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Biotropica. 2019;00:1–10. wileyonlinelibrary.com/journal/btp
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© 2019 The Association for Tropical Biology and
Conservation
1 | INTRODUCTION
Durian is one of the most economically important fruits in Southeast
Asia, wi th an export val ue of up to US$254.85 millio n in 2013 (Indarti,
2014). Indonesia is one of the primary producers of durian: 859,118
tons were produced in Indonesia during 2014, and it commanded
a higher unit price than any other fruit commodity in the country
(Durian Harvests 2018; Indarti, 2014; Rafani, 2013). Durian consti‐
tutes a significant portion of Indonesia's gross domestic product and
was named by the Indonesian Ministry of Agriculture as one of the
five national fruit priorities, indicating its productivity and sale are
national interests (Rafani, 2013). Despite the fruit 's popularity, pro‐
ductivity of this cash crop is much lower in Indonesia than that of
other fruits, and production is relatively inconsistent here compared
with Thailand and Malaysia (Durian Harvests 2018; Rafani, 2013).
Improvements to durian production would help Indonesia meet do‐
mestic demand and eventually grow a surplus to export to high de‐
mand consumers such as China (Indonesia Investments 2016).
Received:28Novembe r2018
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Revised:6S eptember2019
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Accepted:10September2019
DOI : 10.1111 /bt p.12 712
PAPE R
Contributions of bats to the local economy through durian
pollination in Sulawesi, Indonesia
Sheherazade1,2 | Holly K. Ober1 | Susan M. Tsang3,4
*Associa te Editor : Emilio Bruna; Ha ndling Editor : Isaac Ma rney
1Depar tment of Wildlife Ecology and
Conservation, University of Florida,
Gainesville, FL, USA
2Wildlife Conservation Society Indonesia
Program, Bogor, West Java, Indonesia
3Department of Mammalogy, American
Museum of Natural Histor y, New York, NY,
USA
4Zoology Division, National Museum of the
Philippines, Metro Manila, Philippines
Correspondence
Holly K . Ober, Depa rtment of Wildlife
Ecology and Conservation, Universit y of
Florida, Gainesville, FL 32603, USA.
Email: holly.ober@ufl.edu
Abstract
Durian is economically important for local livelihoods in Indonesia. Our study inves‐
tigated the identity of pollinators of semi‐wild durian and subsequently estimated
the economic contribution of these pollination services. We conducted pollination
exclusion experiments and deployed camera traps at durian trees from October 2017
to January 2018 in an area where the local economy depends on durian production
in West Sulawesi, Indonesia. Durian flowers in the experiment that were accessible
to bats had significantly higher fruit set compared with flowers that were completely
closed to animal visitors or those that could only be visited by insects, suggesting that
bats were the primary durian pollinator. The small, highly nectarivorous cave nectar
bat (Eonycteris spelaea) visited more inflorescences (n = 25) and had visits of much
longer duration (
̄
X
= 116.87 sec/visit) than the two species of flying foxes: Pteropus
alecto (n = 7 inflorescences visited,
̄
X
= 11.07 sec/visit) and Acerodon celebensis (n = 6
inflorescences visited,
̄
X
= 11.60 sec/visit). Visits by large and small bats were influ‐
ential in differentiating successful durian fruit production from unsuccessful. Using a
bioeconomic approach, we conservatively estimate that bat pollination services are
valued at ~$ 117/ha/fruiting season. By demonstrating an ecological link between
bats and the local economy, this research provides an urgent message for Southeast
Asian governments regarding the need to promote bat conservation in order to in‐
crease the production of durian grown under semi‐wild conditions.
Abstract in Indonesia is available with online material.
KEYWORDS
Asia Tenggara, bioeconomic, jasa ekosistem, jumlah buah, kalong, Pteropodidae
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SHEHER AZA DE Et Al .
Durian is incredibly diverse, with 30 species and 76 varieties in
Indonesia alone (Santoso, 2012). Durian flowers are generally self‐
incompatible and require animal vectors for pollination (Bumrungsri,
Sripaoraya, Chongsiri, Sridith & Racey, 2009; Lim & Luders, 1998;
Yumoto, 2000). To date, durian pollination studies have been lim‐
ited to peninsular Southeast A sia (Aziz, Clements, McConkey, et al.,
2017; Bumrungsri et al., 2009), where durian is typically grown in
large plantation systems. In contrast, although plantations of some
durian cultivars exist in Indonesia, most semi‐wild durian sold on
the market there rely on small‐scale farmers who grow the fruits
in agroforestry systems without direct management and interven‐
tion by local farmers (Rafani, 2013). Furthermore, the dissimilarities
in wildlife species assemblages in insular Southeast Asia compared
with peninsular Southeast Asia suggest that pollination systems may
be quite dif ferent between the two regions.
