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Vulture News 68
July 2015
VULTURE NEWS
The Journal of the IUCN Vulture Specialist Group
No. 68 July 2015
CONTENTS
ARTICLES
Status and threats to vultures in China
3
Roller MaMing and Guohua Xu
Blood lead levels in White-Backed Vultures (Gyps africanus) from
Botswana.
25
David Kenny, Richard Reading, Glyn Maude, Peter Hancock
and Beckie Garbett
A preliminary assessment of the palate and tongue for detecting
organophosphorus and carbamate pesticide exposure in the degraded
carcasses of vultures and other animals
Ngaio L. Richards, Irene Zorrilla, Isabel Fernandez, Mónica Calvino,
Joaquin Garcia and Antonio Ruiz
1
32
Vulture News 68
July 2015
SHORT COMMUNICATIONS, NOTES AND REPORTS
New record of African White-backed Vulture (Gyps africanus)
in Europe
52
A. Godino and C. Machado
Attempted Verreaux’s Eagle predation on Rüppell’s Vulture and
breeding observations at Lake Kwenia colony, Kenya.
59
Simon Thomsett and James Aldrich.
IUCN Species Survival Commission: Vulture Specialist Group
Summary updates April 2015 for vultures and VSG activities
RECENT LITERATURE
64
66
69
Peter Mundy
Printed by Jetline Modderfontein, Johannesburg
Published by the Birds of Prey Programme, Endangered Wildlife Trust
Editor: Campbell Murn
Associate Editors: Peter Mundy and Darcy Ogada
Front cover: Adult Himalayan Griffon (Gyps himalayensis) photographed in
Xinjiang, China (R. MaMing)
Back cover: Immature African White-backed Vulture (Gyps africanus)
photographed with a digi-scope in Portugal (A. Godino)
2
Vulture News 68
July 2015
ARTICLES
Status and threats to vultures in China
Roller MaMing* and Guohua Xu
Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, No. 818
Beijing Road, Urumqi, 830011, Xinjiang, P. R. of China.
*Corresponding author: [email protected]
http://dx.doi.org/10.4314/vulnew.v68i1.1
concerns about their lesser-known
Introduction
relatives and the survival of vultures
Populations of three old world
has cultural as well as ecological
vulture species, Gyps bengalensis,
implications.
Gyps tenuirostris and Gyps indicus
studies on these three species, little is
collapsed
Indian
known about population trends in
Subcontinent (Prakash et al. 2012).
highland areas, particularly in China,
These
where there have been few studies of
across
population
the
declines
were
the
anti-inflammatory drug, diclofenac,
Currently, there is little information
that
available
visceral
gout
carrion-eating
extensive
attributed to the use of a nonsteroidal
causes
large
Despite
regarding
the
raptors.
use
of
subsequently leading to renal failure
veterinary diclofenac for livestock in
in vultures that consume carcasses
western China, and little is known
contaminated with the drug (Green et
about populations and dynamics of
al. 2004, Oaks et al. 2004, Naidoo et
vultures in China overall (Pain et al.
al. 2009). This situation raised
2003, Lu et al. 2009, Ma et al.
3
Vulture News 68
2013). Therefore, in this paper we
July 2015
(Di 2003), because there are more
want
background
than seven Old World Vulture
information regarding vultures and
species distributed there (Ma et al.
their protection status in China.
2014). At the same time, nearly 28
to
introduce
Vultures
include
16
living
million people live on the Tibetan
species that occur on the Old World.
Plateau.
However, in China there are more
predominantly on livestock carcasses
vultures species than most other
as food resources and this highlights
countries (eight species), accounting
their ecological importance in the
for 50% of vulture species in the Old
highland
World. They are Bearded Vulture
human corpses also provide a small
(Gypaetus barbatus), White-rumped
fraction of the total food resource to
Vulture
vultures, so the vultures play a
(Gyps
bengalensis),
Himalayan
Griffon
himalayensis),
Eurasian
Some
vultures
ecosystem.
depend
Meanwhile,
(Gyps
unique role in the centuries-old sky
Griffon
burial tradition followed by Tibetan
(Gyps fulvus), Cinereous Vulture
people. In short, vultures have not
(Aegypius monachus), Red-headed
only ecological but also cultural
Vulture (Sarcogyps calvus), Slender-
value. Therefore, extra attention
billed Vulture (Gyps tenuirostris)
should
and Egyptian Vulture (Neophron
conservation of these scavenging
percnopterus) respectively (Zhang &
species.
be
directed
at
the
Yang 1980, Gu et al. 1994, Zheng
2011, Guo and Ma 2012). The
Distribution and Population of
species
Vultures in China
have
an
extensive
geographical distribution, centred on
the northwest, the Tibetan plateau,
The vultures of China have received
Pamir plateau and the southwest
great attention from the government.
minority areas in China. Meanwhile,
The dramatic population crashes of
the
three species of Gyps vulture in the
Tibetan
plateau
has
been
regarded as the kingdom of vultures
south Asia was a good example and
4
Vulture News 68
urged China to take some measures
July 2015
by the court according to the wild
to protect these species. In 1988, the
animal conservation law. On May
Law of the People’s Republic of
20, 2013, Lei was arrested for
China on the Protection of Wildlife
mailing a Cinereous Vulture skeleton
established
illegally, and was sentenced by the
two
categories
of
nationally protected wild animals,
court.
and most species in these two
Despite protection efforts such as
categories are rare and threatened. In
these, most vulture populations are
2001,
still in a downward trend over recent
the
Administration
State
Forestry
an
years. Table 1 presents data on eight
additional list of nationally protected
vulture species in China and the
species that are either beneficial or
world, summarised from government
with
websites,
important
announced
economic
or
the
State
Forestry
scientific value. This list covered an
Administration,
additional 707 species of birds,
International and the IUCN Red List
BirdLife
including many that are common and
of Threatened Species.
widespread in China. In addition to
Based on recent investigations
the nationally protected species,
(Ma 2011), only three vultures are
many provinces have published lists
common
of locally protected wildlife.
himalayensis, Gypaetus barbatus,
Under these laws, there is some
and
in
Aegypius
China:
monachus.
Gyps
The
effective protection for the listed
numbers of other vulture species,
wildlife. For example, in August
such
2002, the defendants Li Yuesheng,
Slender-billed Vulture, are small and
Li Congrong and Li Ziqi caught 26
mostly only recorded one to three
Himalayan Griffons in a nature
times in the past 50 years. According
reserve of Yunnan Province, and all
to data released by the State Forestry
the vultures died in the end, so they
Administration
were sentenced to 10 years, 12 years
population size of the Bearded
and 13 years respectively and fined
as
Egyptian
in
Vulture
2009,
and
the
Vulture was estimated at 92,000
5
Vulture News 68
individuals in China (e.g. 22,018 in
on
Xinjiang, 32,500 in Qinghai, 29,126
distribution
in Gansu, 7,500 in Xizang [Tibet],
BirdLife (2014) and the IUCN Red
800 in Sichuan, 54 in other parts of
List, we estimated the number of the
China) (National Forestry Bureau
eight
2009). However, this species breeds
according to their distribution and
at low densities in other parts of its
population size in the world (Table
range and in some other countries
1).
there are only 200-300 pairs in total.
distributed in China are mainly in the
Furthermore, the global population
western regions of the country (Xu
of the Bearded Vulture is estimated
1995, Ma 2011, Zheng 2011). Figure
to be less than 10,000 individuals.
1 shows the distribution of these
Therefore, there is some doubt over
species and highlights that most
the accuracy of data provided by the
species are centered on the Tibetan
Chinese Forestry Bureau about the
Plateau. Ranges also extend into the
population size of the Bearded
southwest,
Vulture; as a result, we re-calculated
Mongolia (Kenny et al. 2008) and
the population estimate again. Based
the Himalaya.
6
population
The
data
area
vulture
July 2015
and the
described
species
eight
in
vulture
northwest,
by
China
species
Inner
Vulture News 68
July 2015
Table 1: Summary of status, numbers, distribution of Old World Vultures and key threats to vultures in China
Species
Distribution
(summary)
Bearded Vulture
(Gypaetus barbatus)
Bhutan, China, India, Mongolia, Pakistan,
Russia, Central Asia, Middle East, Europe,
North East and East Africa
Bangladesh, Bhutan, China, India, Myanmar,
Pakistan, South-East Asia
White-rumped Vulture
(Gyps bengalensis)
Himalayan Griffon
(Gyps himalayensis)
Eurasian Griffon
(Gyps fulvus)
Cinereous Vulture
(Aegypius monachus)
Red-headed Vulture
(Sarcogyps calvus)
Bhutan, China, India, Pakistan, South-East
Asia, Central Asia
Central Asia, Europe, North Africa, Turkey,
China
Bhutan, China, India, Myanmar, Pakistan,
Mongolia, East Asia, Central Asia, Middle
East, Europe
Bangladesh, Bhutan, Cambodia, China, India,
Laos, Malaysia, Myanmar, Pakistan, Thailand,
Vietnam
Bangladesh, India, Myanmar, South-East Asia
Global
population
(individuals)
2,000-10,000
Global
distribution
(km2)
8,840,000
Current
trend
Red List
Status*
Decreasing
LC
3,500-15,000
4,920,000
Decreasing
CR
100,000499,999
40,000-50,000
3,100,000
Stable
LC
10,200,000
Increasing
LC
21,000-30,000
13,700,000
Decreasing
NT
3,500-15,000
3,690,000
Decreasing
CR
Slender-billed Vulture
1,500-3,750
847,000
Decreasing
NT
(Gyps tenuirostris)
Egyptian Vulture
India, Pakistan, China, Central Asia, Africa,
20,000-61,000
18,700,000
Decreasing
EN
(Neophron
Europe (more southerly countries), Middle East
percnopterus)
* Critically Endangered (CR), Endangered (EN), Near Threatened (NT), and Least Concern (LC). Global population estimates from
BirdLife (2014) and IUCN Red List (2013). Population size in China estimates were based on the world population and distribution area.
7
Vulture News 68
July 2015
Table 1: continued.
Species
Bearded
Vulture
List in
China
Ⅰ
Distribution in China
Est. China
population
Shanxi, Inner Mongolia, Tibet,
Xinjiang, Qinghai, Ningxia, NW
Yunnan, Western Sichuan, Hubei,
Hebei, Shaanxi
The western and SW of Yunnan
100-200
6,9009,900
White-rumped
Vulture
Himalayan
Griffon
Ⅰ
Ⅱ
Xinjiang, Gansu, Qinghai, Tibet,
Ningxia, Sichuan, Western Yunnan
90,000230,000
Eurasian
Griffon
Cinereous
Vulture
Ⅱ
Western Xinjiang, SE Tibet
100-300
Ⅱ
Xinjiang, Qinghai, Gansu, Ningxia,
Mongolia, Shanxi, Sichuan.
Tibet, SE China, Taiwan
9,00015,000
Red-headed
Vulture
Ⅱ
SW Yunnan, SE Tibet
100-300
Slender-billed
Vulture
Ⅱ
SE Tibet
20-100
Western Xinjiang
20-100
Egyptian
Vulture
Ⅱ
8
Chief threats
Research needs
Poisoning, persecution,
habitat loss, disturbance,
power lines, windfarms,
lack of safe food
NSAID poisoning, lack of
safe food
NSAID poisoning, lack of
safe food
Monitoring population, food
habits, breeding ecology
Persecution, poisoning, lack
of safe food, power lines
Disturbance, lack of safe
food, poisoning, secondary
poisoning (NSAIDs)
Persecution, secondary
poisoning, lack of safe food,
intensification of agriculture
NSAID poisoning, lack of
safe food
Disturbance, poisoning,
electrocution, food
availability
NSAIDs, monitoring
population, breeding
NSAIDs, monitoring
population, food habits,
breeding
Monitoring population, food
habits, breeding
NSAIDs, monitoring
population, food habits,
breeding
NSAIDs, monitoring
population, food habits,
breeding
NSAIDs, monitoring
population, food habits,
breeding
Monitoring population, food
habits, breeding
Vulture News 68
July 2015
Figure 1: Distribution maps of the eight vulture species in China
Bearded Vulture
(Gypaetus barbatus)
White-rumped Vulture
(Gyps bengalensis)
Himalayan Griffon
(Gyps himalayensis)
Eurasian Griffon
(Gyps fulvus)
Cinereous Vulture
(Aegypius monachus)
Red-headed Vulture
(Sarcogyps calvus)
9
Vulture News 68
July 2015
Slender-billed Vulture
(Gyps tenuirostris)
Egyptian Vulture
(Neophron percnopterus)
Figure 1: Distribution maps of the eight vulture species in China
usually
geographically
remote,
which adds to time, labour and
logistical costs; many areas are
inaccessible. Finally, there is limited
funding for vulture research in
addition to current government
priorities being directed in other
areas.
Vultures in China are sustained
mainly by feeding on livestock
carcasses in the region. As obligate
scavengers they occupy an important
ecological niche by contributing to
carcass removal and nutrient
recycling.
A
particular
role
performed by vultures relates to the
centuries-old sky burial tradition,
which is followed by nearly five
million Tibetan people (Figure 2).
Domestic Research Status
In China there have been few studies
on large carrion-eating raptors (Ye
1991), especially in relation to
reproductive biology and population
ecology. Published reports are few
and deficient in detail and the
research literature is limited. In
conclusion, little is known about the
breeding biology, habitat preferences
or behaviour and ecology of China’s
vultures, for a number of reasons.
Firstly,
harsh
environmental
conditions and in particular high
altitude, cold climate settings is a
significant obstacle to research work.
Secondly, the relevant areas are
10
Vulture News 68
July 2015
Sky burial is how Tibetan culture
treats its dead. At sky burial sites,
human bodies are typically cut up,
with bones broken into fragments by
burial priests, and these are
consumed entirely by griffons and
other scavengers. A total of 1,200
sky burial sites are distributed over
the Tibetan plateau. Local Buddhist
people believe that the vultures take
the soul of the dead person to
heaven. Because of this, local people
value and protect vultures.
Figure 2: Sky burial and Himalayan Griffon in Tibet
Potential Threats to Vultures in
China
Today, vultures face many survival
problems in China. Poisoning, wind
power stations, poaching, capture,
specimen
trade,
highway
construction and the use of vulture
parts for cultural purposes are all
threats. In particular, due to
development in the western regions
of the country, vultures in China face
a series of threats. Here we describe
some of these threats in greater
detail.
11
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July 2015
deliberately poisoned carcasses, and
vultures become the unintended
victims (Figure 3). In such cases, one
poisoned carcass can kill a large
number of vultures. At one sky
burial site, we were told by local
people that about 100 vultures were
found dead after feeding on a human
carcass (Jin and Yu 2004). This
matter caused quite a shock among
the local community, and as a result,
sky burials were not permitted for
people who died of toxicosis or
infectious diseases, in an attempt to
prevent poisoning of vultures.
