Journal of Threatened Taxa | www.threatenedtaxa.org | 12
September 2019 | 11(11): 14434–14451
A report
on the herpetofauna of Tengchong Section of Gaoligongshan National Nature Reserve, China
Jian-Huan Yang 1,
Xiang-Yuan Huang 2, Jian-Fang Ye 3, Shen-Pin Yang 4,
Xing-Chao Zhang 5 & Bosco
Pui-Lok Chan 6
1,6 Kadoorie
Conservation China, Kadoorie Farm & Botanic
Garden, Lam Kam Road, Tai Po, Hong Kong SAR, China.
2,3,4,5 Yunnan Gaoligongshan
National Nature Reserve (Tengchong Bureau), 157 Laifeng Avenue, Tengchong 679100,
Yunnan Province, China.
1 jhyang@kfbg.org (corresponding
author), 2 baohuqu_hxy@163.com, 3 bhsyjf@126.com, 4 2459746049@qq.com,
5 1169299359@qq.com, 6 boscokf@kfbg.org
Abstract: We present the results from a series of herpetological
surveys conducted in the Tengchong Section of Gaoligongshan National Nature Reserve, Yunnan Province,
China between April 2014 and November 2018.
A total of 59 species of amphibians and reptiles (one salamander, 30
batrachians, four lizards, and 24 snakes) were recorded during the surveys
including three newly described amphibian species and 17 new records for Tengchong, 10 of which also represent new generic records
for the area. Natural history notes of
some little-known species are presented.
Our survey results clearly demonstrate that the herpetofauna diversity
of this mountain range is still underestimated and warrants further systematic
study.
Keywords: Amphibians, ecology, new record, new species,
reptiles, species accounts, Yunnan.
doi: https://doi.org/10.11609/jott.4437.11.11.14434-14451
|
ZooBank: urn:lsid:zoobank.org:pub:F776600D-27E6-4DFF-9E80-0E4E4DF76491
Editor: Thomas Ziegler, University of Cologne, Köln, Germany. Date
of publication: 12 September 2019 (online & print)
Manuscript details: #4437 | Received 27 July 2018 |
Final received 27 June 2019 | Finally accepted 09 August 2019
Citation: Yang, J.-H., X.-Y. Huang, J.-F. Ye, S.-P. Yang, X.-.C. Zhang & B.P.-L. Chan (2019). A report on the herpetofauna of Tengchong
Section of Gaoligongshan National Nature Reserve,
China. Journal of Threatened Taxa 11(11): 14434–14451. https://doi.org/10.11609/jott.4437.11.11.14434-14451
Copyright: © Yang et al. 2019. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by adequate credit to the author(s)
and the source of publication.
Funding: This study is
funded by Kadoorie Farm and Botanic Garden.
Competing interests: The authors declare no competing
interests.
Author details: Jian-Huan Yang: Senior Conservation Officer of
Kadoorie Conservation China Department at Kadoorie Farm and Botanic Garden. Xiang-Yuan
Huang: Head of Research Department of Gaoligongshan
National Nature Reserve (Tengchong Bureau). Jian-Fang
Ye: Technical Officer of Gaoligongshan
National Nature Reserve (Tengchong Bureau). Shen-Pin
Yang: Forest ranger of Gaoligongshan National
Nature Reserve (Tengchong Bureau). Xing-Chao
Zhang: Technical Officer of Gaoligongshan
National Nature Reserve (Tengchong Bureau). Bosco Pui-Lok Chan: Head of Kadoorie
Conservation China Department at Kadoorie Farm and
Botanic Garden.
Author contribution: J-HY: conceived and designed the biodiversity survey, conducted field surveys,analyzed the data, contributed
reagents/materials/analysis tools, prepared figures and/ortables,
authored or reviewed drafts of the paper, approved the final draft. X-YH: conceived and designed the biodiversity
survey, conducted field surveys. J-FY:
conducted field surveys, contributed reagents/materials/analysis tools. S-PY: conducted field surveys, contributed reagents/materials/analysis
tools. X-CZ: conducted field surveys,
contributed reagents/materials/analysis tools.
BP-LC: conceived and designed the biodiversity survey, conducted field
surveys, authored or reviewed drafts of the paper.
Acknowledgements:
We greatly acknowledge Jian Wang,
Run-Lin Li, Jian Zhao, Hai-Long He, Hui-Quan Fu, Li-Yue Liu, Cheng-Kai Wang, Zhi-Hua Zhang, Guo-Liang Yang, as well as other colleagues
and wardens, for their great help during field surveys; Yun Li and Zhao-Chi
Zeng for their assistance on molecular work.
This study is funded by Kadoorie Farm and Botanic
Garden.
INTRODUCTION
The Gaoligongshan Mountains
(hereafter GLGS) is a sub-range at the southwestern end of the Hengduan Mountains, lying along the west bank of the Nujiang River (The Salween) in the western part of Yunnan
Province, China. GLGS is renowned for
its unique geography and significant biodiversity (Stattersfield
et al. 1998; Chaplin 2005; Dumbacher et al.
2011). The first herpetofauna research
of GLGS dates back to the 1860s when western zoologist John Anderson explored
the region (Anderson 1876, 1878).
Subsequent herpetological surveys were conducted from time to time by
Chinese herpetologists, yielding a number of new species endemic to the region
(Zhao & Yang 1997; Stotz et al. 2003; Yang &
Rao 2008; Fei et al. 2009; Chan & Bi 2016).
The Tengchong Section of Gaoligongshan National Nature Reserve (hereafter TC-GLGS)
refers to the reserve area within the Tengchong
county-level District, geographically located on the western slope of southern
GLGS draining the Irrawaddy River (24.933–25.833 0N). For more details of the geography and ecology
of Tengchong and the nature reserve, readers should
refer to Chan et al. (2019, this special issue). In April 2014, a biodiversity survey team,
led by Kadoorie Farm and Botanic Garden, started to conduct
a biodiversity inventory of TC-GLGS. We
herein provide a report on the herpetofauna of TC-GLGS based on our fieldwork.
