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Cover picture: Yellow-breasted Bunting Emberiza aureola, Numrug Protected Area, Dornod province, eastern Mongolia, 3 June 201 5

byYannMuzika

FORKTAIL

Number 32, 2016

CONTENTS

natural history

MUSEUM LIBRARY

3 1 MAY 2017

- - -

J. MUKOVSKY & P. STYBLO

Biometry, ecology and population status of the Endangered Yellow-breasted Bunting Emberiza aureola in the

Svyatoy Nos wetlands. Lake Baikal, eastern Siberia, Russia . 1

SOMYING THUNHIKORN, MATTHEW J. GRAINGER, PHILIP J. K. McGOWAN & TOMMASO SAVINI

Methods used to survey avian species and their potential for surveying ground-dwelling birds in Asia . 5

JOHN D. FARRINGTON

A survey of the autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China . 14

JOHANNES H. FISCHER, NICHOLAS S. BOYD, ADHY MARULY, ANNA-SELMA VAN DER KAADEN, SIMON J. HUSSON & JAMARTIN SIHITE

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia . 26

ARELLEA R. DEWI, NURROHMAN E. PURNOMO, REZA A. AHMADI, I. PURWIANSHARI & MUHAMAD H. ASHSHIDIQI

Field records of Zappey's Flycatcher Cyanoptila cumatilis on Java and Sumatra, with notes on the distribution and status

of Blue-and-white Flycatcher C. cyanomelana in Indonesia . 36

PAUL J. LEADER, DAVID J. STANTON, RICHARD W. LEWTHWAITE & JONATHAN MARTINEZ

A review of the distribution and population of the Collared Crow Corvus torquatus . 41

KHADANANDA PAUDEL, KRISHNA P. BHUSAL, RAJU ACHARYA, ANAND CHAUDHARY, HEM S. BARAL, ISHWARI P. CHAUDHARY, RHYS E.

GREEN, RICHARD J. CUTHBERT &TOBY H. GALLIGAN

Is the population trend of the Bearded Vulture Gypaetus barbatus in Upper Mustang, Nepal, shaped by diclofenac? . 54

L. D. PERERA & A. D. ILANGAKOON

Results of the first systematic boat-based seabird survey in Sri Lanka . 58

HANOM BASHARI & THOMAS ARNDT

Status of the Critically Endangered Yellow-crested Cockatoo Cacatua sulphurea djampeana in the Tanahjampea islands,

Flores Sea, Indonesia . . . . . . . . . . . 62

M. JERI IMANSYAH, DENI PURWANDANA, ACHMAD ARIEFIANDY, Y. JACKSON BENU, TIM S. JESSOP & COLIN R. TRAINOR

Valley-floor censuses of the Critically Endangered Yellow-crested Cockatoo Cacatua sulphurea occidentalis on Komodo

Island, East Nusa Tenggara province, Indonesia, point to a steep population decline over a six-year period . 66

ARNE E. JENSEN & ANGELIQUE SONGCO

The birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines, including accounts of

breeding seabird population trends . 72

Short Notes

TATIANA ROSE C. ABANO, DENNIS JOSEPH I. SALVADOR & JAYSON C. IBANEZ

First nesting record of Philippine Eagle Pithecophaga jefferyi from Luzon, Philippines, with notes on diet and

breeding biology . 86

P. FETTING, S. THORN, M. PACKERT & W. HEIM

First record of Yellow-bellied Tit Pardaliparus venustulus in Russia suggests a significant range extension of a species

formerly endemic to China . 88

YUNBIAO HU & YUEHUA SUN

First breeding record of Slaty Bunting Emberiza siemsseni . . . 90

YI-QIANG FU, MING XIANG, CHI-PING KONG & YONG-HENG WU

Further evidence that wasps prey on nestlings . . . . . . . 91

AIWU JIANG, DEMENG JIANG, EBEN GOODALE, FANG ZHOU & YUANGUANG WEN

Olive-backed Sunbird Cinnyris jugularis assisting Crested Bunting Melophus lathami at the nest: substantiated

evidence for interspecific feeding, Guangxi, south-west China .

.93

Forktail 32 (2016)

P. L. MEAURANGA M. PERERA, SARATH W. KOTAGAMA, EBEN GOODALE & H. S. KATHRIARACHCHI

What happens when the nuclear species is absent? Observations of mixed-species bird flocks in the Hiyare Forest Reserve,

Galle, Sri Lanka . . . 96

MD. REZAUL KARIM & MD. FARID AHSAN

Breeding biology of Jungle Myna Acridotheres fuscus at Chittagong University Campus, Chittagong, Bangladesh . 98

M. S. TANEDO & R. 0. HUTCHINSON

Status of the White Wagtail Motacilla alba in the Philippines including two new subspecies for the country . 100

Guidelines for contributors . . . . . . . . . . . . . . . inside back cover

Forktail 32 (2016): 1-4

Biometry, ecology and population status of the

Endangered Yellow-breasted Bunting Emberiza aureola

in the Svyatoy Nos wetlands. Lake Baikal,

eastern Siberia, Russia

J. MLIKOVSKY & P. STYBLO

Yellow-breasted Buntings Emberiza aureola were common breeding summer visitors to the Svyatoy Nos wetlands in 1991-1994, but their

numbers have declined sharply since then and the species was nearly extinct in this area by 2013-2014. Biometric data from 216 individuals

are given. The birds leave their breeding grounds very early: adult males before 25 July and adult females and juveniles about one month

later. Adult birds do not moult on the breeding grounds in the Svyatoy Nos wetlands. No causes for the collapse in the breeding population

were apparent in the Svyatoy Nos wetlands.

INTRODUCTION

The Yellow-breasted Bunting Emberiza aureola is a widespread

species in the Palearctic Region that breeds from east Finland and

west Russia, east to Kamchatka, south to north Ukraine, north

Kazakhstan, Mongolia, north-east China, Sakhalin Island and

north Japan, migrating to winter in South and South-East Asia

and southern China (Dementyev & Ptushenko 1940, Portenko

& Stubs 1971, Chan 2004, BirdLife International 2016, Copete

& Sharpe 2016). Its numbers are currently sharply decreasing

and, although only first classified as Near Threatened in 2004, its

status was uplifted to Endangered in 2013 (Durnev 2009, Yong et

al. 2015, BirdLife International 2016). ITere we present the results

of our study of these buntings made in the Svyatoy Nos wetlands,

Zabaykalskiy National Park, north-east Lake Baikal, eastern Siberia,

Russia (approximately 53.55°N, 108.95°E), from 1991-2014.

JM and PS studied Yellow-breasted Buntings in the Svyatoy Nos

wetlands in 1991, 1993, 1994,2001 and 2005, andJM worked there

alone in 2013 and 2014. Biometric data and data on seasonality were

only collected in 1991, 1993 and 1994.

The grassy Svyatoy Nos wetlands, about 350 km2 in area, cover

most of the isthmus that links the Svyatoy Nos peninsula with the

mainland. They are part of the ornithologically most important

wetlands in the Lake Baikal region (Mlikovsky & Styblo 1992,

Mlikovsky et al. 2002, Mlikovsky 2009); a description of them is

given by Mlikovsky et al. (1992).

Birds were trapped using mist-nets and the f ollowing biometric

data were measured: body mass (using a Pesola spring scale to

the nearest gram), wing and tail length to nearest mm (Topfer

& Fieynen 2011), wing formula (distances of primaries P2-P8,

numbered from the outside, and of the outermost secondary SI

from the wing tip, in mm (Mlikovsky 1978); PI was always shorter

than the greater wing-coverts). Fatness was scored on a six-degree

scale (T0-T5) following Busse (1970).

RESULTS AND DISCUSSION

Biometry

Biometric data are shown in Table 1, and include the 1991 data

previously listed by Styblo & Mlikovsky (1992). Wing length, tail

length and body mass agree with previously published data on

Yellow-breasted Buntings measured in Russia (Timofeev-Resovskij

1940, Vinogradova etal. 1976, Glutzvon BlotzheimN Bauer 1997).

However, statistical comparisons were not possible, because these

authors did not present the necessary statistical values.

Adult males are longer-winged and longer-tailed than both adult

females and juveniles. Adult females do not differ from juveniles in

wing length, but tend to have slightly longer tails (Table 2). Adult

males are heavier than adult females and juveniles, but adult females

do not differ from juveniles in this respect (Table 2).

The juvenile’s body mass varied with body fatness. Fat score TO:

body mass average: 18.1 ± 1.12 gm (n = 13, range = 16-20 gm); fat

score Tl: 19.4 ± 1.36 gm (n = 16, range = 17-21 gm); fat score T2

19.7 ± 1.37 gm (n = 6, range = 18-21 gm); and fat score T3: 21.0

gm (n = 2, range = 20-22 gm).

Table 1. Biometry of Yellow-breasted Buntings mist-netted in the

Svyatoy Nos wetlands in 1991-1994. Body mass gm, all other data

mm. P = primary (numbered from outside), S = secondary (outermost),

n = number of specimens, SD = standard deviation. For statistical

comparisons of mean values see Table 2.

Table 2. Statistical comparison of mean body dimensions of Yellow¬

breasted Buntings (Table 1). t = t-test value (two-tailed), DF = degree of

freedom, p = probability. Probabilities lower than 0.05 are highlighted

in bold.

J I Ri MLlKOVSKY

2

J. MLlKOVSKY & P. STYBLO

Forktail 32 (2016)

Plate 1. Typical breeding habitat of Yellow-breasted Bunting Emberiza

aureola in the Svyatoy Nos wetlands: more or less isolated shrubs, trees

and groves at the edge of grassy ( Calamagrostis and Carex) marshlands,

10 July 201 3. This was the only site occupied by Yellow-breasted Buntings

in southern Svyatoy Nos wetlands in 2013 and 2014.

Seasonal aspects

Yellow-breasted Buntings were already present in the Svyatoy Nos

wetlands and males were singing when we arrived there on 24June

1991 (Heyrovsky et al. 1992), 6 June 1993 and 16 June 1994. In

1993 we found nests with eggs on 11 June, 16 June, 26 June, 8 July

and 14 July (two) (M. Salek in litt., JM unpubl. data). The earliest

record of young leaving their nest was on 7 July 1991 (Heyrovsky

al. 1992), but a female carrying food was observed as late as 6 August

1991 (Heyrovsky et al. 1992). Young Yellow-breasted Buntings are

known to leave their nest still flightless and to spend the following

two weeks or so in the same vicinity (Shkatulova 1962, Rymkevich

1976). We caught the first fully fledged juveniles in mist-nets on 14

July in 1991 and on 25 July in 1993 (we have no comparable data

from 1994).

We did not observe post-breeding flocking of Yellow-breasted

Buntings or any evidence of autumn migration; the birds simply

disappeared from the wetlands. Our data indicate that the departure

is sex- and age-dependent. In 1991 males were regularly mist-netted

until 16 July, when the work was interrupted for a week. Thereafter,

only two males were mist-netted (26 July and 2 August), although

females and juveniles were regularly mist-netted until 28 August,

when our field-work ceased. In 1993 males were regularly seen

and mist-netted until 24 July (a single was also mist-netted on

1 1 August), whilst females and juveniles were regularly seen and

mist-netted until 27 August (plus a single juvenile on 31 August).

In 1994, when we studied birds in the wetlands from 11 August

to 20 September, no males were mist-netted, whilst females and

juveniles were regularly mist-netted until 22 August (plus single

birds on 27, 29 and 30 August). In summary, these data indicate that

the majority of males left the Svyatoy Nos wetlands before 25 July,

probably immediately after the young fledged, whereas females and

juveniles remained in the wetlands until late August and probably

left their breeding grounds together.

The sex- and age-dependent departure from breeding grounds

is also supported by Havlin & Yurlov (1977), who mist-netted only

two adult males, one adult female and 39 juveniles between 5 and 31

August 1971 at Lake Chany (54.580°N 78.140°E), where Yellow¬

breasted Buntings were common breeding birds.

Neither adult males nor adult females moult in the Svyatoy

Nos wetlands, which concurs with previous data from mainland

Yellow-breasted Buntings of the nominate subspecies (Stresemann

& Stresemann 1969, Rymkevich 1983, 1990, Chernyshov 1991).

Note that adults of the eastern subspecies, Emberiza aureola ornata ,

moult before autumnal migration (Stresemann & Stresemann

1969). We recorded no fattening of adult males before their

Plate 2. An isolated grove in the marshland at the edge of the site shown

in Plate 1, 10 July 2013. One pair of Yellow-breasted Buntings bred in

this grove in 2013 but it was abandoned in 2014. The foggy hills in the

background are the Svyatoy Nos range on the Svyatoy Nos Peninsula.

departure from the wetlands. Most adult females also showed no

fat (fat score TO), although traces of fat were visible around the

furculum of some adult females mist-netted during the second half

of August: fat score TO (3), Tl (3). However, most juveniles already

had fat visible in the region of the furculum and on the belly in the

second half of August: fat score TO (4), Tl (10), T2 (5), T3 (2).

Population status

Yellow-breasted Buntings were by far the commonest songbirds of

the Svyatoy Nos wetlands from 1991-1994 (Heyrovsky etal. 1992,

Styblo & Mlikovsky 1992, and our unpublished data). They were

also known to be very common in suitable habitats around southern

Lake Baikal (Fefelov et al. 2001) and in the wider vicinity of Lake

Baikal during the 1980s and 1990s (Bogorodskiy 1989, Goroshko

2013). We did not estimate the overall population size during the

1990s, but noted where the birds occurred, estimated local densities

and listed all birds trapped during mist-netting. From these data

we estimate the overall population of Yellow-breasted Buntings in

the southern part of the Svyatoy Nos wetlands (i.e. south of Lake

Arangatuy) very roughly to have been some 500-1,000 breeding

pairs at that time. Our visits to the Svyatoy Nos wetlands were

brief in 2001 and 2005, but Yellow-breasted Buntings were still

widespread there in that period.

However, in 2013 we found Yellow-breasted Buntings at only

two sites in the southern part of the wetlands: at least four pairs

(upper limits were not estimated) were breeding at 53.530°N

108.960°E, and a single pair was breeding at 53.56°N 108.94°E,

with adults observed carrying food at both sites. In 2014 our specific

search for Yellow-breasted Buntings covered the whole of the

southern part of the Svyatoy Nos wetlands, but we only found the

species at the 53.530°N 108.960°E site, where seven singing males

were recorded in earlyjuly. Although suitable habitat was apparently

widespread in 2014, all seven of the males were singing on a single

site. No females were seen in 2014; they were presumably incubating

eggs during our study period, but it remains unclear whether all the

singing males were paired or whether any were single.

A comparison of the data from the early 1990s and the early

2010s shows that the local breeding population of Yellow-breasted

Buntings decreased by some 99%. Our anecdotal evidence from

2001 and 2005 suggests that much of the decline in the Svyatoy Nos

area occurred in the decade between 2001 and 2014. At Davsha,

about 100 km north of our study site, a major decline of locally

breeding Yellow-breasted Buntings was recorded in 2000-2001

(Ananin 2015). The few remaining pairs in the Svyatoy Nos

wetlands clearly do not constitute a self-sustaining population and

JIRl MLlKOVSKY

Forktail 32 (2016)

Yellow-breasted Bunting Emberiza aureola in the Svyatoy Nos wetlands, Lake Baikal, Russia

3

the species was nearly extinct here in 2014. This collapse corresponds

with many recent observations from other parts of its breeding

range, including eastern Europe (Romanov 2003, Zav’yalov et

al. 2011a, b, Khokhlova & Artemyev 2012, 2015, Ivanchev et al.

2013, Valuev 2013), Siberia (Popov & Maleev 2008, Durnev 2009,

Ananin 2010, Ryabtsev 2011, 2013, Goroshko 2013, Ananin 2015)

and Japan (Tamada 2006, Tamada et al. 2014).

The reasons for the sharp decline of Yellow-breasted Bunting

populations in the Svyatoy Nos wetlands do not appear to be

related to conditions on the breeding grounds. Plenty ol apparently

suitable habitat was available there in both the 1990s and the

2010s, and we found no apparent differences in the potential food

supply between the two periods, which makes food shortage an

improbable explanation. Yellow-breasted Buntings were neither

hunted nor suffered other anthropogenic disturbance in the Svyatoy

Nos wetlands in either study period. Thus, their population almost

certainly declined due to problems away from their breeding

grounds, i.e. on migration and/or in their wintering areas, where

human pressure, especially but not exclusively overhunting, may

be the main cause of population decline (Ryabtsev 2011, Kamp et

al. 2015, Yong et al. 2015, Copete & Sharpe 2016, Jiao et al. 2016).

ACKNOWLEDGEMENTS

We are grateful to A. Beketov, V. Mel’nikov, E. Ovdin, M. Ovdin and

A. Razuvaev for permission to work in the Zabaykal’skiy National Park.

For assistance in the field we thank David Heyrovsky, Vojtech Kubelka,

Petr Lumpe, Martin Sladecek, V. Sviecka, Miroslav Salek and Frantisek

Zicha. Miroslav Salek kindly supplied data on three nests he found in

1993 and provided helpful comments on the manuscript. JM’s work on the

manuscript was supported in part by a grant from the Ministry of Culture

of the Czech Republic DKRVO 2014/15, DKRVO 2015/16 and DKRVO

2016/17 (National Museum 00023272). The field work in 2013 and 2014

was partly supported by the Ministry of Education, Youth and Sports of the

Czech Republic (Grant MSMT Kontakt II, project LH13278 ‘Interspecific

relationships and predation risks in grassland and wetland bird communities’).

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FORKTAIL 32 (2016): 5-1 3

Methods used to survey avian species and their potential

for surveying ground-dwelling birds in Asia

SOMYING THUNHIKORN, MATTHEW J. GRAINGER, PHILIP J. K. McGOWAN & TOMMASO SAVINI

There is an increasing need for reliable information on bird populations in Asia and several methods have been used for population estimation:

some were based on the way that species were detected (e.g. calling or territorial display) in field surveys and others have been developed

from an understanding of sampling theory. Many bird species in Asia inhabit areas that are challenging to survey; we consider the basis of

some of the more widely used methods in order to assess which are likely to be useful for providing data on populations. We review four

methods: 1) spot mapping; 2) triangulation; 3) distance sampling (using line transects and point counts); and 4) camera trap sampling. Four

aspects were assessed: What has it been used for? What are the method's assumptions? What field protocol is required? What analytical

methods should be used? Spot mapping and triangulation are both based on the ability to detect individuals of the target species in the field,

but lack a statistical basis for converting this into a meaningful estimate about the population surveyed. Distance sampling is, in contrast,

based on sampling theory and meeting some of the assumptions for detecting individuals in the field can be difficult. Nonetheless, it is

increasingly widely used and considered reliablefor making estimates about bird populations. Finally, camera trapping is a useful method

for rare and cryptic species and the analytical techniques that cover the wide range of contexts in which it may be used are being developed.

INTRODUCTION

Quantitative data on populations (i.e. density or size) of a given

species in a specific area are very important for wildlife conservation

in a range of different contexts and for varying purposes. Density

estimates, for example, provide baseline data on species abundance

that can be used to derive population sizes and these can be

monitored over time to assess the suitability of conservation strategies

(Sutherland etal. 2004, Nijman & Menken 2005). Understanding

these population changes is very important ifpolicy and management

plans are to be based on a sound understanding of species status.

Reliable estimates of such population trends require careful design

of the sampling strategy and field protocols that are standardised

and repeatable with high detection probability and low observer

variability (Thompson et al. 1998, Yoccoz et al. 2001, Pollock et

al 2002).

The demand for data to both assess the status of species of

conservation concern and to inform the management of those with

the highest probability of extinction is most acute in the tropics and

subtropics where most threatened vertebrates are thought to occur

(Laurance 2007), the knowledge of species ecology is severely limited,

and habitat loss and illegal huntingpresent serious problems for many

species (Wright & Muller-Tandau 2006). This is compounded by

the difficulty in accessing terrain in areas that are mountainous or

that have dense forest structure (e.g. tropical rainforest), making it

a challenge to relate information about encounter rate (sighting or

vocal detections) to populations (abundance, density or size).

There is, therefore, a considerable need to encourage the

collection and analysis of data that can be used to inform

assessments of species status, wherever this is possible. Yet, for

many who have an interest in avian fieldwork and who are keen to

gather such data but lack detailed knowledge in survey techniques,

determiningwhich method to use and understanding how to use it

properly is difficult. This is because of the complexity of different

contexts in which each method has been used, the purpose of the

study and the various assumptions that have been made when

developing the field protocols and in turning the field data into

population estimates. Although there is a variety of texts available

for surveying birds (e.g. Sutherland 1996, Bibby etal. 1998, 2000), a

range of studies and developments have taken place since these were

published that we seek to reflect here. Furthermore, our aim is to

review, briefly, methods that have long been used or considered for

birds in the tropics. We seek to present a summary of these methods

in a form that will guide potential first-time users towards a method

that will best suit their purpose and circumstances. Although we

consider Asian birds in general, we place special emphasis on ground¬

dwelling species such as pheasants, because they are often of high

conservation concern (e.g. because of ground-snaring) and can be

difficult to detect.

A range of methods have been used to collect data on terrestrial

bird populations elsewhere, but their reliability and usefulness have

not been reviewed critically and related to the data needs of species

in Asia, especially where terrain and habitat are challenging. These

methods include those that have been developed because of the way

individuals in a species are detected (e.g. spot mapping, triangulation

and now camera trapping) and those based on sampling theory (e.g.

distance sampling using both point and line transect). All these

methods have been used in order to generate population estimates of

one sort or another, but there is limited guidance on what methods

are suitable in which circumstances (e.g. the purpose of the survey,

the ecology of the target species and the terrain and habitat being

surveyed). Consequently, we seek to answer the question: what are

the options and which should be considered for a particular purpose

and context? The aim of this synthesis is to provide a succinct review

of the key features of four population estimation methods that have

been used in South and South-East Asia, consider their utility for

ground-dwelling birds in the region, and provide references to further

information. We examine where each method has been used and for

what purpose, the field protocol employed, the analytical methods

required and their statistical assumptions. We also included gibbons

in our review, because their vocalisations show striking parallels

with songbirds (Clarke et al. 2006), and because they have also

been the subject of methodological research in order to estimate

population size from the detection of loud calls and sightings; there

may therefore be lessons that can be learnt for avian population

estimation in the region.

METHODS

We reviewed four methods used to survey birds to provide data that

are relevant to monitoring population changes. These methods are:

1) spot mapping (also known as territory mapping); 2) triangulation;

3) distance sampling using both line and point transects; and 4)

camera trapping. To ensure that we reviewed a wide representation

of appropriate research we conducted a structured search of available

literature. Given our aim and objectives, an exhaustive systematic

review ( sensu Collaboration for Environmental Evidence 2013) of

6

SOMYINGTHUNHIKORN etal.

Forktail 32 (2016)

avian population estimation was not appropriate, so we tailored our

search protocol to maximise efficiency without compromising the

range of literature that we reviewed.

We searched three databases for studies that have used these

methods in published findings, namely: Google Scholar, Newcastle

Library Search and Science Direct. The Newcastle Library Search

includes a wide range of resources (see http://www.ncl.ac.uk/

library/resources/library-search/) and includes most material in

major bibliographic databases and from major journal publishing

companies (e.g. Wiley and Elsevier). Searches were conducted using

standardised search terms that described the methods and sought

to limit the studies identified to those that were taxonomically

relevant. For example, searches for spot mapping were undertaken

using phrases ‘spot mapping’ and ‘territory mapping’ and included

taxonomic terms such as ‘birds’.

Once relevant papers had been identified we reviewed the papers

to extract information that would help us answer four questions:

What has it been used for? What are the method’s assumptions?

What field protocol is required? What analytical methods should be

used? Our overall aim was to provide a succinct review of these key

features, provide references to further information and to consider

how useful these methods are for population estimation of birds in

South and South-east Asia.

RESULTS

Table 1 summarises key aspects of each of the methods reviewed

and we discuss key aspects of that summary below. Please refer to

the table tor further details and sources of information.

Table 1. Comparison of spot mapping, triangulation, distance (point and line transect) and camera trap sampling.

Spot mapping

Triangulation

Distance sampling

Camera trap

£ Density

O

Q_

z:

Q_

1. Population is dosed

^ 2. Species is territorial

.1 3. Species are identified correctly

Q_

E

Density/abundance

distribution

1. Individual calls every morning

2. Animal groups are independent of

each other

3. All individuals/ groups were heard

calling from a station

CL*

~CT

cl*

5-10 consecutive visits

3-5 (gibbons) or

1-4 (Galliformes) consecutive days

Study area divided into a grid,

quadrats, points or strip transects,

= for intensive surveys

E

n 3

uo

Listening posts established at vantage

points and distance and bearing of calls

heard are recorded

m Most widely used formula is: density

(pairs or territories/ha) = number

S of mapped territories/pairs mapped

is divided by size of area (in ha)

surveyed

See (B) below for examples of studies

i Identification of species by sight and

a j

| song/call

"5

O'

CL*

cc

5 Breeding and territorial birds

“O

CL*

Gibbon densities have been estimated

following Brockelman & AN (1987) and

Brockelman & Srikosamatara (1993).

Population indices for Galliformes follow

Gaston (1979)

See (C) below for examples of studies

Identification of species bysightand

song/call and estimation of distance

Gibbons

Galliformes

Density/encounter rate/distribution

1. Individuals on the line or point are always detected

2. Individuals do not move

3. Measurements are exact

3-5 consecutive days

Pointtransect:

Random or stratified across study area and points

with variable radius

Line transect:

Random or stratified across study area and transects

with variable distance

The software programme Distance is widely used,

. but Bayesian approaches (Eguchi & Gerrogette 2009,

Amundson etal. 2014), PAST Program version 2.05

(Jolli & Paddit 2011), and Distance Package in

R Program (Kidwai 2013) are also used

See (D) below for examples of studies

Identification of species by sight and song/call and

estimation of distance

Pointtransect: songbirds

Line transect: wide range of taxa

Population/density/abundance

Capture rate/species richness

Distribution/behaviour/habitat selection

Capture-recapture:

1. Population is constant during study

2. The sample is random

3. Capture probability of each individual > zero

Presence-absence/repeat count:

1. Detection is independent

2. Detection probability ofindividual is constant overtime

10-60 trap day/night

Camera traps should be set to maximise the chances

of detecting target species and the distance between

camera traps must be smaller than territory of target

species

A range of analytical techniques are used, depending

on the study

See (A) below

See (E) belowfor examples of studies

Skill to select camera location and set traps

appropriately

Terrestrial birds and mammals

(A) : The following analytical techniques have been used to calculate abundance and density, depending on context (see text): 1) capture-recapture using CAPTURE; 2) mark-resight-capture using MARK

and R package Software Program; 3) photographic rate; 4) occupancy/presence-absence/repeat count using Presence, MARK software program; 5) spatially explicit capture-recapture (SECR) using

DENSITY program, R package SECR, Bayesian framework in WinBUGS, R package SPACECAP software program.

(B) : Examples of studies using spot mapping for estimating the density of songbirds include Best (1975), Jones etal. (2000), Tomialojc (2004) and Yoon (2010). Examples comparing the accuracy of field

survey methods include Tarvin etal. (1998), Howell etal. (2004), Bocca etal. (2007), Gale etal. (2009), Gottschalk & Huettmann (2011), Greene & Pryde (2012) and Newell etal. (2013).

(C) : Examples of studies using triangulation for estimating gibbon densities include O'Brien etal. (2004), Nijman & Menken (2005), Aldrich etal. (2006), Jiang etal. (2006), Hamard etal. (2010), Luu Quang

Vinh etal. (2010), Phoonjampa etal. (2011), Hoing etal. (2013), Timmins & Duckworth (2013) and Thongbueefa/. (2014). Examples estimating the abundance and distribution (presence-absence) of loud-

calling Galliformes include Garson (1998), Baral etal. (2001), Kaul & Shakya (2001), Jolli & Pandit (2011) and Sailoefa/. (2013). Examples estimating the density of Galliformes include Gaston etal. (1980),

Mahatoefa/. (2006), Poudyal etal. (2009) and Jain & Rana (2013).

(D) : Distance sampling has been used for a wide range of purposes across a range of species and habitats. These include estimating densities of breeding birds (Jarvinen & Vaisanen 1975), moorland

passerines (Thirgood eta/. 1995), Cracidae (Begazo & Bodmer 1998), migrating birds in forest wetlands (Wilson etal. 2000), monitoring seabirds (Certain & Bretagnolle 2008) and studying cetaceans

(Hammonda etal. 2013). Examples of studies estimating the density and abundance of Galliformes in Asia include Azhar etal. (2008), Jolli & Pandit (2011), Kidwai etal. (2011), Ramesh etal. (2011),

Selvan & Sridharan (2012), Kidwai (2013) and Selvan etal. (2013). See also Warren & Baines (2011); studies of encounter rate include Wang etal. (2004) and Ashraf et al. (2005) and of distribution include

Lalthanzara etal. (2014).

(E) : Studies using camera traps to sample populations include: various studies on cat populations, Karanth (1995), Karanth & Nichols (1998), Carbone etal. (2001), Azlan & Sharma (2003), Silver etal.

(2004), Karanth etal. (2006), Soilaso & Cavalcanti (2006), Harmsenefa/. (2010), Tempa etal. (2011) and Lynam etal. (2013); ungulates, Rovero & Marshall (2009) and Asian tapir, Linkieefa/. (2013).

Studies assessing species richness and community composition include Silveira etal. (2003), Bernard etal. (2013) and Liu etal. (2013), and monitoring the status and trend of tropical rainforest terrestrial

vertebrates include Ahumada etal. (2013). Studies using camera trapping to study bird species in Asia include Winarni etal. (2009), Li etal. (2010) and Samejima etal. (2012).

Forktail 32 (2016) Methods used to survey avian species and their potential for surveying ground-dwelling birds in Asia

7

Spot mapping or territory mapping

Spot mapping was first proposed by Williams (1936) and has been

commonly used for intensive surveys to estimate abundance and

density of territorial and singing birds in a relatively small area. It

has largely been used in the temperate habitats of Europe, North

America and New Zealand (e.g. Best 1973, O’Brien etal. 2004, Yoon

2010) and only rarely in the tropics (e.g. Thiollay 1994, Stouffer 2007,

Gale et al. 2009, Peel et al. 2015). It has also been used to test the

effectiveness of other survey methods such as point counts (Howell

et al. 2004), radio-telemetry (Bocca et al. 2007), mark-resighting

(Greene & Pryde 2012) and, in South-East Asia, distance sampling

(Gale etal. 2009) and camera trapping (Suwanrat et al. 2015).

Spot mapping can both overestimate (Enemar et al. 1979, Cyr

et al. 1995) and underestimate population size (Snow 1965, Bell

et al. 1973, Nilsson 1977, Paul & Roth 1983, Streby & Loegering

2012) depending on the detectability of the focal species, the census

period (Enemar etal. 1979), the ability of the observer (O’Connor &

Marchant 1981), the territorial behaviour of the species (Best 1975,

Enemar et al. 1979, Bocca et al. 2007) and sample size (Enemar et

al. 1978).

Assumptions

Turning field data into meaningful population estimates requires

that: 1) populations are stable during the time of study and that

animals remain in their territories during sampling periods; 2)

animals are correctly identified to species; 3) territory owners

are sufficiently conspicuous to be recorded on successive visits; 4)

observers do not differ in their ability to detect animals (Ministry

of Environment 1999). In Asian forests, it is rarely possible to detect

a large enough proportion of individuals in the study area for this

method to be appropriate.

Field protocol

Spot mapping is used during the breeding season for species that

are defending territories using conspicuous behaviours (e.g. song,

visual displays) and can, therefore, be detected easily, or with

animals that have been marked. Study areas may be about 2-4 km2 ,

which are then subdivided to sample units in the shape of a grid,

quadrats, points or strip transects for intensive surveys. Ideally,

data are collected simultaneously by two or more observers and

then combined to produce a map containing all detections of the

species’s territories. Observers should cover every part of the study

area several times, and it has been suggested that each sample unit

requires at least 7-10 visits that should be made during periods

of peak activity (typically in the morning and in the afternoon/

evening). Surveys should be conducted during good weather

conditions (Best 1975, Enemar et al. 1979, Tarvin et al. 1998,

Howell et al. 2004, Tomialojc 2004, Greene & Pryde 2012).

Analysis

The locations where the focal species is recorded from all

observers are combined and mapped, and the spatial pattern of

records (e.g. clustering) is used to determine where territories are

positioned. This can be done in two ways: 1 ) each observer interprets

territorial boundaries by themselves and then an average is taken of

the number of territories that each observer has identified; or 2) a

single map is produced by an experienced observer. The estimate of

territory density can then be calculated by dividing the number of

territories mapped by the size of the area surveyed to give the number

of pairs or territories per hectare or km2.

Recommendations for surveying ground- dwelling birds in Asia

The advantage of using spot mapping is that the method can provide

accurate monitoring of populations of territorial species in a fairly

small area. It is more problematic, and unlikely to be useful, where

the area to be surveyed is large and access is difficult, such as rugged

terrain where access is only via ridges or where there are large tracts of

dense habitats that are difficult to navigate. Spot mapping requires a

high level of observer skill in identifying and documenting bird species

reliably and the field protocol is time consuming. It can be difficult to

use in dense habitat (if sightings are a principal method of detection)

or where bird densities are high (Gregory et al. 2004). Ultimately, it

is likely to be useful for ground-dwelling species in very few cases.

Triangulation or fixed point count or call count

Triangulation was developed for gibbons by Brockelman & Ali

(1987) as a way of surveying these territorial and loud calling species.

It has subsequently been used to estimate the number of gibbon

groups, where the social structure and calling behaviour allow

specific assumptions to be made that provide density or abundance

estimates (e.g. Nijman 2001, Phoonjampa & Brockleman 2008).

Some bird species in Asia, especially pheasants in the Himalayas,

have also been counted by plotting on a map (‘triangulating’) calls

that have been detected by at least two or more observers at the same

time from fixed points that are an appropriate distance apart. This

method has been used to assess the distribution and status of species

such as Western Tragopan Tragopan melanocephalus, Himalayan

Monal Lophophorus impejanus, Cheer Pheasant Catreus wallichi

and Koklass Pheasant Pucrasia macrolopha in the Himalayas of

India, Nepal and Pakistan (Gaston etal. 1980), and for species such

as Indian Peafowl Pavo cristatus in lower elevation areas of India

(Jain & Rana 2013).

Assumptions

Turning field data into a population estimate requires that: 1) each

individual (or individual in a group, if a group is the unit being

surveyed) calls at least once during the study period (Nijman 2001);

and 2) listening posts are selected with the assumption that all

groups calling could be heard (Jiang etal. 2006, Awan etal. 2014).

Field protocol

Vantage points are selected so that calls can be heard from as wide

an area as possible, such as on top of a ridge or where both sides of a

valley can be monitored, and calls of target species are located from

these points (Gaston 1979). The spacing of listening posts depends

on the distance from which the target species can be heard. For

example, it is often assumed that all pheasants within 400 m can be

heard, although some researchers use a fixed radius of 300 m (e.g.

Jolli & Pandit 2011, Awan et al. 2014), hence observers should be

stationed accordingly. Mapping all calls by measuring the compass

bearing and estimating the distance from the observer permits

duplicate records to be eliminated and may show clusters of records

that correspond to the home ranges of particular individuals.

Analysis

The population size, density and abundance index of a target species

in an area can be estimated based on the number of individuals/

groups recorded calling. This is done as follows: 1) the population

of calling birds in an area = the number of the species counted

in the survey area multiplied by [total area/census area], with the

condition that survey area must be more than quarter of the total

study area; 2) density index = maximum number of individuals

heard calling in the area divided by the survey area covered by all

stations; and 3) abundance index is either a) = number of calling

birds heard divided by time spent to survey, expressed as birds/100

hours, or b) = number of calling birds heard divided by number of

stations from which birds were detected or distance between survey

stations, expressed as birds/station or kilometre (Gaston 1979).

Recommendations for surveying ground- dwelling birds in Asia

This method was developed because.it could be used for loud-calling

and territorial species over a large area in a short time span and was

8

SOMYING THUNHIKORN etal.

Forktail 32 (2016)

particularly suitable in rugged or difficult terrain. It was first used for

Himalayan Galliformes at a time when there was limited statistical

underpinning of population estimation and allowed measurements

to be made and understood. As our knowledge of the statistical

assumptions required to permit reliable measures develops and

the degree to which the ecology and behaviour of the target species

meets those assumptions is uncertain, there are questions about the

uselulness of this method without greater statistical underpinning.

For example, caution is required when translating numbers heard

into population measurements, unless it is known what proportion

of the population tends to call (e.g. all males and females or all males

and no females or only some males). Understanding social behaviour

ol gibbons has allowed the method to be applied in some contexts

in Thailand. Overall, there is currently insufficient understanding

of social and calling behaviour ol Asian birds to allow detections

to be translated reliably into population estimates.

Distance sampling

Distance sampling, using both line and point transects (see Field

protocols below), is based on the distance between the observer

and the animal. Distances to observed animals are measured as

the perpendicular distance from the line transect or as the radial

distance from a point transect. The method allows calculation of

a detection function, as the likelihood of detecting the species

decreases with increasing distance from the line or point (Buckland

etal. 1993, Thomas etal. 2010).

Assumptions

Recent advances in distance sampling (Buckland etal. 2001 , 2008,

Laake & Borchers 2004, Thomas et al. 2010), have allowed some

of the original assumptions to be relaxed, leaving three main key

assumptions: 1) individuals on the line or point are detected with

certainty; 2) individuals do not move; and 3) measurements are

exact — this is a key issue for aural detection in dense habitat as

measuring distances precisely is extremely difficult. To address this,

Gale etal. (2009), working in Thai forest, suggest grouping records

together in intervals (e.g. 5, 10, 15, 20, 25, 30, 40, 60, 80 and 100 m)

to reduce error. This can be done in two ways: 1) assigning records to

intervals during fieldwork, which is complicated when conducting

line transects by the need to calculate the perpendicular distance to

the transect line; 2) recording ungrouped data in the the field and

then grouping it prior to analysis (Buckland etal. 1993).

Field protocols

There are two principal field protocols for gathering distance

sampling data: line and point transects. Tine transects can have either

variable length or width or a fixed width or length (strip transect)

(Begazo & Bodmer 1998, Bernardo etal. 2011). An observer walks

along the line transect and records each individual of the target

species by estimating the perpendicular (i.e. shortest) distance from

the individual to the transect line (i.e. not the distance from the

individual to the observer). Point transects are counts from points

(rather than walking along transect) and may have a variable or fixed

radius and a fixed time for recording. These are likely to depend on

the species surveyed (Tarvine?^/. 1998,Marsden 1999, NorveD/^/.

2003, Howell etal. 2004). A thorough assessment of field protocols

and distance sampling’s underlying assumptions has been carried out

on Philippine forest birds by Lee & Marsden (2008). Marsden (1999)

explored the use of point counts for estimating hornbill abundance

on Buru and Seram, Indonesia.

Analysis

The first step in the analysis of distance sampling is modelling the

probability of detection as a function of distance from the point/

transect. This assumes that all individuals at zero distance (i.e.

on the line or point) are detected and that detectability usually

decreases with increasing distance from the line or point (Buckland

1993, Thomas et al. 2010). Most distance sampling analyses use

the standard DISTANCE software (Buckland et al. 1993, 2001,

Thomas et al. 2010) which can provide density estimates from

both line and point transect data. Other software can also be used,

such as the Bayesian approach to line transect analysis (Eguchi

& Gerrodette 2009), Bayesian software for imperfect detection

(Amundson et al. 2014) and the PAST software version 2.05

(Jolli & Pandit 2011). Encounter rates can also be determined for

an estimate of relative abundance (Ashrafe/^/. 2005, Wang etal.

2004). There is also a wide range ol ways in which the data can be

examined and the analytical process can be manipulated so that it

best matches the data gathered.

Recommendations for surveying ground- dwelling birds in Asia

Distance sampling, using both line transects and point counts, is

now recognised as the standard method for estimating density and

determining the probability of detection (i.e. the likelihood that an

individual will be detected if it is present). However, this method

typically requires a sample size of at least 60-80 detections for a

robust model (Buckland 1993). It is being increasingly used in Asia,

and in consequence developments have been required to ensure that

detection patterns of target bird species do not violate the method’s

critical assumptions (e.g. Gale et al. 2009, Lee & Marsden 2008,

Marsden 1999). Nonetheless, as there is a clear analytical protocol

for converting encounters (=detections) into population estimates,

this method should be considered lor surveying ground-dwelling

birds in Asia.

Line transects are suitable for sampling large areas of relatively

open homogeneous habitat and species that are easy to detect,

large or conspicuous and not especially mobile. It may not be

particularly suitable for highly mobile species because of the risk

ol double counting, whereby one individual may be counted two

or more times during one transect or count (Buckland etal. 1993,

Buckland 2006, Buckland etal. 2008, Greene 2012). They are useful

lor monitoring populations ol birds that occur at low densities and

they generate more detections than point transects. Line transect

estimates tend to have lower bias and higher precision (Buckland

2006, Gale et al. 2009).

