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Abstract

Flying foxes are important ecological keystone species on many archipelagoes, and Indonesia is home to over a third of all flying fox species globally. However, the amount of research on this clade belies their importance to natural systems, particularly as they are increasingly threatened by anthropogenic development and hunting. Here, we provide a review of the literature since the publication of the Old World Fruit Bat Action Plan and categorize research priorities as high, medium, or low based on the number of studies conducted. A majority of the research priorities for Indonesian endemics are categorized as medium or high priority. Low priority ratings were in multiple categories for widespread flying fox species found throughout Southeast Asia, though much of the data were from outside of the Indonesian extent of the species range. These research gaps tend to highlight broader patterns of research biases towards western Indonesia, whereas significant research effort is still needed in eastern Indonesia, particularly for vulnerable island taxa. ABSTRAK Kalong merupakan spesies kunci yang memiliki peran penting bagi ekosistem, dan lebih dari sepertiga jumlah spesies yang ada di dunia, ditemukan di Indonesia. Namun, jumlah penelitian tentang spesies kalong tidak mencerminkan akan nilai penting kalong bagi ekosistem dan semakin meningkatnya ancaman akibat aktivitas manusia dan perburuan. Studi ini menyajikan tinjauan literatur yang diterbitkan setelah munculnya publikasi Rencana Aksi Pengelolaan Kelelawar Pemakan Buah (Old World Fruit Bat Action Plan) dan menentukan prioritas penelitian yang meliputi kategori tinggi, sedang dan rendah berdasarkan jumlah studi yang telah dilakukan. Sebagian besar prioritas penelitian untuk spesies endemik Indonesia termasuk di dalam kategori sedang atau tinggi. Penelitian yang dikategorikan sebagai prioritas rendah adalah untuk penelitian spesies kalong yang memiliki daerah distribusi sangat luas meliputi Kawasan Asia Tenggara, meskipun sebagian besar data yang digunakan tidak berasal dari daerah distribusi kalong di Indonesia. Kesenjangan penelitian saat ini dikarenakan adanya kecenderungan untuk melakukan penelitian di kawasan bagian barat Indonesia, padahal upaya untuk melakukan penelitian di kawasan timur Indonesia masih sangat diperlukan, terutama kelompok taksa yang rentan terhadap ancaman dan memiliki sebaran terbatas di pulau tertentu. Kata kunci: kalong, konser vasi, Pter opodidae, Pteropus, ancaman Indonesia is home to over a third of all flying foxes (sensu stricto genus Pteropus and Acerodon, Simmons, 2005); however, research on them is limited relative to other vertebrate taxa, especially mammals, making it difficult to monitor species and create conservation management plans. Yet, they constitute some of the most ecologically important and threatened species on the IUCN Red List and have a plethora of potential threats that cannot 103
Treubia 46: 103113, December 2019
DOI: 10.14203/treubia.v46i0.3792
REVIEW
INDONESIAN FLYING FOXES: RESEARCH AND CONSERVATION STATUS
UPDATE
Susan M. Tsang1,2* and Sigit Wiantoro3
1 Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural History,
New York, New York, USA
2 Mammalogy Section, National Museum of Natural History of the Philippines, Manila, Philippines
3 Zoology Division (Museum Zoologicum Bogoriense), Research Center for Biology, Indonesian Institute
of Sciences, Jl. Raya JakartaBogor Km. 46, Cibinong, Bogor 16911, Indonesia
*Corresponding author: stsang@amnh.org
Received: 15 May 2019; Accepted: 25 November 2019
ABSTRACT
Flying foxes are important ecological keystone species on many archipelagoes, and Indonesia
is home to over a third of all flying fox species globally. However, the amount of research on this
clade belies their importance to natural systems, particularly as they are increasingly threatened by
anthropogenic development and hunting. Here, we provide a review of the literature since the
publication of the Old World Fruit Bat Action Plan and categorize research priorities as high, medium,
or low based on the number of studies conducted. A majority of the research priorities for Indonesian
endemics are categorized as medium or high priority. Low priority ratings were in multiple categories
for widespread flying fox species found throughout Southeast Asia, though much of the data were
from outside of the Indonesian extent of the species range. These research gaps tend to highlight
broader patterns of research biases towards western Indonesia, whereas significant research effort is
still needed in eastern Indonesia, particularly for vulnerable island taxa.
