Summary Of Biology Doctoral Thesis: Study on the diversity and distribution patterns of Amphibians (Amphibia) in karst forests of the north Vietnam and conservation measures

The research objectives of the thesis determine the diversity and distribution characteristics of amphibian species (EN) in some limestone areas of Northern Vietnam. Species composition and genetic relations of two species of Limnonectes and Odorrana frogs in Vietnam. Conservation values ​​and threats to frog species in the study area and recommendations for conservation. To know the detailed research content, invite you to consult the thesis.

MINISTRY OF EDUCATION AND

TRAINING

VIETNAM ACADEMY

OF SCIENCE AND TECHNOLOGY

GRADUATE UNIVERSITY SCIENCE AND TECHNOLOGY

PHAM THE CUONG

STUDY ON THE DIVERSITY AND DISTRIBUTION PATTERNS

OF AMPHIBIANS (AMPHIBIA) IN KARST FORESTS OF THE NORTH VIETNAM AND CONSERVATION MEASURES

Research field: Zoology Code: 62.42.01.03

SUMMARY OF BIOLOGY DOCTORAL THESIS

HA NOI – 2018

This dissertation is submitted to the Committee of the Graduate

University of Science and Technology

Supervisors: 1 Dr Nguyen Quang Truong

2 Dr Le Duc Minh

Referee 1: Ass Prof Dr Le Nguyen Ngat

Referee 2: Ass Prof Dr Hoang Ngoc Thao

Referee 3: Dr Hoang Van Ngoc

The research has been carried out

at the Graduate University of Science and Technology

Date of Oral Presentation:……,… /…… /2018

Copy of this dissertation is available:

National Library of Viet Nam

Graduate University of Science and Technology

INTRODUCTION

1 The necessity of the research

Vietnam is recognized as one of the countries with a high level of biodiversity in the world (Conservation International 2014) In terms of amphibian diversity (Class Amphibia), the species number recorded from Vietnam has been rapidly increased in recent decades: from 82 species in 1996 to 162 species in 2005 and up to 176 species in 2009 and the current species number is ca 230 (Nguyen & Ho 1996, Nguyen

et al 2005, 2009, Frost 2017)

Karst ecosystem is considered as a natural laboratory for taxonomic, ecological, evolutionary and biogeographical research (Clements et al 2006) Karst forests provide a variety of distinct microhabitats like

“isolated islands” and are noted for their high levels of endemism (Clements et al 2006) In Vietnam, limestone forests are extensive in the northeastern, northwestern regions and northern Truong Son Range (Sterling et al 2006)

However, limestone forest is a sensitive ecosystem to the human impacts and it is very difficult to restore Limestone in Vietnam has been exploited for infrastructure and economic development, for example, quarrying for road construction, and cement industry Moreover, the fauna in karst forests is threatened by decline because of forest destruction, overexploitation, tourism development and climate change, in particular, the poikilotherm like amphibians (Sterling et al 2006)

The research entitled "Study on the diversity and distribution patterns of

amphibians (Amphibia) in karst ecosystem of the North Vietnam and conservation measures” aims to assess the diversity of amphibians in

limestone forests of northern Vietnam with special focus on two group

complexes of anuran frogs, Limnonectes and Odorrana, in Vietnam In

addition, recommendations for conservation measures are also provided

2 Objectives

- To assess the diversity of amphibians in some selected limestone forests of northern Vietnam;

- To review taxonomic and phylogenetic relationships of two genus

complexes, Limnonectes and Odorrana, in Vietnam;

- To assess conservation potential and threats to the amphibian fauna and to provide recommendations for conservation

3 Contents

Task 1: Inventory of the species diversity of amphibians in some karst forests in northern Vietnam: Hoa Binh Province in the northwestern region, Cao Bang and Ha Giang provinces in the northeastern region and Cat Ba Island, an offshore island in the Gulf of Tonkin This research also focuses on the discovery of new species and new country records

Task 2: Evaluating distribution patterns of amphibian species across altitudinal gradient (from 0 to 1300 m), habitat types and life modes (on the tree, on the ground, and associated with water)

Task 3: Evaluating biogeographic relationships of amphibian fauna amongstudy sites, between mainland and offshore islands, and between northeastern and northwestern regions to verify the evolutionary barrier

of the Red River

Task 4: Evaluating taxonomy and phylogenetic relationships of two

genus complexes, Odorrana and Limnonectes, based on the

morphological comparison and molecular analyses

Task 5: Assessment of conservation potential based on the following criteria: species diversity, number of endemic and threatened species, possibility of population restoration Evaluation of threats to the amphibian populations and provide recommendations for conservation measure