MATERIALS AND METHODS
From April 2014 to November 2018, we conducted a
series of herpetological surveys in the following 10 sites in or adjacent to
TC-GLGS: Site 1: Nankang; Site 2: Xiaodifang;
Site 3: Dahaoping; Site 4: Hujianglin
(the protected riparian forest along Longchuan
River); Site 5: Linjiapu; Site 6: Tiantaishan;
Site 7: Xiaotianhe; Site 8: Dahetou;
Site 9: Dazhuba; and Site 10: Cizhuhe
(see Fig. 1). For detailed information
on survey sites see Table 1. We followed
the taxonomic treatments of Fei et al. (2009) and Frost (2018) for amphibians,
and Zhao et al. (1998, 1999) and Uetz et al. (2018)
for reptiles. Some voucher specimens are
temporarily kept at the herpetology collection of Kadoorie
Farm and Botanic Garden, Hong Kong [KFBG] for further studies, and others are
deposited at the Museum of Biology, Sun Yat-sen
University, Guangzhou [SYS]. For the
identification of species, references used include Yang (1991), Zhao et al.
(1998, 1999), Fei et al. (2005, 2009, 2012), Zhao (2006), Yang & Rao
(2008), Guo & Deng (2009), Fei & Ye (2016), Yang et al. (2016a, 2016b),
Yang & Huang (2019).
RESULTS
In total, we documented the presence of 59 species of
amphibians and reptiles in TC-GLGS, including one salamander, 30 batrachians,
four lizards and 24 snakes; voucher specimens were collected for all but 12
species (see Appendix 1 for the list of voucher specimens). Leptobrachium
tengchongense, Leptolalax
tengchongensis, and Scutiger
tengchongensis were revealed to be new species
described by our team (Yang et al. 2016a,b; Yang & Huang 2019). A further 17 species have not been previously
reported in TC-GLGS (Xue 1995; Yang & Rao 2008),
and 10 genera were new records for the area.
A species checklist of herpetofauna based on our survey is provided in
Table 2. Voucher photographs were taken
for all species recorded, a selection of species are illustrated below (Images
1–7). In the following, selected species
of special interest are dealt with in detail, including newly described
species, globally threatened species, unidentified species, and those with
taxonomic issues, and where our field data provided additional information on
natural history of little-known species.
Remarks
Tylototriton shanjing (Image 1a)
This is the only tailed amphibian known from Tengchong. It was
found at three sites during the surveys but is believed to be more widespread,
because outside breeding season it disperses into forests, which makes
detection difficult. From April to June
adults congregate to mate in clear puddles and pools in forest as well as
nearby farmland below 2,400m. The
taxonomic chaos between Tylototriton shanjing and its sister-taxon T. verrucosus
is still not fully resolved (Nishikawa et al. 2014; Khatiwada
et al. 2015), and the distribution boundary between these two species is not
determined (Fei et al. 2012; Fei & Ye 2016). In this paper, we retain the validity of T.
shanjing and regard the population in Tengchong as T. shanjing
following Fei et al. (2012). It is
collected as a traditional medicine in most of its range, and is listed as Near
Threatened in the IUCN Red List.
Bufo tuberospinius (Image 1d)
Compared with its sympatric congener B. gargarizans, this toad species is more common in
montane forest habitats up to 2,700m throughout TC-GLGS. It is associated with small streams where
adults breed and lay eggs in pool sections in between April and July. There has been much debate for the validity
of B. tuberospinius since its description;
while some researchers insisted B. tuberospinius
is a valid taxon (Yang et al. 1996; Yang & Rao 2008), others regarded it as
a synonym of B. burmanus distributed in northeastern Myanmar (Fei et al. 2005, 2009, 2012). This has not been fully resolved to date,
thus in this paper we retain the validity of B. tuberospinius
following Frost (2018).
Leptobrachium huashen (Image
2b)
This species is found in the southern portion of
TC-GLGS. Representatives of the genus Leptobrachium from TC-GLGS were previously
regarded as L. chapaensis (Yang 1991; Xue 1995; Yang & Rao 2008), but recent morphological
and molecular research has shown that the population consists of two distinct
species, namely L. huashen in the south and
the newly-described L. tengchongense from the
northern portion (Fei et al. 2005; Rao & Wilkinson 2008; Yang et al.
2016b).
Leptobrachium tengchongense (Image 2c)
This is a new species discovered by our team, which
occurs in the northern portion of TC-GLGS between 2,200–2,500 m (Yang et al.
2016b). According to our fieldwork the
two species of Leptobrachium from
TC-GLGS, L. huashen and L. tengchongense, are allopatric but their ecological
niches, distribution limits and contact zone require further
investigation. L. tengchongense
can be easily distinguished from L. huashen by
having a bicolored iris with upper parts light blue, while the iris is
uniformly dark brown in L. huashen; the black
bands on dorsal surfaces of the limbs are relatively wider in L. tengchongense than in L. huashen
(Yang et al. 2016b).
Leptolalax tengchongensis (Image 2d)
This species was described during a recent survey
(Yang et al. 2016a). Leptolalax
tengchongensis is characterized by having dorsal
skin scattered with fine, reddish tubercles; almost entirely black tympanum;
large black blotches present on flanks; iris not bicolored, uniform dark brown
and scattered with minute, coppery reticulations. Leptolalax
tengchongensis was found along a clear-water
rocky stream and nearby seepage in well-preserved montane moist evergreen
broadleaf forest at 2,100m at Site 5; male calls were heard during the April
and May surveys.
