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Roost of Gray Flying Foxes (Pteropus griseus) in Indonesia and Records of a New Hunting Threat

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Pteropus griseus (gray flying fox) is a species of Old World fruit bat that is listed by the International Union for Conservation of Nature (IUCN) as Data Deficient. The species is found on small islands in the Lesser Sundas and Sulawesi, and is endemic to Indonesia, but no contemporary roosts are known, and the last study of the species was in Timor in the Lesser Sundas. In this study, we describe the first known day roost in Sulawesi for Pteropus griseus and collected anecdotal evidence regarding conservation threats to the colony. We compared data from flying foxes collected from this roost to other P. griseus specimens and those of closely related co-occurring species to confirm its identity. We confirmed that this roost is likely of Pteropus griseus, though the subspecies identity remains to be determined. However, it is newly threatened by middlemen traders of bat meat from North Sulawesi arriving to encourage local villagers near the roost to hunt the bats. Elevated levels of hunting may deplete the entire colony in a single season should no conservation action be taken to safeguard the roost.
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diversity
Communication
Roost of Gray Flying Foxes (Pteropus griseus) in
Indonesia and Records of a New Hunting Threat
Sheherazade 1and Susan M. Tsang 2, 3, *
1Wildlife Ecology and Conservation Department, University of Florida, Gainesville, FL 32603, USA;
sheherazade.jayadi@gmail.com
2Department of Mammalogy, American Museum of Natural History, New York, NY 10024, USA
3Zoology Division, National Museum of the Philippines, Padre Burgos Ave, Ermita, Metro Manila 1000,
Philippines
*Correspondence: stsang@amnh.org; Tel.: +1-917-485-3338
Received: 1 April 2018; Accepted: 14 September 2018; Published: 17 September 2018


Abstract:
Pteropus griseus (gray flying fox) is a species of Old World fruit bat that is listed by the
International Union for Conservation of Nature (IUCN) as Data Deficient. The species is found on
small islands in the Lesser Sundas and Sulawesi, and is endemic to Indonesia, but no contemporary
roosts are known, and the last study of the species was in Timor in the Lesser Sundas. In this study,
we describe the first known day roost in Sulawesi for Pteropus griseus and collected anecdotal evidence
regarding conservation threats to the colony. We compared data from flying foxes collected from
this roost to other P. griseus specimens and those of closely related co-occurring species to confirm
its identity. We confirmed that this roost is likely of Pteropus griseus, though the subspecies identity
remains to be determined. However, it is newly threatened by middlemen traders of bat meat from
North Sulawesi arriving to encourage local villagers near the roost to hunt the bats. Elevated levels of
hunting may deplete the entire colony in a single season should no conservation action be taken to
safeguard the roost.
Keywords: conservation; flying fox; Pteropodidae; roosting ecology; Sulawesi
1. Introduction
Pteropus (Mammalia: Chiroptera), commonly known as flying foxes, fulfill important ecosystem
roles as seed dispersers and pollinators [
1
8
], but are threatened by intensive hunting and habitat
conversion [
9
12
]. Many species are still poorly known because their distributions are largely
restricted to small, remote islands [
13
,
14
], which is correlated with heightened extinction risk [
15
].
Lack of information creates a significant impediment to the conservation of this highly threatened
bat taxa, but logistically this may often be a difficult knowledge gap to fill. Most flying fox species
occur in remote, marginal habitats and require dedicated effort to seek out compared to other bats,
which discourages research. In the Old World Fruit Bat Action Plan [
16
], a majority of flying fox
species do not have enough data to contribute to species threat assessments and require greater survey
and research efforts to understand Pteropus natural history and the threats species face. Without this
information, assessment of the effectiveness of conservation action and where to prioritize resources is
not possible.
One such species is Pteropus griseus (the gray flying fox), which is listed by the International
Union for Conservation of Nature (IUCN) Red List as Data Deficient [
17
]. Data Deficient species
are those defined by the IUCN as those that have “inadequate information to make a direct, or
indirect, assessment of its risk of extinction based on its distribution and/or population status” [
18
].
This definition encapsulates how little is known about this species. Pteropus griseus is endemic to
Diversity 2018,10, 102; doi:10.3390/d10030102 www.mdpi.com/journal/diversity
Diversity 2018,10, 102 2 of 11
Indonesia, and found in the Lesser Sundas, the Banda Islands, and Sulawesi. Their distribution on
relatively remote islands presents logistical challenges to researchers that discourage the collection of
data for threat assessments. Unfortunately, flying foxes are pressured intensely by hunting for the
bushmeat trade in North Sulawesi [
12
], and lack of information on the hunting system and flying
fox populations can result in a lack of conservation effort. To fuel the demand for flying foxes from
the bushmeat market in North Sulawesi province, hunters have started sourcing bats from other
provinces [
12
]. Without adequate fundamental natural history knowledge, such as habitat preferences
or roosting ecology, and population trends of P. griseus, the immediate threat of hunting may extirpate
the species before an IUCN threat status can even be conferred.
Pteropus griseus is found on small islands in the Lesser Sundas and Sulawesi [
13
,
17
], but the only
data available on their natural history originate from the work of Robert Goodwin in Timor in
1979 [
19
]. From the Goodwin (1979) study, we know that P. griseus prefers lowland forest and are
commonly found near sea level (<30 m) but will forage at higher altitudes. Goodwin found individuals
foraging on the fruits of Ficus (figs), Muntingia (the introduced Jamaica cherry), and presumably also
the fruit of Borassus (fan palms) where some individuals were found. Given the significantly different
environments, biogeographic history, and faunal and floral assemblages between Sulawesi [
20
] and
the Lesser Sundas [
21
], the subspecies P. g. mimus (Sulawesi) and P. g. griseus (Timor) likely utilize
food and spatial resources differently in their native landscapes. The Lesser Sundas has the driest and
most seasonal climate of the Indonesian archipelago [
21
], contrasting with the climate of Sulawesi,
where there is no real dry season [
20
]. It is unlikely that the P. griseus of Timor have the same roosting
ecology as those of Sulawesi because of the different landscapes of these two islands. Goodwin [
19
]
only recorded solitary individuals hidden under leaves of Borassus and Corypha fan palms in Timor.