It has been suggested that semi‐wild durian may play a significant
economic role in domestic and local markets (Djajanti, 2006; Kunz,
de Torrez, Bauer, Lobova & Fleming, 2011). However, to the best
of our knowledge, no research has yet investigated the economic
contribution of specific pollinators to the semi‐wild durian trade de‐
spite the known impor tance of pollinators to fruit set. The lack of
understanding of how semi‐wild durian is pollinated limits the ability
of fruit producers to scale up production to increase the economic
impact of durian as a cash crop.
Some durian species possess the classically defined floral traits
of a plant with chiropterophilous pollinator syndrome, suggesting
that bats are their primary pollinators. These floral traits include
white or dull coloration, strong fragrance, and nocturnal blooming
(Troll, 1975; Tschapka & Dressler, 2002). Pteropodid bats, such as
Eonycteris spelaea (common nectar bat), Macroglossus minimus (lesser
long‐tongued fruit bat), and Pteropus spp., are known to be durian
visitors in other parts of Southeast A sia (Aziz, Clements, McConkey,
et al., 2017; Fujita & Tuttle, 1991; Gould, 1977, 1978; Marshall, 1985;
Start, 1974), but the assemblage of durian visitors and its primary
pollinators differ among areas and cultivars. In Malaysian Borneo,
Durio grandiflorus and D. oblongus are primarily pollinated by spi‐
derhunter birds, while D. kutejensis is pollinated by bees, birds, and
bats (Yumoto, 2000). Durio zibethinus in southern Thailand relies
on Eonycteris spelaea as their primar y pollinator (Bumrungsri et al.,
2009, 2013; Stewart & Dudash, 2017). In Indonesia, the primary pol‐
linators of durian are unknown.
Additional investigation of pollination systems will be a nec‐
essary component of effor ts to improve crop production rates in
major semi‐wild durian producing areas throughout Southeast Asia.
Sulawesi is a suitable place for investigation because Sulawesi pro‐
duces multiple cultivars of semi‐wild durian that are of interest to
the agricultural sector, and because a unique assemblage of volant
wildlife occurs here relative to Peninsular Southeast Asia where
durian pollination has been investigated previously. Our study
aims to understand the pollination of semi‐wild durian in Sulawesi,
Indonesia, where durian is an essential local commodity. Thereafter,
we estimate the economic significance of the primar y pollinators to
the local, and potentially regional, economy.
2 | METHODS
2.1 | Study site
This study was conducted in Batetangnga Village, Binuang subdis‐
trict in Polewali Mandar Regency, West Sulawesi (Figure S1), during
the flowering and fruiting season of semi‐wild durian (October to
November 2017 and November 2017 to January 2018, respec tively).
Batetangnga is the most geographically expansive village in the sub‐
district (44.80 km2), comprising 45 percent of the total area (Badan
Pusat Statistik Kabupaten Polewali Mandar 2017). It extends from
the coastal lowlands into inland and montane areas dominated by
secondary forest mixed with various agricultural plantations. In most
of Sulawesi, durian is not grown in monoculture plantations as is typ‐
ical in peninsular Southeast Asia, but is instead sparsely distributed
in secondary forests in managed mixed agroforestry systems along
with cacao (Theobroma cacao), rambutan (Nephelium lappaceum),
langsat (Lansium parasiticum), and mango (Mangifera indica). The av‐
erage annual rainfall in the area is 1954 mm, with peaks usually oc‐
curring in May, June, and December. All investigative protocols in
this study were approved by the University of Florida under IACUC
protocol No. 201709800.
2.2 | Floral characteristic of durian
The durian species at our study site was Durio zibethinus. During the
flowering season, each durian tree has hundreds to thousands of
inflorescences (a cluster of flowers on a stem). Durian flowers are
cauliflorous, meaning tens of flowers are stacked per inflorescence
and grow directly on branches.
Understanding the pollination biology of durian requires an un‐
derstanding of durian's floral characteristics. We observed 10 du‐
rian flowers from five inflorescences in three durian trees located
in different orchards. Due to the tall stature of durian trees (15–
40 m), we selected relatively shorter trees with accessible flowers.
We carried out hourly observations and tests throughout the flow‐
ering period to determine five physiological attributes of the local
durian species (Bumrungsri et al., 2009; Dobat & Peikert‐Holle,
1985; Honsho, Yonemori, Somsri, Subhadrabandhu & Sugiura,
2004; Honsho, Yonemori, Sugiura, Somsri & Subhadrabandhu,
2004; Lim & Luders, 1998; Yumoto, 200 0). We assessed (a) the
time each flower opened; (b) the time each anther dehisced, de‐
termined by noting the presence of a slit on the anther as a sign
that pollen grains had been released; (c) the time stigmas became
receptive, determined by placing a drop of hydrogen peroxide on
each stigma and noting the presence of bubbles as an indication
that the stigma was receptive to pollen; (d) nectar production,
using 100 μl micro‐capillary tubes to draw and measure nectar;
and (e) sucrose concentration of nectar using a sucrose refrac‐
tometer (Extech RF10 0 to 32% Brix Refractometer). All observa‐
tions and tests were conducted star ting at the time durian flowers
bloomed in the late evening until their corollas dropped from ped‐
icels the next morning.