Leptolalax sp. (Image 2f)
This taxon was recorded along clear-water rocky
streams at Sites 3 and 5. At Site 3 male
calls were heard in March when night time air temperature was ca. 3°C. At Site 5, this species was sympatric with L.
tengchongensis, but can be easily distinguished
by the male advertisement calls (peak frequency of male calls 4.1–4.3 kHz in
Leptolalax sp. while 4.5–4.8 kHz in L.
tengchongensis; each call contains 4–6 notes in Leptolalax sp. while consisting of only two notes in
L. tengchongensis (Jian-Huan Yang, unpublished
data, 10 April 2019.) and morphology: L. tengchongensis
has a uniform dark brown iris in life, while Leptolalax
sp. has a bi-colored iris with orange-yellow
upper half and silvery white lower half.
Further molecular and morphological studies are needed to clarify the
taxonomic status of Leptolalax sp.
Leptolalax cf. ventripunctatus (Image 2e)
This species is temporarily allocated to L. ventripunctatus by having longitudinal skin folds on
dorsum; irregular black spots present on venter; dermal fringes on toes narrow;
flank with distinct black spots; and a bicolored iris with orange-yellow upper
half and silvery white lower half (Fei et al. 2009; Yang et al. 2018); however,
its peak frequency of male calls (6.8–7.1 kHz) is remarkably higher than those
of L. ventripunctatus from Yingjiang
county (6.1–6.4 kHz; see Yang et al. 2018).
Due to the great morphological similarity of Leptolalax
species (Rowley et al. 2015), further molecular analysis is needed in order to
obtain the accurate identification. This
is the first record of this species for Tengchong
while the two congeneric species L. tengchongensis
and Leptolalax sp. were recorded in
high-altitude montane areas above 2,100m in TC-GLGS, Leptolalax
cf. ventripunctatus was recorded at 1,360m
with subtropical climate/biome at Site 4.
Megophrys cf. minor
(Image 2g)
This small-sized Megophrys
species appears to be very common throughout TC-GLGS, and was recorded from all
surveyed sites between 2,000–2,300 m.
The cryptic behavior of this species makes
visual detection a real challenge, but male calls were commonly heard along
small streams and seepages in well-preserved forests at 1,900–2,300 m between
April and September. In view of the
taxonomic chaos of small-sized Megophrys in
southern China (Chen et al. 2017), we cannot easily assign this species to any
known species on the basis of morphology.
Further study incorporating molecular, morphological and acoustic
methods is needed to solve this problem.
In this paper, we temporarily allocate this species to Megophrys minor (see also Xue
1995; Yang & Rao 2008; Fei et al. 2009).
Oreolalax sp.
(Image 3a)
A sub-adult
and a juvenile were collected from Site 8 in May 2015. Subsequent molecular study revealed a sister
relationship to Oreolalax jingdongensis in the 16S rRNA gene fragment, but Oreolalax sp. still presents a certain degree of
genetic divergence (Jian-Huan Yang, unpublished data, 10 April 2019.). Morphological comparisons are not possible as
adult specimens with secondary sexual characteristics are lacking, which is
essential for species identification in this genus. Adult specimens are needed to clarify its
taxonomic status. Oreolalax sp. is a new
record for Tengchong.
Scutiger tengchongsnsis (Image 3b)
This species was described by our team during a
previous survey (Yang & Huang 2019).
S. tengchongensis is very distinct from
local anurans by dorsum having large conical-shaped and longitudinal tubercles
covered by numerous tiny black spines; adult males have a pair of pectoral
glands and a pair of axillary glands present on the chest, which are covered by
dense tiny black spines; adult males have inner three fingers with black
nuptial spines (Yang & Huang 2019).
It was found in streamlets and surrounding areas along the main ridge at
3,000m close to Site 7, which represents the southernmost distribution limit of
the genus Scutiger worldwide. Previous southernmost locality known for the
genus was in Fugong County of middle-GLGS, 145km
north of Site 7 (Fei & Ye 2016).
Amolops bellulus (Image 3d)
This torrent frog was found in large rocky streams in
well-preserved forest at elevations between 2100–2350 m, and currently is only
recorded in the northernmost portion of TC-GLGS at sites 8 and 10. This species can be easily distinguished from
other stream frogs by dorsum yellowish-brown above; lower flanks olive-green or
blueish-green; upper lips light brown and unspotted. Adults were usually found perching on rocks
and streamside bushes during surveys in May and June. This species is to date only recorded from
GLGS in Lushui County and Tengchong
City (Yang & Rao 2008; Fei et al. 2012).
Due to the lack of information about its distribution, population and
ecology, it is listed as Data Deficient in the IUCN Red List.
Amolops jinjiangensis
(Image 3e)
A new record for Tengchong,
this species is rarely recorded in TC-GLGS and has been only found twice from
Site 7 in August and October 2018.
During the survey in October, females were found being gravid and males
had distinct nuptial pads on fingers, suggesting they may be breeding at that
season. Molecular analyses revealed this
population to be identical with Amolops jinjiangensis: there was no genetic divergence in the
16S rRNA gene fragment between our specimens and a sequence of A. jinjiangensis from the Genbank
database (Genbank No. EF453741). The TC-GLGS population represents a new
distribution record of this rarely known species and is far away from its known
distribution areas in north-western Yunnan Province and adjoining areas in
Sichuan Province (Fei et al. 2009). A.
jinjiangensis is now listed as Vulnerable in
the IUCN Red.
Odorrana graminea (Image 4a)
A new record
for Tengchong, this large stream frog is widely
distributed in southern China and very common in stream areas (Fei et al.
2009); however, this species was only found at Site 4 (ca. 1400m), although
intensive surveys at other sites (mostly above 2000m) have been made,
suggesting that it may be restricted to relatively low altitude forest areas.
Polypedates braueri (Image 4c)
Recent molecular studies suggested that the species in
the Polypedates leucomystax
complex from Tengchong, which was previously
treated as P. megacephalus (Yang & Rao
2008; Fei et al. 2009), is actually P. braueri (Kuraishi et al. 2013; Pan et al. 2013).
