A survey for northern yellow cheeked gibbon (nomascus annamensis) in central annamite mountain range of vietnam using bioacoustics metthod

MINISTRY OF EDUCATION AND NGUYEN THI HOA A SURVEY FOR NORTHERN YELLOW-CHEEKED GIBBON Nomascus annamensis IN CENTRAL ANNAMITE MOUNTAIN RANGE OF VIETNAM USING BIOACOUSTICS METHOD MASTER

MINISTRY OF EDUCATION AND

NGUYEN THI HOA

A SURVEY FOR NORTHERN YELLOW-CHEEKED GIBBON (Nomascus annamensis) IN CENTRAL ANNAMITE MOUNTAIN RANGE OF

VIETNAM USING BIOACOUSTICS METHOD

MASTER THESIS IN FOREST SCIENCE

MINISTRY OF EDUCATION AND

NGUYEN THI HOA

A SURVEY FOR NORTHERN YELLOW-CHEEKED GIBBON (Nomascus annamensis) IN CENTRAL ANNAMITE MOUNTAIN RANGE OF

VIETNAM USING BIOACOUSTICS METHOD

Major: Forest Science Code: 8620201

MASTER THESIS IN FOREST SCIENCE Academic advisor: Assoc Prof Vu Tien Thinh

Signature:

Hanoi, 2018

Abstract

The Northern yellow-cheeked gibbon (Nomascus annamensis) is a new

species that occurs only in central Vietnam, southern Laos and northern Cambodia Recently, only a few surveys have been carried out on the general status of species, but information on detailed distribution is essential for guiding conservation efforts

To obtain further information on the distribution of N annamensis, I carried out a

study for this gibbon species in three protected areas of Central Annamite Mountain Range of Vietnam which are Hue Saola Nature Reserve (SNR), Quang Nam SNR, and Bach Ma National Park (NP) During total of 90 survey days in 30 recording posts, 66 gibbon calls were recorded that lead to an estimation of at least 41 gibbon groups, of which 22 groups in Hue SNR, 15 groups in Bach Ma NP and 4 groups Quang Nam SNR Of 41 recorded groups, 20 groups were gibbon complex groups,

11 were pairs and 10 were solo individuals 45 males, 43 females and 8 juveniles

are included in 41 groups N annamensis is typical sensitive to the change in habitat areas and human impacts Moreover, most of N annamensis populations

receive little protection while they are facing threats Therefore, urgent and sustainable efforts should be applied as soon as possible

Table of Contents

Abstract i

List of figures iii

List of tables iv

CHAPTER 1 INTRODUCTION 1

CHAPTER 2 LITERATURE REVIEW 3

1 Gibbon status in Vietnam 3

2 Northern yellow-cheeked gibbon (Nomascus annamensis) 4

3 Nomascus annamensis in Vietnam 7

4 Nomascus annamensis vocalization 9

CHAPTER 3 METHOD 12

3.1 Study area 12

3.2 Data collection 13

3.3 Sound analysis 16

CHAPTER 4 RESULTS 18

4.1 Gibbon calls detected 18

4.2 Gibbon group structure detected 23

CHAPTER 5 DISCUSSION 27

CHAPTER 6 CONCLUSION 29

ACKNOWLEDGEMENT 30

REFERRENCES 31

APPENDIX 34

List of figures

Figure 1 Distribution of the six Nomascus gibbons in Vietnam 3

Figure 2 Northern yellow-cheeked gibbon (Nomascus annamensis) 4

Figure 3 Phylogenetic relationships among crested gibbon species base on complete mitochondrial cytochrome b sequence data 5

Figure 4 Spectrograms of N leucogenys, N siki, N annamensis and N gabriellae. 6

Figure 5 The distribution of N.annamensis in Vietnam 8

Figure 6 Typical male‟s (left) and female‟s (right) spectrogram showing the vocalization of gibbons 10

Figure 7 Representative spectrogram showing the parameters measured 11

Figure 8 Bach Ma National Park, Hue and Quang Nam Saola Nature Reserve location 12