4 Scientific and conservation significances

Scientific significance: The research provides updated data about the diversity of amphibians in the karst forests of northern Vietnam The research also provides novel data on taxonomy and phylogenetic

relationships of Limnonectes and Odorrana from Vietnam

Conservation significance: The research provides baseline data for biodiversity conservation planning and management in northern Vietnam

5 New findings

A total 65 species of amphibans were recorded in karst forests of the North Vietnam, comprising 44 species recored from Ngoc Son-Ngo

Luong NR, 32 species recorded from Hang Kia-Pa Co NR, 33 species recorded from Bac Me NR, 21 species recorded from Ha Lang District, and 23 species recorded from Cat Ba NP

New species: Three new species were described as new for science,

Odorrana mutschmanni from Cao Bang Province, Theloderma annae and Rhacophorus hoabinhensis from Hoa Binh Province

New records: Three species, Leptolalax minimus, Odorrana hainanensis, and O lipuensis, were recorded for the first time from

Vietnam and some other new provincial records from northern Vietnam: One species from Cao Bang Province; two species from Ha Giang Province; three species from Hai Phong city; and five species from Hoa Binh Province

Biogeographic relationships: Based on the list of amphibian species recorded from northern Vietnam, the amphibian fauna of the northeastern region was distinctly separated from that of the northwestern region (Similarity Index = 0.6087) Moreover, the amphibian fauna of the karst forests in mainland also differs from that

of the offshore islands (Similarity Index = 0.4706)

Distribution patterns: Most of amphibian species were recorded at elevations below 800 m (58 species), whereas 34 species were found at elevations above 800 m In terms of habitat types, most of amphibian species were recorded in the undisturbed natural forests (58 species), while the species number recorded in the disturbed forest was 33 species and agricultural and residential areas was 16 species The highest number of record species were found on the ground (42 species)

In this study, we also provide taxonomic review of two poorly

known genera of amphibians, Limnonectes (8 species) and Odorrana

(25 species), based on morphological and molecular data with descriptions of two new species for science and three new country records for Vietnam Phylogenetic relationships of these genera were also discussed with remarks on some species complexes

In addition, we evaluated the threats to the amphibian fauna and provided some recommendations for conservation in northern Vietnam

Chapter 1 LITERATURE REVIEW 1.1 Overview of amphibian research in region

Currently, a total 7.697 species of amphibians was recorded in the world (Frost 2017) In the neigboring countries, 432 species have been recorded from China; 152 species from Lao and 79 species from Cambodia (Frost 2017)

In terms of conservation concern, Stuart et al (2004) stated that

168 species of amphibian were extinction and at least 2,500 species are under threatened in the last 20 years (1984-2004)

1.2 Overview of amphibian research in Vietnam

1.2.1 Faunistic inventory and new discoveies

Bourret (1942) reported 171 species and subspecies of amphibians

in Indochina (Vietnam, Laos, Cambodia) Nguyen and Ho (1996) published a checklist of reptiles and amphibians of Vietnam with 82 recorded species of amphibians Nguyen et al (2005) listed 162 species

of amphibians In the recent book, Nguyen et al (2009) recorded a total

of 176 species of amphibians from Vietnam Since 2010 more than 40 new species of amphibians have been described from Vietnam (Forst 2017)

A number of studies on amphibians were conducted in the Northeast, Northwest, Central, Central Highlands, Southern and some offshore islands of Vietnam

1.2.2 Research on biology and ecology

Research on biological and ecological characters of amphibians focused on few species that were kept in captivity, the widespread

species or endemic to Vietnam: Duttaphrynus melanostictus, Hoplobatrachus rugulosus, Limnonectes bannaensis, Hylarana maosonensis, Quasipaa verrucospinosa, Polypedates mutus, Paramesotriton deloustali

1.2.3 Research on tadpoles and bioacoustics

Descriptions of the tadpoles of the following species were mentioned in previous studies (Hendrix et al 2007, Gawor et a 2009, Wildenhues et al 2010, Rauhaus et al 2012, Pham et al 2015):

Rhacophorus annamensis, Hynarana nigrovittata, Rhacophorus

maximus, Theloderma corticale, Amolops cremnobatus Le Thi Quy

(2015) described the tadpoles of 21 amphibian species from Bach Ma National Park, Thua Thien Hue Province