1. Poisoning.
Traditional agricultural practices that
use limited pesticides are practiced
throughout the plateau areas of
China. However, in the northeast in
western Sichuan, Northern Qinghai,
and Southern Gansu, pesticides are
commonly used for controlling pika
(Ochotona spp.), which could cause
secondary poisoning of vultures
(Hernández and Margalida 2008).
Some farmers, aiming to control
other scavengers and predators such
as wolves and wild dogs, lay out
Figure 3: A poisoned Bearded Vulture
The population collapse of three
species of Gyps vultures (Oriental
White-backed
Vulture
Gyps
bengalensis, Long-billed Vulture
Gyps indicus and Slender-billed
Vulture Gyps tenuirostris) due to the
use of veterinary diclofenac in South
Asia (Oaks et al. 2004, Pain et al.
2003) led to these species being
reclassified as Critically Endangered
and diclofenac being banned in the
region. However, the surviving
vultures remain under threat due to
residual diclofenac use (Das et al.
2011) as well as other veterinary
drugs. Currently, it is unknown if
diclofenac is affecting populations of
vultures and other scavenging birds
12
Vulture News 68
July 2015
in China, but given the ubiquitous
nature of the drug prior to the ban,
there is a likely risk. Vultures in
China have a geographic distribution
that overlaps with that of the three
Gyps species in south Asia, and they
share similar foraging behaviors. We
consider that the vultures in China
are highly likely to be subject to
diclofenac poisoning, and this
situation
requires
urgent
investigation.
been established. The largest wind
farm in China is located in Xinjiang
(Figure 4). This brings negative
effects to the survival of raptors. For
example, the design of the grid
structure is often unsafe and
electrical wiring is often bare, which
lacks any measure of protection for
birds. According to investigations,
about 20% raptors are under the
threat of electrocution in the west,
the number of dead raptors as high as
1.36 per kilometre (Mei & Ma 2008).
We were surprised to find up to five
dead raptors under some electricity
poles. These mortalities not only
affect the survival of local raptor
populations, but also the safe
operation of the transmission lines
(Mei & Ma 2008).
2. The threat of the power grid.
At present, the northwest power grid
and Tibet power grid are spreading
into the western areas of China.
Additionally, based on the abundant
wind resources in western China, a
large number of wind farms have
Figure 4: The wind power station in west China
feathers also have a high value, so
some people kill vultures to make
ornaments, which are a deformed
fashion decoration, or trap the
vultures for their plumage. Today,
3. Specimen making and trading.
People have found that vultures have
a special form and a high ornamental
value since the 1990s. Vulture
13
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July 2015
more and more people are addicted
to these fetishes. Specimen trading
for a wide range of uses including
herbariums,
museums,
schools,
research, individual collectors and
the market for animal parts means
that prices for vulture parts remain
very high. For example, a good
vulture specimen can be worth as
much as 12,000 Yuan [~$2,000 US]
or more, and this high value
contributes to demand. In addition,
the Tibetan and Tajik people make
flutes with vulture bones to play
music (Figure 5), which is part of
their traditional culture (MaMing et
al. 2014). Flutes made from vulture
wing bones are very expensive;
prices in Xinjiang can exceed 10,000
Yuan
[~$1,700
US],
which
undoubtedly stimulates harvesting of
vultures from the wild.
Figure 5: The specimen and vulture bone flute in China
of meat has increased sharply, many
animals that died naturally have been
collected by local people (Tashi and
Zhou 2009). Some Han people with
no religious beliefs process these
dead bodies into dry spicy meat
(such as sausage, bacon, dumplings,
jerky, dried meat, etc.) for sale
illegally. Both activities reduce food
for vultures.
4. Food Shortage.
Farm management has gradually
improved in the west of China; death
rates in grazing cattle have greatly
decreased due to improved disease
control and prevention, reducing
food for vultures. Local Islamic
people do not eat animals that have
died naturally, and in the past this
helped vultures, but since the price
14
Vulture News 68
The human population has expanded
very rapidly in the last decade and
with it there has been a sharp
increase in outdoor tourist activities
that can lead to disturbance of
breeding vultures. There are other
reasons for reduced food supply for
vultures. For example, in some areas
deceased humans are buried or
cremated instead of going to sky
burial, whilst declining populations
of Wolves (Canis lupus), Dholes
(Cuon alpinus) and Snow Leopards
(Uncia uncia) have also affected the
food supply of vultures (Ma et al.
2014) in the form of reduced carrion
from predator kills (Figure 6).
July 2015
Between August–October 2012
and March–October 2013, we spent
more than 90 days in the field in
central Tien Shan, and we found
some chicks still in the nest in
September and October. This is a
very unusual phenomenon. We
speculate that the food shortages is a
reason why they are still in the nest
(Ma et al. 2013, Liu et al. 2013,
Clements et al. 2013). At the same
time, in the western region, we found
some vultures breeding earlier than
normal, which may be a strategy
response to climate change, different
land-use practices and food changes
(Houston 1990, Murn and Anderson
2008).
Figure 6: Himalayan Griffons eating a dead yak
15
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July 2015
5. Demand by zoos.
fate of these birds is unknown, but it
is clear they were captured from the
wild as there is no breeding of this
species in zoos. Further, due to
inadequate management, it is likely
that these birds will be dead before
too long, thus requiring that more
wild birds are captured. As a result,
capturing vultures from the wild is
unlikely to end, which will continue
to have a detrimental impact on wild
populations.
In order to attract tourists and make
money, some local zoos and other
venues capture wild vultures for
public display. Visitors pay money to
take pictures and pose with the birds
(Figure 7). At a zoo in Ningbo, it
was observed that in order to
celebrate the construction of a new
enclosure, nine Himalayan Griffons
(Figure 8) were put on display. The
Figure 7: These Cinereous Vultures were caught for sport or entertainment
16
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July 2015
Figure 8: Himalayan Griffons and Cinereous Vultures in Ningbo Zoo
6. Medicinal value.
caught and sold for medicinal
components (Fauna of Medicinal
Animal in China 1979, Li 1981,
Leung 2006). Some Chinese herbal
medicine shops sell desiccated
vulture parts — heads, talons,
feathers, eyes, beaks and hearts —
for traditional medicine or fetishes
(Figure 9). In some areas, we were
surprised to find vulture meat was
traded (Koenig 2006). These uses
stimulate people to kill more
vultures.
The theory of traditional Chinese
medicine considers that vultures,
along with other birds of prey, have
many important medical functions,
especially some unique curative
effects. For example, feather, bone,
meat, beak, claw, faeces and internal
organs such as craw, gizzard or
stomach have all been used for
traditional medicine since ancient
times (Li 1981, Luo 2003, Leung
2006). This leads to vultures being
17
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July 2015
Figure 9: The bones from a Cinereous Vulture for sale in a shop
7. Illegal hunting.
head and leg we removed two
fragment of the shots by emergency
operation (Figure 10). Illegal hunting
is also used to obtain birds for sale
(Figure 11) and to take live samples
for medicinal purposes. The value of
such commodities is high and there
is a ready market for them. These
factors encourage criminals to take
risks to capture raptors for sale.
Illegal hunting in the western region
and central mountains in China is
very widespread. According to a
report, at noon on May 25, 2003, a
Cinereous Vulture was illegally shot
by a hunter in the Yibin County. The
head and foot was badly hurt, and the
bird was taken to a local zoo in a
critical condition. From the vulture
18
Vulture News 68
July 2015
Figure 10: Rescued injured Cinereous Vulture
Figure 11: Cinereous Vulture for sale in Yibin
19
Vulture News 68
July 2015
only play a significant role in
maintaining ecosystem function, they
are highly respected in Buddhist
culture and have a significant role in
terms of cultural unity and social
stability.
The threats to vultures across the
world are numerous (Ledger and
Annegarn 1981, Cunningham 1990,
Camiña and Montelío 2006, McKie
2007, Naidoo et al. 2009, Ogada
2014, Saidu & Buij, 2013, Williams
et al. 2014) and similar threats are
likely to be occurring in China, but
have not been evaluated fully. We
recommend that a detailed evaluation
of these threats takes place, and in
particular quantifying their impact on
vulture populations in China.
Discussion
In recent years, the western regions
of China have seen development in
the form of mining operations, roads
and a growing human population.
This
has
damaged
local
environments, including the habitat
of raptors, and has been a great threat
to vulture populations.
At present, there have been few
studies of the large carrion-eating
raptors in China (Ye 1991) and
published reports are few and limited
in detail. Many statistics about
vultures released by the relevant
departments in China are inaccurate,
so there is a lack of baseline
knowledge about vultures, which
hinders
the
formulation
of
appropriate laws and essential
conservation
measures.
These
species are still poorly understood in
China, but they are facing a
dangerous situation. If vultures
continue to decline, the ecological
and economic implications are hard
to determine at present, but
ecological systems will undoubtedly
be affected negatively. Additionally,
the loss of vultures has serious
cultural and religious implications
(Satheesan 1998), and potentially for
other wildlife and for human health.
Further research is urgently required.
Vultures, as obligate scavengers, not
Acknowledgements
This research was supported by the
National Natural Science Foundation
of China (31572292, 31272291,
30970340). Field workers included
Li Bo, Liu Zheqing, Dao Caiwujiap,
Shan Jiap, Xing Rui, Luo Biao,
Wang Yaotian, Chen Xiting, Li
Weidong, Shi Zhu, Jirige Lite, Ding
Peng, Te Lai, Zhang Tong, Zhao
Xumao, Xu Feng, Sun Dahuan (the
Xinjiang
Bird-watching
Society),HF Cheung (the Hong
Kong Bird Watching Society),
Ablimit Abdukadir, Lin Xuanlong,
20
Vulture News 68
July 2015
MardanTurghan, Shi Lei, Ba Tai, Cai
Dai, Yang Xiaomin, Huang Yahui,
Jiang Yingxin, Jiang Mingyi, Xiang
Wenjun, Maimaitiming Aizijiang,
Ma Yao, Gao Xiaoqing, Ting Zhou
etc.
Keywords: Vultures, population size, status, threatened, China
References
BirdLife International. 2014. Species factsheets: Gypaetus barbatus, Gyps
bengalensis, Gyps himalayensis, Gyps fulvus, Aegypius monachus,
Sarcogyps calvus, Gyps tenuirostris, Neophron percnopterus. Downloaded
from http://www.birdlife.org on 2/5/2014.
Camiña, A. and Montelío, E. 2006. Griffon vulture Gyps fulvus food shortages
in the Ebro Valley (NE Spain) caused by regulations against bovine
spongiform encephalopathy (BSE). Acta Ornithologica 41: 7-13.
Clements, T., Gilbert, M., Rainey, H. J., Cuthbert, R., Eames, J. C., Bunnat,
P., Teak, S., Chansocheat, S., and Setha, T. 2013. Vultures in Cambodia:
population, threats and conservation. Bird Conservation International 23:
7-24.
Cunningham, A. B. 1990. Vultures and the trade in traditional medicine.
Vulture news 24: 3-10.
Das, D., Cuthbert, R. J., Jakati, R. D. 2011. Diclofenac is toxic to the
Himalayan Vulture Gyps himalayensis. Bird Conservation International
21: 72-75.
Di, Z, Y. 2003. The giant among the birds of prey. Man and the Biosphere 8:
36-41. (In Chinese).
Fauna of Medicinal Animal in China. 1979. Tianjin: Tianjin Science and
Technology Press, Tianjin, China. (In Chinese).
Green, R. E., Newton, I. A. N., Shultz, S., Cunningham, A., Gilbert, M., Pain,
D. J., Prakash, V. 2004. Diclofenac poisoning as a cause of vulture
population declines across the Indian subcontinent. Journal of Applied
Ecology 41: 793-800.
Gu, B. Y., Su, H. L. & Caiba, Z. X. 1994. The preliminary research of
Lammergeier breeding in the eastern Tibet. Tibet's Science & Technology
4: 58-62.
21
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July 2015
Guo, H. & Ma, M. 2012. The Egyptian Vulture (Neophron percnopterus):
record of a new bird in China. Chinese Birds 3: 238–239.
Hernández, M. & Margalida, A. 2008. Pesticide abuse in Europe: effects on
the Cinereous vulture (Aegypius monachus) population in Spain.
Ecotoxicology 17: 264-272.
Houston, D. C. 1990. A change in the breeding season of Rüppell's Griffon
Vultures Gyps rueppellii in the Serengeti in response to changes in
ungulate populations. Ibis 132: 36-41.
IUCN Red List of Threatened Species, 2013 (http://www.iucnredlist.org/).
Jin, Y. and Yu, Q. 2004. Vultures in the plateau. Man & Nature 4: 74-79. (In
Chinese).
Kenny, D., Batbayar, N., Tsolmonjav, P., Willis, M.J., Azua, J. & Reading, R.
2008. Dispersal of Eurasian Black Vulture Aegypius monachus fledglings
from the IkhNart Nature Reserve, Mongolia. Vulture News 59:13-19.
Koenig, R. 2006. Vulture research soars as the scavengers' numbers decline.
Science 312: 1591-1592.
Ledger, J. A. and Annegarn, H. J. 1981. Electrocution hazards to the Cape
Vulture (Gyps coprotheres) in South Africa. Biological Conservation 20:
15-24.
Leung, A. Y. 2006. Traditional toxicity documentation of Chinese materia
medica—An overview. Toxicologic Pathology 34: 319–326.
Li, S. Z (Ming Dynasty). 1981. Bencao Gangmu (Compendium of materia
medica). People's Health Publishing House, Beijing, China. (In Chinese).
Liu, C., Huo, Z. P. & Yu, X. P. 2013. Population and conservation status of
the Himalayan Griffon (Gyps himalayensis) at the Drigung Thel
Monastery, Tibet, China. Chinese Birds 4:328–331.
Lu, X., Ke, D. H. & Zeng, X. H. 2009. Status, ecology and conservation of the
Himalayan Griffon Gyps himalayensis (Aves, Accipitridae) in the Tibetan
Plateau. Ambio 38: 166-173.
Luo, X. W. 2003. Bencao Gangmu (Compendium of Materia Medica).
Foreign Languages Press, Beijing, China.
Ma, M. 2011. A checklist on the distribution of the birds in Xinjiang. Science
Press, Beijing, China.
Ma, M., Caiwujiap, D. & Shan, J. 2014. Study of the reproductive behavior of
Himalayan Vulture (Gyps himalayensis) by mini camera-traps in the
Tianshan Mountains. Chinese Journal of Wildlife 35: 414-419.
