The conservation of Accipitridae vultures
of Nepal: a review
Richard J. Harris
3 Burbank Crescent,
Singleton, NSW, 2330, Australia
rha06927@bigpond.net.au
doi: http://dx.doi.org/10.11609/JoTT.o2816.3603-19 | ZooBank: urn:lsid:zoobank.org:pub:9B0EB522-E857-44A2-9D33-F6D79244C50F
Editor: Chris Bowden, Royal Society for
the Protection of Birds, Sandy, UK Date of publication: 26 February 2013 (online
& print)
Manuscript details: Ms # o2816
| Received 30 May 2011 | Final received 06 November 2012 | Finally accepted 07
February 2013
Citation: Harris, R.J. (2013). The
conservation of Accipitridae vultures of Nepal: a review. Journal of
Threatened Taxa 5(2): 3603–3619; doi:10.11609/JoTT.o2816.3603-19.
Copyright: © Harris 2013. Creative Commons Attribution 3.0 Unported License. JoTT
allows unrestricted use of this article in any medium, reproduction and
distribution by providing adequate credit to the authors and the source of
publication.
Funding: Self funded.
Competing Interest: None.
Acknowledgements: I wish
to thank Dr Hem Baral of Himalayan Nature, Nepal and Dr. Iain Taylor of Charles
Sturt University, Australia for their invaluable guidance and advice during the
process of researching and writing this manuscript.
Author Details: Member,
Birdlife Australia
Abstract: Of the nine Accipitridae vulture species found
within Nepal the IUCN categorises White-rumped, Indian Vulture, Slender-billed
and Red-headed Vultures as Critically Endangered and
Egyptian Vulture as Endangered. Dramatic declines have occurred since the mid
1990s with the White-rumped Vulture, Indian Vulture and Slender-billed Vulture
population declining by over 97%. The remaining species are listed as Near
Threatened or Least Concern. Veterinary use of the non-steroidal
anti-inflammatory drug (NSAID) diclofenac has been proven to be a key threat in
the region for Gyps vultures and appears likely that it may also
affect other Accipitridae vultures. The drug is transferred to vultures via
consumption of dead livestock carcass. Ingestion of the drug causes visceral
gout and kidney failure, which leads to the birds’ death. Consumption of
diclofenac and the majority of other non-steroidal anti-inflammatory drugs are
fatal to individuals. Only one NSAID, meloxicam, has been tested and proven
safe for vultures. There are other factors such as food shortage in local
scale, habitat loss, climate change and pesticides/poisoning that play some
role on population decline. Managing vulture conservation across Nepal can be
problematic just as it is throughout the Indian subcontinent due to the
variable level of protection afforded to vultures through legislation and
enforcement in each political region particularly regarding NSAID regulation
and use. However, great gains have been made on removing diclofenac from sale
within the Indian subcontinent. Continuing and enhancing the holistic
conservation approach between all stakeholders, government and non-government
organisations, across the species range is required to conserve them for future
generations. Indeed, it is likely that a number of species will become extinct
if a greater conservation effort is not forthcoming in the very near future.
Keywords: Diclofenac, Gyps, Nepal,
NSAIDs, threatening processes, vulture.
Abbreviations: BCN - Bird Conservation
Nepal; DDT - Dichlorodiphenyltrichloroethane; DFZ - Diclofenac Free Zone; GIS -
Geographic Information System; IUCN - International Union for Conservation of
Nature; NGOs - Non-government Organisations; NSAIDs - Non-steroidal
Anti-inflammatory Drugs; SAVE - Saving Asia’s Vultures from Extinction; VDC -
Village Development Committee; VSZ - Vulture Safe Zone.
For
figures, images, tables -- click here
Introduction
Nepal supports nine
Accipitridae vulture species (Baral et
al. 2003; DeCandido et al. 2012; IUCN 2012h; Subedi &
DeCandido unpub.). These are
Lammergeier Gypaetus barbatus, Egyptian Vulture Neophron percnopterus,
White-rumped Vulture Gyps bengalensis, Indian Vulture G. indicus)
(recent visitor), Slender-billed Vulture G. tenuirostris, Himalayan
Vulture G. himalayensis, Griffon Vulture G. fulvus (a passage
migrant), Cinereous Vulture Aegypius monachus (a winter visitor) and
Red-headed Vulture Sarcogyps calvus. Taxonomy and nomenclature follow
BirdLife International (2011).
Three Gyps species,
White-rumped Vulture, Indian Vulture and Slender-billed Vulture, and one Sarcogypsspecies, Red-headed Vulture, are found across the Indian subcontinent and are
in grave danger of extinction. The
three Gyps species have rapidly declined by more than 97% since the mid
1990s (Gilbert et al. 2002; Cuthbert et al. 2006;
Baral & Gautam 2007; Arshad et al. 2009). Recent data suggests that Red-headed
Vultures are likely to decline by at least 90% by end 2016 (Cuthbert et
al. 2006). The IUCN has classified
these four vulture species as Critically Endangered (IUCN, 2012c,f,g,j). Population of Egyptian Vulture (Cuthbert et al. 2006) and
Himalayan Vulture (Acharya et al. 2009) is also declining. Little is known about the population
trends of other vulture species.
Wild ungulates are not a
large part of the diet of these species in Nepal. Their diet consists mainly of domestic
livestock (Baral 2010). Population
declines were first noticed in India in the early 1990s (Satheeson 1999), while
the linking of the deaths to the veterinary use of the NSAID diclofenac did not
occur until 2003 (Oaks et al. 2004; Shultz et al. 2004). Between
2000–2003 Oaks et al. (2004) studied the high adult and subadult
mortality resultant of renal failure and visceral gout. Their study revealed a direct
correlation between renal failure, visceral gout and the diclofenac residue
presence in the kidney or liver. Diclofenac is commonly used to treat pain and inflammation in livestock
in India, Pakistan and Nepal (Green et al. 2004; Oaks et al. 2004; Shultz et
al. 2004). Controlled experiments
confirmed the contributory relationship of diclofenac poisoning on both captive
Asian and African White-backed Vultures (Oaks et al. 2004; Swan et al.
2006). Vultures are carrion feeders
consuming both fresh and putrid dead animals. Considerable aggregations can
form during consumption of carcases (Gilbert et al. 2006; Jackson et al.
2008). Vultures are exposed to
diclofenac when they feed on carcases of livestock that were dosed with the
drug shortly before death. Birds
die as a result of visceral gout that subsequently causes kidney failure. Death usually occurs within a few days
of exposure (Green et al. 2004; Oaks et al. 2004; Swan et al. 2006).
The use of NSAIDs along with
other threats introduced by humans continues to impact on population viability
of many vulture species. Vultures
play a key role in the wider landscape as providers of ecosystem services
(Sekercioglu 2006; Olea & Mateo-Tomás 2009), and were previously heavily
relied upon to help dispose off animal and human remains in India, Nepal and
Tibet (Rahmani 2004; IUCN 2012c). This review outlines distribution, population status and principal
threats to Accipitridae vultures that are resident within, or migrate to Nepal,
with emphasis on human induced impacts on individuals and populations. I also outline current conservation
efforts in Nepal, some of which I observed during November-December 2010.
Study
Area
Nepal is located between two
of the world’s most highly populated countries, China to the north and India to
the south, east and west. It is
located between 26020’–30026’N & 80015’–88010’E. The majority of Nepal lies in central
Himalaya and covers an area of 147,181km2 averaging 870km from east
to west with a population of approximately 30 million people (Government of
Nepal 2010; RAOnline 2010b).
