vulture news journal

Vulture News 68 July 2015

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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 32

Ngaio L. Richards, Irene Zorrilla, Isabel Fernandez, Mónica Calvino,

Joaquin Garcia and Antonio Ruiz


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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 64

Summary updates April 2015 for vultures and VSG activities 66

RECENT LITERATURE 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)


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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

Introduction

Populations of three old world

vulture species, Gyps bengalensis,

Gyps tenuirostris and Gyps indicus

collapsed across the Indian

Subcontinent (Prakash et al. 2012).

These population declines were

attributed to the use of a nonsteroidal

anti-inflammatory drug, diclofenac,

that causes visceral gout

subsequently leading to renal failure

in vultures that consume carcasses

contaminated with the drug (Green et

al. 2004, Oaks et al. 2004, Naidoo et

al. 2009). This situation raised

concerns about their lesser-known

relatives and the survival of vultures

has cultural as well as ecological

implications. Despite extensive

studies on these three species, little is

known about population trends in

highland areas, particularly in China,

where there have been few studies of

the large carrion-eating raptors.

Currently, there is little information

available regarding the use of

veterinary diclofenac for livestock in

western China, and little is known

about populations and dynamics of

vultures in China overall (Pain et al.

2003, Lu et al. 2009, Ma et al.


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2013). Therefore, in this paper we

want to introduce background

information regarding vultures and

their protection status in China.

Vultures include 16 living

species that occur on the Old World.

However, in China there are more

vultures species than most other

countries (eight species), accounting

for 50% of vulture species in the Old

World. They are 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), Slender-

billed Vulture (Gyps tenuirostris)

and Egyptian Vulture (Neophron

percnopterus) respectively (Zhang &

Yang 1980, Gu et al. 1994, Zheng

2011, Guo and Ma 2012). The

species have an extensive

geographical distribution, centred on

the northwest, the Tibetan plateau,

Pamir plateau and the southwest

minority areas in China. Meanwhile,

the Tibetan plateau has been

regarded as the kingdom of vultures

(Di 2003), because there are more

than seven Old World Vulture

species distributed there (Ma et al.

2014). At the same time, nearly 28

million people live on the Tibetan

Plateau. Some vultures depend

predominantly on livestock carcasses

as food resources and this highlights

their ecological importance in the

highland ecosystem. Meanwhile,

human corpses also provide a small

fraction of the total food resource to

vultures, so the vultures play a

unique role in the centuries-old sky

burial tradition followed by Tibetan

people. In short, vultures have not

only ecological but also cultural

value. Therefore, extra attention

should be directed at the

conservation of these scavenging

species.

Distribution and Population of

Vultures in China

The vultures of China have received

great attention from the government.

The dramatic population crashes of

three species of Gyps vulture in the

south Asia was a good example and


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urged China to take some measures

to protect these species. In 1988, the

Law of the People’s Republic of

China on the Protection of Wildlife

established two categories of

nationally protected wild animals,

and most species in these two

categories are rare and threatened. In

2001, the State Forestry

Administration announced an

additional list of nationally protected

species that are either beneficial or

with important economic or

scientific value. This list covered an

additional 707 species of birds,

including many that are common and

widespread in China. In addition to

the nationally protected species,

many provinces have published lists

of locally protected wildlife.

Under these laws, there is some

effective protection for the listed

wildlife. For example, in August

2002, the defendants Li Yuesheng,

Li Congrong and Li Ziqi caught 26

Himalayan Griffons in a nature

reserve of Yunnan Province, and all

the vultures died in the end, so they

were sentenced to 10 years, 12 years

and 13 years respectively and fined

by the court according to the wild

animal conservation law. On May

20, 2013, Lei was arrested for

mailing a Cinereous Vulture skeleton

illegally, and was sentenced by the

court.

Despite protection efforts such as

these, most vulture populations are

still in a downward trend over recent

years. Table 1 presents data on eight

vulture species in China and the

world, summarised from government

websites, the State Forestry

Administration, BirdLife

International and the IUCN Red List

of Threatened Species.