Figure 9 Study area and recorder locations in three protected areas in 2016 15

Figure 10 Sound windows in Raven software 16

Figure 11 Recording locations with N annamensis calls in Hue SNR 19

Figure 12 Recording locations with N annamensis calls in Bach Ma NP 20

Figure 13 Recording locations with N annamensis calls in Quang Nam SNR 21

Figure 14 Averaged number of gibbon group per recording site detected by bioacoustics analysis 22

Figure 15 Some types of gibbon call‟s structure recorded in the study areas 24

Figure 16 The percentage of N annamensis group structure types 25

Figure 17 Number of males, females and juvenile N annamensis detected in three protected areas in 2016 26

List of tables

Table 1 Number of recording posts with gibbon calls 18 Table 2 Number of gibbon group per recording site detected by bioacoustics

analysis 22

Table 3 The number of gibbon call structure types 25

Table 4 N annamensis group structure and averaged group size in three protected

areas 26

CHAPTER 1 INTRODUCTION

The Central Annamite Mountain Range of Vietnam is considered as one of the country‟s biodiversity hotspots and of worldwide importance identified by WWF The region is habitat for many rare and endemic species including the

recently rediscovered for the first time after 15 years Saola (Pseudoryx nghetinhensis), Giant muntjac (Muntiacus vuquangensis), Truong Son muntjac (Muntiacus truongsonensis), Grey-shanked douc langur (Pygathryx cinerea), Red- shanked douc langur (Pygathrix nemaeus), and Asian elephant (Elephas maximus)

as well as the Northern yellow-cheeked gibbon (Nomascus annamensis)

The Northern yellow-cheeked gibbon was described as a new species of

Hylobatidae in 2010 (Van Ngoc Thinh et al 2010) Previously, N annamensis was undistinguished with N gabriellae and N siki because of their similarities in morphology and sound of calls However, Van Ngoc Thinh et al (2010) proved the

differences in their vocalization and mitochondrial DNA, then described and

published N annamesis as a new species in 2010 Up to date, N annamensis has

been recorded only in central Vietnam, Laos and Cambodia, thus, it can be seen that this gibbon species is endemic species in Indochina region (Rawson et al 2011)

Although, the general distribution of N annamensis is well known, the detail

information about the exact distribution range and occurrence inside protected areas, as well as estimates of population size and structure are lacking (Van Thien et

al 2017) Similar to the other crested gibbons species, the remaining number of N annamensis has been decreasing by illegal hunting, habitat loss due to illegal

logging, conversion of forest land into agriculture and plantation lands Therefore,

conservation actions should be urgently employed for N annamensis

Gibbons are typically inconspicuous and are often hard to find because of their low visibility and unpredictable behavior in response to human Luckily, under ideal conditions the gibbon calls can be heard up to 3 kilometers away (Rawson 2004) For this reason, the occurrence of gibbon can be detected by their calls Traditionally, the occurrence of gibbon species were investigated by human survey The surveyor record all information of heard or observed gibbons while they move

simple, easy to conduct and can be reliable However, the information is accurate only when it is collected by highly experienced and skillful surveyors who have ability to identify gibbon groups and individuals In order to approach gibbon group, they may have to move in large area The presence and movement of surveyors can effect to animal‟s behavior (McDonald et al 2007)

Currently, bioacoustics analysis is a promising method for monitoring the presence, distribution, movement and behavior of terrestrial animals including gibbon species (Wilson et al 2014) Bioacoustics analysis requires hardware and software components Hardware is recording equipment used to record animal‟s sounds, while software refers to computer program that can enter, interpret and analysis the recorded sound files

In order to contribute to N annamensis conservation, I conducted a study

titled “A survey for Northern yellow-cheeked gibbon (Nomascus annamensis) in

Central Annamite Mountain Range of Vietnam using bioacoustics method”

The goal of the study is to obtain the information of N annamensis population in

three protected areas in Central Annamite Mountain Range of Vietnam including Hue SNR, Bach Ma NP and Quang Nam SNR This goal is followed by 2 specific

objectives: (1) assessing number of N annamensis groups in three protected areas; (2) and assessing detailed information of N annamensis group size and structure