Topography
Nepal is generally divided
into five broad biogeographic regions (Fig. 1). These are the Terai <750m, Siwaliks
700–1,500 m, Middle Mountains 1,500– 2,700 m, High Mountains
2,200–4,000 m, and High Himalaya 4,000–8,000 m. Eight of the highest peaks in the world
and the world’s deepest gorge (5,791m) in the Kali Gandaki Valley,are located in this region. The
snowline varies from 5,000m in the east to 4,000m in the west (RAOnline
2010b). All five bioregions
parallel each other, from east to west, as continuous ecological belts,
occasionally bisected by the country’s river systems (RAOnline 2010c).
Climate
Nepal has a great deal of
variation in climate with five identified climatic zones (Table 1) based on
altitude (Savada 1991; Vetaas & Grytnes 2002). The significant differences in climatic
conditions are principally correlated with the enormous variation in altitude
from the south to the north of the country (Savada 1991; RAOnline 2010a).
Conservation Status of Nepal’s vultures
There has been a catastrophic
decline in the populations of three Gyps species in the Indian
subcontinent, White-rumped Vulture, Indian Vulture and Slender-billed
Vulture (Table 2) (Gilbert et al. 2002; Prakash et al. 2003). Red-headedVulture has also suffered catastrophic declines in the Indian subcontinent
including Nepal (Cuthbert et al. 2006) believed to be primarily due to
diclofenac poisoning (Green et al. 2004; Meteyer et al. 2005; Cuthbert et al.
2006; Swan et al. 2006; Cuthbert et al. 2007; Naidoo & Swan 2009). This has resulted in the
reclassification of these species (Table 3) to Critically Endangered (IUCN
2012h).
Egyptian Vultures are a
long-lived species, which are classified as Endangered because of recent and
extremely rapid population declines in India and Nepal. The suspected cause is
poisoning by the veterinary drug diclofenac. Severe long-term declines have also
occurred in Europe and West Africa, plus ongoing declines throughout much of
the rest of this species range in Africa (IUCN 2012i).
Cinereous Vultures qualify as
Near Threatened. They have a moderately small population that appears to
be suffering an ongoing decline in its Asiatic strongholds, even though in
parts of Europe numbers are now increasing (IUCN 2012a).
Himalayan Vulture, Griffon
Vulture and Lammergeier are listed as Least Concern. They do not meet the definition for
Vulnerable under range size criterion (Extent of Occurrence
<20,000km2 combined with a declining or fluctuating range size,
habitat extent/quality, or population size and a small number of locations or
severe fragmentation) (IUCN 2012b,d,e). Population trends of Himalayan Vulture
and Lammergeier show declines through much of their range (Acharya et al. 2009;
IUCN 2012b) while Griffon Vulture appear to be increasing (IUCN 2012d).
Species
Distribution
All species maps below except
for the Indian Vulture were derived from GIS polygon shape files supplied by
Birdlife International (Birdlife International & NatureServe 2011). The Indian Vulture record was obtained
from location data recorded by Tulsi Subedi and Robert DeCandido during their
visit to a vulture feeding station near Pitauli, Nepal in December 2011 (Subedi
& DeCandido unpub.)
White-rumped Vulture (Fig. 2)
White-rumped Vultures range
from Myanmar in the east through to Pakistan and India in the west (IUCN
2012c). The global population is
estimated to be from 2,500 to 10,000 mature individuals (Birdlife International
2012; IUCN 2012c).
In Nepal, this species occurs
mostly below 1,000m in the Terai plains and less frequently in hilly regions up
to 1,800m over summer where it frequents light woodland, human habitation, and
open areas (Grimmett et al. 2000; Prakash et al. 2003). Communal roost sites
are also regularly used (Gilbert et al. 2006). It breeds in colonies in tall trees such
as Bombax ceiba and Ficus religiosa, often near human habitation
(Paudel 2008; Baral 2010; IUCN 2012c). It is a social species, usually found in conspecific flocks. Movements are poorly known, although
Gilbert et al. (2007) showed that a satellite-tagged individual can forage over a vast range. The degree of connectivity of
seemingly separate populations and conspecific flocks is not known (IUCN
2012c). The total population has dramatically declined since the mid 1990s to
the point that it is highly threatened with extinction (Prakash et al. 2003).
Indian Vulture (Fig. 3)
Until recently, this species
had not been recorded in Nepal. Two
individuals were observed in December 2011 near Pithauli, Nepal. This species may have been overlooked
previously due to its similarity to Slender-billed Vulture (DeCandido et
al. 2012; Subedi & DeCandido unpub.). Indian Vultures normally range through southeastern Pakistan and
peninsular India south of the Gangetic plain. The global population is estimated to be
about 45,000 mature individuals (Birdlife International 2012).
Indian Vultures are found
within cities, towns and villages associated with cultivated areas. It also inhabits open and wooded areas,
and is often associated with White-rumped Vulture when scavenging. Indian Vultures nest almost exclusively
in small colonies on cliffs and ruins, rarely in trees (Birdlife International
2012).
Slender-billed Vulture (Fig. 4)
Slender-billed Vultures range
through southern Nepal. They also
occur from Myanmar in the east to northern India in the west. This species formerly occurred more
widely in Southeast Asia (IUCN 2012g). Global population of this species is estimated to be from 2,500 to
10,000 mature individuals (Birdlife International, 2012).
Slender-billed Vultures
inhabit open forests up to 1,500m in the vicinity of human habitation (Grimmett et al. 2000; IUCN 2012g). It is
a carrion feeder often scavenging at rubbish dumps and slaughterhouses. Nesting
sites are located in trees usually at a height between 7m and 14m, often near
villages (Baral 2010; IUCN 2012g).
Himalayan Vulture (Fig. 5)
This species is widespread
and locally common in Nepal, usually between 900m and 4,000m (Grimmett et al.
2000). However, numbers are
declining in Upper Mustang, Nepal (Acharya et al. 2009). It ranges from China in the east through
northern India to Kazakhstan at the northern extremity of its range (IUCN
2012e). The global population is estimated to be 100,000 mature individuals (Birdlife
International 2012). It inhabits
grasslands, temperate-grasslands and rocky areas such as cliffs and mountain
peaks. Breeding occurs between 600–4,500 m. Non-breeding birds migrate to lower
altitudes to spend the boreal winter in the plains (Li & Kasorndorkbua
2008). Numbers of Himalayan Vulture
migrating to these areas and into India are increasing (Acharya et al. 2009).
Griffon Vulture (Fig. 6)
The Griffon Vulture is a
wide-ranging species found from Mongolia and China in the east through Nepal to
northwestern Africa. Global
population appears to be quite large and increasing (IUCN 2012d) and is
estimated to be around 100,000 mature individuals (Birdlife International
2012). It is widespread in Nepal
and found frequently below 915m. During summer, individuals have often been observed in higher altitudes
up to 3,050m (Grimmett et al. 2000). This species inhabits shrublands,
grasslands and rocky areas similar to Himalayan Vulture (IUCN 2012d).
Red-headed Vulture (Fig. 7)
The Red-headed Vulture is an
uncommon resident in Nepal generally observed below 2,000m in open country near
habitation and wooded hills (Grimmett et al. 2000). It is sparsely distributed and declining
but still fairly common in the western Himalayan foothills of India (IUCN 2012j). Historical reports indicate that this
species was widespread and generally abundant, but it has undergone a
population and range decline since the 1990s. Evidence from India indicates that the
species started undergoing a rapid decline (41% per year) in about 1999, and
declined by 94% between 2000 and 2003 (Cuthbert et al. 2006). The global population is estimated to be
from 2,500 to 10,000 mature individuals (Birdlife International 2012).
