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

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MINISTRY OF EDUCATION AND MINISTRY OF AGRICULTURE AND TRAINING RURAL DEVELOPMENT VIETNAM NATIONAL UNIVERSITY OF FORESTRY  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 Hanoi, 2018 MINISTRY OF EDUCATION AND MINISTRY OF AGRICULTURE AND TRAINING RURAL DEVELOPMENT VIETNAM NATIONAL UNIVERSITY OF FORESTRY  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 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 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 i Table of Contents Abstract i List of figures iii List of tables iv CHAPTER INTRODUCTION .1 CHAPTER LITERATURE REVIEW Gibbon status in Vietnam Northern yellow-cheeked gibbon (Nomascus annamensis) Nomascus annamensis in Vietnam Nomascus annamensis vocalization CHAPTER METHOD 12 3.1 Study area 12 3.2 Data collection 13 3.3 Sound analysis 16 CHAPTER RESULTS 18 4.1 Gibbon calls detected 18 4.2 Gibbon group structure detected 23 CHAPTER DISCUSSION 27 CHAPTER CONCLUSION 29 ACKNOWLEDGEMENT 30 REFERRENCES .31 APPENDIX .34 ii List of figures Figure Distribution of the six Nomascus gibbons in Vietnam .3 Figure Northern yellow-cheeked gibbon (Nomascus annamensis) .4 Figure Phylogenetic relationships among crested gibbon species base on complete mitochondrial cytochrome b sequence data Figure Spectrograms of N leucogenys, N siki, N annamensis and N gabriellae Figure The distribution of N.annamensis in Vietnam Figure Typical male‟s (left) and female‟s (right) spectrogram showing the vocalization of gibbons .10 Figure Representative spectrogram showing the parameters measured 11 Figure Bach Ma National Park, Hue and Quang Nam Saola Nature Reserve location 12 Figure 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 iii List of tables Table Number of recording posts with gibbon calls 18 Table Number of gibbon group per recording site detected by bioacoustics analysis 22 Table The number of gibbon call structure types 25 Table N annamensis group structure and averaged group size in three protected areas 26 iv CHAPTER 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), Redshanked 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 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 along the survey transects or stay at listening/observing posts This method is 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 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 LITERATURE REVIEW 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 (Nomascus Eastern nasutus), black gibbon Western black gibbon (Nomascus concolor), Northern white-cheeked leucogenys), gibbon gibbon Southern (Nomascus yellow-cheeked (Nomascus white-cheeked siki), gibbon Northern Figure Distribution of the six (Nomascus Nomascus gibbons in Vietnam annamensis), Southern yellow-cheeked Source: Rawson et al 2011 gibbon (Nomascus gabriellae) (Fig 1) 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 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 Northern yellow-cheeked gibbon (Nomascus annamensis) a) Adult male; b) Adult female Source: Endangered Primate Rescue Center (EPRC) thus, these detected N annamensis numbers are higher and more representative for whole population in the areas As the result of habitat loss and negative influences of human activities, the number of Northern yellow-cheeked gibbon in Quang Nam SNR seems to reduce The usual family group of gibbon is a bonded male and female, and will also include the offspring of the bonded pair (Sommer and Reichard 2000) It has long been believed that gibbons form only monogamous social groups that include an adult male and female and their immature offspring Recent research has shed light on the social structure of gibbons, though, and while many form long-term pair bonds, extra-pair copulations may occur (Reichard 1995) In my