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Bird Conservation International, page 1of 18. © BirdLife International, 2012
doi:10.1017/S0959270912000093
Vultures in Cambodia: population, threats
and conservation
TOM CLEMENTS, MARTIN GILBERT, HUGO J. RAINEY,
RICHARD CUTHBERT, JONATHAN C. EAMES, PECH BUNNAT,
SENG TEAK, SONG CHANSOCHEAT and TAN SETHA
Summary
Asian vultures have undergone dramatic declines of 90–99% in the Indian Subcontinent, as
a consequence of poisoning by veterinary use of the drug diclofenac, and are at a high risk of
extinction. Cambodia supports one of the only populations of three species (White-rumped
Vulture Gyps bengalensis, Slender-billed Vulture G. tenuirostris and Red-headed Vulture
Sarcogyps calvus) outside of South Asia where diclofenac use is not widespread. Conservation of
the Cambodian sub-populations is therefore a global priority. This study analyses the results of
a long-term research programme into Cambodian vultures that was initiated in 2004. Population
sizes of each species are estimated at 50–200+ individuals, ranging across an area of approximately
300 km by 250 km, including adjacent areas in Laos and Vietnam. The principal causes of vulture
mortality were poisoning (73%), probably as an accidental consequence of local hunting and fishing
practices, and hunting or capture for traditional medicine (15%). This represents a significant loss
from such a small population of long-lived, slow breeding, species such as vultures. Cambodian
vultures are severely food limited and are primarily dependent on domestic ungulate carcasses, as
wild ungulate populations have been severely depleted over the past 20 years. Local people across
the vulture range still follow traditional animal husbandry practices, including releasing livestock
into the open deciduous dipterocarp forest areas when they are not needed for work, providing the
food source. Reducing threats through limiting the use of poisons (which are also harmful for
human health) and supplementary food provisioning in the short to medium-term through ‘vulture
restaurants’is critical if Cambodian vultures are to be conserved.
Introduction
The South Asian vulture crisis has been well documented since the first dramatic declines were
detected in India (Prakash 1999). Seven species of vultures are resident in South Asia, and three of
these, White-rumped Vulture Gyps bengalensis (hereafter WRV) and Slender-billed Vulture Gyps
tenuirostris (SBV) and Red-headed Vulture Sarcogyps calvus (RHV), are also resident in South-
East Asia. These species were historically highly abundant in South Asia, as religious and cultural
practices ensured a plentiful food supply of livestock carcasses (Houston 1985). Populations of
resident vultures in South Asia declined rapidly during the 1990s and 2000s (Prakash 1999, Prakash
et al. 2003,2007, Gilbert et al. 2006, Pain et al. 2008, Das et al. 2011), as a consequence of
veterinary use of diclofenac, a non-steroidal anti-inflammatory drug (Oaks et al. 2004). The drug
is so toxic to vultures that the observed population declines could have been caused by the
contamination of a very small proportion (between 1:130 and 1:760) of livestock carcasses (Green
et al. 2004). By 2007, the population of WRV in India was reduced to one thousandth of 1992
levels, while SBV is thought to number only 1,000 individuals (Prakash et al. 2007), and RHV has
been reduced to only 9% of the population that occurred in the early 1990s (Cuthbert et al. 2006).
All of these species are now listed as “Critically Endangered”on the IUCN Red List (BirdLife
International 2008)andathighriskofextinction.TheGovernmentsofIndia,NepalandPakistan
have banned manufacturing and veterinary use ofdiclofenac.However,itisstillcurrentlyused
illegally for veterinary purposes and it is not knownhowlongitwilltakeforallusetocease.Inthe
interim, conservation groups in South Asia have established captive breeding centres to ensure that
some birds survive (Pain et al. 2008).
By contrast to South Asia, the vulture populations in South-East Asia declined much earlier.
Three species, WRV, SBV and RHV, bred commonly in the first half of the 20
th
century, ranging
from Myanmar across Thailand and Indochina reaching Yunnan province in China and extending
south to Peninsular Malaysia (Pain et al. 2003). By the 1980s, however, Thai populations of all
three species had plummeted (Round and Chantrasmi 1985, Round 1988), and they had
disappeared from Malaysia (Wells 1999) and Yunnan (Zheng Guangmei and Wang Qishan
1998). Widespread conflict meant that little was known from Indochina (Cambodia, Lao People’s
Democratic Republic (PDR) and Vietnam) until surveys in the late 1980s and 1990s. These
surveys found that vultures were confined to areas bordering Cambodia in Lao PDR (Thewlis
et al. 1998) and Vietnam (Le Xuan Canh et al. 1997, Brickle et al. 1998, Eames et al. 2004), and
that all three species were widespread but nowhere abundant in the north and north-east in
deciduous dipterocarp woodland of Cambodia (Barzen 1995, Desai and Lic Vuthy 1996, Timmins
and Men 1998, Goes 1999, Long et al. 2000, Timmins and Ou 2001). Data are too sparse to
determine the causes of this reduction in vulture range and abundance, but likely explanations
include widespread collapses in populations of wild ungulates and changes in husbandry of
domestic stock, as well as potentially direct persecution. By the 2000s, therefore, South-East
Asian populations of WRV, SBV and RHV were restricted to Myanmar (Hla et al. 2011) and
Indochina, focused on an area of northern and eastern Cambodia measuring approximately 300
km east-west and 250 km north-south and including border areas in Lao PDR and Vietnam
(Figure 1). These populations are not thought to have significant exposure to diclofenac and
therefore represent the best long-term chance for in situ conservation.
This paper analyses the results of a long-term research programme on Cambodian vultures that
was initiated by a consortium of Government agencies and non-governmental organisations
(NGOs) in 2004 in response to the observed declines in South Asia (WCS et al. 2004). The
principal research objectives were to analyse the threats to vulture species, understand ranging
behaviour, monitor nesting sites, determine population sizes, and monitor trends at supplemental
feeding sites to establish future management and conservation measures.
Methods
Research was undertaken at seven long-term research sites across the observed vulture range,
chosen because vultures were known to be present or breeding (Figure 1): Preah Vihear Protected
Forest (PVPF, since January 2003), Western Siempang (since December 2004), Phnom Prich
Wildlife Sanctuary (PPWS, since July 2005), Lomphat Wildlife Sanctuary (LWS, since October
2005), Mondulkiri Protected Forest (MPF, since October 2005), Kulen Promtep Wildlife Sanctuary
(KPWS, since April 2007) and the Seasan River (since June 2007). At each site a supplemental
feeding station was established to monitor population trends and the surrounding area was
surveyed for threats, nesting sites, and vultures every 1–2months by teams of local village
rangers, for 10–20 days each month. Details of survey methodologies are given below. Research
officers visited the sites for verification purposes and conducted additional surveys at other sites
where vultures were recorded. Data are presented here until the end of June 2011.
Threat assessments
At each site, local village rangers recorded threats to vultures where they were encountered. All
cases were investigated through interviews with local people to determine the details. In addition,
T. Clements et al. 2
Figure 1. Distribution of Vultures in Indochina, showing long-term study sites, nesting colonies
and data from satellite tagged birds. Data are based on the field surveys and records from the late
1990s onwards (see main text for references).