No common day roost was found, though there were no mentions of specific efforts to determine
whether the species roosted as larger groups. Additionally, the higher diversity of larger pteropodid
species on Sulawesi (14 species of Pteropodinae compared to six on Timor) presents potentially higher
competition for limited spatial resources (i.e., roost sites). Previous field expeditions by both of authors
indicated that day roosts for large colonies are primarily located in mangroves. However, mangroves
are one of the most threatened landscapes in the world [
22
] and data from other parts of Indonesia
indicate a loss of at least 80% of mangroves [
23
,
24
]. These preferred roost sites then become a limiting
resource for flying fox species that may push competition.
In this study, we describe the only known contemporary common day roost (simplified here to
“roost”) of P. griseus in Sulawesi. The roost was initially found while surveying Central Sulawesi for
flying foxes during a separate pollination study by one of the authors for her thesis work (Sheherazade,
unpublished data). The individuals of interest have obvious morphological differences from the two,
more common species (P. alecto and A. celebensis), found in Central Sulawesi. However, historically,
Sulawesi satellite islands also had closely allied species such as P. hypomelanus macassaricus and
P. speciosus, which look similar to P. griseus. The only specimens of P. griseus from Central Sulawesi
were previously collected by J. J. Menden in 1938 on the nearby island of Peleng [
13
]. However, no other
contemporary records exist for the species on Sulawesi. We aim to confirm the identity of the captured
bats as P. griseus to ensure appropriate conservation action is taken. Without presenting data to clarify
that this is different from the two more commonly hunted species (P. alecto and A. celebensis), protected
status cannot be conferred to P. griseus in Indonesia and long-term conservation management cannot
occur. We present data to confirm the species identification and include notes on its distribution and
threats. The implications for our findings regarding hunting threats are considered in greater detail as
it pertains to the persistence of the population and protection of the roost site.
2. Materials and Methods
The study was conducted on the offshore island of Mantalu Daka, Sulawesi, Indonesia in June
and November 2017 (Figure 1). This island is located within the administrative area of Longkoga
Barat/Timur Village in Bualemo subdistrict, Banggai, Central Sulawesi. Mantalu Daka is Saluan,
Diversity 2018,10, 102 3 of 11
one of the local dialects, for Big Island (Bahasa Indonesian: Pulau Besar), and is ~1.5 km in length.
A second island north of the village is called Mantalu Ise, Saluan for Small Island (Bahasa Indonesian:
Pulau Kecil), and is ~300 m in length. Plant species on the island were identified using regional and
country-specific reference guides for mangroves [23,25,26].
Diversity 2018, 10, x FOR PEER REVIEW 3 of 12
second island north of the village is called Mantalu Ise, Saluan for Small Island (Bahasa Indonesian:
Pulau Kecil), and is ~300 m in length. Plant species on the island were identified using regional and
country-specific reference guides for mangroves [23,25,26].
Figure 1. Study site in Mantalu Daka, Bualemo, Central Sulawesi.
The outer part of the island is comprised of typical coastal vegetation dominated by mangroves
(Excoecaria agallocha, Pemphis acidula, and Xylocarpus rumphii) and other secondary vegetation
(Casuarina equisetifolia, Scaevola taccada, Inocarpus fagifer, Streblus asper, Trema sp., Premna corymbosa,
and spiny forests). Crop plants, such as coconut, papaya, mango, and corn, planted by the local
people were also found on the island. The fishermen and farmers commute between nearby villages
on the mainland of Sulawesi and Mantalu Daka, but there are no permanent inhabitants on the
island due to the lack of freshwater and high prevalence of mosquitoes. The inner core of the island
consisted of dense spiny forest with quicksand pits, gradually deepening into a mangrove swamp.
We captured flying foxes following procedures described in Methods of Capturing and
Handling Bats [27], with some modifications to minimize disturbance caused by capturing activities
(S. Wiantoro, pers. comm., 2018). All protocols were approved by the University of Florida under
Institutional Animal Care and Use Committee (IACUC) protocol #201709800. We stacked two mist
nets (Avinet 2.6 × 9 m, 38 mm mesh size, 4 shelves) using a double pulley system on a pair of 10 m
aluminum poles placed at the edge of the island near a known flyway far from the day roost. The
roost was found while one of the authors (Sheherazade) was surveying Central Sulawesi for sites to
conduct a pollination experiment and determined there were three, not two species, at that roost
when capturing the bats to swab their fur. We opened the mist nets from 2:00 a.m. to 6:00 a.m. to
capture flying foxes returning to their roost. We previously conducted reconnaissance on the island
to determine all possible flyways returning to the roost. We adjusted the position of the mist nets at
least 100 m away from the previous position around the perimeter of the island every two or three
nights to prevent permanent shifts in the flight paths used by the bats and to reduce predictability of
mist net position. The island is not very large (area under 0.5 km2) and we were limited in how far
Figure 1. Study site in Mantalu Daka, Bualemo, Central Sulawesi.
The outer part of the island is comprised of typical coastal vegetation dominated by mangroves
(Excoecaria agallocha,Pemphis acidula, and Xylocarpus rumphii) and other secondary vegetation
(Casuarina equisetifolia,Scaevola taccada,Inocarpus fagifer,Streblus asper,Trema sp., Premna corymbosa,
and spiny forests). Crop plants, such as coconut, papaya, mango, and corn, planted by the local people
were also found on the island. The fishermen and farmers commute between nearby villages on the
mainland of Sulawesi and Mantalu Daka, but there are no permanent inhabitants on the island due to
the lack of freshwater and high prevalence of mosquitoes. The inner core of the island consisted of
dense spiny forest with quicksand pits, gradually deepening into a mangrove swamp.