In addition, the bioacoustic analysis is a useful approach to study biology and taxonomy of amphibians Le Trung Dung (2016) described the biaocoustics of 11 amphibians species

1.2.4 Research on phylogenetic relationships

Frost et al (2006) provided a comprehensive phylogenetic tree of amphibian species of the world Li et al (2008, 2009), Biju et al (2010), Orlov et al (2012), Kuraishi et al (2012), Li et al (2012), Yu et al (2010, 2013), Nguyen et al (2015), Poyarkov et al (2015) studied on taxonomy and phylogenetic relationships of various groups of Rhacophoridae

1.2.5 Research on pathology and conservation issues

Rowley et al (2013), Nguyen et al (2013), Martel et al (2014), Laking et al (2017) and Nguyen et al (2017) have identified a number

of amphibian populations that infected with Batrachochytrium dendrobatidis and B salamandrivorans

Rowley et al (2010, 2016) assessed threats to the populations of amphibians in Southeast Asia, including Vietnam Key impacts include

habitat loss, overexploitation for food, medicinal and pet trade

1.2.6 Research on amphibians in northern Vietnam

Although numerous field excursions have been conducted in northern Vietnam, most of surveys were conducted in evergreen forests such as Tay Yen Tu, Tay Con Linh, Phia Oac-Phia Den, Hoang Lien, Muong Nhe, Sop Cop, and Copia nature reserves (Hecht et al 2013, Bain & Nguyen 2004, Nguyen Thien Tao 2009, Orlov et al 2001, Le Trung Dung 2016, Pham Van Anh 2016) Research in limestone karst ecosystems are still limited with descriptions of new species, namely

Tylototrion ziegleri from Cao Bang and Ha Giang provinces, Liuixalus calcarius and Philautus catbaensis from Cat Ba Island (Nishikawa et

al 2013, Milto et al 2013)

1.2.7 Research on Limnonectes and Odorrana in Vietnam

Genus Limnonectes: Limnonectes is one of the most diverse

groups of amphibians to date with 68 currently recognized species and

16 of which have been described in the last ten years (Frost 2017) According to Nguyen et al (2009), five species of the genus

Limnonectes are currently recorded from Vietnam However, some

taxonomic changes have been published in recent years Due to their morphological similarity, species that were previously thought to be widespread are now being recognized as complexes of species with

much narrower distributions

Genus Odorrana: Odorrana is one of the most diverse groups of

amphibians to date with 58 currently recognized species, more than 20

of which have been described in the last ten years (Frost 2017) Due to morphological similarity in the genus, species that were formally thought to be widespread are now being recognized as complexes of species with much narrower distributions Further study on taxonomic

and genetic relationships should be continued

1.3 Natural conditions of the study area

1.3.1 Natural conditions of North Vietnam

The North Vietnam bordered by China’s Guangxi Province to the northeast and Yunnan Province to the northwest, and by Laos along its western border (Sterling et al 2006)

Limestone kart forests: Most of the limestone mountain area in

Vietnam is distributed in northern Viet Nam, partly in Quang Binh province In the Gulf of Tonkin, there are thousands of limestone islands

in Ha Long Bay next to each other with Cat Ba Island as the center (Sterling et al 2006)

Vegetation: The dominant forest type in northern Vietnam is

evergreen, including both broad-leaved and coniferous plants, with pockets of semi-evergreen forest Coastal mangrove formations and forests growing on limestone are also important elements of the north’s

natural landscape diversity (Sterling et al 2006)

Fauna: Northern Vietnam’s animal communities are a mixture of

tropical and subtropical species, many of which are unique to the northern third of the country Within the region, the Red River may be

an effective barrier to movement (or coincide with one) for some groups, such as amphibians and reptiles, resulting in different species

and communities in the northeast and northwest (Sterling et al 2006)

1.3.2 Natural conditions of survey sites

Field surveys were conducted in the limestone forestin northern Vietnam

Northwest:

Ngoc Son-Ngo Luong Nature Reserve (Hoa Binh Province):

This NR is located in Tan Lac and Lac Son districts with a total area of 19.254 ha The area is characterized by limestone mountains, with steep terrain and rugged terrain Between the limestone mountains there are several flat valleys running in the north-west direction The altitude

ranges from 100-1.065 m (Birdlife International 2004)

