New records of amphibians from Thuong Tien Nature Reserve, Hoa

Herpetology Notes, volume 7: 51-58 (2014) (published online on 4 February 2014)
New records of amphibians from Thuong Tien Nature Reserve,
Hoa Binh Province, Vietnam
Vinh Quang Luu1,4,5,*, Canh Xuan Le2, Huy Quang Do1, Tuoi Thi Hoang3,
Truong Quang Nguyen2,4, Michael Bonkowski4 and Thomas Ziegler4,5
Abstract. Six species of amphibians are reported for the first time from Thuong Tien Nature Reserve, Hoa Binh Province,
Vietnam: Babina chapaensis, Kurixalus bisacculus, Theloderma asperum, Rhacophorus kio, R. feae, and Tylototriton
asperrimus. These new findings bring the total number of amphibian species to 33 in Thuong Tien Nature Reserve.
Keywords. Ranidae, Rhacophoridae, Salamandridae, distribution, taxonomy, Hoa Binh Province.
Introduction
In their recent checklist Nguyen, Ho and Nguyen
(2009) recorded a total of 177 species of amphibians
from Vietnam. Since then new country records and new
species descriptions of amphibians have been regularly
published from the country (e.g., Ziegler and Nguyen,
2010; Nguyen et al., 2012, 2013; Luu et al., 2013). These
new discoveries clearly underscore the underestimated
diversity of amphibians in Vietnam, particularly in
remote areas. Thuong Tien Nature Reserve is located
between the Kim Boi and Lac Son districts in the Hoa
Binh Province, in northwestern Vietnam, covering an
area of 7,308 hectares of montane evergreen forest
(Figs. 1, 2A). The topography of Thuong Tien Nature
Reserve is characterized by medium-high mountains,
which reach elevations of over 1,000 m (Tordoff et al.,
2004). Although this protected area was established in
2000, the herpetofauna of Thuong Tien Nature Reserve
is still poorly studied. Hoang and Luu (2009) recently
provided the first preliminary list of 27 amphibian
species from this area. As a result of additional field
surveys conducted in Thuong Tien Nature Reserve in
2009, we herein report six new records of amphibians
from this natural reserve as well as from Hoa Binh
Province.
Material and Methods
­ Department of Wildlife, Faculty of Natural Resource and
Environmental Management, Vietnam Forestry University,
Xuan Mai, Chuong My, Hanoi, Vietnam.
E-mail: [email protected]
2
Institute of Ecology and Biological Resources, Vietnam
Academy of Science and Technology, 18 Hoang Quoc Viet
Road, Hanoi, Vietnam. E-mail: [email protected]
3
­ Biodiversity Center, Faculty of Natural Resource and
Environmental Management, Vietnam Forestry University,
Xuan Mai, Chuong My, Hanoi, Vietnam.
E-mail: [email protected]
4
Zoological Institute, University of Cologne, Zülpicher Strasse
47b, D-50674 Cologne, Germany.
E-mail: [email protected]
5
AG Zoologischer Garten Köln, Riehler Strasse 173, D-50735
Cologne, Germany. E-mail: [email protected]
*
Corresponding author
1
Field surveys were conducted in the Thuong Tien
Nature Reserve (NR) by V. Q. Luu, L. D. Phan, L. X.
Tran, H. K. Can, T. Bui, T. H. Nguyen, T. V. Ninh, C. H.
Nguyen (VQL et al.) from 5 March to 28 April and from
20 to 28 July 2009. Field surveys had previously been
conducted by VQL et al. from 22 February to 14 April
2008 at elevations below 500 m a.s.l. and additional
surveys in 2009 were carried out at elevations between
500 and 720 m a.s.l. After taking photographs, the
specimens were anaesthetized, fixed in 40-70% ethanol
and subsequently stored in 70% ethanol. Specimens
were deposited in the collection of the Vietnam Forestry
Univeristy (VFU), Hanoi, Vietnam.
Measurements were taken with a digital calliper to
the nearest 0.1 mm. Abbreviations are as follows: a.s.l.:
above sea level; SVL (snout-vent length): from tip of
52
Vinh Quang Luu et al.
Figure 1. Map showing the Thuong Tien Nature Reserve, Hoa Binh Province, in northern Vietnam.
snout to anterior margin of cloaca; TaL (tail length):
from posterior margin of cloaca to tip of tail; HL (head
length): from the rear of the lower jaw to the tip of the
snout; HW (maximum head width): at commissure of
jaws; SN: distance from tip of snout to nostril; EN:
distance from front of eye to nostril; terminology of
morphological characters followed Nguyen et al. (2012)
for anurans and Nguyen et al. (2009) for salamanders.
Statistic analyses were performed with the PAST
Statistics software version 2.17 (Hammer et al., 2001).
The Sorensen coefficient was used to compare the
similarity of the species compositions between Thuong
Tien NR and nearby karst formations in the northwestern
region. The lists of amphibian species from nearby
protected areas were obtained from the literature, i.e.,
Nguyen et al. (2003) for Cuc Phuong National Park
(Ninh Binh Province), Nguyen et al. (2000) for Hang Kia
– Pa Co NR (Hoa Binh Province), and Le et al. (2008)
for Ngoc Son – