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A rapid assessment of flying fox (Pteropus spp.) colonies in Cambodia

  • July 2014
Authors:
Sébastien ravon
Sébastien ravon
Sébastien ravon
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Neil Furey at Independent
Neil Furey
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Vibol Hul at Institut Pasteur International Network
Vibol Hul
Julien Cappelle at Cirad - La recherche agronomique pour le développement
Julien Cappelle
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14
© Centre for Biodiversity Conservation, Phnom Penh
S. Ravon et al.
Cambodian Journal of Natural History 2014 (1) 14–18
Short Communication
A rapid assessment of fl ying fox (
Pteropus
spp.) colonies in
Cambodia
Sébastien RAVON1, Neil M. FUREY2,*, HUL Vibol3 and Julien CAPPELLE1,4
1 Institut Pasteur du Cambodge, Epidemiology and Public Health Unit, BP983, Phnom Penh, Cambodia.
2 Fauna & Flora International (Cambodia Programme), PO Box 1380, No. 19, Street 360, Boeng Keng Kong 1, Phnom
Penh, 12000, Cambodia.
3 Institut Pasteur du Cambodge, Virology Unit, BP983, Phnom Penh, Cambodia.
4 Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), UR Animal et
Gestion Intégrée des Risques (AGIRs), F-34398, Montpellier, France.
*Corresponding author. Email neil.furey@fauna-fl ora.org
Paper submitted 11 May 2014, revised manuscript accepted 10 July 2014.
CITATION: Ravon, S., Furey, N.M., Hul V. & Cappelle, J. (2014) A rapid assessment of fl ying fox (Pteropus spp.) colonies in
Cambodia. Cambodian Journal of Natural History, 2014, 14–18.
Flying foxes (Chiroptera: Pteropodidae: Pteropus) are
among the few wide-ranging frugivores still found
in many parts of Southeast Asia and play important
seed-dispersion and pollination roles in their ecosys-
tems (Cox et al., 1991; Fujita & Tu le, 1991; Struebig et
al., 2007). Three fl ying fox species were depicted for
Cambodia in the range maps of Francis (2008): large
fl ying fox Pteropus vampyrus, Lyle’s fl ying fox P. lylei
and island fl ying fox P. hypomelanus. These species are
currently considered to be globally Near-threatened,
Vulnerable and Least Concern by the IUCN (Bates et
al., 2008; Bumrungsri et al., 2008; Francis et al., 2008)
respectively, and as nationally common (P. vampyrus
and P. lylei) or nationally rare (P. hypomelanus) in
Cambodian legislation (MAFF, 2007). All three species
are included in Appendix II of CITES, but almost
nothing is known about their conservation status in
Cambodia. Although likely present, the occurrence
of P. vampyrus remains unconfi rmed, having yet to
be validated by the unequivocal documentation of a
live animal or museum specimen to our knowledge.
As colony surveys are central to determining conser-
vation priorities for fl ying foxes (Mickleburgh et al.,
1992), we provide here the fi ndings of a rapid assess-
ment of pteropodid colonies in Cambodia.
Using an unpublished list of roost sites provided
by the Wildlife Conservation Society, supplemented
by additional sites reported by local fi eld workers,
we conducted fi eld surveys between June 2013 and
February 2014 to assess all of the known or suspected
Pteropus colonies in Cambodia. At every site, the
location and basic se ing of the roost environment
was recorded and standardized estimates of roost
populations made using direct census methods, and,
where possible, nightly dispersal counts (Kunz et al.,
1996). Eff orts were also made to identify the species
present at each site, but because these necessarily
relied upon impressions of relative size (Francis,
2008) using binoculars, species identifi cations were
uncertain and so no a empts were made to estimate
total population sizes for each species. As P. hypome-
lanus primarily occurs in coastal areas and on marine
islands, however (Francis, 2008), we assumed that the
species present at all inland sites surveyed were P.
lylei and/or P. vampyrus (Fig. 1).