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SHEHER AZA DE Et Al .
2.3 | Pollination biology of durian
We chose seven 18–20 m tall durian trees for a pollination exclusion
experiment, using two criteria to select focal trees. First, a sufficient
number of inflorescences per tree were required to accommodate all
the treatments (described below). Second, only trees that could be
climbed without safety concerns were considered (e.g., it was imprac‐
tical to cl imb durian trees t hat were slipper y, had extre mely large trunk
diameter s, or had ant nests). Each durian tree in this study belonged to
a different orchard but grew in a similar environment (e.g., in forests
with medium canopy cover and high intensity of sunlight and rainfall).
Individual trees were located 0.5 to 2.0 km apart. All trees were ap‐
proximately the same height, and therefore likely of similar age.
For every target tree, we selected 3–6 durian inflorescences
that had ~30 flowers each. We assigned each inflorescence to one
of the three treatments: closed, insec t, and open pollination (Figure
S2). We attempted to install each set of three treatments (closed,
insect, and open) at one height before installing the next set of three
treatments at a different height within the 15–20 m height range.
For example, we established one set of three treatments at the first
3 inflorescences we found meeting the above criteria at 16 m height,
then another set of three treatments at 18 m height.
For the closed pollination treatment, we bagged each inflores‐
cence before the flower bloomed with a bag made of a mesh fabric
that allowed light, rain, and gas exchange bet ween flowers and the
ambient environment, but prohibited any animals from accessing the
flowers. For the insect pollination treatment, inflorescences were
enclosed with specialized nets made of the same garden fabric but
manually perforated to allow only insects to access flowers (perfo‐
ration size = 1.5 cm). For the open pollination treatment, we did not
prevent access to the inflorescences by any potential visitors. We la‐
beled all inflorescences to indicate replicate number, treatment, and
experiment date. We had 36, 30, and 25 replicates (inflorescences)
for open, insect, and closed treatments, respectively. Because du‐
rian flowers may have late acting self‐incompatibility (Bumrungsri
et al., 2009; Honsho, Yonemori, Somsri, et al., 2004) and to avoid
overestimating pollination services by relying only on initial fruit set
(Bos et al., 2007), we monitored and counted durian fruit set for all
replicates on days 10, 20, 30, and 60 following the establishment of
each treatment (Figure S3).
We used Kruskal–Wallis and Dunn's tests (Dinno, 2017) to de‐
termine whether each treatment produced significantly different
amounts of durian fruit. We considered fruit set on days 20 and 60
to be indicative of pollination and reproduction success, respectively
(Aziz, Clements, McConkey, et al., 2017). We visualized data using
ggplot2 from the R package “ggplot2” (Wickham & Chang, 2016).
2.4 | Durian pollinators
We used camera traps to determine which animals visited durian
flowers (Figure S2). We deployed a camera trap (Bushnell Trophy
Cam HD Essential E2 12 MP Trail Camera) on a branch in front
of each durian inflorescence that received the open pollination
treatment (n = 36). The distance between inflorescences and cam‐
era traps ranged from 0.30 to 1.5 m. Camera traps were active
during the entire flowering period for each inflorescence, record‐
ing day and night visitation rates of animals that fed on durian
floral products (nectar or the whole flowers). We programmed
the camera traps to capture videos with a maximum length of
15 s, with 5 min intervals between consecutive recordings. We
recorded the number of interactions between each animal spe‐
cies and each inflorescence as well as the duration of each visit as
a proxy for the contribution of each pollinator species to durian
production. The videos also documented the foraging behavior of
each animal visitor, which helped us determine which species con‐
tacted stigma and anthers (and presumably benefitted durian by
serving as primary pollinators), which visited flowers but did not
contact stigma and anthers, and which ate the whole flowers (and
were thus detrimental to durian).
We used Generalized Linear Mixed‐effect Models (GLMMs) to
determine whether only the presence of certain animal species at in‐
florescences, the number of interactions between certain species and
inflorescences, and/or the duration of visits of certain species to inflo‐
rescences was influential in affecting the success or failure of durian
fruit pro duction. Only t hose species that visited >3 inflorescences were
included in these analyses. We checked for multicollinearity among
variables using function “ggpairs” (package “GGally”) to extract the cor‐
relation coefficient and function “vifcor” (package “usdm”) to calculate
the VIF (Variance Inflation Factor) (Naimi, 2017; Schloerke et al., 2018).