Critically Endangered Vultures in Cambodia 3
research officers undertook comprehensive threat assessments through semi-structured inter-
views with key informants: local wildlife traders, hunters, government officials and veterinary
establishments. Diclofenac availability was assessed through market surveys and interviews with
pharmacies carried out by research officers, focusing on veterinary preparations and health
products for livestock treatment. Data on human diclofenac preparations were also collected, since
these can also be given to cattle. Diclofenac surveys were completed in all range provinces and in
most district towns, and repeated at yearly intervals. The health status of vultures was assessed
through examination of all birds that were trapped during the course of the project (see below) or
were brought into care temporarily as a result of injury. Blood samples were taken for serology
profiling, haemoparasitology, and phylogenetic studies.
Vulture food availability was assessed using two methods: field surveys for all types of carcass
(wild and domestic animals) and household interviews regarding mortality of domestic livestock
only. Field surveys for carcasses were undertaken at monthly intervals between 2005 and 2008 by
local rangers at three sites (LWS, PVPF and Siempang). Suitable carcasses included domestic
livestock (buffalo, cows, pigs and dogs) and wild ungulates such as gaur Bos gaurus, banteng
B. javanicus, sambar Rusa unicolor, Eld’s deer Rucervus eldii and wild pigs Sus scrofa. For each
carcass found, the species, size, details of origin and the vultures present were recorded. Household
interviews were conducted in 2004 by research officers in villages surrounding one site (PVPF), to
determine the number of domestic livestock that were lost or died in the forest each year.
Vulture ranging behaviour
Satellite telemetry was used to determine vulture ranging behaviour. Vultures were caught at
artificially baited feeding sites using a remotely operated Q-net (which uses high tension elastic to
propel a 20 x16 ft net), monofilament nooses and padded leg-hold traps. Capture rate was low as
vultures were quickly sensitised to the techniques employed and became increasingly wary.
Satellite transmitters (80 g Argos bird-borne transmitter, North Star Science and Technology
LLC.) were fitted to two adult SBVs (SBV3and SBV4) and a WRV (WRV6) caught in May 2005 in
PVPF, and an adult WRV (WRV8) captured in April 2006 in MPF. Home-range area was
estimated using 100% minimum convex polygons generated using filtered fixes for each vulture
using the software “Ranges7”(Kenward 2001; Kenward et al. 2003). Tracking resolution was set
at 1,000 m to take account of the estimated accuracy of location classes.
Monitoring nesting sites
Vulture nesting sites were identified by local rangers, with specific targeted surveys during October–
December (late wet season) when breeding commences. Nest surveys concentrated on known
breeding locations, areas visited by satellite-tagged birds, and areas with emergent trees along
watercourses and small hills, which are used by vultures in South Asia (Gilbert et al. 2006). Where
nests were located, local people were employed as protectors, receiving a payment contingent on
ensuring nests were not collected or disturbed by people. Data were recorded on vulture species,
location and the characteristics of nesting sites and verified by research officers. Repeat visits by
research officers were undertaken towards the end of the breeding season, in March and April (late
dry season), in order to determine the number of chicks that successfully fledged.
Monitoring vulture population size and trends
Species populations were monitored at supplemental feeding stations (‘vulture restaurants’)
established at each research site. Supplemental feeding was initiated because the threat assess-
ments identified lack of food as one of the factors limiting vulture populations. Restaurants were
conducted monthly by slaughtering one 150–250 kg cow or buffalo purchased from local villagers
T. Clements et al. 4
at each of the research sites, with the exception of MPF and PPWS where the restaurant was
alternated on a bimonthly basis. Restaurant dates were staggered to maximise the food provisioning
effect, allowing vultures to potentially move between restaurants across the range. Each restaurant
was monitored until the carcass had been completely removed (usually 2–5days). Data were
collected on the vulture species present and age composition, with age classes recorded as adult,
subadult (birds yet to attain adult plumage) and juvenile for WRV and SBV, and adult male, adult
female and juvenile for RHV. Data were analysed using generalised linear models with quasi-
Poisson errors and a log-link function in R 2.12.2(R Core Development Team 2011) to investigate
differences between research sites and trends over time for each species. The selected models had
the lowest quasi-AICc score and weights of at least 0.5(Burnham et al. 2011).
The minimum number alive method (Krebs 1966) was used to estimate the minimum population
of each species of vulture through an annual vulture census. The census was first conducted in July
2004, and repeated in May 2006 and annually thereafter. During the census, counts were undertaken
simultaneously at multiple restaurants, both at research sites and other locations, throughout the
vulture range. Since counts were simultaneous it was not possible for birds to travel between sites,
preventing double counting. Two counts were conducted each year, separated by 10–14 days, during
May–July, just after the breeding season. The maximum total number of each species recorded
across all the census sites was used as the estimate of the minimum number alive.
Results
Threat assessments
Diclofenac availability: Veterinary use of diclofenac was not recorded from the range provinces,
and formulations of the drug for veterinary use were only encountered once over the six years.
Poisoning and direct persecution: Poisoning was responsible for 60% of the 25 incidents of
vulture deaths, leading to 74% of the 42 recorded mortalities (Table 1). Some poisoned birds were
rescued and survived following veterinary care. Direct persecution (such as shooting of vultures
with guns or slingshots) was the next most significant cause of vulture deaths, accounting for 10%
of mortalities. One WRV from Phnom Tamao Wildlife Rescue Center and one RHV in Siem Reap
province were killed for perceived value in Khmer medicine.
Food Limitation: Comprehensive field surveys at three sites over areas of approximately
500 km
2
indicated that one carcass is available every 22–36 days (Table 2a). All carcasses
encountered during surveys were domestic buffaloes, cows, or domestic dogs. A small number of
wild ungulate and pig carcasses were recorded from research sites outside of the survey period.
Household interviews in the villages using a 250 km
2
area of PVPF, indicated that livestock
densities are seven animals km
-2
. Every year around 18–32 animals died or were lost in the forest
(Table 2b), an average of one domestic carcass every 11–21 days. By contrast, densities of large
wild ungulates in the study areas are approximately 1–3animals km
-2
(Table 2c). At least two
birds, a RHV and a tagged WRV (WRV8) recovered in Quang Nam province in Vietnam, are
thought to have died due to starvation. The poor body condition of both birds and location far
outside the normal range is perhaps indicative of the difficulty vultures face in finding food.
Vulture health: Eleven of the 12 serum samples taken from captured vultures contained
antibodies to avian encephalomyelitis virus, and one (RHV) had antibodies to avian paramyxovirus
type 1(Newcastle disease virus). However, only one mortality case from disease was recorded,
a WRV at Phnom Tamao Wildlife Rescue Center that died during an outbreak of highly pathogenic
avian influenza virus subtype H5N1(HPAI H5N1) (Table 1).