Point transects are suitable for patchy, dense vegetation and

difficult terrain. The field protocol is sufficient to describe basic

biological patterns and is suitable for common forest species and

those occurring at high density, especially in species-rich habitats

where the observer can concentrate on detecting and identifying

each species. It is convenient and easier lor observers who have no

previous experience. Disadvantages include the risk of flushing a

target species as the observer approaches a point transect, and much

time can be lost travelling between points, which is not efficient for

low density species or for monitoring rare birds. It is not suitable for

large multi-species groups or situations where there is a high density

of individuals at the transect point. It is more sensitive to sampling

error because the area sampled by a point transect is calculated using

distance from observer to animal directly whereas for line transect

it is calculated using the perpendicular distance. However, it is

possible to reduce error in measurement distance by grouping data

into intervals or categories (Jarvinen & Vaisanen 1975, Buckland et

al. 1993, Buckland 2006, Buckland etal. 2008, Thomas etal. 2010,

Hartley & Greene 2012).

Camera trapping

In the 1880s, George Shira was the first to develop a method using

a trip wire and flash system in which a wild animal photographed

itself (Kucera & Barrett 2011). Camera trapping is now seen as a

method for studying rare and highly cryptic species and has been

used to assess species richness, community composition, activity

pattern, habitat selection, abundance and density. Karanth (1995)

Forktail 32 (2016) Methods used to survey avian species and their potential for surveying ground-dwelling birds in Asia

9

first used cameras to estimate tiger density in India, a species in

which individuals can be identified by their stripe pattern. This

was followed by the development of a sampling design to estimate

tiger population size and density across the country (Karanth &

Nichols 1998). Subsequently, camera trapping has developed to

allow population estimation of species in which individuals cannot

be recognised individually (see e.g. Rowcliffe etal. 2008, Samejima

et al. 2012) and for an Asian pheasant (Suwanrat et al. 2015).

Assumptions

There are two main population estimation techniques that use

camera trap data and each has assumptions. The first, which relies on

the identification of individuals of the target species, uses capture-

recapture and requires that: 1) the population size is constant

during the sampling period; 2) sampling is random; and 3) every

individual in the population has a capture probability greater than

zero (Harmsen etal. 2010). The second method, which does not need

individual identification, is repeated presence-absence and repeated

count survey and requires that: 1) animal detections are independent;

2) the population is closed (i.e. the number of individuals in the study

area is assumed to be constant across surveys); and 3) the detection

probability of a single animal is assumed to be constant across time

(Royle & Nichols 2003, Royle 2004). Estimating the trapping rate

for populations where members cannot be identified as individuals

requires that: 1) animals conform adequately to the model used to

describe the detection process; 2) photographs represent independent

contacts between animal and camera trap; and 3) the population is

closed (Rowcliffe et al. 2008, Foster & Harmsen 2012).

Field protocol

Camera traps should be set in an area by dividing it into a grid and

selecting a representative position which maximises the chances

of detecting the target species. The distance between camera trap

locations must be smaller than the territory size of the target

species to avoid ‘holes’ between camera traps (O’Connell et al.

2011, Foster & Harmsen 2012). However, for species that cannot

be identified individually, it is essential to ensure that the same

individual is not detected in two adjacent camera traps and this

is done by determining a time interval (e.g. 1 hour) after which it

is assumed that the records are of different individuals (Suwanrat

2015). Camera traps are generally left in the study area for 10-60

days. Some camera trap studies use bait and/or scent lures to attract

target species to increase the chances of their detection (Rovero et

al. 2000); however, this has consequences for the calculation of

detection probability and estimate of population or occupancy.

Analysis

Population estimation using camera trap data may involve one

of five methods. First, capture-recapture (CR), where every

individual in a sample can be identified using unique natural

markers to estimate abundance (Foster & Harmsen 2012). It can

be calculated in software packages such as CAPTURE (Rexstad

& Burnham 1992), the closed capture model in MARK (available

to download from http://www.phidot.org/software/mark) or using

the Rcapture Package in R (Rivest & Baillargeon 2015). Second,

capture-mark-recapture or capture-mark-resight, which is a

method that does not require that all animals in the sample are

marked. It estimates abundance using the frequency of marked

and unmarked individuals and can also be performed in software

packages such as mark-resight model in MARK and mra Package

in R (McDonald et al. 2015), This method does, however, require

that the number of marked animals is known and so a sample

of the population must be captured and marked prior to camera

trapping (Foster & Harmsen 2012). The third method is assessment

of the photographic rate (= capture rate), which does not require

the recognition of individuals to provide a density estimate. This

models the process of contact between animal and camera trap

(Rovero & Marshell 2009, Foster & Harmsen 2012) and is most

effective for species that are relatively wide-ranging (>1 km/day),

although it is necessary to know the speed at which the animal

moves. It is not suitable for territorial species or where the area to be

sampled is small (Rowcliffe etal. 2008). Fourth, occupancy/ repeated

presence-absence/repeated counts for species can be used where

individuals cannot be identified. This analysis can be conducted

using PRESENCE (Mackenzie etal. 2002, Royle & Nichols 2003,

Royle 2004) or MARK. Finally, spatially explicit capture-recapture

(SECR) models, which do not require the intermediate step of

estimating an effective trapping area. These models have advantages

over traditional capture-recapture models and can be conducted

in a range of programmes (Tobler & Powell 2013). Animals are

assumed to be distributed independently in space to occupy home

ranges. It can be used to provide density estimates using Program

DENSITY (available for download from http://www.otago.ac.nz/

density/) or SECR Package in R (Efford 2016).

After the abundance has been calculated, the density can be

determined when the effective sample area is known. This can be

done in two ways: 1) half of the mean maximum distance moved

by individuals between camera traps for those captured more than

once [‘mean maximum distance moved’ or MMDM]; and 2) half

of the diameter of an average animal’s home range (O’Connell et

al. 2011, Foster & Harmsen 2012).

Recommendations for surveying ground -dwelling birds in Asia

Camera trapping involves little disturbance to wildlife once cameras

are set and allows detection of ground-dwelling birds that are

otherwise found very rarely. Skill is required to select the location

for the cameras and then to set them to maximise the likelihood of

detections, depending on the target species. Camera trap sampling

offers many exciting prospects for field surveys with a range of

purposes, such as presence-absence, species richness and population

size (abundance and density) in an area. It is being increasingly used

in Asia, usually for ground-dwelling species (e.g. Samejima et al.

2012, Fi et al. 2010, Winarni et al. 2009)

Appropriate analytical methods for the estimation of density

are, however, still being developed and evaluated, as discussed above,

and challenges remain. For example, capture-mark-recapture

based on the frequency of marked and unmarked individuals

requires knowledge of the number of marked animals prior to

camera trapping (Foster & Harmen 2012) and assessment of the

rate at which a species is captured on cameras (where individuals

cannot be identified) requires the description and calibration of the

relationship between capture rate and density (Carbone etal. 2001,

Rowcliffe et al. 2008, 2013, Foster & Harmsen 2012). Although

challenges remain, analytical progress is rapid.

CONCLUSION

Each method we have reviewed has benefits for one group of

species or another. Two methods are based on ease of detection of

individuals in the target species (spot mapping and triangulation)

and their application to species in Asia requires careful assessment of

the robustness of the assumptions behind the analysis. Both distance

sampling methods are derived from a clear analytical framework that

translates field encounters into a reliable assessment of density. They

are based on explicit analytical assumptions and recent advances that

address some of the more difficult-to-satisfy assumptions mean that

these methods can now be used in more challenging field conditions

than previously. The final method, camera trapping, is based partly

on technology that allows the detection of individuals in species

that have long been very difficult to detect in adequate numbers for

any sort of population estimation. Methods for translating these

10

SOMYINGTHUNHIKORN etal.

Forktail 32 (201 6)

encounters into population estimates are developing rapidly and

are more robust for some species than others.

This review of methods may be used as a baseline for considering

what field method might be used to make a population estimate of

a bird species that either has characteristics that make it difficult to

detect or it occupies challenging terrain or habitat, such as mountains

or tropical rainforest. Whilst the specific requirements for any study

will depend on, amongst other factors, consideration of the detection

characteristics of the target species, the terrain and habitat, and the

question(s) being asked, some generalities can be drawn.

Distance sampling (line transect or point transect) appears

the most suitable method for species that can be detected (by sight

or call) at a close distance, and species that can be found at fixed

locations (such as display scrapes or dancing grounds) and do

not move much or move slowly (e.g. Grey Peacock Pheasant

Polyplectron bicalcaratum and Hainan Peacock Pheasant

P. katsumatae).

Population estimates of species that are difficult to detect

because they do not call or are visually cryptic and are mobile and

those where individuals can be recognised are best made using

camera trapping and capture-recapture techniques for abundance

and then estimating density. For mobile, cryptic species that are

not individually identifiable the most suitable field method is also

camera trapping, but the analytical procedure would be different.

Finally, although there is no formal statistical procedure for

making population estimates using spot mapping, this can still be

valuable in appropriate contexts. These include where the target

species is territorial, with appropriate conspicuous behaviour that

can be detected easily, and the sample area is compact and can be

easily traversed.

ACKNOWLEDGEMENTS

We sincerely thank the Royal Golden Jubilee PhD Program, The National

Research Council of Thailand for supporting ST. The British Council

provided financial support for ST to visit Newcastle University, UK, whilst

the manuscript was developed, and Newcastle University’s School of Biology

provided facilities.

Philip J. K. McGowan and SomyingThunhikorn contributed equally to

this work as senior authors.

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Somying THUNHIKORN, Conservation Ecology Program,

School of Bioresources & Technology, King Mongkut's

University of Technology Thonburi, 49 Soi Thian Thale 25, Bang

Khun Thian Chai Thale Road, Tha Kham, Bang Khun Thian,

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com

Matthew J. GRAINGER and Philip J. K. McGOWAN, School

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mcgowan@newcastle.ac.uk

Tommaso SAVINI, Conservation Ecology Program, School

of Bioresources & Technology, King Mongkut's University of

Technology Thonburi, 49 Soi Thian Thale 25, Bang Khun Thian

Chai Thale Road, Tha Kham, Bang Khun Thian, Bangkok 10150,

Thailand.

FORKTAIL 32 (2016): 14-25

A survey of the autumn 2009 and spring 2010 bird

migrations at Lhasa, Tibet Autonomous Region, China

JOHN D. FARRINGTON

Between July 2009 and May 2010 an extensive ornithological survey was carried out at Lhasa, Tibet Autonomous Region, China, in the city

wetland complex focused on the Lhalu Wetland National Nature Reserve and the adjacent Lhalu and Lhasa rivers wetland complex. Counts

were made along a series of transects on a weekly basis, generally consisting of two full field days each week. During the survey 113 avian

species were seen, with arrival and departure dates of most migratory species being determined: 21 species were summer visitors, 22 winter

visitors, 22 passage migrants, 12 altitudinal migrants, 3 vagrants, 1 probable escapee and 32 residents. Autumn migration began in early

September, continued until late December and was of particular interest for shorebird passage. Spring migration began in mid-February

and was ongoing in May when the survey was concluded; it was of particular interest for passage waterfowl. A review of, and comparison

with, historical records was made and a number of species that have undergone significant declines since the 1940s have been identified.

Sightings of Baikal Teal Sibirionetta formosa, Little Egret Egretta garzetta, Lesser Grey Shrike Lanius minor, Rufous-vented Tit Periparus

rubidiventris and Red-throated Pipit Anthus cervinus are believed to be the first in the Lhasa city area. The Lhalu Wetland National Nature

Reserve and the adjacent Lhalu River and Lhasa River wetland complex appear to qualify for designation as a Ramsar Wetland of International

Importance under Criterion 6 based on their Ruddy Shelduck Tadorna ferruginea population. The Lhasa wetlands also appear to qualify under

Criterion 2 based on the winter population of the Vulnerable Black-necked Crane Grus nigricollis and passage Common Pochard Aythya ferina.

INTRODUCTION

The city of Lhasa (29.650°N 91.1 17°E), Tibet Autonomous Region,

China, lies at about 3,650 m in the Lhasa River valley on the southern

Tibetan plateau. In spite of the high altitude, the combination of

intense solar radiation, a southerly latitude and relatively sheltered

location have created a mild microclimate within the much harsher

environments of the Chang Tang region to the north and the high

plateau to the south, both of which lie above 4,500 m. Average

monthly minimum and maximum temperatures at Lhasa over the

period 1955-2007 were about -9 to +7°C in January and 10-22°C

in July, the coldest and warmest months respectively (NMC 2014).

As a consequence of this mild climate, birds are abundant year-

round in the Lhasa valley, an important crossroads for various bird

migration routes between South Asia, the Tibetan plateau, Central

Asia and Siberia. Birds found in the Lhasa valley include winter

residents that breed to the north, summer visitors wintering at lower

altitudes to the south and east, passage migrants, and altitudinal

migrants found on the valley floor in winter and on the surrounding

mountain slopes in summer. In addition there are resident wetland,

grassland, bush and forest dwelling birds.

Although the birds of the Lhasa region have been quite

extensively documented (see e.g. Waddel 1905, Walton 1906, Ludlow

1950, Vaurie 1972, Zheng et al. 1983, Robson 1986, Bishop et al.

2000, Bishop & Drolma2007, Lang et al. 2007, Lagdore/v?/. 2009,

Lu 2009, Lu et al. 2010, Yang et al. 2011), there is little data about

the arrival and departure times of migrants. Published data on bird

migration at Lhasa has mainly been limited to general comments on

the months and seasons when species were seen (e.g. Ludlow 1950).

Although Vaurie (1972) collated bird sightings data from the field

notes of various explorers of the Tibetan plateau, these covered the

entire plateau over many decades and do not provide a systematic

evaluation of the timing of bird migration at any specific location.

In fact, the only reliable dates I was able to find for the arrival of

a given species at Lhasa were for the Grey-backed Shrike Lanius

tepbronotus — these lay between 15-25 April in five years between

1991 and 1998, and even then no departure dates were recorded

(Tsering 2000).

The avifauna survey reported here took place over nearly 10

months between July 2009 and May 2010; in addition to the dates

of sightings, counts of most species were also made. These provide

a record of both arrival and departure dates of migratory birds at

Lhasa, and of the period over which the greatest numbers of a species

passed through (see Appendix 1). During this survey, I recorded 113

species. Previously, between September 2005 and April 2008,1 made

opportunistic observations around Lhasa: during 2006 two species,

Little Owl Athene noctua and Common Rosefinch Carpodacus

erythrinus , the former regarded as resident and the latter as a summer

visitor, were recorded in the area surveyed in 2009-10 but were not

encountered during the survey itself. This brought the Lhasa species

count to 115,ofwhich81 were considered to be primarily migrants.

METHODS

The survey was made over a 43-week period from 1 1 July 2009 to

3 May 2010, although no observations were made between 25 July

and 24 August 2009. The survey ‘week’ was arbitrarily considered to

begin on Friday and observations, usually lasting 6-10 hours, were

normally carried out on two days — Saturday and Sunday — each

week, although in seven survey-weeks only one day was possible

whilst in four weeks three days were worked. A number of days were

cut short due to other commitments or bad weather (including a

severe sandstorm). Observations were made using lOx magnification

binoculars while walking and cycling a series of 16 selected transects

around Lhasa (Table 1). Identification was confirmed where

necessary using MacKinnon & Phillipps (2000) as the primary

reference and Grimmett et al. (1999) as a secondary reference.

The main focus of the survey was the Lhalu Wetland National

Nature Reserve along with the nearby Lhalu and Lhasa river

wetlands, although occasional observations were made in various

parks, wooded areas, shrub and pasturelands around the city (Table

1). The main study transects along the Lhalu wetland and Lhalu and

Lhasa rivers were surveyed, mainly on a weekly basis, permitting

the timing of the arrival and departure of migratory birds to be

documented to within about a week during the autumn and spring

migration periods. The weekly counts provide a conservative estimate

of the numbers of the various birds recorded on the transects,

allowing a good estimate of the relative abundance of the species

observed to be made.

RESULTS

Survey findings on the timing of migration through Lhasa on a

weekly basis are summarised in Tables 2-6, while detailed species

Forktail 32 (201 6) Survey of autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China

15

Table 1 . Summary of survey transects.

Note: Species' systematic names are listed in Appendix 1 .

Code

A

C

D

E

F

G

H

I

J

K

L

M

N

0

P

counts are summarised in Appendix 1. In terms of seasonal

occurrence in the environs of Lhasa city, of the 115 bird species

recorded, 22 were summer visitors (including Common Rosefinch,

see above), 22 winter visitors, 22 passage migrants, 12 altitudinal

migrants, 33 residents (including Little Owl, see above), 3 vagrants

(all probably first records for the Lhasa area — -see below) and

1 presumed escaped cage-bird — Crested Myna Acridotberes

cristatellus , seen only on 11 July 2009 at the east Lhalu wetland.

Autumn migration began in early September and continued

until late December: passage shorebirds were particularly

interesting. Seven species were not seen on return spring passage:

Common Snipe Gallinago gallinago, Wood Sandpiper Tringa

glareola, Temminck’s Stint Calidris temminckii , Ruff C. pugnax ,

Pacific Golden Plover Pluvialis fulva, Little Ringed Plover

Charadrius dubius and Lesser Sand Plover C. mongolus (Table 4).

Spring migration began in about mid-February and continued

at least into early May when the surveys were terminated. Spring

migration was of particular interest for waterfowl, with five species

not seen in autumn: Eurasian Wigeon Mareca penelope, Northern

Shoveler Spatula clypeata. Northern Pintail Anas acuta, Tufted

Y)ucV.Aythyafuligula and Baikal Teal Sibirionetta formosa (Tables

4 and 5). However, Eurasian Wigeon, Northern Pintail and Tufted

Duck over-winter in large numbers at Yamdrok Yumtso Lake, just 75

km south-west of Lhasa (Lang etal. 2007). Peak counts ofwintering

ducks occurred from about mid-January to late February, with small

numbers of a few species over-summering in Lhasa city, e.g. Ruddy

Shelduck Tadorna ferruginea , Goosander Mergus merganser and

Mallard Anas platyrhynchos (see Appendix 1). Conversely, a few

predominantly summer visitors also over-wintered in Lhasa in small

numbers, including Common Hoopoe Upupa epops. Oriental Turtle

Dove Streptopelia orientalis and Grey-backed Shrike (Appendix 1),

see also Lang et al. (2007). Altitudinal migrants began appearing

16

JOHN D. FARRINGTON

Forktail 32 (2016)

Table 3. Lhasa survey 2009-2010 arrival and departure dates of winter visitors.

on the valley floor between late September and early November and

typically departed in April and early May (Table 5). The greatest

species diversity was between 1 and 3 May 2010, when 58 species

were recorded (Appendix 1).

Although detailed notes on breeding were not kept, conspicuous

breeding species at Lhasa included Goosander (eight young seen

on the Lhasa river on 25 August 2007), Chinese Spot-billed Duck

Anas zonorbyncha (seen with young on 1 1 July 2009 in the east

Lhalu — see below), Common Moorhen Gallinula chloropus (seen

with one young on 27 September 2009 on the Lhalu River park

pond). Common Coot Fulica atra , (first young of the year seen on

25 April 2010 in the west Lhalu) and Grey-backed Shrike (fledged

young common in August and September around the Lhalu).

Sightings of particular interest

Chinese Spot-biiled Duck Anas zonorbyncha and

Indian Spot-billed Duck A. poecilorhyncha

Both Spot-billed Duck species (Carboneras & Kirwan 2016, del

Hoyo et al. 2016) were recorded on the Lhalu. A population of

Chinese Spot-billed Duck, distinguished by their brown tertials,

that bred on the Lhalu (see above) was last seen in 2009 on

24 October and not again until 24 April 2010. Birds with the

prominent white tertials characteristic of Indian Spot-billed Duck

A. poecilorhyncha were first seen on 17 October 2009 and over¬

wintered on the Lhalu, where one remained until 1 May 2010. The

first record of Spot-billed Duck at Lhasa was by Ludlow (1950) in

Forktail 32 (2016) Survey of autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China

17

winter 1943; He apparently only saw one pair of what is now known

as the Chinese Spot-billed Duck, indicating a significant increase in

this species at Lhasa since that time. Maximum counts during my

survey were 50 Chinese Spot-billed Ducks on 3 October 2009 and

39 Indian Spot-billed Ducks on 31 October — 1 November 2009.

Northern Shoveler Spatula clypeata

Although recorded by Ludlow (1950), there were no further records

from the Lhasa area for the rest of the twentieth century (Lang et

al. 2007). However, Yang etal. (2011) reported the species between

2006 and 2010, although without providing dates or locations. I first

recorded a single male Northern Shoveler on 24 February 2008 in

the middle Penpo valley, 27 km north of Lhasa. During the survey

period, the peak count was seven at the east Lhalu Wetland on 27

March 2010.

Baikal Teal Sibirionetta formosa

On 20 March 2010, a single male was observed for about 20 minutes

dabbling with the resident Common Coots on the shallow pond

in the Lhalu River park in west Lhasa (transect C), until flushed

by two stone-throwing boys. I have been unable to find any earlier

published records in the survey area and it is presumably a first

record. There are two earlier unpublished records of the species

from the broacier Tibetan plateau region, at Qinghai Lake on 28

October 2006 and in the vicinity of Lijiang, Yunnan, on 3 April

2007 (Hornskov 2006, 2007).

Derbyan Parakeet Psittacula derbiana (NT)

This species, a resident in the forests of Nyingchi prefecture, Tibet,

some 300 km east of Lhasa, is one of the most popular cage-birds in

Lhasa city and a feral population, presumably of cage-bird origin, is

present, although at risk of re-capture by traders (Lang etal. 2007).

The largest numbers are in the poplars of the Norbulingka (transect

K), although the species can occasionally be seen anywhere in the

city with a significant grove of trees.

Black-necked Crane Grus nigricollis (VU)

My first record of this species in Lhasa was a pair flying south

on 28 October 2005, high above the Tchip Valley (transect G),

while the last was on 20 March 2010 in the east part of the Lhalu.

Although the Black-necked Crane population as a whole may

be increasing (Farrington & Zhang 2013, Archibald et al. 2016,

BirdLife International 2016), changing agricultural practices in

wintering areas can make former crane habitat unsuitable (Bishop

Table 4. Lhasa survey 2009-2010 arrival and departure of passage migrants.

Table 5. 2009-2010 arrival and departure dates of altitudinal migrants on the Lhasa valley floor.

18

JOHN D. FARRINGTON

Forktail 32 (2016)

et al. 2000, Bishop & Drolma 2007). In the vicinity of Lhasa,

autumn ploughing of fields and the proliferation of greenhouse

farming have eliminated large tracts of former crane habitat, whilst

a willow planting campaign in 2008 in pastures near the confluence

of the Lhalu and Lhasa rivers made previously open crane habitat

unsuitable, as does late-winter gravel extraction from the bed of the

Lhasa River at the same location. The latter could easily be remedied

by re-scheduling seasonal gravel extraction operations to April,

after the cranes leave. The single largest group of Black-necked

Cranes seen in this area was about 75 on 31 January 2009, when

all gravel extraction and processing work stopped for several weeks

for the Chinese Lunar New Year holiday. This species probably

formerly bred in the area, as both Walton (1906) and Ludlow

(1950) reported Black-necked Crane chicks at Lhasa in summer.

Temminck's Stint Calidris temminckii

A maximum count of two over three consecutive survey-weeks

between 27 September and 11 October 2009, on the sandy bed

of a concrete canal pond in the north-east of the Lhalu wetland.

Although recorded widely on the Tibetan plateau, the only mention

of the genus I have found in Lhasa is simply 'Erolia sp. Stints pass

through Lhasa in autumn’ (Ludlow 1950, Vaurie 1972).

Pacific Goiden Plover Pluvialis fulva

One recorded on the east Lhalu wetland on 1 1 October 2009 is the

first known record from Lhasa since an observation ‘in autumn’

1942 by Ludlow (1950). Walton (1906) noted that he shot the only

representative of this species that he saw at Lhasa, on 1 3 September

1904.

White-tailed Eagle Haliaeetus albicilla

Regularly recorded at Lhasa from 28 November 2009 to 20

February 2010. On 17 January 2010 a group of eight, including

three juveniles, was bickering over a large fish caught from the

Lhasa River levee ponds (transect E). A pair was regularly seen on

a meadow in the east Lhalu, whilst others often rested on the gravel

bars at the confluence of the Lhasa and Lhalu rivers. Robson (1986)

first recorded the species in the same general area on 4 March 1986.

The highest count during this survey was 11 on 23 January 2010,

whereas the highest count reported by Lang et al. (2007) was four

on 22 December 1991.

Cinereous Vulture Aegypius monachus (NT)

Regularly seen either circling over or resting on the gravel bars near

the confluence of the Lhalu and Lhasa rivers between 28 November

2009 and 31 January 2010, with a high count of six resting there

on 17 January 2010. First recorded by Robson (1986) in the same

general area, with two seen on 4 March 1986; Lang et al. (2007)

never saw more than one bird at a time.

Little Egret Egretta garzetta

Eight on the east Lhalu wetland on 11 July 2009 may be a first

record for Lhasa since no earlier records could be located. This

group appeared to have summered on the Lhalu, with five last seen

on 17 October 2009. The following spring only one Little Egret

was seen, on 17 April 2010, although the species may simply be a

late spring arrival at Lhasa. Farrington et al. (2013) reported the

recent appearance of the Little Egret on the north Tibetan Plateau.

Lesser Grey Shrike Lanius minor

A single bird was perched on rock piles in a barren field near the

mouth of the Lhalu River on 15 and 22 November 2009, some

2,000 km south-east of the species’s usual Central Asian breeding

grounds. A snowstorm in western China a month earlier (Xinhua

Forktail 32 (201 6) Survey of autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China

19

2009) may have played a role in the bird’s appearance; it is believed

to be a first record for the Lhasa region.

Bluethroat Luscinia svecica

On 12 September 2009 a bird was skulking at the water’s edge

under Datura stramonium plants on a pond dyke in the east Lhalu

wetland. Recorded up to the end of the 1940s between Lhasa and

the Chumbi valley, mostly in September and October, by Walton

(1906), Ludlow (1950) and Hugh Richardson; I have been unable to

find any further records of this species between the 1940s and 2009.

Author’s note: according to Ludlow (1950), Hugh Richardson lived

in Lhasa from 1936 to 1940 and between 1946 and 1950.

Rufous-vented Tit Periparus rubidiventris

I saw single birds on three occasions, in the forest below Drepung

Monastery (transect F) on 22 November 2009 and in the willow

groves in the south-east Lhalu Wetland on 10 and 25 January 2010.

I have found no other records from Lhasa and this may be a first

record for the Lhasa city area.

Bam Swallow Hirundo rustica

The only previous record of this species for the Lhasa region is an

unspecified sighting (Yang etal. 2011) between October 2006 and

January 2010. During my survey, a maximum of six Barn Swallows

were regularly seen over the eastern Lhalu wetland between 18 July

and 19 September 2009. The lack of earlier records suggests that

it is a relatively new summer visitor to Lhasa. The species was not

seen in spring 2010 and presumably arrived after 3 May, the last

day of observation. In 201 1, at the Longbao Reserve, Qinghai, Barn

Swallows were first recorded on 3 June (Farrington etal. 2013).

Plain Laughingthrush Garrulax davidi

Although endemic to the north-east Tibetan plateau and northern

China, released/escaped cage-birds are seen in Lhasa (Lang et al.

2007) and a feral breeding population maybe establishing itself in

the city. The largest number seen was seven birds around willow

thickets in the south-east Lhalu wetland on 20 March 2010.

Red-throated Pipit Anthus cervinus

On 25 April 2010 a bird in breeding plumage recorded on a short-

cropped, swampy meadow in the north-east Lhalu wetland, with a

flock of Oriental Skylarks Alauda gulgula, is believed to be a first

record for the greater Lhasa region.

Plain Mountain Finch Leucosticte nemoricola

Although the species is fairly common on mountain slopes and open

valleys of the Himalaya and the Tibetan plateau, the only previous

record from Lhasa was on 11 July 2005 at Drepung Monastery

(Thorne & Thorne 2007). During my survey, the species was first

seen on 16 January 2010 in shrub thickets in the north-east Lhalu

wetland, where it was fairly common, with a peak count of 35 on

16 February. The last sighting was on the eastern Lhalu valley floor

on 3 April 2010.

DISCUSSION

Notably, one large caveat to the survey results was that the Lhasa

River was not visited during March 2010, thus species found

primarily on transects D and E are probably under-reported for that

month. A subtlety of the migration pattern of Goosander through

Lhasa not revealed by Appendix 1 is that the first females were seen

on 1 3 September 2009 whereas mature males were not seen until 1

November, 49 days later. A number of resident high-altitude species

relatively common elsewhere in the Lhasa region and beyond were

conspicuously absent throughout; these included Rufous-necked

Snowfinch Pyrgilauda ruficollis and White-rumped Snowfinch P.

taczanowskii, Tibetan Lark Melanocorypha maxima and Tibetan

Eared Pheasant Crossoptilon harmani.

Despite weekly observations during my survey, I was unable to

determine the arrival and/or departure dates as well as seasonality

ol occurrence for the following 18 species: Gadwall Marecastrepera,

Mallard, Goosander, Eurasian Cuckoo Cuculus canorus , Pacific

Swi hApuspacificus, Common Greenshank Tringanebularia, Green

Sandpiper T. ochropus , Pallas’s Gull Larus ichthyaetus , Brown¬

headed Gull L. brunnicephalus , Little Egret, Hodgson’s Redstart

Phoenicurus hodgsoni , Rufous-vented Tit, Barn Swallow, Asian

House Martin Delichon dasypus , Greenish Warbler Pby/loscopus

trochiloides , Rosy Pipit Anthus roseatus , Brown Accentor Prunella

fulvescens and Beautiful Rosefinch Carpodacus pulcherrimus. The

data available for these species is summarised in Tables 2-6.

A review of Walton (1906) and Ludlow (1950) revealed that, in

addition to the significant sightings included in the results section

above, the status of the following migratory and resident species

has changed significantly since the first half of the 20th century.

Ferruginous Duck Aythya nyroca (NT)

Described by Walton (1906) as breeding at Lhasa and far

outnumbering other duck species in August and September; Ludlow

(1950) noted that it was common and breeding at Lhasa. However,

the highest count in my survey was only 10 birds, on 20 November

and 26 December 2009, both in the west Lhalu wetland. It was not

seen in summer: the first sighting was on 1 November 2009, with

two birds still present on 1 May 2010. This species was not reported

by Lang et al. (2007) but was recorded by Yang et al. (2011). My

earlier records were at the Lhasa River levee ponds — on 13 and 24

February 2007 (not counted: seven birds) and on 23 December

2007 (two birds).

Eurasian Wryneck Jynx torquilla

Observed by both Walton (1906) and Ludlow (1950) who regarded

it as ‘fairly common’. The last known record of this species is from

Zheng etal. (1983), who made their last survey at Lhasa in 1976.

Common Coot Fulica atra

Walton (1906) noted that Common Coots abounded in the marshes

at Lhasa, but were not seen elsewhere in southern Tibet. However, the

species was not mentioned by Ludlow (1950) and not recorded again

until Lang et al. (2007), who considered it uncommon. Although

depicted as a winter visitor to southern Tibet (MacKinnon & Phillips

2000, del Hoyo & Collar 2014), the species is now resident at Lhasa

and the most numerous species seen there year-round.

Solitary Snipe Gallinago solitaria and Pintail Snipe 6, stenura

Solitary Snipe Gallinago solitaria was listed by Ludlow (1950) as

common in autumn and winter, whilst he listed Pintail Snipe G.

stenura as an autumn passage migrant. During my survey. Common

Snipe on autumn passage were distinguished by the white trailing

edges to their wings. Most snipes not identified as Common Snipe

were gregarious and had buff-coloured face markings. They were seen

at the same location on the banks ol the Lhalu River near its mouth

between 18 October 2009 and 7 February 2010, the largest group

being eight on 8 November 2009. These were thought to be Pintail

Snipes, apparently winter visitors, not passage migrants. I did not

definitively identify a Solitary Snipe.

Osprey Pandion haliaetus

Only recorded at Lhasa by Ludlow (1950) who saw it ‘occasionally .

Pallas's Fish Eagle Haliaeetus leueoryphus (VU)

Recorded by Walton (1906) as ‘oftefi seen at Lhasa’ and by Ludlow

(1950) as ‘not uncommon’, but not recorded subsequently.

20

JOHN D. FARRINGTON

Forktail 32 (2016)

Great Cormorant Phalacrocorax carbo

Walton (1906) recorded this species in August and September;

Ludlow (1950) noted that it was common in autumn, but not seen

‘in the depth of winter’. During my survey this species was a winter

visitor, seen in Lhasa only from 1 November 2009 until 18 April

2010, with a peak count of 34 along the Lhasa River on 31 January

2010.

Common Raven Corvus corax

Waddel (1905) found Common Ravens Corvus corax to be ‘the

commonest of all the birds’ in south-central Tibet, Walton (1906)

noted that they were ‘common everywhere’ in southern Tibet and

Ludlow (1950) said that they came to Lhasa ‘in their hundreds to

roost on Chogpori’, 0.5 km west of Potala Square. During my survey,

I did see not a single raven in Lhasa, although the species was regularly

seen in small numbers around rural communities on the Tibetan

plateau. This change is probably due to increased urbanisation in the

Lhasa valley and improved methods of garbage disposal.

Hodgson's Redstart Phoenicurus hodgsoni

This species, described by Ludlow (1950) as ‘common in summer’

at Lhasa, is now rather rare.

Blue-fronted Redstart Phoenicurus frontalis

According to Ludlow (1950), this species was only recorded at Lhasa

by Hugh Richardson (see above); today it is still fairly common in

the Himalaya and eastern Tibetan Plateau.

Red-rumped Swallow Hirundo daurica

Described as very common in summer at Lhasa by Walton (1906)

and Ludlow (1950), this species has not been recorded at Lhasa

since, although it is common elsewhere on the east Tibetan plateau,

notably in the river valleys on either side of Jyekundo in Qinghai.

The Barn Swallow, apparently a recent arrival in Lhasa (see results

above), may be moving into the vacant niche.

Giant Babax Babax waddelli (NT)

Although recorded by Waddel (1905) and Walton (1906) elsewhere

in southern Tibet, Ludlow (1950) first recorded this species in Lhasa

city, noting that it was ‘moderately common’ and ‘a favourite cage

bird’. During my study, a single pair was seen several times in winter

and spring in willow and sea buckthorn thickets on the east side of

the Lhalu wetland. The apparent decline is presumably due to the

recent rapid urbanisation of Lhasa and to trapping for the cage-bird

trade. It remains locally common in suitable brushy habitat around

rural communities outside Lhasa.

Several factors may have influenced changes in populations of

migratory birds at Lhasa. Perhaps the most dramatic has been the

rapid urbanisation that began in the late 1980s and which has led to

the disappearance of large areas of parkland, agricultural land and

wetlands as the city has grown. For example, Li (2005) estimated

that the area of the Lhalu wetland declined from 12 km2 in 1951 to

6.2 km2 in 2000. A second more positive development has been a

partial restoration of the eastern Lhalu wetland from 2008-2009,

which converted about 125 ha of wet meadow heavily grazed by

cows to diked open-water ponds of varying depth. At the height of

the decline of the Lhalu in 2002, before it was declared a national

nature reserve in 2005, Li (2005) stated that only 28 species of birds

occurred there and only five were seen regularly (Li 2005, Li & Pan

2013). The present survey recorded 89 bird species on the Lhalu and

in adjacent poplar groves and willow/sea buckthorn thickets (Tables

2-6), with duck numbers on the Lhalu having increased as a result

of the wetland restoration.

A third major factor affecting bird migration patterns at Lhasa

is certainly climate change. Harrer (1954) described ice-skating on

a tributary of the Lhasa River in the late 1940s; ice-skating was not

possible at any time during my stay in Lhasa from 2005 to 2010,

although a thin layer of ice does still partially cover the Lhalu

in winter. Climate change impacts on the Tibetan plateau since

the late 1970s have included rising temperatures and a decline in

the area of shallow, permafrost-controlled wetlands favoured by

migratory waterfowl (Wang et al. 2006, Farrington 2009). One

possible consequence of warming plateau temperatures may be

the arrival in Lhasa of Cattle Egret Bubulcus ibis and Little Egret,

species more typical of the tropical lowlands of South and South-

East Asia. Cattle Egrets were first recorded at Lhasa by Lagdor

et al. (2009) during their 2002-2003 survey, although Vaurie

(1972) reported a record from Gyangtse before 1950. Warming

temperatures, and presumably less ice on wetlands, may also explain

why Ferruginous Duck and Great Cormorant now over-winter at

Lhasa whereas formerly they did not appear to do so (e.g. Ludlow

1950, Lang et al. 2007). With the great interest in recent years

in emerging climate change impacts on bird migration (Cotton

2003, Ahola et al. 2004, Crick 2004, Moller et al. 2008), it is

hoped that this study will provide a good phenological snapshot

for future comparison.

Finally, the Lhalu Wetland National Nature Reserve and the

adjacent Lhalu River and Lhasa River wetland complex appear

to qualify for designation as a Ramsar Wetland of International

Importance under Criterion 6 based on their Ruddy Shelduck

population, with a maximum count of 1 ,200 (Appendix 1), which

greatly exceeds the present minimum required species 1% threshold

of 710 (Ramsar 2009, Wetlands International 2013). The Lhasa

wetlands also appear to qualify under Criterion 2, whereby a

wetland is considered internationally important if it supports

Vulnerable, Endangered or Critically Endangered species (Ramsar

2009), based on the wintering Vulnerable Black-necked Crane and

passage Common Pochard populations.

ACKNOWLEDGEMENTS

This study, although not funded, was made possible by the many colleagues

who supported my stay in Lhasa, to whom I am eternally grateful for that rare

opportunity. My thanks also go to other colleagues who provided reference

material or helped to identify birds from images. Special thanks go to Graham

Kern for library research on my behalf and to Zelma Menard for sharing her

love of birds with my family.

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Forktail 32 (2016)

Appendix 1-1 Lhasa species counts July to December 2009.

Notes: for details of transects see Table 1 ; a transect letter in brackets, e.g. (A), indicates that this transect was only partially completed on a given day;'x' indicates that a species was seen but not counted; peak

survey species counts for the complete survey are shown in bold. Status in Lhasa: R = resident, W = winter visitor, S = summer visitor, P = passage migrant, A = altitudinal migrant, V = vagrant.

C V >_

. — rsj

Date (2009) :=

P Wood Sandpiper Tringa glareola

P Common Sandpiper Actitis hypoleucos

P Temminck's Stint Calidris temminckii

P Ruff Calidris pugnax

R Ibisbill Ibidorhynchastruthersii

P Pacific Golden Plover Pluvialis fulva

P Little Ringed Plover Charadrius dubius

P Kentish Plover Charadrius alexandrirws

P Lesser Sand Plover Charadrius mongolus

W Northern Lapwing Vanellus vanellus

W Pallas's Gull Larus ichthyaetus

W Brown-headed Gull Larus brurnicephalus

S Common Tern Sterna hirundo

R Black Kite Milvus migrans

W White-tailed Eagle Haliaeetus albicilla

R Bearded Vulture Gypaetus barbatus

R Himalayan Griffon Gyps himalayensis

W Cinereous Vulture Aegypius monachus

W Hen Harrier Circus cyaneus

W Common Buzzard Buteo buteo

W Long-legged Buzzard Buteo rufinus

W Upland Buzzard Buteo hemilasius

R Golden Eagle Aguiia chrysaetos

R Common Kestrel Falco tinnunculus

P Great Crested Grebe Podiceps cristatus

3 3

1 2

10 18 22

13 3

2

31 33 27 62 54 17 32 28 22

10 19 20 44 70 50 46

5 3

2

62

3 7

2 1

15 20

48 63

2 2

1

2

1 1

1 2

Forktail 32 (2016) Survey of autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China

23

<L> 4=-

_Q *-»

O O

t— -O

QJ £=

Date (2009)

24

JOHN D. FARRINGTON

Forktail 32 (2016)

Appendix 1-2 Lhasa species counts January to May 2010.

Notes: for details of transects see Table 1 ; a transect letter in brackets, e.g. (A), indicates that this transect was only partially completed on a given day; Y indicates that a species was seen but not counted; peak

survey species counts for the complete survey are shown in bold.

Date (2010)

rvj m

ABE

(A) (B)

Eurasian Cuckoo (uculuscanoms

Derbyan Parakeet Psittacula derbiana

Pacific Swift Apus pacificus

Eurasian Eagle Owl Bubo bubo

Rock Dove Columba livia

Hill Pigeon Columba rupestris

Oriental Turtle Dove Streptopelia orientals

Black-necked Crane Grusnigricollis

Common Moorhen Gallinula chloropus

Common Coot Fullcaatra

Pintail Snipe Gallinagostenura

Common Snipe Gallinagogallinago

Common Redshank Tringa totanus

Common Greenshank Tringa nebularia

Green Sandpiper Tringa ochropus

Wood Sandpiper Tringa glareola

Common Sandpiper Actitis hypoleucos

Temminck's Stint Calidris temminckii

Ruff Calidris pugnax

Ibisbill Ibidorhynchastruthersii

Pacific Golden Plover Pluvialis fulva

Little Ringed Plover Charadrius dubius

Kentish Plover Charadrius alexandrinus

Lesser Sand Plover Charadrius mongolus

Northern Lapwing Vanellusvanellus

Pallas's Gull Larus ichthyaetus

Brown-headed Gull Larusbrunnicephalus

Common Tern Sterna hirundo

Black Kite Milvus migrans

White-tailed Eagle Haliaeetus albiciila

Bearded Vulture Gypaetus barbatus

Himalayan Griffon Gyps himalayensis

Cinereous Vulture Aegypiusmonachus

Hen Harrier Circus cyaneus

Common Buzzard Buteo buteo

Long-legged Buzzard Buteo rufhus

Upland Buzzard Buteo hemilasius

Golden Eagle Aquila chrysaetos

Common Kestrel Falco tinnunculus

Great Crested Grebe Podiceps cristatus

80

4

2

1

317

5

387

2

3

2

2

34

3

24

23

59

5

1

380

3

11

2

75

1

276

x

76

13

372

2

25

45

2 1

57

3

2

282

34

27

9

6

1

229

20

3

3

70

3

2

5

120

12

22

6

x

53

33

10

29

23

4 4 2 3

234 223 229 243

14

38

2

7

34

35

24

2

192

30

5 3

2

1

19 29 20 57 25 40

28

1 37

2 2 1

40 5 64 31 55

1

11

2 2

1 1

2

7

35

1

1

55

2 1

1

2

2 1

3 2 2 2

1 1 3

1

10

26

3

167

37

2

2

26 21 2

55 90 81 90 45 94 115 36 25

32 54 120 214 142 105

1 7

1 1

Forktail 32 (2016) Survey of autumn 2009 and spring 2010 bird migrations at Lhasa, Tibet Autonomous Region, China

25

FORKTAIL 32 (2016): 26-35

An inventory of the avifauna of the Bukit Batikap

Protection Forest, Central Kalimantan, Indonesia

JOHANNES H. FISCHER, NICHOLAS S. BOYD, ADHY MARULY, ANNA-SELMA VAN DER KAADEN,

SIMON J. HUSSON & JAMARTIN SIHITE

We carried out a two-year inventory of the avifauna of the Bukit Batikap Protection Forest, located in the north-west of Central Kalimantan,

Indonesia. A total of 275 species were recorded, one of which is classified as Critically Endangered, two as Endangered and 11 as Vulnerable

in the IUCN Red List (2015). In addition, 20 species were endemic to Borneo and one undescribed species ('Spectacled Flowerpecker') was

recorded in Indonesia for the first time. A further two species were new records for Kalimantan and four were new for Central Kalimantan

province. Together, our results highlight the high conservation value of the Ulu Barito Important Bird Area.

INTRODUCTION

Until now most ornithological work on Borneo has been carried

out in the Malaysian part of the island (the states of Sarawak and

Sabah) and in coastal areas of Kalimantan, Indonesia (Mann 2008).

The northern interior of the province of Central Kalimantan, in

common with many other inland and montane areas of Kalimantan,

has received little attention. Among the only published information

is a series of reported sightings from short visits to this area by

Holmes & Burton (1987) and a later detailed study on the Busang

and Murung rivers by Wilkinson et al. (1991). Results from these

surveys led to the declaration of the Ulu Barito Important Bird and

Biodiversity Area (IBA), as designated by Birdlife International

(2014) based on the presence of globally threatened, range-

restricted and biome-restricted species (criteria Al, A2 and A3).

No further surveys in this part of Central Kalimantan were carried

out until very recently (Woxvold & Noske 2011, van Berkel et al.

2012, CWeyne et al. 2012) and these have improved our knowledge

of the biodiversity of the region. In this paper we build on these

earlier studies by presenting the results of an avifaunal inventory

of Bukit Batikap Protection Forest. This is the most northerly part

of the Ulu Barito IBA that has been surveyed to date.

The Bukit Batikap Protection Forest is located entirely within

Murung Raya district of Central Kalimantan province and is part

of the Muller-Schwaner mountain ranee that forms the central

O

spine of Borneo and from which all major rivers originate. It

is a 456,000 ha area of almost undisturbed tropical rainforest,

surrounding the headwaters of the Joloi and Busang rivers, two

major tributaries of the Barito River. Elevations range from 100 m

to 1,580 m. Forest vegetation at lower elevations is dominated by

trees of the Dipterocarpaceae family, resulting in mixed dipterocarp

forests typical of the interior of Borneo. At around 200 to 350 m

the forest type changes to hill forest characterised by reduced

diversity of dipterocarp trees. This type of forest was encountered

up to 750 m. Patches of kerangas (heath forest on peaty soils) were

rare in the area. The Ulu Barito IBA is protected for the purpose of

watershed conservation and logging is prohibited here. Therefore,

the vast majority of the forest is in primary condition, although

a few large timber trees have been illegally felled in areas close to

rivers. Strips of riparian forest are present along all rivers, as well

as secondary regrowth from historical crop cultivation. The local

populace from small villages outside the protected area enter to

collect products of commercial value, 'mchi&inggaharu (Agarwood

Aquilaria malaccensis), gold, swiftlet nests, fish, and other wildlife

for meat and the pet trade, as well as body parts. The forest is

the site of an orangutan reintroduction project with over 130

Bornean Orangutans Pongo pygmaeus reintroduced by the Bornean

Orangutan Survival Foundation (BOSF) by late 2014 (Husson et

al. 2015). The objective of our avifaunal inventory was to describe

the bird diversity of the area and, to a lesser extent, to understand

the breeding and migratory behaviour of the species present.

METHODS

All observations were made in the Joloi-Posu Valley in the

south of the Protection Forest (Figure 1), bounded by 0.159°N

to 0.085°S and 113.466°E to 113.619°E, by researchers based at

Camp Totatjalu Held station (0.041°N 113.499°E). Sightings

were recorded by four experienced birdwatchers (JF, NB, AM and

AvdK) from January 2014 to December 2015, covering both dry

and wet seasons (Table 1). Sightings were mostly collected between

06h00 and 22h00, with occasional exceptions where sightings

were also made in early morning (from 04h00) and at night-time

Table 1. Periods during which avian species were recorded at Bukit

Batikap Protection Forest, Central Kalimantan, Indonesia, by Adhy

Maruly (AM), Anna van der Kaaden, (AvdK), Johannes H. Fischer (JHF)

and Nicholas S. Boyd (NSB).

Fig ure 1. Map showing the study location in Bukit Batikap Protection

forest, within Central Kalimantan (inset), and major rivers.

Forktail 32 (2016)

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia

27

(until OOhOO). We identified birds visually with the aid of Myers

(2010) and Phillipps & Phillipps (201 1, 2014) and by calls usingthe

database xeno-canto (www.xeno-canto.org). Information was also

provided by local people from nearby villages, but a conservative

approach was used when evaluating this data. For all sightings we

noted the number of individuals, altitude, date, sex and age where

possible. Furthermore, we recorded evidence of nests and nesting

behaviour as well as information on roosting and lekking sites. Note

that the study was not designed to estimate population densities.

Most sightings originated from altitudes between 150 to 280 m

along the rivers and their associated edges as well as the forest

interior. Occasional visits to hills provided sightings from altitudes

up to 750 m and occasional visits further downstream provided

sightings from altitudes between 150 m and 120 m.

RESULTS AND DISCUSSION

During our survey we recorded a total of 275 species (Appendix

1), of which 20 were endemic and one near-endemic to Borneo,

74 species were classified as Near Threatened, 11 as Vulnerable, 2

as Endangered and 1 as Critically Endangered (IUCN 2015). Of

the 275 species we confirmed that 251 were known to be residents

of Borneo, 30 were winter visitors and 17 were passage migrants,

with some species falling into more than one category (Mann

2008). Furthermore, one species previously not known to occur in

Indonesia, ‘Spectacled Flowerpecker’ species novum , two species

previously unknown from Kalimantan — Malayan Night Heron

Gorsachius melanolophus and Zappey’s Flycatcher Cyanoptila

cumatilis — and four species previously unknown from Central

Kalimantan — Red-legged Crake Rallina fasciata , Peregrine Falcon

Falco peregrinus. Scaly-breasted Bulbul Pycnonotus squamatus and

Paddyfield Pipit Anthus rufulus — were present in the study area.

Some of the threatened species were seen in fairly large numbers

and this demonstrates the importance of the area for bird diversity

and conservation, and boosts the IBA status accorded to the Ulu

Barito region of Central Kalimantan.

A considerable amount of time (almost nine months) was spent

on site and included the migration and fruiting seasons, as well as a

masting event. This enabled us to record a higher number of species

than earlier studies, thus portraying the huge bird diversity of this

part of Borneo. However, it should be noted that the study was

biased towards the lowlands of Bukit Batikap Protection Forest

and therefore that sub-montane and montane species are likely

to be under-recorded. In addition, it should also be noted that

some species were not recorded, e.g. Bornean Crestless Fireback

Lophura pyronota, Bonaparte’s Nightjar Caprimulgus concretus ,

Cinnamon-headed Green Pigeon Treron fulvicollis , Hook-billed

Bulbul Setornis criniger and Brown-backed Flowerpecker Dicaeum

everetti. This may due to the rarity or unobtrusiveness of certain

species, or their dependence on habitats that are scarce in the area.

On the other hand, they may simply not be present as absence

remains a hard thing to prove (Tingley & Beissinger 2009).

Bukit Batikap Protection Forest is currently protected for

forest and wildlife conservation, but several species are nonetheless

exploited for a number of purposes, including the cage-bird trade,

which targets species such as Straw-headed Bulbul Pycnonotus

zeylanicus (resulting in its potential local extinction); leafbirds

Chloropsis spp., Blue-rumped Parrot Psittinus cyanurus and Blue-

crowned Hanging Parrot Loriculus galgulus\ hornbill heads for

trade (see species accounts below) and swiftlet Collocalia spp.

nests for human consumption, a major economic activity in this

region. Several timber products are also sourced here. Although

the surrounding forests are part of the same IBA, they are not

protected. Instead they are designated for logging and coal

mining, and the development of road networks may cause future

encroachment and conversion to large-scale agriculture, such as

oil palm plantations. Despite these threats, the Bukit Batikap

Protection Forest is located in the heart of one the largest remaining

expanses ol tropical rainforest in the world and the diversity of birds

and other wildlife here reflects that. Conservation actions by BOSF

and the Indonesian Government to protect (recently) reintroduced

orangutans give hope for the continued protection of these forests.

Selected species accounts

In the following section, we present notes on records of species

classified as Critically Endangered, Endangered or Vulnerable in

the IUCN Red List (2015), all endemic species and other species

we consider notable. Taxonomy and nomenclature in the following

section is based on Inskipp et al. (1996). Species deviating from

Inskipp et al. (1996) are marked with an asterisk (*).

Long-billed Partridge Rhizothera longirostris (NT)

A pair was heard duetting close to Posu River (160 m) from late

October to early November 2014 as well as in March 2015. This is

the third record of this species from Central Kalimantan (Mann

2008).

Black Partridge Melanoperdix nigra ( VU)

According to some local people, this species is not uncommon in the

area, although others are completely unfamiliar with it. During this

survey, it was recorded with certainty on three occasions from three

different localities (between 170 and 210 m). All observations were

of groups of four to eight individuals. This species was most likely

under-recorded due to the fact that its vocalisations remain little

known (van Balen & Fischer 2016). To establish better knowledge

about the status and distribution of Black Partridge, a study of its

true vocalisations is needed (BirdLife International 2001, van Balen

& Fischer 2016).

*Bornean Crested Fireback Lophura ignita (NT)

This Bornean endemic seems to be much more common than

Bulwer’s Pheasant L. bulweri , the other Lophura pheasant found

in this area. Individuals were seen weekly between January and

May 2014 and daily during the fruiting season in June and July

2014, but less regularly from October 2014 to December 2015. It

was observed that this species is actively snared in Bukit Batikap

Protection Forest. We treat this as a new endemic species following

McGowan et al. (2014).

Bulwer's Pheasant Lophura bulweri (VU)

Local people claimed to know of up to three leks of this Bornean

endemic. One presumed lekking site at 200 m was visited twice.

On 24 January 2014, one or two individuals were heard calling

around lOhOO, but remained out of sight, similar to descriptions

in Phillipps & Phillipps (201 1). On 27 February 2014, the lek was

visited again around llhOO, but nothing was recorded. On a later

date, a female was observed crossing the Posu River (160 m), not

far from this lekking site. Singles and small groups of up to eight

individuals were occasionally recorded foraging on the riverbanks

of Posu and Joloi Rivers between February and July 2014, but none

were recorded in January 2014 nor between October 2014 and

December 2015. Some local people said that Bulwer’s Pheasants

were only present between February and September, but others were

unfamiliar with any migratory behaviour. More surprisingly and

worryingly, one resident stated that male birds were occasionally

caught at lekking sites, not for food, but in order to make local cock

fights more entertaining.

Bornean Peacock Pheasant Polyplectron schieiermacheri (EN)

Most local inhabitants were also familiar with this Bornean

endemic and described it as rare or very rare. A calling male was

28

JOHANNES H. FISCHER etal.

Forktail 32 (2016)

heard on several dates close to the field station (160 m) and a male

and female were observed here. Later a female was observed crossing

the helipad close to the field station, suggesting that this species

might not avoid open spaces within the forest. A male was also seen

crossing Joloi River far upstream (180 m) and one was heard calling

in the same area on a later date. Two males were heard calling to

each other west of Joloi River (200 m), indicating at least two, and

quite possibly four, territories in the area. A sound recording of

this species can be found on www.xeno-canto.org (XC180008).

However, no vocalisations were heard from October 2014 to

December 2015. There are few recent records of this rare pheasant

(Frederiksson & Nijman 2004, Wielstra & Pieterse 2009).

Malaysian Honeyguide Indicator archipeiagicus (NT)

Observed at two different locations (190 m and 350 m); these are

the third and fourth documented records for Central Kalimantan

of this species (Mann 2008, Woxvold & Noske 201 1). A recording

of its call can be found on www.xeno-canto.org (XC177935).

Maroon Woodpecker Blythipieus rubiginosus

The most commonly encountered woodpecker in this area. A nest

was found in a small tree 1 m above the ground on 13 April 2014,

contradicting Myers (2010) who states that this species nests at

20 m or higher.

Great Slaty Woodpecker Mulieripicus pulverulentus (V U)

Recorded on several dates from different localities (between 160

and 180 m). One unusually large group of six individuals was found

by the Posu River.

Bornean Barbet Megalaima eximia

This endemic species was heard only once near the Joloi River at

the surprisingly low altitude of 160 m; it normally occurs at higher

elevations, but our sighting concurs with a record from the nearby

Mohot River, where a single individual was found at a similar

altitude (van Berkel etal. 2012). Our sighting might be explained

by altitudinal migration as fruits were ripening more quickly at

lower altitudes (JHF pers. obs.). There are only six previous records

of this species from Kalimantan (Mann 2008, Brickie et al. 2010,

van Berkel et al. 2012, Cheyne et al. 2012).

*Bornean Brown Barbet Caloramphus fuliginosus

This species is treated as a Bornean endemic following Short et

al. (2014). It was recorded regularly from different locations, all

between 160 and 280 m.

Helmeted Hornbill Buceros vigil (CR)

All hornbill species in Borneo are hunted, but this species is one of

the most intensively hunted throughout its range, mainly for the

ivory trade (Phillipps & Phillipps 2014, Collar 2015, Beastall et

al. 2016). This was seen during February and March 2014 when

a large number (>100) of hunters visited the Bukit Batikap area

to hunt Helmeted and other hornbill species exclusively for their

casques, confirming the speculation that organised crime targets

this species (Collar 2015, Eaton et al. 2015, Beastall etal. 2016).

A group of three hunters shot two Helmeted Hornbills and three

Black Hornbills Anthracoceros malayanus in one day, while another

group of two hunters shot two Rhinoceros Hornbills B. rhinoceros

in one day. A Helmeted Hornbill was also shot at on 30 January

2015. Although no targeted study has been conducted to assess

the impact of hunting, the abundance of Helmeted Hornbills in

Bukit Batikap Protection Forest seemed to drop markedly after

March 2014. A detailed study is necessary to assess the impact of

hunting, as the recent elevation from Near Threatened to Critically

Endangered illustrates (Collar 2015, IUCN 2015, Beastall et al.

2016).

Common Kingfisher Alcedo atthis

Individuals were found close to the Posu River (170 m) on 21

April 2014 and on the Joloi River (180 m) on 14 November 2014,

4 February 2015 and 18 March 2015. These are the third to sixth

records for Kalimantan according to Mann (2008), but Holmes &

Burton (1987) also recorded this species in Kalimantan. Another

individual was recorded in 2011 on the Babuat River (S. Jones in

litt. 2014).

* Black-faced Kingfisher Lacedo melanops

This species has been split from Banded Kingfisher L. pulchella and

is treated as a new endemic species following del Hoyo etal. (2014).

It was first recorded on 16 Februyary 2014 and heard regularly from

several localities between 160 and 180 m.

Bornean Ground Cuckoo Carpococcyx radiatus (NT)

This elusive endemic (Frederiksson & Nijman 2004) was heard at

five different locations between 160 and 180 m but was seen only

once. A sound recording of this species can be found on www.

xeno-canto.org (XC177800).

Short-toed Coucal Centropus rectunguis (VU) (Plate 1)

Seen and heard regularly from at least five different localities

between 160 and 170 m, the species appeared to be as common

as Greater Coucal C. sinensis in this area, but was reported solely

from undisturbed mixed dipterocarp forest and never from areas

with natural disturbance — such as areas with wind damage or

tree fall — or man-made disturbance. There are only three prior

records of this species from Central Kalimantan (Mann 2008,

Cheyne etal. 2012).

Waterfall Swift Hydrochous gigas (NT)

Recorded only twice with certainty. The first record was from a

small hill west of the Posu River (280 m) on 19 January 2014 and

the other near the Joloi River (170 m) on 10 February 2014. These

birds were identified based on their size (several other species

were close by, allowing direct comparison), with deeply forked

tail, completely dark colouration and smoother, more direct flight

behaviour than those of swiff let species. Furthermore, local people

are surprisingly familiar with a swift species that breeds behind

waterfalls, suggesting that this species breeds in the area. There are

few records of this species for Borneo and Mann (2008) reports

none from Kalimantan, although both Wilkinson etal. (1991) and

S. Jones {in litt. 2014) recorded its presence on the Busang River

and the Joloi River respectively. Therefore this record is treated as

the third record for Kalimantan.

Mossy-nest Swiftlet Coliocaiia salangana, Black-nest

Swiftiet C. maxima and Edible-nest Swiftlet C, fuciphaga

Although these three species of Coliocaiia swifflets are said to be

unidentifiable away from their nests (Phillipps & Phillipps 2014), a

great deal of time was spent identifying swiftlets flying over rivers.

All three species were identified based on tail shape, colour, size

and flight behaviour (Myers 2010). Local Dayaks confirmed that

they recognised nest types of all three species and claimed that

they were present in caves in the area. No caves were visited, but

harvesting of swiflet nests from caves in the area provides a major

source of income to the local Dayak people.

Large Frogmouth Batrachostomus auritus (NT) (Plate 2)

Four individuals were observed on several dates from three

different locations (100-160 m). A nest was found on a branch

overhanging the Joli River and a bird was present on the nest from

at least 18 February until 9 March 2014. This is only the fourth

record of this species for Kalimantan (Mann 2008, Woxvold &

Noske 201 1).

Forktail 32 (2016)

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia

29

Large Green Pigeon Treron capellei (VU)

By far the most common Treron pigeon, it was observed

approximately every other day. Three nests only 50 to 100 m apart

were found on 17 January 2014 near the field station (160 m). Large

congregations of this species were observed regularly, with numbers

reaching 40 individuals in a single flock. Recent records of numbers

of this magnitude are very rare (BirdLife International 2001, Iqbal

etal. 2012), underlining the importance of this area for the species.

Red-legged Crake Rallina fasciata

A single bird was observed in late October and early December 2014

close to the field station (160 m), possibly attracted by food scraps.

Two individuals were observed at the same site between September

and December 2015 and the apparent absence of the species during

the Palaearctic summer suggests that it may be migratory (Mann

2008). This species is a very scarce resident and passage migrant

and this record is the first for Central Kalimantan, although it is

probably under-recorded (Mann 2008).

Pintail Snipe Gailinago stenura

and Swimhoe's Snipe G. megala

On 11 April 2014, 24 Gailinago snipes were flushed close to the

Posu River (160 m), one of which called, and on 17 April 2014

another six individuals were flushed from a pebble beach on the

Joloi River (130 m), again one individual called. Both calls were

recorded and analysed and can be found on www.xeno-canto.

org (XC176562 and XC176561 respectively). Although the first

call most resembled Pintail Snipe and the second a Swinhoe's

Snipe, sources are not conclusive about the use of vocalisations

as an identification tool to distinguish between the two species

(F. Rheindt in litt. 2014). Several unidentified snipes were also

observed in November 2014 and on 12 April 2015. A study of the

vocalisations of these two species and their value as an identification

tool might help to confirm these and further records of these

species, and could provide much insight about their distribution

and migration. There are few definitive records of these species

from Kalimantan, this would be the second for Pintail Snipe and

the third for Swinhoe's Snipe (Mann 2008).

Red-necked Phalarope Phalaropus lobatus

On 16 October 2015 an individual in first-winter plumage was

observed on the Joloi River. Mann (2008) reports that this species

is a local passage migrant, but we consider a record this far inland

noteworthy.

Wallace's Hawk Eagle Spizeatus nanus (VU)

On 20 April 2014 an adult, with two juveniles close by, was

observed near the Joloi River (170 m), indicating that this species

was breeding locally. Two months later, probably the same birds

were observed a little further upstream (160 m), indicating that the

juveniles were still accompanying the adult. Later a single bird was

observed above the Joloi River (170 m).

Peregrine Falcon Fako peregrinus

On 2 February 2014 one was seen flying over the field station

(160 m); it could not be identified to subspecies level, but was

assumed to be of a migratory race. Records of migrants of this

species in Borneo are rare, except on the north-west coast. This is

the first record of the species for Central Kalimantan (Mann 2008).

Storm's Stork Ciconia stormi (EN)

An individual was observed several times above the Joloi River

(170 m) and appeared to land close by. According to local people,

this species was regularly seen at this site and a possible nest was

found here in early December 2014. A single bird was also seen

soaring above the Posu River (160 m) and landed close by. In

November and December 2015 additional sightings were made of

single birds on the Joloi River (170 m).

Malayan Night Heron Gorsachius melanolophus

An adult was observed on the banks of the Joloi River (150 m) on 29

October 2014. On 23 March 2015 another individual that appeared

to be moulting from juvenile to adult plumage was seen on the

banks of the Joloi River (160 m). These are the first definite records

of this occasional winter visitor for Kalimantan (Mann 2008).

*Bornean Banded Pitta Pitta schwaneri

This taxon is treated here as an endemic species, following Rheindt

& Eaton (2010). It was found close to the Posu River (170 m) and

a sound recording of this individual can be found on www.xeno-

canto. org (XC177931). This is only the third record of the species

for Central Kalimantan (Mann 2008, van Berkel et al. 2012,

Cheyne et al. 2012).

Biue-headed Pitta Pitta baudii (Plate 3)

A Bornean endemic, males were heard and seen regularly between

160 and 220 m, with male/female pairs observed twice.

Hooded Pitta Pitta sordida

This was by far the most common pitta in the area, although

sightings were mostly confined to riverbanks and riparian forest

strips along the Posu and Joloi Rivers. An active nest was found

on 1 July 2014 by other project members; this is a substantial

expansion of the breeding season according to Erritzoe (2014)

and Myers (2010).

Blue-banded Pitta Pitta arquata

This Bornean endemic species was heard only once, near the Posu

River (170 m) on 17 February 2014. Two individuals were observed

by other staff members in foothills east of the Joloi River (180 m)

in March 2014. Garnet Pitta P. granatina appears to be much more

common in this area. Even after analysis of sonograms of almost

all monotone whistles, no other records of Blue-banded Pitta were

confirmed. These are the second and third records for Central

Kalimantan (Mann 2008).

Fairy Pitta Pitta nympha (VU) (Plate 4)

An individual was found on 13 April 2014 close to the Posu River

(170 m) in mixed dipterocarp forest and was seen again on the night

of 15 April 2014, roosting in alow tree about 200 m from where it

was first seen. On 10 December 2014 a bird was again found close

to the Posu River (170 m) and the species was recorded between

the Posu and Joloi rivers (200 m) on 17 October 2015 and by the

Posu River (170 m) on 20 October 2015. Between October and

December 2015 the species was recorded from at least three other

different sites. A bird was also recorded in 2013 by other staff

members, near the Posu River (160 m) and remained at this site

in riverside vegetation from at least 4 February to 17 March. These

records are the third to tenth for Kalimantan (Mann 2008, van

Berkel etal. 2012). Given this large number of records from Bukit

Batikap Protection Forest, we infer that this area is an important

wintering or migration site for this Vulnerable species.

Blue-winged Pitta Pitta moluceensis (Plate 5)

A local and uncommon migratory species; one bird remained

near the field station in a patch of bamboo (160 m) from at least 2

February to 10 April 2014 and called regularly. Other individuals

were heard and seen between these two dates further upstream on

the Posu River (180 m) and close to the Joloi River (170 m). The

species was also observed in late November and early December

2014, on 17 January 2015 and on 4 April 2015 close to the Posu

River (160 m).

30

JOHANNES H. FISCHER eto/.

Forktail 32 (2016)

Hose's Broadbili Calyptomena hosii (NT)

Three individuals of this spectacular endemic were observed in a

mixed feeding flock foraging on figs in the hills east of the Joloi

River (210 m) on 20 November 2015. This is the first published

record for Central Kalimantan (Mann 2008), although there is an

unpublished record front the hills near PurukCahu from 2011 (S.

Jones in litt. 2014) and therefore we treat this as the second record

for Central Kalimantan.

Railbabbler Eupetes macrocews (NT)

This species was heard calling from three different locations (150—

180 m), but remained unseen. A sound recording can be found on

www.xeno-canto.org (XC177801). Recent records of this species

from Borneo are rare (Mann 2008).

Bornean Whistler Pachycephala hypoxantha

This endemic species was heard on one of the hills

(750 m) east of the Joloi River, but remained out of sight. This is only

the sixth record of this species for Kalimantan (Brickie etal. 2010).

Bornean Bristiehead Pityriasis gymnocephala (NT) (Plate 6)

This endemic was only recorded on three occasions in the area

(160-280 m), supporting the suggestion that it is scarce in lowland

dipterocarp forests (Phillipps & Phillipps 2011).

*Hair-crested Drongo Dicrurus hottentottus

Several of this mainly submontane species (Mann 2008) were

observed from different sites (160-180 m) but it appeared rather

scarce. Surprisingly this is only the sixth confirmed record for

Kalimantan (Mann 2008, Brickie etal. 2010, Woxvold & Noske

2011, Cheyne et al. 2012).

Chestnut-capped Thrush Zoothera interpres (NT)

Only one individual was observed, several times, in November and

December 2015 near the Posu River (160 m). This species is under

pressure due to trapping for the songbird trade (Eaton et al. 2015).

This is only the second record for Central Kalimantan (van Berkel

etal. 2012).

Fulvous-chested Jungle Flycatcher Rhinomyas olivacea

One was found at 500 m east of the Joloi River. A sound recording

can be found on www.xeno-canto.org (XC179628). This is the

first published record for Central Kalimantan according to Mann

(2008), although a good sound recording of this species from the

Busang River area can be found onwww.xeno-canto.org (XC69388)

and an unpublished record exists from Muara Joloi from 2011

(N. Brickie in litt. 2016). Therefore, it is treated here as the third

record of this species for Central Kalimantan. At lower elevations

(160-270 m) Grey-chested Jungle Flycatchers A. umbratilis were

encountered regularly. A bird with intermediate plumage features

and a slightly different song to the Grey-chested Jungle Flycatcher

but similar to intermediate birds described by Wilkinson et al.

(1991) was observed to the west of the Joloi River (200 m).

*Zappey's Flycatcher Cyanoptila cumatilis

and Blue-and-white Flycatcher C. cyanomeiana

Two male Cyanoptila sp. flycatchers were observed on 26 March

2014 by the Posu River (180 m). One of these was later identified

as Zappey’s Flycatcher C. cumatilis (F. Rheindt in litt. 2014). This

is the first record of Zappey’s Flycatcher for Kalimantan (Mann

2008), although it is likely that this species is under-recorded

as it was formerly considered conspecific with Blue-and-white

Flycatcher C. cyanomeiana (Leader & Carey 2012).

A male Blue-and-white Flycatcher was observed on 9 March

2015 at 280 m. This is the first confirmed record for Kalimantan

of this species, the five previous records (Brickie et al. 2010, Dewi

et al. 2016) predate Leader & Carey (2012) and were not identified

to taxon level.

Bornean Blue Flycatcher Cyornis superbus

This Bornean endemic was recorded from several different locations

(160-180 m). On 24 March 2014 a female was seen carrying nesting

material. This is only the fourth documented record for Central

Kalimantan (Mann 2008, van Berkel et al. 2012, Cheyne et al.

2012).

Large-billed Blue Flycatcher Cyornis caeruiatus (VU) (Plate 7)

Seen regularly between 160 and 180 m from 16 February 2014.

This is the second documented record of this species for Central

Kalimantan (Mann 2008, Cheyne etal. 2012).

Siberian Blue Robin Luscinia cyane

A female was observed on 19 April 2014 close to the Posu River (170

m), a male was seen on the hills (320 m) east of the Joloi River on 1

April 2015 and a pair was present east of the Posu River in November

and December 2015. These are the first to third published records

of this migratory species for Kalimantan (Mann 2008), although

there is an unpublished record of a male from the Mohot River in

2011 (S. Jones in litt. 2014). Therefore we treat these records as the

second to fourth records for Kalimantan, which is surprising as the

species is a widespread passage migrant and winter visitor in most

parts of Borneo (Mann 2008).

Straw-headed Bulbul Pycnonotus zeytanicus (VU)

Local people were very familiar with this species and keen to obtain

any pertinent information as it is an extremely popular cage bird,

persecuted with such vigour that its Vulnerable status is no longer

appropriate (Eaton et al. 2015). Not surprisingly, this species was

recorded on only seven occasions between January and July 2014

(160-180 m). It is a cause for concern that no records were made

between October 2014 and December 2015 suggesting that even

in very remote parts of Kalimantan, trapping pressure is pushing

this species to extinction (Brickie et al. 2010, Eaton et al. 2015).

The immense pressure on this species may already have caused its

local extinction in the Bukit Batikap Protection Forest, as the lack

of records in 2015 suggests.

Scaly-breasted Bulbul Pycnonotus squamatus (NT)

Seen once in a mixed-species flock on a small hill (280 m) south of

the Posu River on 24 January 2015. This is the first record of this

species for Central Kalimantan (Mann 2008).

Arctic Warbler Phyiloscopus borealis

This migratory species actually consists of three cryptic taxa,

split by Alstrom etal. (2011), and all are likely to occur in Borneo

(Phillipps & Phillipps 2014); they are very difficult to identify

using plumage characteristics, but vocalisations, especially

song, are good indicators (Alstrom 2011). In March and April

2014 several Phyiloscopus sp. were singing along the Posu River

(160-170 m). After analysis of the sonograms (www.xeno-canto.

org XC177805 and XC177892) it was clear that these birds

were Arctic Warblers (Figure 2). The Japanese Leaf Warbler P.

xanthodryas and Kamchatka Leaf Warbler P. examinandus have

not yet been recorded in Borneo, but the latter has been found on

the Philippines (Hoefferle et al. 2013), indicating that it could be

found on Borneo too.

Sooty-capped Babbler Malacopteron affine (NT)

One of the most abundant babbler species in this area. On 25 April

2014 a pair was observed with newly-fledged juveniles. This is an

extension of the breeding season indicated by Collar & Robson

(2014) and Myers (2010).

JOHANNES, H. FISCHER JOHANNES H. FISCHER JOY JOHANNES H. FISCHER

Forktail 32 (2016)

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia

31

Plate 1. Short-toed Coucal Centropus rectunguis, 22 April 2014.

Plate 2. Large Frogmouth Batrachostomus auritus on

18 February 2014.

Plate 4. Fairy Pitta Pitta nympha,'\5 March 2013.

nest,

Plate 3. Blue-headed Pitta Pitta baudii, 25 February 2014.

Plate 5. Blue-winged Pitta Pitta moluccensis, 10 February 2014.

Plate 6. Bornean Bristlehead Pytiriasis gymnocephala, 3 April 2015.

Plate 7. Male Large-billed Blue Flycatcher Cyornis caerulatus, Plate 8. Plain Flowerpecker Dicaeum minullum, 6 March 2015.

16 April 2014.

All images were taken in Bukit Batikap Protection Forest, Central Kalimantan, Indonesia.

NICHOLAS S. BOYD NICHOLAS S. BOYD ADHY MARULY JOHANNES H. FISCHER

JOHANNES H. FISCHER

32

JOHANNES H. FISCHER etol.

Forktail 32 (2016)

7 000-

6 800-

6 600-

6.400 -

6 200-

6 000-

5 800 -

5600-

5.400-

5 200-

5 000-

4 600-

4.400-

4.200-

4 000-

3 800-

3 600-

3400-

3.200-

3 000-

2 800-

2 600-

2 400-

1 996

MflZ

SO 797

-i - - - 1 - - - 1 - - - r-

1.2 14 16 18

Figure 2. Sonogram of

Arctic Warbler Phylloscopus

borealis song, Bukit Batikap

Protection Forest, Central

Kalimantan, Indonesia, 26

March 2014.

Grey-breasted Babbler Malacopteron albogulare (NT)

Occasionally observed in mixed dipterocarp forest (160-220 m).

This species prefers low nutrient forests such as peatswamps or

kerangas, but also found in mixed dipterocarp forests (Sheldon

1987, Dutson et al. 1991). Yong et al. (2014) suggested uplisting

this species to Vulnerable.

Bornean Wren Babbler Ptilocichla leucogrammica (VU)

Seen only once, close to the Posu River (170 m), but heard on

several occasions at the same location. This is the fourth record

of this endemic species for Central Kalimantan (Wilkinson et

al. 1991, Mann 2008, Woxvold & Noske 2011, N. Brickie in litt.

2016).

Black-throated Wren Babbler Napothera atrigularis (NT)

Two individuals were observed near the Joloi River (160 m), only

the second record of this endemic species for Central Kalimantan

(Woxvold & Noske 2011).

White-necked Babbler Stachyris leucotis (NT)

Two individuals were seen on one of the hills (360 m) east of the

Joloi River on 23 January 2015 and a single singing bird was seen

near the Joloi River (170 m) on 11 April 2015; the second and

third records of this species for Central Kalimantan (Mann 2008).

Chestnut-crested Yuhina Yuhina everetti

Small flocks of this endemic species were observed regularly on the

hills (170-410m). There is only one previous record of this species

from Central Kalimantan (Mann 2008).

Yellow-rumped Flowerpecker Prionochiius xemthopygius

This Bornean endemic occurred together with Crimson-breasted

Flowerpecker P. percussus in the area and their coexistence was also

recorded by Fiolmes & Burton (1987) at the mouth of the Joloi

River and by Wilkinson et al. (1991) on the Busang River, contra

Myers (2010) who stated that these species are not known to occur

together. Yellow-rumped Flowerpecker was found between 160

and 280 m, but Crimson-breasted Flowerpecker was only found at

160 m. The Ulu Barito IBA lies within the overlap of the ranges of

these two species (Wilkinson et al. 1991), but Crimson-breasted

Flowerpecker appears to be much less common in the Bukit Batikap

Protection Forest.

Plain Flowerpecker Dicaeum minullum (Plate 8)

This species, rare on Borneo, was recorded on a small hill (280 m)

south of the Posu River on 6 March 2015. This is the second record

for Central Kalimantan (Mann 2008), although Wilkinson et al.

(1991) suspected that it was present in the Ulu Barito area.

*'Spectacled Flowerpecker' Species novum

Tli is potentially new species, probably a member of genus Dicaeum,

has not yet been formally described. It was first reported by

Edwards et al. (2009) from Danum Valley, Sabah, with a handful

of subsequent reports from Labi Road, Brunei, in 2014 and the

Malian Basin, Sabah, in 2014 (Sykes & Loseby 2015). This taxon,

which is probably endemic to Borneo (Phillipps & Phillipps 2014),

was observed in Bukit Batikap Protection Forest between January

and December 2015 on a small hill (280 m) south of the Posu

River, with recordings of the call being made on 9 March and

25 November (www.xeno-canto.org XC239907 and XC301233).

This is a significant extension of the currently known range of

this taxon to the south of Borneo’s mountainous spine and is the

first record for both Kalimantan and Indonesia (Boyd et al. 2016).

Bornean Spiderhunter Arachnothera everetti

This endemic species was recorded from just three different locations

(160-180 m). There are only three previous records for Central

Kalimantan, although it may be under-recorded due to confusion

with the very similar Grey-breasted Spiderhunter A. modesta

(Wilkinson et al. 1991, Mann 2008, Woxvold & Noske 2011,

Cheyne et al. 2012).

Paddyfield Pipit Anthus rufulus

A single bird flew over the field station on 30 September 2015.

Surprisingly, this is the first published record for Central

Kalimantan, but the species has probably been overlooked (Mann

2008).

RECOMMENDATIONS

We recommend formal structured and targeted surveys within

this area, as well as in other areas in the Ulu Barito IBA, to

estimate population densities and confirm the importance of

this region for key species. In particular, as the Ulu Barito IBA

is one of the few places that host several very rare Galliformids, a

special study focused on these elusive birds would greatly improve

the understanding of their conservation requirements (Fuller &

Garson 2000, Fuller et al. 2000, BirdLife International 2001).

Furthermore, a detailed study devoted to determining the impact

of huntinghornbills for their casques seems valuable (Collar 2015).

ACKNOWLEDGEMENTS

The BOSF Bukit Batikap Protection Forest orangutan reintroduction project

is grateful for the funding and support from BHP Billiton, Svenska Postkod

Forktail 32 (2016)

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia

33

Stiftelsen, US Fish and Wildlife Service, Great Apes Conservation Fund, Save

The Orangutan Foundation, The Orangutan Project, Mohamed Bin Zayed

Conservation Fund, Margot Marsh Biodiversity Foundation, Orangutan

Outreach Pt. Musim Mas and the BOSF’s global sister organisations. JF, NB

and AvdK are indebted to BOSF in general and the field staff in particular

for making the visit to this remote site possible. We also thank Bas van Balen,

James Eaton, Sander Pieterse, Frank Rheindt, Jelle Scharringa and Ben Wielstra

for their help with several identification challenges. We thank Samuel Jones

and Nick Brickie for sharing their unpublished records and we are grateful to

FFeiko Wittmer, Nick Brickie and an anonymous reviewer for considerable

improvements to the manuscript.

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34

JOHANNES H. FISCHER etai.

Forktail 32 (2016)

Johannes H. FISCHER, School of Biological Sciences, Victoria

University of Wellington, PO Box 600, Wellington 6012, New

Zealand. Email: johannesftscher@live.nl

Nicholas S. BOYD, Borneo Orangutan Survival Foundation,

Jalan Papandayan 10, Bogor 16151, Indonesia. Email: nick_

boyd@hotmail.co.uk

Adhy MARULY, Borneo Orangutan Survival Foundation, Jalan

Papandayan 10, Bogor 16151, Indonesia. Email: amaruly@

yahoo.co.id

Anna-Selma VAN DER KAADEN, Faculty of Geosciences,

Graduate School of Geosciences, Utrecht University,

Heidelberglaan 2 3584 CS, Utrecht, The Netherlands. Email:

a.vanderkaaden@uu.nl

Simon J. HUSSON, Borneo Orangutan Survival Foundation,

Jalan Papandayan 10, Bogor 16151, Indonesia. Email:

simonhusson@orangutan.or.id

Jamartin SIHITE, Borneo Orangutan Survival Foundation,

Jalan Papandayan 10, Bogor 16151, Indonesia. Email: jhs_

sihite@yahoo.com

Appendix 1.