We dropped variables with high correlation coefficients (|r| > .5)] and
VIF factor > 10. Then, we used function “glmer” in R package lme 4
to test GLMMs (Bates et al., 2019), with durian tree as a random ef‐
fect and a binomial distribution for our response variable that was ex‐
pressed as success or failure of durian fruit production. We determined
which models had the most support from the data using Multi‐Model
Inference w ith function “m odel.sel” in R pa ckage MuMIn (Bar ton, 2019).
We also assessed the temporal aspect of durian foraging of each
bat species and determined whether there was temporal resource
partitioning among bat species. We converted time of visitation to
radians and used non‐parametric kernel density estimates to display
each species’ temporal foraging activity as a continuous distribution
over a 24‐hr cycle (Frey, Fisher, Burton & Volpe, 2017). We generated
the estimates and density plots using package “overlap” in R with Δ1
estimator (Dhat1) (Meredith & Ridout, 2017a). We then used a de‐
scriptive measure of the degree of similarity to evaluate overlap be‐
tween each pair of species, with values ranging from 0 (no overlap)
to 1 (complete overlap) (Frey et al., 2017; Ridout & Linkie, 2009). To
determine confidence intervals (CI) of the overlap, we used smoothed
bootstrap with 10,000 resamples then selected basic0 output from
bootCI as our CI (Meredith & Ridout, 2017b). All statistical analyses
were conducted using R 1.0.136 ( https ://cran.r‐proje ct.org).
2.5 | Economic value of bat pollination services
We used a bioeconomic approach to estimate bat pollination ser‐
vices to durian, using a formula originally developed to calculate
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SHEHER AZA DE Et Al .
insect pollination services (Gallai, Salles, Settele & Vaissière, 2009).
We modified the formula “Insect Pollination Economic Value” to
“Pollination Economic Value (PEV)”:
where: i = crop; x = region; Pix = price of crop i produced in x;
Qix = quantity produced in region x; Di = dependence ratio of the
crop i on bat pollination.
Dependence ratio (0–1), Di, expresses the degree of durian de‐
pendency on pollination. It is calculated by subtracting fruit set of
bagged flowers (closed pollination) from fruit set of unbagged flow‐
ers (open pollination), divided by the fruit set of unbagged flowers
(Kasina, Mburu, Kraemer & Holm‐Mueller, 2009). In our case, we cal‐
culated durian dependence ratios in a similar manner, but we used
fruit set of bagged flowers subjected to insect pollination for closed
pollination treatments since insects may also pollinate durian flowers.
3 | RESULTS
3.1 | Floral characteristic of durian
Durian flowers had distinct attributes that conform to the chirop‐
terophilous syndrome, which included dull coloration of the co‐
rolla, heavy fragrance, and night‐blooming behaviors. Each flower
was open and receptive for only a single night. The flowers started
to open at 1530 hr and fully opened around 1800 hr. Pollen was
released (anther dehiscence) after 1830 hr, about the same time
when stigmas became receptive. Stigmas remained receptive until
the corollas dropped early in the morning before sunrise. The
average volume of nectar produced by each durian flower was
167.4 μl ± 15.11 (SE) (range: 79–240 μl, n = 10) (Figure S4). Nectar
contained approximately 13.53% ± 0.48 (SE) (range: 9.95–16%,
n = 10) of sucrose.
3.2 | Pollination biology of durian
Overall, durian subjected to the open pollination treatments had sig‐
nificantly higher fruit set compared to durian with insect and closed
pollination treatments both on day 20, which represents pollination
success (X2 = 38 .39, p < .0001), and day 60, which represents repro‐
ductive success (X2 = 32.52, p < .00 01) (Figure 1). The average num‐
ber of fruits set in open, insect, and closed pollination treatment s on
day 60 was 1.69 ± 0.37 (SE) (range: 0–10 fruits, n = 36), 0.27 ± 0.11
(SE) (range: 0–2 fruits, n = 30), and 0.04 ± 0.04 (SE) (range: 0–1 fruit,
n = 25), respectively.