We captured flying foxes following procedures described in Methods of Capturing and Handling
Bats [
27
], with some modifications to minimize disturbance caused by capturing activities (S. Wiantoro,
pers. comm., 2018). All protocols were approved by the University of Florida under Institutional
Animal Care and Use Committee (IACUC) protocol #201709800. We stacked two mist nets
(Avinet 2.6
×
9 m, 38 mm mesh size, 4 shelves) using a double pulley system on a pair of 10 m aluminum
poles placed at the edge of the island near a known flyway far from the day roost. The roost was
found while one of the authors (Sheherazade) was surveying Central Sulawesi for sites to conduct a
pollination experiment and determined there were three, not two species, at that roost when capturing
the bats to swab their fur. We opened the mist nets from 2:00 a.m. to 6:00 a.m. to capture flying
foxes returning to their roost. We previously conducted reconnaissance on the island to determine all
possible flyways returning to the roost. We adjusted the position of the mist nets at least 100 m away
from the previous position around the perimeter of the island every two or three nights to prevent
permanent shifts in the flight paths used by the bats and to reduce predictability of mist net position.
The island is not very large (area under 0.5 km
2
) and we were limited in how far apart we could place
the mist nets since bats were returning primarily from the southeast, where Mt. Tompotika is located.
Diversity 2018,10, 102 4 of 11
We immediately extracted each flying fox from the net upon capture, recorded the sex and age class
(adult, subadult, or juvenile determined by joint fusion [
28
]), and measured external characteristics
(forearm length, ear length, hind foot length, greatest skull length, and mass) using digital calipers and
Pesola scales. We placed a small dot of non-toxic nail polish on one of the hind foot claws to indicate
capture and prevent resampling of the same individual prior to release.
We compared species identities and measurements to flying foxes caught in 2012 from Central
Sulawesi by one of the authors (Susan M. Tsang) and Sigit Wiantoro. These specimens have previously
been verified by a combination of genetic analyses and comparison to reference material and natural
history collection notes [
29
,
30
]. This includes comparative material to P. hypomelanus macassaricus,
which has an overlapping distribution with some P. griseus subspecies in Sulawesi.
Along with some local community members, we conducted a bi-weekly preliminary census via an
emergence count in June and November 2017 starting at dusk when the bats first leave the roost until
all had completed their exit. Anecdotal evidence about roost characteristics and flying fox hunting
were also collected from hunters and fisherman in nearby villages, and evidence and equipment from
past hunting events were collected.
3. Results
The P. griseus roost was located at the center of the mangrove swamp on Mantalu Daka.
We were unable to identify the mangrove tree species in the central swamp due to the lack of visible
roots and flowers. The inner core of spiny forest and quicksand pits make the inner core of the
mangrove, where the bats primarily roost, difficult to traverse.
Three species of flying foxes were identified at the roost during a reconnaissance survey in
December 2016—Pteropus griseus,P. alecto (black flying fox), and Acerodon celebensis (Sulawesi flying
fox). The latter two species are easily identified by sight given their significantly larger size and distinct
coloration—P. alecto is entirely dark brown to black with a forearm (FA) range of 140 to 175 mm,
and A. celebensis is blonde with a brown face with a FA range 125 to 142 mm. In contrast, P. griseus
is smaller (FA range of 113 to 130 mm) and has a lighter gray head with a body in various shades of
brown [
13
]. In total, 52 flying foxes were captured (33 individuals in June and 19 individuals in
November) after a total of 72 mist net hours. All captures of adults were P. griseus. Of the total
number of P. griseus captured, only 17 were adults, with the rest a mix of juveniles and subadults.
We captured only one juvenile of A. celebensis in June. Both P. alecto and A. celebensis flew much higher
than P. griseus and would require higher canopy nets to capture, which was not possible given the
coastal terrain.
Pteropus griseus was the smallest species found on the island (Table 1, and see Supplementary
Table S1 for all data along with measurements of historical specimens at Museum Zoologicum
Bogoriense, Indonesian Institute of Sciences (MZB-LIPI)). One individual was excluded from the
morphological analyses because its greatest skull length (GSL) was anomalously large (99.2 mm),
although all other features conformed to P. griseus. The skull measurements would be outside the
range of any of the potential species and would require further investigation to confirm its species
identity. We ruled out the possibility of our captured individuals being P. hypomelanus macassaricus since
our captures had significantly smaller forearm lengths (t=
2.01, p< 0.05). Additionally, we ruled out
P. speciosus (at one point considered a subspecies of P. griseus) since our captures were significantly larger.
The range of morphological measurements from this study also generally agree with that of Bergmans
and Rozendaal’s examination of Sulawesi pteropodids [
31
], which gives a forearm range of 118 to
128 mm for P. griseus. While it was difficult to confirm the subspecies identities of the individuals in this
study based on scant external characteristics data from reference material, the pelage coloration was
rather distinct in those captured in Mantalu Daka. Pteropus griseus on this island had a brown-orange
mantle, a tawny (orange-brown or yellow-brown) underbelly, mixing with light grayish hairs as the
ventral fur neared the tibia. The head and face were distinctly light gray, darkening somewhat near the
crown, and fur was scant around the eyes and muzzle (Figure 2). There were a couple of individuals
Diversity 2018,10, 102 5 of 11
noted in photographs that differed in the head coloration (a darker gray-brown rostrum surrounded
by brown-orange), but none of these were captured in hand for comparison. Andersen [
30
] describes
P. g. mimus as having a brown and tawny coloration, P. g. pallidus as dark brown with flecks of pale
gray hairs, and P. g. griseus as similar to P. g. mimus but considerably lighter in color. This pelage
coloration would lend support for identification as P. g. griseus, but more study over the course of
the year is needed to determine whether the pelage observed in this study represents only a single
phase of coloration. For nightly foraging, P. griseus were observed going to the dense, more species-rich
rainforest of Mt. Tompotika on mainland Sulawesi to forage.