Hang Kia-Pa Co Nature Reserve (Hoa Binh Province): Hang

Kia-Pa Co Nature Reserve is located in Mai Chau District with a total area of 5.257 ha There are many high and pointed limestone blocks, the highest peak of which is 1.536m in the Northwest of the area, the height decreasing to the East Most of the nature reserve stands at over

500 m (Birdlife International 2004)

Northeast:

Bac Me Nature Reserve (Ha Giang Province): This NR is located

in Bac Me District with a total area of 9.042 ha, Bac Me Nature Reserve is located in the depression of the Gam River to the south-east

of Ha Giang Province, with steep terrain and strong splinters with many peaks above 1000 m along the Song Gam gulf (Biodiversity Report Bac

Me Nature Reserve 2009)

Ha Lang Forest (Cao Bang Province): Ha Lang District has a

limestone karst topography that occupies most of the area, at an altitude

of 100-750 m above sea level According to the biodiversity conservation planning of Cao Bang Province, a nature reserve will be established in this district with an area of 7.343 ha (Decree No 697/QĐ-UBND)

Cat Ba National Park: Cat Ba is the largest island of the Cat Ba

Archipelago with a total area of 26.241 ha Cat Ba National Park is located in the limestone archipelago of hundreds of large and small islands at the height of 100-150 m, the highest point is Cao Vong peak 331m and the area of this protected area is 16.196 ha (www.vuonquocgiacatba.com.vn)

CHAPTER 2 MATERIALS AND METHODS 2.1 Field survey and study sites

Fifteen field surveys with 119 days were conducted from 2014 to 2017

Survey sites: Cat Ba National Park (Hai Phong City), Ha Lang

Disstrict (Cao Bang Province), Bac Me Nature Reserve (Ha Giang

Province), Hang Kia-Pa Co and Ngoc Son-Ngo Luong nature reserves

(Hoa Binh Province)

Sampling of Limnonectes and Odorrana: Twenty field surveys with

200 days were conducted in more than twenty provinces in Vietnam

from 2014 to 2017

Molecular analysis was carried out at the Institute of Ecology and

Biological Resources and Vietnam National Museum of Nature, and

Hanoi University of Science

2.2 Methods

2.2.1 Sampling

Excursions were carried out during the day and at night in different

habitat types

Survey transects were set up along the streams, pools, small ponds

or along the forest paths, under the leaf litter or on the tree branches, we

thus also survey the forest near the cave entrances and cliffs

2.2.2 Laboratory work

2.2.2.1 Morphological examination

Taxonomic identification: Morphological comparisons were made

with the voucher specimens which are deposited in the collections of

the Institute of Ecology and Biological Resources and Vietnam

National Museum of Nature For taxonomic identification, we used the

following documents: Bourret (1942), Bain et al (2003), Ohler et al

(2011), Orlov et al (2003, 2006, 2012), Suwannapoom et al (2016),

Taylor (1962), and othe related documents that were cited in each

species account Species names followed Nguyen et al (2009), Frost

(2017) and recently published papers

2.2.2.2 Molecular analysis

A fragment of mitochondrial gene (cytochrome b, 12S, 16S) was

sequenced to investigate phylogenetic relationships of all species of the

genus Limnonectes and Odorrana in Vietnam

The sequences were aligned using ClustalX v2.1 (Thompson et al 1997), selected the optimal model using Modeltest v3.7 (Posada and Crandal 1998), analyzed using Bayesian inference (BI) as implemented

in Mr.Bayes v3.1.2 (Ronquist et al 2012)

We used BI and maximum-likelihood (ML) approaches to reconstruct the mitochondrial gene tree (matrilineal genealogy) The analyses used a concatenation of COI and 16S rRNA sequences

2.2.3 Distribution patterns

Habitat: Species composition were assessed in different habitat types (agricultural and residential areas, disturbed natural forests, undisturbed natural forests)

Altitudinal gradient: We compared the species composition of amphibians between elevations below 800 m and above 800 m

Life modes: Species composition of amphibians was evaluated based on three life modes: on the trees, on the ground, and associated with water

2.2.4 Conservation status

Conservation status of threatened species was referred to the Vietnam Red Data Book (2007); IUCN Red List (2017); CITES appendices (2017); the Governmental Decree No 32/2006/ND-CP; and the Governmental Decree No 160/2013/ND-CP The endemic species of Vietnam are species that currenly known only from Vietnam