3.3 | Durian pollinators
Durian visitors consisted of four vertebrate species (three species of
bat and one arboreal marsupial) and two invertebrate species (one
species of bee and moth). The three bat species (the small Eonycteris
spelaea and the larger Pteropus alecto (black flying fox) and the
Acerodon celebensis (Sulawesi flying fox)) were the primary visitors
to durian flowers in the open pollination treatment (2, Table 1). Bats
were responsible for visits to 38 of the 43 inflorescences where ani‐
mal visit s were recorded. We cou ld easily diffe rentiate these th ree bat
species in the camera trap videos, as E. spelaea was distinctly smaller
PEV
=
∑I
i=1∑X
x=1
(Pix ×Qix ×Di
)
FIGURE 1 The number of durian fruit
set under three pollination exclusion
treatments. Box and whisker plots show
the minimum, first quartile, mean, third
quartile, and maximum values for each
treatment
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SHEHER AZA DE Et Al .
than the others and had brightest (grayish) fur, whereas A . celeben‐
sis appeared smaller and brighter than P. al ec to due to differences
in fur reflectance. All three species were observed drinking nectar
from durian floral tubes without destroying the flowers. Although
A. celebensis and P. a lec to have large bodies relative to durian flowers,
they hung from tree branches and bent their head toward the flow‐
ers when drinking and therefore did not damage the inflorescences.
Eonycteris spelaea (the smallest of the three bat species) was the
most frequent visitor to the durian flowers and had visits of longer
duration than P. al ect o and A. celebensis (large bats/flying foxes)
(Table 1). After dropping the metric describing the number of inter‐
actions of large bats with flowers due to multicollinearity, regres‐
sion analyses showed that the model that received the most support
given the data (model with the lowest AICc) indicated the presence
of large bats was most influential to durian success (R2 = 0.244 and
marginal R2 = 0.029) (Table 2). However, the weight of evidence in
support of each of the top five models was similar, indicating that all
five variables investigated explained the success of durian produc‐
tion (presence of large and small bats, duration of visits of large and
small bats, and number of visits of small bats), and that this analysis
FIGURE 2 Three bat species fed on durian nectar. (1) Eonycteris spealea hung on durian flowers while feeding (a), sometimes accidentally
pulled off flower reproductive organs (stigma and anther) (b), and convincingly served as pollinator as bat head touched lower reproductive
organs while feeding on nectar (c). (2) Pteropus alecto hung on branches while feeding on nectar (a), grabbed a flower but did not pull it off
(b), and convincingly pollinated, as its head touched flower reproductive organs (c). (3) Acerodon celebensis hung on branches while feeding
on nectar (a), bat licked it s fur (b), and convincingly served as pollinator as its head touched flower reproductive organs (c)
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SHEHER AZA DE Et Al .
lacked adequate power to conclusively determine which of these
factors was most influential due to small sample size.
All three bat species showed a single nightly peak in visita‐
tion to durian. Eonycteris spelaea and P. ale cto showed similar
temporal foraging activity on durian nectar (overlap = 0.88), feed‐
ing on durian nectar throughout much of the night, with a peak
between 2300 hr and 2400 hr. However, both of these species
showed different temporal foraging activity from A. celebensis
(overlap estimate of E. spelaea—A. celebensis = 0.45; overlap of
P. ale cto—A. celebensis = 0.41) . Acerodon celebensis foraged at du‐
rian flowers earlier in the night than the other bat species, from
2000 hr to 2300 hr, with a peak bet ween 2000 hr and 2100 hr
(Figure 3). P teropus alecto was always seen foraging alone and
exhibiting resource defending behavior against other bats. In
contrast, we once observed t wo individuals of A. celebensis feed‐
ing together on the same durian inflorescences, and on several
occasions observed 2–3 individuals of E. spelaea feeding together
on the same durian inflorescences.
A small number of inflorescences were visited by animals other
than bats. While the mean duration of visits by Strigocuscus cele‐
bensis (small Sulawesi cuscus) were longer than that of any other
animal visitor, this species destructively consumed the flowers,
and flowers consumed by cuscus were no longer available to any
other animal species. The cuscus is thus not acting as an effective
pollinator for durian and in fact may have a negative impact on
durian fruit production (Figure S5). Insects such as moths and bees
were rarely documented visiting durian flowers, perhaps in part
because they did not trigger the camera traps as reliably as larger
TABLE 1 Identity of animals that visited durian flowers in Sulawesi, the number of visits by each, the duration of their visits, and the
number of inflorescences visited
Family Species Common names
Number of
visits
Total duration of all
visits (sec)
Number of inflo-
rescences visited
Pteropodidae Eonycteris spelaea Common nectar bat 82 2474 25
Pteropus alecto Black flying fox 15 180 7
Acerodon celebensis Sulawesi flying fox 10 110 6
Phalangeridae Strigocuscus celebensis Small Sulawesi cuscus 42335 2
Apidae Apis dorsata Giant honey bee 530 2
Erebidae Unknown Moth 115 1
Model kloglikelihood AICc ΔAICc weight
d ~ pres_lb + (1|tree) 3 −21.176 4 9.1 0.00 0.235
d ~ pres_sb + (1|tree) 3 −21.345 49.4 0.34 0 .198
d ~ dur_lb + (1|tree) 3 −21.455 49.7 0.56 0.178
d ~ ni_sb + dur_sb + (1|tree) 4 −20 .22 6 49.7 0.64 0.171
d ~ dur_sb + dur_lb + (1|tree) 4 −20 .398 50.1 0.98 0.14 4
d ~ pres_sb + pres_lb + (1|tree) 4 −21.0 4 8 51.4 2.29 0.075
Note: k = number of model parameters; d = durian production (success/failure); pres_lb = pres‐
ence of large bats at durian (Pteropus alecto or Acerodon celebensis); pres_sb = presence of small
bats at durian (Eonycteris spelaea); ni_sb = number of interactions between small bats and durian;
dur_lb = duration of visit s of large bats to durian (min); dur_sb = duration of visits of small bats to
durian (min); and random effect = tree.