Diversity 2018, 10, x FOR PEER REVIEW 5 of 12
and muzzle (Figure 2). There were a couple of individuals noted in photographs that differed in the
head coloration (a darker gray-brown rostrum surrounded by brown-orange), but none of these
were captured in hand for comparison. Andersen [30] describes P. g. mimus as having a brown and
tawny coloration, P. g. pallidus as dark brown with flecks of pale gray hairs, and P. g. griseus as
similar to P. g. mimus but considerably lighter in color. This pelage coloration would lend support for
identification as P. g. griseus, but more study over the course of the year is needed to determine
whether the pelage observed in this study represents only a single phase of coloration. For nightly
foraging, P. griseus were observed going to the dense, more species-rich rainforest of Mt. Tompotika
on mainland Sulawesi to forage.
Figure 2. (a) Pteropus griseus roosting in the mangrove swamp showing ventral coloration; and (b) P.
griseus in hand, showing light head coloration.
Figure 2.
(
a
)Pteropus griseus roosting in the mangrove swamp showing ventral coloration;
and (b)P. griseus in hand, showing light head coloration.
During the first capture season in June 2017, a large, mixed colony of flying foxes was recorded
emerging at dusk every day, with a steady stream of bats that lasted approximately 25 min.
The bats were primarily of larger individuals, likely P. alecto or A. celebensis. The identity of the
bats as P. alecto or A. celebensis was corroborated by what hunters were taking to the market. However,
the colony size shrank by November and emergence took only 10 min and the flow of bats was largely
reduced. Only small to medium individuals were seen, presumably P. griseus. Based on the preliminary
census, there were around 300 to 500 bats. According to the local people, the higher level of hunting was
initiated by the arrival of middlemen traders of bat bushmeat from North Sulawesi in 2017 requesting
that locals hunt the bats. Hunting occurs throughout the year, with peaks in June and November.
Pteropus alecto and A. celebensis were intensely hunted and comprised a majority of the hunters’ take
because they roosted on the outer part of the island, making them considerably easier to catch and
more accessible. Pteropus griseus roosted in the inner part of the island surrounded by swamps and
mosquito swarms, which makes they more difficult to catch but not exempt from hunting pressure.
The middlemen did not appear during the second capture season (November 2017), and there were no
longer any groups of P. alecto and A. celebensis readily visible at the outer edge of the island. However,
given that our captures were only of P. griseus and the only bats seen were small, we do not think a
substantial group of P. alecto or A. celebensis are found any longer on this island. There were no other
reports of any sizeable groups of bats suddenly appearing elsewhere either. We ruled out migration of
flying foxes to follow food resources as there were no fruit masting events in Sulawesi in 2017 that
would cause a large colony to relocate to another site, and there was no subsequent return after a year
had passed reported by the villagers or local conservationists. Fishing hooks and ropes were found
along the flight path used by P. griseus (Figure 3). This equipment was commonly used to hunt flying
foxes in Central Sulawesi. Tens of fishing hooks were hung along a rope that spans between two tall
trees in the bat flight path. The wings would then be torn by the hooks, causing the bats to fall to
the ground or to be stuck on the hooks. Hunters would leave the equipment overnight and collect
the flying foxes the next morning. Some hunters also used large slingshots to shoot the bats directly
(Figure 3). Using these methods, a few hunters could gather tens to hundreds of flying foxes per day
according to the estimates given to us by the local villagers of Longkoga Barat/Timur.
Diversity 2018,10, 102 6 of 11
Table 1.
Morphological measurements (mean and range) of adult Pteropus griseus captured in Central Sulawesi in this study (n= 16) compared to other references.
One rogue taxa was omitted from the morphological analyses due to its anomalously larger greatest skull length (99.2 mm). All measurements are in millimeters or
grams. Character codes are as follows: FA = forearm length; GSL = greatest skull length; HF = hind foot length. Comparisons were made with specimens collected by
Johannes J. Menden on Peleng Island (deposited at American Museum of Natural History (AMNH)), unpublished data from expeditions by Susan M. Tsang and
Sigit Wiantoro in 2012 and from the literature, including Andersen (1912) [30] and Kitchener and Maryanto (1995) [29].
Measurements This Study P. griseus
Peleng Isl.
P. h.
macassaricus
P. h.
macassaricus P. g. mimus P. g. griseus P. g. griseus P. g. pallidus P. g. pallidus P. speciosus
Source Sheherazade J.J. Menden
(AMNH)
Tsang and
Wiantoro Andersen Andersen
Kitchener
and
Maryanto
Andersen Kitchener and
Maryanto Andersen Andersen
n16 4 3 4 Paratype 10 4 6 5 2
Mean FA 126.06 - 131.8 - 127.5 119.3 - 126.6 - 121.75
Range 116–131 - 123–138 131–145 - 113.8–128.1 114.5–118 121.4–129.9 113.5–119 120.5–123
Mean GSL 60.79 59 - 64 59.8 56.26 - 56.39 - 57
Range 55.9–70.15 58.2–60.0 - - - 54.69–59.19 - 54.80–59.44 56–59 -
Mean Mass 292.13 - 273.33 - - - - - - -
Range 230–370 - 210–310 - - - - - - -
Diversity 2018,10, 102 7 of 11
Diversity 2018, 10, x FOR PEER REVIEW 7 of 12
During the first capture season in June 2017, a large, mixed colony of flying foxes was recorded
emerging at dusk every day, with a steady stream of bats that lasted approximately 25 min. The bats
were primarily of larger individuals, likely P. alecto or A. celebensis. The identity of the bats as P. alecto
or A. celebensis was corroborated by what hunters were taking to the market. However, the colony
size shrank by November and emergence took only 10 min and the flow of bats was largely reduced.