2.3 Materials

A total of 524 specimens of amphibians were collected in karst forests of the North Vietnam for morphorlogical analysis

A total of 148 specimens of Limnonectes and 232 specimens of Odorrana were collected in Vietnam for morphorlogical analysis

A total of 150 tissue samples, consisting of 46 tissue samples of

Limnonectes, 74 tissue samples of Odorrana, and 30 tissue samples of Liuixalus, Rhacophus, and Theloderma, were use for molecular analysis

Chapter 3 RESULTS AND DISCUSSION 3.1 Species composition of amphibians

3.1.1 List of recorded species

A collection of 524 specimens of amphibians was collected from different survey sites in the research areas

Species composition: A total of 65 species belonging to 30 genera, 8 families, 3 orders, comprising 44 species (26 genera, 7 families, 2 orders) recorded from Ngoc Son-Ngo Luong NR, 32 species (21 genera, 6 families, 1 orders) recorded from Hang Kia-Pa Co NR, 33 species (20 genera, 7 families,

2 orders) recorded from Bac Me NR, 21 species (12 genera, 5 families, 1 orders) recorded from Ha Lang District, and 23 species (15 genera, 5 families,

1 orders) recorded from Cat Ba NP (Table 3.1)

In terms of species diversity, Rhacophoridae is the most diverse family with 9 recorded genera and 21 recorded species (Figure 3.1)

Figure 3.1 Species diversity of amphibian families

Table 3.1 List of amphibians recorded in the research areas

1 Cóc nhà Duttaphrynus melanostictus (Schneider, 1799) + + + + +

2 Cóc rừng Ingerophrynus galeatus (Günther, 1864) +

Họ Cóc bùn Megophryidae Bonaparte, 1850

3 Cóc mày sa pa Leptobrachium chapaense (Bourret, 1937) + +

4 Cóc mày nhỏ Leptolalax minimus (Taylor, 1962) (**) + +

5 Cóc mày Leptolalax pelodytoides (Boulenger, 1893) + +

6 Cóc mày đêm Leptolalax nyx Ohler, Wollenberg,

Grosjean, Hendrix, Vences, Ziegler &

Dubois, 2011

+

7 Cóc núi Ophryophryne pachyproctus Kou, 1985 + +

8 Cóc núi miệng nhỏ Ophyryophryne microstoma Boulenger, 1903 +

9 Cóc mắt bên Megophrys major (Boulenger, 1908) + + +

Họ Nhái bầu Microhylidae Günther, 1858 +

10 Cóc đốm Kalophrynus interlineatus (Blyth, 1855) +

12 Nhái bầu bec-mo Microhyla berdmorei (Blyth, 1856) +

13 Nhái bầu bút-lơ Microhyla butleri Boulenger, 1900 + +

14 Nhái bầu hoa Microhyla fissipes Boulenger, 1884 (*) + + +

15 Nhái bầu Microhyla mukhlesuri Hasan, Islam,

Kuramoto, Kurabayashi & Sumida, 2014

+ +

16 Nhái bầu hây-môn Microhyla heymonsi Vogt, 1911 + + + + +

17 Nhái bầu vân Microhyla pulchra (Hallowell, 1861) + + + +

18 Nhái bầu trơn Micryletta inornata (Boulenger, 1890) + +

Họ Ếch nhái

chính thức

Dicroglossidae Anderson, 1871

19 Ngoé Fejervarya limnocharis (Gravenhost, 1829) + + + + +

20 Ếch đồng Hoplobatrachus rugulosus (Wiegmann, 1834) + + + + +

21 Ếch nhẽo ban-na Limnonectes bannaensis Ye, Fei & Jiang, 2007 + + + +

22 Ếch lim-boc Limnonectes limborgi (Sclater, 1892) (*) +

24 Ếch gai bau-len-go Quasipaa boulengeri (Gunther,1899) +

25 Ếch gai sần Quasipaa verrucospinosa (Bourret, 1937) + +

26 Cóc nước sần Occidozyga lima (Gravenhorst, 1829) + + +

27 Cóc nước mac-ten Occidozyga martensii (Peters, 1867) + +

Họ Ếch nhái Ranidae Rafinesque, 1814

28 Ếch bám đá Amolops ricketti (Boulenger, 1899) + + +

29 Chàng hiu Hylarana macrodactyla (Günther, 1858)(*) + +

30 Chàng đài bắc Hylarana taipehensis (Van Denburgh, 1909) + + +

32 Ếch xanh Odorrana chloronota (Günther, 1876) + + + +

33 Ếch bám đá hoa Odorrana geminata Bain, Stuart, Nguyen,

Che & Rao, 2009

+

34 Ếch hải nam Odorrana hainanensis Fei, Ye & Li, 2001(**) +

35 Ếch li-pu Odorrana lipuensis Mo, Chen, Wu, Zhang

& Zhou, 2015 (**)