Rhacophorus puerensis (Image 4d, 4e)
This species was recorded from the southernmost and
northernmost portions of TC-GLGS at Sites 1, 2 and 10 at 2,100–2,880 m
elevation, suggesting that it is widely distributed in TC-GLGS. During the breeding season from late April to
May, male calls were heard from the ground in puddle and grassland at forest
edge, and eggs were laid in foam nests in soft mud around still water. Due to the lack of information about its
distribution, population and ecology, it is listed as Data Deficient in the
IUCN Red List.
Gracixalus sp.
(Image 4h)
This is the first record of the genus Gracixalus from GLGS (Fei et al. 2009;
Fei & Ye 2016). Male calls of this
species were widely recorded from south to north in TC-GLGS during surveys
between April to July. The frogs were
very difficult to collect, however, because all males were calling from the upper
layers of small trees/shrubs ca. 3m from above the ground. Only one pair (one calling male and one
gravid female) was found together inside a small tree hole from Site 3 in May
2018. Subsequent molecular study revealed a sister relationship to Gracixalus tianlinensis
from northwestern Guangxi in the 16S rRNA gene
fragment, but Gracixalus sp. still presents a
certain degree of genetic divergence (Jian-Huan Yang, unpublished data, 10
April 2019). Detailed integrative
taxonomical studies incorporating morphological, molecular and acoustic data is
underway in order to clarify its taxonomic status.
Lycodon fasciatus (Image 6a)
One sub-adult specimen was collected from Site 7 in
October 2018, which matches the diagnosis of Lycodon
fasciatus by having one small preocular; loreal
elongate, not in contact with eye on left side while in narrow contact with eye
on right side; temporals: 2+3; supralabials eight, 2nd
to 4th ones touching the eye; dorsal scale rows 17:17:15, keeled on
dorsal rows 7–9; solid black above with 34 and 16 transverse pinkish-brown
bands (in 2–3 scales wide) on body and tail respectively; ventrals
195; and subcaudals 86, paired (Zhao et al. 1999; Zhao 2006).
Lycodon cf. septentrionalis (Image 6b)
A new record for Tengchong. One adult female specimen (snout-vent length
955mm, tail length 210mm) was collected from Site 7 in Oct 2018, which matches
the diagnosis of Lycodon septentrionalis by having one preocular; loreal not in
contact with eye; temporals: 2+2; supralabials seven,
3rd and 4th ones touching the eye; dorsal scale rows
17:17:15, smooth throughout the body (however, versus feebly keeled in the
original description); ventrals 221; subcaudals 74,
paired; solid black above with 29 and 13 narrow white transverse bands on body
and tail respectively (Zhao et al. 1999; Zhao 2006).
Rhabdophis himalayanus (Image 7a)
A new record for Tengchong. A single juvenile specimen (snout-vent length
256mm, tail length 78mm) was collected from Site 4 at 1,360m in June 2017,
which matches the diagnosis of Rhabdophis himalayanus by having one preocular, postoculars three; temporals: 2+2, supralabials
8/8, 4th and 5th touching the eye; dorsal scale rows
19:19:17; ventrals 163; subcaudals 82, paired; two
distinct narrow orange yellow transverse bands at nuchal region, narrow and
short dark brown transverse bands present on dorsum of body (Zhao 2006). In China, this rare species was previously
only known from southeastern Tibet and Gongshan County in northern GLGS (Zhao et al. 1999; Zhao
2006).
Ophiophagus hannah
A new record for Tengchong. Three adults were encountered at Site 4 at
1,360m between 13.00h and 16.00h on 9 May 2017.
Intensive surveys at other sites failed to detect this large-sized
species, suggesting that it may be restricted to relatively low altitude forest
areas in Tengchong.
Despite its wide distribution range worldwide, the King Cobra faces
great pressures from habitat loss and over-exploitation (Stuart et al. 2012),
and it is now listed as Vulnerable in the IUCN Red List.
Sinomicrurus kelloggi (Image
7c)
This is the first record of the genus Sinomicrurus from GLGS. A photo of an individual of Sinomicrurus species was taken by a TC-GLGS warden
at 2,020m from Site 3, but the specimen was not collected. The snake matches the diagnosis of Sinomicrurus kelloggi
by having reddish-brown dorsum and narrow transverse cross-bars above body and
tail, an inverted V shape of creamy white band present on head (Zhao et al.
1998; Zhao 2006). It is the third record
of the species from Yunnan Province (Yang & Rao 2008; Sun et al. 2015).
Pareas nigriceps (Image 7e)
This is a new generic record for GLGS. A single individual was recorded at Site 3 in
May 2015, found at night on shrub in old-growth forest at 2,050m. Pareas nigriceps is a newly-described snake species from
adjacent Xiaoheishan in Longling
County, with the type locality reported as 24.83671°N, 98.76185°E (2,067m) (Guo
& Deng 2009). Our record represents
the second documented locality for the species, and a slight northern range
expansion. Brief measurements and
scalation characters of the specimen: SYS r001222, SVL: 525.9mm; tail length:
133.1mm. Supralabials
7/7, 7th elongate and largest; infralabials 7/7; preocular one; subocular one; postocular absent;
temporals: 1+2; ventrals 184; subcaudals 73, paired;
dorsal scale rows 15:15:15, dorsal five rows slightly keeled; vertebrate scale
slightly enlarged. Due to the lack of
information on distribution, status and ecology of this recently described
species, it is listed as Data Deficient in the IUCN Red List.
Pareas sp.