Direct censuses were undertaken by visually
counting the bats during the day at each site with the
aid of 8 x 42 binoculars and manual hand-counters,
whereas nightly dispersal counts began at dusk when
the bats emerged to forage until all had left the roost
site (typically from 1830 h to 1910 h). The la er was
15
© Centre for Biodiversity Conservation, Phnom PenhCambodian Journal of Natural History 2014 (1) 14–18
Flying fox colonies
site-based conservationists around the country, it
appears likely these comprise most of the fl ying fox
colonies in Cambodia. (The possibility that other
colonies might be discovered in the future cannot be
excluded, however, particularly in poorly surveyed
coastal regions and areas surrounding the Tonle Sap
Lake). At least one interview was completed at each
site. According to local informants, all of the colonies
assessed were present year-round. Off spring were
largely reported by respondents as appearing in April
each year, and this is supported by monthly observa-
tions at the Wat Pi Chey Sa Kor (Kandal Province) and
Wat Bay Dam Ram (Ba ambang Province) colonies
where mating takes place in November and parturi-
tion primarily occurs in April (Hul, 2013; J. Cappelle,
unpublished data).
Most of the roost sites were situated inside the
grounds or within the vicinity of a religious or govern-
confi rmed by checking roost trees with a spotlight
after the dispersal count at each site. Due to the
density of bats and brevity of the evening dispersal,
in some instances bats were counted in groups of 10
as they dispersed. The higher count from the two
methods was rounded down to the nearest hundred
and accepted as the estimated population size for a
given site. Interviews were also undertaken by the
fi rst author with local authorities and residents at
roost sites to determine: (i) the status of the colony
(permanent or seasonal); (ii) annual breeding periods
(defi ned as birth periods); (iii) whether the colony
receives any protection; (iv) conservation threats at
each site; and (v) local perceptions concerning the
fl ying fox colony.
Over the course of the rapid fi eld survey, 12
roost sites were located and assessed (Table 1, Fig.
2). Based on our experience and discussions with
Fig. 1 Flying foxes on Koh Trong Island on the Mekong River (© Gordon Congdon, left) and Koh Bong Island off the
coast of Cambodia (© Jeremy Holden, right). The species on the left is thought to be P. lylei and the species on the right
P. hypomelanus.
16
© Centre for Biodiversity Conservation, Phnom Penh
S. Ravon et al.
Cambodian Journal of Natural History 2014 (1) 14–18
Fig. 2 Locations and
relative sizes of 12 fl ying
fox colonies in Cambodia.
Table 1 Summary characteristics of 12 fl ying fox colonies in Cambodia. Key: * Site where hunting of bats was reported
or observed; 1 DC = Direct Census, ND = Night Dispersal, n/a = not applicable; 2 Value given is the highest fi gure from
the count methods, rounded down to the nearest hundred.
# Site Name (Province) Latitude,
Longitude Census Date Roost Environment Census
Methods1
Population
Estimate2
1 Ang Trapeang Thmor
(Banteay Meanchey)
13.804 N,
103.261 E.
14 Aug 2013 One roost tree on small
island in reservoir.
DC ≈200
2 Wat Bay Dam Ram
(Ba ambang)
12.993 N,
103.161 E.
23 Jun 2013 Pagoda. Three roost
trees in site vicinity.
DC / ND ≈1,400
3 Royal Gardens *
(Siem Reap)
13.363 N,
103.859 E.
10 Aug 2013 Offi cial site. 14 roost
trees in urban park.
DC / ND ≈5,000
4 Kampong Thom *
(Kampong Thom)
12.714 N,
104.883 E.
8 Aug 2013 Offi cial site. Three roost
trees along roadside.
DC / ND ≈6,000
5 Koh Trong Island
(Kratie)
12.507 N,
105.993 E.
26 Aug 2013 Pagoda. Two roost trees
on site perimeter.
DC ≈200
6 Koh Chreng Island *
(Kratie)
12.361 N,
106.044 E.
27 Aug 2013 Pagoda. 17 roost trees
on site perimeter.
DC ≈900
7 Wat Srey Santaor *
(Kampong Cham)
11.915 N,
105.183 E.
8 Aug 2013 Pagoda. Small forest on
site perimeter.
n/a Extirpated
8 Council for Development
of Cambodia
(Phnom Penh)
11.577 N,
104.924 E.
18 Oct 2013 Offi cial site. One roost
tree on site perimeter.