Ranging behaviour
Minimum convex polygon (MCP) estimates of 2,315 km
2
,5,704 km
2
and 12,155 km
2
were
obtained for three birds, WRV6, WRV8and SBV4, which were tracked for 119,81 and 81 days
Critically Endangered Vultures in Cambodia 5
respectively. Due to the low number of independent points obtained for each bird, kernel
contours could not be reliably calculated. Mortality of two vultures (WRV6and SBV4) was
confirmed 119 and 81 days after application of the transmitters while the units were still
functional, and the death of WRV8was confirmed 472 days after application, 13 months after the
transmitter ceased functioning. Data are not given from one further bird, SBV3, whose satellite
transmitter ceased functioning after only 12 days due to hardware failure.
Nesting sites
Nests of all three species were located, primarily at the LWS, PVPF, Seasan, Siempang, and MPF
sites (Table 3). Causes of nesting failure included raiding by macaques Macaca fascicularis
(10 WRV nests destroyed in the 2007–2008 season) or disturbances such as fire. SBV and WRV
nested in separate colonies, WRV often beside rivers or on small hills, whereas RHV nested
singly, although sometimes associated with colonies of both SBV and WRV. Nesting trees were
large and tall, often of the Dipterocarpaceae family. In all cases only one chick per nest was
observed.
Vulture population size and trends
Numbers of all three species of vulture have fluctuated significantly over time and between sites
(Table 4). Greater numbers of RHV were also recorded in the wet season (P,0.01, Table 4); the
effect of season was not significant for the other species. There was a significantly positive
relationship between the numbers of each species present. The total numbers of WRV and SBV at
the restaurant sites increased strongly in the early years of the monitoring programme and have
remained stable since 2008 (Figure 2), whereas numbers of RHV recorded are constant or
declining slightly (Figure 2). Similar patterns are seen with the census data, with WRV increasing
by 100% and SBV by 50% between 2004 and 2008 (Table 5). WRV numbers were greatest at the
two northerly sites (PVPF and Siempang) that also recorded the largest increases, are stable at the
two central sites (Seasan and LWS), and are declining at the two southerly and easterly sites
Table 1. Recorded incidences of vulture deaths or poisonings and the number of mortalities between
November 2003 and the end of June 2011. Survey coverage was not equal in all years. RHV 5Red-headed
Vulture, SBV 5Slender-billed Vulture and WRV 5White-rumped Vulture.
Cause of death Numbers of Incidences Number of Mortalities Notes
RHV SBV WRV Total (%) RHV SBV WRV Total (%)
Human Origins
- Use in human
medicine
112(8%) 112(5%) WRV was stolen
from a Zoo
- Poisoned 8 1 6 15 (60%) 7 1 23 31 (74%) An additional 6birds
survived
- Killed 134(16%) 134(10%) Includes WRV6
(shot in Laos)
and SBV4
Disease
- Avian Influenza 11(4%) 11(2%) WRV at the Zoo
Other
- Starving/Poor
condition
22(8%) 22(5%) Includes WRV8
(found in Vietnam)
- Unknown 11(4%) 22(5%)
Totals 9 2 14 25 8 2 32 42
T. Clements et al. 6
Table 2. Availability of food for vultures from field surveys for wild and domestic animal carcasses and household interviews of mortalities of domestic livestock.
(a) Field Surveys for wild and domestic animal carcasses across 500 km
2
at three study sites
Site Year Survey
Period
Wild Animal
Carcasses
Domestic Animal Carcasses Survey
Effort/Carcass
Carcass
density
Buffalo Cow Dog Total
PVPF 2005-6 12 months 0 3 6 1 10 36 days 0.02/km
2
Siempang 2005-6 12 months 0 8 3 5 16 22 days 0.03/km
2
LWS 2006-8 24 months 0 5 19 2 26 28 days 0.05/km
2
(b) Number of domestic livestock (cows and buffaloes) reported to have died or been lost in the forest in a 250km
2
area of PVPF, based on household interviews in 2002 and
2003. The projected total number lost or died in the forest is also given, based on applying the same mortality rates to all domestic livestock in the villages.
Site Year Number of domestic cows/buffaloes Domestic Livestock died or lost in forest Carcass Density
PVPF 2002 1752 (density 57/km
2
)17 0.07/km
2
2003 32 0.13/km
2
(c) Estimates of wild large ungulate populations and densities from field surveys
Site Year Density (animals/km
2
) Reference
PVPF 2010 1.2WCS, unpublished data
PPWS 2010 1.7Gray et al. 2011
MPF 2010 3.8Gray et al. 2011
Seima 2008 2.7O’Kelly et al. 2011
Critically Endangered Vultures in Cambodia 7
(MPF and PPWS). Counts of SBV increased strongly at Siempang, which recorded the largest
numbers, are relatively stable at PVPF, Seasan and LWS, and are also declining at MPF and
PPWS. Vulture numbers were low in KPWS, to the far north-west of the other sites (data not
shown). RHV numbers are low and stable at all sites, with the exception of MPF and PPWS where
numbers are again declining. The percentage of juvenile and sub-adult birds was approximately
30% for each species (RHV 32%, WRV 31%, SBV 27%) between January and March 2009,
when reliable data are available. The minimum population size was 201 WRV, 46 SBV and 45
RHV in 2010; numbers counted were slightly lower in 2011 (Table 5).
Table 3. Vulture nests recorded during 2004–2011 across all sites, and the number of birds known to have
fledged.
Year Red-headed Vulture White-rumped Vulture Slender-billed Vulture
Nests Fledged Nests Fledged Nests Fledged
2004-55 no data 32 no data
2005-6 28 5
2006-7 2 1 15 4 7 7
2007-8 2 1 19 5 6 4
2008-9 3 3 11 10 7 7
2009-10 3 3 25 25 8 8
2010-11 6 1 11 6 3 1
Table 4. Generalised linear models for trends in the number of vultures recorded at the research sites, using
quasi-poisson errors and a log link function. The selected models had the lowest quasi-AICc score and weights
of at least 0.5(Burnham et al. 2011). Significance values for the null hypothesis of zero effect: ns 5not-
significant, * 5P,0.05, ** 5P,0.01, *** 5P,0.001).