22
Vulture News 68
July 2015
Ma, M., Caiwujiap, D. & Xu, G.H. 2013. Why are juvenile Himalayan
Vultures Gyps himalayensis in the Xinjiang Tien Shan still at the nest in
October? Birding ASIA 20: 84-92.
MaMing R, Zhao X. M., Xu G. H., Caiwu J., Zhang T., Ding P. and Xu F.
2014. Raptor conservation and culture in the west of China. Ela Journal 3:
23-29.
McKie, R. 2007. Vulture numbers are cut to the bone — Extinction fears for a
scavenger vital to preserving ecosystems. Vulture News 56: 95-96.
Mei, Y. & Ma, M. 2008. The accident investigation of grid electric shock
raptor to death in west China. Chinese Journal of Zoology 43: 114-117.
Murn, C. & Anderson, M. D. 2008. Activity patterns of African White-backed
Vultures Gyps africanus in relation to different land-use practices and
food availability. Ostrich 79: 191-198.
Naidoo, V., Wolter, K., Cuthbert R., Duncan, N. 2009. Veterinary diclofenac
threatens Africa’s endangered vulture species. Regulatory toxicology and
pharmacology 53: 205-208.
National Forestry Bureau. 2009. Resource survey on the key animals in
China. China Forestry Publishing House, Beijing, China. (In Chinese).
Oaks, J.L., Gilbert, M., Virani, M. Z., Watson, R. T. & Meteyer, C. U. 2004.
Diclofenac residues as the cause of vulture population decline in Pakistan.
Nature 427: 630–633.
Ogada, D. L. 2014. The power of poison: pesticide poisoning of Africa's
wildlife. Annals of the New York Academy of Sciences 1322: 1-20.
Pain, D.J., Cunningham, A.A., Donald, P.F., Duckworth, J.W., Houston, D.C.,
Katzner, T., Parry-Jones, J., Poole, C., Prakash, V., Round, P. & Timmins,
R. 2003. Causes and effects of temporospatial declines of Gyps Vultures in
Asia. Conservation Biology 17: 661-671.
Prakash, V., Bishwakarma, M. C., Chaudhary, A., Cuthbert, R., & Dave, R.
2012. The population decline of Gyps Vultures in India and Nepal has
slowed since veterinary use of diclofenac was banned. PLoS ONE 7(11):
e49118.
Saidu, Y. & Buij, R. 2013. Traditional medicine trade in vulture parts in
northern Nigeria. Vulture News 65: 4-14.
Satheesan, S.M. 1998. The role of vultures in the disposal of human corpses
in India and Tibet. Vulture News 39: 32–33.
23
Vulture News 68
July 2015
Tashi, S. & Zhou, J. 2009. My Himalayan Vulture. Supported by Eu-China
Programme
(http://video.sina.com.cn/p/news/green/v/2011-0124/141461244735.html)
Wildlife Protection Law of the People's Republic of China. 2004.
(http://www.gov.cn/fwxx/bw/lyj/content_396083.htm).
Williams, V. L., Cunningham, A. B., Kemp, A. C. & Bruyns, R. K. 2014.
Risks to birds traded for African traditional medicine: A quantitative
assessment. PloS one 9(8): e105397.
Xu, W.S. 1995. China's birds of prey. China Forestry Publishing, Beijing,
China.
Ye, X.T. 1991. Distribution and status of the Cinereous Vulture Aegypius
monachus in China. Birds of Prey Bulletin 4: 51-56.
Zhang, F.Y. & Yang, R.L. 1980. The Lammergeyer in the southern Gansu.
Acta Zoologica Sinica 26: 86-90.
Zheng, G.M. 2011. A checklist on the classification and distribution of the
birds of China. Science Press, Beijing, China.
******
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Blood lead levels in White-Backed Vultures (Gyps africanus)
from Botswana, Africa
David Kenny1,2*, Richard Reading1,2, Glyn Maude1,2, Peter Hancock2,
Beckie Garbett2
1
Denver Zoological Foundation, E. 2300 Steele St, Denver, Colorado 80205, USA.
2
Raptors Botswana, Box Hak 33, Maun, Botswana, Africa.
*
Corresponding author: [email protected]
http://dx.doi.org/10.4314/vulnew.v68i1.2
Introduction
hematopoietic, reproductive, and
nervous systems (Locke & Thomas
1996, Redig & Cruz-Martinez 2009).
It is the most common heavy metal
poison reported for avian species,
including raptors (Mautino 1997).
Lead toxicity from hunter-spent lead
ammunition is the major impediment
to the recovery of the California
Condor (Gymnogyps californianus)
in North America (Finkelstein et al.
2012, Stringfield 2012). There have
been documented lead toxicity
reports for vultures from both the
New World (South and North
America) and the Old World
(Europe, Africa, and Asia). Vulture
species reported with lead toxicity
include the New World Andean
Currently vulture populations in subSaharan Africa are dramatically
declining due to direct and indirect
poisoning with pesticides (Ogada
2014, Virani 2011).
During a
tagging and radio telemetry study
from 2012 thru 2015 involving
several species of vultures in
Botswana, the Denver Zoological
Foundation in collaboration with
Raptors Botswana investigated lead
exposure as another issue that might
affect the persistence of vultures in
Africa in the future.
Lead toxicity in avian species
manifests itself as a cumulative,
multi-systemic disease affecting the
liver, kidney, heart, gastrointestinal,
25
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July 2015
Condor (Vultur gryphus), California
Condor, and Turkey Vulture
(Cathartes aura) and the Old World
Griffon Vulture (Gyps fulvus),
Pyrenean Bearded Vulture (Gypaetus
barbatus), Eurasian Black Vulture
(Aegypius monachus) and Egyptian
Vulture (Neophron percnopterus)
(Hernández & Margalida 2009,
Mateo 2009, Nam & Lee 2009,
Rodriguez-Ramos et al. 2009, Kelly
et al. 2011, Lambertucci et al. 2011,
Stringfield 2012).
However, we
discovered no published reports for
lead toxicity in African vultures.
lead analysis. We obtained blood
samples from 477 White-Backed
Vultures (WbV, Gyps africanus) for
blood lead testing. Blood lead level
(BLL) analyses were performed with
the portable LeadCare® I clinical
analyzer in 2012 and the LeadCare®
II clinical analyzer in 2013 thru 2015
(LeadCare® I & II, Magellan
Diagnostics,
North
Billerica,
Massachusetts 01862, U.S.A.).
The LeadCare® I reports BLLs
down to 0 µg/dl and the LeadCare
II® reports values <3.3 μg/dl as
“Low” and both the LeadCare® I &
II analyzers report values >65 μg/dl
as “High”. For statistical analysis
we assigned a value of 1.6 ± μg/dl
for levels determined as “Low” and a
value of 66 μg/dl for levels reported
as “High” from both analyzers.
There were 72 results reported as
“Low” and 7 as “High”.
We
therefore consider our results to be
conservative for BLLs.
Methods
We captured vultures in several
regions of Botswana. For capture we
used bait and a gas-propelled canon
net system (WCS NetBlaster™,
Wildlife Control Supplies, East
Granby, CT 06026, USA) with a
portable nitrogen tank to charge the
canon and a 13 m x 17.3 m braided
nylon net with a 5.1 cm mesh and
21.8 kg breaking strain. We
restrained captured birds in dorsal
recumbency for venipuncture from
the ventral ulnaris vein.
We
transferred blood to a purple-top tube
(ethylenediaminetetraacetic
acid
tube, 250-500 μl fill, Capiject,
Terumo
Medical
Corporation,
Elkton, Maryland 21921, U.S.A.) for
Results
Across all samples (n = 477), mean
BLL was 10.6 µg/dl (SE ±0.52
µg/dl) , and the median BLL was 6.8
µg/dl. We divided the results into
three categories; <10 µg/dl, 10 - <45
µg/dl, and >45 µg/dl (Figure 1). As
per Finkelstein et al. (2012), for
California Condors, a blood level
26
Vulture News 68
July 2015
≥10 µg/dl is consistent with exposure
while ≥45 µg/dl is toxic and a
candidate for chelation therapy.
Applying these categories to this
study 28.51% (n = 136) of the birds
had BLLs consistent with exposure
while an additional 2.31% (n = 11)
of the birds were consistent with
toxicity (Figure 1).
Therefore
30.77% of these randomly captured
birds exceeded the background 10
µg/dl level.
We immediately
released birds following processing
and prior to analysis so there was no
possibility to follow up or treat
individuals with elevated BLLs.
80%
70%
69.18% (n = 330)
60%
50%
40%
28.51% (n = 136)
30%
20%
10%
2.31% (n = 11)
0%
<10 µg/dl
10 to <45 µg/dl
BLL categories
>45 µg/dl
Figure 1: Percentage of 477 White-backed Vultures (WbV, Gyps africanus)
with different blood lead levels (BLL) for in Botswana.
27
Vulture News 68
July 2015
fragmentation would potentially
expose many vultures to lead
fragments from carcasses or gut piles
left in the field. We have no
knowledge if there is significant lead
contamination in soil or water and
available to avian scavengers in
Botswana.
The Centers for Disease Control
and Prevention (CDC) has adopted
the position that there is no
acceptable BLL for humans (Pain
1995, Brown & Wheeler 2013). All
the known effects of lead on living
organisms are deleterious, so there is
no safe BLL (Pain 1995). The subtle
effects of low-level chronic lead
exposure may go unnoticed, but
affected animals may be less fit and
more susceptible to morbidity and
mortality. We are concerned that the
cumulative subclinical negative
effects from chronic lead toxicity
may affect long-term survival for
these
long-lived
and
slow
reproducing vulture species.
In
conclusion,
pesticide
poisoning is one of the main factors
responsible for the major reduction
of vulture populations in subSaharan Africa and certainly requires
an immediate response by the
conservation community. In this
report we have described an
additional problem for vultures – the
ingestion of lead. Our results show
Discussion
We did not determine the definitive
source/s for elevated BLLs in this
study but hypothesize that potential
sources are hunter-spent lead
ammunition, soil, and/or water. The
highest mean BLL we determined
was 17.7 µg/dl (n = 33) on a hunting
ranch while the lowest was 6.4 µg/dl
(n = 42) in a National Park. We
therefore suspect that spent lead
ammunition is at least partially
responsible for the WbV BLLs. We
plan to continue sampling other areas
in Botswana, including hunting
ranches and protected areas, and
analyze and report on statistically
significant
differences
between
capture sites.
As previously described lead
poisoning
from
hunter-spent
ammunition is a significant issue
negatively impacting the recovery of
the California Condor. Spent lead
ammunition in Botswana may
originate from legal hunting or
illegal poaching activities. Modern
firearms achieve high velocities
causing lead-based bullets to
fragment widely along the wound
tract (Stroud & Hunt 2009). In a deer
study, 74% of the offal piles
examined contained >100 fragments
distributed along the wound channel
(Hunt et al. 2006). This degree of
28
Vulture News 68
July 2015
that this is already happening in
Botswana and we suspect in other
African countries. Following hunting
activities, carcasses or gut piles with
lead ammunition fragments left in
the field are available for scavengers.
As with pesticides, lead-poisoned
birds may die and go unnoticed in
the bush. More insidious is chronic
low-level lead poisoning which
might reduce fitness pushing
increasingly smaller populations
closer to extinction. Solutions to lead
poisoning should be proactive,
science-based
and
address
ecological, social, economic, and
political concerns. A first step in
reducing lead levels in the avian
scavenger environment would be to
replace lead-based ammunition with
non-lead substitutes. Soil and water
as sources for lead in vultures also
merit additional future investigation.
Acknowledgements
We thank the Botswana Department
of Wildlife and National Parks
(Research Division) for granting
permits to conduct this research. We
also thank staff from the Denver
Zoological Foundation, Raptors
Botswana, KANABO Conservation
Link, White Buffalo, and Stuart and
Teresa Graham for assistance with
capture, processing, and financial
support.
References
Brown, M.J. & Wheeler, W. 2013. Blood lead levels in children aged 1-5
years – United States, 1999-2010. Morbidity and Mortality Report April
5, 2013/62:245-248.
Finkelstein, M.E., Doak, D.F., George, D., Burnett, J., Church, M., Grantham,
J. & Smith, D.R. 2012. Lead poisoning and the deceptive recovery of the
critically endangered California condor. Pp. 11449-11454 in: Paine, R.T.
(ed.). Proceedings of the National Academy of Sciences of the United
States of America, July 10, 109. www.pnas.org/cgi/doi/10.1073/pnas.
1203141109.
Hernández, M. & Margalida, A. 2009. Assessing the risk of lead exposure for
the conservation of the endangered Pyrenean bearded vulture (Gypaetus
barbatus) population. Environmental Research 109: 837-842.
29
Vulture News 68
July 2015
Hunt, W.G., Burnham, W., Parish, C.N., Burnham, K.K., Mutch, B. & Oaks
J.L. 2006. Bullet fragments in deer remains: implication for lead exposure
in scavengers. Wildlife Society Bulletin 34:167-170.
Kelly, T.R., Bloom, P.H., Torres, S.G., Hernandez, Y.Z., Poppenga, R.H.,
Boyce, W.M. & Johnson C.K. 2011. Impact of the California lead
ammunition ban on reducing lead exposure in golden eagles and turkey
vultures. PLOS ONE,
www.plosone.org/article/info%3Ad01%2F10.1371%fjournal.pone.00176
56.pdf.
Lambertucci, S.A., Donázar, J.A,. Huertas, A.D., Jiménez, B., Sáez, M.,
Sanchez-Zapata, J.A. & Hiraldo, F. 2011. Widening the problem of lead
poisoning to a South American top scavenger: lead concentrations in
feathers of wild Andean condors. Biological Conservation 144:14641471.
Locke, L.N. & Thomas, N.J. 1996. Lead Poisoning of waterfowl and raptors.
Pp. 108-117 in: Fairbrother, A., Locke, L.N. & Hoff, G.L. (eds.).
Noninfectious Diseases of Wildlife, 2nd ed. Iowa State University Press,
Ames, Iowa U.S.A. 219 pp.
Mateo, R. 2009. Lead poisoning in wild birds in Europe and the regulations
adopted by different countries. Pp. 71-98 in: Watson, R.T. Fuller, M.
Pokras, M. & Hunt, W.G. (eds.). Proceedings of the Conference:
Ingestion of spent lead ammunition: Implications of wildlife and humans.
12-15 May 2008, Boise State University, Boise, Idaho U.S.A. 383 pp.
Mautino, M. 1997. Lead and zinc intoxication in zoological medicine. Journal
of Zoo and Wildlife Medicine 28: 28-35.