DC / ND ≈1,800
9 Wat Prek Chey Lech *
(Kandal)
11.465 N,
105.235 E.
1 Aug 2013 Pagoda. Five roost trees
on site perimeter.
DC / ND ≈500
10 Wat Pi Chey Sa Kor *
(Kandal)
11.200 N,
105.058 E.
15 Jan 2014 Pagoda. 21 roost trees
on site perimeter.
DC / ND ≈4,000
11 Wat Veal Lbang
(Prey Veng)
11.173 N,
105.310 E.
17 Jan 2014 Pagoda. 12 roost trees in
site vicinity.
DC ≈700
12 Koh Bong Island
(Sihanoukville)
10.759 N,
103.265 E.
1 Feb 2014 Three roost trees in
forest on small private
island.
DC ≈200
17
© Centre for Biodiversity Conservation, Phnom PenhCambodian Journal of Natural History 2014 (1) 14–18
Flying fox colonies
colony areas to eliminate misconceptions regarding
their medicinal values and to generate local support
for their protection. To this end, a website (www.
facebook.com/CFFCPH) has been developed to
gain public information about fl ying fox colonies
in Cambodia, which we hope will help to stimulate
greater conservation interest in these charismatic and
inherently vulnerable animals.
Acknowledgements
The authors are grateful to Mr Prak Bali for his assis-
tance in fi nding fl ying fox colonies, Benjamin Hayes
for his advice and to the SE Asian Bat Conservation
and Research Unit for their support. We also thank the
two anonymous reviewers who kindly commented on
the text. The study was supported by the SouthEast
Asia Encephalitis project which is funded by Aviesan
Sud and Fondation Total.
References
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ment building, which apparently aff orded them some
protection from hunting (seven roosts were near a
pagoda and three were near a government building).
Only two roosts were protected by a natural barrier:
the very small uninhabited islands of Ang Trapaeng
Thmor and Koh Bong in the country’s Northwest and
Southwest respectively (Table 1, Fig. 2). This situa-
tion is similar to Thailand—another predominantly
Buddhist country—where many fl ying fox colonies
are near pagodas (Wacharapluesadee et al., 2010),
but diff ers from the Philippines—a largely Christian
and Muslim country—where most colonies are in
forest areas (Mildenstein, 2012). Religion may there-
fore play an important role in fl ying fox conservation
in Cambodia, and a be er understanding of local
perceptions of bats could aid the design of more eff ec-
tive conservation initiatives.
Despite the potential infl uence of religious views
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medicinal use was reported at half of the 12 sites in
Table 1. In fact, one colony in Srey Santaor (Kampong
Cham Province) was recently extirpated by large-scale
hunting, despite protests from local monks (Prak Bali,
pers. comm.), and colonies at other sites could well
be declining. Even though most of the remnant fl ying
fox colonies in Cambodia now appear to be confi ned
to sites which aff ord some measure of protection,
the bats are still actively hunted while foraging or
occur in non-protected areas (Timmins, 2008; present
study). Thus, while there is a clear need for further
surveys—preferably entailing synchronized counts
employing standard methods at all known colonies to
establish seasonal variation and population trends—
our data nonetheless suggest that fl ying fox colonies
in mainland Cambodia are heavily threatened and by
no means nationally common.
This poses an obvious concern, not least because
fl ying foxes can cease to be eff ective seed dispersers
long before they become rare (McConkey & Drake,
2006). Besides their ecological services to humans,
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pathogens of public health importance in Cambodia.
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in national fl ying fox populations some years ago
(Reynes et al., 2005), but very li le information is
available on the risk of transmission to domestic
animals and humans in the country. Further research
on the status and ecology of Cambodian Pteropus is
therefore central to overcoming current challenges to
reliable fi eld identifi cation and designing conserva-
tion plans and public health risk mitigation strategies.