Keywords: bats, conser vation, Pter opodidae, Pteropus, thr eats
ABSTRAK
Kalong merupakan spesies kunci yang memiliki peran penting bagi ekosistem, dan lebih dari
sepertiga jumlah spesies yang ada di dunia, ditemukan di Indonesia. Namun, jumlah penelitian tentang
spesies kalong tidak mencerminkan akan nilai penting kalong bagi ekosistem dan semakin
meningkatnya ancaman akibat aktivitas manusia dan perburuan. Studi ini menyajikan tinjauan literatur
yang diterbitkan setelah munculnya publikasi Rencana Aksi Pengelolaan Kelelawar Pemakan Buah
(Old World Fruit Bat Action Plan) dan menentukan prioritas penelitian yang meliputi kategori tinggi,
sedang dan rendah berdasarkan jumlah studi yang telah dilakukan. Sebagian besar prioritas penelitian
untuk spesies endemik Indonesia termasuk di dalam kategori sedang atau tinggi. Penelitian yang
dikategorikan sebagai prioritas rendah adalah untuk penelitian spesies kalong yang memiliki daerah
distribusi sangat luas meliputi Kawasan Asia Tenggara, meskipun sebagian besar data yang digunakan
tidak berasal dari daerah distribusi kalong di Indonesia. Kesenjangan penelitian saat ini dikarenakan
adanya kecenderungan untuk melakukan penelitian di kawasan bagian barat Indonesia, padahal upaya
untuk melakukan penelitian di kawasan timur Indonesia masih sangat diperlukan, terutama kelompok
taksa yang rentan terhadap ancaman dan memiliki sebaran terbatas di pulau tertentu.
Kata kunci: kalong, konser vasi, Pteropodidae, Pteropus, ancaman
Indonesia is home to over a third of all flying foxes (sensu stricto genus Pteropus and
Acerodon, Simmons, 2005); however, research on them is limited relative to other vertebrate
taxa, especially mammals, making it difficult to monitor species and create conservation
management plans. Yet, they constitute some of the most ecologically important and
threatened species on the IUCN Red List and have a plethora of potential threats that cannot
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Treubia 46: 103114, December 2019
be dealt with due to lack of information (Mickleburgh et al., 2002; IUCN, 2016). Six flying
fox species have gone extinct in recent history, all of which have been island endemics
(Simmons, 2005; Helgen et al., 2009). This highlights the need to study Indonesian flying
foxes to prevent their extinction, as many of the Indonesian species are also island endemics.
Additionally, they fulfill important ecological roles as seed dispersers and pollinators (Fujita
& Tuttle, 1991; Sheherazade et al., 2019), along with as natural reservoir hosts for zoonotic
pathogens (Wang, et al., 2008), meaning decline of a species could lead to negative impacts in
other parts of the natural ecosystem. However, there is a tendency to focus on the most visible
species, and a guide to what has been completed already would help identify where research
priorities are. Other barriers to research, such as lack of access to literature for scientists in
developing countries, make it difficult to create novel projects that address core issues or data
gaps relevant to conservation priorities (Tsang et al., 2016).
This study aims to review and recommend directions for research on flying foxes in
Indonesia to better guide in-country conservation efforts for aspiring researchers and
practitioners, along with data needed for listing species. This study is also important to the
revision of the Old World Fruit Bat Action Plan, which is currently underway, in reflecting on
what some of the worlds most threatened fruit bats need on a fundamental level in research
before conservation or management action is even possible. We specifically chose to focus on
Indonesian flying fox species only, as their level of diversity (23 species) is significantly
higher than in any other country (e.g. second highest number of flying foxes are found on
Papua New Guinea, which has less than half the Indonesian species total).
For Indonesian flying foxes, we included Pteropus (20 species) and A cerodon (3
species), and also added in two closely related pteropodids in tribe Pteropodini, Neopteryx
frosti and Styloctenium wallacei. Searches were conducted in the following databases:
Scopus, Web of Science, Google Scholar, ResearchGate, and gray literature (such as grant or
NGO reports, or student theses). The reviewed literature prioritized studies with newly
generated data and focus on information that usually goes into an IUCN Red List threat
assessment: taxonomy, population data, habitat preferences/roosting ecology, diet, threats,
and conservation actions, including whether the species is in a protected area. We also
included notes based on our own fieldwork and collections-based research at the Museum
Zoologicum Bogoriense, American Museum of Natural History, National Museum of Natural
History at the Smithsonian Institution, Field Museum of Natural History, and National
Museum of Natural History of the Philippines. Taxonomy and subspecies distributions follow
Simmons (2005), with more recent literature noted in each species account if relevant.