Egyptian Vulture (Fig. 8)
Egyptian
Vultures are mostly found in open country near habitation. This species has been observed up to
915m in Nepal with excursions to 3,800m during summer (Grimmett et al.
2000). They occupy a large range
from India and Kazakhstan in the east through to western Africa. The core population occurs in Ethiopia,
East Africa, Arabia and the Indian subcontinent. Global population is likely from 21,000
to 67,200 mature individuals (Birdlife International 2012). These birds winter within the resident
range (IUCN, 2012i).
Cinereous Vulture (Fig. 9)
Cinereous Vultures range
through Nepal principally north of the Terai. They are also found from Mongolia and mainland China in the east through to Turkey in the
west. There is also a small
population in Spain and France (IUCN 2012a). The global population is
decreasing and is likely from 14,000 to 20,000 mature individuals (Birdlife
International 2012).
In areas where there are few
domestic livestock, populations of Cinereous Vultures are declining. This is likely due to an overall reduction
of available food sources (Milner-Gulland et al. 2001). Little is known about population trends
on wintering grounds, although wintering populations appear to be declining in
Nepal and increasing in India (IUCN 2012a).
Lammergeier (Fig. 10)
The Lammergeier is a
reasonably common resident in Nepal occurring between 1,200–4,100 m
(Grimmett et al. 2000) where it inhabits grasslands, shrubland, rocky areas, artificial and urban areas (IUCN 2012b). It ranges from Mongolia and China west
to Afghanistan. It is also found
from Iran to Turkey, eastern and north western Africa
and Spain. The global population
may be small, approximately 2,000 to 10,000 mature individuals, however at this
time does not meet the criteria as a threatened species (Birdlife International
2012; IUCN 2012b).
Existing and Potential Threatening
Processes
The main contributory factor
causing declines in many vulture species is the use of the veterinary drug
diclofenac (Oaks et al. 2004; Shultz et al. 2004), which has been available and
in use since c. 1990 in India (Pain et al. 2008). The population of
White-rumped and Slender-billed Vultures are now quite small mostly due
to diclofenac.
Lammergeier and Egyptian
Vulture are now also declining rapidly but there is no direct evidence that
diclofenac is the cause. However,
the geographic extent and rate of decline is similar to the Gypspopulations suggesting diclofenac (Cuthbert et al. 2006). The decline from many
other parts of their former ranges may have been exacerbated by food shortages,
persecution, infectious diseases and chemical contaminants (Cuthbert et
al. 2006). However, these causes
have been ruled out for Gyps species (Pain et al. 2003; Prakash et al.
2003).
Further declines have
resulted from human impacts such as human population growth and associated
deforestation, grazing and cropping and the resulting reduction of traditional
food sources (Guzmán et al. 2006; Baral & Gautam 2007; Margalida et al.
2007, 2009; Morán-lópez, Guzmán et al. 2006; Zuberogoitia et al. 2008). Infectious diseases, environmental
contamination, deliberate and accidental poisoning along with exploitation and
persecution (Rahmani 2004) may also contribute to population declines.
1. Consumption of NSAIDs
Diclofenac is largely
regarded as one of the most devastating environmental toxicants in recent times
(Naidoo & Swan 2009) and has been found to be highly toxic to at least six
of the eight Gyps species (Swan et al. 2006; Das et al. 2011). Dead vultures, which were contaminated
with diclofenac residues, have been recovered across India, Nepal and Pakistan
(Shultz et al. 2004; Oaks et al. 2004). Analysis of 38 kidney samples from White-rumped Vulture obtained from
Pakistan during 2000–2002 found that all 25 birds that died with visceral
gout also had detectable levels of diclofenac. Thirteen that died without visceral gout
did not have any detectable diclofenac (Oaks et al. 2004). Unfortunately, vultures do not have the
biological means to excrete the drug (Baral 2010). Therefore, small quantities of
diclofenac may kill an individual or group of vultures.
After accidental exposure to
diclofenac through their food chain via the ingestion of tissues from dead
livestock treated with the drug, populations of three species of Gypsvultures in South Asia, the White-rumped Vulture, Slender-billed Vulture and
Indian Vulture have collapsed over the last decade. All are resident in Nepal (Oaks et al.
2004; Shultz et al. 2004; Naidoo & Swan 2009; IUCN 2012c,f,g) except possibly the Indian Vulture which was only
recently accepted as authentic sightings by the Nepal Rare Bird Committee
(DeCandido et al. 2012). Adding to this alarming trend the Himalayan Vulture is also suffering
substantial declines in some areas likely due to diclofenac poisoning (Acharya et al. 2009; Das et al. 2011). In the Annapurna Conservation Area, Mustang, Nepal the Himalayan Vulture
is not suffering the same level of decline as other areas have. This is likely due to different foraging
behaviours than other Gyps species and/or less use of diclofenac (Virani
et al. 2008). Other vulture
populations, including the Indian Vulture, Red-headed Vulture and Egyptian
Vulture, have also recently undergone rapid declines in India (Prakash et al.
2003; Cuthbert et al. 2006; Prakash et al. 2007). Diclofenac has been banned in Nepal,
India and Pakistan since 2006, and Bangladesh in 2010 (Pain et al. 2008; Baral
2010). However, illegal use still
occurs including the illicit use of human diclofenac on animals (Paudel 2008;
Taggart et al. 2009; Baral 2010). Given the overwhelming evidence that diclofenac is the major cause of
vulture declines (Green et al. 2004, 2007) and that diclofenac is toxic to all Gypsspecies (Swan et al. 2006; Das et al. 2011), it stands to reason that
differences in declines between regions will correspond to differences in
diclofenac availability and use.
Cuthbert et al. (2007)
pointed out in their study that other NSAIDs are also harmful to other species
of scavenging birds. Carprofen and
flunixin appeared to carry a high risk of renal damage in birds
which backed up previous claims by Klein et al. (1994) and Clyde &
Murphy cited in Cuthbert et al. (2007). Naidoo et al. (2010) demonstrated in their study that, ketoprofen is
toxic to two South African Gyps species at doses that would be
encountered in the wild if they consumed flesh from livestock carcasses within
hours of their treatment. The
symptoms and clinical signs at necropsy, visceral gout and kidney damage, were
identical to those found in Gyps species resident in Nepal.
It is of concern that a
number of NSAIDs have not been tested and proven safe for vultures. Many are in widespread use within the
range of resident and migratory Accipitridae vultures. These include metamizole,
phenylbutazone, ibuprofen, naproxen, nimesulide (Taggart et al. 2010)
and aceclofenac (Sharma 2012). As
the toxicity of these drugs to vultures is unknown, there may well be similar
effects on individuals and populations that diclofenac and ketoprofen have
demonstrated. At this time, the
only NSAID that has been tested and proven safe for vultures is meloxicam
(Cuthbert et al. 2007; Naidoo et al. 2007). Research by Prakash et al. (2006) on
poultry suggests that nimesulide may be safe for vultures,however rigorous testing is required before this drug is proven safe.
2. Ingestion of Chemicals and
Lead
Poisoning resulting from
chemical contaminants such as agricultural chemicals can be responsible for
high mortality rates and reduced reproductive success in many species including
raptors (Pain et al. 2003) and thus Accipitridae vultures. Organochlorines such as DDT are
responsible for reproductive failure and high mortality rates of avain
predators and scavengers in many countries (Provini & Galassi, 1999;
Muralidharan et al. 2008; van Drooge et al. 2008; Dhananjayan et al.