(Image 7d)
A single specimen was collected from Site 9 which
cannot be allocated to any known species in the genus. Brief measurements and scalation characters
of the specimen: nasal one; loreal touching the eye; prefrontal touching the
eye; subocular and postocular
fused; infralabials seven; anterior temporals two, posterior temporials three; 11 middle rows of dorsal scales keeled at
mid-body; vertebral scales not enlarged; ventral scales 173; subcaudals 62,
paired. More specimens and genetic
analyses are needed to clarify the taxonomic status of this taxon.
DISCUSSION
Our survey greatly enhances our understanding of the
herpetofauna diversity of TC-GLGS, with discoveries of at least three species
new to science and a series of new regional records, including 10 new generic
records. A number of collected species
are yet to be thoroughly identified due to the lack of specimen series, and
some of these may prove to be new when more collections or genetic data become
available in the future. Information for
most recorded species can also be found in Chan & Bi (2016). Since we focused our efforts on well-protected
montane forests at the elevation band between 1900m and 3000m (see table 1), a
number of herpetofauna previously recorded from Tengchong
(Xue 1995; Zhao & Yang 1997; Yang & Rao 2008)
were not detected during our survey: Hoplobatrachus
rugulosus (Wiegmann), Microhyla heymonsi
Vogt, Hemidactylus bowringii
(Gray), Hemiphyllodactylus
yunnanensis (Boulenger),
Acanthosaura lepidogaster
(Cuvier), Calotes emma
Gray, Calotes jerdoni Günther, Sphenomorphus
incognitus (Thompson), S. maculatus
(Blyth), Ahaetulla prasina
(Boie), Atretium yunnanensis Anderson, Plagiopholis
blakewayi Boulenger, Ptyas korros
(Schlegel), P. mucosa (Linnaeus), Naja
kaouthia Lesson, and Trimeresurus
albolabris Gray. Most of these missing species occur at lower
elevations and/or in disturbed habitats, where we invested little survey
effort. Further surveys in these
habitats are needed to ascertain the current status and distribution of these
species. Our results clearly highlight
the fact that the herpetofauna of GLGS remains imperfectly studied and its
diversity is undoubtedly underestimated.
Future herpetological expeditions will probably uncover more exciting
findings in TC-GLGS, especially in higher altitude habitats of the reserve.
The natural forests of Gaoligongshan
National Nature Reserve have been well protected, and we found few
anthropogenic activities which are threatening the survival of amphibians and
reptiles, however, local populations of certain large-sized frogs are being
suppressed by over-collecting for human consumption, in particular Nanorana yunnanensis
which fetches high prices (USD 30–40 per kilogram) in local markets; its wild
population has declined dramatically and is now listed as Endangered in the
IUCN Red List. Our interviews also
revealed that local people opportunistically collect large “rat snakes” from
the genera Elaphe and Orthriophis
for consumption. Education outreach
targeting this issue is called for if populations of the affected species are
to recover to a natural level.
Table 1. Survey localities and dates in Tengchong Section of Gaoligongshan
National Nature Reserve for this study, sorted by latitude from south to north.
Site
no. |
Location |
Elevation
covered (m) |
Survey
dates |
Site 1 |
Nankang |
2,180 |
24–25.iv.2014 13–14.ix.2018 |
Site 2 |
Xiaodifang |
2,150–2,400 |
10.iii.2015 |
Site 3 |
Dahaoping |
2,020–2,400 |
23–24.ix.2014 11–12.iii.2015 |
|
|
|
15–17.v.2015 27–28.vii.2015 22–23.v.2018 |
Site 4 |
Hujianglin |
1,360 |
9.v.2016 24–26.vi.2017 |
Site 5 |
Linjiapu |
1,900–3,000 |
28–30.iv.2014 9–10.xii.2014
15–17.v.2015 |
Site 6 |
Tiantaishan |
1,850–2,300 |
29–30.vii.2015 |
Site 7 |
Xiaotianhe |
2,000–3,100 |
22–23.vi.2017 |
Site 8 |
Dahetou |
2,000–2,300 |
26–27.iv.2014 13–14.iii.2015 17–18.iii.2016 24.vii.2017 23–4.iii.2018 24–25.v.2018 |
Site9 |
Dazhuba |
2,070–2,200 |
20–21.v.2015 |
Site 10 |
Cizhuhe |
2,050–2,920 |
26–28.ix.2014 11–12.xii.2014 18–19.v.2015 31.vii.–1.viii.2015 20–21.iii.2016 10–11.v.2016 |
Table 2. Amphibians and reptiles recorded in Tengchong Section of Gaoligongshan
National Nature Reserve, 2014–2018. For site details refer to Table 1.