Nam, D-H. & Lee, D-P. 2009. Abnormal lead exposure in globally threatened
Cinereous vultures (Aegypius monachus) wintering in South Korea.
Ecotoxicology 18: 225-229.
Ogada, D.L. 2014. The power of poison: pesticide poisoning of Africa’s
wildlife. Annals of the New York Academy of Sciences 1322 (2014) 1-20.
doi: 10.1111/nyas. 12405.
Pain, D.J. 1995. Lead in the environment. Pp. 356-391 in: Hoffman, D.J.,
Rattner, B.A., Burton, G.A. & Cairns, J. (eds.). Handbook of
Ecotoxicology. CRC Press, Boca Raton, Florida U.S.A. 755 pp.
30
Vulture News 68
July 2015
Redig, P.T. & Cruz-Martinez, L. 2009. Lead poisoning. Pp. 228-229 in: Tully,
T.N., Dorrestein, G.M. & Jones, A.K. (eds.). Handbook of Avian
Medicine, 2nd ed. Saunders Elsevier, Philadelphia, PA U.S.A. 456 pp.
Rodriguez-Ramos, J., Gutierrez, V., Höfle, U., Mateo, R., Monsalve, L.,
Crespo, E. & Blanco, J.M. 2009. Lead in Griffon and Cinereous
Vultures in central Spain: correlations between clinical signs and blood
lead levels. Pp. 235-236 in: Watson, R.T., Fuller, M., Pokras, M. &
Hunt, W.G. (eds.). Proceedings of the Conference: Ingestion of spent
lead ammunition: Implications of wildlife and humans.12-15 May 2008,
Boise State University, Boise, Idaho U.S.A. 383 pp.
Stringfield, C. 2012. The California Condor (Gymnogyps californianus)
veterinary program: 1997-2010. Pp. 286-296 in: Miller, E.R. & Fowler,
M.E. (eds.). Fowler’s Zoo and Wild Animal Medicine: Current
Therapy, Vol. 7. Elsevier Saunders, St. Louis, MO U.S.A. 669 pp.
Stroud, R.K. &. Hunt, W.G. 2009. Gunshot wounds: a source of lead in the
environment. Pp. 119-125 in: Watson, R.T., Fuller, M., Pokras, M. &
Hunt, W.G. (eds.). Proceedings of the Conference: Ingestion of spent
lead ammunition: Implications of wildlife and humans. 12-15 May 2008,
Boise State University, Boise, Idaho U.S.A. 383 pp.
Virani, M.Z., Kendall, C., Njoroge, P. & Thomsett, S. 2011. Major declines in
the abundance of vultures and other scavenging raptors in and around
the Masai Mara ecosystem, Kenya. Biological Conservation 144: 746752.
******
31
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A preliminary assessment of the palate and tongue for
detecting organophosphorus and carbamate pesticide
exposure in the degraded carcasses of vultures and other
animals
Ngaio L. Richards1, Irene Zorrilla2, Isabel Fernandez2, Mónica Calvino2,
Joaquin Garcia2, Antonio Ruiz3
1
Working Dogs for Conservation, 52 Eustis Road, Three Forks, Montana 59752, USA.
2
Environmental and Water Agency of Andalusía, Division of Integrated Environmental
Quality, Regional Ministry of Environment and Spatial Planning, Center for Analysis
and Diagnosis of Wildlife - CAD, Avda. Lope de Vega, 9, Málaga 29010, Spain.
3
Environmental and Water Agency of Andalusía, Division: Strategy for the Control of
Poisons and Other Threats to Endangered Wildlife, Avda. Johan Gutenberg s/n. 41092
La Cartuja, Seville, Spain.
*Corresponding author: [email protected]
ABSTRACT
In many regions of the world, organophosphorus (OP) and carbamate (CM)
pesticides are used to poison wildlife thought to be competing with human
activities (e.g. hunting). Vultures may be secondarily poisoned or directly
targeted, e.g. for muti or traditional medicine. Some OPs and CMs are so
acutely toxic that animals will die with poisoned material still in their mouths
- un-swallowed, before traces may have spread to other parts of the body.
Even when death is more prolonged, the tissues in which residues have
accumulated may deteriorate before the carcass is discovered, minimizing the
chances of recovering viable samples for toxicological analyses that would
conclusively identify poisoning as the cause of death. With all these factors in
mind, we investigated the feasibility of detecting OP and CM pesticides in the
oral cavity, with emphasis on the tongue and palate. A total of 60 degraded
carcasses (n = 28 avian and 32 mammalian) recovered from various scenes of
wildlife crime in Andalucía, southern Spain, where poisoning was suspected,
32
Vulture News 68
July 2015
were submitted to the Center for Analysis and Diagnosis of Wildlife in
Málaga for necropsy and toxicological analyses. Of these, 20 and 24 avian
and mammalian tongues, respectively, could be recovered for analysis.
Separately, the palate from one degraded Cinereous Vulture Aegypius
monachus carcass was also opportunistically retrieved and analyzed following
an incident of vulture mass-mortality in which nine Griffon Vultures Gyps
fulvus also perished. Residues or presence of OPs and CMs were detected in
one avian tongue (analyzed with food from the mouth) and four mammalian
tongues. Our findings suggest avian tongues alone are not optimal, but canid
tongues and those of larger mammals may lend themselves well to analysis.
Detection of the OP chlorfenvinphos (3.39 mg/kg) in the Cinereous Vulture
palate (the only part of the carcass in which residues were detected) indicates
this is a promising sample. To our knowledge, this represents the first time
that OP and CM pesticides have been detected in tongue and palate samples.
We recommend further exploration of oral cavity samples, especially within
the context of the risk that residues therein may pose to human health.
http://dx.doi.org/10.4314/vulnew.v68i1.3
carbamate (CM) pesticides in
question are so acutely toxic that
animals die with the poison-laced
material still in their mouths,
sometimes before they can swallow
it, and before residues can spread to,
and be incorporated by, other parts
of the body (Figure 1). Should this
be the case, analysis of typically
favored samples like stomach
contents would not reflect that
exposure had occurred (Mineau et al.
2011). And, even when a poisoning
death
is
more
protracted,
conventionally-analyzed
samples
(i.e. soft tissues) could be degraded
Introduction
Vultures and other wildlife as well as
domesticated animals around the
world are being deliberately or
secondarily poisoned at an alarming
rate, primarily due to human-wildlife
conflict (Ogada 2014). They are also
being poisoned with pesticides for
human consumption - either as food
(Odino 2012, Ogada et al. 2015) or
for use in traditional medicine
(Mander et al. 2007, McKean et al.
2013, Saidu and Buij 2013, Ogada
2014, Ogada et al. 2015). Many of
the organophosphorus (OP) and
33
Vulture News 68
July 2015
between when the animal dies and
the carcass is actually found, and/or
parts of it may have been scavenged,
thereby limiting its viability for
toxicological analyses (Richards et
al. 2014).
Figure 1: When the pesticides used to poison wildlife are acutely toxic,
animals (such as this African White-backed Vulture Gyps africanus) may die
with food in their mouths, and before residues can reach other parts of the
body. Photo courtesy of Andre Botha.
A handful of studies have examined
the feasibility of detecting OP and
CM pesticides in talons, feet and
beaks, which better withstand
environmental degradation than soft
tissues. Importantly, these also
represent the first likely point of
contact animals will have with these
pesticides, as they paw at, step on, or
grasp poisoned items prior to
ingesting them. Simulating a dermal
contact scenario, goslings were
exposed to turf sprayed with the OP
diazinon (O,O - diethyl O - (2isopropyl-6-methyl-4-pyrimidinyl)
phosphorothioate); residues were
subsequently detected in their feet
after these were removed and
34
Vulture News 68
July 2015
weathered for seven days (Vyas et
al. 2003). Similarly, eastern Screechowls Megascops asio were exposed
to baits laced with CM carbofuran
(2,3
dihydro-2,2-dimethyl-7benzofuranyl methylcarbamate) and
residues were detected in their talons
after these had been weathered for 28
days post-exposure (Vyas et al.
2005). Residues of carbofuran and
two of its primary metabolites (3ketocarbofuran
and
3hydroxycarbofuran)
were
also
identified in the highly weathered
talons and beak of an African Whitebacked Vulture Gyps africanus
recovered from an agricultural field
in Kenya (Otieno et al. 2010, Otieno
et al. 2012). We have also detected
CMs (e.g., aldicarb) and OPs (e.g.,
chlorfenvinphos) in beaks and talons
taken from the degraded carcasses of
birds submitted to the Center for
Analysis and Diagnosis of Wildlife
(CAD) in Málaga, southern Spain,
during routine wildlife forensic
investigations (Richards et al. in
prep). Nonetheless, despite their
established utility and viability, it
does not appear as yet that any of
these ‘alternative’ samples are
routinely collected, analyzed or
considered when pesticide poisoning
is suspected, even in the absence of
other more ‘conventional’ samples
like soft tissues.
After talons, feet and beaks, the
oral cavity/mouth is the next and
likely last point of contact with
pesticides prior to death. Since
pesticide-poisoned food rests on the
tongue, we reasoned that residues
might be detectible therein. We
therefore sampled and analyzed the
tongues from a selection of
mammalian and avian carcasses that
were degraded, and where pesticide
poisoning was suspected to have
caused death.
Here we report on our findings
from both the analysis of tongues
and the palate, offer further
recommendations for refinement,
and propose potential applications.
Our aims were to a) assess the
feasibility of detecting OP and/or
CM pesticide residues in the tongue
and palate; b) provide additional
tools for determining cause of death
in degraded carcasses, and, c)
promote broader awareness and use
of these and other ‘alternative’
samples in a wildlife forensic
context. To our knowledge this is the
first time that either the tongue or the
palate has been analyzed for residues
of OPs, CMs or any other class of
pesticide, during the course of a
wildlife forensics investigation or
otherwise.
35
Vulture News 68
July 2015
protocols (as detailed in Fajardo et
al.
2015),
during
routine
investigations under the Andalusian
government’s
antipoisoning/poaching
strategy
(described in Fajardo et al. 2012).
The carcasses were submitted to the
CAD for necropsy and toxicological
analyses. All toxicologically viable
samples (e.g., stomach contents,
digestive tracts) were collected for
analysis and for comparison with the
tongues.
Materials and Methods
Carcass collection
A total of 60 carcasses (28 avian, of
these 7 vultures; and 32 mammalian)
in varying stages of decomposition
or degradation, and where pesticide
poisoning was suspected as the cause
of death, were selected for this
preliminary study (Tables 1a and
1b). Each carcass was collected
according to specific forensic
Table 1a: Summary of degraded bird carcasses (n = 28) recovered by species and
weights of tongue samples recovered (n = 20)
Species
Carcasses Tongues Tongue weights
sampled
(g)
Buzzard, Eurasian Buteo buteo
1
1
1.1
Chicken, domestic Gallus gallus
1
1
0.1
Eagle, Bonelli’s Aquila fasciata
1
0
Not obtained
Eagle, Booted Aquila pennata
3
2
0.78, 0.9
Eagle, Spanish Imperial Aquila adalberti
2
2
0.79, 2.41
Jackdaw, Eurasian Corvus monedula
2
2
0.15, 0.53
Kestrel, Eurasian Falco tinnunculus
1
0
Not obtained
Kite, Black Milvus migrans
5
4
0.49 - 1.72
Kite, Red Milvus milvus
1
0
Not obtained
Osprey Pandion haliaetus
1
1
0.46
Owl, Eurasian eagle Bubo bubo
2
2
2.34, 3.20
Owl, Tawny Strix aluco
1
0
Not obtained
Vulture, Cinereous Aegypius monachus
1
0
Not obtained
Vulture, Egyptian Neophron
percnopterus
Vulture, Griffon Gyps fulvus
3
2
0.69, 1.01
3
3
3.48 - 5.98
TOTALS
28
20
36
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July 2015
Table 1b: Summary of degraded mammalian carcasses (n = 32) recovered by species
and weights of tongue samples recovered (n = 24)
Species
Carcasses
Tongues
sampled
Badger, Eurasian Meles meles
1
1
Tongue
weights
(g)
5.0
Cat, domestic Felis catus
7
6
2.52 – 5.66
Dog, domestic Canis lupus
familiaris
Fox, Red, European Vulpes vulpes
crucigera
Genet, Common Genetta genetta
10
9
4.2 – 7.19
9
4
0.52 – 9.71
1
1
4.72
Hare, Iberian Lepus granatensis
1
1
5.4
Polecat, European Mustela
putorius
Rabbit, European Oryctolagus
cuniculus
Weasel, Least Mustela nivalis
1
1
0.55
1
1
2.07
1
1
0.35
TOTALS
32
24
The tongue samples were cut from
the mouth at their base - unless the
carcass was in such poor condition
that they could not be removed as an
individual sample. Following an
incident of mass vulture mortality in
southern Spain in which nine Griffon
Vulture Gyps fulvus carcasses were
recovered with that of a Cinereous
Vulture Aegypius monachus (see
Fajardo et al. 2014 for details), we
also opportunistically analyzed the
palate of the Cinereous Vulture. The
palates from the Cinereous vulture
carcass (recovered in a degraded
condition) and the Griffon Vulture
carcasses were also excised (Figures
2a to 2f).
37
Vulture News 68
July 2015
Figure 2a
Figure 2b.
Figure 2c.
Figure 2d.
Figure 2e.
Figure 2f.
Figure 2a : Cinereous Vulture head, showing the extent of carcass degradation.
Figure 2b: Ventral aspect of Cinereous Vulture head.
Figure 2c: Removal of the beak.
Figures 2d/2e: Palate being removed for processing and toxicological analysis.
Figure 2f: Cinereous Vulture head after complete removal of palate material.
Reproduced with permission from D. de la Bodega, SEO Birdlife (Fajardo et al. 2014).
38
Vulture News 68
July 2015
Sample preparation and analysis for
pesticide residues
(GC-MS/MS) with ion trap (IT) and
triple quadrupole (QqQ) analyzers,
or
ultra-performance
liquid
chromatography mass spectrometry
(UHPLC-MS/MS)
with
triple
quadrupole (QqQ) analyzer. For GCdetectible pesticides, the limits of
detection (LODs) ranged from 0.001
to 0.436 g L−1 and the limits of
quantification (LOQs) ranged from
0.003 to 1.452 g L−1. For LCdetectible pesticides, the LODs
ranged from 0.003 to 1.048 g L−1 and
the LOQs ranged from 0.011 to
3.494 g L−1 (Cazorla et al. 2011). All
toxicological
analyses
were
conducted in accordance with EU
Directive 2002/657/CE (concerning
the performance of analytical
methods and the interpretation of
results)
and
EU
Regulation
1107/2009 CE (concerning the
regulation
of
commercial
insecticides). A list of the pesticides
that were screened, and their
individual limits of detection, is
provided in Appendix 1 (online
version only).