2011). Farmers in India use large
concentrations of pesticides with their use increasing during the 1980’s which may well have affected migrating vultures and
the Nepal vulture population along the border regions. However, evidence suggests that over the
last decade pesticide use may have reduced slightly (Pain et al. 2003).
Between 2000 and 2002 Oaks et
al. (2004) performed 259 post-mortem examinations on adult and sub-adult
White-rumped Vultures in Pakistan. Detailed necropsies were carried out on 14 without visceral gout and 28
with visceral gout. Each of these
42 birds was screened for a wide range of contaminants (Table 4).
Most tests resulted in below
toxin concentrations other than one case of lead toxicity and one of
organophosphate poisoning. Further
research is required in Nepal to ascertain the level of use and environmental
contamination by both agricultural and industrial chemicals and heavy metals. However, it is unlikely that pesticide
and herbicide chemical contamination will have the same impact as NSAIDs (Pain
et al. 2003). The ingestion and
bioaccumulation of lead in bone tissues can also be a major problem in
long-living birds of prey including vultures (Mateo et al. 1999, 2001; Gangoso
et al. 2009).
Recent research on broad spectrum animal husbandry antibiotics by Lemus et al.
(2009) has found that fluoroquinolone residues were obtained from most
unhatched eggs sampled in Central Spain. Fluoroquinolone is a commonly used antimicrobial drug, and is the drug
of choice for the majority of most common diseases in livestock and
poultry. The toxic effects of
fluoroquinolone were found to be detrimental to the development of embryos and
may thus promote hatching failure. On death, fluoroquinolone treated stocks are often deposited in
traditional livestock carcass dumps or vulture restaurants. Gyps vultures in this area of
Spain, feed at these vulture restaurants and carcass dumps. This results in chemical contamination
of those individuals feeding on the carcases. It is not known if related impacts
result in vulture deaths in Nepal. Further research is required to determine if similar contamination is
actually occurring.
3. Consumption of poison
baits
Deliberate and accidental
poisoning can have a significant impact on vulture populations, however, it
cannot be certain if direct persecution in Nepal is impacting on resident
vulture species (Pain et
al. 2003; Rahmani 2004). Targeted
poisoning of carnivores does occur in Nepal even though it is illegal. This makes it almost impossible to
measure the extent or importance of the problem. Considering that vultures feed in a
communal manner with large aggregations around carcases, it is possible that a
small number of carcases could have serious consequences for vulture
populations already in decline in a similar manner that diclofenac has impacted
(Rahmani 2004). Monitoring the
scale and importance of poisoning of vulture populations is required to assist
in assessing population impacts.
4. Consumption of human made
non-food items
Houston et al. (2007) studied
the implications of condors and vultures consuming junk material such as
indigestible, non-food and other human-made objects. The material consisted of glass, china,
plastic, metal, rocks, sticks, grass, wool, fur and other items. Gypsvultures specialise in feeding on muscle and viscera from large mammals
(Houston et al. 2007). It is
hypothesised that the consumed fragments are mistaken for bone fragments, a
source of calcium required in their diet. Females require a higher amount of calcium to produce eggshells and
chicks are fed bone fragments to provide calcium for healthy growth. However, the slow growth rate of vulture
chicks requires less calcium than other raptors (Houston 1978) therefore
ingestion of bone fragments is also likely to be less.
Vultures may also consume
junk to help in forming pellets for regurgitating keratin such as hair, hoofs
and horn. Indigestible fibrous material, such as grass, leaves, twigs and bark, has been
found in pellets along with solid objects (Benson et al. 2004). The normal ingestion of indigestible
materials is clearly an adaptive behaviour to assist in regurgitation of
pellets. The swallowing of human
litter with sharp edges can harm an individual internally and may be life
threatening. Similarly, human
litter that is toxic to vultures may also be consumed. Some of these junk items are fed to chicks which results in an accumulation in their gut. As chicks’ oesophagus muscles are not as
strong as their parents they may not have the strength to eject them (Houston
et al. 2007).
The level of impact in
relation to death rates from ingestion of human made objects has not been
sufficiently studied to provide conclusive results. Accipitridae vultures of Nepal may well
be affected to some degree by this behaviour.
5. Anthropogenic Climate
Change
There is overwhelming
evidence that modification of the environment by humans will more than likely
result in future climate change. Human induced activities such as energy use, industrial processes,
solvent and other product use, agriculture, land use change and forestry, and
waste are driving increases in greenhouse gas emissions that in turn are
drivers of climate change. Climate
change is now occurring at a faster rate than has previously occurred
naturally. Anthropogenic climate
change is likely to involve both changes in average temperature conditions and
changes to the frequency of occurrence of extreme events (DECC 2005; Solomon et
al. 2007).
Before 1970, the Nepal
region’s climate consisted of general cooling or constant trends. In the mid
1970s a warming trend started, that continues today. These trends are
consistent with the majority of the northern hemisphere. The relatively high rate of warming in
Nepal after the mid-1970s is due predominantly to the high rates of warming in
the high elevation areas of the Himalayas and middle mountains (Shrestha et
al. 1999). The result is the retreat of glaciers as is being experienced in
many places around the Earth (Oerlemans & Fortuin 1992; Dyurgerov &
Meier 1997; Joughin et al. 2004).
This process will result in
the displacement of many species, populations and communities that can move
across the landscape and possible extinction of many others that are restricted
in movement. Species at risk
include those with poor mobility, narrow ranges, specific host relationships,
isolated and specialised species and those with large home ranges and long
generations (DECC 2005) such as vultures. Changes in climate allow one to predict that the generalised effects of
human induced climate change would increase breeding failure in the future in
vulture populations. However,
nesting habitats may be extended to higher altitudes as these areas warm
(Morán-lópez et al. 2006).
6. Deforestation
Deforestation through
urbanisation, agricultural practices and logging activities has resulted in
extensive fragmentation (Gautam et al. 2004; Bhattarai et al. 2009) and thus a
reduction in habitat. Many tree species
are exported for commercial gain (Mathew 1987). Communities also harvest most of the
mature trees from community managed forests while
allowing younger trees to mature for future use. B. ceibaprovides excellent building material and brings a reasonable price for individuals
or communities. In 2002, 40 mature B.
ceiba trees were harvested in the Rampur area to support a community school
(Baral et al. 2007). This type of
activity significantly reduces available nesting and roosting habitat for
Accipitridae vultures (Baral et al. 2005, 2007).
Baral & Heinen (2007)
found in the western area of the Terai that firewood is the main source of
energy. This is common throughout
Nepal particularly in the low income rural areas
(Amacher et al. 1993). Baral &
Heinen (2007) also found that thatch is most commonly used as a roofing
material, while timber is the dominant choice for housing and furniture. Community based conservation measures
have gone some way towards reducing the loss of mature trees and promoting
sustainable management (Jones 2007). The unceasing use and decline of these resources, particularly timber,
will continue to erode the available habitat for Accipitridae species unless
major reforms to industry and community activities occur.
Conservation Programmes
In Nepal there are a range of
current actions and programmes in process for the conservation of vultures (BCN
2009). Many of these programmes
complement each other; however, there are two major limiting features. Within Nepal, human resources are in short
supply and/or financial restraints may limit the potential of some of these
conservation activities (Government of Nepal 2009). Further efforts are required to enhance
conservation outcomes for Accipitridae vultures. There is also a need for continuing and
enhancing concentrated unilateral conservation efforts within the Asian and
Indian subcontinents, which will strengthen the knowledge base and conservation
outcomes.