Campaigns to raise awareness are also required in
18
© Centre for Biodiversity Conservation, Phnom Penh
S. Ravon et al.
Cambodian Journal of Natural History 2014 (1) 14–18
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Pteropus vampyrus, the largest bat in the world, has a broad geographic range covering much of Southeast Asia. The wide distribution of P. vampyrus and its ability to cross oceanic expanses makes management of this threatened species an international concern. Pteropus vampyrus is an essential seed disperser and pollinator of rain forest trees, many of which are ecologically and economically important. Understanding population dynamics of P. vampyrus is thus critical to addressing conservation issues and global health concerns. We used phylogenetic inference and population genetic indices to infer past gene flow between populations of P. vampyrus throughout most of the species’ range. Population genetic parameters indicate low levels of nucleotide variability with high haplotype diversity across its range, implying a demographic scenario of recent population expansion after a bottleneck. Subspecies were not found to be monophyletic from the genetic data, which may reflect some level of genetic variation on even shallower time scales. The low level of population genetic structure throughout the species range is not necessarily surprising given its high vagility and seasonal migratory behavior. However, it cannot be entirely excluded that these results may reflect historical connectivity or lineage sorting issues rather than more recent persistent gene flow. These findings highlight the need for international cooperation and monitoring to ensure persistence of populations and to create a species management plan that can protect the species throughout its range. Increased genetic sampling is needed to ascertain P. vampyrus’ commonly used dispersal routes and to assess the possibility of asymmetric gene flow among populations.
... In Buddhist countries (Cambodia, Myanmar, Thailand and Vietnam), most roost sites of large fruit bats are found in the gardens around temples and monasteries because of the protection the monks provide (e.g. Ravon et al. 2014;T. Mildenstein unpublished data). ...
Exploitation of Bats for Bushmeat and Medicine
Chapter
Full-text available
  • Jan 2016
Bat hunting for consumption as bushmeat and medicine is widespread and affects at least 167 species of bats (or c. 13 % of the world’s bat species), in Africa, Asia, across the islands of Oceania, and to a lesser extent in Central and South America. Hunting is particularly prevalent among the large-bodied fruit bats of the Old World tropics, where half (50 %, 92/183) the extant species in the family Pteropodidae are hunted. Pteropodids that are hunted are six times more likely to be Red Listed as threatened: 66 % of species in IUCN threatened categories (CR, EN, VU, NT), compared to 11 % of species in the ‘Least Concern’ (LC) category. However, there still appears to be an information gap at the international level. One third of the hunted species on the Red List are not considered threatened by that hunting, and nearly a quarter of the bat species included in this review are not listed as hunted in IUCN Red List species accounts. This review has resulted in a comprehensive list of hunted bats that doubles the number of species known from either the IUCN Red List species accounts or a questionnaire circulated in 2004. More research is needed on the impacts of unregulated hunting, as well as on the sustainability of regulated hunting programs. In the absence of population size and growth data, legislators and managers should be precautionary in their attitude towards hunting. Roost site protection should be a priority as it is both logistically simpler than patrolling bat foraging grounds and reduces the comparatively larger scale mortality and stress that hunting at the roost can cause. Education and awareness campaigns within local communities should demonstrate how bats are a limited resource and emphasize characteristics (nocturnal, slow reproducing and colonial) that make them particularly vulnerable to hunting pressure .
... © Centre for Biodiversity Conservation, Phnom Penh Cambodian Journal of Natural History 2014 (1)[14][15][16][17][18] ...
Cambodian Journal of Natural History Volume 2014 Issue 1
Book
Full-text available
  • Aug 2014
Mapping Risk of Nipah Virus Transmission from Bats to Humans in Thailand
Article
Full-text available
Nipah virus (NiV) is a zoonotic virus that can pose a serious threat to human and livestock health. Old-world fruit bats (Pteropus spp.) are the natural reservoir hosts for NiV, and Pteropus lylei, Lyle's flying fox, is an important host of NiV in mainland Southeast Asia. NiV can be transmitted from bats to humans directly via bat-contaminated foods (i.e., date palm sap or fruit) or indirectly via livestock or other intermediate animal hosts. Here we construct risk maps for NiV spillover and transmission by combining ecological niche models for the P. lylei bat reservoir with other spatial data related to direct or indirect NiV transmission (livestock density, foodborne sources including fruit production, and human population). We predict the current and future (2050 and 2070) distribution of P. lylei across Thailand, Cambodia, and Vietnam. Our best-fit model predicted that central and western regions of Thailand and small areas in Cambodia are currently the most suitable habitats for P. lylei. However, due to climate change, the species range is predicted to expand to include lower northern, northeastern, eastern, and upper southern Thailand and almost all of Cambodia and lower southern Vietnam. This expansion will create additional risk areas for human infection from P. lylei in Thailand. Our combined predictive risk maps showed that central Thailand, inhabited by 2.3 million people, is considered highly suitable for the zoonotic transmission of NiV from P. lylei. These current and future NiV transmission risk maps can be used to prioritize sites for active virus surveillance and developing awareness and prevention programs to reduce the risk of NiV spillover and spread in Thailand.