Variable Degrees of
Freedom
F-value
(significance)
Coefficient
(significance)
White-rumped Vulture
Date (polynomial function) 28.80***
Site 5 120.31***
Site * Date (polynomial function) 10 6.80***
Number of Red-headed Vultures 1 21.00*** 0.013*
Number of Slender-billed Vultures 1 75.19*** 0.037***
Residual deviance 51850.6on 406 degrees of freedom
Slender-billed Vulture
Date (polynomial function) 23.87*
Site 5 133.57***
Site * Date (polynomial function) 10 3.14***
Season 12.41 n.s. - 0.160**
Number of Red-headed Vulture 1 34.25*** 0.041***
Number of White-rumped Vulture 1 118.58*** 0.023***
Residual deviance 5859.6on 405 degrees of freedom
Red-headed Vulture
Date (polynomial function) 2 12.97***
Site 5 43.87***
Site * Date (polynomial function) 10 7.89***
Season 18.74** 0.166***
Number of Slender-billed Vultures 1 20.61*** 0.024***
Residual deviance 5687.9on 406 degrees of freedom
T. Clements et al. 8
Discussion
Threats to Cambodian vultures
Carnivorous and scavenging species are strongly limited by food availability (Krebs 2009). The
three vulture species are obligate carrion feeders, feeding on carcasses of a range of species,
including ungulates. Pain et al. (2003) suggest that food shortage in the latter part of the 20th
century may have played a major part in vulture declines in South-East Asia. Wild ungulate
populations crashed in the region from uncontrolled hunting (Srikosamatara and Suteethorn
1995, Duckworth and Hedges 1998, Duckworth et al. 1999, Baillie et al. 2004), particularly in the
open habitats where hunting is easier. Population estimates of large wild ungulates (gaur,
banteng, Eld’s deer, sambar and wild pigs) at the study sites and surrounding areas are less than
four animals km
-2
(Gray et al. 2011,O’Kelly et al. 2011, WCS unpubl. data). By contrast,
densities of gaur and sambar alone at some national parks in India are approximately 16 animals
km
-2
(Jathanna et al. 2003), indicating that Cambodian densities are extremely low. Vultures are
therefore likely to be highly dependent on domestic ungulates, which commonly exist at higher
densities than wild ungulates (seven animals or more km
-2
). It should be noted that in parts of
India, Pakistan and Nepal where WRV still occur, or occurred until recently, densities of
domesticated bovines are typically 20–80 animals km
-2
(NDDB 2006, Wint and Robinson 2006).
In Cambodia, traditional livestock husbandry practices allow animals to range freely across the
deciduous forest for much of the year (particularly in the dry season), often unattended, where
they may die or become lost, sometimes not returning for several years. Carcasses of animals that
die in the forest may provide a significant supply of carrion for vultures if mortalities go
undetected (otherwise meat is taken by local people). Insecurity and intensification of agriculture
have led to a reduction in this practice in many Cambodian provinces (for example around Tonle
Sap and the Mekong floodplain). The remaining vulture range corresponds exactly to those
Cambodian provinces where livestock are still allowed to range freely.
Calculations based on the energetic requirements of vultures suggest that carcasses of domestic
ungulates in Cambodia should be more than capable of supporting the population. Assuming
a daily feeding requirement for a vulture is 0.341 kg/ungulate tissue per day (Swan et al. 2006
Protocol S1), a population of 300 birds requires an annual food availability of around 39,540 kg
per year. This could be provided by around 100 bovine carcasses per year, assuming an average
carcass mass of 503 kg (for Bos taurus, B. indicus and Bubalus bubalis in South Asia;
R. J. Cuthbert unpublished data) and that edible tissues comprise around 77% of a bovine live
carcass weight (Green et al. 2006). Available data on the densities of domestic ungulate carcasses
(Table 2), suggest that these food requirements could be met by livestock mortalities. However,
what these calculations fail to estimate is the proportion of carcasses found by vultures and the
proportion consumed by other scavengers, which is likely to be significant given the dense forests
found across much of the vulture range in Cambodia. Moreover, the timing of carcass availability
may be significant given that livestock generally return to villages during the wet season, when
vultures may have to rely more on much scarcer wild ungulate carcasses. These calculations also
suggest that the relatively modest feeding requirements of Cambodia’s vultures (around 100
bovine carcasses per year) are increasingly well supplemented by restaurant sites, which supply
around 70 carcasses per year. These calculations suggest that such modest supplementary feeding
could be an effective conservation measure to overcome the issue of food limitation within
Cambodia and this may help explain the increasing numbers of vultures recorded in Cambodia
during the course of this study.
The major recorded source of mortality for Cambodian vultures is secondary poisoning, usually
relating to the misuse of poisons (possibly organophospates normally used in agriculture) for
hunting or fishing. Poisons are either emptied into waterholes (trapeangs), or delivered in bait
such as rice, fish or fruit to catch scavenging species (such as storks) and frugivores. Vultures are
not the intended targets of these activities, but die from consuming other animals that were killed
Critically Endangered Vultures in Cambodia 9
T. Clements et al. 10
from ingesting poisoned bait. Poisons such as strychnine or organophosphates, used for control of
carnivores or other scavengers such as feral dogs (Cheke 1972), have also killed vultures in
Cambodia. The social feeding behaviour of vultures combined with the scarcity of food in
Cambodia increases the potential that groups of feeding birds may be affected by a single
poisoning event. Poisoning is known to be a significant cause of vulture deaths in other regions
(e.g. Hernández and Margalida 2008,2009), and even low incidences of poisoning can cause
dramatic declines in long-lived birds such as vultures if poisoning results in high mortality rates
and breeding failure (Green et al. 2004; Oro et al. 2008).
A limited number of mortalities due to direct persecution, by firearms or home-made weapons
or use in traditional medicine, were also observed. During the 1970s–1990s, firearms were highly
abundant in Cambodia (Wille 2006), which may have led to widespread hunting and persecution
of birds. However, the majority of these weapons have been brought under Government control
or destroyed (EU ASAC 2009), which may have contributed to a significant reduction in hunting
pressure from the late 1990s onwards. Vulture parts are not used in traditional Chinese medicine,
but they may have some perceived value in Khmer medicine. At least two birds were taken for
their parts and interview reports suggest that traders have visited villages within the remaining
vulture range in Siempang and PVPF requesting capture of birds possibly for sale to Thailand or
Lao PDR (Timmins et al. 2003).
There is limited evidence that diseases affect vultures in Cambodia, as the only known mortality
due to disease was a captive bird during an outbreak of HPAI H5N1Almost all the vultures
sampled carried antibodies to avian encephalomyelitis virus, indicating high rates of exposure, but
the epidemiological significance of this is not clear. Avian encephalomyelitis is a picornavirus that
causes neural deficits in young poultry, and has only rarely been reported in wild birds (galliforms
and ducks; Gerlach, 1994).
Nesting birds in Cambodia are particularly vulnerable to collection and disturbance (Clements
et al. 2010). Nest protection schemes, where local people are employed to guard vulture colonies
and receive a bonus if the nest fledges, have proved effective at ensuring breeding is successful
and locating new breeding sites. This is part of a wider programme in Cambodia that protects
breeding sites for globally threatened species (Clements et al. 2010).
Cambodia remains the only country in the range of these vulture species where veterinary
preparations of diclofenac are not widely available (based on extensive surveys), giving vultures an
Figure 2. Number of (a) White-rumped, (b) Slender-billed and (c) Red-headed vultures recorded at
the six main vulture feeding stations and the total numbers for each species during January 2003–
June 2011. The predicted values and 95% confidence intervals for the best fitting generalised linear
model of vulture numbers are also shown. Sites are arranged in order from north-west to south-
east. Data from KPWS are not shown as counts were low with 1–8RHV normally recorded.
Table 5. Minimum vulture population size for Red-headed, White-rumped and Slender-billed vultures
between 2004 and 2011 recorded during the vulture census.