Bird species recorded in Bukit Batikap Protection Forest from January 2014 to December 201 5. Taxonomy and

nomenclature is based on Inskipp etai (1996) with the exception of those species marked with an *

Key: t= Bornean endemic, ft = Bornean near-endemic. Threat status: CR = Critically Endangered. EN = Endangered. VU = Vulnerable. NT = Near Threatened.

Occurrence in Borneo (Mann 2008): R = resident. W = winter visitor. P = passage migrant.

Forktail 32 (2016)

An inventory of the avifauna of the Bukit Batikap Protection Forest, Central Kalimantan, Indonesia

35

FORKTAIL 32 (2016): 36-40

Field records of Zappey's Flycatcher Cyanoptila cumatilis

on Java and Sumatra, with notes on the distribution

and status of Blue-and-white Flycatcher C. cyanomelana

in Indonesia

ARELLEA R. DEWI, NURROHMAN E. PURNOMO, REZA A. AHMADI, I. PURWIANSHARI & MUHAMAD H. ASHSHIDIQI

Zappey's Flycatcher Cyanoptila cumatilis was a long-forgotten taxon that is now recognised as a distinct species from Blue-and-white

Flycatcher C. cyanomelana. Its distribution, especially during the non-breeding season, is poorly known. In Indonesia it was known from

two records from Sumatra and a single record from Java. Observations from Flalimun Salak National Park in February 2014 and Cibodas

Botanical Gardens in March 2015 revealed new records of Zappey's Flycatcher from mainland Java. Published information and observations

by Indonesian birdwatchers confirm the presence of the two races of Blue-and-white Flycatcher ( cyanomelana and intermedia) on Java and

suggest that it is a much commoner migrant than previously believed.

INTRODUCTION

Zappey’s Flycatcher Cyanoptila cumatilis is a valid species that was

previously considered to be a race of the Blue-and-white Flycatcher

C. cyanomelana (Thayer & Bangs 1909, Leader & Carey 2012).

Zappey’s Flycatcher differs from the latter in having a blue wash on

the throat, breast and ear-coverts, similar to the blue upperparts,

whereas in the Blue-and-white Flycatcher these areas are black (race

cyanomelana ) or blackish (race intermedia ), in contrast to the blue

upperparts. The distribution and status of Zappey’s Flycatcher is

still not fully known. Leader & Carey (2012) state that it breeds in

central China, north to Beijing, west to Shaanxi and south to north¬

west Hubei. Clement (2015) noted that during the non-breeding

season the taxon cumatilis migrates to Laos and Vietnam, the Greater

Sundas in Indonesia, and Luzon and Palawan in rhe Philippines.

However, cumatilis has in fact been seen over a wider area during

the non-breeding season — Hong Kong, South Korea, Peninsular

Malaysia and Sabah: images can be found on Oriental Bird Images

(http://orientalbirdimages.org/search.php ?Bird_ID=2945) and

Borneo Bird Images (http://www.borneobirdimages.com/species/

zappey-at-s_flycatcher#navigation).

Very little information is available on rhe distribution of Zappey’s

Flycatcher in Indonesia and, as far as we are aware, there is only

a handful of published records from Java and Sumatra. The only

Figure 1 . Locations of Cyanoptila cumatilis, C. cyanomelana cyanomelana, C. cyanomelana intermedia, C. cyanomelana undetermined and undetermined

female and immature birds recorded in Indonesia from 1 894 to 201 5.

BRUNEI

DARUSSALAM

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♦

☆

☆ Cyanoptila cumatilis

o Cyanoptila cyanomelana cyanomelana

• Cyanoptila cyanomelana intermedia

+ Cyanoptila cyanomelana undetermined

? Cyanoptila undetermined

0 _ 375 _ Z50 _

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N D O N E S I A

TIMOF

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Kilometers

Esri, HERE. DeLorme, Mapmylndia, © OpenStreetMap contributors, and the GIS user

Forktail 32 (2016)

Field records of Zappey's Flycatcher Cyanoptila cumatilis on Java and Sumatra, Indonesia

37

previous confirmed record from Java is a male collected from the

Karimoen Djawa Islands (now Karimunjawa) by K. W. Dammerman

on 25 November 1930 (Chasen & Kloss 1933). A record by Bartels &

Stresemann (1929) gave no specific information about the number,

sex or location of the birds observed. Records from Sumatra can

first be traced from van Marie & Voous (1988), where one male —

from Kaban on 22 February 1916 (de Beaufort 1921) — and three

females are reported. However, knowledge of the plumage of females

and first-winter birds is far from complete and it is not possible to

distinguish between the females and first-winter birds of the two

species (Leader & Carey 2012); therefore, the females noted by

van Marie & Voous (1988) and all other records of females and

first-winter birds cannot be assigned to either species until further

research has been carried out. There is one recent record, a single

bird in Bukit Barisan Selatan National Park in September 2014

(Eaton 2014). James Eaton (in litt. 2016) confirmed that this was

an immature male Zappey’s Flycatcher that was just distinguishable

from Blue-and-white Flycatcher.

The closely related Blue-and-white Flycatcher is regarded as a rare

winter visitor to Sumatra and Java (MacKinnon & Phillipps 1993),

although some earlier records may relate to Zappey’s. Furthermore,

Blue-and-white Flycatcher has recently been observed further east

in Indonesia, in Bali (Mason 2011, Hjerppe 2015) and Sulawesi

(Rheindt & Verbelen 2011).

Here we present recent records of Zappey’s Flycatcher on Java

and also investigate the distribution and status of Blue-and-white

Flycatcher in Indonesia, particularly on Java, which suggest that the

species is more common than previously thought.

METHODS

Surveys of three areas in West Java were made, the first by ARA in

Halimun Salak National Park on 22 February 20 1 4, and the second

and third by ARD, NEP, IP & MHA between 16-20 March 2015

in Cibodas Botanical Gardens and Gede Pangrango National Park.

In Halimun Salak NP, the Kawah Ratu track was followed

from Gunung Bunder (6.717°S 106.71 1°E). The track is in tropical

rainforest, with more open forest around Kawah Ratu ( 1 ,400 m), and

all birds were recorded along it from 06h00 to 1 2h00. Observations

in the 80 ha Cibodas Botanical Garden (6.740°S 107.004°E) were

made on 16, 17, 18 and 20 March 2015. It is a coniferous park lying

between 1,200 and 1,400 m. Observations covered the entire area,

which was divided into four blocks, each surveyed by two observers.

Surveys were carried out from 07h00- 1 lhOO and 14h00- 17h00. A

survey was made in Gede Pangrango NP (6.749°S 106.990°E) on

19 March by following the Cibereum waterfall track (1,300-1,700

m) from 06h00 to 12h00.

We also traced records of Zappey’s and Blue-and-white

Flycatchers in Indonesia from published information and

information gathered from Indonesian birdwatchers.

RESULTS

Single Zappey’s Flycatchers were recorded in two of the survey

sites. The first, a single male in Halimun Salak NP on 22 February

2014, was observed by ARA at about 1,300 m in forest on the

Kawah Ratu track at 1 lhOO. The weather was cloudy but visibility

was good, and the bird was observed at about 8- 1 5 m for about 30

seconds. The all blue appearance of the upperparts (with a lack of

moult contrast in the upper coverts) confirmed that the bird was an

adult male. It appeared larger than the resident Indigo Flycatcher

Eumyias indigo, which might be a cause of contusion, but the stark

contrast between the blue throat and the white belly removed any

possible doubt.

The second record was of a single male at 08h30 on 20 March

2015, a cloudy morning after earlier rain, seen by ARD and NEP in

Cibodas Botanical Gardens at 1,350 m, and confirmatory images

were obtained (Plates 1 & 2). The bird was not disturbed by the

observers’ presence and was approached to about 5 m. It perched

quietly on a branch of a conifer for about a half minute, then

moved to another tree before it flew off and disappeared. At first

ARD and NEP thought it was an Indigo Flycatcher, but its larger

size and the appearance of its tail led them to conclude that it was

a Blue-and-white Flycatcher. However, subsequent examination of

the images highlighted the contrasting blue throat and white belly

and, after discussion on the Indonesian birdwatchers Facebook

group (Pengamat Burung Indonesia), the bird’s identification as a

male Zappey’s Flycatcher was confirmed.

Three Blue-and-white Flycatchers were also recorded in Cibodas

Botanical Garden. NEP and IP observed a single male perched on a

tree at 1,295 m on 16 March (Plate 3) and at 08h00 on the following

day, ARD and MHA saw a male perched in the tree canopy at the

same location. On 18 March, at 1 lh39, NEP and IP found a male

moving from branch to branch in a conifer at 1,342 m. There were

also two records of female Cyanoptila sp. on 16 and 17 March. We

were unable to determine whether any of these sightings were of the

same individuals or not.

DISCUSSION

Previous confirmed records of Zappey’s Flycatcher in Indonesia

consisted of one from Java (Chasen & Kloss 1933) and two from

Sumatra (de Beaufort 1921, Eaton 2014). Our records from

Halimun Salak NP and Cibodas Botanical Gardens are the first of

the species on Java for more than 80 years. Falling in February and

March, at the start of the northern migration period, they suggest

that Java maybe the most southerly wintering location of the species.

A compilation of Blue-and-white Flycatcher observations from

published information and birdwatchers’ records in Indonesia

produced 30 confirmed records (Table l). There were six records

from Sumatra: one of the race cyanomelana, one of intermedia and

four of undetermined race. Historical records (from 1913 to 1998)

were all from mainland Sumatra. However, recent observations

have been made on Sumatra’s satellite islands, Bangka and Belitung

(Syahputra pers. comm., M. Iqbal pers. comm.). There are only four

records from Kalimantan, without any information as to the race(s)

concerned (Biittikofer 1899, Rice 1989, Holmes 1997, Brickie et

al. 2010, Wielstra et al. 2012). On Bali there is one record of race

cyanomelana and four of undetermined race, all from the highlands

of Bedugul and north Payangan (Mason 2011, Hjerppe 2015).

Most records of Blue-and-white Flycatcher were from Java, with

1 1 records during the 1 1 years 2005-2015, nine of them between

2011 and 2015 — one of undetermined race, five of cyanomelana

and three of intermedia-, two of the latter were from East Java (C.

Fitri Riani pers. comm, H. Cahyono pers. comm.) and one from

Plawangan Hill, Mount Merapi National Park, Central Java (F.

Mufti pers. comm.).

There have been 13 records of undetermined Cyanoptila species

in the last four years (2012-2015) — females and first-winter birds

that cannot be determined to species level. Some of the females show

a gradation in the colour of breast and belly whereas others show a

sharper contrast between a brown breast and white belly (Plates 5

& 6) that might be evidence of age-related changes.

It is interesting that almost half of the Blue-and-white Flycatcher

records from Java were from Mount Merapi NP, where the species

was previously thought to be a rare visitor (Yuniatmoko &

Nurcahyadi 2013). In December 2015, up to 13 individuals were

recorded there by three observers. However, due to the similarity of

the plumages of some birds, it is only certain that there were seven

38

ARELLEA R. DEWI etal.

Forktail 32 (2016)

Plate 1. Lateral view of adult male Zappey's Flycatcher Cyanoptila

cumatilis, Cibodas Botanical Gardens, Java, Indonesia, 20 March 201 5.

Plate 4. Female Zappey's/Blue-and-white Flycatcher, Cibodas Botanical

Gardens, 1 7 March 2015.

Plate 2. Ventral view of the same bird, Cibodas Botanical Gardens, 20

March 2015.

Plate 3. Adult male nominate Blue-and-white Flycatcher C. cyanometana,

Cibodas Botanical Gardens, 1 6 March 201 5.

Plate 5. Female Zappey's/Blue-and-white Flycatcher with gradation from

breast to belly, Cibodas Botanical Gardens, 1 7 March 2015.

Plate 6. Female Zappey's/Blue-and-white Flycatcher with strong contrast

between breast and belly, Turgo Hill, Gunung Merapi National Park, 8

March 2014.

MA'ARUF ERAWAN ARELLEA R. DEWI ARELLEA R. DEWI

Forktail 32 (2016)

Field records of Zappey's Flycatcher Cyanoptila cumatilis on Java and Sumatra, Indonesia

39

Table 1. Compilation of Indonesian records of Cyanoptila cumatilis, C. cyanomelana cyanomeiana, C. cyanomeiana intermedia, C. cyanomelana

undetermined and undetermined female and immature birds between 1 894 and 2015.

‘although the specimen label described it as'male', the image of the specimen obtained from the Naturalis curators shows a characterisitc brown female.

40

ARELLEAR. DEWIero/.

Forktail 32 (2016)

different individuals present during the month, six of which were

of indeterminate race on Plawangan Hill on 6 December 2015

(M. Erawan pers. comm.) and a single adult male intermedia on

Pronojiwo Hill on 13 December 2015 (F. Mufti pers. comm.).

These Javan records indicate that Blue-and-white Flycatcher is

not as rare as previously thought and suggest that it may be a common

migrant. It appears that the species was previously overlooked (or

assumed to be the smaller resident Indigo Flycatcher), but the

growing numbers of birdwatchers and photographers have led

to more comprehensive documentation of records, with positive

identification from images.

The fact that there were no records of Zappey’s Flycatcher from

Java since Chasen& Kloss (1933) until our records in 20 14 and 2015

is probably due to its lack of recognition as a species and its similarity

to the Blue-and-white Flycatcher. In our experience, these closely-

related species can be found in the same location at the same time of

year, so the identification ol these taxa requires care and attention.

Zappey’s Flycatcher was not listed in Sukmantoro et al. (2007)

as it had not been recognised as a species at that time and it has no

Indonesian common name. We suggest Sikatan Cina as its Indonesian

name, linking it to its known breeding area and distinguishing it from

the Blue-and-white Flycatcher, Sikatan Biru-putih.

ACKNOWLEDGEMENTS

We thank all those who helped with surveys: Andri Nugroho, Andi Asmara

Cipta Putra, Panji Gusti Akbar and Amanina Khusna Maulida of the Pygmy Tit

team, KPB Bionic UNY and all the team from KPB Perenjak HIM AKOVA IPB.

Cibodas Botanical Gardens, Gede Pangrango National Park and Halimun Salak

National Park kindly allowed us to carry out surveys. Special thanks go to Imam

Taufiqurrahman for help in Gede Pangrango, providing various references as well

as commenting on the manuscript. Thanks also to Muhammad Iqbal for sharing

observations from Sumatra and providing information from the literature, and

Steven van der Mije and Pepijn Kamminga of Naturalis Biodiversity Centre

for providing information about the specimens in the Naturalis collection. The

following kindly provided field records: AgungSatria Wibowo, Ahmad Zulfikar

Abdullah, Boedi Setiawan. Budi Hermawan, Citra Fitri Riani, Faradlina Mufti,

Heru Cahyono, Irwan Yuniatmoko, Joko Setiyono, Ma’aruf Erawan, Syahputra

and Waskito Kukuh W ibowo. Finally, we would like to thank the Forktail editors

and two reviewers for their valuable input.

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of East Sumatra. Ardea 10: 171-174.

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Java nachgewiesenen vogel. Treubia 1 1 : 89-146.

Brickie, N. W„ Eaton, J. A. & Rheindt, F. E. (2010) A rapid bird survey of the

Menyapa mountains, East Kalimantan, Indonesia. Forktail 26: 31-41.

Buij, R., Fox, E. A. & Wich, S. A. (2006) Birds of Gunung Leuser National Park,

Northern Sumatra. Kukila 1 3: 23-41 .

Buttikofer, J. (1899) Zoological results of the Dutch scientific expedition to

Central Borneo. Notes from Leyden Museum 21:1 45-276.

Chasen, F. N. & Kloss, C. B. (1933) On a small collection of birds from the

Karimoen Djawa Islands. Treubia 14: 165-171.

Clement, P. (2015) Blue-and-white Flycatcher (Cyanoptila cyanomelana). HBW

Alive ('http://www.hbw.com/node/59077 accessed 15/12/2015).

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Kloss, C. B. (1 931 ) An account of the Sumatran birds in the Zoological Museum,

Buitenzorg, with descriptions of nine new races. Treubia 1 3: 299-370.

Leader, P. J. & Carey, G. J. (2012) Zappey's Flycatcher Cyanoptila cumatilis, a

forgotten Chinese breeding endemic. Forktail 28: 121-128.

MacKinnon, J. & Phillipps, K. ( 1 993) A field guide to the birds of Borneo, Sumatra,

Java and Bali. New York: Oxford University Press,

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Ornithologists' Union. BOU Checklist 10.

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additions to the avifauna. Kukila 1 5: 1 -30.

Naturalis (2016a) Cyanoptila cyanomelana cumatilis Thayer & Bangs. Coll.

Groeneveldt available from http://bioportal.naturalis.nl/. Search for

'RMNH.AVES.1 38405'.

Naturalis (2016b) Cyanoptila cyanomelana cumatilis Thayer & Bangs. Coll.

Groeneveldt available from http://bioportal.naturalis.nl/. Search for

'RMNH.AVES.1 38406'.

Nijman, V. & Setiawan, I. (2001 ) Rapid assessment of fauna diversity in Dieng

Mountains. Final report. Bandung: YPAL/Mitra Dieng/Gibbon Foundation.

Rice, C. G. (1989) A further range extension of the Black-breasted Thrush

Chlamydochaera jefferyi in Kalimantan. Kukila 4: 47-48.

Rheindt, F. E. & Verbelen, F. (201 1) First record of Blue-and-white Flycatcher

Cyanoptila cyanomelana in the Wallacean region. Kukila 1 5: 80-82.

Robinson, H. C. & Kloss, C. B. (1 920) On a collection of birds from N. E. Sumatra

II. J. Straits Branch R. Asiatic Soc. 80: 72-1 33.

Robinson, H. C. & Kloss, C. B. (1924) On a large collection of birds chiefly

from West Sumatra made by Mr. E. Jacobson. J. Fed. Malay States Mus.

1 1: 189-347.

Sukmantoro, W., Irham, M., Novarino,W., Hasudungan, F., Kemp, N.&Muchtar,

M. (2007) Daftar Burung Indonesia no. 2. Bogor: Indonesian Ornithologists'

Union.

Thayer, J. E. & Bangs, O. (1909) Description of new birds from Central China.

Bull. Mus. Comp. Zool. Harvard 52(8): 1 37-141.

Widodo, W. (2013) Avian study as environment indicators in the mountain

Sawal forest, Ciamis, West Java. Prosiding Seminar Biologi 10(6): 256-267.

Wielstra, B„ Boorsma, T. & Pieterse, S. N. (2012) An update on the avifauna

of Gunung Lumut Protection Forest (East Kalimantan) reinforcing the

potential conservation value of Hutan Adat. Kukila 1 6: 1 -1 5.

Wisnubudi, G. (2009) Penggunaan strata vegetasi oleh burung di kawasan

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Yogyakarta: Taman Nasional Gunung Merapi.

Arellea R. DEWI, Kelompok Pengamot Burung Bionic

Universitas Negeri Yogyokarto (KPB BIONIC UNY),

Gelanggang Organisasi Mohasiswo Fakultas Motemotika

dan llmu Pengetahuan Alam Universitas Negeri Yogyakarta,

Karangmalang, Depok, Sleman 55281, Indonesia

Email: arellea44@gmail.com

Reza A. AHMADI, Himpunan Mahasiswa Konservasi

Sumberdaya Hutan dan Ekowisata (HIMAKOVA) Institut

Pertanian Bogor, Tangkaran Himakova, Departemen

Konservasi Sumberdaya Hutan dan Ekowisata, Fakultas

Kehutanan IPB 16680, PO BOX 168, Dramaga Bogor, Indonesia

Email: reza.conservationist@gmail.com

Nurrohman E. PURNOMO, Insiwi PURWIANSHARI and

Muhamad H. ASHSHIDIQI, Kelompok Pengamat Burung

Bionic Universitas Negeri Yogyakarta (KPB BIONIC UNY)

FORKTAIL 32 (2016): 41-53

A review of the distribution and population of the

Collared Crow Corvus torquatus

PAUL J. LEADER, DAVID J. STANTON, RICHARD W. LEWTHWAITE & JONATHAN MARTINEZ

Abstract: The Collared Crow Corvus torquatus is a species largely restricted to China and is currently listed as Near Threatened. This paper

reviews historical changes in the distribution of Collared Crow in China and, based on modern records from China, Vietnam and Taiwan,

provides the first systematic global population estimate for the species. Based on field surveys in Guangdong province, China, during

2003-2014, evidence is presented that shows it is absent from vast areas of habitat suitable for the species in that province and indicates that

a previous population estimate made in 2007 by BirdLife International, based on an extrapolation of numbers from one of its strongholds in

Hong Kong, is flawed. A revised population of less than 2,000 individuals is substantially less than the 15,000-30,000 previously estimated,

and it is recommended that the species be uplisted to Vulnerable.

INTRODUCTION

The Collared Crow Corvus torquatus is found mainly in the People’s

Republic of China, being resident in the south and east, reaching

southern Hebei in the north-east, Gansu in the west and Yunnan

and Hainan in the south-west (Cheng 1987, BirdLife International

2016). Outside mainland China, it is known only from northern

Vietnam and Taiwan, where it is restricted to Kinmen Island (just

off the coast of mainland China) and the main island of Taiwan,

where it is accidental (Brazil 2009, BirdLife International 2016).

It is currently listed as Near Threatened on the basis that the global

population is experiencing a moderately rapid and ongoing decline

(BirdLife International 2016).

This paper reviews the historical distribution of the species and

presents an up-to-date summary of its distribution and population.

METHODS

Historical literature review (1855-1980)

The authors carried out an extensive review of the historical litera¬

ture (including Chinese ornithological literature) on the distribu¬

tion and population of the Collared Crow in China from 1855 to

1980, commencingwith Robert Swinhoe’s first records from China

to the end of the period covered by Cheng (1987).

Review of recent records (2003-2014)

Records of Collared Crow for the period from 2003 to 2014 were

collated. These were sourced from the published literature; from

online requests for records from Birdforum (http://www.bird-

forum.net/showthread.php?t=288068), ChinaBirdnet.com and

Oriental Birding (orientalbirding@yahoogroups.com); from online

databases BirdTalker (http://birdtalker.net) and eBird (http://ebird.

org); and from direct requests for information. Where necessary,

observers of online records were contacted to request permission

to publish their data. If this could not be obtained such records

were summarised and the reader is referred back to the original

source. Where a number of birds was given as a range (e.g. 10-20),

the lower figure was used. From these records the highest count

from each site was taken and these were summed to arrive at a total

population estimate.

Surveys in Hong Kong, Macau and Guangdong province

Field surveys were carried out in the Hong Kong Special

Administrative Region (hereafter Hong Kong), the Macau Special

Administrative Region (hereafter Macau) and Guangdongprovince

during the period 2003-2014; additional data were sourced from

other reliable observers. Surveys were carried out using a 5 x 5 km

square grid based on that used for Hong Kong (see Carey et al.

2001). Within each square a minimum of two hours continuous

observation was spent in suitable habitat. The Collared Crow is

known to prefer low-lying areas, and shows a very strong association

with wetlands including agricultural areas (particularly rice fields),

riverine plains, lightly wooded country near water or marshes,

fishponds and coastal areas (including mudflats, rocky and sandy

shores). It generally avoids more heavily wooded or hilly country

and developed areas such as parks, gardens and towns (Madge &

Burn 1994, Carey et al. 2001, Carey 2009, BirdLife International

2016, Madge 2016). The survey methodology was fluid to allow

for differences in terrain and infrastructure, but generally followed

roads and paths with prolonged scans of open country, estuaries,

beaches and mudflats as required. Areas of potentially suitable

habitat were identified through a combination of local knowledge,

a review of maps and/or aerial images, and cold searching. Although

the survey period was long (12 years), which could potentially lead

to an over-estimate of the number of individuals present, given the

low numbers recorded during the surveys any over-estimate is not

considered significant.

RESULTS

Historical literature review (1855-1980)

The Collared Crow was formerly common and widespread on the

coast and in the lowlands throughout much of southern China,

south to Hainan and west to central Guangxi; its distribution

also extended north to Beijing and west to northern Shaanxi, west

Sichuan and eastern Yunnan (Appendix 1). Armand David, who

travelled widely in the north, west and south of China between

1862 and 1874, considered it ‘one of the most characteristic birds

of the Chinese avifauna ... particularly widespread in southern

provinces ... sedentary’ (David & Oustalet 1877).

Other authors who provided first-hand accounts of the species

in southern China between the 1850s and 1930s also regarded it

as resident and without exception used terms such as ‘common’,

‘very common’, ‘frequently occurs’, ‘often met with’, ‘abounds’,

‘large numbers’ or ‘assembling by the hundreds’ when describing

its abundance. The localities referred to included Xiamen, Fujian,

in the 1850s (Swinhoe 1860); Hong Kong, Guangzhou and Macau

in 1860 (Swinhoe 1861a); the lowlands of north and north-west

Hainan in 1868 (Swinhoe 1870); the entire Lower Yangtse

basin from eastern Hubei to the delta in the 1880s (Styan 1891);

Fuzhou and Shantou on the Fujian-Guangdong coast in the

1880s and 1890s (La Touche 1892, Streich 1903, La Touche &

Rickett 1905); Zhenjiang, Jiangsu in the early 1900s (La Touche

1906-1907); Hong Kong, Macau, the Pearl River Delta, the

42

PAUL J. LEADER etal.

Forktail 32 (2016)

North River north to Shaoguan, and the West River from the

Pearl River Delta through western Guangdong to central Guangxi

in the years 1900-1908 (Vaughan & Jones 1913); Shasi, Hubei

in 1917-1919 (La Touche 1922); Jiangsu and Anhui south of the

Yangtse in 1921-1922 (Koltoff 1932); the lowlands of Guangxi in

the years 1927-1931 (Yen 1933-1934); Nanjing, Jiangsu in 1930

(Ascherson 1930); Zhejiang in the early 1930s (Shaw 1934) and

north and south-west Guangdong in the early 1930s (Yen 1932,

Jabouille 1935). The above accounts paint a consistent picture of a

common and widespread species.

Its abundance on the South China coast and along the Yangtse

was not matched at Shanghai, where it was only found occasionally

(Sowerby 1943). North of the Yangtse River, it was recorded in

Beijing in 1860 and 1900-1901 (Swinhoe 1861b, 1863, Walton

1903), Sichuan in 1868-1869 (David 1871), Hebei at least up to the

1920s (Wilder & Hubbard 1924), Shandong in the 1920s (LeFevre

1962), Henan in the 1930s (Fu 1937), Shaanxi in 1957-1958 (Cheng

et al. 1962), and on unknown dates in Shanxi, Gansu, Guizhou

and north-east Yunnan (Cheng 1987). Except in Henan, where Fu

(1937) stated that it was common on the plains, it was generally

considered to be much less common in the north of its range than

in the south.

In the late 1950s, when the study of birds resumed following a

period ot invasion and civil war, ornithology in China was largely

concerned with ascertaining whether a particular species was

harmful or beneficial to farming and forestry, and the status and

distribution of the Collared Crow was much less clear. However, the

fact that the stomach contents of 63 Collared Crows were analysed

in one study alone in Fujian in 1957 (Cheng 1963), indicated that

the species was still present in good numbers locally in China in

the late 1950s.

Review of recent records (2003-2014)

Records were collated from mainland China, Taiwan and Vietnam

for the period 2003-2014. The peak count from each individual site

was taken and summing these counts provides population estimates

of 1,709 individuals for China, 18 for Taiwan and 120 for Vietnam,

a total of 1,847 individuals. The locations of records are shown in

Figure 1 and summarised in Table 1 and a detailed breakdown of the

records is provided in Appendix 2. The provinces/municipalities in

China with the largest populations were Henan (451 individuals),

Hong Kong (362), Hubei (223), Anhui (170) and Zhejiang (146).

In Taiwan it was restricted to Kinmen Island (about 25 km east

of the coast of mainland China) with a population estimate of 18

individuals. In Vietnam 120 individuals were reported from Cao

Bang province.

The distribution pattern broadly matches that in the published

literature, covering an area of 2,400,000 km2 (excluding isolated

records from Beijing and Hebei which were considered by the

observers to be wandering individuals). Of particular note were

the numbers from the Dabie Shan in central China. Large numbers

were reported from Shangcheng, Gushi and Huaibin counties,

Henan province, between 4-10 December 2014, with an estimated

400-500 individuals in a total of more than 7,000 crows, including

Carrion Crow C. corone , Large-billed Crow C. macrorhynchus,

Daurian Jackdaw C. dauuricus and Rook C. frugilegus. Interviews

with local villagers revealed that Collared Crows were very common

in the area (Henan Wild Bird Society in litt. 30 January 2015).

The Dabie Shan range covers Henan, Hubei and Anhui provinces

(Figure 1) and Liu et al. (2008) listed Collared Crow from all

three areas during 2004-2006. Based on the data presented here,

525 birds were recorded in the Dabie Shan — Henan (412), Hubei

(109) and Anhui (4). These records indicate that the Dabie Shan

Figure I.The distribution of Collared Crow records 2003-2014 (the main stronghold in the Dabie Shan is outlined).

Forktail 32 (2016)

A review of the distribution and population of the Collared Crow Corvus torquatus

43

Shaoguan

Mcizhou

Qingyuan

Heyuan

Chaozhou

Zhaoqing

Huizhou

Jieyarg

Shantou

iuongzhou

:oshan

Shanwci

Dongguan[

Zhongshan

lZhuho!*&

Jiangmen

Yangjiang

Maoming

Zhonjiang

100 150

r Kilometers

200

| Absent

I Present

Figure 2. The distribution of Collared Crow records in Guangdong, Hong Kong and Macau 2003-2014 (the grid is 5 km x 5 km and the presence

or absence of Collared Crows is shown).

is currently the most important stronghold for the species with

about 30% of the total population, followed by Hong Kong with

about 20%.

Surveys of Hong Kong, Macau and Guangdong province

In total 714 squares (5 km x 3 km) were surveyed in Guangdong

(605), Macau (3) and Hong Kong (106). Of the 21 prefectures in

Guangdong province 17 were surveyed, and 9% of all squares in

Guangdong, Macau and Hong Kong were surveyed. The results of

the surveys are summarised in Table 2, and the squares surveyed

shown in Figure 2. In Guangdong the species was recorded from

12 squares, of which 10 were in Shenzhen (immediately to the

north of Hong Kong) and the others were from Yangjiang county

(four individuals) and Huizhou county (a single bird). Records

in Shenzhen and Huizhou county came from large reservoirs

surrounded by orchards or shrubland. The four birds in Yangjiang

county were on a small cultivated plain with extensive rice fields.

The plain itself was surrounded by low (100-300 m) hills, mostly

covered by shrubland and small orchards. It is noteworthy that such

habitats were regularly encountered in other areas, but no Collared

Crows were found.

In Hong Kong it was recorded from 38 of the squares surveyed,

and there were no records from Macau.

DISCUSSION

The findings presented here give a clear picture of the decline of

the Collared Crow. The current situation in Guangdong province,

where it was once clearly much more common and widespread (see

Appendix 1), is indicative of a major decline in both abundance

and distribution. There are clear indications of similar declines

in other provinces, notably Chongqing, Fujian, Hainan (where it

was last recorded in 1963), Hebei, Jiangsu, Macau and Shaanxi.

There are no recent records from Shandong, Shanghai, Shanxi and

Tianjin, hence, although the historical literature suggests it was

never common in these provinces, this would indicate a reduction

in the range of the species.

The revised population estimate presented here of less than

2,000 individuals is substantially lower than the current population

estimate of 15,000-30,000 individuals (BirdLife International

2016). This estimate was largely based on the assumption that

its distribution and abundance in Hong Kong is mirrored across

the rest of its range (S. Chan in litt. 2007, BirdLife International

2016), and whilst it could be argued that there are populations

which remain to be discovered, given that this is a large, readily

identifiable, open-country species it is considered untenable that a

further 13,000-28,000 have been overlooked. In Guangdongit was

recorded in 12 (2%) of 605 squares surveyed, with 15 individuals

recorded, whereas in Hong Kong 362 individuals were recorded in

38 (36%) of 106 squares surveyed. Large areas of Guangdong not

surveyed consist of extensive tracts of habitat unsuitable for this

species and, although not included in the surveys described here,

the hills and forests of Guangdong are relatively well surveyed and

there are very few records from these areas. In a comprehensive

review of birds at nine forest sites in south-east China between

1984 and 1996, Lewthwaite (1996) reported the species trom

only one site, Ba Bao Shan, in Guangdong, where up to three were

seen at 600 m on two dates in June and December. This situation

was confirmed by Lee et al. (2006) who did not record Collared

44

PAUL J. LEADER etal.

Forktail 32 (2016)

Table 1. Summary of all records of Collared Crow during the period

2003-2014.

The list of provinces and municipalities includes all those with historical records.

Historical status: * uncommon; ** uncommon to common; *** common to very common

Crow in surveys of 54 forest areas in southern China, including

Guangdong. More significantly, Zou & Ye (2016), in a review of

all historical records for Guangdong province, listed it from only

15 locations; Guangzhou, Shaoguan, Shenzhen (four sites), Zhuhai,

Shantou, Zhaoqing, Huizhou, Meijing River, Heyuan, Yangjiang,

Qingyuan and Yanfu City.

It is of note that in contrast to the Collared Crow, the

Large-billed Crow remains a common and widespread species

in Guangdong province (pers. obs.). This is thought to be due to

differences in habitat preference, with Large-billed Crow found

mostly in hill forest whereas Collared Crow occurs largely in the

lowlands, which inevitably brings it close to human habitation, thus

making it more vulnerable to persecution and secondary poisoning.

Corvid populations typically include a proportion of non¬

breeding birds and, whilst the breeding ecology of Collared Crow

is little-known, studies of similar species such as Carrion Crow

and American Crow C. brachyrhynchos indicate that breeding

commences when birds are two years old and that a high proportion

of the populations of both species are non-breeding birds (Roselaar

1994, McGowan 1997). Estimates of the proportion of non-breeding

birds in Carrion Crow populations include 77% in Sweden, 50-73%

in Scotland and 40% in France; however, the proportion of non¬

breeding birds could be even higher than this as non-breeding birds

are known to form scattered flocks and even hold territories (Roselaar

1994). Detailed surveys at a roost at Mai Po Nature Reserve, Hong

Kong, indicate that between 49-91% of the population remain in

communal roosts over the breeding season (Stanton et al. in prep.)

and are therefore presumably non-breeding birds.

Based on the population estimate in Table 1, and taking an

indicative range of 40-80% as a guide for the probable proportion

of non-breeding birds in Collared Crow populations, the number

of mature individuals (20-60% of the population) would be in

the range of 400-1,100 birds. This is substantially lower than the

estimate of 10,000-19,999 mature individuals provided by BirdLife

International (2016).

The exact timing of the decline in Collared Crow numbers

in China is difficult to pinpoint. However, it is likely that major

changes in agricultural practices in the 1950s have contributed

significantly and, whilst current threats are unclear, it is assumed

that loss of food supply owing to agricultural intensification and

an associated over-use of pesticides remain major problems. The

low numbers in Guangdong province relative to the numbers in

Hong Kong would indicate that this is an ongoing constraint.

Persecution in some areas by humans is a casual factor (BirdLife

International 2016, Madge 2016) and it is traded at markets in

southern China, although the scale of such trade is unknown

(Kadoorie Farm & Botanic Garden 2004). However, some declines

are much more recent. For example, at Kinmen Island, Taiwan,

up to 176 individuals were recorded in 1989 but it has declined

significantly since then (BirdLife International 2016) to a current

population of about 18 individuals (Table 2). Based on the findings

of this study, this alone accounts for a decline of about 8% in the

world population.

Conservation status

As noted above, both the population estimate and number of

mature adults given by BirdLife International (2016) are considered

to be major over-estimates and a review of the threat status for

Collared Crow is required. Applying IUCN Red List criteria, the

number of mature individuals is probably best placed in the 2,500-

10,000 range. It is difficult to clearly determine subpopulations

Table 2. Summary of coverage and results of surveys conducted in

Guangdong province, Macau and Hong Kong 2003-2014.

Forktail 32 (2016)

A review of the distribution and population of the Collared Crow Corvus torquatus

45

and it could be argued that, given the lack of geographical barriers,

the species should be treated as one subpopulation linked by

dispersal. With less than 10,000 individuals, a continuing decline,

and all mature individuals in the same subpopulation, it would

therefore qualify as Vulnerable under C2(a)(ii). As such it is

proposed that Collared Crow be uplisted from Near Threatened

to Vulnerable.

Further research

There are clearly major gaps in our understanding of the ecology

of Collared Crow and a more detailed understanding of habitat

requirements (beyond a preference for wetlands) and the breeding

ecology of the species are required. In particular, studies of the

age of first breeding and proportions of non-breeding birds are

critical to an adequate assessment of its status. Further surveys in

the Dabie Shan to investigate seasonal variation in numbers and

habitat utilisation are recommended. Surveys in northern Vietnam

looking for additional sites for the species are also recommended.

Finally, communal roosts in Hong Kong have been counted on a

systematic basis for a number of years and such counts enable long¬

term population trends to be assessed (Stanton etal. 2014); studies

of similar roosts elsewhere would be welcome.

ACKNOWLEDGEMENTS

We thank the following: for help with locating books and papers, F. E. Warr

and Alison Harding (BMNH), Linda Birch (Edward Grey Institute, Oxford

University) and Inter-Library Loan staff (Chinese University of Hong Kong);

for help with translation from Chinese, Y.-L. Mo-yung and Grace Yang.

Thanks to Katherine Leung for help with obtaining information through

ChinaBirdnet, Tommy Hui for help with collation and translating website

data, and Jenny Hui and Lag Wan for help with mapping. Jonathan Eames

and Pan Chih Yuan provided details of sightings in Vietnam and Taiwan

respectively, and Rob Martin provided helpful feedback on a draft manuscript.

Finally, this paper would not have been possible without the contributors who

have provided records as detailed in Appendix 2.

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beginning of May, 1860. Ibis 3: 23-57.

Swinhoe, R. (1861b) Notes on ornithology taken between Takoo and Peking,

in the neighbourhood of the Peiho River, Province of Chelee, North

China, from August to December, 1860. Ibis 3: 323-345.

Swinhoe, R. (1863) Catalogue of the birds of China, with remarks principally

on their geographical distribution. Proc. Zool. Soc. London 1863:

259-339.

Swinhoe, R. (1870) On the ornithology of Flainan. Ibis (2)6: 77-97, 230-256,

342-367.

Traylor, M. A. (1967) A collection of birds from Szechwan. Fieldiana Zool.

53 (1): 3-67.

Forktail 32 (2016)

A review of the distribution and population of the Collared Crow Corvus torquatus

47

Vaughan, R. E. & Jones, K. H. (1913) The birds of Hong Kong, Macao, and the

West River or Si Kiang in south-east China, with special reference to their

nidification and seasonal movements. Ibis 55: 17-76, 163-201, 351-384.

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birdingnerd.blogspot.hk/2010/08/china-trip-report-summer-2010.html

on 24/08/2014.

Walton, H. A. (1903) Notes on the birds of Peking. Ibis 45: 19-35.

Wang J. X., Wu S. X., Huang G. Y„ Yang W. Y„ Cai Z. Y„ Cai S. Q. & Xiao Q. I.

(1991) A pictorial guide to the birds of Taiwan. Taipei: Wild Bird Society

Press of Taiwan and Japan. (In Chinese.)

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China Branch of the Royal Asiatic Soc. 55: 156-239.

Wu Z. K„ Lin Q. W., Yang J. L„ Liu J. C.& Wu L. (1986) The avifauna of Guizhou.

Guizhou: People's Publishing House. (In Chinese.)

Yang L. & Yang X. J.: eds. (2004) The avifauna of Yunnan, China, 2. Kunming:

Yunnan Science and Technology Press.

Yen K. Y. (1930) Birds from Yaoshan, Kwangsi. Bull. Dept. Biology, Sun Yatsen

University 5: 1-32.

Yen K. Y. (1932) Etude d'une collection d'oiseaux du nord du Kwangtung.

Bull. Mus. d'Histoire Naturelle 4: 243-261.

Yen K. Y. (1933-1934) Les oiseaux du Kwangsi. L'oiseau et la revue francaise

d'ornithoiogiel : 204-243, 615-638, 755-788; 4: 24-51, 297-317, 489-507.

Zou F.-S. & Ye G.-F., eds. (2016) Distribution list of Guangdong terrestrial

vertebrates. Guangzhou: Guangdong Science and Technology Press

(In Chinese and English).

Zheng Z.-W., Zhang C.-L. & Hu H.-J. (2008) Baseline survey and holistic

characters of bird in Guangzhou, China. Chinese J. Zoo 1 43(1): 122-133.

(In Chinese.)

Zhong F., Dong W., Li W. & Huang X. (2012) Community structure and

diversity of birds in Meijiang River valley. Ecol. & Environ. Science 21 (5):

825-833. (In Chinese.)