Sample
preparation,
pesticides
residue extraction and multiscreening methods were all adapted
from those described by Zoun &
Spierenburg (1989). Briefly, 5 g of
each sample were ground in a mortar
with 10 g of anhydrous sodium
sulphate (Merck) and 60 ml of
dichloromethane (Merck). After 10
minutes shaking, these were filtered
(Whatman,
nº1
paper)
and
rotavaporated to dryness (BÜCHI R200). The sample was then
reconstituted in 6 ml of ethanol
(Panreac) and filtered through glass
wool. Finally, sample cleanup was
obtained via solid phase extraction
(Extrabond C18 500 mg 3/ml,
Sharlab
S.L.).
Aliquots
(40
microliters) of these extracts were
initially screened qualitatively, via
thin-layer chromatography (TLC) at
the CAD. If a positive result was
obtained, i.e., indicating the presence
of an OP or a CM, another aliquot (1
ml) was screened at the Laboratorio
Analítico Bioclínico (LAB) in
Almería (southern Spain). Each
aliquot was analyzed for a suite of
278 pesticides (including OPs, CMs,
organochlorines, strychnine and
pyrethroids) using either gas
chromatography–mass spectrometry
Results
Sixty carcasses were recovered for
this preliminary study: 28 avian
carcasses spanning 15 species
(including three Egyptian Vultures
Neophron
percnopterus,
three
39
Vulture News 68
July 2015
Griffon Vultures and one Cinereous
Vulture) and 32
mammalian
carcasses of 10 species. Of these, 20
avian and 24 mammalian tongues
were recovered for analysis. Tables
1a and 1b summarize the species
represented, as well as the number of
carcasses and tongues recovered
from each. The range of weights of
the tongues is also provided for
consideration of the viability of this
sample in relation to others (see
Discussion).
were screened for the suite of
compounds (and hence were
included in the total sample tally),
and is indicated where found with an
asterisk in Table 2, however we did
not further consider it in our analysis
since its lone presence (absent DDE
and other breakdown metabolites
such
as
DDD)
indicates
environmental persistence from
historical agricultural usage, rather
than deliberate pesticide poisoning.
Twenty (20) avian and 24
mammalian tongues were retrieved
and analyzed. No OP or CM
pesticides were detected in any of the
avian tongue samples, however the
presence of carbofuran was detected
in three of the mammalian tongues
(two red foxes and one domestic
dog; Table 3b). An additional six
avian and six mammalian tongues
were pooled with oral contents for
analysis.
Methamidophos
was
(qualitatively) detected in one of the
avian pooled samples (Egyptian
Vulture; Table 3a) and carbofuran
was detected in one of the
mammalian pooled samples (Red
Fox; Table 3b). Two avian and two
mammalian tongues pooled with
other carcass components tested
negative for pesticide residues.
To allow a more refined
comparison of the tongue relative to
other samples, Tables 3a and 3b list
all carcass samples that tested
positive for an OP and/or a CM
pesticide, by species.
Analysis of tongues relative to other
carcass samples
From the 60 recovered carcasses, a
total of 151 samples were retrieved,
78 from birds and 73 from mammals.
Of these, 11 avian and 19
mammalian samples tested positive
for an OP or CM pesticide. Eight of
the
positives
were
detected
qualitative, i.e., via TLC, only. To
better assess the viability of the
tongue, we categorized pooled
samples including the tongue from a
given carcass separately from pooled
samples that did not include it. These
results are summarized in Table 2.
We note that 11 livers (three from
birds and eight from mammals) were
neither included in the total sample
count nor in our analysis, because
these samples were only screened for
anticoagulant rodenticides. The
organochlorine
p,p’-DDE
was
detected in five avian samples that
40
Vulture News 68
July 2015
Table 2: Summary of all samples (n = 151) collected from avian carcasses (n = 28) and mammal carcasses (n = 32)
Sample type
Avian
Insects recovered from carcasses
3
Positive (key to abbreviations
below)
0
Mammal
Positive
4
1: Cara
Digestive tractb,*
20
4: A(2), M(1,1a)
2
0
Feather
Liver
Oral cavity/content
Organs, pooledc,*
1
0
1
12
0
0
1: CPF
1: CFVa
N/A
1
2
8
N/A
0
1: Cara
2: Car
Pellet
Stomach contents
2
1
1: CFVa
1: CPF
N/A
22
N/A
11: A (6), Car (4 (1a)), M (1)
Talons/material held inside
Tongue only
Tongue + oral contents
Tongue + various pooled samplesd
Various pooled samplese,f,*
4
20
6
2
6
1: A
0
1 Ma
0
1: CFVa,g
N/A
24
6
2
2
N/A
3: Car
1: Car
0
0
TOTALS
78
11
73
19
a. QUAL = qualitative, i.e., detection by TLC only; b. Digestive tract includes: larynx, esophagus, trachea, crop, gizzard, proventriculus;
c. Pooled due to poor carcass condition; *p,p-DDE detected (n = 3 organs, pooled; 1 digestive tract and 1 various pooled samples);
d, e. In case of highly degraded/skeletonized carcass, any possibly viable samples were pooled for analysis; f. Tongues not included
g. Crop + insects recovered from carcass
A = aldicarb only or aldicarb and metabolites aldicarb sulfoxide or aldicarb sulfone; Car = carbofuran only or carbofuran and metabolite
3-hydroxycarbofuran; CFV = chlorfenvinphos; CPF = chlorpyrifos; M = methamidophos
41
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July 2015
Table 3a: Pesticides detected in samples (n = 11) from degraded avian carcasses (n = 4)
Species
Black Kite
Animals
sampled
(n)
1
Samples
(n)
3
Sample description
Pesticide
Residues
detected
(mg g -1)
Digestive tract (larynx, esophagus, trachea)
Aldicarb
50.25
Digestive tract (gizzard)
Talon (skin from)
Cinereous
Vulture
1
3
Black Kite
1
2
Egyptian
Vulture
1
3
0.04
Aldicarb
Aldicarb sulfoxide*
Aldicarb sulfone*
Organs
Pellet
Digestive tract (crop) + insects from carcass
Stomach contents
Oral cavity/contents = bait adhering to beak
Digestive tract (gizzard + proventriculus)
Tongue + oral cavity/contents
Digestive tract (larynx, esophagus, trachea)
*A metabolite of aldicarb
QUAL = qualitatively detected only, via thin layer chromatography
42
Chlorphenvinfos
Chlorpyrifos
Methamidophos
0.38
0.29
0.01
QUAL
QUAL
QUAL
2.03
2.96
QUAL
QUAL
6.57
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July 2015
Table 3b: Range of pesticide residues detected in samples (n = 10) from degraded mammal carcasses (n = 19)
Species
Samples
Cat, domestic
Animals
sampled
3
3
Stomach contents
Aldicarb
Aldicarb, Aldicarb sulfoxide
Dog, domestic
3
3
Stomach contents
Aldicarb
Aldicarb, Aldicarb sulfoxide
66
12, 3.6
6, 30
Cat, domestic
Dog, domestic
1
1
2
1
1
4
Stomach contents
Organs, pooled
Oral cavity/oral contents
Stomach contents
Stomach contents
Tongue
Insects from carcass
Organs, pooled
Methamidophos
Carbofuran
Carbofuran
1.87
0.34
QUAL
QUAL
118, 0.03
0.03, 0.01
QUAL
1.82
Red fox
3
7
Sample description
Stomach contents (2)
Tongues (2)
Tongue + oral contents
43
Pesticide
Carbofuran, 3-hydroxy
carbofuran
Carbofuran
Carbofuran, 3-hydroxy
carbofuran
Residues detected
(mg g -1)
54
0.32, 0.03
15, 7.2
5.28, 0.01
4.03, 0.04
0.34, 0.02
0.06, 0.03
0.94, 0.02
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July 2015
Table 4 compares the residue levels
detected in the tongues relative to
other samples retrieved from the
same carcass. Of the OPs and CMs
screened for, only carbofuran and its
3-hydroxy metabolite were detected
in mammalian (canid) tongue
samples. Compounds were never
only detected in the tongue rather
than in other samples taken from the
same carcass (but see results of the
Cinereous Vulture palate, below).
The residue levels of carbofuran
detected in tongue samples were
always the lowest relative to other
analyzed samples. However, we note
that levels of the 3-hydroxy
metabolite detected in the tongue
were sometimes similar to those
found in the stomach contents.
Table 4: Comparison of residue levels of carbofuran and methamidophos
detected in the tongue and other samples from the same carcass
Species
Animals
sampled
Pesticide
detected
Red fox
3
Carbofuran, 3hydroxy
carbofuran
Domestic
dog
Egyptian
Vulture
1
1
Methamidophos
44
Detected in
Tongue
Stomach contents
Residues
(mg kg-1)
0.34, 0.02
5.28, 0.01
Tongue
Insects from carcass
Stomach contents
0.06, 0.03
QUAL
4.03, 0.04
Tongue + oral contents
Organs
0.94, 0.02
1.82, 1.2
Tongue
0.03, 0.01
Stomach contents
Tongue + oral contents
Digestive tract (gizzard
+ proventriculus)
Digestive tract ((larynx,
esophagus, trachea)
118, 0.03
QUAL
QUAL
6.57
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July 2015
Analysis of the Cinereous vulture
palate
required for further investigation into
the circumstances surrounding the
vulture mortality event, and five
suspects
were
eventually
apprehended and charged. The
particulars of this case detailed in
Fajardo et al. (2014).
The analysis of this vulture palate
arose under separate circumstances.
The nine Griffon Vultures and one
Cinereous Vulture found dead
around a horse carcass in southern
Spain were recovered for analysis
(Fajardo et al. 2014). The carcass of
the Cinereous Vulture was analyzed
first, since the species is classified as
‘Near
Threatened’
(Birdlife
International 2015) and is therefore
accorded a higher degree of
protection than Griffon Vultures
(CMA 2001). Time since death was
estimated at between 15 and 20 days,
and the only parts of the Cinereous
vulture carcass initially deemed
viable for analysis – the mummified
organs - tested negative for any toxic
compound. Therefore, cause of death
was deemed ‘inconclusive’ at first.
However, after residues of the OP
chlorfenvinphos were detected in
two of the Griffon Vultures, the
Cinereous vulture carcass was reexamined, this time the palate was
removed for analysis (Figures 2a to
2f), and residues of chlorfenvinphos
(3.39 mg/kg) were detected therein.
The detection of residues in the
palate of this ‘Near Threatened’
species subsequently provided the
impetus and regulatory justification
Discussion
Tables 1a and 1b summarize the
range of weights recorded for avian
(0.1 – 5.98 g) and mammalian
tongues (0.35 – 9.71 g). Our results
indicate that the tongues of mammals
(in this case, canids) are likely better
suited for detecting OP and CM
pesticides than those of birds
because of their much greater surface
area, which provides increased
contact with residues and more
sample for single or repeat analysis.
However, we hasten to add that the
viability of the avian tongue may
also be species-dependent, since a
sufficient sample may be recovered
from larger birds like vultures (Table
1a). As such, this sample should be
considered for opportunistic analysis
in the absence of other samples. And,
when available, the avian tongue can
and should be pooled with
mouth/oral contents to improve
detection rates (as with the Egyptian
vulture carcass (Table 3a)). At the
CAD, we have on several occasions
45
Vulture News 68
July 2015
detected toxic compounds in the oral
cavity of birds. For example,
carbofuran was detected in bait
material retrieved from the mouth of
a Black Kite Milvus migrans (0.3
mg/kg) whose carcass was so
degraded that species identification
was virtually impossible (CAD,
unpublished report; Figure 3).
Figure 3: Degraded black kite Milvus migrans carcass with bait material in its
mouth
Stomach contents are often favoured
for toxicological analyses. Here, the
stomach contents were retrieved
from 22 of the 32 mammals and half
of these tested positive for an OP or
CM pesticide (Table 2, 3b). By
contrast, one stomach content sample
from the 28 avian recovered
carcasses was deemed in sufficiently
good condition for analysis – that of
a Black Kite – and in which 2.03 mg
kg-1 chlorpyrifos was detected (Table
3a). Interestingly, while the kite’s
tongue tested negative, residues
46
Vulture News 68
July 2015
(2.96 mg kg-1) were detected in the
mouth and oral contents (Table 3a).
Although based on a single
sample,
the
finding
of
chlorfenvinphos residues in the
palate of the Cinereous vulture is
promising and warrants pursuit in
suspected wildlife poisoning cases,
particularly when carcasses are
highly degraded, and when other
alternative and robust matrices such
as talons are either unavailable or
themselves in poor condition. The
palate
is
shielded
from
environmental conditions that might
degrade other parts of a carcass and
destroy pesticide residues therein.
Depletion of moisture during
desiccation likely concentrates any
residues present in the palate, and
since the OP and CM compounds in
question are highly toxic, a
confirmatory finding of exposure in
this sample provides conclusive
evidence of ingestion and is also
highly indicative that this led to the
animal’s death.
Generally, we suggest greater
consideration
of
oral
contents/palates/tongues
during
necropsy and toxicological analysis
of avian and mammal carcasses.
Further, we recommend collecting
and analysing the tongues of
mammalian scavengers that fall
victim to pesticide poisoning, (e.g.,
lion, hyena, and bear) regardless of
whether the carcass is degraded - to
evaluate the viability of this sample
in larger mammals than were
assessed in the present study. We
note that while avian tongues
recovered from degraded carcasses
may not be optimal samples,
opportunistic collection of tongues
from relatively fresh avian carcasses
in which poisoning is suspected
(especially in larger birds such as
vultures), followed by controlled
drying, may improve the viability of
the sample, which would be
beneficial in places with limited
means of keeping carcasses (and soft
tissues etc.) frozen, in addition to
general space constraints. In this
regard, the best option may be
simply to collect the head (and
talons/feet) for later analysis.
Finally, we strongly encourage
greater
analysis
of
oral
contents/tongues/palates for reasons
of utmost human safety. In several
African countries, pesticides may be
used to incapacitate or kill vultures
for ‘traditional medicine’ purposes or
‘muti’ (Mander et al. 2007, McKean
et al. 2013, Saidu & Buij 2013,
Ogada 2014, Ogada et al. 2015).
These vulture heads are then sold to
people for personal consumption,
and they are likely fresher than the
carcasses analyzed in the present
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Vulture News 68
July 2015
study. It would therefore be highly
relevant to examine vulture heads
offered for purchase at markets to
determine whether pesticide residues
are present, and to assess potential
risks for human health.