study, nearly half number of detected groups have complex structures including monogamous and extra-pair copulation, the rest half is pair and solitary structures The average group size is 2.34 ± 0.15, and largest group size is (see Appendix 1) This result reflects the common group structure type of N annamensis that similar to previous researches However, the number of individuals per groups estimated here does not include the infant individuals because they does not make calls With this study, at least 96 individuals including 45 males, 43 females and juveniles were detected It means gender imbalance is not problem of gibbon population in three protected areas Using sound recorder and sound analysis can provide accurate results in detecting number and structure of gibbon group With the recorded files and sound analysis software, surveyor have more time to analyze the gibbon sound and define the group than in field Although being a promising way to detect the gibbon status, errors still could be occurred The accuracy of this method depends on the quality of recorder, the condition of weather, and the competence of sound analyzer Protecting habitat and controlling the hunting of N annamensis is the most important action for conserving all remaining population of this species in Vietnam It is necessary to call more fund for species conserving Further research also should be encouraged to contribute completely information of gibbon status in the entire distribution range 28 CHAPTER CONCLUSION Northern yellow-cheeked gibbon calls occurred in 19 recording posts in three protected areas During 90 days of surveying, 66 gibbon calls were recorded At least 41 groups of N annamensis were recorded, of which 22 groups were located in Hue SNR, 15 groups in Bach Ma NP and groups in Quang Nam SNR The averaged group number of N annamensis per location of Hue SNR, Bach Ma NP and Quang Nam SNR orderly are 2.2, 1.5 and 0.4 groups/location The dominant structure of N.annamensis is complex group structure In total of 41 recorded groups, 20 (49%) were gibbon complex group, 11 (27%) pairs and 10 (24%) solo individuals This result is similar with previous finding of other researchers on gibbon social structure The group size are 2.36 ± 0.21, 2.40 ± 0.25 and 2.00 ± 0.41 individuals/ group in Hue SNR, Bach Ma NP and Quang Nam SNR respectively Combining between acoustic analysis result and information on group size and structure, at least 96 individuals of Northern yellow-cheeked gibbons were identified including 45 males, 43 females and juveniles The most effective solutions for gibbon conservation in these three protected areas include protecting habitat, controlling the hunting, raising fund, and enhancing gibbon status surveys monitoring 29 ACKNOWLEDGEMENT This thesis was impossible without the support of various lectures of International Master Program at Vietnam National University of Forestry I am grateful to my advisor Assoc Professor Vu Tien Thinh for giving me a constant support and enthusiasm guidance during the time of research and writing of this thesis Special thanks to WWF-Vietnam for their kindly support, providing data and information to help me complete this study Sincerely thanks to all of my friends and family who always encourage, and support me during this strenuous time 30 REFERRENCES Books/Journal Dickinson, CJ, and VN Thinh 2006 “An Assessment of the Fauna and Flora of the Green Corridor Forest Landscape, Thua Thien Hue Province, Vietnam.” Report Geissmann, Thomas 2000 “Vietnam Primate Conservation Status Review 2000, Part 1: Gibbons.” Fauna and Flora International, Indochina Programme, Hanoi, 2000 Geissmann 2002 “Duet-Splitting and the Evolution of Gibbon Songs.” Biological Reviews 77 (1): 57–76 Ha, Nguyen Manh 2004 “Result of Primate Survey in Quang Binh Province.” Journal of Agriculture and Rural Development 2: 263–64 Ha, Nguyen