(male, female and juvenile)

CHAPTER 2 LITERATURE REVIEW

1 Gibbon status in Vietnam

Vietnam is home to several gibbon species They can be found from the most northerly subtropical forest in the north to tropical monsoon lowland forests in the south The status of gibbon in Vietnam can be considered to be an indicator for the general status of the country‟s biodiversity and natural environment Therefore, conservation status review of gibbon in Vietnam was carried out by Geissmann et al (2000) and then by Rawson et al (2011) The authors of newest publication have conducted a survey that collated records of gibbons from all sites in Vietnam known

to have gibbons and where information can be assessed to be reliable Rawson et al (2011) has provided a comprehensive information on the status of gibbon in Vietnam According to Rawson et al

(2011), all gibbons in Vietnam are

classified into the genus of crested

gibbon Nomascus Totally, there are

seven species of Nomascus, all located in

the eastern Mekong River in Cambodia,

China, Laos and Vietnam, six of which

are found in Vietnam The species in

Vietnam being, from north to south

orderly are Eastern black gibbon

(Nomascus nasutus), Western black

gibbon (Nomascus concolor), Northern

white-cheeked gibbon (Nomascus

leucogenys), Southern white-cheeked

gibbon (Nomascus siki), Northern

yellow-cheeked gibbon (Nomascus

annamensis), Southern yellow-cheeked

gibbon (Nomascus gabriellae) (Fig 1)

Figure 1 Distribution of the six

Nomascus gibbons in Vietnam

Source: Rawson et al 2011

Although, Vietnam holds more species of Nomascus than any other country, gibbon

population in Vietnam are currently undergoing a crisis and this is indicative of trends in wildlife population within the country

2 Northern yellow-cheeked gibbon (Nomascus annamensis)

Diagnosis and description

Nomascus annamensis is the most recently described Nomascus gibbon

species (Van Ngoc Thinh et al 2010) The species was previously confused as

either N gabriellae or N siki because of resembles morphologically and vocally

Adult N annamensis clearly differ from N leucogenys and N siki (Mootnick and Fan 2011), but are very similar to N gabriellae (See Appendix 3)

Males are black with cheek whiskers ranging in color from yellowish, deep orange hued and light brown (Fig 2a) Females are golden yellow with a brown to black pack on the crown of their head (Fig 2b)

a)

b)

Figure 2 Northern yellow-cheeked gibbon (Nomascus annamensis)

a) Adult male; b) Adult female

Source: Endangered Primate Rescue Center (EPRC)

According to complete mitochondrial cytochrome b gene sequence data (Fig

3), N annamensis is closest related to N gabriellae In specifically, N annamensis‟s gen (n = 22) differs from N gabriellae (n = 69), N siki (n = 32) and

N leucogenys (n = 29)

Figure 3 Phylogenetic relationships among crested gibbon species base on

complete mitochondrial cytochrome b sequence data

Source: Van Ngoc Thinh, et al 2010

By using a discriminant function analysis, Van Ngoc Thinh et al (2010) demonstrated the differences in several acoustic feature such frequency and tempo (Fig 4) from the other crested gibbon species

Figure 4 Spectrograms of N leucogenys, N siki, N annamensis and N gabriellae

Source: Van Ngoc Thinh et al 2010

Etymology

- English name: northern yellow-cheeked gibbon

- French name: Gibbon à joues jaunes du Nord

- German name: Nördlicher Gelbwangen Schopfgibbon

Geographic range

Base on Van Ngoc Thinh‟s review, N annamensis occurs in the central and

southern provinces of Attapu, Champasak, Salavan, Savannakhet and Xekong of Laos; north of the Srepok River (about 13°30‟ N) in Stung Treng and Rattanakiri

Provinces of Cambodia and from approximately the Thach Han River (about 16°40‟ - 16°50‟ N) in Quang Tri Province to the Ba River (about 13°00‟ - 13°10‟N)

in Gia Lai and Phu Yen Provinces in Vietnam

Habitat and ecology

N annamensis occurs in broadleaf evergreen and semi-evergreen forest They

spent the majority of their time feeding on fruit, followed by young leaves, flowers and mature leaves (Hon et al 2018)