Questions about any of the
sampling and analytical procedures
are welcomed, and may be addressed
to the corresponding authors.
hard work and skill of poison
detection dog handler José Luis
Soria Marin, and the dogs
themselves: Cleo, Aura and Sabina,
who have each assisted in finding
some of the carcasses discussed in
this paper. Thanks also to all CAD
staff for their involvement and to the
personnel at LAB in Almería for
their prompt analysis of these
samples. We also thank David de la
Bodega of SEO Birdlife for
permission to include some relevant
details of the Cinereous Vulture case,
including the figures, from the book
he edited about the illegal use of
poisoned bats in Spain (see Fajardo
et al. 2014). Thanks to Andre Botha
for permission to use his photograph
of a poisoned vulture. The support of
Dr. Iñigo Fajardo, Dirección General
Gestion Medio Natural, Junta de
Andalucía,
is
gratefully
acknowledged
and
always
appreciated. This manuscript was
significantly improved by the
comments of Christina Davidson and
by one anonymous reviewer.
Acknowledgements
We extend sincere thanks to our
dedicated field personnel, especially:
Lieutenant José Antonio Alfaro
Moreno and Sergeant Francisco
Velasco Jiménez of SEPRONA de la
Guardia Civil in Huelva Province,
and Agent Lauren Infante, Medio
Ambiente. Their rigorous crime
scene
investigation,
meticulous
preservation of sample and carcass
integrity, and above all, their
unflinching
commitment
to
safeguarding both wildlife and
people from poisoning is to be
commended. We also recognize the
Key words: organophosphorus, carbamate, carbofuran, chlorfenvinphos,
chlorpyrifos, methamidophos, insecticide, pesticide, carcass, vulture, canid,
palate, tongue, mummification, autolysis, muti
48
Vulture News 68
July 2015
References
BirdLife International 2013. Aegypius monachus. The IUCN Red List of
Threatened Species. Version 2014.3. <www.iucnredlist.org>. Downloaded
on 30 May 2015.
Cazorla, R., Fernandez, J.L., Romero, R., Garrido, A. & Martínez, J.L. 2011.
Single solid phase extraction method for the simultaneous analysis of
polar and non-polar pesticides in urine samples by gas chromatography
and ultra high pressure liquid chromatography coupled to tandem mass
spectrometry. Talanta 85:183–196
Consejería de Medía Ambiente (CMA) 2001. Libro rojo de los vertebrados
amenazados de Andalucía. Sevilla: Consejería de Medio Ambiente, Junta
de Andalucía
Fajardo, I., Velasco, F. & Richards, N. 2015. Técnica forense y policía
científica (Forensic technique and pólice science). In: Manual de
Protección Legal de la Biodiversidad para los Agentes de la Autoridad
Ambiental en Andalucía (3rd Ed.); Fajardo, I., Martín, J., Ruiz, A. (eds);
Consejería de Medio Ambiente, Junta de Andalucía: Sevilla, Spain, 2015,
pp 318-363
Fajardo, I., Ruiz, A., Velasco, F., Zorrilla, I. & Richards, N.L. 2014. La
investigación en los casos de uso ilegal de veneno: procedimiento y
técnicas de investicación. Nuevos retos, nuevos métodos (Procedures and
techniques for investigating cases of illegal use of poison: responding to
new challenges with new methods). In: Bodega Zugasti D., de la (ed) Uso
ilegal de cebos envenenados. Investigación y análisis jurídico (Illegal use
of poisoned baits; Investigation and judicial analyses). SEO/BirdLifeProyecto Life + VENENO: Madrid, pp 55-85
Fajardo, I., Ruiz, A., Zorrilla, I., Valero, A., Fernandez, I., Saez, E., Molino,
F.M. & Olivares, J. 2012. Use of specialised canine units to detect
poisoned baits and recover forensic evidence in Andalucía (southern
Spain). In: Richards, N.L. (ed) Carbofuran and wildlife poisoning: global
perspectives and forensic approaches. John Wiley & Sons, Ltd.: United
Kingdom, pp 147-155
Mander, M., Diedrichs N., Ntuli L., Mavundla K., Williams V. & McKean S.
2007. Survey of the Trade in Vultures for the Traditional Health Industry
49
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July 2015
in South Africa. Report for Ezemvelo KZN Wildlife, Pietermaritzburg. 54
pp.
McKean, S., Mander, M., Diederichs, N., Ntuli, L., Mavundla, K., Williams,
V. & and Wakelin, J. 2013. The impact of traditional use on vultures in
South Africa. Vulture News 65: 15-36
Mineau, P., Porter, S. & Meteyer, C.U. 2012. Carbofuran: toxicity, diagnosing
poisoning and rehabilitation of poisoned birds. In: Richards, N.L. (ed)
Carbofuran and wildlife poisoning: global perspectives and forensic
approaches. John Wiley & Sons, Ltd.: United Kingdom, pp 19-38
Odino, M. 2012. Measuring the conservation threat to birds in Kenya from
deliberate pesticide poisoning: a case study of suspected carbofuran
poisoning using Furadan in Bunyala Rice Irrigation Scheme. In: Richards,
N.L. (ed) Carbofuran and wildlife poisoning: global perspectives and
forensic approaches. John Wiley & Sons, Ltd.: United Kingdom, pp 53-70
Ogada, D.L., Shaw, P., Beyers, R.L., Buij, R., Murn, C., Thiollay, J.M.,
Beale, C.M., Holdo, R.M., Pomeroy, D., Baker, N., Krüger, S.C., Botha,
A., Virani, M.Z., Monadjem, A. & Sinclair, R.E. 2015. Another
continental vulture crisis: Africa’s vultures collapsing toward extinction.
Conservation Letters doi: 10.1111/conl.12182.
Ogada, D. 2014. The power of poison: pesticide poisoning of Africa’s
wildlife. Annals of the New York Academy of Sciences 1322:1-20
Otieno, P., Lalah, J.O. & Virani, M.Z. 2012. Forensic analysis of carbofuran
in vultures and environmental samples collected from Laikipia and Isiolo
Districts. In: Richards, N.L. (ed) Carbofuran and wildlife poisoning:
global perspectives and forensic approaches. John Wiley & Sons, Ltd.:
United Kingdom, pp 77-81
Otieno, P.O., Lalah, J.O., Virani, M.Z., Jondiko, I.O. & Schramm, K.W. 2010.
Carbofuran and its toxic metabolites provide forensic evidence for
Furadan exposure in vultures Gyps africanus in Kenya. Bulletin of
Environmental Contamination & Toxicology 84: 536-544
Richards, N.L., Hall, S.W., Harrison, N.M., Gautam, L., Scott, K.S., Dowling,
G., Zorrilla, I. & Fajardo, I. 2014. Merging wildlife and environmental
monitoring approaches with forensic principles: Application of
unconventional and non-invasive sampling in eco-pharmacovigilance.
Journal of Forensic Research 5: 228 doi: 10.4172/2157-7145.1000228
50
Vulture News 68
July 2015
Saidu, J. & Buij, R. 2013. Traditional medicine trade in vulture parts in
northern Nigeria. Vulture News 65: 4-14
Vyas, N.B., Spann, J.W., Hulse, C.S., Bauer, W. & Olson, S. 2005. From the
field: Carbofuran detected on weathered raptor carcass feet. Wildlife
Society Bulletin 33:1178-1182
Vyas, N.B., Spann, J.W., Hulse, C.S., Torez, M., Williams, B.I., Leffel, R.
2003. Decomposed gosling feet provide evidence of insecticide exposure.
Environmental Monitoring & Assessment 98: 351-361.
Zoun, P.E.F. & Spierenburg, T.J. 1989. Determination of cholinesteraseinhibiting pesticides and some of their metabolites in cases of animal
poisoning using thin-layer chromatography. Journal of Chromatography
462: 448-453
******
51
Vulture News 68
July 2015
SHORT COMMUNICATIONS, NOTES AND
REPORTS
New record of African White-backed Vulture (Gyps
africanus) in Europe
A. Godino* & C. Machado
Centro de Estudos da Avifauna Ibérica, 7005-138, Évora, Portugal
*
Corresponding author: [email protected]
The African White-backed Vulture
(Gyps africanus) was the most
common vulture in Africa, with a
wide distribution along the entire
Sahel region, into East and Southern
Africa (IUCN, 2014). From the
beginning of 21st Century, this
species has exhibited declines across
much of its range, from 50% to 90%
in different regions (Nikolaus 2006,
Thiollay 2006, Virani et al., 2011,
Ogada et al. 2015). Due to this
situation, the global conservation
category of this vulture has been
decreased to Endangered (IUCN,
2014).
Outside the African range, in
Europe, few records exist of African
White-backed Vultures. The first
recorded observation of this species
in Europe was in October 2006, with
one bird photographed at the most
southwesterly point of Portugal, San
Vicente Cape (Jara et al. 2008).
After this first observation, three
more records have been collected on
the north side of Gibraltar Strait
(southern Spain): an immature,
possibly a 2nd year bird, in
September 2008; a 2nd year bird
killed by a wind turbine in June 2009
(Dies et al. 2011) and another
immature bird in September 2011
(Gutiérrez et al. 2013). More
recently, in May 2014, the first
observation of the species in North
Africa was recorded at Tetouan in
northern Morocco, on the southern
side of Gibraltar Strait (El Khamlichi
et al. 2014).
Here we report a new observation
of an African White-backed Vulture
in southeast Portugal, in the
protected
area
of
Moura/Mourão/Barrancos, close to
the Spanish border (N 38.2280, E
7.1570).
52
Vulture News 68
July 2015
On August 24th 2014, whilst at
the Biological Station of Garducho
(Mourão Council), we observed a
group of 70 Eurasian Griffons (Gyps
fulvus) landing at a cow carcass,
approximately 200 m from the
building.
During
initial
observations,
whilst using a telescope to search for
tagged birds, we noticed a vulture
that was clearly different to the other
vultures present. Closer observation
enabled
more
details
and
characteristics to be observed, and
these revealed a bird with a darker
face than the Eurasian Griffons in
addition to streaked chest feathers
with a narrow light area along the
centre of these feathers (Figure 1).
The vulture was also much smaller in
size compared to the other vultures
close to it (Figure 2). The age of this
African White-backed Vulture was
estimated as a 2-3 years (A. Botha
personal communication).
Figure 1: Gyps africanus photographed in Portugal
This new observation in SE Portugal
is the 5th record of this species in
Europe. It is also the most northerly
observation and the first outside the
53
Vulture News 68
July 2015
Gibraltar Strait and San Vicente
Cape areas, which are both in the
southern Iberian Peninsula.
These areas, and especially
because the Gibraltar Strait is the
most important bird migration
corridor in Western Europe (Zalles
& Bildstein 2000), have important
concentrations of vultures during
spring and autumn migrations. They
are also adjacent to the most
important breeding population of
vultures in the southern Iberian
Peninsula, with almost
2000
breeding pairs of Eurasian Griffons
(Garrido & Romero 2009).
Figure 2: Gyps africanus next to Gyps fulvus photographed in Portugal
observation of Rüppell’s Griffon in
Spain was in 1990 (Fernández 1998)
and in the subsequent decade, no
fewer than 23 observations have
been confirmed in Spain and
Portugal (Gutiérrez 2003). Since that
time, there has been a notable
Although the occurrence of African
White-backed Vultures in the Iberian
Peninsula is a relatively recent
situation, it is not new for other
typically African vulture species,
such as the Rüppell’s Griffon (Gyps
rueppellii). The first recorded
54
Vulture News 68
July 2015
increase in records of Rüppell’s
Griffon in the Iberian Peninsula, with
most of the observation around the
Gibraltar Strait area (De Juana 2006,
Gutiérrez et al. 2010). An
unsuccessful breeding attempt has
also been recorded in eastern central
Portugal (Costa et al. 2003), whilst
several records of this species exist
in southeast France in 2013 from a
bird that was wing-tagged in
Portugal (Godino & Machado 2013,
Godino & Machado in prep.).
Gutiérrez (2003) suggests that the
increasing number of Rüppell’s
Griffon sightings in Europe is due to
the
species
associating
with
increasing wintering population of
Eurasian Griffons in West Africa;
more than 5000 Eurasian Griffons
cross the Gibraltar Strait during
autumn migration (Camiña, 2004).
This migratory population comes
into contact in its wintering areas
with local Rüppell’s Griffon
populations (Roy 2005), and when
the Eurasian Griffons return to
Europe in the spring, some Rüppell’s
Griffons join them on this return.
The relatively recent and still few
observations of African Whitebacked Vultures in the Iberian
Peninsula could be a precursor of a
similar process. In both cases the
first records have occurred in the
same
geographical
area
(the
Gibraltar Strait) and during similar
periods – the end of summer and
early autumn (Jara et al. 2008, Dies
et al. 2011, Gutiérrez et al. 2013). In
this context, another raptor species,
the North African Long-Legged
Buzzard (Buteo rufinus cirtensis),
had a similar process in the past and
has been recently recorded breeding
in the Gibraltar Strait area in
southern Spain (Elorriaga & Muñoz,
2010).
Both Rüppell’s Griffon and
African
White-backed
Vulture
populations are in strong decline
across West Africa (Nikolaus, 2006;
Thiollay, 2006; IUCN, 2014, Ogada
et al. 2015), almost certainly in areas
where these populations come into
contact with wintering Eurasian
Griffons. However, in spite of these
population declines, the number of
Rüppell’s Griffons seen in the
Iberian Peninsula is increasing (De
Juana 2006, Gutiérrez et al. 2010).
These contrary situations indicate
that a range of factors is very likely
to be responsible, and it has been
suggested that the influence of global
climate
change
should
be
investigated (Ramírez et al. 2011).
With vulture populations, and in
particular the African White-backed
Vulture, undergoing declines in West
Africa, the new record reported here
could be an indicator of an
55
Vulture News 68
July 2015
increasing movement pattern into
Europe for this species, in the same
way as Rüppell’s Griffon. Due to the
critical situation of the African
White-backed Vulture, it is urgently
necessary to research the reasons of
this process, in particular the
evolution of vulture populations in
southwest Europe with movements
of African vultures into this region.
Acknowledgments
Special thanks to J. Elorriaga, D.
Forsman, R. El Khamlichi and A.
Botha for the comments and help
with the identification. Thanks also
to the Centro de Estudos da Avifauna
Ibérica (CEAI) to facilitate the
material for this observation and to
C. Murn for improving and
reviewing this note.
References
Camiña, A. 2004. Griffon Vulture Gyps fulvus monitoring in Spain: current
research and conservation projects. In Chancellor, R.D. & B.-U. Meyburg
(eds.). Raptors Worldwide. WWGBP/MME, Berlin.