Based on recent investigations

(Ma 2011), only three vultures are

common in China: Gyps

himalayensis, Gypaetus barbatus,

and Aegypius monachus. The

numbers of other vulture species,

such as Egyptian Vulture and

Slender-billed Vulture, are small and

mostly only recorded one to three

times in the past 50 years. According

to data released by the State Forestry

Administration in 2009, the

population size of the Bearded

Vulture was estimated at 92,000


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individuals in China (e.g. 22,018 in

Xinjiang, 32,500 in Qinghai, 29,126

in Gansu, 7,500 in Xizang [Tibet],

800 in Sichuan, 54 in other parts of

China) (National Forestry Bureau

2009). However, this species breeds

at low densities in other parts of its

range and in some other countries

there are only 200-300 pairs in total.

Furthermore, the global population

of the Bearded Vulture is estimated

to be less than 10,000 individuals.

Therefore, there is some doubt over

the accuracy of data provided by the

Chinese Forestry Bureau about the

population size of the Bearded

Vulture; as a result, we re-calculated

the population estimate again. Based

on population data and the

distribution area described by

BirdLife (2014) and the IUCN Red

List, we estimated the number of the

eight vulture species in China

according to their distribution and

population size in the world (Table

1). The eight vulture species

distributed in China are mainly in the

western regions of the country (Xu

1995, Ma 2011, Zheng 2011). Figure

1 shows the distribution of these

species and highlights that most

species are centered on the Tibetan

Plateau. Ranges also extend into the

southwest, northwest, Inner

Mongolia (Kenny et al. 2008) and

the Himalaya.


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Table 1: Summary of status, numbers, distribution of Old World Vultures and key threats to vultures in China

Species Distribution

(summary)

Global

population

(individuals)

Global

distribution

(km2)

Current

trend

Red List

Status*

Bearded Vulture

(Gypaetus barbatus)

Bhutan, China, India, Mongolia, Pakistan,

Russia, Central Asia, Middle East, Europe,

North East and East Africa

2,000-10,000 8,840,000 Decreasing LC

White-rumped Vulture

(Gyps bengalensis)

Bangladesh, Bhutan, China, India, Myanmar,

Pakistan, South-East Asia

3,500-15,000 4,920,000 Decreasing CR

Himalayan Griffon

(Gyps himalayensis)

Bhutan, China, India, Pakistan, South-East

Asia, Central Asia

100,000-

499,999

3,100,000 Stable LC

Eurasian Griffon

(Gyps fulvus)

Central Asia, Europe, North Africa, Turkey,

China

40,000-50,000 10,200,000 Increasing LC

Cinereous Vulture

(Aegypius monachus)

Bhutan, China, India, Myanmar, Pakistan,

Mongolia, East Asia, Central Asia, Middle

East, Europe

21,000-30,000 13,700,000 Decreasing NT

Red-headed Vulture

(Sarcogyps calvus)

Bangladesh, Bhutan, Cambodia, China, India,

Laos, Malaysia, Myanmar, Pakistan, Thailand,

Vietnam

3,500-15,000 3,690,000 Decreasing CR

Slender-billed Vulture

(Gyps tenuirostris)

Bangladesh, India, Myanmar, South-East Asia 1,500-3,750 847,000 Decreasing NT

Egyptian Vulture

(Neophron

percnopterus)

India, Pakistan, China, Central Asia, Africa,

Europe (more southerly countries), Middle East

20,000-61,000 18,700,000 Decreasing EN

* 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.