Manh, Thach Mai Hoang, Pham Trong Anh, Le Manh Hung, Nguyen Truong Son, Nguyen Van Dat, and Do Quang Huy 2005 “Status of White Cheek-Crested Gibbon (Nomascus Leucogenys) in North Central of Vietnam.” Center for Natural Resources and Environmental Studies, Hanoi, Vietnam Haimoff, Elliott H 1984 “Acoustic and Organizational Features of Gibbon Songs.” The Lesse Apes Hoang, Minh, Tu Van Khanh, Huynh Van Thuong, and Barney Long 2005 “Primate Conservation in Quang Nam Province, Central Vietnam.” Tam Ky, Vietnam: WWF Indochina and Quang Nam Forest Protection Department Hon, Naven, Alison M Behie, Jessica M Rothman, and Ken G Ryan 2018 “Nutritional Composition of the Diet of the Northern Yellow-Cheeked Crested Gibbon (Nomascus Annamensis) in Northeastern Cambodia.” Primates, 1–8 Hradec, Michal, Pavel Linhart, Luděk Bartoš, and Petra Bolechová 2017 “The Traits of the Great Calls in the Juvenile and Adolescent Gibbon Males Nomascus Gabriellae.” PloS One 12 (3): e0173959 10 Koda, Hiroki, Chisako Oyakawa, Akemi Kato, Daisuke Shimizu, Yasuhiro Koyama, and Satoshi Hasegawa 2014 “Immature Male Gibbons Produce Female-Specific Songs.” Primates 55 (1): 13–17 11 Konrad, Roger, and Thomas Geissmann 2006 “Vocal Diversity and Taxonomy of Nomascus in Cambodia.” International Journal of Primatology 27 (3): 713 12 Lan, LV, S Ziegler, and T Grever 2002 “Utilization of Forest Products and Environmental Services in Bach Ma National Park, Vietnam.” German Development Service, Hanoi Vietnam Google Scholar 13 McDonald, Paul G, Anahita JN Kazem, and Jonathan Wright 2007 “A Critical Analysis of „False-Feeding‟Behavior in a Cooperatively Breeding Bird: Disturbance Effects, Satiated Nestlings or Deception?” Behavioral Ecology and Sociobiology 61 (10): 1623–35 14 Merker, Björn, and Cathleen Cox 1999 “Development of the Female Great Call in Hylobates Gabriellae: A Case Study.” Folia Primatologica 70 (2): 97–106 15 Mootnick, Alan R, and Peng‐Fei Fan 2011 “A Comparative Study of Crested Gibbons (Nomascus).” American Journal of Primatology 73 (2): 135–54 16 Rawson, Benjamin M, Paul Insua-Cao, Nguyen Manh Ha, Van Ngoc Thinh, Hoang Minh Duc, Simpon Mahood, Thomas Geissmann, and Christian Roos 2011 “The Conservation Status of Gibbons in Vietnam.” Fauna & Flora International/Conservation International, Hanoi, Vietnam, 13–116 17 Rawson, BM 2004 “Vocalisation Patterns in the Yellow-Cheeked Crested Gibbon (Nomascus Gabriellae).” Conservation of Primates in Vietnam, 130–36 18 Reichard, Ulrich 1995 “Extra‐pair Copulations in a Monogamous Gibbon (Hylobates Lar).” Ethology 100 (2): 99–112 19 Robson, CR, JC Eames, M Newman, Nguyen Cu, and Truong Van La 1991 “Forest Bird Surveys in Vietnam 1989/90, Final Report.” International Council for Bird Preservation, Cambrige, UK 20 Sommer, Volker, and Ulrich Reichard 2000 “14• Rethinking Monogamy: The Gibbon Case.” Primate Males: Causes and Consequences of Variation in Group Composition, 159 21 Tallents, Lucy, Thomas Geissmann, Trinh Dinh Hoang, and La Quang Trung 2001 “Survey for Crested Gibbons (Genus Nomascus) in Bach Ma National Park, Viet Nam, April 2001.” Fauna & Flora International, Indochina Programme, Hanoi, Vietnam 22 Thinh, VN, LQ Khanh, and D Tuoc 2002 “The Tiger (Panthera Tigris) Ecology in Bach Ma National Park.” Phu Loc Save the Tiger Fund 23 Van Ngoc Thinh, Mootnick AR, Vu Ngoc Thanh, and C Roos 2010 “A New Species of Crested Gibbon, from the Central Annamite Mountain Range.” Vietnamese Journal of Primatology (4): 1–12 24 Van Thien, Nguyen, Nguyen Quang Hoa Anh, Le Vu Khoi Van Ngoc Thinh, and Christian Roos 2017 “Distribution of the Northern Yellow-Cheeked Gibbon (Nomascus Annamensis) in Central Vietnam.” Vietnamese Journal of Primatology, 83 25 Vu Tien, Thinh, Dinh Le Thi, Dung Tran Van, Hoa Nguyen Thi, Thanh Nguyen Chi, Hai Dong Thanh, Manh Nguyen Dac, Toan Giang Trong, Van Nguyen Huu, and Tung Thao A 2017 “Application of Automatic Recorder and Sound Analysis in Surveying the Presence and Distribution of Bird Species in Ngoc Linh Nature Reserve, Quang Nam Province.” 