Costa H, Bolton M, Matias R, Moore CC, Tomé R. 2003. Aves de ocorrência
rara ou accidental em Portugal. Relátorio do Comité Portugués de
Raridades referente aos anos de 1999, 2000 e 2001. Anuário Ornitológico
1:3-35.
De Juana, E. 2006. Aves raras de España. Lynx Edicions. Barcelona.
Dies, J.I., J.A. Lorenzo, R. Gutiérrez, E. García, G. Gorospe, J. Martí-Aledo,
P. Gutiérrez, C. Vidal, S. Sales y D. López-Velasco. 2011. Observaciones
de aves raras en España 2009. Ardeola 58:441-480.
El Khamlichi, R., K. El Haoua & M. Amezian. 2014. Gyps africanus: a new
specie
for
Morocco.
http://moroccanbirds.blogspot.com/2014_05_01_archive.html
Elorriaga, J. & Muñoz, A.R. 2010. First breeding record of North African
Long-legged Buzzard Buteo rufinus cirtensis in continental Europe.
British Birds 103:399-401.
Fernández y Fernández Arroyo, F.J. 1998. Observaciones de buitres africanos
en España. Rev. Fac. Ciencias de la UNED, Nº 1.
56
Vulture News 68
July 2015
Garrido, J.R. y F. Romero. 2009. El buitre leonado en Andalucía. In, J.C. del
Moral (Ed.). El buitre leonado en España. Población reproductora en 2008
y método de censo. SEO/BirdLife, Madrid.
Godino A. & Machado C. 2013. Grifo de Rüppell. Primeira marcaçao desta
espécie com placa alar em Portugal. http://naturlink.sapo.pt
Gutiérrez, R. 2003. Occurrence of Rüppell’s Griffon Vulture in Europe. Dutch
Birding 25:289-303.
Gutiérrez, R. Elorriaga, J. & Daly, S. 2010. How many Rüppell’s vultures do
we have in Spain? An attempt to photo-identify the birds in autumn 2010.
Retrieved from http://www.rarebirds.net/arbsi036.htm
Gutiérrez, R., J.A. Lorenzo, J. Elorriaga, G. Gorospe, D. López-Velasco, J.
Martí-Aledo, G. Rodriguez y S. Sales. 2013. Observaciones de aves raras
en España, 2011. Ardeola 60: 437-506.
IUCN. 2014. Red List of Threatened Species. Version
www.iucnredlist.org. Downloaded on 30 August 2014.
2014.2.
Jara. J., H. Costa, R. Matias, C.C. Moore, C. Noivo & R. Tipper. 2008.
Relatório do Comité Português de Raridades referente aos anos de 2006 e
2007. Anuário Ornitológico. Vol 6. Sociedade Portuguesa para o Estudo
das Aves.
Nikolaus, G. 2006. Commentary: where have the African vultures gone?
Vulture News:65-67.
Ogada, D. L., Shaw, P., Beyers, R. L., Buij, R., Murn, C., Thiollay, J-M.,
Beale, C. M., Holdo, R. M., Pomeroy, C., Baker, N., Krüger, S. C., Botha,
A., Virani, M. Z., Monadjem, A. & Sinclair, A. R. E. (2015). Another
continental vulture crisis: Africa’s vultures collapsing toward extinction.
Conservation Letters doi: 10.1111/conl.12182
Ramírez, J., A.R. Muñoz, A. Onrubia, A. de la Cruz, D. Cuenca, J.M.
González & G.M. Arroyo. 2011. Spring movements of Rüppell’s Vulture
Gyps rueppellii across the Strait of Gibraltar. Ostrich 82:71-73.
Roy, K. 2005. Sightings of European Griffon Vultures Gyps fulvus in eastern
Gambia from December 1999 to January 2005. Vulture News 53: 20-23.
57
Vulture News 68
July 2015
Thiollay, J-M. 2006. Several declines of large birds in the northern Sahel of
West Africa: a long-term assessment. Bird Conservation International 16:
353-365.
Virani, M., Kendall, C., Njoroge, P. & Thomsett, S. 2011. Major declines in
the abundance of vultures and other scavenging raptors in and around the
Masai Mara ecosystem, Kenya. Biological Conservation 144:746-752.
Zalles, J.L., and K.L. Bildstein. 2000. Raptor watch: A global directory of
raptor migration sites. Cambridge, UK. BirdLife International; Kempton,
PA: Hawk Mountain Sanctuary.
******
58
Vulture News 68
July 2015
Attempted Verreaux’s Eagle predation on Rüppell’s Vulture
and breeding observations at Lake Kwenia colony, Kenya
Simon Thomsett1* and James Aldrich
1
Ornithology Section. Dept of Zoology, National Museums of Kenya, Nairobi, Kenya
*
Corresponding author: [email protected]
Summary
A Verreaux’s Eagle (Aquila verreauxii) was observed to attack in mid-air a
fully grown juvenile Rüppell’s Vulture (Gyps rueppellii). This event including
observations on the breeding of these vultures at Kwenia are presented. Other
notes are given for the nesting of Rüppell’s Vultures at this site.
al. (1992) question if this behaviour
is recorded in Rüppell’s Vulture
(Gyps rueppellii).
Despite
observations
of
behaviour
between
Verreaux’s
Eagles and nesting Rüppell’s
Vultures in Kenya, Tanzania and
Ethiopia for some 30 years by one of
the authors (ST), the vocal intensity
described above was not recorded
despite hundreds of observed
interactions between the two species.
In contrast, Rüppell’s Vultures paid
little or no attention to Verreaux’s
Eagles even if they flew within 1020 metres of their young. Rarely, the
eagles did appear to have the intent
to predate chicks by looking directly
Introduction
The predation of Cape Vulture (Gyps
coprotheres) pulli by Verreaux’s
Eagle is well-known in South Africa
(Mundy et al. 1992, Gargett 1993).
These Verreaux’s Eagle individuals
or pairs patrol the Cape Vulture
breeding cliffs looking for unfledged
chicks and even eggs (although
unsuccessfully) on ledges. The Cape
Vultures are recorded as having a
“distinctive and hoarse call” when
Verreaux’s Eagles patrol in such a
manner and that “the uproar of these
griffons has to be heard to be
believed”. This is accompanied by
aggressive gesturing, and Mundy et
59
Vulture News 68
July 2015
at exposed chicks and banking round
to re-inspect the possibilities. Parent
Rüppell’s Vultures have been seen to
react by opening wings and
stretching out their heads (but with
minimal vocalisation) to very closeflying Verreaux’s Eagles, but these
events are characterised by their
rarity and lack of intensity despite
ample opportunity. The “distinctive”
call and anti-predator behaviour
shown by the Cape Vulture is
therefore not a distinct part of the
behavioural repertoire of Rüppell’s
Vulture. Another aspect possibly
influencing behavioural differences
is the close proximity of nests and
synchronous breeding of Cape
Vultures, as opposed to the generally
more widely-spaced nesting and
asynchronous breeding of the
equatorial nesting Rüppell’s Vulture
(Virani et al 2012). A group uproar
would be impossible with widely
spaced nests.
part of a long-term study site (Virani
et al. 2012), although in 2013 the
colony is threatened by intensive
agriculture and land developers
directly below the cliffs. Some of the
filming required nest-ledge camera
positions to film chicks and a crude
bird-hide was built halfway down the
cliff. From these vantage points we
were able to see into two nest ledges
with chicks and had a clear view of
nearly all roosting and nesting ledges
running 2km north and 2km south. In
over 10 years no attempted predation
by Verreaux’s Eagles has been
witnessed at Kwenia (ST, personal
observation) nor cited in publications
on this species (Mundy et al. 1992,
Virani et al. 2012).
During the 15 day intensive
observation, an adult pair of
Verreaux’s Eagles known to nest
4km south west of the colony would
visit the cliffs and were seen on at
least four occasions flying very close
to the nests. On 22/1/13, three
vultures were seen to react with
alarm at the very close proximity of
the eagle pair circling within 4m of
an occupied ledge. On 3/2/13 the
pair circled a ledge 20m directly
below, flying within 1-2m of adult
Rüppell’s Vultures with young.
Although the intent of the pair
seemed focussed on the ledge, no
vocalisations were heard. A juvenile
The Kwenia colony
Between 22/1/13 and 15/2/13, a BBC
film crew was camped on top of
Kwenia, the largest Rüppell’s
Vulture colony in southern Kenya,
filming a documentary on vultures.
The Kwenia colony numbers some
150-200 Rüppell’s Vultures, contains
approximately 64 nests and has been
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Vulture News 68
July 2015
1.5-2 year old female Verreaux’s
Eagle spent much time on these
cliffs, perched and flying near the
ledges throughout the 15 day period.
It appeared to be sufficiently far
from the adult pair’s nest but on at
least four occasions the eagle was
escorted away by the adult vulture
pair using a low intensity aggressive
pursuit. The sub-adult often sat like a
sentinel on outcrops overlooking
nesting ledges or made sorties to
circle and craned its neck at vulture
chicks in the nest with obvious intent
and interest in unattended vulture
chicks.
At that time there was a low
occupancy of nests with six young
ranging from 50-100 days and one
pair incubating. Significantly, these
chicks were not visible from the
ground even with the best optical and
photographic equipment and were
only detected after days of intense
observation from the hide placed
halfway down the cliff or by
climbing to nesting ledges. Methods
previously employed to survey this
cliff by the authors and colleagues
(Virani. et al 2012), could easily
have overlooked these nests from the
ground
survey.
For
absolute
accuracy this emphasises the need
for intense observation methods
coupled with close cliff ledge access
and/or distant multiday behavioural
observations if all nests are to be
enumerated. It is plausible that
optimum sites (well-shadowed and
discreet) are competed for and used
first, and that secondary sites get
occupied later when there is less
choice. This may explain the
difficulty in detecting active nests
when only a small number of birds
are nesting.
Description
predation
of
the
attempted
At 12PM on 14/2/13, JA was filming
halfway down the cliff and heard a
loud rushing and flapping sound
above. Upon turning three large birds
were seen tumbling to the ground
some 150m out from the cliff face.
Two hit the very steep scree some
110m below, followed immediately
by an adult Rüppell’s Vulture.
What followed was videoed some
five seconds after impact and is here
described. The dense tangle of
commifera made the video unusable
for the documentary, but it shows
that on impact with the ground the
eagle disengaged from the juvenile
vulture, which was seen on its back
and was 3m down a steep slope. 2m
away up slope was an adult
Rüppell’s Vulture, possibly the
parent. Immediately the eagle had
three Rock Hyrax (Procavia
61
Vulture News 68
July 2015
johnstoni) running away from it.
After four seconds the eagle turned
toward the juvenile vulture and
jumped onto it with both feet taking
it by the head. This rotated the
vulture onto its chest. A few seconds
later the adult vulture, itself
threatened by an attack, turned and
flew away, presumably accepting the
futility of its ability to protect the
young vulture. The eagle was on its
tibio-tarsal pads, wings partly spread
for balance with the vulture head
down out of sight under the sprawled
body, convulsively gripping the head
with its feet. For some 15 seconds
the vulture lay motionless except for
when the eagle made occasional
kneading clutches. The vulture was
apparently being suffocated, and had
only moments to live, when three
large Rock Hyrax appeared and
bounded toward the eagle. The eagle
was alarmed and left the vulture,
moving 4m down slope; it stayed for
five seconds before flying away. The
eagle may also have been wary of
the cameraman immediately above it
on the cliff. The vulture recovered
somewhat and after a minute tried to
move but rolled helplessly on its
back down slope, a broken wing
hindering its ability to right itself.
After five minutes the Verreaux’s
Eagle flew back overhead, mobbed
by a pair of Fork-tailed Drongos
(seen riding on its nape!). The eagle
perched on a tree immediately above
the vulture, where it was persistently
attacked by the Drongos. The eagle
was aware of the cameraman above
and this, plus the Drongos and the
defensive hyrax, combined to make
it fly away. The eagle remained
patrolling above. After some 30
minutes a troop of Olive Baboons
(Padio anubis) were seen moving
towards the scene in a deliberate and
curious manner.
A decision was made to rescue
the vulture as a stalemate had
occurred in which our presence was
influencing the outcome with an
increased probability of it being
found by baboons and killed. Given
that the species is Endangered, and
we could rescue it easily, a coordinated effort was made by local
Masai community members radioed
below, and by abseiling to the
ground. The vulture was found to
have a shattered humerus either from
impact by the eagle in the sky or
when it hit the ground. It had blood
coming out of the mouth and a small
but deep hole in the top of the skull.
The bird showed no downy tufts
on its flight or contour feathers. Its
worn tail tips with protruding unfeathered 2.5cm spines and the
presence of some abraded tips on
secondaries indicated that it had
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Vulture News 68
July 2015
The Verreaux’s Eagle continued
to survey the cliffs and if it indeed
specialised in taking chicks on
ledges or flying young vultures, its
impact would be very significant. It
was not seen to attempt any attack on
the numerous Rock Hyrax, Helmeted
Guineafowl (Numida meleagris) or
Kirk’s Dik Dik (Madoqua kirkii). It
could be able to entirely predate that
seasons’ young on the colony in a
matter of weeks. Perhaps in these
cases the trapping and translocation
of “problem eagles” is supported.
fledged at least a month or more
previously. The down on the head
was full and uniform indicating it
had not fed at carcasses. The bird
was taken for surgery by Sarah
Higgins to Dr Sangay Gautama’s
surgery in Nairobi to pin the left
humerus. It later developed poor coordination in the right leg that
worsened. After two months it
regained mobility in the leg and has
near complete function of the wing.
The partial paralysis and recovery
suggests a central nervous injury
(perhaps the puncture in the skull). It
began a contour moult in mid-2013
only five months later, with
secondaries moulted in August,
suggesting it may have been 4-5
months old when attacked and not a
very recently fledged bird.
Acknowledgments.
Charlie Hamilton James, Sarah
Higgins, Little Owl Sanctuary, Dr
Sangay Gautama, Amyn Khan, Titus
Kaii.
References
Gargett, V. 1993. The Black Eagle: Verreaux’s Eagle in Southern Africa.
Academic Press, London.
Mundy, P., Butchard, D., Ledger, L., Piper, S. 1992. The Vultures of Africa.
Acorn Books and Russel Friedman Books in association with the Vulture
Study Group, Johannesburg.
Virani. M, Monadjem. A, Thomsett.S and Kendall. C. 2012. Seasonal
variation in breeding Rüppell’s Vultures Gyps rueppellii at Kwenia,
southern Kenya and implications for conservation. Bird Conservation
International 22: 260–269.