Only small to medium individuals were seen, presumably P. griseus. Based on the preliminary
census, there were around 300 to 500 bats. According to the local people, the higher level of hunting
was initiated by the arrival of middlemen traders of bat bushmeat from North Sulawesi in 2017
requesting that locals hunt the bats. Hunting occurs throughout the year, with peaks in June and
November. Pteropus alecto and A. celebensis were intensely hunted and comprised a majority of the
hunters’ take because they roosted on the outer part of the island, making them considerably easier
to catch and more accessible. Pteropus griseus roosted in the inner part of the island surrounded by
swamps and mosquito swarms, which makes they more difficult to catch but not exempt from
hunting pressure. The middlemen did not appear during the second capture season (November
2017), and there were no longer any groups of P. alecto and A. celebensis readily visible at the outer
edge of the island. However, given that our captures were only of P. griseus and the only bats seen
were small, we do not think a substantial group of P. alecto or A. celebensis are found any longer on
this island. There were no other reports of any sizeable groups of bats suddenly appearing elsewhere
either. We ruled out migration of flying foxes to follow food resources as there were no fruit masting
events in Sulawesi in 2017 that would cause a large colony to relocate to another site, and there was
no subsequent return after a year had passed reported by the villagers or local conservationists.
Fishing hooks and ropes were found along the flight path used by P. griseus (Figure 3). This
equipment was commonly used to hunt flying foxes in Central Sulawesi. Tens of fishing hooks were
hung along a rope that spans between two tall trees in the bat flight path. The wings would then be
torn by the hooks, causing the bats to fall to the ground or to be stuck on the hooks. Hunters would
leave the equipment overnight and collect the flying foxes the next morning. Some hunters also used
large slingshots to shoot the bats directly (Figure 3). Using these methods, a few hunters could
gather tens to hundreds of flying foxes per day according to the estimates given to us by the local
villagers of Longkoga Barat/Timur.
Figure 3. Hunting equipment for flying fox: (a) fishing hooks; (b) remains of a flying fox wing ripped
by a fishing hook; (c) slingshot used to shoot the bats.
According to the people of Longkoga Barat/Timur village, flying fox hunting on the island is
driven by demand for bushmeat from markets in North Sulawesi. As noted from our previous
study, the extirpation of flying fox colonies from North Sulawesi province has driven hunters to
attempt to source bats from other provinces instead [12]. The villagers reported intense hunting
occurred between the two capture seasons in this study, resulting in a noticeable decrease in the
observable colony size due to hunting-related loss of bats or relocation to another island. During the
beginning of this study, the three flying fox species were always seen on the island, but only P.
griseus was found during the second capture season. A middleman trader came to Longkoga
Barat/Timur village and asked the villagers to hunt the flying foxes for them. Each flying fox was
Figure 3.
Hunting equipment for flying fox: (
a
) fishing hooks; (
b
) remains of a flying fox wing ripped
by a fishing hook; (c) slingshot used to shoot the bats.
According to the people of Longkoga Barat/Timur village, flying fox hunting on the island is
driven by demand for bushmeat from markets in North Sulawesi. As noted from our previous study,
the extirpation of flying fox colonies from North Sulawesi province has driven hunters to attempt to
source bats from other provinces instead [
12
]. The villagers reported intense hunting occurred between
the two capture seasons in this study, resulting in a noticeable decrease in the observable colony size
due to hunting-related loss of bats or relocation to another island. During the beginning of this study,
the three flying fox species were always seen on the island, but only P. griseus was found during the
second capture season. A middleman trader came to Longkoga Barat/Timur village and asked the
villagers to hunt the flying foxes for them. Each flying fox was worth Rp 5000, or USD 0.36. This was
an order of magnitude lower for the bats compared to the market price in North Sulawesi (Rp 50,000
or USD 3.63 per individual).
4. Discussion
The discovery of a day roost of P. griseus overturns previous misconceptions that they only occur
as individuals or small groups [
32
], and their colonial roosting habits should spur on further action to
document roost sites. Additionally, the discovery of a roost of P. griseus within the reach of hunters
and middlemen from the North Sulawesi market should spur more conservation action, as this is the
only known existing roost of P. griseus.
In their review of specimens collected from Sulawesi and its satellite islands, Bergmans and
Rozendaal [
31
], notes that P. g. mimus was found on Selayar, in South Sulawesi, and its type locality is
Ujung Padang (present day Makassar), also in South Sulawesi. There are no modern (post-1970s)
records of P. griseus near Makassar. Despite Bergmans and Rozedaal [
31
] publishing on P. griseus in
1988, they only examined historical specimens from 1908 and did not conduct any new fieldwork
Type specimens of P. griseus from Sulawesi date back to the late 19th century. The elevated level of
development around Makassar, the largest city on Sulawesi, makes it rather unlikely that P. griseus
are found near there anymore. The historical distribution and the newly discovered roost in this
study point to a species distribution that is largely restricted to the satellite islands of Sulawesi,
not the Sulawesi mainland. Here, we observed the species primarily flying to foraging areas on
mainland Sulawesi closest to their roosts and then returns to their roost at dawn. This is a distance of
about 20 to 25 km each way only. However, the current IUCN range map has all of Sulawesi shaded
as part of the distribution of P. griseus, which is likely an overestimation (Figure 4). Additionally,
one of the authors (Susan M. Tsang) and her collaborators have conducted multiple expeditions
starting in 2012 to the present in Sulawesi, with concentrated efforts in Central Sulawesi, and have not
discovered any groups of P. griseus. The IUCN Red List map [
17
] needs to be updated to reflect the
restricted distribution of P. griseus, as its limited distribution on small islands means that it faces
heightened extinction risk.