Taxon |
Chinese
common name |
Site
1 |
Site
2 |
Site
3 |
Site
4 |
Site
5 |
Site
6 |
Site
7 |
Site
8 |
Site
9 |
Site
10 |
AMPHIBIA |
|
|
|
|
|
|
|
|
|
|
|
Bombinatoridae |
|
|
|
|
|
|
|
|
|
|
|
Bombina
maxima (Boulenger,
1905)* |
´óõëÁåó¸* |
|
|
|
|
|
|
|
|
|
X |
Bufonidae |
|
|
|
|
|
|
|
|
|
|
|
Bufo gargarizans Cantor,
1842* |
Öлªó¸òÜ* |
|
|
|
|
|
|
|
X |
|
X |
Bufo tuberospinius
(Yang, Liu & Rao, 1996) |
ð༬Ϫó¸ |
|
|
X |
|
X |
|
X |
X |
X |
X |
Duttaphrynus melanosticus (Schneider,
1799) |
ºÚ¿ôó¸òÜ |
|
|
X |
X |
|
|
|
|
|
|
Dicroglossidae |
|
|
|
|
|
|
|
|
|
|
|
Fejervarya multistriata (Hallowell,
1861) |
ÔóÍÜ |
|
|
|
X |
|
|
X |
|
|
|
Nanorana yunnanensis (Anderson,
1879) |
Ë«Íż¬ÐØÍÜ |
|
X |
X |
|
X |
X |
X |
X |
X |
X |
Hylidae |
|
|
|
|
|
|
|
|
|
|
|
Hyla annectans (Jerdon, 1870) |
»ªÎ÷ÓêÍÜ |
|
|
|
X |
|
X |
X |
X |
X |
X |
Megophryidae |
|
|
|
|
|
|
|
|
|
|
|
Brachytarsophrys feae (Boulenger,
1887) |
·ÑÊ϶ÌÍÈó¸ |
|
|
X |
|
|
|
|
|
|
|
Leptobrachium huashen Fei & Ye, 2005 |
»ªÉîÄâ÷Úó¸ |
|
|
X |
|
X |
|
|
|
|
|
Leptobrachium tengchongense Yang, Wang
& Chan, 2016** |
ÌÚ³åÄâ÷Úó¸** |
|
|
|
|
|
|
X |
X |
|
X |
Leptolalax tengchongensis
Yang, Wang, Chen & Rao, 2016** |
ÌÚ³åÕÆÍ»ó¸** |
|
|
|
|
X |
|
|
|
|
|
Leptolalax
cf. ventripunctatus Fei, Ye & Li, 1990* |
¸¹°ßÕÆÍ»ó¸* |
|
|
|
X |
|
|
|
|
|
|
Leptolalax sp.* |
ÕÆÍ»ó¸ÊôÒ»ÖÖ* |
|
|
X |
|
X |
|
|
|
|
|
Megophrys glandulosa Fei, Ye
& Huang, 1990 |
ÏÙ½Çó¸ |
|
|
X |
X |
X |
|
X |
X |
X |
X |
Megophrys
cf. minor Stejneger, 1926 |
С½Ç󸣨Ôݶ¨£© |
|
X |
X |
|
X |
X |
X |
X |
X |
X |
Oreolalax
sp.* |
³Ýó¸ÊôÒ»ÖÖ* |
|
|
|
|
|
|
X |
X |
|
X |
Scutiger tengchongensis Yang
& Huang, 2019** |
ÌÚ³å³ÝÍ»ó¸** |
|
|
|
|
|
|
X |
|
|
|
Microhylidae |
|
|
|
|
|
|
|
|
|
|
|
Microhyla fissipes Boulenger, 1884 |
ÊÎÎƼ§ÍÜ |
|
|
X |
X |
|
|
|
|
|
|
Ranidae |
|
|
|
|
|
|
|
|
|
|
|
Amolops bellulus Liu, Yang,
Ferraris & Matsui, 2000 |
ÀöÍÄÍÜ |
|
|
|
|
|
|
|
X |
|
X |
Amolops jingjiangensis Su,
Yang & Li, 1986* |
½ð½ÍÄÍÜ* |
|
|
|
|
|
|
|
X |
|
|
Amolops viridimaculatus
(Jiang, 1983) |
Â̵ãÍÄÍÜ |
|
|
X |
|
X |
|
X |
X |
|
|
Babina pleuraden (Boulenger, 1904) |
µáÍÜ |
X |
X |
X |
|
X |
X |
X |
X |
|
X |
Odorrana andersonii (Boulenger, 1882) |
ÔÆÄϳôÍÜ |
|
X |
|
X |
X |
|
X |
X |
X |
X |
Odorrana graminea (Boulenger, 1900)* |
´óÂ̳ôÍÜ* |
|
|
|
X |
|
|
|
|
|
|
Rana
chaochiaoensis Liu,
1946 |
ÕѾõÁÖÍÜ |
|
|
X |
|
X |
|
X |
X |
|
X |
Rhacophoridae |
|
|
|
|
|
|
|
|
|
|
|
Gracixalus
sp.* |
ÏËÊ÷ÍÜÊôÒ»ÖÖ* |
|
|
X |
|
|
|
|
X |
X |
X |
Polypedates braueri (Vogt, 1911) |
²¼ÊÏÊ÷ÍÜ |
|
|
X |
X |
|
X |
X |
X |
X |
X |
Rhacophorus
burmanus (Andersson,
1939) |
ÃåµéÊ÷ÍÜ |
|
|
X |
|
X |
|
|
X |
X |
X |
Rhacophorus
puerensis
(He, 1999) |
ÆÕ¶©Ê÷ÍÜ |
X |
X |
|
|
|
|
|
|
|
X |
Rhacophorus
rhodopus Liu
& Hu, 1960 |
ºìõëÊ÷ÍÜ |
|
|
X |
X |
|
|
X |
X |
|
|
Salamandridae |
|
|
|
|
|
|
|
|
|
|
|
Tylototriton shanjing Nussbaum,
Brodie & Yang, 1995 |
ºìñ§ðàó¢ |
X |
|
X |
|
|
|
|
|
|
X |
REPTILIA |
|
|
|
|
|
|
|
|
|
|
|
Agamidae |
|
|
|
|
|
|
|
|
|
|
|
Japalura yunnanensis Anderson,
1878 |
ÔÆÄÏÅÊòá |
X |
|
X |
|
X |
|
X |
|
|
|
Pseudocalotes kakhienensis (Anderson,
1879) |
°öÎ÷ÄâÊ÷òá |
|
|
|
|
|
|
X |
|
|
|
Scincidae |
|
|
|
|
|
|
|
|
|
|
|
Scincella doriae (Boulenger,
1887)* |
³¤Ö«»¬òá* |
X |
|
X |
|
|
|
|
|
|
|
Sphenomorphus indicus
(Gray, 1853) |
Ó¡¶ÈòÑòá |
X |
|
|
|
|
X |
X |
|
|
|
Colubroidea |
|
|
|
|
|
|
|
|
|
|
|
Archelaphe bella (Stanley, 1917)* |
·½»¨Ð¡Í·Éß* |
|
|
X |
|
|
|
|
X |
|
|
Coelognathus
radiatus (Boie, 1827) |
È©Ë÷½õÉß |
|
|
|
X |
|
|
|
|
|
|
Elaphe carinata (Günther,
1864) |
Íõ½õÉß |
|
|
|
|
|
X |
X |
X |
|
|
Hebius octolineatum (Boulenger, 1904) |
°ËÏ߸¹Á´Éß |
|
|
|
|
|
|
|
X |
X |
X |
Hebius modestum (Günther,
1875) |
¸¹°ß¸¹Á´Éß |
|
|
|
|
|
|
|
X |
X |
|
Lycodon fasciatus (Anderson,
1879) |
Ë«È«Á´Éß |
|
|
X |
|
|
|
|
X |
|
|
Lycodon cf.