From greener times: a new species of Thick-thumbed Myotis from Phnom Penh, Cambodia
Article
Full-text available
A new species of Myotis is described from Cambodia. The species is characterized by its fleshy, bicoloured thumb, large foot sole, full dentition, relatively short rostrum, and high frontal part of the skull. The species is currently only known from the city of Phnom Penh.
Pteropus vampyrus
Article
Full-text available
  • Jan 2008
Intensive hunting of large flying foxes Pteropus vampyrus natunae in Central Kalimantan, Indonesian Borneo
Article
Full-text available
Pteropus vampyrus natunae, the Bornean subspecies of the large flying fox, has important roles in pollination but unsustainable hunting has been reported in Malaysian states. We provide the first description of hunting techniques and intensity in Indonesian Borneo. In forests around Palangka Raya this species is captured in canopy-level nets to support trade in the provincial capital. We estimate that in 2003 4,500 individuals were extracted from a single location in 30 days, which, together with trends reported in interviews with hunters and traders, suggests that hunting in this region is intensive and probably causing severe population declines. Further surveys are needed throughout Kalimantan to determine if this trend is occurring around other cities and whether intervention is needed to safeguard viable populations.
A Longitudinal Study of the Prevalence of Nipah Virus in Pteropus lylei Bats in Thailand: Evidence for Seasonal Preference in Disease Transmission
Article
Full-text available
After 12 serial Nipah virus outbreaks in humans since 1998, it has been noted that all except the initial event in Malaysia occurred during the first 5 months of the year. Increasingly higher morbidity and mortality have been observed in subsequent outbreaks in India and Bangladesh. This may have been related to different virus strains and transmission capability from bat to human without the need for an amplifying host and direct human-to-human transmission. A survey of virus strains in Pteropus lylei and seasonal preference for spillover of these viruses was completed in seven provinces of Central Thailand between May 2005 and June 2007. Nipah virus RNA sequences, which belonged to those of the Malaysian and Bangladesh strains, were detected in the urine of these bats, with the Bangladesh strain being dominant. Highest recovery of Nipah virus RNA was observed in May. Of two provincial sites where monthly surveys were done, the Bangladesh strain was almost exclusively detected during April to June. The Malaysian strain was found dispersed during December to June. Although direct contact during breeding (in December to April) was believed to be an important transmission factor, our results may not entirely support the role of breeding activities in spillage of virus. Greater virus shedding over extended periods in the case of the Malaysian strain and the highest peak of virus detection in May in the case of the Bangladesh strain when offspring started to separate may suggest that there may be responsible mechanisms other than direct contact during breeding in the same roost. Knowledge of seasonal preferences of Nipah virus shedding in P. lylei will help us to better understand the dynamics of Nipah virus transmission and have implications for disease management.
Nipah Virus in Lyle's Flying Foxes, Cambodia
Article
Full-text available
We conducted a survey in Cambodia in 2000 on henipavirus infection among several bat species, including flying foxes, and persons exposed to these animals. Among 1,072 bat serum samples tested by enzyme-linked immunosorbent assay, antibodies reactive to Nipah virus (NiV) antigen were detected only in Pteropus lylei species; Cynopterus sphinx, Hipposideros larvatus, Scotophilus kuhlii, Chaerephon plicata, Taphozous melanopogon, and T. theobaldi species were negative. Seroneutralization applied on a subset of 156 serum samples confirmed these results. None of the 8 human serum samples was NiV seropositive with the seroneutralization test. One virus isolate exhibiting cytopathic effect with syncytia was obtained from 769 urine samples collected at roosts of P. lylei specimens. Partial molecular characterization of this isolate demonstrated that it was closely related to NiV. These results strengthen the hypothesis that flying foxes could be the natural host of NiV. Surveillance of human cases should be implemented.