Diversity 2018,10, 102 8 of 11
Diversity 2018, 10, x FOR PEER REVIEW 9 of 12
Figure 4. Map of suggested distribution (orange) for Pteropus griseus in Sulawesi for the IUCN Red
List. The distribution takes into account precise localities where P. griseus has been found and
represented by collection and observation records. We have included the current IUCN Red List
distribution (striped pink) in order to highlight the large difference in geographic range estimates for
Sulawesi using the old distribution. This maps excludes Pteropus griseus from other major
archipelagoes in Indonesia.
Flying fox conservation should be addressed by action at both the markets and at the roost.
While hunting can occur at the roost or at foraging sites, roost protection is one of the most
important actions to ensure persistence of a flying fox species, particularly when roost sites are
known and threats are acute and can be contained [11]. Working in collaboration with the local
village, such as Longkoga Barat/Timur in this study, roost protection and environmental education
about the importance of flying foxes to the ecosystem and human livelihoods can act as successful
efforts to rebuff hunting [10,11]. As the authors have previously suggested in their market study
[12], it is important to recognize that bushmeat consumption is tightly linked to religious holidays
and reducing demand with conservation non-governmental organizations (NGOs), relevant
government agencies, and churches in North Sulawesi is important to the overall goal of flying fox
conservation in all of Sulawesi. The loss of flying foxes may have profound impacts on native
Figure 4.
Map of suggested distribution (orange) for Pteropus griseus in Sulawesi for the IUCN Red List.
The distribution takes into account precise localities where P. griseus has been found and represented
by collection and observation records. We have included the current IUCN Red List distribution
(striped pink) in order to highlight the large difference in geographic range estimates for Sulawesi using
the old distribution. This maps excludes Pteropus griseus from other major archipelagoes in Indonesia.
The signs of disappearances of P. alecto and A. celebensis suggest an alarming population trend in
flying fox species that will likely be mirrored in P. griseus should no conservation action be taken.
As the other species become rarer, it is likely that hunters will enter further into the swamp and
locate the P. griseus roost. Hunting at the roost poses a direct threat to the survivorship of individuals.
Hunting activity can also indirectly decrease survivorship due to frequent roost disturbances leading to
injuries, higher stress, or large-scale infant mortality from when fleeing mothers drop pups [
11
].
The small colony size of P. griseus makes the species especially vulnerable to hunting. While the
preliminary census requires more repeated counts to obtain a more precise measure of the colony
size, the estimate of 300 to 500 individuals only in November 2017 is few enough bats that a hunter
could wipe out the colony after a single season of hunting events. Given the current observed rate of
hunting, the roost would likely face extirpation should this be allowed to continue. A change in the
IUCN Red List status to Endangered may be warranted for the species, as this is the only known roost
Diversity 2018,10, 102 9 of 11
currently, it faces a direct threat from intensive hunting, the roost does not exist in a protected area and
no action is currently being taken, and there are only several hundred individuals. Hunting of flying
foxes in Sulawesi has already extirpated colonies of flying foxes closer to the North Sulawesi markets
and the expansion of the North Sulawesi hunting network to other Sulawesi provinces was noted
by hunters in a previous study conducted by the authors in 2013 [
12
], and now recorded first-hand
in this study. We have begun to monitor the population more closely and are exploring options for
conservation action to promote the persistence of P. griseus on this island. This colony may represent
one of the only opportunities to study the roosting ecology and diet of the species, and its protection
should be considered a high conservation priority.
Flying fox conservation should be addressed by action at both the markets and at the roost.
While hunting can occur at the roost or at foraging sites, roost protection is one of the most important
actions to ensure persistence of a flying fox species, particularly when roost sites are known and threats
are acute and can be contained [
11
]. Working in collaboration with the local village, such as Longkoga
Barat/Timur in this study, roost protection and environmental education about the importance of flying
foxes to the ecosystem and human livelihoods can act as successful efforts to rebuff hunting [
10
,
11
].
As the authors have previously suggested in their market study [12], it is important to recognize that
bushmeat consumption is tightly linked to religious holidays and reducing demand with conservation
non-governmental organizations (NGOs), relevant government agencies, and churches in North
Sulawesi is important to the overall goal of flying fox conservation in all of Sulawesi. The loss of flying
foxes may have profound impacts on native ecosystems and human well-being due to loss of their
ecological services important to ecologically and economically important plants [
33
36
]. In particular,
flying foxes in Sulawesi have significant roles as durian pollinators, which are of great economic
significance at the local and national level (Sheherazade, pers. obs.).
This study highlights how little fundamental knowledge we have of flying foxes and where they
are and is a call to action to address the most basic recommendation expressed in the Old World
Fruit Bat Action Plan in 1992—surveying to collect distribution, habitat, or ecological information.
Surveys are especially important in poorly studied areas with high pteropodid species richness.
Compared to other pteropodid species, Pteropus species require specific, dedicated efforts to find,
monitor, and study, making them particularly vulnerable to lack of data being an impediment to
creating conservation management plans. Based on the current global flying fox distribution data,
remote islands likely provide an important refuge for Pteropus species, but which islands and what
kind of landscapes has not been clarified due to lack of research efforts. However, island landscapes
are some of the most threatened by climate change due to eustatic sea level rise. Consequently,
these islands may become rarer in the future and result in flying fox colonies roosting at suboptimal
sites, i.e., closer to villages in more accessible forests. This presents more opportunities for hunting to
occur, as it will become easier and knowledge of flying fox colony locations will increase among the
public. To discourage hunting, engagement with more local communities would not only serve to help
with local conservation action but also with locating roost sites in remote areas where researchers have
yet to explore. This engagement creates critical opportunities for perception changes that can benefit
conservation, as local communities can become a part of the discovery and management process.