Status and conservation

The Northern yellow-cheeked gibbon was described as a new species, thus is yet to be evaluated for the IUCN Red List and the 2007 Vietnam Red Data Book

CITES Appendix I - this species is threatened with extinction and international trade is permitted only in exceptions circumstances

3 Nomascus annamensis in Vietnam

Status and distribution

The status and distribution of Nomascus annamensis were first described in Vietnam by Geissmann 2000, but under the consideration as N siki and N gabriellae Until 2010, after its vocalizations and genetic were studied, N annamensis was confirmed as a new crested gibbon species At that time, the presence of N annamensis was recorded in at least nine provinces and 11

designated protected areas, two proposed nature reserves and two watershed management areas

As the results of Nguyen Manh Ha‟s study (2009), the largest known

population of N annamensis in Vietnam was found in Dak Rong and Phong Dien

Nature Reserves These nature reserves and surrounding districts in Quang Tri and Thua Thien Hue Provinces have been subject to considerable biodiversity surveying and monitoring over the long time, so in some way it is the area has the largest

known population Two areas that may also support important populations of N annamensis are Song Thanh and Ngoc Linh Nature Reserves in Quang Ngai and

Quang Nam Provinces; and Kon Ka Kinh National Park, Kon Cha Rang Nature Reserve and surrounding production forests in Kon Tum Province

Additionally, the occurrence of N annamensis has been confirmed in eight

protected areas in central Vietnam (Fig 5): Bac Huong Hoa NR (10 groups), Dakrong NR (7 groups), Phong Dien NR (10 groups), Bach Ma NP (13 groups), Hue SNR (8 groups), Song Thanh NR (2 groups), Chu Mom Ray NP (14 groups) and Kon Ka Kinh NP (7 groups) (Van Thien et al 2017)

Figure 5 The distribution of N.annamensis in Vietnam

Source: Rawson et al 2011

Threats

Illegal hunting and habitat loss are the principle threats to N annamensis in

Vietnam (Rawson et al 2011) The species is hunted to supply commercial demand

from the pet trade and zoos, traditional medicine and local use (Ha et al 2005) N annamensis is special sensitive to the change in habitat Loss and fragmentation of

forest habitats due to legal and illegal logging, conversion for agriculture, and construction of roads and hydroelectric dams, is occurring throughout the national

range of N annamensis All these activities influence strongly to the species

population in Vietnam

Nomascus annamensis in Hue SNR, Bach Ma NP and Quang Nam SNR

Although the survey coverage was incomplete and the total gibbon population was unknown, it was suggested at least 14 gibbon groups occurred in Hue SNR (Van Ngoc Thinh et al 2007; Nguyen Quang Hoa Anh et al 2010)

In Bach Ma NP, based on surveys in 1990 - 1991, Eames and Robson estimated a total population for the park of 23 - 30 individuals Survey coverage of the site is not complete and the total gibbon population is unknown (Robson et al 1991) In 2001, eight groups were recorded, including two solitary males, in an area

of 600 ha (Tallents et al 2001) Then, five gibbon groups were recorded in an area

of 1,000 ha in 2005 (Van Ngoc Thinh et al 2010)

In Quang Nam Saola Nature Reserve, N annamensis likely to occur within

this site In 2005, 30 gibbon groups were recorded in 13 widespread locations in nearby localities (Hoang et al 2005) and in 1997, gibbons were documented within Dong Giang District and other nearby districts (Wikramanayake and Vũ 1997) Currently, the status of all gibbon populations in this reserve are unknown and it appears that the population actually within this area is insignificant

4 Nomascus annamensis vocalization

Beside human, gibbons are only hominoids who both sexes engage in elaborate, cyclical vocal displays called song (Merker and Cox 1999) The songs are emitted by not only individual but also the monogamous and territorial gibbon pair The vocal repertoire of the gibbons is sex-specific

