components. The seed deposition microsite is the most critical factor for survival of hemi-epi-
phytic figs, so total SDE was biased toward quality.
Dispersal distance
All three animal species potentially disperse seeds beyond the tree crowns. Given that mechan-
ical seed dispersal distance is generally within 10 m of the tree [55], Mueller’s gibbons and hel-
meted hornbills provide higher opportunities for long distance dispersal—over 100 m—than
binturongs. The former two species showed similar dispersal patterns as they rarely dispersed
seeds within 100 m, but almost no ingested seeds of Mueller’s gibbons were dispersed over 1
km, whereas over 50% of those of helmeted hornbills were. Because binturongs frequently rest
at the feeding sites [29], some of the dispersed seeds accumulate in the same places (M Naka-
bayashi, pers. obs.) and 16% of seeds are dispersed within 10 m of the parent trees. However,
they frequently change feeding and rest sites [29,56], thus scattering these seeds across their
ranges and 55% of seeds are dispersed over 100m. Mueller’s gibbons and helmeted hornbills
dispersed seeds over 100 m with higher probability than binturongs, and helmeted hornbills
were the only reliable dispersers of over 1 km among the three species.
Generally, longer distance dispersal is exhibited by animals having larger home-range size
[57], but this tendency is likely to depend on the behavior of animals. Although binturongs
have much larger home-range sizes (1.5–4.2 km
2
; [29]) than Mueller’s gibbons (0.3 km
2
; [30]),
the mean dispersal distance of the two species are almost the same. This difference is relevant
to the binturongs’ feeding strategy. They tend to stay at the same feeding patch for a long dura-
tion [29], so their daily movement distance is much shorter (228 m; [29]) than that of Mueller’s
gibbons (1113 m; [30]). Meanwhile, helmeted hornbills have the largest dispersal distance
because they might have the largest home-range based on data for similarly sized hornbills
(4.1–34.9 km
2
; [39]).
Dynamic of hemi-epiphytic figs
Binturongs are effective seed dispersers for hemi-epiphytic figs, but they are not the only ones.
In this study, we demonstrated that ingested fig seeds by all the study animals were viable, and
most were notably transported away from the parent trees. Although helmeted hornbills were
less effective than binturongs, some of their feces stuck to the potential germination sites. Fig
seeds in knotholes showed the highest survival rates among the potential germination micro-
sites [15]. When knotholes were used for breeding nests [58], some seeds survived fortuitously
on the lip of the cavity [59], while most were dispersed to the forest floor around the nest [60].
Considering that over 50% of ingested seeds would be dispersed to more than 1 km, they are
critically important long-distance seed dispersal agents for promoting gene flow among popu-
lations [55]. Another closely related species to binturongs, the small-toothed palm civet Arcto-
galidia trivirgata, also exhibits similar defecatory habits (M Nakabayashi, pers. obs.). Because
they usually consume hemi-epiphytic figs [47], they are also potentially effective seed dispers-
ers. Secondary seed dispersal by ants [61,62] should also be considered; although, the most fre-
quently observed canopy ant, Pheidole, could also be a seed predator in Borneo [62]. These
animals may increase the probability of seeds hitting suitable establishment sites.
A single fig tree produces a massive amount of seeds per single fruiting event (400,000–
13,000,000), maximizing the probability of establishment [23]. Therefore, most fig-eating
Seed dispersal of hemi-epiphytic figs
PLOS ONE | https://doi.org/10.1371/journal.pone.0217590 June 13, 2019 12 / 17
animals can be potential seed dispersal agents when they defecate some viable seeds [6,22];
though, over 50% of hemi-epiphytic fig seeds fell under the parent trees [23]. Fig fruit size
demonstrates the importance of large-bodied effective seed dispersers of hemi-epiphytic figs,
such as binturongs and helmeted hornbills. They feed on fig fruits of a broad size range (1–7
cm in diameter; [29,63]), including F.stupenda, one of the largest hemi-epiphytic figs on Bor-
neo [1]. Ficus species that bear large fruits on Borneo are usually climbers and trees that germi-
nate on forest floors, but there are several hemi-epiphytic figs that bear large fruits, such as F.