(i) Vulture Restaurants: The establishment of vulture
restaurants in Nepal is influencing the recovery of vulture population that are on the brink of extinction. These restaurants provide safe
diclofenac-free food sources in close proximity to breeding sites. As a result breeding records have increased
for White-rumped Vultures near vulture restaurants (BCN 2009). The restaurants purchase old and
unproductive cattle from farmers who are happy to sell them (Baral 2010). The cattle are then treated with a safe
drug whenever required and managed at the rescue centre until their natural death. Any diclofenac in their system has
sufficient time to be excreted before death. After death, the carcass is left out for
the vultures to feed on (Aryal 2010; Baral 2010). Vulture restaurants have now been
successfully introduced to Pithouli Village in East Nawalparasi, Gaindahwa
Lake, Lumbini, Rupandehi District, Laimatiya VDC and Bijouri VDC of Dang,
Kailali and Kaski districts (Government of Nepal 2009). Gilbert et al. (2007) found that vulture
restaurants can reduce, but not eliminate, vulture mortality through diclofenac
exposure and thus provide a valuable interim measure in reducing population
declines locally until diclofenac can be totally withdrawn from use. Vulture restaurants also provide a valuable
tool for education by promoting public awareness of the vultures’ plight and
safe use of NSAIDs. This concept
called Vulture Safe Zone (VSZ) comprises of an inner core with a 50km radius
and an outer buffer zone, 50–100 km radius, which has been tested free of
diclofenac and other veterinary drugs toxic to vultures (SAVE 2011). VSZs have now expanded and combined
becoming Diclofenac Free Zones (DFZ) in 16 districts covering an area of 30,344
km2 (BCN 2011).
(ii) Captive Breeding: A vulture conservation
breeding centre has been constructed at Kasara, Chitwan National Park through
the joint efforts of the Nepal Government and NGOs. Their breeding and holding aviaries
house 22 pairs of White-rumped Vultures (BCN 2009). Successful captive breeding
programmes have resulted in positive outcomes for vultures. Sarrazin & Babalt (1996) showed that
immature released vultures had an equal breeding success rate as wild
pairs. During 2010/11, 20
White-rumped Vulture chicks were collected for the captive breeding programme
at Kasara, Chitwan National Park. This brings the total number of the captive population to 60, enhancing
the future captive breeding programme (BCN 2011). Provided human induced threats are
managed successfully, there is a high probability that individuals released
from Nepal’s captive breeding programme will survive and reproduce.
(iii) Community Education: In Nepal, the first
International Vulture Awareness Day was held on 05 September 2009. Awareness programmes were held at 35
different districts attracting 8,200 participants from the general public,
industry and media through to academics. The media coverage was extensive with over 50 articles in print and
electronic media (BCN 2009).
During 2011, 66 awareness
programmes were organised in the DFZ districts with the involvement of 26,000
people. In February, SAVE was
launched in Kathmandu. Key
government authorities, conservation organisations and other stakeholders
attended.
In March 2011 in the Kailali
District, a meeting was held between government and NGO officials on cooperative
trans-boundary conservation between India and Nepal (BCN 2011). Detailed discussion highlighted the need
for cooperative trans-boundary conservation and the establishment of VSZs along
the border of the two countries.
The Department of Livestock
Service now actively undertakes vulture awareness workshops as part of its
annual programme. This programme
promotes and actively generates awareness on the use of meloxicam rather than
diclofenac for livestock treatment to various levels of the government, NGOs,
veterinary communities and drug traders (BCN 2011).
Ongoing public education has
helped generate positive attitudes towards vulture conservation (BCN 2009,
2011). BCN has also been involved
in monitoring and education work promoting the advocacy of using the safe NSAID
meloxicam and removing diclofenac from sale.
(iv) Diclofenac Ban: Following the ban of
manufacturing and import of diclofenac in Nepal in June 2006, efforts have been
made to promote the safe alternative meloxicam (Swan et al. 2006; Cuthbert et
al. 2007; Naidoo et al. 2007; Swarup et al. 2007; Government of Nepal
2009). Cuthbert et al. (2007)
demonstrated that meloxicam was safe to use on six species of Gypsvultures and at least 54 other raptor and scavenging bird species. Meloxicam is widely available throughout
Nepal; however, some of the general population arestill using diclofenac due to lower cost and possibly non-acceptance. Remaining stockpiles of diclofenac were
legally used until stocks were depleted or until the three
year shelf life expired in May 2009. All veterinary diclofenac appearing in
the market from May 2009 has been illegally obtained. Diclofenac is currently a legal
pharmaceutical for human use and has been used on cattle as an alternative to
the veterinary drug. The open
border policy with India allows the uncontrolled importation of diclofenac
(Aryal 2010; Baral 2010).
In 2008, Paudel (2008)
surveyed 12 agro-vet shops in the vicinity of Lumbini and found that 75% had
diclofenac for sale. Currently, regular
up to date monitoring of agro-vets and pharmaceuticals within the DFZs has
demonstrated that there is now no veterinary diclofenac available in these
markets. However, there has been a
small amount of human diclofenac reported. The use of human NSAIDs must be
prohibited in veterinary practice while existing laws need to be strictly
enforced. Government officials are alerted to and continue to work on this
issue (BCN 2011). It is important
to emphasise that ongoing education of the industry, workforce and their end
users on the negative impacts of this drug has resulted in positive outcomes
(BCN 2011).
Future needs
Currently there are two
relevant action plans that cover India and Nepal (Government of India 2006;
Government of Nepal 2009). Both these
plans cover all species mentioned in this document however do not provide in
depth biological and ecological data and species management information that
would enhance recovery prospects for each individual species. There is a need for individual recovery
plans tailored for each of these threatened species. Examples of this format of recovery plan
can be viewed from various government web sites (Australian Government 2012;
New Zealand Government 2012). It
would be beneficial to these species if governments and NGOs within the range
of each species jointly participated in formulating recovery plans. This would facilitate species-specific
outcomes complimenting existing action plans. Individual countries may have greater
impact issues than others, necessitating the need for a unilateral approach.
A holistic approach is
required that provides education for the general public, government and NGOs
through these plans. Utilisation of
as many media avenues as possible would enhance education outcomes. Education should encompass ecosystem
services that vultures provide for the human population while recognising and
providing direction on the impacts that people have on vulture ecology. People need to understand that if
vulture populations decrease, other consumers of carcases such as feral dogs,
jackals and rats will increase. This in turn brings with it human health issues such as rabies. Further research is required to
facilitate the effective education of society particularly on how society will
be affected if vulture populations decline further or disappear from Nepal’s
ecosystems.
Research is also urgently
required to determine the principle threat or cumulative threats causing the
declines of Red-headed Vultures and Egyptian Vultures. Diclofenac may be the principle cause,
as with other Accipitridae vultures, however at this time it is not
conclusively known. If further
research is not conducted on these two species and effective management plans
are not put in place, I fear that Red-headed Vultures and Egyptian Vultures in
particular, and indeed a number of other Accipitridae vultures may well be
faced with extinction in the very near future.
References
Acharya, R., R. Cuthbert, H.S. Baral & K.B. Shah (2009). Rapid population declines of
Himalayan Griffon Gyps himalayensis in Upper Mustang, Nepal. Bird
Conservation International 19(01): 99–107.
Amacher, G.S., W.F. Hyde & B.R. Joshee (1993). Joint production and
consumption in traditional households: Fuelwood and crop residues in two
districts in Nepal. Journal of Development Studies 30(1):
206–225.