Zhou Y. Y„ Qin Y. L., Wang Y. P. & Yu S. J. (1981) On the terrestrial vertebrates

of the Dinghu Shan area. Guangdong Zoot. Soc. Coll. Theses 2: 48-60.

(In Chinese.)

Zhuang X., Cao S. & Hu G. (2013) Survey of vertebrate resources at Dapeng

Peninsula National Geological Park, Shenzhen. Tropical Geography 33(5):

584-587. (In Chinese.)

PAULJ. LEADER& DAVID J. STANTON, AECLtd, 127 Commercial

Centre, Palm Springs, New Territories, Hong Kong. Email: pjt@

aechk.hk (corresponding author), djs@aechk.hk

JONATHAN MARTINEZ, 14 bis, Ruedes Temples, 45240 La Ferte-

Saint-Aubin, France. Email: jonathmartinez@gmaii.com

RICHARD W. LEWTHWAITE, 2 Villa Paloma, Shuen Wan, TaiPo,

Hong Kong. Email: myrivp@gmaii.com

Appendix 1.

Historical distribution of Collared Crow in China andTaiwan 1855-1980.

Overview

David & Oustalet (1 877) noted This crow is one of the most characteristic

birds of the Chinese avifauna. It is found in all parts of the Chinese

Empire outside the mountainous zone, but it is particularly widespread

in southern provinces. It lives in pairs in paddyfields and in the vicinity

of watercourses, and hardly ever ventures into the interior of villages

like its congeners. It is a sedentary species'.

Styan (1891) commented 'A very common resident [in the Lower Yangtse

Basin in the 1880s]... Generally seen singly or in pairs, but in winter a

number will sometimes congregate together. When out shooting I have

been followed for a long distance by at least thirty of them hovering

close overhead, attracted by my dog. They will sometimes follow one

thus for a mile'.

Note: Styan's recording area 'the Lower Yangtse Basin' extended over

the final 1,000 km of the Yangtse River's course between Wuhan and

the Delta, including parts of southern Hubei, northern Jiangxi, southern

Anhui, southern Jiangsu, northern Zhejiang and Shanghai.

Ascherson (1930) commented that 'All the way up the Yangtze and in

the country around Nanking [Nanjing], one is amazed at the numbers

and conspicuousness of the nests of the Magpies, Collared Crows and

Black-eared Kites'.

Distribution by province

Localities and dates of Specimens listed in this section are as enumerated

in the literature and/or listed in museum collections. Acronyms for

museums are as follows:

NHMUK - Natural History Museum, Tring, UK

MCZ - Museum of Comparative Zoology, Massachusetts, USA

ZMB - Universitat Humboldt, Museum fur Naturkunde, Berlin, Germany

RMNH - Naturalis Biodiversity Center, Leiden, Netherlands

Anhui

Abundance/distribution:

Koltoff (1932):'Common [in eastern Anhui in 1922]. Two pairs bred near

Chuchow [Chuzhou].'

Chong (1936): 'The Collared Crow is commonly resided on the plain or

low-hills [in southern Anhui in the 1930s].'

Specimens :

Huang Shan, September 1933 (Chong 1936); Jinhuashan, 25 October

1948 (Cheng 1960).

Beijing

Abundance/distribution:

Swinhoe (1861 b): 'I occasionally saw this species [between Tianjin and

Beijing in I860]'.

Walton (1903): 'In the middle of August [1 900], when I reached Peking,

there were very few of these handsome crows; from October onwards

they arrived in large numbers, and were quite common during the winter.'

Hemmingsen &Guildal (1968): 'Both in winter and summer [in the 1940s]

adults and young are met with in small numbers near water'.

Piechocki (1958): 'I saw them in the rice fields at the beginning of May

[1956]'.

Fiebig (1983): Three active nests found in the Summer Palace grounds,

14 April 1977.

Specimens:

14 January 1898 (MCZ); 3 January 1957, 1 2 and 25 November 1958, 10

September 1961 (Cao 1987).

Chongqing

Abundance/distribution:

Morrison (1948): 'A common bird everywhere [the city of Chongqing

and hills 50 km to its north in the years 1 943-1 945], but generally seen

in the hills in pairs'.

Specimens :

Changshou, 4 April 1 908 (MCZ); Chongqing, May 1 930 (Shaw 1 932).

Fujian

Abundance/distribution:

Swinhoe (1860): 'The common crow [at Xiamen in 1855-1859] ... a

permanent resident'.

La Touche (1892):'Common and resident [at Fuzhou in the late 1880s]'.

La Touche & Rickett (1905): 'The common crow [at Fuzhou in the late

1 890s] ... an early breeder'.

Caldwell & Caldwell (1931): 'This is the well known Parson Crow of the

plains. It may be seen singly or in colonies practically everywhere [in

southern Fujian in the 1 920s]. It abounds in newly ploughed fields and

partly flooded regions ... It is a common scavenger along rivers. At all

times the crows are sociable, but in winter doubly so, assembling by the

hundreds at some common roosting place'.

Cheng (1936a, b): Up to seven individuals recorded on the campus of

Fukien Christian University, Fuzhou in a summer bird survey, June-

August 1 936 and at Changle around the same time.

Cheng (1941a, b): Recorded in summer and winter on the river south of

Shaowu including a total of 24 individuals counted, 26-28 August 1940.

48

PAUL J. LEADER etal.

Forktail 32 (2016)

Specimens:

Xiamen (two), April 1860 (RMNH); Xiamen, April 1861 (BMNH); Fuzhou,

15 December 1895, February 1896, December 1896, 20 January 1913,

December 1913 (three) (MCZ); unknown locality (two), 1903-1909

(Martens 1910); Fuzhou, December 1928 (Kuroda 1929); Shaowu, 24

June 1 937 (Jordans & Niethammer 1 940).

Gansu

Abundance/distribution:

Cheng (1987); Recorded in the southern part of the province.

Guangdong, Hong Kong and Macau

Abundance/distribution:

Swinhoe (1861a): 'Common [in Guangzhou, Flong Kong and Macau in

February-May I860]'.

La Touche (1892) 'Common and resident [at Shantou in the late 1880s]'.

Streich (1903): A common resident at Shantou in the period 1889-1902.

Kershaw (1904): 'Very common and resident [in the Hong Kong-Macao

area in the early 1900s]'.

Vaughan & Jones (1 91 3): 'A common bird throughout the districts treated

in this article [Hong Kong, Macau, the Pearl River Delta, the North River

north to Shaoguan and the West River from the Pearl River Delta through

western Guangdong to Guixian in central Guangxi in 1900-1908] ...

never found far away from water, either salt or fresh ... during the winter

months selects certain favoured roosting-places ... and to these, at the

close of day, large numbers may be seen winging their way from the

feeding-grounds'.

Mell (1922): 'Resident, probably common throughout the province'.

Yen (1930):'Much more common [in northern Guangdong in 1930-1931]

than the preceding species [C. macrorhynchus]'.

Jabouille (1935): 'Much more common [in Zhanjiang in 1932-1933] than

the preceding species [C. macrorhynchus]'

Gressit (1940): One on the Lingnan College campus [now Sun Yat-sen

University], Guangzhou in winter 1939/1940.

Zhou et a/.( 1 981 ): In the Dinghu Shan area, Zhaoqing 1959-1966.

Liao (1982): In the Dinghu Shan area in 1979-1980 in similar numbers

to previous years.

Guan etal. (1986): Breeding on Sanzao Island in the Pearl River Delta in

1980-1981.

Sun et a!. (2003): Recorded from Nan’ao Island with counts of up to 3

between 14-17 June 2001 .

Zou & Ye (2016): Listed from the prefectures/cities of Guangzhou,

Shaoguan, Shenzhen, Zhuhai, Shantou, Zhaoqing, Huizhou, Meijiang

River, Heyuan, Yangjiang, Qingyuan and Yunfu.

Specimens:

Naozhou Island, 2 February 1868 (Swinhoe 1870); Macau, 14 March

1 902 (NHMUK);'Nam Long' [untraced locality on North River], 22 March

1905 (NHMUK); Fengwan, 3 April 1916, Xiaokeng, 5 February 1917

(ZMB); northern Guangdong (three), 19 March 1930, 8 January 1931

(Yen 1930); Zhanjiang (three), 1 and 12 May 1932 (Jabouille 1935);

Lianshan, Yangshan, Lianping, Qieyang, Lufeng, Chao'an, Chenghai and

Guangzhou, late 1 950s-early 1 960s (SCIEA 1991).

Guangxi

Abundance/distribution:

Vaughan & Jones (1 91 3): 'A common bird [along the West River from

Wuzhou to Guixian in the early 1 900s]'.

Yen (1930) 'A common resident up to 250m [at Yao Shan]'.

Yen (1933-1 934) 'Sedentary [in central and eastern Guangxi] and even

more common than the preceding species [C. macrorhynchus]'.

Specimens:

Pingnan, 20 April 1931 (Yen 1933-1934).

Guizhou

Abundance/distribution:

Wu etal. (1986): Flocks of several tens encountered in the vicinity of villages

and farmland (300-2,400 m) in winter and spring in 1 963-1982, and a nest

containing two young birds found at Longlixian on 28 April 1981.

Specimens:

Yinjiang, 25 April 1 964, Xingyi, 23 October 1 974, Chishui, 24 April 1 975,

Zunyi, 20 May 1975, Suiyang, 8 and 13 December 1976, Guiding, 18

November 1977, Jiangkou, 15 March 1978, Xifeng, 7 December 1978

(Wu etal. 1986).

Hainan

Last recorded 1963.

Abundance/distribution:

Swinhoe (1870): 'In the plains of the north and north-west of Hainan

this bird frequently occurs ... it is evident that they are early breeders

in Hainan as in South China'.

Ogilvie-Grant (1900): Seen at Haikou, 5-9 Marchf 1899 per John

Whitehead's diary.

Specimens:

Haikou (three), February/March 1868 (Swinhoe 1870); Haikou, 1890 or

1891 (Hartlaub 1892); Haikou (10), February-April, November-December

1902, Ledong, 11 March 1903, Utoshi, 21 March 1903 (Hartert 1910);

Haikou, 20 January 1 920 (Kuroda 1921); Wenchang, January, February

and June in the late 1950s or early 1960s (Cheng &Tan 1973); Wanning,

31 May 1960, Lingshui, 7 and 13 February 1963 (South China Institute

of Endangered Animals collection, Guangzhou, China).

Hebei

Abundance/distribution:

Wilder & Hubbard (1924): 'Fairly common resident throughout the

province, but less common at the seashore and in the mountains. It

also seems less common in summer than at other seasons. Lays in April

and May'.

Specimens:

Xian and Hejian in the 1920s or 1930s (Seys & Licent 1933-1934 in

Hemmingsen & Guildal 1968).

Henan

Abundance/distribution:

Fu (1937):'Sedentary and common on the plain [in the years 1931-1934]'.

Hubei

Abundance/distribution:

La Touche ( 1 922): 'A common resident [at Shashi inthe years 1917-1919]'.

Specimens:

Yichang, October or November 1 880 (Slater 1 882); Yichang 1 0 October

(three) and 31 October 1907, 'Chang Koo Hsien' [untraced locality in

western Hubei], 3 February 1908 (MCZ).

Hunan

Specimens:

Dongting Lake, 21 November 1898 (Ogilvie-Grant 1900); Changde, 24

and 26 October, Hengshan, 4 April, Liling, 9 June, Leiyang, 27 November,

Zixing, 1 3 November, Yizhang, 9 November in 1 955 and 1 957 (Cheng et

al. 1960-1961).

Jiangxi

Abundance/distribution:

Presumably recorded in the north of the province by Styan (1891).

Jiangsu

Abundance/distribution:

La Touche (1906-1 907): 'A very common resident [at Zhenjiang in the

early 1900s]'.

Koltoff (1932):'Common [in Jiangsu south oftheYangtse River in 1921-

1922]; not so common north of the river'. The author also reported the

progress of 31 pairs nesting in the plains and hills near Zhenjiang and

mentioned another pair at Suzhou.

Ascherson ( 1 930): 'Very common [at Nanjing in April-May 1930]'.

Chang (1932): 'One of the common crows [in the vicinity of Nanjing,

1931-1932]'

Chong (1938):'One of the common residents [in Nanjing, 1925-1936]'.

Specimens:

Nanjing, 25 October 1923 (MCZ), Nanjing (ten), unknown dates 1925-

1936 (Chong 1938).

Shaanxi

Abundance/distribution:

Cheng et al. (1962): Up to 12 birds encountered in a single day in the

Qinling mountains in April— July, 1957-1958.

Specimens:

Yang Xian, Zhanba, unknown dates in 1957-1958 (Cheng etal. 1962).

Shandong

Abundance/distribution:

LeFevre (1 962):'Most numerous in western Shantung [1 923-1 927]. They

decrease in numbers as one goes from Tsinan [Qinan] towardsTsingtao

[Qingdao], so that as one reaches the central part of the province, one

rarely sees them ... during the winter they can be seen in numbers at

Tsinan ... a bird of the plain'. The author also reported a pair seen at

Weishan on 1 6-1 7 and 26 January 1 925, seven seen by George Wilder

at Dexian on 14 April 1935 and two at Ling Xian on 26 April 1936.

Specimens:

Laiyang, 5 May 1909, Qinan, 30 June 1911, Jimo, 1 1 October 1912,

'Hsingtsunchai' (untraced locality in eastern Shandong), 27 June 1937

(LeFevre 1962).

Forktail 32 (2016)

A review of the distribution and population of the Collared Crow Corvus torquatus

49

Shanghai

Abundance/distribution :

Sowerby (1943): 'A permanent resident ... may occasionally be seen

passing over city and suburban districts of Shanghai [between the 1920s

and early 1 940s], but is not very plentiful . . . Two were seen by me in the

Western District this spring (1943), being joined later in the summer by

four young ones'.

Li etal. (1959): Recorded in all months during surveys, 1951-1959.

Specimens :

28 January 1 884 (NHMUK); unknown dates prior to 1 943 (Sowerby 1 943).

Shanxi

Abundance/distribution:

Cheng (1987): Recorded in the southern part of the province.

Sichuan

Abundance/distribution:

David (1871): Occurs in Sichuan.

Dye (1969): Sightings of 20-30 individuals near the West China Union

University campus, Chengdu in the 1920s and 1930s, but numbers down

in the 1 940s likely as a result of engineering works on the river.

Cheng (1987): Recorded at Kangding.

Specimens:

Washan, 6 November 1 908 (MCZ); Mingshan, 7 May 1931, near Emei Shan,

23 November 1931 (Traylor 1967);Yaan (five) and Chengdu, July-August

1 934 (Schafer & de Schauensee 1 938); Emei Shan (four) March-June in

1957-1960 (Cheng etal. 1963); Maowen, May 1961 (Cheng etal. 1965);

Baoxing (850-2,300 m), March-May, September, December 1962-1965

(Li etal. 1976).

Tianjin

Specimens:

Tianjin, 1920s or 1930s (Seys & Licent 1933-1934 in Hemmingsen &

Guildal 1968).

Yunnan

Abundance/distribution:

Yang & Yang (2004): Recorded at Kunming and Yongshan (760-2,100 m).

Zhejiang

Moffett & Gee (1913): At Jiangyin, Hangzhou and Mogan Shan on

unknown dates prior to 1913.

Gayot (1922): Recorded on six visits to the Haining area in December,

February and March, 191 7-1920.

Shaw (1934): 'A permanent resident of the plain and foothills [in the

early 1930s] ... single birds or small flocks often met with'.

Specimens:

Hangzhou, 1 6 October 1931, Wenzhou, 24 July 1 932 (Shaw 1 934).

Distribution in Taiwan

Abundance/distribution:

There are only three records from mainland Taiwan, all in the period

1979-1987: at Taichung on 10 October 1979 and 7 August 1981 and at

Nantou on 8 August 1987 (Wang etal. 1991, Severinghaus etal. 2012).

It is/was essentially restricted to Kinmen Island, where up to 176

individuals were recorded in 1989, but it has declined significantly since

then (BirdLife International 2016).

Appendix 2.

Collared Crow records in China, Taiwan and Vietnam, 2003-2014.

50

PAUL J. LEADER etal.

A

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51

52

PAULJ. LEADER etal.

Forktail 32 (2016)

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A review of the distribution and population of the Collared Crow Corvus torquatus

53

* site falls within the Dabie Shan

** maximum count generated from a communal roost count

? data/information unavailable

Hong Kong Birdwatching Society observers:

John Allcock, Ruy & Karen Barretto, Abdel Bizid, Lester Bull, M. L. Chalmers, S. M. Chan, Sonny Chan, Beetle Cheng, Tommy Cheung, William Cheng, Gary Chow, Chris Campion, Cheung Mok, Jose Alberto, Chima,

Chung Yun Tak, Bart De Schutter, D. A. Diskin, G. J. Carey, John Clough, Ho Wai Chun, Ivan Tse, A. J. Hardacre, John & Jemi Holmes, Tony Hung, James Lambert, Katherine Leung, Kwan Po Kuen, Kwok Pun Chau

John, Lai Nga-yee, Lo Chun Fai, Lee Kwok Shing, Richard Lewthwaite, M. Lisse, M. D, Williams, Ms. Jimmy Chim & Mr. William Tsui, Nora Hung, Mike Kilburn, Roger Lee, George Harry/Nenita Miller, Roger

Musgrove, Alan Pong, Bena Smith, Bond Shum, S. H. So, Sung Yik Hei, S. L. Tai, Graham Talbot, Dylan Thomas, Geoff Welch, Captain Wong, Michelle & Peter Wong, Tse Wai Lun & Ying Hak King, Yeung Lee Ki,

Vicky, Ying Hak King and Yu Yat-Tung.

FORKTAIL 32 (2016): 54-57

Is the population trend of the Bearded Vulture Gypaetus

barbatus in Upper Mustang, Nepal, shaped by diclofenac?

KHADANANDA PAUDEL, KRISHNA P. BHUSAL, RAJU ACHARYA, ANAND CHAUDHARY, HEM S. BARAL,

ISHWARI P. CHAUDHARY RHYS E. GREEN, RICHARD J. CUTHBERT & TOBY H. GALLIGAN

The Bearded Vulture (or Lammergeier) Gypaetus barbatus has been uplisted to Near Threatened because of declines throughout most of its

range. In Upper Mustang, Nepal, the species underwent a substantial decline between 2002 and 2008. Diclofenac poisoning, through the

consumption of contaminated livestock carcasses, is a serious threat to a number of scavenging raptors in South Asia. It is not known whether

Bearded Vultures are intolerant to diclofenac; however, the timing and magnitude of the decline in Upper Mustang parallel those seen in the

population of Himalayan Griffons Gyps himalayensis and the populations of six other South Asian vulture species, most of which are known

to be intolerant to diclofenac. In this study, we continued the Upper Mustang survey for Bearded Vultures and use generalised linear models

to examine the population trend between 2002 and 2014. We confirm a substantial decline after 2004 and show that this trend continued,

albeit at a slower rate, up to 2014. However, we also show that subpopulations in remote valleys did not decline. We suggest that these trends

are a strong indication that Bearded Vultures are intolerant of diclofenac and that the biology of the species and additional targeted threats

are limiting its recovery in Upper Mustang.

INTRODUCTION

In 20 1 4, the Bearded Vulture Gypaetus barbatus was uplisted to Near

Threatened in response to declines observed throughout most of its

fragmented range. The global population of the species is estimated

to be between 2,000 and 10,000 individuals and it faces a range

of concurrent threats, including direct persecution, non-targeted

poisoning, nest-site disturbance, decreasing food supplies and

collision with human-made structures (BirdLife International 2015).

Nepal once held one of the largest populations of breeding

Bearded Vultures in the Himalaya (Gil et al. 2009). Two recent

surveys of the species have taken place in the mountain district of

Mustang. The first showed a 73-80% decline between 2002 and

2008 in Upper Mustang (Acharya et al. 2010) whilst the second

showed a stable population in the Lower Mustang between 2002 and

2006 (Giri 2013), although the two surveys differed in their methods

and therefore are not directly comparable. However, the number

of individuals observed per day and per km in the Lower Mustang

study — 0.50-0.80 individuals/day and 0.03-0.05 individuals/

km (Giri 2013) — were comparable with the rates observed at the

end of the Upper Mustang study — 0.76 individuals/day and 0.07

individuals/km (Acharya et al. 2010). The rates at the start of the

Upper Mustang study were considerably higher — 2.79 individuals/

day and 0.35 individuals/km (Acharya et al. 2010). Because the

timing of both surveys was similar, this evidence may suggest that a

similar large decline did indeed occur in Lower Mustang, but before

2002 when the survey first took place.

Diclofenac poisoning is a serious threat to vultures in South

Asia (Oaks et al. 2004, Green et al. 2004, 2007, Shultz et al. 2004).

Vultures are exposed to non-steroidal anti-inflammatory drugs

(NSAIDs), such as diclofenac, through the consumption of carcasses

of recently treated livestock. Diclofenac was available in India from

1994, the same year that declines in vultures were first recorded

there (Cuthbert et al. 2014) and in Nepal shortly after 1994, but

declines in vultures there were first recorded in 2002 (Baral et al.

2004). Certainly, in 1995, in an area adjacent to Upper Mustang, a

survey for Bearded Vultures showed encounter rates similar to those

observed at the start of the Upper Mustang study — 5.10 individuals/

day and 0.38 individuals/km (Gil et al. 2009). Therefore, it is

probable that declines in vultures occurred first in the lowlands and

later in the highlands in Nepal. This conclusion seems logical given

the differences in human cultures, agricultural practices, income

and trade that differentiate the lowland and highland communities,

which led to diclofenac initially being more readily available and

affordable in the lowlands.

Intolerance to diclofenac has been shown in Gyps vultures (Oaks

et al. 2004, Swan et al. 2006, Das et al. 2010) and Aquila eagles

(Sharma et al. 2014), both through experiments and examination

of dead individuals found in the wild. It is not known whether

Bearded Vultures are intolerant to diclofenac. However, the timing

and magnitude of the decline in Upper Mustang are parallel to those

seen in the population of Himalayan Griffon Gyps himalayensis in

Upper Mustang (Acharya et al. 2009) and populations of six other

vulture species in Nepal and India (Cuthbert et al. 2006, Prakash

et al. 2007, Chaudhary et al. 2012), most ofwhich are known to be

intolerant to diclofenac. Since the 2006 ban on diclofenac in Nepal

and India, declines in these populations of vulture have slowed,

stabilised and possibly reversed (Prakash et al. 2012, Galligan et al.

2014). Most notable for this study is the almost complete recovery

of the Himalayan Griffon in the Upper Mustang (Paudel etal. 2015).

In this study, we continued the Upper Mustang survey for Bearded

Vultures for three years following the methods of Acharya et al.

(2010). We combine their data with ours and examine the population

trend between 2002 and 2014 using a refined method of analysis. We

specifically tested whether the population decline in Bearded Vultures

in Upper Mustang had slowed after the 2006 ban on diclofenac.

METHODS

The Upper Mustang, the northern part of the Mustang district, forms

part of the arid trans-Himalayan zone, with steep peaks and deep

valleys at altitudes above 2,850 m. Surveys were conducted in 2002,

2004, 2005, 2008, 2010, 2012 and 2014. Each survey commenced

on or after 13 July and was completed on or before 18 September,

which coincided with the end of the Bearded Vultures’ breeding

season. Variations in start and end dates were a result of adverse

weather conditions delaying and/or suspending surveys.

Two to four surveyors were present on each survey, with at least

one of them having participated in a previous survey. Surveyors used

the main trails used by local people to travel between settlements as

transects, which they walked, as the locals do. Surveys commenced

at 08h00 and ended at 17h30 each day and a consistent walking

pace with regulated rest periods was maintained throughout the day.

All Bearded Vultures observed on both sides of each transect were

counted and all sightings were confirmed by two or more surveyors.

Forktail 32 (2016) Is the population trend of the Bearded Vulture in Upper Mustang, Nepal, shaped by diclofenac?

55

Distinguishable plumage features, associated with age and/ or moult

patterns, and flight patterns (e.g. circling, flying), including altitude

and direction, were agreed by the surveyors present and used to help

identify individual vultures in order to avoid counting the same

individual more than once.

Acharya etal. (2010) surveyed four transects, although they were

not mutually exclusive — two transects covered the same ground in

opposite directions, three transects consisted of outward and return

journeys along the same ground, and two transects radiated no more

than 20 km from the same starting point, which is a short distance

for a Bearded Vulture to fly. In surveys after 20 1 0, we surveyed three

transects (Figure 1) in one direction:

1 ) Kagbeni to Lomanthang (heading north-east), 47 km over 5-7

days

2) Lomanthang to Samjung (heading north-east), 12 km in 1 day

3) Lomanthang to Yara( heading south-east), 18km over l-2days.

In this way, we avoided counting vultures along transects more

than once. Furthermore, these transects followed the same routes

as three transects used by Acharya et al. (2010), enabling us to

use a subset of their data in our analysis. Neither the Lomanthang

to Samjung nor the Lomanthang to Yara transects were surveyed

in 2002. We recalculated walking distances along transects using

Google Earth.

We analysed transects independently since our three transects

radiated from Lomanthang. We considered the Kagbeni to

Lomanthang transect to be our primary transect and used it to

examine the population trend. We considered the other two transects

to be secondary transects and used these to provide additional

information on population trends. We calculated the number

of Bearded Vultures along each transect on each survey day and

survey km per transect. We examined the population trend along

the primary transect by fitting a Poisson linear regression with time

(year) elapsed since the first survey (2002 or 2004) as a continuous

Figure 1. Map of Nepal and Upper Mustang showing three transects:

1) Kagbeni to Lomanthang; 2) Lomanthang to Samjung; and

3) Lomanthang to Yara.

explanatory variable t and coun t as a response variable. We compared

results from the linear regression to those of a quadratic (t + t2)

and cubic (t + T + t3) regression with F tests to test if changes in

population change had occurred. In addition, we added altitude

(m) reached at the end of the day as the continuous explanatory

variable a and the interaction between t and a to the best model

to test if altitude had an effect on population trends. We estimated

the percentage mean annual rate of population change as 100*(1 -

exp(£)), where k is the regression coefficient. Statistical analyses were

performed in R (R Core Team 2015).

RESULTS

Along the primary transect, the total number of Bearded Vultures

declined by 96.4%, from 28 to 1 (Table 1), between 2002 and 2008. A

larger number of vultures was counted in the three subsequent years.

Between 2002 and 2014, the total number declined by 89.3%, from

28 to 3 (Table 1, Figure 2). Our Poisson linear regression estimated a

mean rate of population decline along our primary transect of 19.2%

per year. Neither the quadratic nor cubic terms improved model

fit significantly {p > 0.2), indicating that the number of vultures

continued to decline throughout the study period. We found that

altitude (Table 2) had no effect on population decline [p > 0.6).

Table 1. Total number, number per day and number per kilometre of

Bearded Vultures counted on three transects and during seven survey

years in Upper Mustang.

nc indicates that this transect-year combination was not surveyed.

Table 2. Total number of Bearded Vultures counted per survey day and

survey year along the transect from Kagbeni to Lomanthang. Also shown

is the altitude reached at the end of each survey day, whilst nc indicates

that this transect-year combination was not surveyed.

Figure 2, Total numbers of Bearded Vultures counted along the three

transects during the seven annual surveys in Upper Mustang.

56

KHADANANDA PAUDEL etal.

Forktail 32 (2016)

The total numbers of vultures counted on secondary transects

were similar between 2004 and 2014. These numbers were more

or less stable, with only four or fewer vultures per transect during

the survey period (Table 1). Furthermore, the numbers of vultures

per day and per km were similar for both secondary transects

throughout the survey period (when vultures were present). In

2012 and 2014, similar numbers of vultures were counted along

all three transects (Figure 2), but the number per day and number

per km counted along the primary transect were considerably less

than those counted along the secondary transects when vultures

were present (Table 1).

DISCUSSION

We confirm the sudden and substantial decline in the population

of Bearded Vultures in Upper Mustang between 2004 and 2008

(Acharya et al. 2010). In addition, we show that this trend

continued, albeit at a slower rate, into the next decade. However,

we also show no change in trend in remote valleys during the same

period. The Bearded Vulture population trend contrasts with that

of the Himalayan Griffon observed in Upper Mustang, which has

substantially recovered (Paudel et al. 2015).

Upper Mustang is a small part of the range of Bearded Vultures

in Nepal, so our results may not be applicable to the entire range of

the species. In addition, our survey method meant that data were

collected from a single short period in each year and were thereby

possibly influenced by temporary differences in variables, such as

weather conditions, ranging behaviour and food availability. This is

particularly important for Bearded Vultures, which hold very large

territories — tens of thousands of km2 (Gil et al. 2014). Despite

these limitations, our data, from a transect that we repeatedly

surveyed, suggest a rapid then slower decline in the Bearded Vulture

population. Hence, the population trend we report mirrors those

of all seven vulture species presently being monitored in South

Asia (Prakash et al. 2012, Galligan et al. 2014, Paudel etal. 2015).

Our findings strengthen the case for diclofenac poisoning being

the cause of the observed decline in Bearded Vultures in Upper

Mustang. We know that diclofenac was available in Upper Mustang

before the 2006 ban (Acharya et al. 2010). It seems possible that

Bearded Vultures are not able to tolerate diclofenac given that it

appears that one non -Gyps accipitrid, the Steppe Eagle Aquila

nipalensis , cannot tolerate the drug (Sharma et al. 2014) and to

date no accipitrids have been found to be tolerant of it. Bearded

Vultures are probably also readily exposed to diclofenac residues

in domesticated ungulate carcasses, either through bones, marrow

or soft tissues because, despite specialising in consuming bones,

this species also consumes soft tissues (Ferguson-Lees & Christie

2001, Margalida et al. 2009). It is perhaps curious that the rapid

decline in Bearded Vultures in Upper Mustang appears not to have

started until 2004 and to have continued until 2008; however, it

probably started earlier, as it did in the 'White-rumped Vulture G.

bengalensis in lowland Nepal (Prakash etal. 2012), and diclofenac

was probably used after the ban until stocks ran out, but we lack

the data to test these ideas.

Secondary poisoning (poison bait incidentally killing non-

targeted species) does occur in Nepal and can kill large numbers

of vultures per event, thereby causing local declines in vulture

populations. However, the incidence of poison-baiting is likely to

be far less than the use of diclofenac to treat domestic livestock prior

to the ban (Paudel etal. 2016). For example, at least five poisoning

events in which three Bearded Vultures perished each time would

have had to occur in a single year (September 2004-June 2005)

to cause the observed decline along the primary transect. Such a

high frequency of secondary poisonings has never been recorded

in Nepal (BCN unpublished data). Therefore, in Upper Mustang

the use of diclofenac to treat livestock is the most likely cause of

the observed decline.

Why did we not see declines in populations of Bearded Vultures

in remote valleys as we did in the larger populations in relatively

less remote valleys? An obvious answer is that the decline was

linked to human activities. Our primary transect, despite being

only a walkable path, followed the main thoroughfare in the Upper

Mustang — Kagbeni (with about 1,300 inhabitants), the start of

the primary transect, is 8 km from road and air links with other

Nepalese centres, whilst Lomanthang (900 inhabitants), at the end

of the primary transect, has a road link with Chinese centres only 20

km further north, and hundreds of people live in the many villages

and hamlets between Kagbeni and Tomanthang. In contrast, our

secondary transects followed less frequently used paths to one or

two small and remote hamlets. Given the greater human population,

wealth and trade connections along the primary transect, veterinary

use of diclofenac and thereby contamination of livestock carcasses

was likely to be greater there than along the secondary transects.

Other human activities that threaten Bearded Vultures might also be

greater along the primary transect, including secondary poisoning

and persecution, which we describe below. The secondary transects

followed high altitude valleys, but given that altitude did not affect

the decline along the primary transect, we do not think that altitude

alone protected Bearded Vultures.

Why did we not see a recovery in the population of Bearded

Vultures as we did for the population of Himalayan Griffons in

Upper Mustang? Two possibilities that are not mutually exclusive

are, first, that Bearded Vulture and Himalayan Griffon populations

are not comparable in size and behaviour. Bearded Vultures hold vast

territories and are therefore relatively scarce, whereas Himalayan

Griffons are gregarious and relatively abundant. Paudel etal. (2015)

suggested that Himalayan Griffons in Upper Mustang were able

to recover quickly through regular influxes of large numbers of

immature individuals during their annual migration from Central

to South Asia, but lacked data to show this. In contrast, the recovery

of Bearded Vultures in Upper Mustang is more likely to be reliant

on the irregular addition of immature individuals during annual

non-directional dispersal from Central Asia and probably remote

valleys in the trans-Himalayan zone of Nepal, but we also lack

data to show this. Second, unlike other vulture species, Bearded

Vultures are subject to targeted persecution by local people in

Nepal — adult birds are hunted for their intestines, which are used

to treat diarrhoea, nestlings are collected to bring good fortune to

households, and nests are disturbed or destroyed to recover rope and

fabric that this species often uses as nest-building material (Acharya

et al. 2010, KP pers. obs.). Such additional threats would impede

the recovery of the species, although empirical evidence about the

extent to which these activities threaten the species, in the Upper

Mustang and elsewhere in Nepal, is lacking. Future conservation

research should examine the impact of persecution on populations

of Bearded Vultures throughout Nepal. If persecution is determined

to be a serious threat, then advocacy and awareness programmes

should be undertaken to ensure the survival of Nepal’s globally

important population of Bearded Vultures.

ACKNOWLEDGEMENTS

This research was supported by the Department of National Parks and Wildlife

Conservation, Nepal, the National Trust for Nature Conservation, and the

Annapurna Conservation Area Project, Nepal; it was funded by the UK

Government Darwin Initiative (18-008), the RSPB Centre for Conservation

Science, Cambridge University’s Student Conference on Conservation Science

and Bird Conservation Nepal. We would like to thank Tashi Dindhuk Gurung,

Buddhi Gurung, Manoj Joshi and Buddhi Ram Mahato for their assistance

during the field work.

Forktail 32 (2016) Is the population trend of the Bearded Vulture in Upper Mustang, Nepal, shaped by diclofenac?

57

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Lazimpat, Kathmandu, Nepal.

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FORKTAIL 32 (2016): 58-61

Results of the first systematic boat-based seabird survey

in Sri Lanka

L. D. PERERA & A. D. ILANGAKOON

Sri Lankahashighavifaunal diversity but pelagic seabirds are the least studied group due to the constraints of conducting dedicated surveys

at sea. Most early seabird records were from sightings at coastal viewpoints and the occasional stranding but, in the last few decades, some

data have been collected opportunistically during boat-based cetacean surveys around Sri Lanka. This even resulted in the addition of new

species to Sri Lanka's bird list, indicating that cetacean surveys could become important platforms of opportunity for seabird observation.

In 2008 we initiated the first joint cetacean and seabird survey off south-western Sri Lanka, using compatible survey methodologies. The

avifaunal results from this study are presented and discussed here. The benefits of the combined survey are also highlighted to show how

such replicable surveys can become a useful model for seabird studies in developing countries where resources are limited.

INTRODUCTION

Sri Lanka is an island lying oft the south-east coast of south India

(5.916°-9.833°N 79.700°-81.883°E). Due to its tropical climate,

varied vegetation and diverse habitats, the island is rich in avifauna,

including endemic, resident and migrant birds. While research

studies on the avifauna have been carried out on the island for

well over a century (Warakagoda & Sirivardana 2011), pelagic

seabirds have been the least studied group. This is primarily due

to the financial and practical constraints of examining a group of

birds that are often difficult to study through land-based surveys.

Likewise, dedicated sea-based research cruises to study seabirds

alone are a luxury too costly for a small developing country. Most

records of seabirds were therefore sightings from coastal viewpoints

and the occasional stranding (De Silva 1997), and several such early

sightings were considered as vagrancies or stragglers due to a lack of

knowledge of seabirds (Wijesinghe 1994).

Forty-nine species of seabirds have been recorded on Sri Lanka

since 1880, of which ten are considered vagrants (Warakagoda et

al. 2013). Seven are listed as regular or irregular breeders.

Another important group of little-studied fauna that abound

in Sri Lanka’s waters are the cetaceans, with some species known to

be globally Endangered (Leatherwood & Reeves 1989, Ilangakoon

2006). Being a group of charismatic megafauna, funding for

research on cetaceans is more readily available, hence dedicated

vessel-based cetacean surveys have been carried out in Sri Lanka’s

waters over several decades (Ailing 1986, Ilangakoon et al. 2000,

Ilangakoon 2001 , 2005, 2008, 2009), in the course of some of which

opportunistic data on seabirds were also recorded (Ilangakoon

Figure 1 . Survey sites and transect lines.

2001). Such observations even resulted in the addition of species

not previously recorded in Sri Lankan waters (Karunaratne 1994,

Ilangakoon 2001). These discoveries indicated that vessel-based

cetacean surveys could become an important opportunity for

pelagic seabird observations and data collection in countries such

as Sri Lanka which lack the resources for dedicated seabird surveys.

In order to test the feasibility of carrying out simultaneous

cetacean and seabird studies we initiated the first joint cetacean

and seabird survey off south-western Sri Lanka in 2008-2009. The

primary objective was to pool the available resources and maximise

the benefits of data collection for both these important faunal

groups, using compatible survey methodologies. Elere we present

the results of the avifaunal survey as a cost-effective method of

undertaking seabird studies in developing countries.

METHODS

Two areas off the south-west coast of Sri Lanka with different depth

profiles were selected for the study, which was carried out over a

period of eight months from September 2008 to April 2009. The

selected sites were offBeruwala (6.467°N 79.983°E) and Mirissa

(5.967°N 80.483°E), two fishing ports about 170 km apart (Figure

1). One survey cruise per month was undertaken at each site, using

an 11 m fishing vessel powered by inboard engines, travelling at

an average cruising speed of 10-12 km per hour. A predetermined

saw-tooth-shaped transect line, designed to maximise coverage

of the selected areas, was repeated each month. The transect line

off Beruwala straddled the 50 m depth contour, and the entire

transect was within the continental shelf. In contrast, the transect

line at Mirissa straddled the continental shelf break at 200 m

and included areas of deep water beyond the shelf. Standard line-

transect methodology (Tasker et al. 1984, Strindberg & Buckland

2004) was used to assess the relative abundance of species during

different months in the two selected areas. Surveys were carried out

in suitable weather conditions when the sea-state and visibility were

good. If the sea-state deteriorated to above Beaufort 4 or heavy rain

made visibility too poor, the survey was suspended until conditions

improved or discontinued for the day, depending on the time of day.

Two dedicated seabird observers, equipped with binoculars,

were on watch at all times during surveys, in addition to the cetacean

observers onboard. All bird sightings were recorded as half-hour

counts with the position, species, number, flock composition and

activity on a standard data-sheet designed for the purpose. Basic

environmental parameters such as weather and sea-state were also

recorded and images and video footage were obtained when possible.

The data thus obtained were tabulated and examined in terms of

species composition, relative abundance and distribution in order to

Forktail 32 (2016)

Results of the first systematic boat-based seabird survey in Sri Lanka

59

determine patterns of occurrence and distribution and differences

between sites and months.

RESULTS AND DISCUSSION

*

A total of 16 species of seabirds were observed during the study

period from the two sites (Table 1), including 10 of the 16 members

of the Sternidae family recorded in Sri Lanka. Five of the seven

Sternidae species regularly or irregularly recorded breeding on

Sri Lanka (Wijesinghe 1994) were encountered: Greater Crested

Tern Thalasseus bergii. Roseate Tern Sterna dougallii. Common

Tern Sterna hirundo, Little Tern Sternula albifrons and Bridled

Tern Onychoprion anaetbetus were the most common species

noted during the surveys (Table 1). Other Sternidae encountered

were Common Gull-billed Gelochelidon nilotica , Sooty O.fuscatus ,

Lesser Crested T. bengalensis and White-winged C. leucopterus

Terns (Table 1). Four of the 12 Procellariiformes and two of the

four Stercorariidae recorded for the country were also observed.

Bridled Tern was the most numerous species at both sites

(Table 1), with sightings throughout the study period. This species

was seen in both coastal and pelagic waters, but rarely more than 1 2

km from the coast or very close to the shore, indicating a definite

corridor or flight path. Resting birds were often seen perched on

floating debris. The largest numbers were recorded in September

and October at both sites, while numbers were also slightly higher

off Beruwala from January to March, and off Mirissa in March

(Table l). Bridled Terns are known to be the commonest pelagic

seabird around Sri Lanka (Ilangakoon 2001). They have been

observed breeding among nesting Common Terns on an islet in

Adam’s Bridge in the Gulf of Mannar, off the north-west coast

(Perera 2003), and large numbers of both species were seen in flight

over other islets that may also have been used for nesting. These

observations confirm that Bridled Tern is a breeding resident,

moving in search of food depending on ocean currents and

upwellings (Ffarrison 1985, Robertson 1994). Using land-based

observations, De Silva (2003) claimed a mass southward migration

of this species, with numbers declining dramatically by November

and no sightings thereafter. However, data from the current survey

contradict this and show that significant numbers were present in

coastal waters between November 2008 and April 2009. Sightings

ranged from single individuals to over a hundred birds during half-

hourly counts. Bridled Terns were also often encountered in mixed

flocks with Common Terns and occasionally a few Whiskered and

Little Terns. These mixed-species flocks were always encountered

around visible sea-surface food sources such as baitfish, and

sometimes associated with feeding dolphins.