cucurbitina,F.dubia,F.stupenda, and F.xylophylla [1]. Fruit bats and birds are important
seed dispersers, especially on oceanic islands because they carry seeds from continental lands
[64]. However, because large hemi-epiphytic fig seeds are surrounded by thick and hard flesh
(inflorescence), most birds and bats do not consume whole fig fruits but pick or gnaw the flesh
and leave the seeds untouched (M Nakabayashi, pers. obs. and [65]). Indeed, there are no
hemi-epiphytic figs producing large fruits on newly formed volcanic islands, where birds and
bats are the main seed dispersal agents [64], and these figs are poorly dispersed in the Bornean
rainforest that lacks several large frugivores [10]. Binturongs and helmeted hornbills swallow
these large fig fruits together with seeds (M Nakabayashi pers. obs.). Moreover, given that spe-
cies bearing large fig fruits usually occur at high positions in the canopy [8] where more severe
conditions of water shortage for epiphytes are present, these species could be more dependent
on seed deposition on suitable microsites. Thus, they significantly contribute to the survival of
hemi-epiphytic figs that bear large fruits.
Gibbons and hornbills are generally the most important seed dispersal animals in Southeast
Asian rainforests [21,22]. However, most studies assessing their SDE have used ground-based
plants [34,66]. This study demonstrated that, compared to terrestrial plants, successful seed
dispersal of hemi-epiphytic figs, which requires strict conditions for seedling establishment, by
these frugivores is aleatory and rare, especially in gibbons. They largely depend on figs for
their diet [30], but most previous studies have identified Ficus species only to the genus level.
Therefore, their dependence on hemi-epiphytic species is unclear. Seed deposition on the for-
est floor is optimal for most non-hemi-epiphytic Ficus species, so gibbons definitely contribute
to the seed dispersal of these Ficus species. Directed seed dispersal to specific microsites in the
canopy is limited to specific animal species. Therefore, it may become one of the main factors
regulating low-success hemi-epiphytic fig recruitment in Bornean rainforests.
Our study focused on only three relatively large frugivores, and their SDE at the population
and community levels remains inconclusive. Unfortunately, the important seed dispersers of
these hemi-epiphytic figs are listed as Vulnerable (binturongs [67]) and Critically Endangered
(helmeted hornbills [68]). As populations of both species are decreasing [67,68], if they
become extinct, seed dispersal opportunities for these figs would be drastically decreased, sub-
sequently affecting other animals that feed on them and eventually local ecosystems. More
efforts are urgently needed to implement practical conservation policies for these important
animals. Additionally, more studies are needed to understand the reproductive systems of key-
stone plants, such as hemi-epiphytic figs, in tropical rainforests.
Supporting information
S1 Table. Moved distance (m) from the origin at each hour and empirical gut retention
time (hour) of binturongs, gibbons, and hornbills. a: data of the gut retention time is from
[41]. b: data of the gut retention time is from [35] (a Hylobates muelleri ×agilis). c: data of the
moved distance is from [40] (a Buceros bicornis), and that of gut retention time is from [42] (a
Rhyticeros cassidix)
(DOCX)
Seed dispersal of hemi-epiphytic figs
PLOS ONE | https://doi.org/10.1371/journal.pone.0217590 June 13, 2019 13 / 17
S2 Table. Raw data of visitation length (min.) and feeding speed (sec.).
(XLSX)
S3 Table. Raw data of seed dispersal microsites and fig establishment sites.
(CSV)
S4 Table. Raw data of moved distance from the origin at each hour (m).
(CSV)
Acknowledgments
The authors thank the Sabah Biodiversity Centre, Danum Valley Management Committee,
and Maliau Basin Management Committee for their permission to conduct this research. We
are grateful to field assistants, Azz, Kenneth, Albert, Farizal, and Taufiq for their assistance in
the field, and Q. Phillipps for his assistance in the identification of plant species. We also thank
anonymous reviewers for critical readings.
Author Contributions
Conceptualization: Miyabi Nakabayashi.
Data curation: Miyabi Nakabayashi, Yoichi Inoue.
Formal analysis: Miyabi Nakabayashi.
Funding acquisition: Miyabi Nakabayashi.
Investigation: Miyabi Nakabayashi.
Methodology: Miyabi Nakabayashi.
Project administration: Miyabi Nakabayashi.
Supervision: Masako Izawa.
Writing – original draft: Miyabi Nakabayashi.
Writing – review & editing: Yoichi Inoue, Abdul Hamid Ahmad, Masako Izawa.
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