Date Minimum Population Size
Red-headed Vulture White-rumped Vulture Slender-billed Vulture Total
July 2004 42 90 34 166
May 2006 58 149 31 238
June 2007 40 160 26 226
June 2008 48 191 51 290
June 2009 43 182 41 266
June 2010 45 201 46 292
June 2011 39 183 45 267
Critically Endangered Vultures in Cambodia 11
excellent chance of long-term survival. In early 2009, the National Institute of Animal Health in
Cambodia ordered national veterinary staff to avoid use of diclofenac in veterinary treatments.
Although this does not constitute a legal ban on the drug (as no list of legally approved veterinary
medicines exists as yet), it is an important step in preventing this drug entering the vulture food
chain in Cambodia.
Population size and trends of vultures in Cambodia
A successful monitoring programme must collect accurate data at a sufficient level of precision in
order to detect population changes of a desired magnitude. It must also be within the capacity –
technical, financial and logistical –of management staff (Danielsen et al. 2008). In practice,
achieving both of these is challenging. In India, monitoring was conducted using road surveys
(Prakash et al. 2007), however trials in Cambodia concluded that vulture densities were too low for
this technique to be effective and there are relatively few suitable roads bisecting the vulture range.
Capture-mark resighting methods were evaluated and found to be unsuitable due to the low capture
probabilities. Surveys of breeding sites yielded some population data, but detectability of nest sites
is not known. The census was designed as a low-cost monitoring method that collected data on the
minimum number of birds alive at one time (Krebs 1966). It is not possible to estimate the total
number of vultures in the area, however, because the number of vultures that choose not to visit
the restaurant sites is unknown. Results indicate a minimum of 201 WRV, 48 SBV and 47 RHV in
2010. The numbers recorded are significant in comparison with the only other South-East Asian
population in Myanmar, which was estimated at 141 WRV, 49 SBV and 3RHV in 2006–2007 (Hla
et al. 2011). However these counts were not undertaken simultaneously, so birds could have moved
between sites, inflating the numbers recorded. The Myanmar results may therefore be over-
estimates and are not directly comparable to those from Cambodia.
Between 2004 and 2008 the number of WRV recorded in the census has doubled and SBV has
increased by 50%; numbers have been relatively unchanged since 2008. The relationship between
the census counts and actual population trends is, however, unclear. An increase in vulture
numbers recorded by the census might be indicative of an increasing population, a decrease in food
availability elsewhere in Cambodia (so more birds visit the census sites), or increased habituation of
vultures to the regular feeding sites. At a minimum, the results indicate that the vulture population
is unlikely to have declined since the conservation programme was initiated and perhaps is more
likely to be increasing. Increases were strongest for WRV in the northern sites (PVPF and
Siempang) and for SBV at Siempang, whilst strong decreases were seen for all species at the two
southerly sites (PPWS and MPF). Given that it is unknown what proportion of birds are present but
chose not to visit the restaurant sites, these results could either be due to changing numbers of
vultures at those sites, or due to changes in the proportion of birds in the area visiting the restaurant.
Vultures may become habituated to supplemental feeding sites (Piper 2006), which would cause an
increase in the number observed even if there was no overall change in the population. Habituation
is more likely for the northerly sites because the frequency of feeding events was much greater (1–3
times per month, in comparison with once every 2–3months at the southerly sites), and because
the density of wild ungulates (and hence other food sources) was lower.
Unlike WRV and SBV, RHV has a more cosmopolitan diet and can also feed on reptiles and other
prey (Naoroji 2007); they are therefore less likely to be dependent on feeding from carcasses. RHV
also may show a level of territorial behaviour, unlike the Gyps vultures, and have probably always
existed at lower densities even in South Asia (del Hoyo et al. 1994). The lower numbers of RHV
recorded at the restaurant sites are consistent with these behaviours. However, RHV are distributed
more widely across Cambodia (Figure 1), possibly due to their more cosmopolitan diet, and hence
the true population size of RHV may be significantly greater than the counts obtained.
Vultures range widely across northern and eastern Cambodia, with birds also recorded in
southern Laos and border regions of Vietnam (Figure 1). Although a small number of vultures
T. Clements et al. 12
were tagged in this study for a relatively limited period, some comparisons can be made with
a satellite telemetry study of five adult WRVs marked in Pakistan (Gilbert et al. 2007). These birds
were tracked for 216 days and had home ranges of 68,930 km
2
,40,324 km
2
,4,625 km
2
,1,824 km
2
and 5,069 km
2
respectively. While there is clearly considerable variation in the home range of
individual vultures, the fact that the home range of WRV6and SBV4exceeded that of three of
the birds in Pakistan in a much shorter period of time suggests that birds may be ranging more
widely in Cambodia. This observation would be consistent with variable foraging effort in
environments where food is plentiful (Pakistan) and scarce (Cambodia).
Conservation management
Food provisioning for vultures, otherwise known as ‘vulture restaurants’, is widely used in the
conservation and reintroduction of vulture populations in Africa (Mundy et al. 1992, Piper et al.
1999), Israel (Meretsky and Mannan 1999), Europe (Sarrazin et al. 1994, Carrete et al. 2006) and
condors in North America (Wilbur et al. 1974). Restaurants are thought to have both positive and
negative impacts on vultures (Piper 2006). Positive impacts could include increased nesting success
as has been documented on other threatened raptors (González et al. 2006, but see Margalida 2010),
improved survival rates (Oro et al. 2008), and provision of a safe food source free from potential
poisons (Gilbert et al. 2007, Oro et al. 2008). However, supplemental feeding also changes the
temporal and spatial distribution of food resources so that they become more predictable
(Robb et al. 2008), which may change vulture behaviour (Deygout et al. 2010, Zuberogoitia
et al. 2010), affect fecundity (Carrete et al. 2006) or favour particular individuals or species
(Margalida 2010, Moreno-Opo et al. 2010), including the more dominant Gyps species (Cortés-
Avizanda et al. 2010). These risks were minimised in Cambodia, by staggering the dates of the
restaurants at the different sites, allowing vultures to potentially move between restaurants across
the range, and preventing birds from becoming accustomed to a single site (Deygout et al. 2009).
There was no evidence that restaurants favoured any particular species, and all three species seemed
to be attracted by greater aggregations of birds. Changing the types of food provided at restaurants,
including bigger or smaller carcasses, could further favour increased diversity of vulture species and
other scavengers. Long-term provisioning through vulture restaurants is likely to prove a critical
conservation management activity, given that Cambodian vultures have limited food sources and
restaurants can increase available food supplies in the area by up to 50%.
Food provisioning should be undertaken with local schemes to locate and protect vulture
colonies and a legal ban on diclofenac to ensure the survival of vulture populations. The Royal
Government of Cambodia has instituted measures to ban diclofenac, and their demonstrable
commitment to vulture conservation is greatly welcomed. Local payments to protect nests can be
a cost-effective way to increase breeding success (Clements et al. 2010). The most significant
conservation challenge remaining is to reduce the apparently high levels of direct and indirect
persecution of vultures, particularly from poisoning (responsible for 74% of deaths) and
shooting. Conservation education and advocacy to minimise poisoning and direct persecution
will be essential to limit such losses.