26 Wikramanayake, Eric D, and Văn Dũng Vũ 1997 A Biological and SocioEconomic Survey of West Quang Nam Province, with Recommendations for a Nature Reserve UNDP 27 Wilson, David R, Matthew Battiston, John Brzustowski, and Daniel J Mennill 2014 “Sound Finder: A New Software Approach for Localizing Animals Recorded with a Microphone Array.” Bioacoustics 23 (2): 99–112 Websites: http://www.tourconduongdisan.com/vn/Tin-tuc/Tin-du-lich-Hue/-Thanh-lap-Khubao-ton-Sao-la-tai-tinh-Thua-Thien-Hue.htm APPENDIX Appendix 1: N annamensis group structure detected by acoustic recording analysis Survey Number of Number of Number of Total Average Males Females Offspring individuals number Complex group 1 1 Complex group 2 Pair 1 Individual 0 Individual 0 Complex group 1 Complex group 2 1 Hue SNR Individual 0 Hue SNR Complex group 1 Pair 1 Individual 0 Complex group 1 1 Complex group 2 Complex group Complex group 2 Protected areas Block ID FC Hue SNR Hue SNR Hue SNR 347 Hue SNR Hue SNR 346 Hue SNR Hue SNR Hue SNR 348 351 Hue SNR Hue SNR Hue SNR Hue SNR Hue SNR 349 10 350 Complex group/ pair/ individual number 3 Hue SNR Hue SNR Hue SNR Hue SNR 17 353 18 352 Hue SNR Hue SNR 19 404 Hue SNR Bach Ma NP 57 410 Bach Ma NP Bach Ma NP 70 418 Bach Ma NP Individual 0 Complex group Pair 1 Complex group Complex group Pair 1 Individual 0 Complex group 1 Individual 0 Individual 1 Pair 1 2 3 Bach Ma NP 71 427 Complex group Bach Ma NP 73 417 Pair 1 Bach Ma NP 75 42 Pair 1 Bach Ma NP Complex group 1 1 Bach Ma NP Complex group 2 Complex group 2 Bach Ma NP Pair 1 Bach Ma NP Individual 0 Bach Ma NP 77 419 Bach Ma NP Bach Ma NP 80 417 Bach Ma NP Quang Nam SNR Quang Nam SNR Quang Nam SNR Quang Nam SNR 25 12 27 12 34 22 Complex group 1 Complex group 1 Pair 1 Complex group Pair 1 Individual 0 Pair 1 Appendix 2: Number of gibbon groups, groups‟ structure Hue SNR Survey Block ID X Y Number of Male 347 761817 1784921 Number of offspring Hue SNR 346 768014 1785459 0 1 Hue SNR 348 765346 1783593 Hue SNR 351 764090 1783611 3 Hue SNR 349 767370 1783250 3 Hue SNR 10 350 763290 1782363 Hue SNR 16 353 764763 1776408 0 0 Hue SNR 17 353 767328 1775953 2 Hue SNR 18 352 768934 1775037 Hue SNR 19 404 771384 1776695 3 26 22 52 22 Protected Area Coordination FC Total Number of Female Number of individual Number of group Bach Ma NP 57 410 781542 1776275 1 Bach Ma NP 67 427 791782 1778404 0 0 Bach Ma NP 69 429 791222 1773915 0 0 Bach Ma NP 70 427, 418 780518 1774312 2 Bach Ma NP 71 427 793669 1776574 Bach Ma NP 72 42 794677 1773125 0 0 Bach Ma NP 73 417 795438 1781878 1 Bach Ma NP 75 42 796912 1775222 1 Bach Ma NP 77 419 799966 1779745 6 13 Bach Ma NP 80 417 799427 1781576 15 17 36 15 Total Quang Nam SNR 25 12 765599 1773082 Quang Nam SNR 27 12 765261 1771879 Quang Nam SNR 34 22 775147 1773455 1 Quang Nam SNR 37 21 778004 1773058 0 0 Quang Nam SNR 39 23 780518 1774312 0 0 Quang Nam SNR 40 26 781684 1770166 0 0 Quang Nam SNR 41 38 780971 1768299 0 0 Quang Nam SNR 45 36 786310 1770820 0 0 Quang Nam SNR 47 36 789064 1770281 0 0 Quang Nam SNR 53 45 792183 1769424 0 0 Total 4 Total in protected areas 45 43 96 41 Appendix Some picture of N annamensis, N leucogenys, N siki and N gabriellae Male of N annamensis Photo: Tilo Nadler Male of N leucogenys Photo: Tilo Nadler Adult male of N siki Photo Tilo Nadler Adult male of N gabriellae Photo Tilo Nadler Adult female of N annamensis Photo: Tilo Nadle Adult female of N gabriellae Photo: Tilo Nadler Adult female N siki Photo: Tilo Nadler Adult female N leucogenys Photo: Jurgen ... 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... 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. .. 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

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