Arshad, M., M.J.I. Chaudhary & M. Wink (2009). High
mortality and sex ratio imbalance in a critically declining Oriental
White-backed Vulture population (Gyps bengalensis) in Pakistan. Journal of Ornithology 150: 495–503.
Aryal, M. (2010). Slowly, vulture numbers picking up.<http://ipsnews.net/news.asp?idnews=50067> Downloaded on 14 August 2010.
Australian Government (2012). Threatened
species & ecological communities.<http://www.environment.gov.au/biodiversity/threatened/recovery-list-common.html>
Downloaded on 25 September 2012.
Baral, H.S. (2010: 09 December). [Lecture: Vultures in Nepal].
Baral, H.S., J.B. Giri & M.Z. Virani (2003). On the
decline of Oriental White-backed Vultures Gyps bengalensis in lowland Nepal.Paper presented at the 6th World Conference on Birds of Prey, Berlin.
Baral, N. & R. Gautam (2007). Socio-economic perspectives
on the conservation of Critically Endangered vultures in South Asia: an
empirical study from Nepal. Bird Conservation International 17(02):
131–139.
Baral, N., R. Gautam & B. Tamang (2005). Population
status and breeding ecology of White-rumped Vulture Gyps bengalensis in
Rampur Valley, Nepal. Forktail 21: 87–91.
Baral, N., R. Gautam, N. Timilsina & M.G. Bhat (2007). Conservation implications of
contingent valuation of critically endangered white-rumped vulture Gyps
bengalensis in South Asia. International Journal of
Biodiversity Science & Management 3(3): 145–156.
Baral, N. & J.T. Heinen (2007). Resources use, conservation
attitudes, management intervention and park-people relations in the Western
Terai landscape of Nepal. Environmental Conservation 31(1):
64–72.
BCN (2009). Annual Report (2008/09). Bird Conservation Nepal.
BCN (2011). Annual Report (2010/11). Bird Conservation Nepal.
Benson, P.C., I. Plug & J.C. Dobbs (2004). An analysis of bones and
other materials collected by Cape Vultures at the Kransberg and Blouberg
colonies, Limpopo Province, South Africa. Ostrich 75(3):
118–132.
Bhattarai, K., D. Conway & M. Yousef (2009). Determinants
of deforestation in Nepal’s Central Development Region. Journal of Environmental Management 91(2): 471–488.
BirdLife International (2011). The
BirdLife checklist of the birds of the world, with conservation status and
taxonomic sources. Version 4.
<http://www.birdlife.info/im/species/checklist.zip [.xls zipped 1 MB].> Downloaded on 06 March 2012.
Birdlife International (2012). IUCN Red List for Birds.
<http://www.birdlife.org/> Downloaded on 14 May 2012.
Birdlife International & NatureServe (2011). Bird
species distribution maps of the world (GIS Layers provided by Mark Balman,
Birdlife International) from Birdlife International, Cambridge, UK and
NatureServe, Arlington, USA.
Chaudhary, A., T.R. Subedi, J.B. Giri, H.S. Baral, B. Bidari, H.
Subedi, B. Chaudhary, I. Chaudhary, K. Paudel & R.J. Cuthbert (2012). Population
trends of Critically Endangered Gyps vultures in the lowlands of Nepal. Bird Conservation International 22(03): 270–278.
Cuthbert, R., R.E. Green, S. Ranade, S. Saravanan, D.J. Pain, V.
Prakash & A.A. Cunningham (2006). Rapid population declines of Egyptian Vulture (Neophron
percnopterus) and Red-headed Vulture (Sarcogyps calvus) in India. Animal Conservation 9(3): 349–354.
Cuthbert, R., J. Parry-Jones, R.E. Green & D.J. Pain (2007). NSAIDs and scavenging birds:
Potential impacts beyond Asia’s critically endangered vultures. Biology Letters 3: 91–94.
Das, D., R.J. Cuthbert, R.D. Jakati & V. Prakash (2011). Diclofenac is toxic to the
Himalayan Vulture Gyps himalayensis. Bird Conservation International 21(1):
72–75.
DeCandido, R., T. Subedi & D. Allen (2012). Jatayu: the vulture
restaurants of Nepal. Birding Asia 17: 49–56.
DeCandido, R., T. Subedi & D. Allen (unpub.). Jatayu: The vulture resturants
of Nepal.
DECC (2005). Human-caused climate change - Key
threatening process.
<http://www.threatenedspecies.environment.nsw.gov.au/tsprofile/threat_profile.aspx?id=20025> Downloaded on 12 January 2011.
Dhananjayan, V., S. Muralidharan & P. Jayanthi (2011). Distribution
of persistent organochlorine chemical residues in blood plasma of three species
of vultures from India. Environmental Monitoring
and Assessment 173(1): 803–811.
Dyurgerov, M.B. & M.F. Meier (1997). Year-to-year fluctuations of
global mass balance of small glaciers and their contribution to sea-level changes. Arctic and Alpine Research 29(4):
392–402.
Gangoso, L., P. Álvarez-Lloret, A.A.B. Rodríguez-Navarro, R.
Mateo, F. Hiraldo & J.A. Donázar (2009). Long-term effects of lead
poisoning on bone mineralization in vultures exposed to ammunition sources. Environmental Pollution 157(2): 569–574.
Gautam, A.P., G.P. Shivakoti & E.L. Webb (2004). A review
of forest policies, institutions, and changes in the resource condition in
Nepal. International Forestry Review 6(2):
136–148.
Gilbert, M., M.Z. Virani, R.T. Watson, J.L. Oaks, P.C. Benson,
A.A. Khan, S. Ahmed, J. Chaudhry, M. Arshad, S. Mahmood & Q.A. Shah (2002). Breeding
and mortality of Oriental White-backed Vulture Gyps bengalensis in Punjab
Province, Pakistan. Bird Conservation International 12(4):
311–326.
Gilbert, M., R.T. Watson, S. Ahmed, M. Asim & J.A. Johnson
(2007). Vulture restaurants and their role in reducing diclofenac exposure
in Asian vultures. Bird Conservation International 17(01):
63–77.
Gilbert, M., R.T. Watson, M.Z. Virani, J.L. Oaks, S. Ahmed, M.J.I.
Chaudhry, M. Arshad, S. Mahmood, A. Ali & A.A. Khan (2006). Rapid population declines
and mortality clusters in three Oriental White-backed Vulture Gyps
bengalensis colonies in Pakistan due to diclofenac poisoning. Oryx 40(4): 388–399.
Government of India (2006). Action
Plan for Vulture Conservation in India. Government of
India.
Government of Nepal (2009). Vulture Conservation Action
Plan for Nepal 2009–2013.
Government of Nepal (2010). Country Profile.
<http://www.nepalgov.gov.np/>. Downloaded on 14 August 2010.
Green, R.E., I. Newton, S. Shultz, A.A. Cunningham, M. Gilbert,
D.J. Pain & V. Prakash (2004). Diclofenac poisoning as a cause of vulture population declines
across the Indian subcontinent. Journal of Applied Ecology41: 793–800.
Green, R.E., M.A. Taggart, K.R. Senacha, B. Raghavan, D.J. Pain,
Y. Jhala & R. Cuthbert (2007). Rate of decline of the Oriental White-backed Vulture population
in India estimated from a survey of Diclofenac residues in carcasses of
ungulates. PLoS ONE 2(8): 1–10.
Grimmett, R., C. Inskipp & T. Inskipp (2000). Birds
of Nepal (2nd Edition). Christopher Helm, London.