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Table 1: continued. Species List in

China

Distribution in China

Est. China

population

Chief threats Research needs

Bearded

Vulture

Ⅰ

Shanxi, Inner Mongolia, Tibet,

Xinjiang, Qinghai, Ningxia, NW

Yunnan, Western Sichuan, Hubei,

Hebei, Shaanxi

6,900-

9,900

Poisoning, persecution,

habitat loss, disturbance,

power lines, windfarms,

lack of safe food

Monitoring population, food

habits, breeding ecology

White-rumped

Vulture Ⅰ

The western and SW of Yunnan 100-200 NSAID poisoning, lack of

safe food

NSAIDs, monitoring

population, breeding

Himalayan

Griffon

Ⅱ

Xinjiang, Gansu, Qinghai, Tibet,

Ningxia, Sichuan, Western Yunnan

90,000-

230,000

NSAID poisoning, lack of

safe food

NSAIDs, monitoring

population, food habits,

breeding

Eurasian

Griffon Ⅱ Western Xinjiang, SE Tibet 100-300 Persecution, poisoning, lack

of safe food, power lines


habits, breeding

Cinereous

Vulture

Ⅱ

Xinjiang, Qinghai, Gansu, Ningxia,

Mongolia, Shanxi, Sichuan.

Tibet, SE China, Taiwan

9,000-

15,000

Disturbance, lack of safe

food, poisoning, secondary

poisoning (NSAIDs)

NSAIDs, monitoring


breeding

Red-headed

Vulture

Ⅱ

SW Yunnan, SE Tibet

100-300

Persecution, secondary

poisoning, lack of safe food,

intensification of agriculture

NSAIDs, monitoring


breeding

Slender-billed

Vulture

Ⅱ

SE Tibet

20-100

NSAID poisoning, lack of

safe food

NSAIDs, monitoring


breeding

Egyptian

Vulture

Ⅱ

Western Xinjiang

20-100

Disturbance, poisoning,

electrocution, food

availability


habits, breeding


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Figure 1: Distribution maps of the eight vulture species in China

Bearded Vulture White-rumped Vulture

(Gypaetus barbatus) (Gyps bengalensis)

Himalayan Griffon Eurasian Griffon

(Gyps himalayensis) (Gyps fulvus)

Cinereous Vulture Red-headed Vulture

(Aegypius monachus) (Sarcogyps calvus)


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Slender-billed Vulture Egyptian Vulture

(Gyps tenuirostris) (Neophron percnopterus)

Figure 1: Distribution maps of the eight vulture species in China

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

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).


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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.


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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

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.

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


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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.

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

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).

Figure 4: The wind power station in west China

3. Specimen making and trading.

People have found that vultures have

a special form and a high ornamental

value since the 1990s. Vulture

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,

app:ds:negative%20effects

app:ds:negative%20effects


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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

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

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.


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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).

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


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5. Demand by zoos.

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

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.

Figure 7: These Cinereous Vultures were caught for sport or entertainment


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Figure 8: Himalayan Griffons and Cinereous Vultures in Ningbo Zoo

6. Medicinal value.

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

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.


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Figure 9: The bones from a Cinereous Vulture for sale in a shop

7. Illegal hunting.

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

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.


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Figure 10: Rescued injured Cinereous Vulture

Figure 11: Cinereous Vulture for sale in Yibin


20

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

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.

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,


21

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

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******


25

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

1Denver Zoological Foundation, E. 2300 Steele St, Denver, Colorado 80205, USA.

2Raptors Botswana, Box Hak 33, Maun, Botswana, Africa.



Introduction

Currently vulture populations in sub-

Saharan 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,

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


26

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.

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

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.

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


27

≥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.

Figure 1: Percentage of 477 White-backed Vultures (WbV, Gyps africanus)

with different blood lead levels (BLL) for in Botswana.

69.18%

28.51%

2.31%

0%

10%

20%

30%

40%

50%

60%

70%

80%

<10 µg/dl 10 to <45 µg/dl >45 µg/dl

BLL categories

(n = 330)

(n = 136)

(n = 11)


28

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

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 sub-

Saharan 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


29

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.

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752.

******


32

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 Zorrilla

2, Isabel Fernandez

2, Mónica Calvino

2,

Joaquin Garcia2, Antonio Ruiz

3

1Working Dogs for Conservation, 52 Eustis Road, Three Forks, Montana 59752, USA.

2Environmental 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.

3Environmental 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.


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,


33

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.