Common Tern was the second most-recorded species: numbers

increased in January at Beruwala and in February at Mirissa

(Table 1). Common Tern sightings varied from single birds to groups

of more than forty and were also often found in mixed-species flocks

with Bridled and Whiskered Terns. The species can be described

as a semi-pelagic tern, as birds were seen nearer to the shore than

Bridled Tern, although in smaller numbers.

Whiskered Tern was most often encountered nearer to harbours

or close to the shore, occasionally with Common and Bridled Terns.

Sightings varied from a few individuals to a dozen out at sea. The

species was not seen at either site in September but there was a

steady increase from October, peaking in January at Beruwala and

in February at Mirissa, after which a gradual decline in numbers was

observed (Table 1). This could be due to flocking prior to dispersal

to inland waters, as this species breeds at favoured inland sites.

Little Terns were absent from Beruwala during September and

October and from Mirissa between September and November.

Numbers were generally low except for a high count at Mirissa in

February, with large flocks of 30-80 birds moving in a southerly

direction (Table 1), perhaps paralleling the movement of Whiskered

Terns, although Little Terns also breed on the coast.

Greater Crested Terns were present throughout, but numbers

increased towards the latter part of the study (Table 1), probably

due to the timing of the breeding season, from April to July

(Warakagoda 1994), when they nest on coastal islets and rocky

outcrops. They were observed close to shore as well as further out

at sea, and occasionally perched on floating debris.

Only a single Lesser Crested Tern was seen in the first three

months of the survey. Numbers at Mirissa increased from December

to a maximum of 24 in February, but declined in March and April;

this species is known to be a winter visitor to Sri Lanka (Rasmussen

& Anderton 2012).

One of the biggest surprises during the survey was the sighting

of a single White-faced Storm Petrel Pelagodroma marina , the

first confirmed sighting for Sri Lanka (Hettige 2008), although

Robertson (1994) and Lamsfuss (2000) mentioned that this species

might occur during the south-west monsoon.

Swinhoe’s Storm Petrel Hydrobates monorhis was recorded in

relatively large numbers during the study, particularly in September

and October, when they were seen moving north (Table 1). This was

in contrast to earlier reports which considered the species to be a

Table 1. Species and numbers of seabirds observed each month during surveys at the two study sites, Beruwala (B) and Mirissa (M), September

2008 to April 2009.

60

L. D. PERERA & A. D. ILANGAKOON

summer straggler to Sri Lankan coastal waters (Warakagoda 1994,

Wijesinghe 1994). Opportunistic observations by the authors of 93

Swinhoe’s Storm Petrels oft Mirissa during two days in October

2009 suggest that the species is a more common migrant in Sri

Lanka than previously thought. Onley & Schofield (2007) mention

that it migrates westward from breeding grounds in Japan to the

northern Indian Ocean, although the precise route was unknown.

More recent work in the Singapore Strait suggests that this is a key

migratory route (Poole et al. 2014). The recording of substantial

numbers in this part of the Indian Ocean during the present study

is the first indication that Sri Lanka lies on the species’s migration

route and sheds more light on its movements.

A total of 21 Wilson’s Storm Petrels Oceanites oceanicus was

recorded (Table 1). This species is known to visit Sri Lankan waters;

earlier work off the west coast found much higher numbers during

the south-west monsoon between May and September (Warakagoda

1994, Ilangakoon 2001).

Other Procellariiformes recorded in the present study included

distant views ot two individual Bulweria petrels in September and

October, not identified to species level. However, both Jouanin’s

Petrel Bulweriafallax and Bulwer’s Petrel B. buliuerii have previously

been recorded off Sri Lanka (Karunaratne 1994, Ilangakoon 2001).

The study period was largely outside the south-west monsoon, which

draws to an end in September, when the diversity (De Silva 1997)

and numbers of interesting pelagic species are found to be high

(Ilangakoon 2001).

Two Stercorariidae were recorded — a single South Polar Skua

Catharacta maccormicki at Beruwala in November and a single

Pomarine Skua Stercorarius pomarinus at Mirissa in April.

Full details of the species recorded, numbers seen and dates of

surveys are given in Table 1 and Figure 2. The highest number of

species recorded in a month was seven at both sites — Beruwala in

October and Mirissa in all months except November and January.

The total number of birds observed peaked in January at Beruwala

and February at Mirissa (Figure 2). Mirissa had higher species

richness during the survey period, with 15 species recorded, while

Beruwala had 1 1 . Mirissa also had a slightly higher overall count of

2,658 birds, compared with 2,292 from Beruwala. The reason for

the differences may be due to both the continental shelf and deeper

pelagic waters being covered at Mirissa. However, the differences

are quite small and the survey was carried out over only one year,

so it is not possible to draw any firm conclusions.

Figure 2. Species diversity and relative abundance.

CONCLUSION

Despite not covering the south-west monsoon period (May-

September), our survey added a new species to the list of seabirds

recorded for Sri Lanka, increasing the total to 49 (Warakagoda et al.

2013). Opportunistic observations during the south-west monsoon

on earlier cetacean surveys and tourism-related seabird trips have

added several species to the Sri Lankan list (Ilangakoon 2001,

Pepper & Hettige 2008), indicating higher pelagic bird diversity

during the south-west monsoon. All accepted records of new species

during the last decade have been recorded either during pelagic

birdwatching trips (Pepper & Hettige 2008) or opportunistically

during cetacean surveys (Karunaratne 1994, Ilangakoon 2001); four

new species have thus been added to the Sri Lankan avifauna. We

therefore conclude that joint seabird and cetacean surveys are both

useful and feasible, as seen from the success of the present study.

However, we suggest that future surveys should include the south¬

west monsoon period, although sea conditions would probably be

less than ideal, as this period is important for seabirds and cetaceans,

including some of the more unusual cetacean species in Sri Lanka’s

waters (Ilangakoon 2008).

This survey, the first joint seabird and cetacean survey

undertaken off Sri Lanka, has shown without doubt that

surveys of this nature can maximise benefits for researchers of

both taunal groups, and may be a cost-effective model for

developing countries. As methodologies can be standardised for

both faunal groups, maximum benefit may be derived from scarce

resources. Therefore, we conclude that this methodology can be

replicated in other areas and even include other marine faunal

groups which may be used as indicator species to determine the

health of the oceans.

ACKNOWLEDGEMENTS

We thank the Ocean Park Conservation Foundation HongKongfor funding

this project. We thank members of our research team, Uditha Hettige,

Chinthakade Silva and Ramanijayewardene, for helping with data collection

and Deepal Warakagoda for comments on the draft manuscript and for

providing reference material.

REFERENCES

Ailing, A. (1986) Records of odontocetes in the Northern Indian Ocean

(1981-1982) and off the coast of Sri Lanka (1982-1984).!. Bombay Nat.

Hist. Soc. 83(2): 376-394.

De Silva, R. I. (1997) Watching seabirds on the west coast of Sri Lanka: 1.

Oriental Bird Club Bull. 26: 42-45.

De Silva, R. I. (2003) Mass migration of Bridled Tern ( Sterna anaethetus ) off

the coast of Sri Lanka. Loris 23: 25-31.

Harrison, P. (1985) Seabirds. London: Christopher Helm.

Hettige, U. (2008) Ceylon Bird Club Notes, November 2008.

Ilangakoon, A. (2001) Observing seabirds off the west coast of Sri Lanka.

Loris 22(5): 15-18.

Ilangakoon, A. D. (2005) Research and conservation of marine mammals

in relation to the Bar Reef Marine Sanctuary North-Western Sri Lanka.

Project completion report, Coastal Resources Management Project of

the Coast Conservation Department, Ministry of Fisheries and Ocean

Resources Sri Lanka and Asian Development Bank.

Ilangakoon, A. D. (2006) Cetacean occurrence and distribution around the

Bar Reef Marine Sanctuary, North-west Sri Lanka. J. Nat. Sci. Found.

34(3): 149-154.

Ilangakoon, A. D. (2008) Cetacean species richness and relative abundance

around the Bar Reef Marine Sanctuary, Sri Lanka. J. Bombay Nat. Hist.

Soc. 105: 274-278.

Forktail 32 (2016)

Results of the first systematic boat-based seabird survey in Sri Lanka

61

llangakoon, A. D. (2009) Cetacean survey off southern Sri Lanka, 2008-

2009. Project completion report. Whale and Dolphin Conservation

Society.

llangakoon, A. D., Ratnasooriya, W. D. & Miththapala, S. (2000) Species

diyersity, seasonal variation and capture method of small cetaceans

on the west coast of Sri Lanka. Vidyodaya J. Sci. 9: 37-52.

Karunaratne, L. (1994) Ceylon Bird Club Notes 77-82.

Lamsfuss, G. (2000) Potential new migrant visitors to Sri Lanka. Ceylon Bird

Club Notes, July 2000.

Leatherwood, S. & Reeves, R. R. (1989) Marine mammal research and

conservation in Sri Lanka 1985-1986. UNEP Marine Mammal Technical

Report No. 1. United Nations Environment Programme, Kenya.

On ley, D. & Schofield, P. (2007) Albatrosses, petrels and shearwaters of the

world. London: Christopher Helm.

Pepper, T. & Hettige, U. (2008) A first record of Black-bellied Storm-petrel

Fregetta tropica in Sri Lankan waters. BirdingASIA 10: 92.

Perera, L. (2003) Ceylon Bird Club Notes 127.

Poole, C. M., Davison, G. W. H.& Rajathurai, S. (2014) Marine surveys to study

the movement of seabirds through the Singapore Strait 2010-2013.

Forktail 30:5-9.

Rasmussen, P. C. & Anderton, J. C. (201 2) Birds of South Asia: the Ripley guide.

Second edition. Washington DC, Michigan & Barcelona: Smithsonian

Institution, Michigan State University & Lynx Edicions.

Robertson, A. L. H. (1994) Occurrence of some pelagic seabirds

( Procellariiformes ) in waters off the Indian subcontinent. Forktail 10:

129-140.

Strindberg, S. & Buck land, S.T. (2004) Zigzag survey designs in line transect

sampling. J. Agric. Biol. Envir. S. 9: 443.

Tasker, M. L., Jones, P. H., Dixon, T. & Blake, B. F. (1984) Counting seabirds at

sea from ships: a review of methods employed and a suggestion for a

standardized approach. Auk 101: 567-577.

Warakagoda, D. (1994) Annotated checklist of the seabirds of Sri Lanka

(revised and updated). Ceylon Bird Club Notes 39-54.

Warakagoda, D. H. & Sirivardana, U. (2011) The avifauna of Sri Lanka: an

overview of the current status. Taprobanica 1: 28-35.

Warakagoda, D., Inskipp, C., Inskipp, T. & Grimmett, R. (2013) Birds of Sri

Lanka. London: Christopher Helm.

Wijesinghe, D. P. (1994) Checklist of the birds of Sri Lanka. Colombo: Ceylon

Bird Club.

L. D. PERERA, Bird oriel Wildlife Team, 401/2 Morogahoheno

Rood, Pitipano South, Homagoma, Sri Lonko. Email:

lesterseyx@gmail.com

A. D. ILANGAKOON, 215 Grandburg Place, Maharagama, Sri

Lanka. Email: ai.flukes@gmail.com

FORKTAIL 32 (201 6): 62-65

Status of the Critically Endangered Yellow-crested

Cockatoo Cacatua sulphured djampeana in the

Tanahjampea islands, Flores Sea, Indonesia

HANOM BASHARI & THOMAS ARNDT

Information about the presence and status of the Yellow-crested Cockatoo Cacatua sulphurea djampeana in the Tanahjampea islands has

been lacking for 22 years. During our six-day visit in September 2015 we observed 14 cockatoos on Tanahjampea Island and three on Kalao

Island. Although we assume that the two islands still hold the largest population of the species apart from Komodo and Sumba, a clearly

recognisable decrease in forested areas and especially the loss of large potential nesting trees threatens the existence of this endemic

cockatoo subspecies.

INTRODUCTION

Yellow-crested Cockatoo Cacatua sulphurea occurs in Sulawesi and

the Lesser Sundas Islands, as well as extralimitally on Penida Island

lying close to Bali, and Salembu Besar in the Java Sea (White &

Bruce 1986, Coates & Bishop 1997). This species has suffered (and

may still suffer from) an extremely rapid population decline owing

to unsustainable trapping for the cage-bird trade. It is therefore

classified as Critically Endangered (BirdLife International 2016).

Until recently, only four subspecies sulphurea , abbotti, parvula

and citrinocristata were recognised (Forshaw 1989, Rowley 1997).

However, recent analysis has resulted in the reinstatement of

the subspecies occidentalism occurring from Lombok to Alor and

therefore leaving parvula confined to Timor, and djampeana

restricted to the Tanahjampea Islands. A new subspecies

paulandrewi has been described from the Tukangbesi Islands, in

addition to the existing subspecies sulphurea from the Sulawesi

mainland, abbotti on Masalembu Besar and citrinocristata on Sumba

(Collar & Marsden 2014).

The Tanahjampea islands lie in the Flores Sea, the main islands

being Kayuadi, Tanahjampea, Kalao, Bonerate, Karompa-lompa,

Karompa, Kalaotoa and Madu. Tanahjampea (172 km2), the largest

island, lies about 123 km from the north coast of Flores and 154

km south of the Sulawesi mainland.

There are the following Yellow-crested Cockatoo records from

the Tanahjampea islands: Kayuadi (September 1927), Tanahjampea

(December 1895), Kalao (July 1927), Kalaotoa (May 1927) and

Madu (May 1927) (BirdLife International 2001). A two-day visit to

Tanahjampea Island by Dutson on 23-24 September 1993 resulted

in sightings of two Yellow-crested Cockatoos, but he did not find the

species on Kalao, Bonerate, or Kalaotoa (Dutson 1995). Cockatoos

were not observed during birdwatching tours to Tanahjampea Island

in 201 1, 2013 and 2014 (Eaton & Hutchinson 201 1, Lambert 2013,

Eaton & Nelson 2014).

METHODS

We visited Tanahjampea Island on 8-11 September 2015 from the

beach area to the highest part of the island (520 m). We then visited

Kalao Island (about 18 km south-east of Tanahjampea) on 12-13

September 2015, from the beach area to 150 m (the maximum

altitude of Kalao is 320 m).

We began our searches for Yellow-crested Cockatoos by

interviewing local people about their knowledge of, and experiences

with, the species. Several locations were then visited: five on

Tanahjampea and three on Kalao (Table 1). Each encounter with

cockatoos (seen or heard) was recorded, noting the location using

Table 1. Cockatoo observation trail locations on Tanahjampea and

Kalao, September 2015.

GPS, altitude, type of habitat (forest, forest-garden and garden),

number of birds and notes on their activities. The forest was entirely

secondary but for our purposes did not include tree plantations;

forest-gardens were areas where cultivations formed a mosaic

within forest; and gardens were areas dominated by cultivation,

including tree plantations. Observers attempted to ensure there

was no double counting ol the same individual by carelul tracking

of every cockatoo observed.

Encounter rate was calculated by dividing the total number of

individuals (seen or heard) by the total length of the observation

trail. Stretches ot observation trail that passed through gardens

(non-cockatoo habitat) were not included in the trail length.

The trail in the field was plotted using GPS and the trail length

calculated with Google Earth software.

Observations were carried out in the morning (07h00-llh00)

andafternoon (15h00-18h00). Walking speed was l-2km per hour.

Each trail was walked 1-3 times. If cockatoos were recorded on more

than one visit to a trail, the number of individuals judged present

was taken to be the largest number counted on any one visit. Most

trails were walked by HB and TA together, but some were done by

either HB or TA alone, depending on the location of the trail, time,

and the availability of guides.

RESULTS

Encounters

We encountered Yellow-crested Cockatoos on eight occasions, six

on Tanahjampea (14 birds) and twice on Kalao (three birds) (Table

2). The encounters occurred between 50-385 m on Tanahjampea

and 0-120 m on Kalao. With the exception of one encounter on

Kalao, where two cockatoos flew over a new garden, all encounters

were in forest. Encounter locations are mapped in Figure 1.

The total length of observation trail on both islands was

17.84 km: 14.18 km on Tanahjampea and 3.66 km on Kalao.

Forktail 32 (2016) Yellow-crested Cockatoo Cacatua sulphurea djampeana in the Tanahjampea islands, Indonesia

63

Table 2. Location of Yellow-crested Cockatoos Cacatua sulphurea djampeana on Tanahjampea and Kalao, September 2015

120°40'E

121°00'E

G f^enterfed ’^3

.e

TANAHJAMPEA

FLORES SEA

SULAWESI

Makassar El

{SELAYAR

1TANAHJAMPEA

_ , Labuan Bajo . ,

KALAO

Kombamiati

7°15'S -

Figure 1. Yellow-crested Cockatoo Cacatua sulphurea djampeana sighting locations on Tanahjampea and Kalao, September 2015.

The overall encounter rate was 0.95 individual per km: 0.99 on

Tanahjampea and 0.82 on Kalao.

From our observations and images we can confirm that the

subspecies djampeana has a smaller bill than the birds from

Sulawesi and that the ear-coverts are a strong, bright lemon-yellow

as described by Collar & Marsden (2014).

Behaviour

A typical observation of the species’s behaviour was made by HB at

Bandai, Tanahjampea, on 8 September. A cockatoo pair arrived at a

larg t Dracontomelon tree at 17hl5. The birds perched on the highest

branches, sometimes calling, grooming, auto- or allo-smoothing

their wings or just sitting silently (Plate 1). It seems they also used

the tree as a roostingsite. Several times they left the tree but returned

after a short time. Some parts of the tree had natural holes that might

be used by cockatoos as a nest site (Plate 2). Local people said that

sometimes three cockatoos could be seen in the tree.

TA observed similar behaviour at Buhun Sanrang on 10

September during the morning and afternoon at a partly dead

Dracontomelon tree. Up to four cockatoos including a presumed pair

visited the tree several times during the day, although occasionally

they disappeared for longer periods, but always seemed to stay

close by and returned to the tree within an hour. One member of

the pair was clearly chasing its mate, grooming it, and occasionally

examining a hole in one of the dry branches. During these activities

a third bird was chased away by the presumed male of the pair.

From the behaviour of the birds and the condition of the trees,

it seems that these two Dracontomelon were used for roosting and

were potentially also nesting trees. Some holes in the trees (Plate

2) were possible nest-cavities, although we had no direct evidence

that they were occupied during our visit.

Population

Residents of Tanahjampea said that the cockatoos could be easily seen

on cornfields, especially at the end of the rainy season from March

to June. They often came in a large group and up to 15 birds could

‘raid’ a field. However, almost everybody told us that the present

cockatoo population was much reduced compared with 10-15 years

ago, although they did not offer a definite reason for this.

Kalao residents also told us that cockatoos can be fairly easily

seen during the corn season, when they visit gardens. They believed

that at the time of our visit the cockatoos were deep in the forest,

mostly in the north of the island. We saw one bird when we visited

an area of forest in north-east Kalao. Our local guide told us that

the cockatoo population was already significantly smaller than ten

years ago, when groups up to 30 birds visited the cornfields. Today,

generally only 3-5 birds visit the fields.

Habitat

On our two-day visit to Kalao we observed differences in the

condition of the forests on the island. Forest in the eastern and

central parts looked drier and had almost no large trees (diameter

H. BASHARI

64

HANOM BASHARI & THOMAS ARNDT

Forktail 32 (2016)

Plate 1. Yellow-crested Cockatoo Cacatua sulphured djampeana, Tanahjampea, September 2015.

Plate 2. Dracontomelon tree used by Yellow-crested Cckatoo, September

2015.

greater than 50 cm), while that in the west appeared greener and

might be more suitable habitat for cockatoos or other parrots.

DISCUSSION

Population and habitat

We cannot determine the cockatoo’s population on the two islands

with certainty, but we judge that it cannot be larger than 250 birds

combined. Although Kalao has a larger forested area (Figure 1)

we formed the opinion that theTanahjampea population is larger.

Tanahjampea, Kalao and Kalaotoa (Table 3) are the three

islands of the Tanahjampea group with the greatest forest cover.

We did not visit Kalaotoa and were unable to obtain information

whether the species still survives there or not. However, if the

condition of its forest resembles that on Tanahjampea or Kalao,

Kalaotoa might still host a population of the cockatoo.

We rarely found trees with a diameter of more than 50 cm.

In two encounter locations on Tanahjampea, Bandai and Buhun

Sanrang, the cockatoos were seen on single Dracontomelon trees

with a diameter of more than 50 cm. According to local people, this

tree species is not felled when mature because generally it is hollow

and unsatisfactory to use for timber. Tire situation is even more

extreme on Kalao. Almost no tall trees of large diameter survive.

Threats

Whitten et al. (1987) stated that the forests of the small islands

south of Sulawesi had all been converted to agriculture by 1915,

with the exception of small areas of Tanahjampea and Kalaotoa

(Kalao was not mentioned). Although this assessment proves

or appears to have been overly pessimistic, the main threat is

undoubtedly the complete clearance of forest for agriculture.

These cleared areas ( kebun ) are often found up to 300 m. People

make the new kebun by felling all trees and natural vegetation.

This action not only significantly reduces the forest area but also

prevents the growth of potential nest trees for the cockatoos and

increases the danger of erosion in hilly areas (Plate 3). The absence

of large trees on Tanahjampea and Kalao must affect the species’s

Table 3. Land cover analysis for main islands*.

* Analysis by Indah Ristiana based on Land Cover Map (2011) from General Directorate of Forestry

Mapping and Environment Management, Ministry of Environment and Forestry.

H. BASHARI

H. BASHARI

Forktail 32 (2016) Yellow-crested Cockatoo Cacatua sulphured djampeana in the Tanahjampea islands, Indonesia

65

Plate 3. Clearance of forest for a new kebun on Tanahjampea.

breeding success. Nest-tree characteristics of the Sumba Yellow-

crested Cockatoo C. s. citrinocristata are: total height 30-40 m,

bole height 15-25 m and 59-156 cm diameter at breast height

(Djawarai etal. 2014). Unless further deforestation is stopped and

large diameter trees (particularly Dracontomelon) preserved, there

will be no future nesting sites for the cockatoos, and the population

will rapidly die out.

Hunting and trapping are also a threat to the cockatoos,

particularly on Tanahjampea. Several times we, met residents out

hunting with air-rifles, especially targeting birds. They told us they

had no specific target and sometimes hunted for food, but more

often simply for pleasure. They occasionally shot cockatoos, which

of course is a serious threat to the species. There are no reports on

the poaching of cockatoos on Tanahjampea, but residents indicated

to us that this had occurred in the previous 10 years.

Conservation

Fortunately there is currently no trapping of cockatoos for the pet

trade on Tanahjampea and Kalao. Most people on Tanahjampea

are farmers. Land is used intensively for cashew and coconut

plantations and rice. However, much forest is cleared for non-

intensive kebun that produce corn and tubers. Some farmers already

use an irrigation system but others remain heavily dependent on

rainfall. As a continuous water supply is vital to rice cultivation

as well as for human needs, the retention and improvement of the

remaining forest can be encouraged as a social imperative as well

as a conservation requirement for the Yellow-crested Cockatoo.

A critical part of any conservation strategy must be an awareness

campaign to convince resident farmers and hunters to stop killing

and persecuting the cockatoos.

For future conservation of the cockatoo, the main challenge

is to preserve the remaining forest area including known and

potential nest trees, as well as efforts to ensure successf ul breeding.

The use of nest-boxes, particularly on Kalao, should be considered

as a short-term solution. Sumba Cockatoos have attempted to use

nest-boxes in Manupeu Tanadaru forest (Walker etal. 2001) and

in Laiwanggi Wanggameti National Park (S. Ongo verbally).

A more accurate estimation of the population of the cockatoo

and other parrots is needed as a basis for conservation efforts in

the future.

ACKNOWLEDGEMENTS

We are grateful to those who helped during our travel and fieldwork. Fajarwas

very helpful during our stop-over in Selayar. Makmur Sultan and his family

hosted us warmly in Tanahjampea and Pak Kadir kindly received us when

we were on Kalao. Our thanks also go to the heads of Kembangragi village,

Tanahjampea, and Lambego village, Kalao, for permission to undertake

fieldwork, and to our guides, Pak Subaeli on Tanahjampea and Pak Supandi

on Kalao. Many thanks to Nigel Collar for reviewing the first draft and the

other reviewers for their meaningful feedback. A good map and a brief analysis

of forest cover were provided by Indah Ristiana (Burung Indonesia). Many

thanks for Yohanis Djawarai and Simon Ongo for discussions.

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Hanom BASHARI, Indobird Community, Jl. Pangkalan Batu

Nomor80A, Bogor, 16114, Indonesia.

Email: han_bashari@yahoo.com

Thomas ARNDT, Arndt-Verlag e.K., Brueckenfeldstr. 28, 75015

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Email: arndt@arndt-verlag.de

FORKTAIL 32 (201 6): 66-71

Valley-floor censuses of the Critically Endangered Yellow-

crested Cockatoo Cacatua sulphured occidentalis on

Komodo Island, East Nusa Tenggara province, Indonesia,

point to a steep population decline over a six-year period

M. JERI IMANSYAH, DENI PURWANDANA, ACHMAD ARIEFIANDY, Y. JACKSON BENU, TIM S. JESSOP & COLIN R. TRAINOR

The population of the Critically Endangered Yellow-crested Cockatoo Cacatua sulphurea occidentalis in Komodo National Park, Komodo

Island, East Nusa Tenggara province, Indonesia, is thought to be second largest, but has been little studied. In September-October 2005,

we surveyed cockatoos from vantage points overlooking five coastal valleys, each one on three consecutive days, and in September 2006

counted cockatoos in Loh Sebita valley on five consecutive days. Our method reduced the possibility of double-counting birds because on

each day only the single largest count of cockatoos was used. We compared our 2005 and 2006 data with population census counts from the

same valleys using the same method in September-October 2000. We also collated opportunistic counts of the species on Komodo made

between 1996 and 2015 and checked whether temporal trends were apparent between two 10-year periods. Nest and breeding data were

also collected. A total of 137 cockatoos was recorded in 2005 compared with 340 in 2000, with census counts declining by an average of

60%. In Loh Sebita valley the population declined by 41% between 2000 and 2006. A total of 19 active nests was located, with 25 nestlings/

juveniles recorded, mostly in tall and smooth-trunked Sterculia foetida, S. oblongata and Corypha utan trees, which are apparently selected

to reduce nest predation. Vantage point census counts are a suitable method on Komodo because inland topography renders cockatoo

flocks easily detectable from ridges, although greater survey effort is needed to reduce margins of error. The cause(s) of the sharp population

decline remain unclear but trade is the most likely driver, with other factors such as breeding failure possibly involved. Annual population

and habitat monitoring is needed on Komodo to confirm the causes of decline and specific patrolling is needed to monitor nests.

INTRODUCTION

The Critically Endangered Yellow-crested Cockatoo Cacatua

sulphurea is one of the world’s rarest parrots with a global

population estimated to be between 1,500-7,000 individuals. The

main threats are ongoing capture for trade, loss of tropical forest

habitat to selective logging and swidden agriculture, and killing of

birds as agricultural pests (BirdLife International 2016). A major

population crash occurred in the 1970s, when it was trapped in

very large numbers (BirdLife International 2001). Records held

by the Convention on International Trade in Endangered Species

of Wild Flora and Fauna (CITES) show that at least 96,785 birds

were exported from Indonesia between 1981 and 1992 (BirdLife

International 2001). Harris et al. (2015) examined patterns of

international trade in Yellow-crested Cockatoo and found that

market volumes and prices of birds increased rapidly from 1980 to

1992 as the wild population was decimated.

According to Collar 8c Marsden (2014), Yellow-crested

Cockatoo populations on Nusa Penida and Lombok and east

to Alor, including Komodo, are the subspecies occidentalis , with

parvula restricted to Timor. Although occidentalis historically

occurred widely in Nusa Tenggara, its populations on Lombok,

Sumbawa, Flores and Alor have been decimated by captures for

trade (BirdLife International 2001). The single largest population

is believed to persist on Komodo where, during a 17-day survey

between 3 September and 1 October 2000, a total of 366 Yellow-

crested Cockatoos were counted in eight valleys (each surveyed for

2-3 days), and it was estimated that a further 160 were present at

unsurveyed sites, hence a total figure for Komodo of 500 birds; the

highest individual count was 190 in Loh Liang, the largest valley

surveyed (Agista & Rubyanto 2001).

Our study in 2005 focused on the five valleys, Loh Sebita, Loh

Liang, Loh Pinda (named Loh Lawi in Agista & Rubyanto 2001),

Loh Wau and Loh Wenci (Figure 1), where Agista & Rubyanto

(2001) recorded 340 cockatoos — 93% of their total count. We

exclude data from one site (Loh Gebah with 36 birds) included

in population estimates by Agista and Rubyanto (2001) because

these data were collected by Komodo National Park staff in 1995 or

before. The Loh Gebah count data were also mentioned by BirdLife

International (2001) under the incorrect assumption that they were

also collected in late 2000. We here consider Loh Liang as a single

valley site and pool data of Agista & Rubyanto (2001) for the two

sites ‘Poreng’ and ‘Banu Nggulang’ listed for this valley (BirdLife

International 2001). The main objective was to census cockatoos in

valley-floor samples and compare our results with the 2000 baseline.

These results were included in a project report cited by BirdLife

International (2016), but here we provide more detail. Since our

observations, there has been one further brief survey of cockatoos

on Komodo which was restricted to Loh Liang, the largest valley

(Nandika et al. 2012).

We also noted aspects of nest biology, which may be a key

factor limiting population size (Walker et al. 2005), and describe

habitat composition and extent. These studies are vital to assist

the Komodo National Park management to develop conservation

strategies, identify work priorities and implement site management

(Pet & Subijanto 2001). Because Komodo has been one of the

most regularly visited sites in the Lesser Sundas since the 1980s,

we reviewed opportunistic counts of Yellow-crested Cockatoos by

visiting ornithologists and birdwatchers to determine if temporal

trends were apparent.

STUDY AREAS AND METHODS

Komodo Island (8.594°S 119.431°E) is the largest (311 km2) of

the islands making up Komodo National Park, which is dedicated

primarily to the preservation of intact savannah landscapes, the

iconic Komodo Dragon Varanus komodoensis, and a rich and diverse

marine fauna (PHKA 2000). The island has a rugged topography

with small (0.42-6. 24km2), narrow (<4km wide), lowland (below

150 m) coastal valleys, bordered by ancient steep volcanic hills

and ridgelines which rise 200-600 nr above the valley floors. Tire

valleys are generally linear features which run inland more or less

at right angles to the coastline and are bounded by moderately

ACHMAD ARIEFIANDY

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Yellow-crested Cockatoo Cacatua sulphured occidentalis on Komodo Island, Indonesia

67

Plate 1. View over the Loh Liang valley showing closed deciduous forest in the valley through to grassy and palm-dominated savannah on ridges,

March 2006.

steep to steep slopes and ridges. Komodo Island has a tropical dry

climate dominated by the westerly monsoons, with the monsoon

season (December-March) bringing most of the rainfall and the

south-east trade winds bringing mainly dry weather during the

intervening eight months. Annual rainfall (about 800 mm) is lower

than neighbouring Flores (Labuanbajo, 948 mm), Sumbawa or

Sumba (RePPProT 1989). Droughts and occasional flooding occur.

Figure 1. Survey sites (hatched areas) and Yellow-crested Cockatoo

nest sites (black dots) on Komodo Island. 1 Loh Sebita, 2 Loh Liang,

3 Loh Pinda, 4 Loh Wau and 5 Loh Wenci.

Plate 2. Pair of Yellow-crested Cockatoos Cacatua sulphured occidentalis

at nest-hole in Sterculla foetida tree, March 2006.

During the dry season, May-November, there is very little rainfall,

increasing the risk of droughts which usually occur between July

and October, the driest part of the year. They also bring the risk

of wildfires, which have been known to cause damage in the past.

Our 2005 study took place in the five valleys where Agista

& Rubyanto (2001) recorded most cockatoos: Loh Sebita, Loh

Liang, Loh Pinda, Loh Wau and Loh Wenci (Figure 1). Loh Liang,

the largest valley, is a centre of tourism and other human activity,

because it is near Komodo village, the largest settlement in the park;

the park headquarters are located there.

Habitat types and extent

Valley-floor area (below 50 m altitude) and the habitat composition

in each of the five valleys were analysed using LandsatTM images

(1999) by creating polygons in ArcView 3.2 (ESRI). We classified

terrestrial habitats (excluding mangrove which covers only about

100 ha on Komodo) into one of four habitat types, following Monk

etal. (1997). During an earlier study of the Komodo Dragon, habitat

was ground-truthed by categorised types including dominant tree

species and canopy cover at a series of GPS points. These points

were then used as references for satellite image analysis as part of

a supervised classification. A map was made in Arcview including

ACHMAD ARIEFIANDY

68

M.JERI IMANSYAH etal.

Forktail 32 (2016)

sample points of each habitat type. A 1999 Landsat image was

processed using Erdas Imagine to obtain a map with four habitat

types based on ground-truthed reference points. Using Arcview we

analysed the extent (km2) of each habitat type and calculated the

proportion of each habitat type island-wide and in our valley- floor

study areas (Figure 1).

Natural habitat types on Komodo are: (a) savannah — an open

habitat, with less than 15% canopy cover, up to lOmtall (TSAonketal.

1997), dominated by the palm Borassus flabellifer and Zizipbus sp.

with a grassy understorey on hillsides; (b) open deciduous monsoon

forest — a coastal valley community dominated by tropical dry forest

trees such as Tamarindus indica and Sterculia oblongata growing

to 20 m tall with 50-70% canopy closure (Monk et al. 1997); (c)

closed deciduous monsoon forest — a denser monsoon forest that

exists in coastal valleys, characterised by Tamarindus indica and

Ficus sp. trees; and (d) closed evergreen forest — a tall dense tropical

forest, very limited at lower altitudes, found mainly above 500 m

and characterised mostly by bamboo, rattan, Podocarpus neriifolia

and Calophyllum spectabile (AufFenberg 1981).

Population censuses

In the 2000 census Agista & Rubyanto (2001) counted cockatoo

populations in the morning and afternoon on two consecutive

days (four counts) directly from lookout points about 10 m above

canopy height on ridges overlooking each of the valleys. The hilly

topography of Komodo Island allows excellent vantage points

above monsoon forest in valleys to count cockatoos, and the birds’

behaviour of flying between roosting and feeding sites in the forest

means that a high proportion of birds are likely to be detected in

each valley (Agista & Rubyanto 2001). Although it is very likely

that birds move widely between valleys in larger time-frames, the

reasonable assumption behind this survey technique is that numbers

of birds present in valleys over a period of a few weeks are probably

fairly constant and reflect a degree of temporary site-fidelity. We

therefore sought to replicate this technique in our own census five

years later.

The number of Yellow-crested Cockatoo in the valley floors was

estimated using direct censuses (Bibby et al. 2000) from vantage

points, about 50 m above sea level, on ridges overlooking each valley

(Plate 1). The census was carried out between 1 3 September and 15

October 2005 prior to the main breeding season, and at the same

time of year and using the same protocols as Agista & Rubyanto

(2001). Cockatoos were counted each morning (06h00-08h00) for

three consecutive days (three counts), as they flew from roosting sites

to presumed feeding areas elsewhere in the valleys. From 15 to 19

August 2006, Loh Sebita valley was re-surveyed for five consecutive

mornings (06h00-08h00) and afternoons (I6h00-18h00) — ten

surveys in all.

We avoided double-counting by only accepting the size of the

single largest flock seen during the count period or the sum of several

flocks seen very close in time but geographically separated from each

other (about 100-400 m apart). The results therefore represent a

conservative count, with some birds not detected by the survey team

because they either broke into smaller groups or were foraging in

the canopy or were otherwise obscured. To assess the density of

cockatoos in each valley we divided the highest single-day count

in a valley by its area (derived as described above).

Nesting ecology

During March and April 2005, when nestlings were about to fledge

and were more conspicuous in nest holes (Agista & Rubyanto 2001),

we made systematic searches in each valley to locate nest trees.

Several observers (3-6 people) walked consecutive parallel transects

approximately 25 m apart to find potential nest trees. The length

and number of transects in each valley were determined by valley

area and topography. We only surveyed valley floors to an altitude

of 60 m because expert local knowledge indicated that nesting was

confined to lowland valleys. Each valley was searched for between

3-6 days, a total of about 21 days of effective survey (excluding

travel to and from sites). Nests were deemed to be active if there were

young directly observed at the edge of tree-holes, immature birds

on branches in the nest tree, or adults guarding the nesting location

(Plate 2). A total of 28 trees with 37 potentially active nest-holes

were found with each tree having 1-3 holes suitable for cockatoos.

Most were found on the first day, then on the following days

observations were made to confirm whether they were active and

how many young birds were present. To confirm whether potential

nest trees were in active use, repeated observations 15-30 minutes

in length were made at all active nests in a single valley surveyed

in a single day. Follow-up visits to each active nest were repeated

over the following 3-5 day periods in the three valleys where active

nests were found. Effort to document nest activity and the number

of young cockatoos at each active nest tree therefore varied from a

minimum of 45 minutes to a maximum of approximately 2.5 hours.

Of the 37 holes found, 19 were active, each one in a different tree.

To minimise disturbance, trees were not climbed to inspect nests,

with observations being made using binoculars from a distance

about 30 m.

We recorded a suite of geographic and environmental

information for each nest including coordinates using a Garmin

Etrex Vista GPS, altitude (m), broad vegetation type (savannah,

open deciduous monsoon forest, closed deciduous monsoon forest)

and nest tree species. Structural characters of each nest tree were

also recorded: diameter at breast height (dbh), tree height (m), and

nest height (m above ground). Tree and nest height were measured

with a Suunto Clinometer.

Opportunistic cockatoo counts by visitors

We reviewed Yellow-crested Cockatoo counts from ornithological

trip reports, birdwatching tour reports and eBird (eBird 2015) for

the period 1996-2015, with the objective of checking whether

temporal trends were apparent. We took this action because we

believed these secondary data were independent and unbiased.

However, the data were subject to many limitations: the number of

visits has increased since 2005, with possibly three times as many

visits between 2006-2015 as during 1996-2005; the data were

probably mostly obtained from a geographically small part of the

Loh Liang valley/main tourist area, because most tour groups land

there and pick up the necessary guide to accompany them as they

look for Komodo Dragons — the main focus of almost all visits

together with the opportunity to see Yellow-crested Cockatoos. The

duration of many visits was a half-day or less and the habitats visited

as well as the distance inland ventured by the groups was to some

extent determined by how soon the two primary objectives were

found, seen and photographed to the satisfaction of the participants

(B. R. Sykes in litt. 2016). Written observations in several accounts

included statements such as ‘several birds’ and ‘several pairs’ and thus

were evidently subject to interpretation; likewise, one record of ‘as

many as 100 birds’ (BirdLife International 2001) was considered

to be an outlier which would tend to skew any trend.

Statistical analysis

A Wilcoxon rank-sum test was used to examine whether there

were any differences between the median rank of Yellow-crested

Cockatoo census count data from the five valleys in 2005 compared

to the 2000 data. We tested whether there were differences in

Yellow-crested Cockatoo census counts done in the morning

compared to the afternoon at Loh Sebita in 2006 using a Wilcoxon

rank-sum test. For the 2006 data, we graphed the 95% confidence

intervals of each consecutive census count, and also estimated the

number of census counts that would be needed to achieve a low

margin of error (0.5), with 95% confidence using the calculation

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69

Table 1 . Coverage (km2) and % (in brackets) of the main vegetation types of the five valleys most used by Yellow-crested Cockatoo on Komodo Island.

n = (1.96 [confidence limit for standard normal distribution]

x standard deviation of counts/0. 5)".

RESULTS

Characterisation of habitats on Komodo island

Based on the 1999 LandsatTM image, the overall vegetation cover

on Komodo comprised savannah (59.3%), open deciduous monsoon

forest (25.4%), closed deciduous monsoon forest (12.4%), and closed

evergreen forest (2.8%) (Table 1). The satellite imagery showed that

open deciduous monsoon forest and tropical deciduous monsoon

forest typically occur at lower altitudes (below about 50 m) in coastal

valleys. The five valleys selected for survey in 2005 on the basis

they were the locations most used by Yellow-crested Cockatoo in

2000, were dominated by open deciduous monsoon forest (48.6%)

characterised by Tamarindus indica, Sterculia foetida, Corypha

utan and Schleichera oleosa, and savannah (45.4%) characterised

by Borassus flabellifer.