Houston, D.C. (1978). The effect of food quality on breeding strategy
in Griffon Vultures (Gyps spp). Journal of
Zoology 186(2): 175–184.
Houston, D.C., A. Mee, M. McGrady & I.G. Warkentin (2007). Why do condors and vultures
eat junk?: the implications for conservation. Journal of Raptor Research 41(3): 235–238.
IUCN (2012a). Aegypius monachus.
<http://www.iucnredlist.org/apps/redlist/details/144355/0> Downloaded on
10 October 2012.
IUCN (2012b). Gypaetus barbatus.
<http://www.iucnredlist.org/apps/redlist/details/144346/0> Downloaded on
10 October 2012.
IUCN (2012c). Gyps bengalensis.
<http://www.iucnredlist.org/apps/redlist/details/144350/0> Downloaded on
10 October 2012.
IUCN (2012d). Gyps fulvus.
<http://www.iucnredlist.org/apps/redlist/details/144353/0> Downloaded on
10 October 2012.
IUCN (2012e). Gyps himalayensis.
<http://www.iucnredlist.org/apps/redlist/details/144352/0> Downloaded on
10 October 2012.
IUCN (2012f). Gyps indicus.
<http://www.iucnredlist.org/apps/redlist/details/150691/0> Downloaded on
10 October 2012.
IUCN (2012g). Gyps tenuirostris. <http://www.iucnredlist.org/apps/redlist/details/150673/0>
Downloaded on 10 October 2012.
IUCN (2012h). The IUCN Red List of Threatened Species.Version 2012.2. <http://www.iucnredlist.org> Downloaded on 10 October
2012.
IUCN (2012i). Neophron percnopterus. <http://www.iucnredlist.org/apps/redlist/details/144347/0>
Downloaded on 10 October 2012.
IUCN (2012j). Sarcogyps calvus.
<http://www.iucnredlist.org/apps/redlist/details/144358/0> Downloaded on
10 October 2012.
Jackson, A.L., G.D. Ruxton & D.C. Houston (2008). The effect of social
facilitation on foraging success in vultures: a modelling study. Biology Letters 4: 311–313.
Jones, S. (2007). Tigers, trees and Tharu: An analysis of community forestry in the
buffer zone of the Royal Chitwan National Park, Nepal. Geoforum38: 558–575.
Joughin, I.W., W. Abdalati & M. Fahnestock (2004). Large
fluctuations in speed on Greenland’s Jakobshavn Isbrae Glacier. Nature 435: 608–610.
Klein, P.N., K. Charmatz & J. Langenberg (1994). The effect of flunixin
meglumine (Banamine) on renal function in northern bobwhite (Colinus
virgineansul): an avian model. Proceedings of American
Association of Zoo Vetinarians, 128–131pp.
Lemus, J.Á., G. Blanco, B. Arroyo, F. Martínez & J. Grande
(2009).Fatal embryo chondral damage associated with fluoroquinolones in eggs of
threatened avian scavengers. Environmental Pollution 157(8–9):
2421–2427.
Li, Y.D. & C. Kasorndorkbua (2008). The status
of the Himalayan Griffon Gyps himalayensis in South-East Asia. Forktail 24: 57–62.
Margalida, A., J. Bertran & R. Heredia (2009). Diet and food preferences of
the endangered Bearded Vulture Gypaetus barbatus: a basis for their
conservation Ibis 151: 235–243.
Margalida, A., D. García & Cortés-Avizanda (2007). Factors influencing the
breeding density of Bearded Vultures, Egyptian Vultures and Eurasian Griffon
Vultures in Catalonia (NE Spain): Management implications. Animal
Biodiversity and Conservation 30(2): 189–200.
Mateo, R., R. Cadenas, M. Manez & R. Guitart (2001). Lead Shot
Ingestion in Two Raptor Species from Donana, Spain. Ecotoxicology
and Environmental Safety 48: 6–10.
Mateo, R., J. Estrada, J. Paquet, X. Riera, L. Dominuez, R.
Guitart & A. Martinez-Vilalta (1999). Lead shot ingestion by Marsh Harriers Circus
aeruginosus from the Ebro delta, Spain. Environmental
Pollution 104: 435–440.
Mathew, G. (1987). Insect borers of commercially imported stored timber in the state
of Kerala, India. Journal of Stored Products Research 34(4):
185–190.
Meteyer, C.U., B.A. Rideout, M. Gilbert, H.L. Shivaprasad &
J.L. Oaks (2005). Pathology and proposed pathophysiology of
diclofenac poisoning in free-living and experimentally exposed oriental
White-backed Vultures (Gyps bengalensis). Journal
of Wildlife Diseases 41(4): 707–716.
Milner-Gulland, E.J., M.V. Kholodova, A. Bekenov, O.M. Bukreeva,
I.A. Grachev, L. Amgalan & A.A. Lushchekina (2001). Dramatic declines in Saiga
Antelope populations. Oryx 35(4): 340–345.
Morán-lópez, R., J.M.S. Guzmán, E.C. Borrego & A.V. Sánchez
(2006).Nest-site selection of endangered Cinereous Vulture (Aegypius monachus)
populations affected by anthropogenic disturbance: Present and future
conservation implications. Animal Conservation 9(1): 29–37.
Morán-lópez, R., J.M. Sánchez, E. Costillo, C. Corbacho & A.
Villegas (2006). Spatial variation in anthropic and natural
factors regulating the breeding success of the Cinereous Vulture (Aegypius
monachus) in the SW Iberian Peninsula. Biological
Conservation 130(2): 169–182.
Muralidharan, S., V. Dhananjayan, R. Risebrough, V. Prakash, R.
Jayakumar & P. Bloom (2008). Persistent organochlorine pesticide residues in
tissues and eggs of White-backed Vulture, Gyps bengalensis from
different locations in India. Bulletin of
Environmental Contamination & Toxicology 81(6): 561–565.
Naidoo, V. & G.E. Swan (2009). Diclofenac toxicity in Gyps
vulture is associated with decreased uric acid excretion and not renal portal
vasoconstriction. Comparative Biochemistry and Physiology Part C: Toxicology
& Pharmacology 149(3): 269–274.
Naidoo, V., K. Wolter, A.D. Cromarty, P. Bartels, L. Bekker, L.
Mcgaw, M.A. Taggart, R. Cuthbert & G.E. Swan (2007). The
pharmacokinetics of meloxicam in vultures. Journal
of Veterinary Pharmacology and Therapeutics 31: 128–134.
New Zealand Government (2012). Threatened Species Recovery
Plan archive.
<http://www.doc.govt.nz/publications/science-and-technical/products/series/threatened-species-recovery-plans/archive/>
Downloaded on 25 September 2012.
Oaks, J.L., M. Gilbert, M.Z. Virani, R.T. Watson, C.U. Meteyer,
B.A. Rideout, H.L. Shivaprasad, S. Ahmed, M.J.I. Chaudhry, M. Arshad, S.
Mahmood, A. Ali & A.A. Khan (2004). Diclofenac residues as the
cause of vulture population decline in Pakistan. Nature427: 630–633.
Oerlemans, J. & J.P.F. Fortuin (1992). Sensitivity
of glaciers and small ice caps to greenhouse warming. Science258: 115–117.
Olea, P.P. & P. Mateo-Tomás (2009). The role of traditional
farming practices in ecosystem conservation: The case of transhumance and
vultures. Biological Conservation 142(8): 1844–1853.