Acknowledgements
The Cambodia Vulture Conservation Project is a collaboration between the General Department of
Administration for Nature Conservation and Protection (GDANCP) of the Ministry of
Environment (MoE), the Forestry Administration (FA) of the Ministry of Agriculture, Forestry
and Fisheries (MAFF), the Wildlife Conservation Society (WCS), BirdLife International in
Indochina, World Wide Fund for Nature (WWF), the Angkor Centre for Conservation of
Biodiversity (ACCB) and Wildlife Alliance. We would like to thank the Royal Society for the
Protection of Birds (RSPB), the Disney Wildlife Conservation Fund, the Global Environment
Critically Endangered Vultures in Cambodia 13
Facility –United Nations Development Program, the Darwin Initiative and the Critical Ecosystem
Partnership Fund for their support. The Critical Ecosystem Partnership Fund is a joint initiative
of l’Agence Française de Développement, Conservation International, the Global Environment
Facility, the Government of Japan, the MacArthur Foundation and the World Bank. A fundamental
goal is to ensure civil society is engaged in biodiversity conservation. Comments from Antoni
Margalida, Ainara Cortés-Avizanda and an anonymous reviewer greatly improved an earlier draft.
Finally, we would like to thank Eleanor Briggs for her unwavering support for conservation in
Cambodia over the years.
References
Baillie, J. E. M., Hilton-Taylor, C. and Stuart,
S. N., eds. (2004)
2004
IUCN Red List of
Threatened Species. A global species assess-
ment. Gland, Switzerland and Cambridge,
UK: IUCN.
Barzen, J. (1995) Other SIS sightings in
northeastern Cambodia. Specialist Group
on Storks, Ibises and Spoonbills Newsletter
7:4–5.
BirdLife International (2008)Threatened
birds of the world. Online at http://www.
birdlife.org. Cambridge, UK: BirdLife
International.
Brickle, N., Nguyen Cu, Ha Quy Quynh,
Nguyen Thai Tu Cuong and Hoang Van
San (1998)The status and distribution of
Green Peafowl Pavo muticus in Dak Lak
Province, Vietnam. Hanoi: BirdLife Inter-
national Vietnam Programme / Institute of
Ecology and Biological Resources. (Conser-
vation Report 1).
Burnham, K. P., Anderson, D. R. and
Huyvaert, K. P. (2011) AIC model selection
and multimodel inference in behavioral
ecology: some background, observations,
and comparisons. Behav. Ecol. Sociobiol.
65:23–35.
Carrete, M., Donázar, J. A. and Margalida, A.
(2006) Density-dependent productivity de-
pression in Pyrenean Bearded Vultures:
implications for conservation. Ecol. Appl.
16:1674–1682.
Cheke, A. (1972) Where no vultures fly.
World of Birds 2:15–22.
Clements, T. J. John, A., Nielsen, K., An, D.,
Tan, S. and Milner-Gulland, E. J. (2010)
Payments for biodiversity conservation in
the context of weak institutions: Compari-
son of three programs from Cambodia.
Ecol. Econ. 69:1283–1291.
Cortés-Avizanda, A., Carrete, M., and
Donázar, J. A. (2010) Managing supple-
mentary feeding for avian scavengers:
Guidelines for optimal design using ecolog-
ical criteria. Biol. Conserv. 143:1707–1715.
Cuthbert, R., Green, R. E., Ranade, S.,
Saravanan, S., Pain, D. J., Prakash, V. and
Cunningham, A. A. (2006) Rapid population
declines of Egyptian vulture (Neophron
percnopterus) and Red-headed vulture (Sar-
cogyps calvus) in India. Anim. Conserv. 9:
349–354.
Danielsen, F., Burgess, N. D., Balmford, A.,
Donald, P. F., Funder, M., Jones, J. P. G.,
Alviola, P. A., Balete, D. S., Blomley, T.,
Brashares, J., Child, B., Enghoff, M.,
Fjeldså, J., Holt, S., Hübertz, H., Jensen,
A. E., Jensen, P. M., Massado, J., Mendoza,
M., Ngaga, Y., Poulsen, M. K., Rueda, R.,
Sam, M., Skielboe, T., Stuart-Hill, G.,
Topp-Jørgensen, E. and Yonten, D. (2008)
Local participation in natural resource mon-
itoring: a characterization of approaches.
Conserv. Biol. 23:31–42.
Das, D., Cuthbert, R. J., Jakati, R. D. and
Prakash, V. (2011) Diclofenac is toxic to the
Himalayan Vulture Gyps himalayensis.
Bird Conserv. Internatn.21:72–75.
del Hoyo, J., Elliott, A. and Sargatal, J., eds.
(1994)Handbook of the birds of the world.
Volume
2
: New World vultures to guinea-
fowl. Barcelona: Lynx Edicions.
Deygout, C., Sarrazin, F., Gault, A., and
Bessa-Gomes, C. (2009) Modeling the im-
pact of feeding stations on vulture scaveng-
ing service efficiency. Ecol. Model. 220:
1826–1835.
Deygout, C., Gault, A., Duriez, O., Sarrazin,
F. and Bessa-Gomes, C. (2010) Impact of
food predictability on social facilitation by
T. Clements et al. 14
foraging scavengers. Behav. Ecol. 21:1131–
1139.
Desai, A. and Lic Vuthy (1996)Status and
distribution of large mammals in eastern
Cambodia: results of the first foot surveys
in Mondulkiri and Rattanakiri Provinces.
Phnom Penh: IUCN/FFI/WWF Large
Mammal Conservation Project.
Duckworth, J. W. and Hedges, S. (1998)
Tracking tigers: a review of the status of
tiger, Asian elephant, gaur, and banteng in
Vietnam, Lao, Cambodia, and Yunnan prov-
ince (China) with recommendations for fu-
ture conservation action. Hanoi, Vietnam:
WWF Indochina Programme.
Duckworth, J. W., Salter, R. E. and
Khounboline, K., eds. (1999)Wildlife in
Lao PDR:
1999
status report.Vientiane:
IUCN-The World Conservation Union /
Wildlife Conservation Society / Centre for
Protected Areas and Watershed Management.
Eames, J. C., Nguyen Duc Tu, Le Trong Trai,
Dang Ngoc Can, Ngo Van Tri, Hoang Duc
Dat, Thai Ngoc Tri and Nguyen Thi Thu
He (2004)Final biodiversity report for Yok
Don National Park, Dak Lak Province,
Vietnam: Creating protected areas for re-
source conservation using landscape ecol-
ogy (PARC) project. Hanoi: FPD/UNOPS/
UNDP/Scott Wilson Asia-Pacific Ltd/
Environment and Development Group and
Forest Renewable Resources Ltd.
Eu Asac (2009)Weapons destruction table
1999
-
2006
. EU ASAC (European Union’s
Assistance on Curbing Small Arms and
Light Weapons in the Kingdom of Cambodia)
website www.eu-asac.org. Accessed 15 May
2009.
Gerlach, H. (1994) Chapter 32, Viruses.