+

36 Ếch đá mut-x-man Odorrana mutschmanni Pham, Nguyen, Le,

Bonkowski & Ziegler, 2016(***)

+

38 Ếch ti-an-nan Odorrana tiannanensis (Yang & Li, 1980) +

40 Chẫu chuộc Sylvirana guentheri (Boulenger, 1882) + + + + +

41 Chàng mẫu sơn Sylvirana maosonensis (Bourret, 1937) + +

Notes: (*)-New record for provinces, (**)-New record for Vietnam, (***)-New species Study sites:

1-Ngoc Son-Ngo Luong NR, 2-Hang Kia-Pa Co NR, 3-Bac Me NR, 4-Ha Lang District, 5-Cat Ba NP

3.1.2 New discoveries

- New species: Three new species were described as new for science: Odorrana mutschmanni from Cao Bang Province, Theloderma annae, Rhacophorus hoabinhensis from Hoa Binh Province

- New records for Vietnam: Three species were recorded for the first time from Vietnam: Leptolalax minimus from Hoa Binh Province, Odorrana hainanensis and O lipuensis from Cao Bang Province

- New provincial records: One species (Rhacophorus maximus) was

recorded for the first time from Cao Bang Province, two species

(Leptolalax minimus, Rhacophurus rhodopus) were recorded for first

42 Ếch suối meng-la Sylvirana menglaensis (Fei, Ye & Xie, 2008)(*) + +

Họ Ếch cây Rhacophoridae Hoffman, 1932 +

44 Nhái cây wa-za Gracixalus waza Nguyen, Le, Pham, Nguyen,

45 Nhái cây quang Gracixalus quangi Rowley, Dau, Nguyen,

Cao & Nguyen, 2011 (*)

+ +

46 Nhái cây nhỏ đá vôi Liuixalus calcarius Milto, Poyarkov, Orlov

& Nguyen, 2013

+

47 Nhái cây tay-lo Kurixalus bisacculus (Taylor, 1962) + + + + +

48 Nhái cây cát bà Philautus catbaensis Milto, Poyarkov,

Orlov & Nguyen, 2013

+

49 Ếch cây đầu to Polypedates megacephalus Hallowell, 1861 + + + + +

50 Ếch cây mi-an-ma Polypedates mutus (Smith, 1940) + + + + +

51 Nhái cây tí hon Raorchestes parvulus (Boulenger, 1893) + +

52 Ếch cây xanh đốm Rhacophorus dennysi Blanford, 1881 + +

53 Ếch cây phê Rhacophorus feae (Boulenger, 1893) +

54 Ếch cây ki-ô Rhacophorus kio Ohler & Delorme, 2006 + + + +

55 Ếch cây hòa bình Rhacophorus hoabinhensis Nguyen, Pham,

Nguyen, Eto & Ziegler, 2017(***)

+

56 Ếch cây lớn Rhacophorus maximus Günther, 1858 (*) +

57 Ếch cây oóc-lốp Rhacophorus orlovi Ziegler & Kohler, 2001 + + +

58 Ếch cây màng bơi đỏ Rhacophorus rhodopus Liu & Hu, 1962(*) +

59 Ếch cây sần an-na Thelodema annae Nguyen, Pham, Nguyen,

Ngo & Ziegler, 2016 (***)

+ +

60 Ếch cây sần đốm trắng Theloderma albopunctatum (Liu & Hu, 1962) + + + + +

61 Ếch cây sần bắc bộ Theloderma corticale (Boulenger, 1903)(*) + + + +

62 Ếch cây sần go-don Theloderma gordoni Taylor, 1962(*) +

63 Ếch cây sần đỏ Theloderma lateriticum Bain, Nguyen & Doan,

Bộ Không chân Gymnophiona Müller, 1831

Họ Ếch giun Ichthyophiidae Taylor, 1968

65 Ếch giun ban-na Ichthyophis bannanicus Yang, 1984 +

4 3

2 3

3 2

1 2

3