Pain, D.J., C.G.R. Bowden, A.A. Cunningham, R. Cuthbert, D. Das,
M. Gilbert, R.D. Jakati, Y. Jhala, A.A. Khan, V. Naidoo, J.L. Oaks, J.
Parry-Jones, V. Prakash, A. Rahmani, S.P. Ranade, H.S. Baral, K.R. Senacha, S.
Saravanan, N. Shah, G. Swan, D. Swarup, M.A. Taggart, R.T. Watson, M.Z. Virani,
K. Wolter & R.E. Green (2008). The race to prevent the extinction of South
Asian vultures. Bird Conservation International 18(SupplementS1):
S30–S48.
Pain, D.J., A.A. Cunningham,
P.F. Donald, J.W. Duckworth, D.C. Houston, T. Katzner, J. Parry-Jones, C.
Poole, V. Prakash, P. Rouns & R. Trimmins (2003). Causes and
effects of temporaspatial declines of Gyps vultures in Asia. Conservation Biology 17(3): 661–671.
Paudel, S. (2008). Vanishing vultures and diclofenac prevalence in
Lumbini IBA. Danphe 17(2): 1–3.
Prakash, R.N.C., Y. Anjaneyulu, B. Sivasankari & R.K. Ananda
(2006).Comparative toxicity studies in birds using nimesulide and diclofenac sodium. Environmental
Toxicology and Pharmacology 22.
Prakash, V., R.E. Green, D.J. Pain, S.P. Ranade, S. Saravanan, N.
Prakash, R. Venkitachalam, R. Cuthbert, A.R. Rahmani & A.A. Cunningham
(2007). Recent changes in populations of resident Gyps vultures in
India. Journal of the Bombay Natural History
Society 104(2): 129–135.
Prakash, V., D.J. Pain, A.A. Cunningham, P.F. Donald, N. Prakash,
A. Verma, R. Gargi, S. Sivakumar & A.R. Rahmani (2003). Catastrophic
collapse of Indian white-backed Gyps bengalensis and Long-billed Gyps
indicus vulture populations. Biological
Conservation 109(3): 381–390.
Provini, A. & S. Galassi (1999). Polychlorinated
biphenyls and chlorinated pesticides in bird eggs from Calabria (southern
Italy). Ecotoxicology and Environmental Safety 43:
91–97.
Rahmani, A.R. (2004). Report of the international South Asian Vulture
Recovery Plan Workshop. Buceros 9(1):
1–48.
RAOnline (2010a). Nepal’s Climate.<http://www.raonline.ch/pages/npinfoe_cli.html> Downloaded on 14
September 2010.
RAOnline (2010b). Nepal’s Geology.<http://www.raonline.ch/pages/np/nat/np_geology02.html> Downloaded on 14
August 2010.
RAOnline (2010c). Nepal’s Topography.<http://www.raonline.ch/pages/np/nat/np_geology02a1.html> Downloaded on
01 October 2010.
Sarrazin, F. & R. Barbault (1996). Reintroduction: challenges
and lessons for basic ecology. Trends in Ecology and
Evolution 11(11): 474–478.
Satheeson, S.M. (1999). The decline of vultures in India. Vulture News 40: 35–36.
Savada, A.M. (1991). Nepal: A country study.
<<http://countrystudies.us/nepal/>> Downloaded on 14 September
2010.
SAVE (2011). Vulture Conservation Areas and Vulture Safe
Zones.<http://www.save-vultures.org/Documents/11_08_Vulture_Safe_Zone_definition_Final.pdf>
Downloaded on 25 September 2012.
Sekercioglu, C.H. (2006). Increasing awareness of avian ecological function. Trends in Ecology and Evolution 21(8): 464–471.
Sharma, P. (2012). Aceclofenac as a potential threat to Critically
Endangered vultures in India - a review. Journal of
Raptor Research 46(3): 314–318.
Shrestha, A.B., C.B. Wake, P.A. Mayewski & J.E. Dibb (1999). Maximum temperature trends
in the Himalaya and its vicinity: An analysis based on temperature records from
Nepal for the period 1971–94. Journal of Climate 12(9):
2775–2786.
Shultz,
S., H.S. Baral, S. Charman, A.A. Cunningham, D. Das, G.R. Ghalsasi, M.S.
Goudar, R.E. Green, A. Jones, P. Nighot, D.J. Pain & V. Prakash (2004). Diclofenac poisoning is
widespread in declining vulture populations across the Indian subcontinent. Proceedings of the Royal Society B-Biological Sciences, 271,
S458-S460. Retrieved from
http://rspb.royalsocietypublishing.org/content/271/Suppl_6/S458 doi:10.1098/rsbl.2004.0223
Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt,
M. Tignor & H.L. Miller (eds.) (2007). Contribution of Working Group I to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change, 2007.Cambridge University Press, Cambridge.
Subedi, T. & R. DeCandido (Unpublished). Indian Vulture (Gyps
indicus): A new species for Nepal.
Swan, G., V. Naidoo, R. Cuthbert, R.E. Green, D.J. Pain, D.
Swarup, V. Prakash, M. Taggart, L. Bekker, D. Das, J.r. Diekmann, M. Diekmann,
E. Killian, A. Meharg, R.C. Patra, M. Saini & K. Wolter (2006). Removing the threat of
diclofenac to Critically Endangered Asian Vultures. PLoS
Biology 4(3): 395–402.
Swan, G.E., R. Cuthbert, M. Quevedo, R.E. Green, D.J. Pain, P.
Bartels, A.A. Cunningham, N. Duncan, A.A. Meharg, J.L. Oaks, J. Parry-Jones, S.
Shultz, M.A. Taggart, G. Verdoorn & K. Wolter (2006). Toxicity
of diclofenac to Gyps vultures. Biology Letters2: 279–282.
Swarup, D., R.C. Patra, V. Prakash, R. Cuthbert, D. Das, P. Avari,
D.J. Pain, R.E. Green, A.K. Sharma, M. Saini & M. Taggart (2007). Safety of meloxicam to
critically endangered Gyps vultures and other scavenging birds in India.Animal Conservation 10(2): 192–198.
Taggart, M.A., K.R. Senacha, R.E. Green, R. Cuthbert, Y.V. Jhala,
A.A. Meharg, R. Mateo & D.J. Pain (2009). Analysis of nine NSAIDS in ungulate tissues
available to critically endangered vultures in India. Environmental
Science & Technology 43(12): 4561–4566.
Taggart, M.A., L. Venter, R. Cuthbert, V. Naidoo, K. Wolter, D.
Cromarty, M. Diekmann, N. Duncan & A.A. Meharg (2010). Toxicity of non-steroidal
anti-inflammatory drugs to Gyps vultures: a new threat from ketoprofen. Biology Letters 6: 339–341.
van Drooge, B., R. Mateo, Í. Vives, I. Cardiel & R. Guitart
(2008).Organochlorine residue levels in livers of birds of prey from Spain: Inter-species
comparison in relation with diet and migratory patterns. Environmental
Pollution 153(1): 84–91.
Vetaas, O.R. & J. Grytnes (2002). Distribution
of vascular plants species richness and endemic richness along the Himalayan
elevation gradient in Nepal. Global Ecology and
Biogeography 11: 291–301.
Virani, M.Z., J.B. Giri, R.T. Watson & H.S. Baral (2008). Surveys of
Himalayan Vultures (Gyps himalayensis) in the Annapurna Conservation
Area, Mustang, Nepal. Journal of Raptor Research 42(3):
197–203.
Zuberogoitia, I., J. Zabala, J.A. Martínez, J.E. Martínez & A.
Azkona (2008). Effect of human activities on Egyptian vulture breeding
success. Animal Conservation 11(4):
313–320.