Pp. 862–948 in B. W. Ritchie, G. J. Harrison
and L. R. Harrison eds. Avian medicine:
Principles and application. Lake Worth,
Florida: Zoological Education Network.
Gilbert, M., Watson, R. T., Virani, M. Z.,
Oaks, J. L., Ahmed, S., Chaudhry, M. J. I.,
Arshad, M., Mahmood, S., Ali, A. and
Khan, A. A. (2006) Rapid population de-
clines and mortality clusters in three Orien-
tal white-backed vulture Gyps bengalensis
colonies in Pakistan due to diclofenac poi-
soning. Oryx 40:388–399.
Gilbert, M., Watson, R. T., Ahmed, S., Asim, M.
and Johnson, J. A. (2007)Vulturerestaurants
and their role in reducing diclofenac exposure
in Asian vultures. Bird Conserv. Internatn.
17:63–77.
Goes, F. (1999) Notes on selected bird species
in Cambodia. Forktail 15:25–27.
González, L. M., Margalida, A., Sánchez, R.
and Oria, J. (2006) Supplementary feeding
as an effective tool for improving breeding
success in the Spanish imperial eagle (Aquila
adalberti). Biol. Conserv. 129:477–486.
Gray, T. N. E., Phan, C., Pin, C., and Prum, S.
(2011) Establishing baseline ungulate den-
sities in Mondulkiri Protected Forest and
Phnom Prich Wildlife Sanctuary. Phnom
Penh, Cambodia: WWF.
Green, R. E., Newton, I., Shultz, S.,
Cunningham, A. A., Gilbert, M., Pain, D. J.
and Prakash, V. (2004)Diclofenacpoisoning
as a cause of vulture population declines
across the Indian subcontinent. J. Appl. Ecol.
41:793800.
Green, R. E., Taggart, M. A., Das, D., Pain, D. J.,
Sashikumar, C., Cunningham, A. A. and
Cuthbert, R. (2006) Collapse of Asian
vulture populations: risk of mortality from
residues of the veterinary drug diclofenac in
carcasses of treated cattle. J. Appl. Ecol. 43:
949–956.
Hla, H., Shwe, N. M., Htun, T. W., Zaw, S. M.,
Mahood, S., Eames, J. C. and Pilgrim, J. D.
(2011) Historical and current status of vul-
tures in Myanmar. Bird Conserv. Internatn.
21:376–387.
Hernández, M. and Margalida, A. (2008)
Pesticide abuse in Europe: effects on the
Cinereous Vulture (Aegypius monachus)
population in Spain. Ecotoxicology 17:
264–272.
Hernández, M. and Margalida, A. (2009)
Poison-related mortality effects in the en-
dangered Egyptian vulture (Neophron
percnopterus) population in Spain. Eur. J.
Wild. Res. 55:415–423.
Houston, D. C. (1985) Indian white-backed
vulture Gyps bengalensis. Pp. 465–466 in I.
Newton and R. D. Chancellor, eds. Conser-
vation studies on raptors. Cambridge, UK:
International Council for Bird Preservation.
(Technical Publication No. 5).
Critically Endangered Vultures in Cambodia 15
Jathanna, D., Karanth, K. U. and Johnsingh,
A. J. T. (2003) Estimation of large herbivore
densities in the tropical forests of southern
India using distance sampling. J. Zool.
(Lond.) 2003:285–290.
Kenward, R. E. (2001)A manual for wildlife
radio tagging. London: Academic Press.
Kenward, R. E, South, A. B. and Walls, S. S.
(2003)Ranges
6
v
1
.
2
: For the analysis of
tracking location data. Online manual.
Wareham, UK: Anatrack Ltd.
Krebs, C. J. (1966) Demographic changes in
fluctuating populations of Microtus califor-
nicus.Ecol. Monogr. 36:239–273.
Krebs, C. J. (2009)Ecology.6th edition. San
Francisco: Benjamin Cummings.
Le Xuan Canh, Pham Trong Anh, Duckworth,
J. W., Vu Ngoc Thanh and Lic Vuthy (1997)
A survey of large mammals in Dak Lak
Province, Vietnam. Hanoi: WWF/IUCN.
Long, B., Swan, S. and Kry Masphal (2000)A
wildlife survey of north-eastern Mondul-
kiri Province. Hanoi: Fauna and Flora
International.
Margalida, A. (2010) Supplementary feeding
during the chick-rearing period is ineffec-
tive in increasing the breeding success in
the bearded vulture (Gypaetus barbatus).
Eur. J. Wildl. Res. 56:673–678.
Meretsky, V. J. and Mannan, R. W. (1999)
Supplemental feeding regimes for Egyptian
vultures in the Negev Desert, Israel. J.
Wildl. Manage. 63:107–115.
Moreno-Opo, R., Margalida, A., Arredondo, A.,
Guil, F., Martín, M., Higuero, R., Soria, C.
and Guzmán, J. (2010)Factorsinfluencing the
presence of the Cinereous Vulture Aegy-
pius monachus at carcasses: food preferen-
ces and implications for the management of
supplementary feeding sites. Wildl. Biol.
16:25–34.
Mundy, P., Butchart, D., Ledger, J. and Piper, S.
(1992)The vultures of Africa.London:Aca-
demic Press.
Naoroji, R. (2007)Birds of prey of the Indian
subcontinent. New Delhi, India: Om Books.
NDDB (2006)Indian national dairy develop-
ment board livestock populations in India.
Accessed online on 23/02/2006 at http://
www.nddb.org/statistics/population_india_
species.html
Oaks, J. L., Gilbert, M., Virani, M. Z., Watson,
R. T., Meteyer, C. U., Rideout, B. A.,
Shivaprasad, H. L., Ahmed, S., Chaudhry,
M. J. I., Arshad, M., Mahmood, S., Ali, A.
and Khan, A. A. (2004) Diclofenac residues
as the cause of vulture population decline in
Pakistan. Nature 427:630–633.
O’Kelly, H., Evans, T., Stokes, E., An. D.,
Clements, T., Gately, M., Men, S., Nut, M.,
Pollard, E. and Walston, J. (2011)Status,
trends and potential for recovery of wild
ungulates and tigers in a conservation
landscape in Indochina. Phnom Penh,
Cambodia: Wildlife Conservation Society.
Oro, D., Margalida, A., Carrete, M., Heredia, R.
and Donázar, J. A. (2008)Testingthegood-
ness of supplementary feeding to enhance
population viability in an endangered vul-
ture. PLoS One 3:e4084.
Pain, D. J., Bowden, C. G. R., Cunningham,
A. A., Cuthbert, R., Das, D., Gilbert, M.,
Jakati, R. D., Jhala, Y., Khan, A. A., Naidoo,
V., Oaks, J. L., Parry-Jones, J., Prakash, V.,
Rahmani, A., Ranade, S. P., Baral, H. S.,
Senacha, K. R., Saravanan, S., Shah, N.,
Swan, G., Swarup, D., Taggart, M. A.,
Watson, R. T., Virani, M. Z., Wolter, K.
and Green, R. E. (2008) The race to prevent
the extinction of South Asian vultures. Bird
Conserv. Internatn. 18:S30–S48.