septentrionalis (Günther, 1875)* |
°×Á´Éß* |
|
|
|
|
|
|
|
X |
|
|
Oreocryptophis porphyraceus (Cantor,
1839) |
×ϻҽõÉß |
|
|
X |
|
|
|
|
X |
|
|
Orthriophis taeniurus (Cope,
1861) |
ºÚü½õÉß |
|
|
X |
|
|
|
X |
X |
|
|
Psammodynastes pulverulentus (Boie, 1827) |
×ÏÉ°Éß |
|
|
|
X |
|
|
|
|
|
|
Pseudoxenodon macrops (Blyth, 1855) |
´óÑÛбÁÛÉß |
|
|
X |
|
|
|
X |
X |
|
X |
Ptyas nigromarginata
(Blyth, 1854) |
ºÚÏßÎÚÉÒÉß |
|
|
|
X |
|
|
|
|
|
|
Rhabdophis leonardi (Wall,
1923) |
Ãåµé¾±²ÛÉß |
|
|
X |
|
X |
|
X |
X |
X |
X |
Rhabdophis himalayanus (Günther,
1864)* |
ϲɽ¾±²ÛÉß* |
|
|
|
X |
|
|
|
|
|
|
Rhabdophis subminiatus (Schlegel,
1837) |
ºì²±¾±²ÛÉß |
|
|
|
X |
|
|
|
|
|
|
Sibynophis collaris (Gray, 1853) |
ºÚÁì½£Éß |
|
|
|
|
|
|
|
X |
|
|
Elapidae |
|
|
|
|
|
|
|
|
|
|
|
Bungarus multicinctus Blyth,
1861 |
Òø»·Éß |
|
|
X |
|
|
|
|
|
|
|
Ophiophagus hannah (Cantor, 1836)* |
ÑÛ¾µÍõÉß* |
|
|
|
X |
|
|
|
|
|
|
Sinomicrurus kelloggi (Pope,
1928)* |
¸£½¨ÀöÎÆÉß* |
|
|
X |
|
|
|
|
|
|
|
Pareatidae |
|
|
|
|
|
|
|
|
|
|
|
Pareas sp.* |
¶ÛÍ·ÉßÊôÒ»ÖÖ* |
|
|
|
|
|
|
|
|
X |
|
Pareas nigriceps Guo &
Deng, 2009* |
ºÚ¶¥¶ÛÍ·Éß* |
|
|
X |
|
|
|
|
|
|
|
Viperidae |
|
|
|
|
|
|
|
|
|
|
|
Ovophis monticola (Günther,
1864) |
ɽÀÓÌúÍ· |
|
|
X |
|
X |
X |
X |
X |
X |
X |
Protobothrops jerdonii (Günther,
1875)* |
²Ë»¨ÀÓÌúÍ·* |
|
|
X |
|
|
|
X |
|
X |
|
Trimeresurus yunnanensis Schmidt,
1925 |
ﮀ셖񦂈 |
|
|
|
|
X |
|
X |
X |
|
|
Remarks: Species
distribution is based on our own field data, and do not represent true
distribution range of these species in Tengchong
Section of Gaoligongshan National Nature Reserve.
* represents newly recorded species for Tengchong (refers to Xue 1995;
Yang & Rao 2008); ** represents new species discovered during the surveys.
For
figure & images – click here
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Appendix 1. Voucher specimens
collected during the survey. See materials and methods for museum
abbreviations.
Bombina maxima: SYS a003798–3800, coll. 18 May 2015, from Site 10 by
Jian-Huan Yang (JHY, hereafter); KFBG 14446–14447, coll. 18 May 2015, from Site
10 by JHY.
Bufo tuberospinius: SYS a003811, coll. 17 May 2015, from Site 3 by Jian
Wang (JW, hereafter); KFBG 14350, coll. 27 July 2015, from Site 3 by JHY.
Duttaphrynus melanosticus: KFBG 14457, coll. 25 June 2017, from Site 4 by JHY.
Nanorana yunnanensis: SYS a003763, coll. 18 May 2015, from Site 5 by JHY;
SYS a003796, coll. 17 May 2015, from Site 3 by JW; SYS a003843–3844, coll. 18
May 2015, from Site 10 by JHY; KFBG 14117, coll. 13 March 2015, from Site 8 by
JHY.
Hyla annectans: SYS a003816–3818, coll. 22 May 2015, from Site 10 by
JHY.
Leptobrachium huashen: SYS a003751–3752, coll. 15 May 2015, from Site 5 by
JHY; SYS a003779–3781, coll. 17 May 2015, from Site 3 by JW; KFBG 14301–14302,
coll. 15 May 2015, from Site 5 by JHY.
Leptobrachium tengchongense: SYS a004603, coll. 13 March 2015, SYS a004623–4627,
coll. 17–18 March 2016, from Site 8, by YJH; SYS a004628–4632, coll. 20–21
March 2016, from Site 10, by JHY.
Leptolalax tengchongensis: SYS a004956, coll. on 29 April 2014, SYS
a004957–4602, coll. on 16 May 2015, from Site 5, by JHY
Leptolalax cf. ventripunctatus: KFBG 14462–14464, coll. 25 June 2017, from Site 4 by
JHY.