Comparison of population counts

During the 2005 study, a total of 137 Yellow-crested Cockatoos was

recorded from the five valleys, an overall decline of about 60% since

2000 (Table 2). The largest census count was 62 birds in Loh Liang

whilst the lowest was three birds at Loh Pinda (Table 2). The overall

density ofYellow-crested Cockatoo in 2005 was 10.1 per km2 (Table

2) with the highest at Loh Wau (18.6 per kn+ ) and lowest at Loh

Pinda (1.7 per km2). There was a statistically significant difference

in the mean ranks of cockatoos counted in valleys during the two

study periods (Wilcoxon rank-sum test W= 32.5, p <0.05).

In 2006 at Loh Sebita a maximum of 48 cockatoos (mean/min:

31.7/13; 95% confidence interval: 37.3-54.7) were counted in 10

Table 2. Current and Agista & Rubyanto (2001) census counts (highest

counts, mean and range for 2005 data) of the Yellow-crested Cockatoo

in five valleys on Komodo. Density is largest census count for a valley,

divided by its land area.

Table 3. Mean characteristics of Yellow-crested Cockatoo nest trees

found on Komodo in 2005. dbh = diameter at breast height.

censuses. The mean number of birds counted in the afternoon was

less than morning census counts (26.6 vs. 36.6; Wilcoxon rank-

sum test R= 33, p <0.05). Afternoon census counts were also more

variable than morning counts (SD = 17.1 vs. 10.9). To achieve an

acceptably low margin of error at Loh Sebita (0.5 or 5%), with 95%

confidence, i.e. n = (1.96 x 8.8/0.5)2, a total of74 cockatoo census

counts would be needed.

Opportunistic observations

It was difficult to draw firm conclusions from the analysis of visitor

reports from published and unpublished sources. There were very

large variations in the numbers of cockatoos reported throughout

the period. However, there was a significant increase in the number

of sources reporting low counts of only 4-6 birds per visit from

three visits out of seven between 1996-2005 to 15 out of 24 visits

between 2006-2015, although in contrast a typical morning visit in

June 2015 reported 40+ birds, probably the highest opportunistic

total on record during this period (Birdtour Asia 2015). The second

highest count was more than 30 birds in August 2008 and at least

20 birds were seen during eight visits — three in the first decade and

five in the second decade.

As summarised in the methods section, methodology, skill and

objectives of visitors were unknown and uncontrollable variables;

nevertheless there was undoubtedly a decline in the median number

of cockatoos recorded per visit in the period between 2006-2015

compared with 1996-2005.

Nest ecology

In 2005, a minimum of 25 nestlings or recent fledged birds were

observed in the following locations: in Loh Sebita, of seven nests

three held one young, four contained two; in Loh Liang, of 1 1 nests

nine held one young, two contained two; and in Loh Wau, one

nest had one young (Table 3, Figure 1). Nests were more frequently

located in open deciduous monsoon forest (68%) than savannah

(36%) or closed deciduous monsoon forest (5%). Yellow-crested

Cockatoos mainly nested in Sterculia foetida or S. oblongata trees

in Loh Liang valley and Corypha utan in Loh Sebita; they selected

tall trees and nested high in them (Table 3).

DISCUSSION

Our census counts did not record all Yellow-crested Cockatoos

in the five valley floors surveyed on Komodo, but probably

represent a high proportion of the birds using this habitat. These

counts declined by an average of 60%, from a census count of 340

individuals in 2000 to 137 in 2005. At Loh Sebita counts declined

from 82 birds in 2000 to 50 in 2005 and 48 birds in our 2006

survey, a 41% decline. Despite statistical considerations, and the

potential for birds to move between valleys within and between

survey periods, we are confident that the steep decline is real for the

following reasons: (1) the linear valley-floor topography from coast

to inland is well suited to vantage-point surveys, and the small size of

valleys and high detectability of white cockatoos mean that census

counts of a high proportion of birds present in the valley floors

70

M.JERI IMANSYAH etal.

Forktail 32 (2016)

are relatively straightforward; (2) census counts in the four largest

valleys all showed the same negative trend; (3) we recorded the same

number of cockatoos in Loh Wenci, the smallest valley, as Agista &

Rubyanto (2001), which we interpret as a complete or near-complete

census, although they may not have been the same individual birds;

(4) Nandika e/rf/. (2012) used transect methodology in May 2012

and walked three different transects over three consecutive days

in Loh Liang valley, during which they counted a total of 73-86

birds, a decline around 60% since 2000. Agista & Rubyanto (2001)

estimated that the Yellow-crested Cockatoo population on Komodo

in 2000 was 500 birds. A similar extrapolation of our data, including

unsurveyed habitat, yields a total of approximately 181 individual

birds (137 birds plus approximately 44 birds [32%] from unsurveyed

areas in 2005).

All populations of Yellow-crested Cockatoo have been

devastated by captures and trade over the last 40-50 years (BirdLife

International 2016). There is much uncertainty about estimates

of population sizes on most islands (Collar & Marsden 2014)

because of lack of specific surveys and reliance on approximate

data. On many islands within the original range of the Yellow-

crested Cockatoo it would no longer be possible to make systematic

surveys because birds occupy only a small percentage of their

former habitat, and it seems that only on Sumba, Timor-Leste and

perhaps Komodo do populations of more than about 200 birds

remain (BirdLife International 2001, 2016, Collar & Marsden

2014). We acknowledge that the few cockatoo surveys on Komodo

have had methodological limitations, with the 2000 survey based

on four counts and ours on three (and 10) counts, while Nandika

et al. (2012) surveyed birds along single line transects on three

consecutive mornings in Loh Liang, the largest valley. However,

surveying by different observers is unlikely to be a major source of

data variability for such a conspicuous species, and we are confident

that our methods in the five valleys were similar to those of Agista

& Rubyanto (2001).

A number offactors such as nest failure, high rates ofpredation,

and loss of tree holes might be involved in the rapid population

decline of cockatoos, but the major driver is likely to be ongoing

clandestine capture for trade (see, e.g., Eaton et al. 2015). The main

motivation for this is described by Harris et al. (2015): as the wild

population declines the price increases, which maintains or increases

levels of illegal poaching.

There is very little specific information on cockatoo poaching

on Komodo. As stated by BirdLife International (2001): 'parvula

[i occidentals ] survives best on Komodo owing to the protection

afforded by Komodo National Park’. As early as 1993 park guards

reported to ButchartrY^/. (1996) that cockatoo trapping did occur,

but 1 in remote parts of the national park away from the well-guarded

park headquarters’. Indeed a high proportion of cockatoos have been

recorded in Loh Liang valley near park headquarters: 190 birds

(56%) of all cockatoos recorded in 2000 (Agista & Rubyanto 2001)

and 62 birds (45%) in this study. Agista & Rubyanto (2001) noted

that the presence of poachers who illegally hunted Javan Rusa Deer

Rusa timorensis might lead to opportunistic shooting or trapping

of cockatoos. They, like ourselves, had no direct observations of

cockatoo poaching, but were informed that cockatoos sold in

December 1999 at Sindu market, Mataram, Lombok, were sourced

from Nusa Tenggara including Komodo Island. Although rangers

do undertake regular patrols on Komodo and Rinca primarily for

habitat security (Purwandana et al. 2014), specific patrols may be

necessary for cockatoos, particularly around nest sites during the

breeding season.

Our observations of 19 active nests are not substantial

enough to infer whether poor breeding output might be a factor

associated with the decline of cockatoos on Komodo. There are

also no empirical data available on tree-hole availability. Lowland

valleys offer strikingly different habitat compared with savannah

vegetation on ridges and slopes, with the largest trees with greatest

girths present in lowland valleys. Expert opinion indicates that

cockatoos only breed in lowland valleys on Komodo. Tree-holes

develop in old trees, with some estimates in Australian Eucalyptus

that hollow formation begins after trees reach about 100 years old

(Wormington & Lamb 1999). There is no regional information

on the rate at which trees develop hollows, but palms like Borassus

flabellifer probably develop holes much more quickly than tropical

forest trees. Lowland valleys cover just 11.5% of the island (Table

1), which suggests that large and tall trees with suitable tree-holes

could be very limited on the island.

The rapid decline we describe seems unlikely to be caused

primarily by changes in breeding success, particularly in such a long-

lived bird. Recent workers have speculated on the impact of arboreal

juvenile Komodo Dragons, which are known to be a predator

of cockatoos at nest-holes (D. Agista in litt. 2000). Predation by

Komodo Dragons on cockatoos has undoubtedly occurred for

many tens of thousands of years, but conceivably its impact is now

proportionately greater as cockatoo populations have declined while

Komodo Dragon numbers have remained stable (Purwandana et

al. 2014). We found that cockatoos select tall trees with smooth

bark for nesting, thereby presumably reducing access by arboreal

predators such as juvenile Komodo Dragon and Common Palm

Civet Paradoxurus hermaphrodites. In 2000, cockatoos were found

to be nesting in nine dead Borassus flabellifer palms, using the hole

at the top of the tree, and also a Mangrove Apple Sonneratia alba

(Agista & Rubyanto 2001). Straight bark-free palms may also reduce

predation, while mangrove habitat is little used by Komodo Dragons

(Purwandana etal. 2014). Other factors, such as exceptionally high

rainfall during the breeding season, have been shown to affect

breeding success in Yellow-crested Cockatoos on Sumba (Walker et

al. 2005). Use by cockatoos of dead palms with hollows exposed to

rain, direct sun and heat would also tend to reduce breeding success.

Collar & Marsden (2014) provided a brief update on

population sizes of the various subspecies. Apart from the tiny

abbotti population — 18 birds in 2013 (Nandika et al. 2013) — all

populations appear to be in decline with more than 50-70% of

the remaining population of subspecies occidentalis present on

Komodo. However, the situation on the island of Rinca (which

forms part of the Komodo National Park) is worth noting. In

October 2000, Agista & Rubyanto (2001) counted 22 (Kampung

Rinca site: 19-20 October 2000) and 32 cockatoos (Kampung

Kerora site: 17-18 October 2000) during censuses on Rinca,

and estimated that approximately 100 birds might be present. In

July 2014 during a university undergraduate study in Mbeliling,

western Flores, flocks of 69 and 15 birds were observed, and images

of a flock of 40 birds were obtained; the observations were made

only a few km from Rinca Island, and Aziz (2014) considered that

the cockatoos had originated from Rinca and were using nearby

Flores for feeding. This evidence is too anecdotal to interpret, but

it engenders a degree of optimism and suggests that the situation

on Rinca merits further study.

CONCLUSIONS AND RECOMMENDATIONS

We are confident that the Yellow-crested Cockatoo population on

Komodo suffered a steep decline between 2000 and 2005. Ongoing

population monitoring is needed; we are aware that Komodo

National Park staff have done such monitoring but we were unable

to access these data and monitoring apparently stopped in mid-2014

for lack of funding (Muthiah 2015). The vantage-point counts

used here are a suitable survey method, but sample sizes need to be

increased by surveying both morning and afternoon for 3-5 days

in each valley location and, where possible, having two independent

simultaneous counters positioned on ridges/hillsides at least

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71

400 m apart. This would increase the number of- cockatoo counts

to a minimum of 12 (3 days) or up to 20 (3 days), which would tend

to reduce error in count estimates.

Understanding trends in the cockatoo population should be

the highest priority but, if adequate resources were available, more

detailed work to understand factors limiting populations would

also be valuable, including identifying food tree species and their

annual productivity of fruit, seeds, nuts and flowers, as this might

influence cockatoo survival and reproduction. Assessments of

tree-hole availability, mapping and monitoring of active nest sites,

as well as specific ranger patrols near the main nest sites, would be

helpful. Gathering information on cockatoo poaching has been

difficult, but interviews with park rangers and with traders in

regional markets (e.g. Lombok) maybe useful. Komodo is accessible

and offers excellent opportunities for further study of the cockatoo,

and could be made a high priority for research by national university

students and park rangers.

ACKNOWLEDGEMENTS

Thanks to Dimas G. Anggoro, Niken Yangpatra, and Aris Hidayat (Udayana

University, Bali), Dakosta, Tony Bota, Yusup Sahabun, and Yusup Jenata

(Komodo National Park staff) for their help during the fieldwork. Thanks to

the work of Dian Agista and Dedy Rubyanto on Komodo, whose baseline data

provided a stronger context to interpret our data. Thanks to an anonymous

referee for valuable review comments, and to Brian Sykes and Nigel Collar for

important edits, corrections and clarifications. We also wish to thank Peter

Widmann, who reviewed a previous submission of this manuscript. This

study is part of a conservation and research project on the Komodo Dragon

and terrestrial biodiversity in Komodo National Park, and was made possible

thanks to financial support from the Zoological Society of San Diego for

the Millennium Postdoctoral Fellowship (to TSJ). Additional funds were

contributed by the Ammermund Family Fund, the Offield Family Fund, and

the Oriental Bird Club. Approval for research was conducted under a MOU

between the Zoological Society of San Diego and The Nature Conservancy

(Indonesia Program) and the Indonesian Department of Forest Protection

and Nature Conservation (PHKA).

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Email: halmahera@hotmail.com

FORKTAIL 32 (2016): 72-85

The birds of Tubbataha Reefs Natural Park and World

Heritage Site, Palawan province, Philippines, including

accounts of breeding seabird population trends

ARNE E. JENSEN & ANGELIQUE SONGCO

Data on the seabird population of Tubbataha Reefs Natural Park, Palawan province, Philippines, which lies in the Sulu Sea, date back to 1911.

However, regular surveys and monitoring began only in 1997 and have resulted in a wealth of new information. An annotated list of the 106

recorded species is presented and changes in the population of the seven breeding seabird species and the factors that influence such changes

are discussed. From an estimated 13,500 breeding seabirds in 1981, the population decreased to less than a third of that number in 2003, with

the only Philippine population of Masked Booby Sula dactylatra being extirpated in 1995. Thanks to strict enforcement of a no-visitor policy

from 1997, the population increased to around 32,300 birds in 201 3. The park is the only known breeding area of the subspecies worcesteri of

Black Noddy Anous minutus. It hosts the largest breeding colonies of Brown Booby Sula leucogaster, Greater Crested Tern Thalasseus bergii

and Brown Noddy A. stolidus, and the second-largest populations of Red-footed Booby Sula sula and Sooty Tern Onychoprion fuscatus, in the

Philippine archipelago. Data on other breeding sites of these species in the archipelago are included. Two new species for the Philippines, 14

new species for Palawan province and four globally threatened species, including the Critically Endangered Christmas Frigatebird Fregata

andrewsi, together with first Philippine records of Yellow Wagtail Motacilla flava tschutschensis and M. f. macronyx are described. Since 1981

there has been a reduction in land area of over 40%, but the previously barren islets are now vegetated and this has encouraged expansion

of tree-nesting Red-footed Booby and Black Noddy colonies to the detriment of Brown Booby. Temperature anomalies caused by El Nino

and La Nina events appear to affect the breeding cycle of seabirds.

INTRODUCTION

The uninhabited Tubbataha Reefs Natural Park lies in the Sulu

Sea, 170 km south-east of Puerto Princesa City, Palawan province,

Philippines. The area was designated a protected national marine

park in 1988 and as a natural marine park in 2006. The protected

area was expanded to include the Jessie Beazley Reef in 2010. It was

declared a UNESCO World Heritage Site in 1993 and in 1999 was

included in the Ramsar list ofWetlands of International Importance

(Ramsar 2016, UNESCO 2016).

There have been few studies of birds in the Sulu Sea and

published data on the avifauna of the atolls and islets are largely

based on the collection of specimen or sight records from a century

ago. Early collectors included Richard McGregor in January 1903

and Dean Worcester, who visited the Tubbataha Reefs in June 191 1

and provided the first description of its seabird colony (McGregor

1904, Worcester 1911). No further ornithological surveys were

undertaken in this area until a survey by the Haribon Foundation

for Conservation of Natural Resources in 1981 (Kennedy 1982).

More recent studies have included surveys of the population of

Brown Booby Sula leucogaster (NRMC 1983, Cruz & White

1989, Arquiza & White 1999) and full surveys of the breeding

bird population in 1991, 1993 and 1995 (Heegaard& Jensen 1992,

Magsalay & Toledo 1993, Manamtam 1996). Between 1997 and

2004, WWF-Philippines made several inventories of the seabird

populations (Sabater 2002, Sabater in lift. 2004). From 2004 until

the present day the Tubbataha Reefs Natural Park management

office has carried out regular monitoring and made quarterly

inventories of the seabirds. Comprehensive surveys, assisted by

independent expert ornithologists, have mainly taken place in May

each year (Jensen 2004a, 2005, 2006, 2009, 2010, 2011, 2012, 2013)

and are ongoing; this study covers the period up to the end of 2013.

Effective conservation management involving the restriction of

access and use of resources from the park started only in 1997. Prior

to that, between the early 1960s and early 1990s, local fishermen

from the Cagayancillo islands, Palawan, stayed for up to a month

on the islets to fish and collect sea-turtles, seabirds, and their eggs,

mainly between April and July. By the early 1980s, increasing use

of motorboats had brought larger numbers of fishermen from other

provinces and other countries, together with the introduction

of cyanide and dynamite fishing techniques. Commercial scuba

diving started in 1979 and within a few years the remote reefs were

transformed into a priority destination for local and international

scuba divers (Arquiza & White 1999, Songco 2003, Dygico 2006).

Today the dive season is restricted to three months (mid-March to

mid-June), whilst permits and entrance fees provide the necessary

funds to manage and patrol the park.

STUDY AREA

The 97,000 ha Tubbataha Reefs Natural Park, lying between

8.761°N 119.844°E and 9.052°N 119.817°E, includes the North

and South Atolls and the Jessie Beazley Reef (Figure 1). The total

exposed area of these formations at high tide is about 14,000 m2.

Bird Islet, previously known as North Islet (Plate 1), located

in the North Atoll (8.931°N 119.997°E), had a circumference of

Figure 1. Location of Tubbataha Reefs Natural Park, Sulu Sea. Source:

Arquiza & White (1999).

TER1 AQUINO TERI AQUINO

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

73

Plate 1. Aerial photograph of Bird Islet (formerly named North Islet),

25 April 2012.

Plate 2. Aerial photograph of South Islet, 5 September 2005.

548 m measured along the vegetation line and average high-tide

mark, with a land area of 10,936 m2 in 2013 (Jensen 2013). The

dominant natural vegetation is beach-forest, although about 65%

of the islet is an open barren area with an influx of grasses. This

area, known as the Plaza, is the historical breeding site of ground¬

nesting seabirds.

The circumference of the tiny South Islet, area 2,860 m , in the

South Atoll (8.749°N 119.820°E) is 230 m (Jensen 2013). It was

originally part of a large sandbar but a lighthouse, protected by a

concrete seawall, was constructed in 1978 (Plate 2). Construction of

the seawall led to the growth of beach-forest vegetation, including

about 100 trees, several of them now up to about 9 m tall.

Jessie Beazley Reef (9.052°N 119.817°E) is submerged at high

tide. At average tides, the exposed area — coral pebbles without

vegetation — is about 350 m2. Birds have also been recorded on Amos

Rock, North Atoll (8.850°N 119.900°E) and Black Rock, South

Atoll (8.804°N 119.845°E); both are large coralline boulder and

sand deposits, exposed at low tide. A large bare sandbar at North

Atoll, where the park ranger station is located (8.851°N 1 19.917°E),

also hosts congregations of birds.

METHODS

The Tubbataha Reefs Natural Park management authority

has established a monitoring protocol for seabirds. In 2004,

comprehensive training of park rangers and staff from the

Tubbataha Management Office was undertaken, focused on

identification, monitoring and survey techniques of Breeding

seabirds, based on Bibby et al. (2000). Since then, quarterly direct

counts of the breeding seabird populations, supplemented by regular

distance population monitoring, have become a routine part of

the park rangers’ activities. Annual supervision and identification

of other bird species is carried out by an independent visiting

ornithologist. The supervisory function, mainly carried out in early

May, includes a review of the rangers’ monitoring data and an in-

depth inventory focused on the breeding seabird populations. The

overall seabird population is determined by a combination of direct

counts of adults, immature and juvenile birds, and square counts of

ground-nesting species including nests, eggs, pulli and juveniles. In

addition, in-flight counts, mainly of boobies and frigatebirds, are

made between I6h30and 18h30 (dusk), when most birds congregate

and start roosting. Equipment used includes binoculars, spotting-

scopes, GPS and digital camera.

Distance population monitoring is normally carried out in the

morning on a monthly basis from a boat cruising 50-70 m parallel

to the shoreline, at both Bird and South Islets, and includes two

or three independent estimated counts of all visible seabirds. The

averaged results are used to determine the population variation

trends throughout the year. A total of 91 distance population counts

were carried out between April 2004 and May 2013.

Of the 66 inventories made on behalf of various organisations

between 1981 and November 2013, 13 were between January and

March, 31 from April to June, 9 from July to September and 13

from October to December. Most survey effort (69%) was put in

between 2005 and 2013 and in this period the inventories were made

between 13 April and 10 June, mostly from 5 to 10 May.

All datasets from 1981 ro 2013 were used in the analysis of

seabird population trends, and the dataset from June 1981 (Kennedy

1982), taken in late afternoon when most of the populations were

present, was used as the baseline to determine population trends.

The aggregate counts of populations present on the islets during

the day and the birds returning in the late afternoon were used to

determine the total breeding population of Red-footed Booby Sula

sula and Brown Booby. Data from the evening in-flight counts of

returning Red-footed and Brown Booby were averaged for the period

2004 to 2013; for Red-footed Booby, 59.3% of the adult population

was away during the day, and 37.3% for Brown Booby. Appropriate

adjustments were made to daytime counts made prior to 2004

(Magsalay 1993, Manamtam 1996, Sabater 2002, in litt. 2004) to

facilitate the evaluation of changes to the two species’s populations.

Analysis of the in-flight averages using ANOVA (two-factor without

replication) revealed that the difference between years was not

statistically significant (p = 0.024281) within species and age groups.

Thus, extrapolation ofin-flight percentages from 2004 to 2013 to the

daytime data of earlier years when no in-flight counts were made was

done without compromising the integrity of the datasets.

The results of the seabird inventories collected during the main

breeding season from April to June were compared with the datasets

from other months to estimate the total annual seabird populations.

In addition to the counts of seabirds, changes in their habitat use

were monitored, with habitat changes being analysed from data

collected on the number and status of bushes and trees. From 2004

land areas have been calculated at high tide each year using GPS

measurements and changes recorded.

RESULTS

A total of 106 species has been recorded from the Tubbataha Reefs

Natural Park, of which 1 1 species breed or are known to have bred,

35 species are Philippine residents or species with both resident and

migratory status, and 60 species are migratory. A complete annotated

list of the birds recorded in the park is given in Appendix 1.

Accounts of the breeding species, and other species of particular

interest, are given below; land area and habitat changes observed

during the survey period and the consequences for the avian species

of the park are reviewed in the discussion section.

Selected species accounts

Species marked t are new records for the Philippines and species

marked * are not listed for Palawan province by Dickinson et al.

(1991) or Kennedy et al. (2000).

Nvrri/\iT

74

ARNE E. JENSEN & ANGELIQUE SONGCO

Forktail 32 (2016)

Breeding species

The following 1 1 species are known to breed or to have bred in the

Tubbataha Reefs Natural Park.

* Barred Rail Hypotaenidia torquata

First records 5 and 6 May 2003, two adults on both Bird Islet and

South Islet. It is believed to breed regularly on Bird Islet, a pair with

a nest containing five eggs was found there on 30 July 2005; also

seen there in 2013.

Green-backed Heron Butorides striata

First record 6 May 2004, bred irregularly on Bird Islet and South

Islet in 2004, 2006, 2007, 2012 and 2013. Evidence of breeding

was found on South Islet, 7 May 2007, when a pair was recorded

at a nest (Jensen 2007).

Pacific Reef Egret Egretta sacra

First record 24 October 1991, 40 birds (Heegaard & Jensen 1992).

Typically 7 pairs breed annually, on both Bird and South Islets; nests

hold up to five eggs. Of 108 observations, 92 were dark morph birds.

Outside the breeding season inter-island movements may occur (e.g.

40 birds present in October 1991, 39 in October 2006).

Masked Booby Sula dactylatra

Tubbataha Reefs formerly held the only known Philippine breeding

population of this species (Dickinson et al. 1991, Kennedy et al.

2000). Worcester (191 1) discovered a large colony on Bird Islet on 29

Plate 3. The last Masked Booby Sula dactylatra at Bird Islet, May 1995.

June 1911, whilst in June 1981 Kennedy (1982) estimated 150 adults

were present. Anthropogenic pressures, including egg and fledgling

collection, caused a terminal population decline (Arquiza & White

1999, Songco 2003). In April 1989 a minimum of 30 adults were

recorded (Arquiza & White 1999), whereas on 26 October 1991

only 5 adults and 1 immature were present (Heegaard & Jensen

1992) and as late as April 1993 two fledglings were confiscated

from a fishing boat (Palaganas & Perez 1993). The last park record

(Plate 3) was of one adult on 23 June 1995 (A. Manamtam pers.

comm. 1996). The species is now extirpated from the Philippines;

the last known record was an immature at sea off Camiguin Island,

Cagayan, Luzon, September 2002 (I. Sarenas in litt. 2004).

Red-footed Booby Sula sula

The first record for the park, involving eight non-breeding adults,

was from South Islet on 15 June 1981 (Kennedy 1982) and this

was followed by the first record from Bird Islet on 25 October

1991 (Heegaard & Jensen 1992). There were no further records on

either islet until 2000 when two adults were recorded on Bird Islet,

followed by 44 in 2001 and 43 in 2002, when three pairs nested for

the first time. A breeding colony was established on Bird Islet in

April 2004, when there was a huge influx of 2,435 adults, and 931

nests were counted. The following year 4,083 adults and 913 nests

were counted; numbers then remained in the range 2,500-2,900

until October 2009 when they peaked at 7,047. The birds nested

in all the available suitable trees and vegetation, sometimes near

ground-level but, since the start of colonisation, all mature trees

used by the species have died due to loss of foliage — used for nest¬

building — and the effect of the birds’ faeces. Colonisation of South

Islet did not start until October 2009 (Heegaard & Jensen 1992,

Manamtam 1996, Sabater 2002, Jensen 2004a, 2005, 2007, 2009);

in May 2010, 90 adults with six nests were counted, whilst in May

2013, 593 adults with 279 nests were counted (Jensen 2013)

Data collected by park rangers between 2004 and 2013

confirmed that the species breeds throughout the year (Table 1,

Figure 2), although more nests are found between October and

December than earlier in the year, e.g. 931 nests in November

2004 and 1,125 nests in October 2009. The largest numbers of

pulli recorded were 472 in October 2008 and 482 in August

2011. In November 2013, 2,975 adults were counted on Bird

Islet, with 494 nests. Data from other colonies indicate that the

incubation period is about 45 days and time to fledging 100-140

days (Carboneras^r^/. 2016); birds generally breed once annually,

although seasons may be missed, particularly during El Nino years.

The total annual breeding population is estimated to lie between

7,000 and 7,500 adults.

Table 1. Red-footed Booby 1981-2013. Maximum counts of adults and nests per year.

3.000

7,000

6.000

5.000

4.000

3.000

2.000

1.000

0

2001 2002 2003 2004 2005 2006 2007 2003 2009 2010 2011 2012 2013

Figure 2. Red-footed Booby population

changes and nesting records 2000-2013.

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

75

Other Philippine breeding sites: the species is known to breed

at three other sites: Cawili Island, Cagayancillo, Palawan (9.482°N

121.036°E), 448 adults (19 nests), 6 May 2007; Bancoran Island,

Mapun (formerly Cagayan de Tawi-Tawi), Tawi-Tawi (7.958°N

1 18.666°E), 4,576 adults (314 nests), 16 May 2007; and Bancauan

Reef, Mapun, Tawi-Tawi (7.763°N 1 18.525°E), 8,206 adults (2,085

nests), 18 May 2007 (Jensen 2007).

Brown Booby Sula ieucogaster

The first record was from Bird Islet on 29 June 191 1, when Worcester

(1911) recorded an ‘enormous’ population there and noted that

the species ‘covered’ South Islet. He also found ‘numerous’ nesting

pairs on Black Rock — the sandbars around this rock have since

disappeared and the area is submerged at high tide (Kennedy 1982,

Heegaard & Jensen 1992). The only subsequent breeding record on

South Islet (16 adults) was in June 1981 (Kennedy 1982). From a

count of 3, 768 adults in June 1981 (Kennedy 1982), the population

declined to an estimated 1 ,000 in April 1989 (White & Calumpong

1992), followed by a low of 600 in October 1991 (Heegaard &

Jensen 1992), then rising to 2,060 in March 1995 (Manamtam

1996) and a high count of 2,402 in 1997 before a new low of 527

in March 1999 (Sabater 2002). It again stood at only 577 in 2002

and, although in May 2005 numbers rose to 1,877 (Jensen 2005),

they again fell sharply to around 1,000 between 2Q06 and 2008.

The population gradually increased to a count of 2, 155 in 2013, still

43% lower than in 1981 (Table 2) and today the adult population

is estimated to be 2,200-2,500 adult birds (Figure 3). The species

breeds throughout the year, with the highest counts in November

2011: 588 nests, 167 eggs and 339 pull i, and May 2013: 618 nests,

532 eggs and 28 pulli.

Other Philippine breeding sites: apart from Tubbataha Reefs,

the Philippine breeding population is now restricted to Maender

Reef, Palawan (8.107°N 118.418°E), 16 adults with five nests on

19 May 2007, and Bancauan Reef, Mapun, Tawi-Tawi, six adults

with two nests on 16 May 2007. Information from the Philippine

Navy indicates that it may still breed on Lawak Island, Kalayaan

Islands, Palawan, but only in small numbers (A. Bundgar pers.

comm. 2005, A. Area pers. comm. 2006). It is extirpated from

Bancoran Reef (Jensen 2007) where it had bred in large numbers

(Worcester 191 1) and no is longer found at Didicas Rock, Cagayan,

Luzon (Allen eta/. 2006).

Greater Crested Tern Thalasseus bergii

First recorded in June 1911 by Worcester (1911), who reported

large groups with eggs on Bird Islet. He did not visit South Islet

but instead found the species breeding in large numbers on nearby

Black Rock. In June 1981, when Kennedy counted 1,132 eggs

(corresponding to 2,264 adults), the species bred only on South Islet,

but abandoned the islet as a breeding site during the 1980s when

the main location, a large barren sandbar, gradually submerged.

Breeding on South Islet was recorded again in 1995 and between

2000 and 2003, with 560 adults counted in 2002; since then

Table 2. Brown Booby 1981-2013. Maximum counts of adults and of nests per year.

1981 1989 1991 1992 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Adults 3,768 1,000 600 2,000 893 2,060 2,402 1,716 527 1,045 850 577 623 847 1,877 1,110 1,016 1,059 1,273 1,442 1,846 1,888 2,155

Nests Present Present 299 Present Present 763 367 225 192 215 69 163 139 117 45 250 89 497 453 513 575 507 618

•4.000

3,500

3.000

2.SOO

2,000

1.500

1,000

SOO

O

■ Adults - Nests

1931 1939 1991 1992 1993 1995 1997 199S 1999 2000 2001 2002 2003 2004 2005 2006 2007 2003 2009 2010 2011 2012 2013

Fig ure 3. Brown Booby population and

highest numbers of nests 1981-2013

Table 3. Greater Crested Tern 1981-2013. Maximum counts of adults and eggs per year.

Figure 4. Greater Crested Tern population

and highest numbers of eggs 1981-2013.

76

ARNE E. JENSEN & ANGELIQUE SONGCO

Forktail 32 (2016)

up to 640 adults have been recorded in May counts but, despite

some displaying, there has been no evidence of breeding. In 1981,

Kennedy (1982) found no breeding birds on Bird Islet, although the

species was present there in 1982, 1989, 1991 and 1993 (NRMC

1983, Heegaard & Jensen 1992, Magsalay & Toledo 1993), but

breeding was not recorded until 1995 (Manamtam 1996) or again

until August 2000, when 2,300 adults were present with juveniles

(Sabater 2002). The population has since fluctuated, although it

increased to 9,154 adults with 3,939 eggs in May 2013- The highest

number of pulli (2,540) was recorded in July 2006. Overall, the

population decreased from 2,264 in 1981 (Kennedy 1982) to only

335 in 1995, but recovered to reach 10,500 adults in August 2013

(Table 3, Figure 4).

Greater Crested Terns breed mainly from May to August and

in some years from October to November (2004-2006, 2009). It

is generally absent from the park between December and March.

From October to December the breedingpopulation is smaller, with

a peak count of 2,000 individuals in November 2004. Based on

the peak counts of the two breeding populations, the total annual

population is estimated to be between 12,000-12,500 adults.

Other Philippine breeding sites: breeding was reported from

Maender Reef, Palawan, where numerous groups were noted in

June 1911 (Worcester 1911) but not in June 2002 (Sabater 2002);

however, in May 2007, 210 adults with four nests were seen (Jensen

2007). The species may breed in small numbers at Sinamahan Cay,

Balabac (Matillano etal. 2006), but is now extirpated from Bancuan

Reef, Mapun, Tawi-Tawi, where more than 100 pairs bred in 1985

(Caretaker M. Bantala pers. comm. 2004).

Sooty Tern Onychoprion fuscatus

The first record by Kennedy (1982) was of 35 non-breeding adults on

Bird Islet on 13 June 1981; he subsequently reported 5,000 breeding

adults on South Islet (Kennedy 1982). It disappeared from South

Islet as a breeding species during the 1980s, apparently due to the

loss of suitable breeding habitat, and there is only one subsequent

breeding record from here, 23 adults on 26 May 2002 (Sabater

2002). On Bird Islet it was reported to be present in 1982 (NRMC

1989) and in October 1991 more than 830 pulli, equivalent to about

1 ,660 adults, were noted there (Heegaard & Jensen 1991), whilst in

March 1995, 455 juveniles were counted among adults (Manamtam

1996). In the 1990s and early 2000s the population on Bird Islet

was subject to large fluctuations and the species was largely absent

and did not breed in 1998 and 2003, but it has bred continuously

there since 2004, albeit in small numbers in some years.

There are two subpopulations of Sooty Terns breeding on

Bird Islet: the larger population normally breeds from the end of

February to July, whilst a smaller population (absent in 2004, 2006

and 2012), averaging 2,400 individuals, breeds from September

to November. The species is usually absent from the park from

December to the end of February, except in February 2011 when

1,585 pulli were recorded, indicating that breeding started as early

as December the previous year. When adults return to Tubbataha

Reefs, they continue to be pelagic by day, settling on land at night

for courtship and territorial claims; this continues for 6-7 weeks

before egg-laying starts. Since the counts are made during the hours

of daylight, the numbers of birds from the beginning of the breeding

season may be an under-estimate. The total annual breeding

population in peak years is estimated to be 15,000-16,000 adults.

The highest spring breeding count was 10,866adultswith 5,515 eggs

in May 2010 (Table 4, Figure 5), and the highest autumn breeding

count was 4,331 adults in October 2009. In July 2006, 3,100 pulli

were counted, with 7,920 adults.

Other Philippine breeding sites: the only other breeding site

is Lawak Island, Kalaayan, Palawan (McManus 1994, P. Alino in

litt. 2009), where breeding numbers are thought to be greater than

at Tubbataha Reefs; in 2005 the seasonal egg harvest was 16 large

baskets (A. Bungar pers. comm. 2005).

Brown Noddy Anous stolidus

Tire first record was in June 1911 when Worcester (1911) reported

numerous birds nesting on Bird Islet. In June 1981, 1,100 adults

were counted there by Kennedy (1982), who also found 518 nests on

South Islet. However, in October 1991 Heegaard & Jensen (1992)

found only 25 non-breeding birds on Bird Islet and 65 non-breeders

on South Islet; in 1993 Magsalay & Toledo (1993) found 200 adults

on Bird Islet and 15 on South Islet, whereas in 1996 Manamtam

(1996) found about 600 adults on Bird Islet and 43 on South Islet,

several of them with nests. On Bird Islet, only 37 bred in 2001, 375

in 2002 but none in 2003. However, from 2004 the species bred

annually in increasing numbers, from 216 birds in 2004 to 1,742 in

2011, before declining to 1,163 in 2013. A high count of 573 nests

holding 405 eggs was made in May 2013. The species was absent

from South Islet in 1998, 1999 and 2001 but, with 40 recorded

in 2000 and 450 in 2002 (Sabater 2002), 115 in 2003 and 868 in

2006; in 2013, adults numbered 525.

The population declined from the 2,136 individuals recorded

in June 1981 and, after 30 years of fluctuation, only returned to this

order of magnitude in May 201 1. It was absent in 1998 and 1999 but

present in fluctuating numbers every year since 2000. The species is

present from late April to early November, breeding mainly from

May to August, although more than 300 juveniles were recorded

in late October 2009 (Table 5, Figure 6).

Table 4. Sooty Tern 1981-2013. Maximum spring counts of adults and eggs/pulli per year.

■ Adults a E^ps/Pull. Figure 5. Sooty Tern population and

highest numbers of eggs/pulli 1981-2013.

I

1931

1991 1993

1995 1997 1993 1999 2000 2001

2002 2003 2003 2005 2006 2007 2008 2009 2010 2011 2012

2013

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

77

Other Philippine breeding sites: in the Sulu Sea the species is

restricted to Maender Reef, Palawan, where 90 adults (six pairs with

nests) were recorded on 19 May 2007 (Jensen 2007). Photographic

documentation and interviews with navy personnel indicate that

more than 300 individuals breed on Lawalc Island, Kalayaan Islands,

from February (A. Arcapers. comm. 2006, P. Alino in litt. 2009).

It may breed on Manlanat (Lantao) Island, Jomalig, Quezon (J. C.

T. Gonzalez in litt. 2002).

Black Noddy Anous minutus

The subspecies worcesteri , first found on 24 September 1910 on

Cawili Island, Cagayancillo, Palawan (Worcester 191 1), now breeds

on Tubbataha Reefs. The first record was of 147 adults on South

Islet in June 1981 (Kennedy 1982); birds were also present there but

did not breed in 1993 and 1999. However, it bred on South Islet in

small numbers between 2000 and 2002 and started breeding there

again from October 2005, when 215 adults were counted; numbers

then rose from 3,300 in 2006 to 8,250 in 2013. The species was first

documented on Bird Islet in May 1991 (Palaganas & Perez 1993),

when large numbers were breeding in the lettuce trees and where, in

October 1991, Heegaard &Jensen (1992) counted 1,503 nests with

almost fully-fledged juveniles, equating to about 3,000 breeding

adults. In May 1993 Magsalay & Toledo (1993) recorded a total

of 2, 230 adults, the majority of which were breeding on Bird Islet.

In June 1995 Manamtam (1996) found 3,564 nests on Bird Islet,

containing 713 pulli and 1,070 eggs — equivalent to a population

of7,128 adults. The Bird Islet population then fluctuated between

3,250 and 4,552 in the period 1997-2000 before about 7,000 were

recorded in 2001, although it then collapsed to about 800 in 2004.

In 2005 most of the breeding population were still on Bird Islet

(6,400 adults) but thereafter the Bird Islet breeding population

declined, probably due to loss of habitat — -only about 2,500 adults

were present there in May 201 3. As numbers declined on Bird Islet,

those on South Islet increased correspondingly— 215 in October

2005, 3,300 in 2006 and 8,250 in 2013, when a record number of

10,656 adults were counted in May on both islets (Table 6, Figure 7).

The Black Noddy breeds mainly from late April to August and,

in 1991, 1997, 2008 and 2009, also bred from September to October;

it is normally absent from Tubbahata Reefs between November

and March. The October breeding population is the smaller of the

two, with peak counts of 3,500 individuals in October 1997 and

2,700 individuals in October 2009. Based on peak counts of the

two breeding populations, the total annual population is estimated

to be between 12,000 and 13,000 adults.

Other Philippine breeding sites: the only other known breeding

site is Cawili Island, Cagayancillo (Kennedy etal. 2000). According

to a resident who had lived on the island since 1959, the species

abruptly disappeared in 1987 (W. Dosongpers.comm. 2007).

Eurasian Tree Sparrow Passer montanus

First recorded from Bird Islet on 25 October 1991 (Heegaard &

Jensen 1992); six to eight birds now breed there annually. Recorded

Table 5. Brown Noddy 1981-2013. Maximum counts of adults and nests per year.

1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013

Adults 2,136 90 215 643 175 0 0 500 37 775 115 336 834 1,228 750 860 1,570 1,775 2,042 1,492 1,688

Nests 518 0 0 20 54 0 0 83 11 134 45 115 75 416 56 334 384 655 924 709 771

2,500

2.000

1.500

1.000

500

O

Figure 6. Brown Noddy population and

highest numbers of nests 1981-2013.