Figure 6 Typical male‟s (left) and female‟s (right) spectrogram showing the

“great call” phrases A complete “great call” has typically 5-13 notes that further split into “oo” notes, “bark” notes and a “twitter” part (Fig 6 - right) (Konrad and Geissmann 2006) The “oo” phase consists long notes of slowly increasing frequency of ≤1 kHz/s “Bark” (subsequent) notes are short, with a steep frequency increase of >1 kHz/s After the climax of the acceleration, bark notes tail off into the twitter phase The last phase often are not taken in measurements, because twitter notes do not carry very far and the sonogram line is hardly visible for these notes The male gibbon song is shorter, more regular and belongs to a band from 1

to 2 kHz, while the female gibbon song is longer, with larger amplitude from 0.5 to

3 kHz Accordingly, differences in male and female gibbon songs of mature individuals can be easily determined

Initially, a “great call” has been reported as specifically produced by only adult females (Geissmann 2002) However, more recently it has been documented that immature gibbon male can also produce the sound that similar to “great call” (Koda et al 2014) Therefore, it is required to be careful in identification of group

structure “Great calls” of sons were shorter, started higher and ended lower than those of their mothers (Fig 7)

Figure 7 Representative spectrogram showing the parameters measured: Start F

(frequency at call onset), End F (frequency at call offset), Delay; Number of syllables (black number = syllable mother, red number = syllable juvenile male) and song organization of mother's (M) and juvenile's (J) “great calls” Dashed line represents notes of juvenile's “great call”: N(J)-“note juvenile, T(J) – “twitter” juvenile; solid line represents notes of mother's “great call” O – “oo” notes, B –

“bark” notes, T – “twitter”

Source: Hradec et al 2017

CHAPTER 3 METHOD

3.1 Study area

In my study, I used available data which collected by WWF - Vietnam in three contiguous protected areas are Thua Thien Hue SNR, Bach Ma NP and Quang Nam SNR bordering Thua Thien Hue and Quang Nam provinces (Fig 8) in 2016

Bach Ma National Park is

located in the southern edge of

Thua Thien Hue Province in central

Vietnam The area of the park is

located within the coordinate of

16o05‟ - 16o15‟N and 107o43‟ –

107o53‟E In order to conserve the

rich forest between northern and

southern Vietnam, this national

park was established in 1991 (Lan

et al 2002)

The park area is about 220

km2, of which 169 km2 is forest

land and 51 km2 have no forest

cover The forested area includes

27 km2 rich forest, 59 km2 medium

forest, 65 km2 poor forest and the

rest area is young forest (Thinh et

Figure 8 Bach Ma National Park, Hue and Quang Nam Saola Nature Reserve location

Source: Author

al 2002) Because of human affect, no primary forest now remains in Bach Ma NP

Bach Ma NP is located in the central Annamite Mountains and situates on a high mountain ridge that runs west-east from Laotian border to the East Sea This ridge is considered as a biogeographical boundary between the faunas and floras of northern and southern Vietnam National park has steep and rugged terrain with a number of peaks above 1000 meters, the highest peak is Mount Bach Ma at 1,448

meters As the result of having typical topography, Bach Ma NP has long been known as one of the highest priority biodiversity conservation areas (BirdLife)

More specifically, the park is home to a diverse range of species, including 2,373 species of plants and fungi and 2,115 species of animals (Keo & Thien An, 2011) In its diverse, Bach Ma NP also been identified as one of the Vietnamese regions that support significant populations of primates that are of national

importance (Dickinson et al 2006), such as red-shanked douc langurs (Pygathrix nemaeus) and North yellow-cheeked crested gibbon (Nomascus annamensis)

(Robson et al 1991) However, the current status of many of these species at the national park is unclear

Hue and Quang Nam Saola Nature Reserve are two new reserves which were established in 2010 and 2011, respectively, with the aim to protect the survival of