******
63
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July 2015
IUCN SPECIES SURVIVAL COMMISSION:
VULTURE SPECIALIST GROUP
Aim
The IUCN SSC Vulture Specialist Group aims to advocate and create greater
awareness of the plight of vultures and coordinate effective conservation
activities to their benefit.
The Vulture Specialist Group will support and work closely with BirdLife
International as the Red List Authority for birds, but with particular reference
to the global status of Vultures.
Key activities/Outputs:
Conservation and management
- Identify and communicate information about emerging threats to
vultures globally
- Promote the use of appropriate mitigation measures to address threats
where possible
- Facilitate the sharing of expertise and knowledge between regions
where appropriate
- Support CITES, at national and international level, in vulture-related
issues
Research and monitoring
- Conduct and promote scientific research on ecology and habitat use
by vultures to support management decisions regarding the
conservation of these
- Promote and encourage sustained population monitoring at key sites
for vultures using appropriate monitoring methods
- Identify gaps in knowledge and promote applied research into such
species, threats or habitats where appropriate
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Dissemination and Communication
- Promote and facilitate the exchange of knowledge and expertise with
regard to vultures and their conservation
- Use Vulture News as the official print journal for the Vulture
Specialist Group to disseminate information about vultures and their
conservation
- Make available published and unpublished information about
vultures on a website
- Ensure that the wider public and interest groups receive regular
information and updates on the conservation of vultures
Partnership and Advocacy
- Work with governments, research institutions, conservation
organisations and communities to develop and implement effective
conservation measures
- Support and promote the conservation of vultures through the
International Vulture Awareness Day working with its partner
organisations
For more details contact either of the Vulture Specialist Group Co-chairs:
Chris Bowden
[email protected]
André Botha
[email protected]
African Regional Co-chairs: Munir Virani, Kariuki N’danganga
European Regional Co-chairs: Alvaro Camiña, José Tavares
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Summary updates April 2015 for vultures and VSG activities
The 6th September 2014 saw the
celebration of the 6th International
Vulture Awareness Day with 28
countries and 160 organisations
registering on the event’s website
www.vultureday.org and working
towards creating greater awareness
of these birds and the challenges they
face. More details on activities of the
individual partners can be found on
the website.
The second meeting of the CMS
Raptors MoU Technical Advisory
Group took place in Abu Dhabi,
U.A.E. from 16th-19th March 2015.
Most
significantly,
a
special
Working Group was established for
the conservation of vultures across
the Africa-Eurasian flyway. It will
focus on coordinating and promoting
the
conservation,
monitoring,
research and awareness-raising. A
particular objective of the group was
to forge closer working ties with the
IUCN SSC VSG and its members.
– they confirm that veterinary
diclofenac represents a real risk to
European vultures, and therefore that
a number of risk management
measures should be taken to avoid
the poisoning of vultures, including
more regulation, veterinary controls,
better labelling and information
and/or a ban of the drug. The
EMA´s remit and position recognises
that only a ban reduces the risks to
zero, but it is now up to the EU
Commission to decide whether they
will start a formal referral process
and it seems likely that action may
only come after dead vultures are
found in the field conclusively
poisoned by diclofenac. Veterinary
diclofenac is already approved for
sale in five EU countries, including
Italy and crucially Spain, which
holds 90% of all European vultures.
It is marketed by the Italian company
FATRO, which used loopholes in the
EU risk assessment guidelines for
veterinary drugs to get it approved in
Italy and Spain, in spite of the solid
body of evidence about its impacts
on vultures and other wildlife. The
Spanish Govt. also held a meeting
with Local Govt. and conservation
community experts, which resulted
in a detailed internal report that
concluded that risks are lower than in
Diclofenac in Europe
As requested by the European
Commission,
the
European
Medicines
Agency
(EMA)
published
their
long-awaited
technical position on the vulturekilling drug diclofenac in December
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Asia and that the EMA position
should be adhered to. Diclofenac
already caused catastrophic declines
of three resident South Asian vulture
species, including 99.9% decline of
Gyps bengalensis previously thought
to be the most abundant large raptor
in the world. See #banvetdiclofenac!
www.4vultures.org
and
www.birdlife.org for updates etc.
(Note VSG prompted high level
letters from IUCN’s SSC to EU
Commissioners highlighting this
topic)
A national action planning
workshop took place in Harare,
Zimbabwe on the 26th and 27th
March 2015. Earlier in 2014
(March), based on a review of
various documents the BirdLife
Africa Partnership Secretariat, a draft
“Action framework for vultures in
Africa” was shared and since then 14
African national BirdLife Partners
have indicated that vultures are part
of their planned activities and
priorities,
reflecting
growing
international awareness and concern
for Africa’s vultures and growing
momentum for addressing this. At
the CMS meeting, plans for a second
Pan African Vulture Summit were
put forward which will hopefully
take place in Senegal Oct 2016
linked to the Pan
African
Ornithological Congress.
Windfarms
A major increase in windfarm
proposals is underway particularly
across Asia, Africa and the Middle
East which is likely to affect vulture
populations. There is an immediate
need to refine the pre- and postconstruction impact studies to
minimise the potential effects on
vultures from wind farms.
Asia
The SAVE consortium met in
Dhaka, Bangladesh in November
2014, updating the new ‘Blueprint’
Recovery Plan document. The report
with updated priorities and version
of the Blueprint is available under
latest news: www.save-vultures.org
The meeting was notable in that the
Chief Guest, Bangladesh Finance
Minister endorsed SAVE priorities,
and most notably the banning of
Africa
A Workshop about vultures in South
Africa took place on 6th-7th Nov
2014 at VulPro facilities near
Pretoria. There was also a workshop
for the Bearded Vulture South
African group.
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ketoprofen. The first Vulture Safe
Zone in Bangladesh was also
formally recognised by Government
at the meeting.
In India, the eagerly awaited ban
of multi-dose vials of human
diclofenac is apparently close but has
not yet come through. The need for
vulture safety-testing of all similar
(NSAID) veterinary products is also
something that has become top
priority and final approval/funding
from the Indian Government is
eagerly awaited.
******
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RECENT LITERATURE
P.J. Mundy
AL BULUSHI, A., AL HARTHI, S., AL FARSI, G., AL ARAIMI, J. & AL
HUMAIDI, J. (2013). Apparent increases in Egyptian vulture populations
in the Sultanate of Oman. Phoenix 29: 15 - 17.
An estimated 65-80 pairs on Masirah Island, but with a productivity of
only 0.46 fledglings per pair. At a new dump site in northern Oman, 238
vultures (incl. 188 adults) were counted on 9 October 2012.
(email: [email protected])
ALLAN, D. (2013). Cape Vulture. Apocalypse now? African Birdlife 1 (2):
58-59.
Red listed as Vulnerable by the IUCN, it faces a great array of threats –
poisoning first, then electrocutions by and collisions with powerlines,
wind farms, drowning, disturbance, and food shortage. “The day of
reckoning may well be upon [it]”.
CHAUDHRY, M.J.I., OGADA, D.L., MALIK, R.N., VIRANI, M. Z. &
GIOVANNI, M.D. (2012). First evidence that populations of the critically
endangered Long-billed Vulture Gyps indicus in Pakistan have increased
following the ban of the toxic veterinary drug diclofenac in south Asia.
Bird Conservation International 22: 389-397.
A colony in SE Pakistan (Karunjhar Hills), neighbouring the Rann of
Kutch of India, was monitored before (2003-2006) and after (2007-2012)
the subcontinental ban on diclofenac in 2006. All parameters declined
steeply to 2007, then increased markedly in 2008 and thereafter remained
the same.
(email for M.Z. Virani: [email protected])
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CHOMBA, C. & M’SIMUKO, E. (2013). Nesting patterns of raptors; White
backed vulture (Gyps africanus) and African Fish Eagle (Haliaeetus
vocifer), in Lochinvar National Park on the kafue [sic] flats, Zambia.
Open Journal of Ecology 3: 325-330.
Eight occupied nests of the vulture were found (and five for the eagle).
Most were on Faidherbia albida, at an average height of 16.6 metres, and
in woodland communities. Abandoned nests were within 100m of human
disturbance. (This article is poorly edited, does not refer to previous
literature, and the two photos are taken from Incarta, and the eagle is an
American Bald Eagle!).
(email : [email protected])
DEMEY, R. (ed.) (2013). Recent reports. Bulletin African Bird Club 20 (1):
92 -108.
(p. 98) Ruppell’s Griffons were photographed in the Mole National Park,
Ghana, by David Hoddinott on 18 December 2012; the photo is included
(all three birds are RGs). (p.100) An immature Cinereous Vulture was
seen on passage with Eurasian Griffons over Meknes, Morocco, on 14
November 2012 by J. Franchimont. (p. 105) An immature Hooded Vulture
(Empangeni) and three Lappet-faced Vultures (Winterton) were seen in
KwaZulu-Natal, South Africa, in August and July respectively, out of
normal range.
(email: [email protected])
FINLAYSON, C., BROWN, K., et al. (2012). Birds of a feather: Neanderthal
exploitation of raptors and corvids. PloS ONE 7(9): e45927.
The dark/black remiges of all four species of vulture in Europe (and also
perhaps Gyps melitensis) feature in Palaeolithic sites of Neanderthal
humans, along with other species of birds. It’s clear that the pre-modern
humans used the feathers as personal ornaments in symbolic behaviour.
(email: [email protected])
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FISHER, I. (2013). Vultures are starting to soar again. Birds (RSPB
magazine) 25(5): 2-3.
A brief note of optimism on the situation in the Indian subcontinent. With
four photos of Oriental White backed Vulture. But wait … “other
veterinary drugs may have a similar effect …”
(email: [email protected])
GUTIÉRREZ, R., LORENZO, J.A., et al. (2012). Observaciones de aves
raras en Espaňa, 2010. Ardeola 59: 372-373.
Up to and including 2010, there have been 45 sightings of 60 individuals
of Rüppell’s Griffon in the Iberian peninsula, validated by the rarities
committee.
(email: [email protected])
MUNDY, P.J. (2013). Out of Africa? Some notes on Arabian vultures.
Phoenix 29: 6-7.
The subspecies of the Bearded Vulture is considered to be the nominate
barbatus, Rüppell’s Griffon is considered to have occurred, a photo of the
Lappet-faced Vulture is of the negevensis subspecies, and the Egyptian
Vulture occurs as the nominate percnopterus subspecies
(email: [email protected])
MURN, C. (2012). Field identification of individual White-headed Vultures
Trigonoceps occipitalis using plumage patterns - an information theoretic
approach. Bird Study 59: 515-521.
Thirty wild birds (ages not stated) were photographed from the side to
highlight the upper median wing coverts. The pattern of these differed
from left to right on the same bird, but each bird (adults?) had a unique
pattern. The variations enable birds to be individually identified.
(email: [email protected])
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MURN, C., COMBRINK, L., RONALDSON, G. S., THOMPSON, C. &
BOTHA, A. (2013). Population estimates of three vulture species in
Kruger National Park, South Africa. Ostrich 84: 1-9.
A T-square plotless density estimator was the method used, calibrated by
aerial survey counts. Across the whole park, White-backed Vultures were
estimated at 904 pairs (95% C.I. ±162), the Lappet-faced Vulture at 78
pairs (±18), and the White-headed Vulture at 60 pairs (± 13).
(email: [email protected])
PHIPPS, W. L., WILLIS, S. G., WOLTER, K. & NAIDOO, V. (2013).
Foraging ranges of immature African white-backed vultures (Gyps
africanus ) and their use of protected areas in southern Africa. PLoS ONE
8(1): e52813. 11pp.
Using GPS-GSM units on six birds, and tracking them for up to 313 days.
Distances travelled averaged 22-49 km per day, but the maximum in one
day was 267 km. Average and maximum flight speeds were 51 and 107
km/h respectively. Average foraging range covered was 269 000 km2.
Protected areas were infrequently visited. Two birds visited ‘restaurants’
regularly.
(email: [email protected])
PORTER, R.F. & SULEIMAN, A.S. (2012). The Egyptian Vulture Neophron
percnopterus on Socotra, Yemen: population, ecology, conservation, and
ethno-ornithology. Sandgrouse 34: 44-62.
A fascinating and well-documented introduction to the Egyptian Vulture
of the island of Socotra (area: 3579 km2). An estimate of 1900 birds (incl.
800 pairs) was produced, which is of global significance. The vultures are
not persecuted, trapped or poisoned by the locals, who “like them”.
(email: [email protected])
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PRAKASH, V., BISHWAKARMA, M.C., et al. (2012). The population
decline of Gyps vultures in India and Nepal has slowed since veterinary
use of diclofenac was banned. PLoS ONE 7 (11): e49118. 10 pp.
Road strip counts since 1991 were used. By 2007, the Oriental Whitebacked Vulture had declined in India by 99.9%, and the Long-billed
Griffon and Slender-billed Vulture (combined) by 96.8%. Use of
diclofenac was banned in 2006; by means of much mathematics and
statistics, the decline is seen to have slowed by 2011 and may even have
reversed!
(email: [email protected])
SHOBRAK, M. (2012). The decline of the Griffon Vulture in Saudi Arabia.
Phoenix 28: 7-8.
At seven sites in SW Saudi Arabia there were 45 nests in 1999. By 2010,
only five nests were seen at one site. Probably several factors have caused
this decline.
(email: [email protected])
THERON, N. (2013). New IBA for Cape Vulture. IBA Newsletter [Birdlife
South Africa] 3: 7.
Surveys in the north-eastern regions of the Eastern Cape revealed approx.
800 pairs of Cape Griffons. A new IBA for the species has been proposed
here.
(email: [email protected])
******
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The production and printing of this issue of Vulture News was sponsored by
Sasol.
Sasol - adding protection to natural life
Sasol is passionately involved in numerous environmental and conservation
projects in South Africa and has integrated the concept and pursuit of
sustainable development into its business values.
The group supports endangered species such as wild dogs and vultures and
sponsors a series of books on flora and fauna as well as bird-call recordings. It
has also invested in community bird watching facilities and wildlife
conservation programmes.
At the Sasol Wild Dog Camp at the De Wildt Research Station near Brits in
the North-West, the group sponsors the quarantine facilities and shares an
interest in the reintroduction of captive-bred wild dogs into national
conservation parks.
Sasol also supports several projects for the treatment and rehabilitation of
traumatised wild animals and birds, funds school level environmental
education programmes, and is involved in nature conservation at community
level, such as the establishment of game conservancies adjacent to the Sasol
factories at Secunda and Sasolburg.
Another significant initiative is Sasol Sensory Trail at Delta Park in
Johannesburg which was especially conceived to enable people with
disabilities to enjoy the environment.
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