Pain, D. J., Cunningham, A. A., Donald, P. F.,
Duckworth, J. W., Houston, D. C., Katzner,
T., Parry-Jones, J., Poole, C. M., Prakash, V.,
Round, P. D. and Timmins, R. J. (2003)
Causes and effects of temporospatial declines
of Gyps vultures in Asia. Conserv. Biol. 17:
661–671.
Piper, S. E. (2006) Supplementary feeding
programmes: how necessary are they for
the maintenance of numerous and healthy
populations. Pp. 41–50 in D. C. Houston
and S. E. Piper, eds. Proceedings of the
international conference on conservation
and management of vulture populations.
Thessaloniki, Greece: Natural History Mu-
seum of Crete.
Piper, S. E., Boshoff, A. E. and Scott, H. A.
(1999) Modelling survival rates in the Cape
Griffon Gyps coprotheres, with emphasis
on the effects of supplementary feeding.
Bird Study 46 (Suppl.): S230–238.
T. Clements et al. 16
Prakash, V. (1999) Status of vultures in Keo-
ladeo National Park, Bharatpur, Rajasthan,
with special reference to population crash in
Gyps species. J. Bombay Nat. Hist. Soc. 96:
365–378.
Prakash, V., Green, R. E., Pain, D. J.,
Ranade, S. P., Saravanan, S., Prakash, N.,
Venkitachalam, R., Cuthbert, R., Rahmani,
A. and Cunningham, A. A. (2007) Recent
changes in populations of resident Gyps
vultures. J. Bombay Nat. Hist. Soc. 104:
129–135.
Prakash, V., Pain, D. J., Cunningham, A. A.,
Donald, P. F., Prakash, N., Verma, A.,
Gargi, R., Sivakumar, S. and Rahmani,
A. R. (2003) Catastrophic collapse of Indian
white-backed Gyps bengalensis and long-
billed Gyps indicus vulture populations.
Biol. Conserv. 109:381–390.
R Development Core Team (2011)R: A
language and environment for statistical
computing. Vienna, Austria: R Foundation
for Statistical Computing. http://www.
R-project.org/.
Robb, G. N., McDonald, R. A., Chamberlain,
D. E. and Bearhop, S. (2008) Food for
thought: supplementary feeding as a driver
of ecological change in avian populations.
Front. Ecol. Environ. 6:476–484.
Round, P. D. (1988)Resident forest birds
in Thailand. Cambridge, UK: Interna-
tional Council for Bird Preservation
(Monograph 2).
Round, P. D. and Chantrasmi, V. (1985)A
status report on birds of prey in Thailand.
Proc. Third East Asian Bird Protection
Conference:291–297.
Sarrazin, F., Bagnolini, C., Pinna, J. L.,
Danchin, E. and Clobert, J. (1994) High
survival of Griffon vultures (Gyps fulvus
fulvus) in a reintroduced population. Auk
111:853–862.
Srikosamatara, S. and Suteethorn, V. (1995)
Populations of gaur and banteng and their
management in Thailand. Nat. Hist. Bull.
Siam Soc. 43:55–83.
Swan, G. E., Naidoo, V., Cuthbert, R.,
Green, R. E., Pain, D. J., Swarup, D.,
Prakash, V., Taggart, M., Bekker, L., Das,
D., Diekmann, J., Diekmann, M., Killian, E.,
Meharg, A., Patra, R. C., Saini, M. and
Wolter, K. (2006) Removing the threat of
diclofenac to Critically Endangered Asian
vultures. PLoS Biol. 4:1–8. Protocol S1.
Estimating likely MLE of Meloxicam. DOI:
10.1371/journal.pbio.0040066.sd001.
Thewlis, R. M., Timmins, R. J., Evans, T. D.
and Duckworth, J. W. (1998) The conser-
vation status of birds in Laos: a review of
key species. Bird Conserv. Internatn. 8
(supplement): 1–159.
Timmins, R. J. and Men Soriyun (1998)A
wildlife survey of the Tonle San and Tonle
Srepok river basins in north-eastern
Cambodia. Phnom Penh: Fauna and Flora
International and Wildlife Protection Office.
Timmins, R. J. and Ou Ratanak (2001)The
importance of Phnom Prich Wildlife Sanc-
tuary and adjacent areas for the conserva-
tion of tigers and other key species. Hanoi
and Phnom Penh: WWF Indochina
Programme.
Timmins, R. J., Pech, B. and Prum, S. (2003)
An assessment of the conservation impor-
tance of the Western Siem Pang area,
Stung Treng province, Cambodia. Phnom
Penh: WWF Cambodia Program.
WCS, BirdLife International, WWF, MoE and
MAFF (2004)Cambodia vulture conserva-
tion action Plan. Phnom Penh: Wildlife
Conservation Society, BirdLife Interna-
tional, World Wide Fund for Nature, Min-
istry of Environment and Ministry of
Agriculture, Forestry and Fisheries.
Wells, D. R. (1999)The birds of the Thai-
Malay Peninsula, Vol.
1
: Non-passerines.
London: Academic Press.
Wilbur, S. R., Carrier, W. D. and Borneman,
J. C. (1974) Supplemental feeding program
for California Condors. J. Wildl. Manage.
38:343–346.
Wille, C. (2006)How many weapons are
there in Cambodia? Small arms survey:
Geneva, Switzerland.
Wint, W. and Robinson, T. (2006)Gridded
livestock of the world. FAO: Rome.
Zheng Guangmei and Wang Qishan (1998)
China Red Data Book of endangered ani-
mals: Aves. Beijing: Science Press.
Zuberogoitia, I., Martínez, J. E., Margalida, A.,
Gómez, I., Azkona, A. and Martínez, J. A.
(2010) Reduced food availability induces
behavioural changes in Griffon Vultures
Gyps fulvus.Ornis Fennica 87:52–60.
Critically Endangered Vultures in Cambodia 17
TOM CLEMENTS*
1
, MARTIN GILBERT, HUGO J. RAINEY
Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY 10460, USA
1
and
Department of Zoology, University of Cambridge, Downing Street, Cambridge CB23EJ, UK.
JONATHAN C. EAMES
BirdLife International in Indochina, N6/2+3, Lane 25, Lang Ha Street, Hanoi, Vietnam.
SENG TEAK
World Wide Fund for Nature –Cambodia Program, House #54, Street 352, Boeung Keng Kang I,
PO Box 2467, Phnom Penh, Cambodia.
RICHARD CUTHBERT
Conservation Science, Royal Society for the Protection of Birds, The Lodge, Sandy, Bedfordshire,
SG19 2DL, UK.
TAN SETHA
Ministry of Agriculture, Forestry and Fisheries, Royal Government of Cambodia, Cambodia.
PECH BUNNAT, SONG CHANSOCHEAT
Ministry of Environment, Royal Government of Cambodia, Cambodia.
*Author for correspondence; email: tclements@wcs.org
Received 31 December 2010; revision accepted 17 January 2012
T. Clements et al. 18