Supplementary Materials:
The following are available online at http://www.mdpi.com/1424-2818/10/3/102/s1,
Table S1: Raw measurement data of Pteropus griseus captured in this study.
Author Contributions: S.M.T. and S.S. both conceived and designed the study, did the fieldwork, and wrote the
paper. S.M.T. did the taxonomic work and literature review.
Funding:
Funding for this study was provided by the Center for International Forestry–USAID Indonesia, Rufford
Small Grant 21903-1, Bat Conservation International, Tropical Conservation and Development University of
Florida, and IdeaWild to Sheherazade. Past fieldwork for Susan M. Tsang was funded by the American
Philosophical Society, the National Geographic Society (9272-13), the Fulbright Student Research Fellowship,
and the National Science Foundation (OISE-1108298).
Diversity 2018,10, 102 10 of 11
Acknowledgments:
We thank Government Agency of Maritime Affairs and Fisheries of Central Sulawesi,
Integrated Permit Service Agency of Central Sulawesi, Ministry of Research, Technology, and Higher Education
(RISTEK), and local Nature Conservation Agency (Balai Konservasi Sumber Daya Alam, BKSDA) for permits and
field assistance. We thank Sigit Wiantoro for his friendship, expertise, and assistance in granting access to collection
material at MZB-LIPI. We thank Holly Ober, Todd Palmer and Bette Loiselle for advising and feedback that have
greatly improved this research. Last but not least, the people of Longkoga Barat/Timur and Alliance for Tompotika
Conservation for their support and assistance; Wendy Achmmad Mustaqim for the help for plant identification;
Asnim Alyoihana Lanusi, Silvi Dwi Anasari, Zulfikar Hekmatyar, Muh. Fatsul Syawal Dg Matorang, Zainullah
Putra Asila, Eka, Ramlin, Om Ambi, Om Barka, and Om Darto for their assistance in the field. Thanks as well to
the two anonymous reviewers whose comments greatly improved this manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
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... In more developed areas, day roosts may occur at "safe" locations such as botanical gardens, temples, or culturally significant sites. Some roosts in the Philippines and Indonesia also have been or are being developed into ecotourism objects, which can then afford them some level of protection locally, though balancing the needs of the bats with tourism demands requires careful management to ensure sustainable development (e.g., Sheherazade, 2018;Aguirre, 2020;Santosa et al., 2020). The work of NGOs with local governments and communities can also lead to the establishment of flying fox sanctuaries at priority sites, providing critical formal protection and monitoring (BCI, 2016). ...
... Only a handful of countries where flying foxes are native have formal national legislation that considers them a protected species, such as Australia, Malaysia, and Thailand (more complete list of legislation in Aziz et al. (2016)) and have implemented hunting bans or limit the number of hunting licenses issued. At some sites, formal protection on a community or local level is possible (Sheherazade, 2018). This is particularly important for safeguarding roosting sites for threatened flying fox species along with creating community buy-in for protection of the bats in the long-term. ...
Chapter
Island taxa face heightened extinction risk due the lower population sizes, reduced land area, and barriers to dispersal. These factors combined with global climate change and anthropogenic pressure intensify the level of extinction that threaten island species. A group that is experiencing these types of threats are the flying foxes—giant fruit bats that are found on islands throughout the Paleotropics. As some of the only larger bodied frugivores or nectarivores in island ecosystems, these species are important keystone taxa that provide pollination and seed dispersal services to the plant community. Hunting, habitat loss, and climate change all threaten flying foxes and jeopardize the stability of island ecosystems. While some formal legal protection is afforded in parts of their range, flying foxes still require more conservation intervention to help species recover and persist through these challenging times. These actions can range from activities that directly impact species survival, such as roost protection and captive breeding, to the broader need for public awareness and education to reduce persecution against these bats. There are also multiple gaps in knowledge about their natural history that need to be filled should well-informed policymaking and conservation hope to save these bats for future generations.
... Bushmeat trade has been widely recognized as having a strong impact on animal populations (Ling and Milner-Gulland, 2006). Regarding flying-foxes, hunting has been probably the main factor leading to the extinction of P. tokudae on Guam (IUCN, 2020a; Pierson and Rainey, 1992a;Sheherazade and Tsang, 2018;Vincenot et al., 2017b;Wiles and Payne, 1986). Poaching can occur directly at roosts, leading to a large number of animals killed in addition to disturbance, the latter being identified as one of the main factor causing roost desertion (MacKinnon et al., 2003;Niel and Lebreton, 2005;Pierson and Rainey, 1992a). ...
Thesis
Full-text available
Habitat degradation, invasive species and overexploitation are currently the three main threats to biodiversity. Here we present a study on the population status of two sympatric flying fox species, Pteropus ornatus (endemic) and P. tonganus (native), and the impact of hunting and predation by the feral cat Felis catus in New Caledonia. The study of flying fox roost occupancy in the North Province shows a 33% disapearance in 40 years. The flying fox population on Grande Terre is estimated at about 735,000 individuals (of both species) and the annual hunting rate at 7%. Integrated stochastic modelling of this population suggests that current harvesting levels could lead to a decline of up to 80% in the next 30 years. Temporary hunting ban and/or protected areas appear, in addition to being combinable, to be the most acceptable and effective management options for hunters. An analysis of the data available worldwide shows that all forms of cats prey on bats in all habitats and that this threat is probably largely underestimated. Finally, initial results suggest that flying fox predation by feral cats in New Caledonia is of the same order of magnitude as hunting. This study proposes a framework for assessing the sustainability of hunting game species in an integrated adaptive management approach, taking into account other threat factors such as invasive species.