Prioritization. We used the previous Old World Fruit Bat Action Plan (Mickleburgh et al.,
1992) as the baseline for this study, and anything published after 1992 and not cited by the
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Tsang & Wiantoro: Indonesian flying foxes: research and conservation status update
Action Plan are considered new literaturein this study. We omitted: 1) studies related to
pathogen discovery, as these data are not considered when assessing the IUCN Red List
status; 2) studies that use a Pteropus or A cerodon species as a representative of larger clades,
as those studies usually are not attempting to resolve long-standing taxonomic issues for those
specific taxa; and 3) review papers that are citing past papers but do not add further
understanding to the species. Inclusion of these papers would overinflate the amount of prior
research recorded. Whether knowledge gaps were addressed or not was rated based on
whether any literature with new data were generated: high priority (0 studies), medium
priority (1-2 studies), low priority (3+ studies). If there was discussion in the text of species-
specific issues, those papers were included. Review papers were only included if the original
source could not be accessed. For widespread taxa, we include information on the species
from other countries in its range. This is necessary since flying foxes can be transboundary,
though we indicate whether those data are missing from the Indonesian part of its distribution.
In total, we reviewed 86 papers, reports or status assessments. We summarized species
priorities in Table 1, with specific citations in Appendix 1. Almost all of the categories for
Indonesian endemics were of high or medium priority. A majority of the high priority ratings
belonged to species on very remote and isolated islands, or species that do not form large
aggregate colonies at day roosts. These results reflect issues in accessibility to field sites and
difficulties in tracking solitary animals in complex landscapes.
A majority (2 of 17) of the low priorityratings were of widespread species that are
also found in other countries. These studies can be informative for Indonesian species, but
that is highly dependent on the species. For instance, P. vampyrus sumatrensis is well-studied
in peninsular Malaysia, and that particular population crosses into Sumatra often (Epstein et
al., 2009) and is the same subspecies as that of the rest of Sumatra (Tsang et al., 2018),
making the findings relevant to species management planning throughout the island.
However, with P. alecto alecto in Sulawesi compared to P. alecto gouldi in Australia, there are
different human-animal interfaces, different habitats in the landscape, and fewer sympatric
flying fox species, making the contributions from only a single subspecies to the IUCN Red
List assessment inapplicable to the species across its range.
Remarks. Many of the priorities and recommended actions listed in Mickleburgh (1992) have
not been addressed, and those still stand as large knowledge gaps. The relative lack of
Indonesia-specific data does not allow for more localized conservation planning.
Additionally, though some of the taxonomic studies are listed as medium priority, many of
them only found enough evidence to suggest the species needs further review, but has yet to
fully resolve the issue. We also caution the incorrect interpretation of low priorityto mean
that no research is needed in that area. If a species is highly threatened, that may have been
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the original thrust for conducting more research on the species, and each individual species
level of threat must also be taken into account to some degree when selecting priorities.
These difficulties in accessibility and tracking of flying foxes mirror knowledge gaps
of Indonesian biodiversity in general, especially in eastern Indonesia. This is an important
distinction, as there are more flying fox species eastward where there are both more islands
and fewer native terrestrial mammals to fill in ecological roles (Corbet & Hill, 1992).
Published research is heavily biased towards Sundaland, especially Kalimantan (Giam &
Wilcove, 2012), and that needs to change if the goal is to reduce extinction risk to threatened
endemic island taxa.
Not all studies require high-tech tools, but most require that time is spent
understanding a local landscape and then tracking and observing the flying foxes. An example
from another low-resource country would be from recent studies on monitoring and diet of
flying foxes from Myanmar (Win & Mya, 2015; Oo et al., 2017). These studies relied on
observations over an extended period of time, and in some instances were able to reveal
important information about the species natural history and potential threats. A second
example are reproductive ecology studies of bats from Malaysia (Nurul-Ain et al., 2017) and
Vietnam (Furey et al., 2012), which can contribute to the breeding information known about a
species. These above types of data are important to the IUCN and other practitioners, as they
bridge knowledge gaps that hinder the creation of actionable items, such as formation of a
species or habitat management plan.