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

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


34

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 - (2-

isopropyl-6-methyl-4-pyrimidinyl)

phosphorothioate); residues were

subsequently detected in their feet

after these were removed and


35

weathered for seven days (Vyas et

al. 2003). Similarly, eastern Screech-

owls Megascops asio were exposed

to baits laced with CM carbofuran

(2,3 - dihydro-2,2-dimethyl-7-

benzofuranyl 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 (3-

ketocarbofuran and 3-

hydroxycarbofuran) were also

identified in the highly weathered

talons and beak of an African White-

backed 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.


36

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

protocols (as detailed in Fajardo et

al. 2015), during routine

investigations under the Andalusian

government’s anti-

poisoning/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.

Table 1a: Summary of degraded bird carcasses (n = 28) recovered by species and

weights of tongue samples recovered (n = 20)

Species Carcasses Tongues

sampled

Tongue weights

(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

3 2 0.69, 1.01

Vulture, Griffon Gyps fulvus 3 3 3.48 - 5.98

TOTALS

28

20


37

Table 1b: Summary of degraded mammalian carcasses (n = 32) recovered by species

and weights of tongue samples recovered (n = 24)

Species Carcasses Tongues

sampled

Tongue

weights

(g)

Badger, Eurasian Meles meles 1 1 5.0

Cat, domestic Felis catus 7 6 2.52 – 5.66

Dog, domestic Canis lupus

familiaris

10 9 4.2 – 7.19

Fox, Red, European Vulpes vulpes

crucigera

9 4 0.52 – 9.71

Genet, Common Genetta genetta 1 1 4.72

Hare, Iberian Lepus granatensis 1 1 5.4

Polecat, European Mustela

putorius

1 1 0.55

Rabbit, European Oryctolagus

cuniculus

1 1 2.07

Weasel, Least Mustela nivalis 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).


38

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).


39

Sample preparation and analysis for

pesticide residues

Sample preparation, pesticides

residue extraction and multi-

screening 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 R-

200). 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

(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 GC-

detectible 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 LC-

detectible 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).

Results

Sixty carcasses were recovered for

this preliminary study: 28 avian

carcasses spanning 15 species

(including three Egyptian Vultures

Neophron percnopterus, three


40

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).

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

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.


41

Table 2: Summary of all samples (n = 151) collected from avian carcasses (n = 28) and mammal carcasses (n = 32)

Sample type Avian Positive (key to abbreviations

below)

Mammal Positive

Insects recovered from carcasses 3 0 4 1: Cara

Digestive tractb,* 20 4: A(2), M(1,1a) 2 0

Feather 1 0 N/A N/A

Liver 0 0 1 0

Oral cavity/content 1 1: CPF 2 1: Cara

Organs, pooledc,* 12 1: CFVa 8 2: Car

Pellet 2 1: CFVa N/A N/A

Stomach contents 1 1: CPF 22 11: A (6), Car (4 (1a)), M (1)

Talons/material held inside 4 1: A N/A N/A

Tongue only 20 0 24 3: Car

Tongue + oral contents 6 1 Ma 6 1: Car

Tongue + various pooled samplesd 2 0 2 0

Various pooled samplese,f,* 6 1: CFVa,g 2 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


42

Table 3a: Pesticides detected in samples (n = 11) from degraded avian carcasses (n = 4)

Species

Animals

sampled

(n)

Samples

(n)

Sample description

Pesticide

Residues

detected

(mg g -1)

Black Kite

1

3

Digestive tract (larynx, esophagus, trachea)

Digestive tract (gizzard)

Talon (skin from)

Aldicarb

Aldicarb

Aldicarb sulfoxide*

Aldicarb sulfone*

50.25

0.04

0.38

0.29

0.01

Cinereous

Vulture

1 3 Organs

Pellet

Digestive tract (crop) + insects from carcass

Chlorphenvinfos

QUAL

QUAL

QUAL

Black Kite 1

2 Stomach contents

Oral cavity/contents = bait adhering to beak

Chlorpyrifos 2.03

2.96

Egyptian

Vulture

1 3 Digestive tract (gizzard + proventriculus)