... The species can be generally found roosting in areas close to human settlements. Recently, A. celebensis has been classified as Vulnerable by the IUCN (The International Union for Conservation of Nature) Red List due to declining populations in some areas [22] and based on CITES (Convention of International Trade on Endangered Flora and Fauna Species), this species is included in Appendix II. Apart from hunting and trading threats in the northern part of the island [23,24], disturbances and clearing of roosting trees have also been identified as one causes of species decline. ...
... Citations Genus Pteropus P. alecto (Webb and Tidemann, 1995;Loughland, 1998;Palmer and Woinarski, 1999;Vardon and Tidemann, 2000;Palmer et al., 2000;Vardon et al., 2001;Markus, 2002;Markus and Blackshaw, 2002;Helgen, 2004;Markus and Hall, 2004;Fox, 2006;Phillips et al., 2007;Saroyo, 2011;Maryanto et al., 2011;Roberts et al., 2012;Sheherazade and Tsang, 2015;Neaves et al., 2018;Sheherazade et al., 2019;Tsang et al., 2019) P. aruensis (Lee et al., 2017) P. caniceps (Flannery, 1995;Tsang et al., 2019) P. chrysoproctus (Flannery, 1995;Tsang et al., 2015Tsang et al., , 2019Tsang, 2016a) P. conspicillatus (Webb and Tidemann, 1995;Fox, 2006;Parsons et al., 2006Parsons et al., , 2010Fox et al., 2008Fox et al., , 2012Shilton et al., 2008;Almeida et al., 2014;Tait et al., 2014;Neaves et al., 2018;Westcott et al., 2018;Tsang et al., 2019) P. hypomelanus (Flannery, 1995;Jones and Kunz, 2000;Bastian Jr. et al., 2002;Colgan and da Costa, 2002;Saroyo, 2011;Almeida et al., 2014;Thong et al., 2015;Aziz et al., 2017cAziz et al., , 2017bAziz et al., , 2017aOo et al., 2017) P. griseus (Goodwin, 1979;Kitchener and Maryanto, 1995;Mickleburgh et al., 2009;Saroyo, 2011;Almeida et al., 2014;Sheherazade and Tsang, 2018;Tsang et al., 2019) P. keyensis (Flannery, 1995) P. lombocensis (Kitchener and Maryanto, 1995;Mickleburgh et al., 2009;Almeida et al., 2014;Tsang, 2016b;Tsang et al., 2019) P. macrotis (Flannery, 1995;Almeida et al., 2014) P. melanopogon (Flannery, 1995;Tsang et al., 2015) P. melanotus (Aul et al., 2014;Flakus et al., 2014;Woinarski et al., 2014;Phalen et al., 2018;Todd et al., 2018) P. neohibernicus (Flannery, 1995;Bonaccorso, 1998;Breed et (Flannery, 1995;Maryanto and Kitchener, 1999;Almeida et al., 2014;Wiantoro and Maryanto, 2016;Tsang et al., 2019) P. pohlei (Almeida et al., 2014;Flannery, 1995) P. pumilus (Bastian Jr. et al., 2002;Riley, 2002;Paguntalan and Jakosalem, 2004;O'Malley et al., 2006;Alcazar et al., 2008;Almeida et al., 2014;Deligero, 2018;Tsang et al., 2019) P. speciosus (Bastian Jr. et al., 2002;Almeida et al., 2014) P. temminckii (Flannery, 1995;Helgen and Bonaccorso, 2013;Tsang et al., 2015, 2019) P. vampyrus Mohd-Azlan et al., 2001;Bastian Jr. et al., 2002;van Weerd and Guerrero, 2003;Gumal, 2004;Paguntalan and Jakosalem, 2004;Cayunda et al., 2004;Esselstyn et al., 2004;Mildenstein et al., 2005;Stier and Mildenstein, 2005;Struebig et al., 2007;Soegiharto, 2009;Epstein et al., 2009;Breed et al., 2010;Harrison et al., 2011;Scheffers et al., 2012;Croes, 2012;Clements, 2013;Almeida et al., 2014;Bennett and Roth, 2015;Chng et al., 2015Chng et al., , 2016Tanalgo, 2017;Tsang et al., 2018Tsang et al., , 2019) Genus Acerodon Acerodon celebensis (Almeida et al., 2014;Flannery, 1995;Riley, 2002;Lee et al., 2005;Mickleburgh et al., 2009;Saroyo, 2011;Tsang, 2015, 2018;Tsang and Sheherazade, 2016;Sheherazade et al., 2019;Tsang et al., 2019) Acerodon humilis (Flannery, 1995;Riley, 2002;Lee et al., 2005) Acerodon mackloti ...
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... Bushmeat trade has been widely recognized as having a strong impact on animal populations [62]. Regarding flying-foxes, hunting has been probably the main factor leading to the extinction of P. tokudae on Guam [11,13,20,63,64]. Poaching can occur directly at roosts, leading to a large number of animals killed in addition to disturbance, the latter being identified as one of the main factor causing roost desertion [20,51,65]. ...
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... Data-deficient species can be under immediate threat and require urgent conservation action, as a recent paper highlights for the gray flying fox (Pteropus griseus), a species classified as data deficient but rapidly disappearing because of hunting pressures in Indonesia. 188 Lack of data on populations also inhibits scientific inquiry to identify stressors or determine whether conservation actions result in desired outcomes. Unsurprisingly, the problem of data deficiency is not evenly distributed across the planet and vexingly peaks in tropical regions, such as Amazonia and equatorial Africa, where bat species richness is highest but resources for research and management are more limited (Fig. 1). ...
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