Saola (Pseudoryx nghetinhensis) in Vietnam Hue SNP lies within the coordinates

of 16o03‟-16o09‟ N and 107o25‟-107o39‟ E The NR covers an area of 15,500 hectares, part of which is the large area of primary natural forest remaining in Central Annamite Mountains The NR is home to over 1,200 fauna and flora species

including a number of rare and endemic species such as Pseudoryx nghetinhensis, Muntiacus truongsonensis, Muntiacus vuquangensis and Nesolagus timminsi

(tourconduongdisan) The area of Quang Nam SNR is about 16,500 hectares which covers 4 towns in Tay Giang and Nam Giang districts The NR plays a role as the habitat of many rare wildlife and plants listed in Vietnam and IUCN Red Lists

Bach Ma National Park and Hue, Quang Nam Saola Nature Reserve are adjacent together and form a continuous protected landscape, covering a large area stretching from the Vietnamese coast to Xe Sap National Biodiversity Conservation Area in Lao PDR This secures a landscape corridor which is less vulnerable to the impacts of development, climate change and human pressure

(Fig 9) Each location was continuously recorded in 3 days by small Sony recorders

Point surveying were simultaneously set up with automatic recorder application and nearby recorder‟s locations At each site, a team of 3 to 5 WWF staffs established a listening/ observing posts Each posts also was surveyed in 3 continuous days Surveys began at 5:00am and ended at 10:00 am, in order to be in position during the peak singing time of the gibbon The survey teams have enough knowledge and skill to accurately locate the calling groups by mapping the angle and estimated distance to gibbon groups

During hearing and observing, all information of gibbon groups was recorded in the data sheet as below:

DATA SHEET OF GIBBON SURVEY

Protected Area: ………… Station Number: ……… Date: ……… Coordination: X: ………… Y: ……… Elevation: ……… m Surveyor: ……… Weather conditions:

Singing time

Group structure

Recording file Stating Ending

Figure 9 Study area and recorder locations in three protected areas in 2016

3.3 Sound analysis

Determining number of gibbon group

There are several software that can display the sound sonograms such as Avisoft SASLab Pro, Avisoft SASLab Lite, Avisoft SASLab Recorder, Audacity,

Luscinia, and so on I chose Raven Pro because of it simple and has diverse features

RAVEN software is a bioacoustics research program developed by The Cornell Lab of Ornithology It is a program used for the acquisition, visualization, measurement and analysis the sounds (birds.cornell.edu) Raven is combination of Raven Pro, Raven Exhibit and Raven Lite Raven Pro interface provide environment to open a sound file, navigate the default waveform and spectrogram views, and use selections to play or zoom in on particular parts of sound file Raven Exhibit is a sound visualization and recording system optimized for public displays, exhibits, training, and educational outreach application in places such as science museums, zoos, aquariums, and nature centers Raven Lite is software that lets users record, save and visualize sounds as spectrograms and waveforms The sound of each species has different frequency range, speed of pitch modulation, vocabulary size, and sound duration (Vu Tien et al 2017) that lead to different in spectrum of frequencies called spectrogram (Fig.10)

Figure 10 Sound windows in Raven software

The analyzing process was performed as follow:

- Converting sound data file obtained in the field to a typical format as WAV

- Launching Raven Pro Interactive Sound Analysis Software

- Running the program and analysis

The spectrogram of record sound file were carefully check Whenever a gibbon call was detected, it would be heard again to be surely confirmed

Determining gibbon group structure

The number of gibbon group and group structure could be determined based on the differences in the vocalization of mature males and females shown in spectrograms

The songs of pairs or groups of gibbon could be too far away to determine the number of calls in these songs, and two solitary individuals could be heard/recorded repeatedly Therefore, I could report only the minimum group numbers in each day based on the composition of calling individuals The maximum number of gibbon group detected in a day within 3 surveying days could be considered as the total gibbon group number at a site

CHAPTER 4 RESULTS 4.1 Gibbon calls detected

The number and percentage of recording posts with gibbon calls is highest in Hue SNR and lowest in Quang Nam SNR (Table 1 and Fig 11, 12, 13)

Table 1 Number of recording posts with gibbon calls

Protected areas Number of

recording posts

Number of recording posts with gibbon calls

Percentage of recording posts with gibbon calls