TABLE 2 Results of Generalized
Linear Mixed‐Effect Models (GLMMs) to
determine which factors contribute most
to the success of durian fruit production
at 60 days
FIGURE 3 Temporal overlap of foraging activit y between the three pairs of bat species that visited durian flowers. The gray shading
indicates the time when pairs of species were both actively foraging at durian flowers. The y‐axis shows the kernel density estimates of
activity
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SHEHER AZA DE Et Al .
vertebrates, or perhaps because nets used to exclude vertebrates
while allowing access to insects may have inadvertently deterred
insects. Regardless of documented visitation rates, inflorescences
subjected to insect pollination treatments had much lower fruit
set relative to the open pollination treatments, suggesting that al‐
though insects are capable of pollinating durian flowers, they are
much less efficient than bats. During the day (0600–1800), camera
traps also recorded bees and Aethopyga siparaja (crimson sunbird)
visiting durian flowers. The birds visited unopened flower buds
and punctured the base of the buds with their beak (Figure S6).
The stigma and anthers were left untouched because the flowers
were still closed, indicating it is unlikely diurnal birds could func‐
tion as durian pollinators.
3.4 | Economic value of bat pollination services
The degree to which durian depends on bats as pollinators, the
durian dependence ratio, was calculated as 0.84. In Batetangnga
Village, durian fruiting season only occurs once per year and lasts
for approximately two months. In our study, durian flowering season
occurred from October to November 2017, and then the fruiting and
harvesting season occurred from January to early April 2018. During
this period, the total durian production in Batetangnga Village was
~1,497,600 fruits according to the locals. The villagers sold durian
at a per unit price rather than by weight, with each fruit command‐
ing IDR 5000 (~US$0.35) during our study period. Thus, we esti‐
mate that bat pollination services were wor th IDR 6.3 billion (~US
450,00 0). Because Batetangnga Village encompasses ~44.8 km2, bat
pollination services are valued at ~117/ha in this region during this
durian fruiting season.
4 | DISCUSSION
Our study provides the first evidence that duria n flowers in Sulawesi,
Indonesia are pollinated primarily by bats. Several observations sup‐
port this evidence: (a) Each flower was open and receptive at night,
which is a time of day when bats were active; (b) bats visited the
greatest number of inflorescences and had the longest total duration
of visits; (c) bats came into contact with anthers and stigmas without
damaging flowers, whereas other visitors caused damage to flowers
or did not contact anthers and stigmas; and (d) extremely low fruit
set occurred via insect pollinators when vertebrates were prevented
from accessing flowers during exclosure experiments. These results
corroborate findings from other studies in Thailand and Malaysia in
which the same durian species, Durio zibethinus, showed similar flo‐
ral traits and also relied on bats for pollination (Aziz, Clements, Peng,
et al., 2017; Bumrungsri et al., 2009). Our findings underscore the
importance of bat s for the pollination of this highly valuable fruit in
Southeast Asia.
Among nocturnal animals, bats may increase the probability of
successful durian pollination by transferring sufficient loads of pol‐
len among different durian trees. Previous studies have documented
that pteropodid bats are long‐distance pollen dispersers that can
deposit large loads of pollen (Acharya, Racey, Sotthibandhu &
Bumrungsri, 2015). For example, E. spelaea, the main visitors of du‐
rian flowers in this study, travels up to 38 km while foraging (Start,
1974). Such long‐distance pollen dispersers are important for low‐
density plant species such as the durian, especially when grown in
agroforestry systems, as is typical in Indonesia (Retnowati, 2003;
Salafsk y, 1995). Long‐distance pollination also increases the proba‐
bility of pollen coming from genetically distant and distinct individ‐
uals, which is important to successful pollination and production of
high quality durian fruits (Honsho et al., 2009).