Tongue + oral cavity/contents

Digestive tract (larynx, esophagus, trachea)

Methamidophos QUAL

QUAL

6.57

*A metabolite of aldicarb

QUAL = qualitatively detected only, via thin layer chromatography


43

Table 3b: Range of pesticide residues detected in samples (n = 10) from degraded mammal carcasses (n = 19)

Species Animals

sampled

Samples Sample description Pesticide Residues detected

(mg g -1)

Cat, domestic 3 3 Stomach contents Aldicarb

Aldicarb, Aldicarb sulfoxide

54

0.32, 0.03

15, 7.2

Dog, domestic 3 3 Stomach contents

Aldicarb

Aldicarb, Aldicarb sulfoxide

66

12, 3.6

6, 30

1 1 Stomach contents Methamidophos 1.87

Cat, domestic 1 1 Organs, pooled Carbofuran 0.34

Dog, domestic

2 4 Oral cavity/oral contents

Stomach contents

Carbofuran QUAL

QUAL

Stomach contents

Tongue

Carbofuran, 3-hydroxy

carbofuran

118, 0.03

0.03, 0.01

Red fox

3 7 Insects from carcass

Organs, pooled

Carbofuran QUAL

1.82

Stomach contents (2)

Tongues (2)

Tongue + oral contents

Carbofuran, 3-hydroxy

carbofuran

5.28, 0.01

4.03, 0.04

0.34, 0.02

0.06, 0.03

0.94, 0.02


44

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

Detected in

Residues

(mg kg-1)

Red fox

3

Carbofuran, 3-

hydroxy

carbofuran

Tongue

Stomach contents

Tongue

Insects from carcass

Stomach contents


Organs

0.34, 0.02

5.28, 0.01

0.06, 0.03

QUAL

4.03, 0.04

0.94, 0.02

1.82, 1.2

Domestic

dog

1 Tongue

Stomach contents

0.03, 0.01

118, 0.03

Egyptian

Vulture

1

Methamidophos


Digestive tract (gizzard

+ proventriculus)

Digestive tract ((larynx,

esophagus, trachea)

QUAL

QUAL

6.57


45

Analysis of the Cinereous vulture

palate

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 re-

examined, 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

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).

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


46

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


47

(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


48

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.

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

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.

Key words: organophosphorus, carbamate, carbofuran, chlorfenvinphos,

chlorpyrifos, methamidophos, insecticide, pesticide, carcass, vulture, canid,

palate, tongue, mummification, autolysis, muti


49

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******


52

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


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).


53

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


54

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

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

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


55

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 White-

backed 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


56

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.


57

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 2014.2.

www.iucnredlist.org. Downloaded on 30 August 2014.

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.


58

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.

******


59

Attempted Verreaux’s Eagle predation on Rüppell’s Vulture

and breeding observations at Lake Kwenia colony, Kenya

Simon Thomsett

1* and James Aldrich

1Ornithology Section. Dept of Zoology, National Museums of Kenya, Nairobi, Kenya


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.

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

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 10-

20 metres of their young. Rarely, the

eagles did appear to have the intent

to predate chicks by looking directly


60

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 close-

flying 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.

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

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


61

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 of the attempted

predation

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


62

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 co-

ordinated 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 un-

feathered 2.5cm spines and the

presence of some abraded tips on

secondaries indicated that it had


63

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 co-

ordination 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.

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.

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.

******


64

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


65

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 André Botha

[email protected] [email protected]

African Regional Co-chairs: Munir Virani, Kariuki N’danganga

European Regional Co-chairs: Alvaro Camiña, José Tavares


66

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.

Diclofenac in Europe

As requested by the European

Commission, the European

Medicines Agency (EMA)

published their long-awaited

technical position on the vulture-

killing drug diclofenac in December

– 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


67

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)

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 post-

construction impact studies to

minimise the potential effects on

vultures from wind farms.

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.

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.

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


68

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.

******


69

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])


70

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.


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.



71

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 …”


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.


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


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.



72

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).


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.


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”.



73

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 White-

backed 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!


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.


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.


******


74

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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