Old World Fruit Bats An Action Plan for their Conservation
Book
  • Jan 1992
Nipah virus in Lyle's flying foxes, Cambodia
Article
Flying Foxes (Chiroptera: Pteropodidae): Threatened Animals of Key Ecological and Economic Importance
Article
Flying foxes are animals of extraordinary ecological and economic importance throughout forests of the Old World tropics Nearly 200 species play an essential role as forest pollinators and seed dispersers, yet they are frequently misunderstood intensely persecuted and exceptionally vulnerable to extinction Their role in the propagation of numerous important plants remains virtually uninvestigated. However, our review of already available literature demonstrates that at least 289 plant species rely to vatying degrees on large populations of flying foxes for propagation. These plants, in addition to their many ecological contributing produce some 448 economically valuable products. The fact that flying foxes are increasingly threaten and that few baseline data exist on population trends is cause for concern Many appear to be in severe decline, and several species are already extinct. We present initial observations on flying fox importance and survival threats in hopes of highlighting research and conservation needs.
Flying Foxes as Strong Interactors in South Pacific Island Ecosystems: A Conservation Hypothesis
Article
The dependency of highly endemic island floras on few potential pollinators in depauperate island faunas suggests that pollinators and seed dispersers may be crucial in the preservation of biodiversity in isolated oceanic islands. We discuss the hypothesis that flying foxes are “strong interactors” in South Pacific islands where they serve as the principal pollinators and seed dispersers, This suggests that the ongoing decline and ultimate extinction of flying fox species on Pacific islands may lead to a cascade of linked plant extinctions. We propose an empirical test of this hypothesis: comparisons of plant reproductive success in Guam, which has virtually lost its flying fox populations, and Samoa, where significant populations remain. Resumen: La dependencia de floras isleñas altamente endemicas en algunos polinizadores potenciales en faunas islenas depauperizadas sugiere que los polinizadores y los dispersadores de semillas pueden ser cruciales en la conservacion de la diversidad biologica en islas oceanicas aisladas. Discutimos la hipotesis de que los murcielagos fnugiwros (Pteropus sp.) son fuertes interactores en las islas del Pacifico sur, en donde funcionan como los principales agentes de polinizacion y de disperseón de semillas Esto sugiere que la continua disminucion y futura extinción de las especies de murciélagos frugivoros podrian llevara una extinción de plantas en cadena. Hemos propuesto una prueba empirica de esta hipótesis, mediante la comparación del éxito reproductivo de lasplantas en Guam, que prácticamente ha perdido sus poblaciones de murciélagos frugiwros, con el de Samoa, donde persisten poblaciones impmtantes.
Flying foxes cease to function as seed dispersers long before they become rare
Article
Rare species play limited ecological roles, but particular behavioral traits may predispose species to become functionally extinct before becoming rare. Flying foxes (Pteropodid fruit bats) are important dispersers of large seeds, but their effectiveness is hypothesized to depend on high population density that induces aggressive interactions. In a Pacific archipelago, we quantified the proportion of seeds that flying foxes dispersed beyond the fruiting canopy, across a range of sites that differed in flying fox abundance. We found the relationship between ecological function (seed dispersal) and flying fox abundance was nonlinear and consistent with the hypothesis. For most trees in sites below a threshold abundance of flying foxes, flying foxes dispersed < 1% of the seeds they handled. Above the threshold, dispersal away from trees increased to 58% as animal abundance approximately doubled. Hence, flying foxes may cease to be effective seed dispersers long before becoming rare. As many species' populations decline worldwide, identifying those with threshold relationships is an important precursor to preservation of ecologically effective densities.
Conservation of endangered fl ying foxes in the Philippines: eff ects of anthropogenic disturbance and methods for monitoring
  • Jan 2012
  • T L Mildenstein
Mildenstein, T.L. (2012) Conservation of endangered fl ying foxes in the Philippines: eff ects of anthropogenic disturbance and methods for monitoring. PhD thesis, University of Montana, USA.