Leptolalax sp.: KFBG
14111–14115, coll. on 11 March 2015, from site 3 by JHY; KFBG 14295–14296, coll.
on 15 May 2015, from Site 5 by JHY.
Megophrys glandulosa: SYS a003757–3758, SYS a003762, coll. 15 May 2015,
from site 5 by JHY; SYS a003792–3795, coll. 17 May 2015, from Site 3 by JW.
Megophrys cf. minor: SYS a003755, SYS a00376–3761, SYS a003767, coll. 15
May 2015, from Site 5 by JHY; SYS a003782–3798, coll. 17 May 2015, from Site 3
by JW; SYS a003821–3827, SYS a003837–3839, coll. 18 May 2015, from Site 10 by
JHY.
Oreolalax sp.: KFBG
14356–14357, coll. 18 May 2015, from Site 10 by JHY.
Scutiger tengchongensis: SYS a005793–5797, coll. on 22 June 2017, from Site
7, by JHY and Shen-Pin Yang (SPY).
Microhyla fissipes: KFBG 14354, coll. 17 July 2015, from Site 3 by JHY;
KFBG 14465, coll. 9 May 2016, from Site 4 by JHY.
Amolops bellulus: KFBG 14425–14427, coll. 11 May 2016, from Site 10 by
JHY.
Amolops jinjiangensis: KFBG 14561–14567, coll. 20 October 2017, from Site
8, by SPY.
Amolops viridimaculatus: SYS a003753–3754, coll. 15 May 2015, from Site 5 by
JHY; SYS a003797, SYS a003812–3813, coll. 17 May 2015, from Site 3 by JW.
Babina pleuraden: SYS a003775–3778, coll. 17 May 2015, from Site 3 by
JW.
Odorrana andersoni: SYS a003820, SYS a003831–3834, coll. 18 May 2015,
from Site 10 by JHY.
Odorrana graminea: KFBG 14429, coll. 9 May 2016, from Site 4 by JHY.
Rana chaochiaoensis: SYS a003819, coll. 18 May 2015, from Site 10 by JHY;
KFBG 14460–14461, 29 April 2014, from Site 5 by JHY.
Gracixalus sp.: KFBG 14558–15559, coll. 22 May 2018, from
Site 3 by JHY.
Polypedates braueri: SYS a003770, SYS a003774, SYS a003814–3815 coll. 17
May 2015, from Site 3 by JW; SYS a003835–3836, SYS a003841–3842, coll. 18 May
2015, from Site 10 by JHY.
Rhacophorus rhodopus: KFBG 14352--14353, coll. 27 July 2015, from Site 3
by JHY.
Rhacophorus burmanus: SYS a003764, coll. 15 May 2015, from Site 5 by JHY;
SYS a003829–3830, SYS a003840, coll. 18 May 2015, from Site 10 by JHY.
Rhacophorus puerensis: SYS a003771–3772, coll. 17 May 2015, from Site 3 by
JW.
Tylototriton shanjing: SYS a003768–3769, coll. 17 May 2015, from Site 3 by
JW.
Japalura yunnanensis: SYS r001215, coll. 15 May 2015, from site 5 by JHY;
SYS r001220, coll. 17 May 2015, from Site 3 by JW; KFBG 14389–14390, coll. 15
May 2015, from Site 5 by JHY.
Pseudocalotes kakhienensis: KFBG 14391–14392, coll. February 2018, from Site 7
by SPY.
Scincella doriae: KFBG 14361, coll. 24 April 2014, from Site 1 by JHY;
KFBG 14362, coll. 17 May 2015, from Site 3 by JW.
Sphenomorphus indicus: KFBG 14459, coll. February 2018, from Site 7 by SPY.
Archelaphe bella: KFBG 14466–14467, coll. 23 May 2018, from Site 3 by
JHY.
Hebius octolineatum: SYS r001223, coll. 18 May 2015, from Site 10 by JHY;
SYS r001225, coll. 20 May 2015, from Site 9 by JHY.
Hebius modestum: KFBG 14557,
coll. 11 May 2018, from Site 7 by SPY.
Lycodon fasciatus: KFBG 14578,
coll. 22 October 2018, from Site 7 by SPY.
Lycodon cf. septentrionalis: KFBG 14579, coll. 22 October 2018, from Site 7 by
SPY.
Oreocryptophis porphyraceus: KFBG 14576, coll. 13 July 2018, from Site 7 by SPY.
Psammodynastes pulverulentus: KFBG 14456, coll. 25 June 2017, from Site 4 by JHY.
Pseudoxenodon macrops: KFBG 14450, coll. June 2017, from Site 3 by Philip
Lo; KFBG 14451, coll. 13 March 2015, from Site 7 by JHY.
Rhabdophis leonardi: SYS r001221, Dahaoping;
SYS r001224, Site 9; KFBG 14344, coll. September 2014, from Site 8 by JHY; KFBG
14345, coll. 20 May 2015, from Site 9 by JHY; KFBG 14346, coll. 27 April 2014,
from Site 8 by JHY; KFBG 14347, coll. 17 May 2015, from Site 10 by JHY; KFBG
14348, coll. on 19 July 2015, from Site 8 by JHY.
Rhabdophis himalayanus: KFBG 14458, coll. 25 June 2017, from Site 4 by JHY.
Pareas sp.: KFBG 14360,
coll. 20 May 2015, from Site 9 by JHY
Pareas nigriceps: SYS r001222, coll. 17 May 2015, from Site 3 by JW.
Ovophis monticola: SYS r001217, coll. 15 May 2015, from Site 5 by JHY.
Protobothrops jerdonii: SYS r001218, coll. 17 May 2015, from Site 3 by JW.
Trimeresurus yunnanensis: SYS r001216,
coll. 15 May 2015, from Site 5 by JHY.