Table 6. Black Noddy 1981-2013. Maximum counts of adults and nests per year.

12000

lOOOO

8000

4000

2000

O

1981 1991 1993 1995 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 200S 2009 2010 2011 2012 2013

Figure 7. Black Noddy population and

highest numbers of nests 1981-2013.

78

ARNE E. JENSEN & ANGELIQUE SONGCO

Forktail 32 (2016)

on South Islet since 2010, with up to eight individuals present. The

species also occurs irregularly at the Ranger Station.

Other species of particular interest

* Northern Shoveler Spatula clypeata

One record, from the Ranger Station on 26 October 2006 (WBCP

2006). An uncommon migrant to the Philippines in suitable

habitats (Kennedy etal. 2000).

White-tailed Tropicbird Phaethon lepturus

One record, an adult between North Atoll and Jessie Beazley Reef,

1 May 2006. An apricot tinge on the elongated tail feathers, lower

belly and undertail-coverts, suggested subspecies dorothea , although

fulvus could not be ruled out. The seven Philippine records include

one from Palawan, on 19 June 1995 at Sultana Shoal, Cagayancillo

(Manamtam 1996, WBCP 2008, 2012). The species, widespread

in the Pacific, is considered to be accidental in the Philippines

(Kennedy etal. 2000).

* Buff-banded Rail Hypotaenidia philippertsis

One record from Bird Islet, 14 May 2010, and one other Palawan

record from Coron Island, 16 February 2009 (WBCP 2009). The

species is a locally common resident in other parts of the Philippines

(Kennedy etal. 2000).

t Swinhoe's Storm Petrel Hydrobates monorhis (NT)

The first Philippine record of this Near Threatened species, on 11

May 2013, involved a bird at sea (9. 136°N 1 19.6l4°E), 20 km west-

north-west of Jessie Beazley Reef (Jensen etal. 2015). The species

breeds as close as on small islets offTaiwan and over-winters in the

Indian Ocean (Birdlife International 2015). It is likely that it is

regular although perhaps rare or uncommon in Philippine waters.

* Wedge-tailed Shearwater Ardena pacifiea

First record, one at sea off South Islet, 24 October 1991 (Heegaard

Sc Jensen 1992). There are four subsequent records from the park:

an undated 1995 record (Manamtam 1996); one near Jessie Beazley

Reef, 1 1 May 2005; one injured bird on Bird Islet, 27-29 October

2007; and one over the open sea off North Atoll, 6 May 2008. Other

records from Palawan province include an unpublished record

of one 25 nautical miles off Palawan, 26 June 1980 (Gast 1999),

one off Cagayancillo Island, 6 May 2007, and one near Calusa

Island, Cagayancillo, 8 May 2008 (WBCP 2007, 2008). Although

considered to be an accidental, rare pelagic species (Kennedy et al.

2000), more than 100 records since 2004, e.g. from Cagayan and

Surigao provinces, suggest that, although uncommon, it is a regular

migrant to the Philippines (Allen et al. 2006, WBCP 2010, P.

Bourdin in litt. 2013).

Japanese Night Heron Corsachius goisagi (EN)

One record of this Endangered species from South Islet, 10

May 2005, an adult found dead (Jensen 2005). The following

measurements were taken: bill: 44 mm, tarsus: 66 mm, wing:

267 mm. Rare migrant recorded from north, central and south

Philippines, including Palawan (Kennedy etal. 2000).

* Black-crowned Night Heron Nycticorax nycticorax

One record, an immature bird at the Ranger Station, 15 May 2010.

There is an unpublished record from Santa Lourdes Beach, Puerto

Princesa, Palawan, on 17 May 1980 (Gast 1999), and an immature

bird was on Bancoran Island, Mapun, Tawi-Tawi province, on

19 May 2007 (A. Manamtam in litt. 2007). Although listed as

migratory (Dickinson etal. 1991, Kennedy etal. 2000), since 2003

breeding colonies have been documented, e.g. Baras Bird Sanctuary,

Sultan Kudarat, Mindanao; Paranaque City, Metro Manila; San

Simon and Candaba, Pampanga, Luzon; and the Hundred Islands

National Park, Pangasinan, Luzon (WBCP 2003, 2004, 2007,

2008,2009,2012).

Chinese Egret Egretta eulophotes (VU)

Lirst recorded from Bird Islet on 23 March 1995 (Manamtam 1996).

There were eight subsequent records of up to three birds, between

April 2006 and May 2012. Sixteen individuals were recorded on

Bird Islet, two at the Ranger Station, and one on South Islet. A rare

migrant in the Philippines, recorded in declining numbers, with

most records from the Visayas, central Philippines (Kennedy etal.

2000, DENR-PAWB 2012).

Great Frigatebird Fregata minor

The species is listed for Bird and South Islets of Tubbataha Reefs

by Kennedy etal. (2000) but without further details. There are no

records of the species in Kennedy (1982). A 1995 record is undated

(Manamtam 1996).

Bird Islet: the first dated record was of six adults and one

immature, 5 May 2001 (Sabater 2002). Since then the species has

been recorded throughout the year, with peak counts of 28 adults

and two immature birds on 10 June 2002 and 21 adults and 7

immatures on 8 May 2005. Numbers had fallen to just five adults in

2013, apparently due to the decline and subsequent disappearance

of tall trees used for roosting.

South Islet: not recorded before 2011. On 8 May 2013, 13 adults

and three immature birds were observed. The appearance of the

species here may be associated with kleptoparasitism of the newly

established colony of Red-footed Booby and the presence of tall

trees suitable for night roosts.

The species’s resident status in the Philippines is based on a

historical claimed breeding record Irom Cawili Island, Cagayancillo,

Palawan (Worcester 1911). Worcester did not find nests or eggs

but based his conclusion on the presence of immature birds and

some males with puffed-out scarlet pouches. He wrote, ‘the species

apparently had finished nesting but immature birds were present

in large numbers’, and recommended a visit to Cawili Island ‘in

the season where possibly the frigate birds would be found mating’.

According to Wilfredo Dosong (pers. comm. 2007), a resident of

Cawili Island since 1959, the species had not bred on the island in

his time, although both immature and adult birds were present

throughout the year. At the country’s largest known frigatebird roost,

on Bancauan Island, Mapun, Tawi-Tawi, the senior caretaker claimed

that in around 1985 the species bred from December onwards.

However, despite a search for nests and other evidence of breeding on

17-19 October 2004 and 16 May 2007, no nesting birds or nests were

found (Jensen 2004b, 2007). In the absence of confirmatory data,

it appears more likely that the species is migratory, with the main

distribution in the Sulu Sea. Frigatebirds are biennial breeders —

young birds are dependent on adults for more than a year — hence

the year-round presence of adults at Tubbataha Reefs and elsewhere

in the Sulu Sea should not be taken as indicative of local breeding.

The majority of records on both Cawili and Bancuan Islands are of

immatures (Jensen 2004b, 2007), suggesting that these birds are

present in the Philippines until they reach maturity.

* Christmas Frigatebird Fregata andrewsi (CR)

Only recently confirmed for the Philippines, the species has been

seen only in the Sulu Sea (Jensen & Tan 2010), except for one

record, 22 January 2013, La Mesa Dam, Quezon City, Metro Manila

(Jensen etal. 2015). In the Sulu Sea it has been documented from

five Philippine islets and eight adjacent islands and islets off Sabah,

Malaysia (Jensen 2007). Bancauan Island, Mapun, Tawi-Tawi,

where up to 70 birds, both juveniles and adults, have been observed,

is an important roost site (Jensen 2004b, 2007, Jensen & Tan 2010).

Frigatebirds normally congregate in the greatest numbers just before

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

79

dusk; juvenile Christmas Frigatebirds may consequently have been

overlooked in mixed frigatebird flocks.

First record from Bird Islet, 5 May 2003, an adult female and a

juvenile (Norwin Abes in lift. 2004). There were 29 records between

May 2003 and May 2013: 16 adults (15 females and one male),

ten immatures (3 males and 7 female) and only three juveniles,

estimated to be one to two years old, have been identified (Jensen

& Tan 2010, Jensen 2011, 2012).

Eurasian Curlew Numenius arquata (NT)

One record from Bird Islet, 26 October 1991, comprised four birds

(Heegaard & Jensen 1992). Locally uncommon migrant, recorded

from north, central and south Philippines, including Palawan

(Kennedy etal. 2000).

* Black-tailed Godwit Limosa limosa (NT)

First record of 11 birds on 26 October 1991 (Heegaard & Jensen

1992), then one on 28 October 2006 and one on 7 May 2008 (all

from Bird Islet). A rather rare and local migrant in the north and

central Philippines, there are internationally important roost sites

of this Near Threatened species on Negros Occidental and Cebu

(Kennedy eta/. 2000, DENR-PAWB 2012).

* Bar-tailed Godwit Limosa iapponica

One record of three birds from Bird Islet, 26 October 1991, and one

there, 7 May 2008. According to Kennedy etal. (2000), the species

is an uncommon migrant in the Philippines.

* Red Knot Calidris canutus

One record from Bird Islet, 26 October 1991. According to Kennedy

etal. (2000), the species is an uncommon migrant in the Philippines.

* Sanderling Calidris alba

Three records from Bird Islet, on 29 April 2006, 7 May 2007 and 8

May 2011, and one from South Islet on 30 April 2006. Four other

Palawan records: three birds, Pandan Island, Honda Bay, Puerto

Princesa and one, Sabang Beach, Puerto Princesa, in April 2008

(WBCP 2008); one bird, Manamoc Island, Cuyo Archipelago, 23

April 2010 (WBCP 2010): and one, ArrecefH Island, Honda Bay,

Puerto Princesa, 12 November 2011 (WBCP 2011). The species is

an uncommon migrant to the Philippines (Kennedy etal. 2000).

Grey-tailed Tattler Tringa brevipes (NT)

Eighteen counts, one in October 1991 and 17 between 1999 and

2013, recorded 502 individuals — 412 from Bird Islet and 90 from

South Islet. Fourteen of the counts were made in April-May, one

in March, one in September and two in October. Most sightings

occurred during southwards migration, with a peak count of 237

birds in October 1991. Peak counts during northwards migration

were 43 birds in both March 1991 and May 2004.

The average numbers of birds counted, arranged in 5-year

intervals between 1999 and 2013, shows a declining trend: 21

individuals annually in 1999-2003, 17 annually in 2004-2008,

and just two annually in 2009-2013. The number of birds during

the southward migration dropped from 237 individuals in October

1991 to 65 in September 2000 and just eight in October 2006.

Recent evidence suggests that the global population of the

species declined between 1987 and 2011 and it is currently listed as

Near Threatened, due to an estimated overall decline of 20-29% in

Australia over the last 25 years (van Gils & Wiersma 2014). Numbers

migrating through Japan in autumn have declined by 57% between

1983 and 2007 (Amano etal. 2010).

Ruddy Turnstone Arenaria interpres

The earliest counts are from October 1991 and March 1995. The

species has been recorded in every year from 1997 to 2013, with 25

counts made: two in January, one in March, two in April, 14 in May,

one in August, three in October and two in November. The counts

resulted in a total of 870 birds, of which 691 were recorded on Bird

Islet and 179 on South Islet. Most birds were seen during southward

migration, with a peak count of 174 individuals in October 1991.

The highest count during northward migration was 95 in March

and a winter high count of 47 occurred in January 2006.

The average number of birds counted in April and May, arranged

in 5-year intervals between 1999 and 2013, was 24 individuals

annually for the decade 1999 to 2008. However, the average for

2009 to 2013 was only five birds annually. The number of birds

during the southward migration period dropped from 174 in

October 1991 to 94 in October 2006. Although the data are

limited, they suggest either a change in migration phenology or

that the population over-wintering in and transmigrating through

Tubbataha Reefs is undergoing a decline

* Pomarine Skua Stercorarius pomarinus

One record of a light phase adult passing South Atoll on 10 May

2005. A bird passing North Atoll on 8 May 2009 may have been

this species. Additional records from the Sulu Sea include one at

Manuc Manucan Reef (7.717°N 118.450°E), Mapun, Tawi-Tawi,

21 October 2004 (WBCP 2004); two between Cagayancillo and

Cawili Islands, Cagayancillo, Palawan, 6 May 2007 (WBCP 2007);

and up to 50 off Patikul (6.089°N 121.105°E),Jolo Island, Sulu, 19

December 2012 (WBCP 2012). Although listed as a rare migrant

(Kennedy etal. 2000), records since 2004 confirm that the species

occurs annually in the Philippines (WBCP 2004, 2005, 2008,

2010,2011,2012).

* White-throated Kingfisher Halcyon gularis

One record from South Islet of a single taken by a Peregrine Falcon

Falco peregrinus, 30 April 2006. The species is a fairly common

resident in the Philippines (Kennedy et al. 2000).

* Oriental Skylark Alauda gulgula

One record of a bird passing northwards at the Ranger Station,

8 May 2005. An uncommon resident in the Philippines, but no

information about inter-island movement (Kennedy etal. 2000).

* Clamorous Reed Warbler Acrocephalus stentoreus

One individual was caught in a mist-net on South Islet, 10 May

2005, and released the same day. It is an uncommon resident in

the Philippines, but there is no information about inter-island

movement (Kennedy etal. 2000).

Purple-backed Starling Agropsar sturninus

One record from Bird Islet, 26 October 1991, two birds observed

(Heegaard & Jensen 1992); the second of only three Philippine

records (Jensen et al. 2015).

+ Rosy Starling Pastor roseus

First Philippines record from South Islet, 1 0 May 2009, one adult in

non-breeding plumage. Two subsequent records (Jensen etal. 2015).

Yellow Wagtail Motacilla flava

A male of subspecies macronyx on Bird Islet, 7 May 2005, was the

first record of this taxon from the Philippines (Jensen 2005). It was

identified by its uniform grey crown and ear-coverts, the absence

of a supercilium, green upper back, bright yellow underparts and

distinctive whitish wing-bars. Subspecies macronyx breeds from

Transbaikalia, Amurland and Ussuriland, Far East Russia to

Mongolia, Manchuria and China and winters in South-East Asia

and south-east China (Tyler etal. 2016).

A male tschutschensis Yellow Wagtail recorded on Bird Islet

on 14 May 2010 was the first Philippines record of this taxon, and

ARNE E. JENSEN

80

ARNE E. JENSEN & ANGELIQUE SONGCO

Forktail 32 (2016)

another male was there, 9-10 May 2013 (Jensen 2010, 2013). The

bird showed a pale grey head, blackish ear-coverts and a long white

supercilium. Subspecies tschutschensis breeds from north-east Siberia

to the most easterly parts of north-eastern Russia and western and

northern parts ol Alaska, and winters mainly in South-East Asia

south to most of the Indonesian islands (Tyler et al. 2016).

DISCUSSION

Changes to land area

Bird Islet (formerly known as North Islet) has undergone major

changes since June 1911, when it was a Tow flat sandy island some

400 meters long by 150 wide’ (Worcester 1911); by 1981 it was

described as 268 m long and 70 m wide at high tide (Kennedy 1982).

The area of the islet has decreased from an estimated 60,000 m2 in

1911, to 18,760 m2 in 1981, 17,000 m2 in 2004 and about 10,930

m2 in 2013 (Jensen 2013). After a change of only 9% between

1981 and 2004, the following 10 years to 2013 saw a lurther 35%

reduction — blocks of the sandstone, with surface soil, up to 1 m2 in

area, are now broken off the islet by wave action during high tides or

stormy weather (Plate 4). This severe erosion has seriously damaged

the south and north-west shorelines and reduced the area available

to the ground-nesting boobies (Kennedy 1982, Jensen 2006).

South Islet, in contrast, is relatively stable due to the concrete

seawall constructed in 1978, although an adjacent wide barren

sandbar, which hosted dense tern colonies in 1981 (Kennedy

1982) has disappeared. Other changes in land area include the

disappearance of an unnamed sandy islet at Black Rock on the

South Atoll (Worcester 191 1, Kennedy 1982).

Global sea-levels rose at a mean rate of 1.8 mm per year for the

past century (Douglas 1997, Church & White 2006); however,

between 1993 and 2003 rates have been estimated to be 2.8-3. 1 mm

Plate 4. Bird Islet, 9 May 2013. Erosion has caused a decrease in land

area of more than 40% since 1981.

per year (Bindoff et al. 2007). Since 1990, the number of tropical

cyclones in the west Pacific has increased, although the number of

resulting typhoons making landfall on the Philippines has remained

constant at about 20 per year. However, the typhoon path, intensity

and duration have changed — today more typhoons make landfall

on the central Philippines and also impact the previously relatively

typhoon-free Sulu Sea (Emmanuel 2007). The rise in sea-level,

together with the increased frequency and intensity of storms

crossing the Sulu Sea, appear to be the main factors that are causing

the changes in land area. Changes in sea currents are a contributory

factor, causing major movements of sand deposits, which have led

to the emergence of numerous temporary sand cays in the reef flats

of the atolls, the disappearance of the major sandbars at Black Rock

and around South Islet and, between 2008 and 2010, a substantial

decrease in the area of a major sandbar adjoining Bird Islet (Kennedy

1982, Aquino et al. 201 1, Jensen 2013).

Habitat changes

Both Bird and South Islets have changed progressively from barren

to fully-vegetated habitats, influencing the make-up of breeding bird

species. The vegetation is now predominantly lettuce tree Pisonia alba

and octopus bush Argusia argentea with tropical almond Terminalia

catappa , and a few stands of coconut palm Cocos nucifera. Butter daisy

Melampodium divarication , purslane Portulaca oleracea, purple-top

chloris Chloris inflata and Setagaria geniculata also occur (Kennedy

1982, Palaganas & Perez 1993, Jensen 2007).

In 191 1, Bird Islet was barren, except for a few stands of purslane

(Worcester 191 1), and remained so for the next 70 years (Kennedy

1982). By 1991 dense young beach-forest with more than 100

trees had developed on the north, east and south-east shorelines

(Heegaard & Jensen 1992); bush and tree numbers increased to

about 500 — many up to 9 m tall — by 2004. However, since then

the massive influx of breeding Red-footed Boobies has destroyed

this habitat; by 2013 nearly all mature trees were dead and bushy

vegetation was deteriorating due to the activities of this species

( Jensen 2013). The destruction of vegetative cover by Red-footed

Boobies caused most of the Black Noddies, which had nested

in the lettuce trees since 1991, to move to South Islet (Jensen

2013). On Bird Islet in 1991 there was an 8,000 m2 open grassy

area known as ‘the Plaza’ (Heegaard & Jensen 1992), which was

the historical breeding site of ground-nesting seabirds. By 2002

it had been reduced to only about 1,100 m" by the rapid spread of

introduced tamarind Leucaena leucocephala (White et al. 2004).

In 2007 tamarind was eradicated by the park staff and the Plaza

(Plate 5) has expanded to 4,840 m2 (Jensen 2013). Species which

use trees for night roosts, such as frigatebirds, including the

Critically Endangered Christmas Frigatebird, have benefited from

the increased vegetative cover. Conversely, the increased vegetative

cover that resulted from the building of the seawall on South Islet

when the lighthouse was built in 1978 may have contributed to

the decline and subsequent disappearance of the ground-breeding

Greater Crested Tern and Sooty Tern from that location. South

Islet was largely barren in 1981, apart from a few bushes (Kennedy

1982). In 1991 Heegaard & Jensen (1992) found considerable native

beach-forest vegetation with relatively tall trees with thick foliage,

together with dense bushy vegetation (Plate 6). In 2013 there were

about 130 trees, although since 2011 the condition of nearly half of

them has deteriorated due to the presence of breeding Red-footed

Boobies (Jensen 2013).

Changes in the breeding seabird population

The park is the only known breeding area of the subspecies worcesteri

of the Black Noddy. This taxon formerly bred on Cawili Island until

1987 and may also occur on Ashmore Reef, north-west Australia

(Gochfeld et al. 2016). Within the Philippines it hosts the only

major colony of Brown Booby, the second-largest populations of

ARNE E. JENSEN ARNE E. JENSEN

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

81

A

Plate 5. Bird Islet, May 201 3. The main breeding ground for Brown Booby

Sula leucogaster and Greater Crested Tern Thalasseus bergii at the Plaza.

In the background are dead trees killed by the high breeding density

of Red-footed Booby Sula sula.

Plate 6. South Islet, 8 May 2013. Dense vegetation with breeding Black

Noddy Anous minutus.

Red-footed Booby and SootyTern, and the largest breeding colonies

of Greater Crested Tern and Brown Noddy.

Using the count results from June 1981 (Kennedy 1982) as a

baseline to determine variations and trends over time, it can be

concluded that there have been considerable changes in the seabird

populations of the park. The number of breeding seabird species

declined from seven in 1981 to six by 1995 and the ranking of the

three most abundant species in 1981 — Sooty Tern (5,070), Brown

Booby (3,768) and Greater Crested Tern (2,264) — changed over

the period to 2013 to Black Noddy (10,656), Greater Crested Tern

(10,500) and SootyTern (3,771).

From about 13,540 adults of all species in 1981, the breeding

population decreased to about 5,450 in 1991, a 60% decline. It

increased to more than 11,000 in 1995 before again declining to

only about 4,990 in 1998. Between 1999 and 2002 the average

breeding population increased to 12,460 individuals but in 2003

the population was just 4,320 individuals, less than a third of

Kennedy’s count in 1981. However, since 2004 there has been a

gradual population increase to an all-time high of about 32,300

individuals in 2012 and 2013, 138% higher than the first count of

1981 (Figure 8).

There are significant differences in the population trends

of tree-nesting and ground-nesting seabirds. The population of

ground-nesting species in 2013 was 35% higher than in 1981. This

is due to an increase in the Greater Crested Tern population from

about 2,260 individuals in 1981 to nearly 10,500 in 2013. Other

species had lower populations in 2013 than in 1981: the Brown

Booby population (2,155) is 43% lower and the Brown Noddy

population (1,688) is 21% lower. The Masked Booby population

declined rapidly in the 1970s and by 1981 numbered only 150

adults; it was extirpated from Tubbataha Reefs Natural Park, and

the Philippines, in 1995.

Because of the growth of suitable habitats for the tree-nesting

Black Noddy and Red-footed Booby, these two species have

undergone a remarkable increase: from only 147 Black Noddies

in 1981 to about 10,650 in 2013, and from just six breeding Red¬

footed Boobies in 2002 to about 4,490 in 2012. It is probable that

the Black Noddy population originated from Cawili Island, from

where it disappeared abruptly in 1987 (W. Dosong pers. comm.

2007). A large number of fishermen settled on Cawili Island from

1975 to 1977, increasing the killing of seabirds and converting most

of the beach-forest on the island to agricultural lands (Arquiza &

White 1999), which may explain the species’s disappearance irom

Cawili Island and the corresponding breeding in large numbers on

Tubbataha Reefs (Palaganas & Perez 1993).

There have been considerable fluctuations between some years

in the breeding numbers of Greater Crested Tern, Sooty Tern and

Brown Noddy. There was an apparent absence of these species

in 1998, of Greater Crested and Brown Noddy in 1999, and of

Sooty Tern again in 2003, whilst in some years there are unusually

high breeding numbers of Greater Crested Tern (2005-2006 and

2012-2013) and of Sooty Tern (1999, 2001, 2006, 2010 and 2012).

These population peaks could indicate irregular population trends

which may be associated with sea-surface temperature variations,

as concluded by Devney et al. (2009). They found that population

declines of pelagic seabirds were related to the frequency and

intensity of El Nino anomalies in the western tropical Pacific.

There have been eight moderate to strong El Nino and four La

Nina events since seabird data collection started at Tubbataha Reefs

in 1981 (Null 2014, WMO 2014). The absence of breeding Greater

Crested Terns and Brown Noddies in 1998 to 1999 and of Sooty

Terns in 1998 coincides with the El Nino/La Nina anomalies in

Figures. Breeding seabird population

trends in Tubbataha Reefs Natural

Park 1981-2013.

Total population

— Tree-breeders

Ground-breeders

Linear (Total population}

82

ARNE E. JENSEN & ANGELIQUE SONGCO

Forktail 32 (2016)

1997 to 1999, while an El Nino period in 2002 to 2003 coincided

with the absence of Sooty Terns in 2003.

Devney etal. (2009) showed that El Nino generated sea-surface

temperature anomalies and 'intense El Nino events can severely

impact seabird populations, often months in advance of peak

temperature anomalies’. Recent phenological analysis of seabird

data from Tubbataha Reefs by Carcallas (2013) suggests that the

higher the chlorophyll concentration, which occurred in January

to March, the earlier the Sooty Terns start egg-laying, while the

peak sea-surface temperature was strongly linked to the start of egg-

laying for the Greater Crested Tern. However, the overall increase

in the sea-surface temperature did not negatively influence the adult

seabird population in the park over time.

Factors affecting the seabird population

Negative anthropogenic factors affecting seabirds included the

seasonal collection of eggs and chicks and frequent disturbance

of the breeding colonies by visiting fishermen and scuba divers

up to 1998, when the islets were closed to visitors. Park staff have

documented a growing number of avian casualties caused by marine

debris, which may cause many fatalities through entanglement in

discarded or lost fishing gear and the ingestion of toxic chemicals

from degrading plastics (Pierce et al. 2004, Gregory 2009, Eidt

2012, Lavers & Hutton 2014). In Tubbataha Reefs Natural Park

marine flotsam, particularly plastic, is increasingly used as nesting

material by seabirds. Other factors affecting seabirds include

climate-change related variations in sea-surface temperature,

changes in severity and movement patterns of typhoons, and a rise

in sea-level, causing breeding failure and reducing the area available

to birds for breeding.

Both Worcester (1911) and Kennedy (1981) encountered egg-

collectors during their brief visits. Many fishing crews survived

on fish, birds and their eggs taken from Tubbataha Reefs, while

commercial dive-boat crews were observed with drums full of

seabird eggs (Kennedy 1982, Arquiza & White 1999). The frequency

of disturbance and egg collection by visiting divers and fishermen

intensified during periods of good weather from March to May

and in October. Heegaard & Jensen (1992) found 25 fishing vessels

from Cagayancillo, Cebu and Taiwan anchored around Bird Islet

in October 1991 , with nearly 80 people in and around the breeding

seabird colony, evidently causing disturbance.

The seabird population trends correlate well with the intensity

of anthropogenic pressures. By 1998, when the no-visitor policy was

enforced, the Brown Booby population had declined by over 50%

since the 1981 count by Kennedy (1982) and ‘lag effects’ probably

caused the decline to continue to 85% by 2002; since then there has

been a slow increase, although it is still about 43% lower than in

1981. Today the park’s Bird and South Islets may be the only Sulu

Sea islets which continue to be free of human-introduced predators

and from human disturbance (Jensen 2007).

Bird Islet has an altitude of 1.5-2 m (Kennedy 1982); a

reduction in area, particularly of the lower-lying Brown Booby

breeding area on the Plaza, has caused this species to move its

breeding area onto higher ground. Upper-level projections for

sea-level rise to the end of the twenty-first century are up to 1

m above current levels (Gregory 2013). A rise in sea-level of this

magnitude would reduce the area of the islet from about 11,000 m2

to an estimated 5,000 m“, a major reduction in available breeding

area, probably leading to a reduction in the population of Brown

Booby and ground-nesting tern species.

The population dynamics of the seabirds of the Tubbataha Reefs

is complex, and requires further research: there are no studies of the

reproduction and survival rates of Philippine seabirds; dispersal of

the juvenile and adult populations outside the breeding period is also

unknown; and the impact of marine debris on the park’s seabirds is

yet to be documented. The presence of protected seabird colonies in

Tubbataha Reefs Natural Park provides opportunities for avifaunal

research that could fill gaps in our knowledge and further enhance

the effective conservation and management of seabirds.

ACKNOWLEDGEMENTS

We dedicate this paper to the Tubbataha Reef Natural Park marine rangers

employed by the Philippine Navy, the Philippine Coast Guard, the Tubbataha

Management Office and the Municipality of Cagayancillo, who have been

instrumental in collecting the data presented herein, and to Tim Fisher,

whose untimely passing has left our endangered seabirds with one less zealous

advocate. Special thanks go to Noel Bundal, Segundo Conales and Roy

Magbanua for consistent and untiring data collection. We thank the Tubbataha

Protected Area Management Board and WWF-Philippines for logistical

support for the annual May inventories. We thank Marivel Dygico, Captain

Ronald de Roa and the crew of the WWF research vessel M/Y Navorca for

their participation in the surveys and for safe enjoyable passages to and from

Tubbataha. Special thanks to Teri Aquino, Robert Brinks, Melvin Calderon,

Anton Carag, Cristobal Cayetano, Robert Hutchinson, Godfrey Jakosalem,

Arturo Manamtam, Maia Melacio, Nadia Palomar, Lisa-Marie Paguntalan,

Sylvia and Tonji Ramos and Gregg Yan, who provided valuable volunteer

assistance during the fieldwork from 2004 to 2013. Our sincere appreciation

goes to Teri Aquino for permission to use her images. The draft manuscript was

critically reviewed by David James whose expert comments greatly improved

its accuracy.

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Appendix 1

Annotated list of the birds of Tubbataha Reefs Natural Park

Key: t = new records for the Philippines, * = species not listed for Palawan province by Dickinson etal. (1991) or Kennedy etal. (2000).

Area = location of records in Tubbataha Reefs Natural Park: B = Bird Islet, S = South Islet, RS = Ranger Station, A = Amos Rock, J = Jessie Beazley Reef, P = pelagic.

Status in Philippines, based on Kennedy etal. (2000): M = Migrant, R = Resident.

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No. = total number of birds seen.

Forktail 32 (2016) Birds of Tubbataha Reefs Natural Park and World Heritage Site, Palawan province, Philippines

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86

SHORT NOTES

Forktail 32 (2016)

First nesting record of Philippine Eagle Pithecophaga jefferyi from Luzon,

Philippines, with notes on diet and breeding biology

TATIANA ROSE C. ABANO, DENNIS JOSEPH I. SALVADOR & JAYSON C. IBANEZ

Introduction

The Critically Endangered Philippine Eagle Pithecophaga jefferyi is

one of the world's largest forest eagles and is known to occur only

on the Philippine islands of Luzon, Leyte, Samar and Mindanao

(BirdLife International 2016). Since its discovery (Ogilvie-Grant

1897), most studies pertaining to the biology of the species have

been focused on Mindanao. Exploration of Luzon has led to the

detection of adult eagle pairs and young birds; however, no active

nest has previously been found. Here we report the first discovery

and observation of an active Philippine Eagle nest in 2015 and

record the nest characteristics, prey items and breeding biology of

the eagles on Luzon. We also report details of what we believe was

another Philippine Eagle nest found in 2013.

Fieldwork

We searched for Philippine Eagles and their nests in the northern

Cordillera range of Calanasan, Apayao province, Luzon, during

intermittent expeditions between November 2011 and April 2015.

Our survey sites in the range consisted of predominantly secondary

dipterocarp and montane forests in mountainous terrain from

100 to 1,200 m. We divided the 2,592 km2 study area into a 5 km

x 5 km grid map, and systematically selected survey locations

based on local reports of eagle sightings and appropriate forested

habitat.

Our first success was on 22 March 2013 when we discovered a

large stick nest in the interior of montane forest in the northern

Cordillera range at 1,098 m. After making sure the nest was empty,

we climbed the tree — an almaciga Agathis philippinensis, similar

to some of the trees used by Philippine Eagles for nesting on

Mindanao — using ropes and harnesses. The nest was 1.02 m in

diameter and 0.73 m deep, and we judged that it was too big to

belong to a smaller Philippine raptor; we had already seen the nests

of, for example, North Philippine Hawk Eagle Nisaetus philippensis

in the same mountainous area, but this nest was significantly larger

and we concluded that only Philippine Eagles would build a nest of

this size. We also found evidence that the nest had recently been

in use: twigs on the nest bowl appeared intact and fresh, whilst

foliage and epiphytes surrounding the nest appeared recently torn

and had not yet grown over it.

It appeared that the nest had been deliberately located so that

it was concealed by the epiphytes surrounding it. It is interesting

to note that we had seen a juvenile Philippine Eagle about

3.1 km from this nest-site about a week earlier. However, we have

no evidence linking this bird directly to this nest; although the nest

was empty, we monitored it for a few months but never saw either

juvenile or adult birds return to it.

We surveyed for eagles from vantage points on hilltops and in

the canopy of tail trees. When an eagle was detected, we made a

systematic ground search for potential nest trees using locations

from which they had emerged or where they descended into

the forest canopy. After a series of sightings that included a food

delivery by one of the adult eagles, we found the active nest on 21

April 2015 and observed it from 29 April to 1 September. The nest

was on a densely forested slope of lowland dipterocarp at about

450 m, built at a height of 31 m in the middle canopy of a 2.29 m

dbh Hopea sp. tree. The nest was surrounded by towering pandan

Freycinetia sp. epiphytes (in much the same way as the empty

nest found in 2013) and was substantially concealed by the thick

foliage of an adjacent Rauvolfa sp. tree (Plate 1). It was roughly

circular in shape, 1.54 m in diameter and 0.5 m deep. Based on the

development of nestlings on Mindanao (Kennedy 1977, Ibanez et

al. 2003, Ibanez 2007), we estimated the age of the chickto be over

one month when the nest was found. Hence the egg was probably

laid towards the end of January 2015 and hatched around the end

of March, indicating that the onset of breeding of Philippine Eagles

on Luzon was relatively delayed compared with those on Mindanao.

The 2015 nest site was about 31.45 km north of the disused

nest found in 2013, located within an area protected under the

'Lapat' system, an adaptation of traditional indigenous natural

resources management (Sadao 2010) by local government and

central government offices working together (Local Government

Unit [LGU] Calanasan & Community Environment and Natural

Resources Office [CENRO] Calanasan 2011).

We recorded nest activity at 10 minute intervals, and also

opportunistically recorded rarer events such as practice flights

and other noteworthy behaviour when they occurred outside this

sampling regime. We followed Marti et al. (1987) in computing the

biomass of the food items (quantity x weight) and their percentage

biomass (individual biomass/total biomass x 100). We also computed

the numerical percentage (number/total numberx 100). The weights

of food items were based on the mean specimen weights published

by Kinnaird & O'Brien (2007) and FMNH (2010), plus data provided

by E. Sy and B. Santos (unpubl. data).

Philippine Eagles are sexually dimorphic, with females weighing

nearly a third more than males. Apart from their size difference,

the male and female adults were distinguished from each other

through features peculiar to each bird, such as relative size and

structure of tarsi, the presence of torn and moulted feathers, and

other plumage features.

Nest monitoring results

We monitored eagle activity at the nest and food deliveries to the

nest daily using a 20-56x spotting scope from a canopy observation

hide located about 60 m away. In total, we spent 977 daytime

hours over 92 days up to 1 September monitoring the nest and the

eagles' activities. The main everyday activities (89.8%) of the chick

recorded from the nestling to the pre-fledging stage were related

to general maintenance such as perching, sleeping, preening and

defecating (n = 5,267 individual records). Five percent of activities

involved feeding by the adults and feeding on its own (n = 294).

Other significant activities included vocalising (3.6%, n = 210),

object play consisting of grabbing and biting at sprigs (1.3%, n =

75), and flapping exercises (0.4%, n = 18), all of which became more

frequent as the chick grew; the chick's developmental milestones

are given in Table 1 . On 20 July, about two weeks before the nestling

began practice flights, the opportunity arose to carefully trap it

for examination and to attach a ring and transmitter. Comparison

of its size and weight at that time with nestlings of a similar age

monitored on Mindanao indicated that it was a female.

We documented a total of 59 food items brought to the

nest, consisting of 12 vertebrate species. The two most common

were Northern Luzon Giant Cloud Rat Phloeomys pallidus and

Smooth-scaled Mountain Rat Snake Ptyas luzonensis. The cloud

rats were also the most important food item in terms of biomass

contribution. The rest of the food items were other rat snakes,

monitor lizards, macaques, civets and a flying fox. There were

also portions of unidentified birds that we suspect were Northern

Rufous Hornbills Bucerosfiydrocorax and of unidentified rodents that

were most likely to be Philippine Forest Rats Rattus everetti. Many

items were already decapitated and dismembered so that they

TATIANA ROSE C. ABANO

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87

Plate 1. Philippine Eagle Pithecophaga jefferyi nest in the canopy of a

Hopea sp. tree, 11 May 2015.

could not be identified with certainty. In terms of biomass, mammals

(57.6%) made the largest contribution to the chick's diet, but in terms

of the number of food items, reptiles made up 37.4%, mammals

32.3%, birds 10.2% and unidentifiable items 20.3% (Table 2).

Discussion

Although we found no significant difference in the placement of

the nests compared with those on Mindanao, where the mean

nest diameter is 2 m (Gonzales 1968, Kennedy 1985, Ibanez 2007),

the nests on Luzon were relatively smaller. This difference in size

and the atypical concealment of the nest by surrounding foliage

are probably adaptations to protect it from strong winds during

typhoons. The egg-laying time on Luzon appeared to be somewhat

delayed compared with the typical September-December egg-

laying season on Mindanao (Kennedy 1985, Ibanez 2007). This

delay is probably another adaptation to cope with the typhoon

season — typhoons occur about 80% more frequently on Luzon

than on Mindanao (PAGASA 2011) and affect the region more

frequently in the period from July to December (PAGASA 2015).

Although, as reported in Table 1, we saw the juvenile flying away

from the nest-tree to another tree 100 m away on 26 August 2015,

Table 1. Summaryofthedateson which indicators of the development

of the young Philippine Eagle in the Luzon nest were first documented;

the estimated hatching date was the end of March 2015

Date Indicators of juvenile development

1 May 2015 Object plays; weak vocalisations; momentary upright posture; walking with tiny steps

6 May 2015 Flapping exercises

9-May 2015 Feeding independently but with the adult female on the nest

24 Jun 2015 Feeding independently on leftovers without an adult on the nest; improving upright

posture, perching and other activities

26 Jun 2015 Feeding independently on fresh prey delivered by the adults

7 Aug 2015 Practising flights out of the nest bowl and hopping and flying from one branch to

another in the canopy above

26 Aug 2015 Flight from nest tree to another tree 100 m away

this was not the final time that the juvenile made use of the nest:

she continued to return to the nest-tree and to be seen in the close

vicinity a number of times after that date. Based on our experience

of the behaviour of juvenile Philippine Eagles on Mindanao, we

would anticipate that she is likely to finally move away from this

area around the end of 2016. Likewise, the same hypothesis —

based on Mindanao breeding period observations that, following

an incubation period of about two months, a juvenile eagle will

mostly reside in or close to its birthplace for a period of around 21

months — may be applied to the young eagle seen in mid-March

2013. It was never seen again in the area close to the recently

vacated nest-site that we found on 22 March 2013, implying that if

it did originate there it was already on the move when we saw it. If

that was the case, its parents may have bred early in 2011 (around

January), similar to the 2015 Luzon pair.

Both the Luzon nests were located deep in forest interiors; this

is different from Mindanao where the majority of nests are within

100 m of the forest edge (Bueser et at. 2003). However, whilst the

nestfound in 2013 at 1,098 m was well within the known altitudinal

range on Mindanao — 630-1,434 m (Ibanez 2007) — the 2015 nest

at about 450 m is about 200 m lower than previously reported on

Mindanao.

Table 2. Summary of the food items delivered by the adult Philippine

Eagles.

%of Weight Biomass

Food item No. total (kg) (kg) %

*based on one specimen only

Plate 2. Adult female eagle feeding young, 6 May 2015.

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88

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Forktail 32 (2016)

Our records of food deliveries to the Luzon nest also revealed

important differences between Luzon and Mindanao. In terms of

biomass contribution, the Northern Luzon Giant Cloud Rat was the

most important prey species on Luzon, unlike Mindanao where the

Long-tailed Macaques made up the highest biomass contribution

(36.5%). In numerical terms the Northern Luzon Giant Cloud Rat was

also one of the top prey species on Luzon, in place of the Philippine

Flying Lemur Cynocephalus volans and Mindanao Flying Squirrel

Petinomys crinitus, the most numerous prey items on Mindanao

(Kennedy 1985, Ibanez etal. 2003, Ibanez 2007); these two species

are absent from Luzon. On Luzon, reptiles numerically accounted for

37.4% of the prey items, compared with less than 10% on Mindanao

(Kennedy 1985, Ibahez2007), suggesting a greater variety of available

prey on Luzon. Finally, it is noteworthy that no domestic animals

were recorded from the Luzon nest, contrary to the observations of

Concepcion etal. (2006) and Ibanez (2007) on Mindanao.

The differences in both nest location (altitude and habitat)

and breeding period discovered during the investigation of

this first confirmed breeding record on Luzon suggest that

some temporal and rangeadjustments may be needed in ongoing