4.1 | Pollinator assemblage of durian in Sulawesi
In our study area, the pollinator assemblage of durian is more diverse
than those in Tioman Island, Malaysia (Aziz, Clements, McConkey,
et al., 2017) and souther n Thailand (Bumrungsri et al ., 2009), possibly
because Sulawesi has a comparatively higher diversity of pteropo‐
did bats (Mickleburgh, Hutson & Racey, 1992; Simmons, 2005). Our
study indicates that E. spelaea, a generalist nectarivore, is a durian
pollinator in Sulawesi, much like it is in other regions (Aziz, Clement s,
McConkey, et al., 2017; Bumrungsri et al., 2009). Also, our study pro‐
vides the first record of durian pollination services by P. al ecto and
the endemic, intensively hunted A. celebensis, highlighting that these
endangered flying foxes are also key pollinators of durian.
Nectarivorous bat species are thought to be more important
pollinators than the primarily frugivorous bat species (Stewart &
Dudash, 2017). However, the potential role of all flying foxes (bats
of the genera Pteropus and Acerodon) as pollinators should not be
overlooked, as flowers are an important dietary component for
these species and their tongue morphology indicates they are able
to exploit nectar (Aziz, Clements, McConkey, et al., 2017; Banack &
Grant, 2002; Brit, Hall & Smith, 1997; Palmer, Price & Bach, 2000).
Our study demonstrates that Pteropus and Acerodon are important
pollinators for semi‐wild durian in Sulawesi, as their visitation to the
flowers contributed to mature fruit set. Although our exclusion ex‐
periments unequivocally indicated bats were the primary pollinators
of durian, the results of our GLMM analyses suggested our sample
sizes were too small to definitively determine which aspect of bat
visitations was most influential to durian fruit set. We recommend
additional research with larger sample sizes in the future.
Visitation by large pteropodid bats is important to durian fruit
production. Compared with smaller species, flying foxes are likely to
deposit larger loads of pollen and move them over longer distances,
increasing the likelihood of successful pollination. In Australia,
P. ale cto individuals are known to forage up to 20 km (Markus &
Hall, 2004; Vardon et al., 2001). Other species of flying foxes are
also recognized as long‐distance pollinators: P. poliocephalus flies
17–25 km during foraging bouts (Spencer, Palmer & Parr y‐Jones,
1991); Pteropus tonganus 5–22 km (Banack & Grant, 2002); Pteropus
rufus 1–7 km (Oleksy, Racey & Jones, 2015); and Pteropus vampyrus
88–363 km (Epstein et al., 2009). Further investigation to quantify
pollen loads carried by various species of bats and assessments of
8
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SHEHER AZA DE Et Al .
their pollen transfer effectiveness could increase understanding of
the contributions of each species to pollination for specific plant
species (Sheherazade, 2018). Nevertheless, the present exclusion
study provides convincing evidence regarding the need to enhance
bats to increase durian production.
4.2 | Resource partitioning among bat species
Bats may partition resources either temporally or spatially. We
found some evidence of temporal partitioning in durian visitation by
the bats. Peak foraging occurred simultaneously for E. spelaea and
P. ale cto, and this peak occurred later in the night than peak activity
of A. celebensis. The two large species appear to partition resources
temporally within nights. This partition may be a function of interfer‐
ence, if smaller bats cannot visit the flowers that are being used by
larger bats, or a function of roost location relative to the plants we
monitored, which would determine the time after sunset bats start
foraging at these plants.
We could not directly test whether the bats partitioned their
use of nectar resources within trees by height because we deployed
all the camera traps at similar heights, 15–20 m above the ground.
However, we heard loud squeaking sounds and wing‐clapping from
the canopy of 30–40 m durian trees during the flowering season.
Local people rep orted similar obs ervations. We susp ect these sound s
were P. a le cto and/or A. celebensis that foraged considerably higher
in the trees compared with the smaller E. spelaea. Accessing flowers
higher in the trees would be easier and energetically less costly for
these large pteropodid bats, which are less maneuverable below the
canopy than the smaller bats (Palmer et al., 2000). Previous studies
corrobo rate this idea of spat ial partitio ning between sp ecies: Pteropus
hypomelanus fed at greater heights in durian trees (6–20 m) than
E. spelaea (<6 m) in Peninsular Malaysia (Aziz, Clements, McConkey,
et al., 2017); P. giganteus fed at greater heights in Madhuca latifolia
trees than Cynopterus sphinx (Nathan, Karuppudurai, Raghuram
& Marimuthu, 2009); and P. giganteus foraged at greater heights
(15–20 m) than C. sphinx in kapok trees (Singaravelan & Marimuthu,
2004). Our obser vations suggest that resource partitioning occurs
spatially between small and large pteropodid bats (i.e., larger bats for‐
age predominantly at greater heights within trees than smaller bats),
whereas it occurs temporally between two large pteropodid bats (i.e.,
A. celebensis forages earlier in the night than P. ale cto). Because du‐
rian trees grow taller with age, conservation of both small and large
bat species may be important to ensure durian fruit production on
trees of all ages grown under semi‐wild conditions.