With the right amount of support and targeted research, Indonesia could make big
gains in all areas of research, including on bats, in the years to come. Given the wide breadth
of types of research needed for flying foxes, students could potentially learn a variety of skills
that are useful for multiple types of careers after they have completed their studies. This
requires that budding scientists are encouraged to pursue natural history and are given the
tools and guidance needed to determine where their efforts could potentially have the most
impact. Flying foxes are especially relevant to discussions related to sustainability, forestry,
agriculture, fisheries and tourism, as these bats affect habitats that are critical to all of these
sectors, and studies aimed at addressing knowledge gaps have the potential for making a
significant impact for both bats and society. Furthermore, a fuller understanding of the natural
history of flying foxes could be strategically utilized in education and outreach campaigns to
target socially relevant pressure points for promoting flying fox conservation. Since many of
the threats that face flying foxes are human-induced (e.g. hunting of Pteropus alecto and
Acerodon celebensis from Sheherazade & Tsang 2015, or habitat conversion for Moluccan
Pteropus from Tsang et al., 2015), engagement with the public is essential to species
persistence, and that cannot be done well unless educational and developmental activities are
couched in good science.
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Table 1. Summar y of resear ch prior ities by species. High pr iority (0 studies) is shad ed in black, medium
priority (1 to 2 studies) is shaded in gray, and low priority is unshaded. An additional asterisk (*) indicates
which category had a majority of studies from other parts of the species distribution outside of Indonesia.
Numbers represent number of studies that contains data on the relevant subject, with fields intentionally left
blank if there were no studies at all. The full list of citations is sorted by species in Appendix 1.
Species Taxonomy Habitat Threats Diet Reproduction Conservation
Pteropus alecto 5* 6* 2 5* 3* 5*
Pteropus aruensis 1
Pteropus caniceps 1 1 1 1 1
Pteropus chrysoproctus 1 1 1 1
Pteropus conspicillatus 7* 3* 1* 1* 2* 2*
Pteropus griseus 3 1 3 1
Pteropus hypomelanus 3* 3* 3* 4* 1* 2
Pteropus keyensis 1
Pteropus lombocensis 4 1 1 1 1
Pteropus macrotis 1 1 1 1
Pteropus melanopogon 1 1 1 1 1
Pteropus melanotus 1* 1* 1* 1* 2*
Pteropus neohibernicus 2* 1* 2 2* 1*
Pteropus ocularis 1 1 1
Pteropus personatus 3 2
Pteropus pohlei 1 1 1 1
Pteropus pumilus 3* 5* 2* 2*
Pteropus speciosus 2
Pteropus temminckii 1 2 1 1
Pteropus vampyrus 4 7* 10* 2* 1* 5*
Acerodon celebensis 3 5 3 1 2
Acerodon humilis 1 2
Acerodon mackloti 1
Neopteryx frosti 1 1
Styloctenium wallacei 1 1
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ACKNOWLEDGMENTS
We thank the Ministry of Research and Technology (RISTEK) and the Ministry of the
Environment and Forestry of the Republic of Indonesia for their support of this project. This
review was part of a larger body of research funded by the Fulbright Indonesia Student
Research Fellowship and the National Geographic Society Young Explorers Grant (9272-13)
awarded to S.M. Tsang and in part by the National Institute of Allergy and Infectious
Diseases under Grant No. 1R21A|105050 to D.J. Lohman and N.B. Simmons.
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Appendices
Appendix 1. All literature cited for each flying fox species used to categorize priorities in Table 1. For P.
griseus, we included Goodwin (1979) as new literature because the Old World Action Plan (Mickleburgh,
1992) did not recount ecological information for this species under the species account.
Species Citations
Genus Pter opus
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., 2015, 2019; Tsang, 2016a)
P. conspicillatus (Webb and Tidemann, 1995; Fox, 2006; Parsons et al., 2006, 2010; Fox et al.,
2008, 2012; Shilton 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.,
2017c, 2017b, 2017a; Oo 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; Kitchener et al., 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 al., 2010; Pangau-Adam et al., 2012;
Almeida et al., 2014; Fatem et al., 2014; Tsang et al. 2019)
P. ocularis (Tsang et al., 2015, 2019; Tsang, 2016c)
P. personatus (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; OMalley
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 (Kunz and Jones, 2000; 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., 2015,
2016; Tanalgo, 2017; Tsang et al., 2018, 2019)
Genus Acerodon
Acerodon celebensis (Almeida et al., 2014; Flannery, 1995; Riley, 2002; Lee et al., 2005; Mickleburgh
et al., 2009; Saroyo, 2011; Sheherazade and 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 (Tsang et al., 2019)
Other Pteropodini
Neopteryx frosti (Almeida et al., 2014; Sheherazade and Tsang, 2015)
Styloctenium wallacei (Esselstyn, 2007; Mickleburgh et al., 2009; Maryanto et al., 2011)
113
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