4.3 | Appeal for bat conservation
Our study experimentally demonstrates the importance of pollina‐
tion services provided by several species of pteropodid bats for the
production of semi‐wild durian in Sulawesi, Indonesia. These pol‐
lination services are valued as much as US$117/ha/fruiting season
for the production of 1500 tons of durian fruit in Batetangnga vil‐
lage. This value is similar to the direct economic benefits estimated
for bee pollination services to coffee in Costa Rica and Colombia
(Bravo‐monroy, Tzanopoulos & Potts, 2015; Ricketts, Daily, Ehrlich
& Michener, 2004). However, this valuation should be treated with
caution and considered a rough estimate since our study lasted a
short period and was conducted in only one village. Total durian
production was based simply on an estimate provided by a knowl‐
edgeable local, because the official data about fruit production this
year were not generated yet by the local government agency. We
assumed all the fruits were traded locally and used a single local
price to derive our estimates. Fruits sold outside the village likely
commanded a higher price, so our use of the local price may have
underestimated the actual value of bat pollination services to durian
production in the region.
Conservation of bats in Sulawesi should be promoted to pre‐
vent loss of productivity of plant species that rely on them for pol‐
lination. This conservation is notably absent for A. celebensis and
P. ale cto, which are large species that are intensely hunted through‐
out Sulawesi to support bushmeat markets in North Sulawesi
(Sheherazade & Tsang, 2015). The endemic A. celebensis is already
listed as Vulnerable on the IUCN Red List due to declines caused
by human actions (Tsang & Sheherazade, 2016). Additional loss of
these bat s may have a profound impac t both ecologically and eco‐
nomically. In our study region, bat pollination services are not only
important to the local economy, but also culturally valuable in the
production of durian used during communal durian feasts which hold
high significance for the local people.
We recommend the prioritization of bat protection by the
Indonesian government and conservation NGOs. The conserva‐
tion of bats should incorporate in situ protection of bat roosts (e.g.,
mangroves, which are the primar y roosts for flying foxes) and for‐
aging areas (e.g., primar y forests and mixed plantations), reduction
of hunting of bats as bushmeat in North Sulawesi, legislation for
bat protection and hunting quotas, and outreach programs to raise
awareness about the importance of bats.
This study provides evidence that enhanced conservation
of bats could potentially improve the productivity of durian in
Indonesia to fulfill the high domestic market demand. In addition,
governments of Indonesia and other Southeast Asian nations
should consider the potential of marketing their organic semi‐wild
durian pollinated by bats. Investigation of international markets
for this organic fruit and engagement with relevant stakeholders
would be needed to evaluate the viability of such an initiative.
Organic fruits command higher prices in the market than non‐or‐
ganic fruits (Reganold & Wachter, 2016). An increase in perceived
quality by consumers may increase the value of durian, and as a
result, decrease trade deficits without the need to increase crop
yield nor convert additional land from forest to agricultural pro‐
duction. Advertisements could also target a larger, wealthier inter‐
national clientele for the sale of organic durian, thereby increasing
the market reach to an audience that has more disposable income
(Gasik, 2017). This “re‐branding” of semi‐wild durian could be ad‐
vantageous to the Indonesian economy and other Southeast Asian
countries, as well as to bat conservation.
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9
SHEHER AZA DE Et Al .
ACKNOWLEDGMENTS
We are grateful for permit granted by Government of West Sulawesi,
Polewali Mandar Regency, Binuang Subdistrict, and Batetangnga
Village. Funding was provided by the Center for International
Forestr y‐USAID Indonesia, Rufford Small Grant, Bat Conservation
International, Tropical Conservation and Development University of
Florida, and IdeaWild to Sheherazade. We thank Prof. Bette Loiselle
and Prof. Todd Palmer and two anonymous reviewers for feedback
that greatly improved this manuscript. We also thank the people of
Batetangnga for their support; Fadli, Hamsul, Openg, and Boneng,
who were great research assistants.
DATA AVAIL ABI LIT Y
Data available from the Dryad Digital Repositor y: https ://doi.
org/10.5061/dryad.j74b646 (Sheherazade, Ober & Tsang, 2019).
ORCID
Holly K. Ober https://orcid.org/0000‐0003‐3780‐6297
Susan M. Tsang https://orcid.org/0000‐0002‐7916‐2074
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SUPPORTING INFORMATION
Additional suppor ting information may be found online in the
Suppor ting Information section at the end of the article.
How to cite this article: Sheherazade, Ober HK, Tsang SM.
Contributions of bat s to the local economy through durian
pollination in Sulawesi, Indonesia. Biotropica. 2019;00:1–10.
https ://doi.or g/10.1111/ btp.12712
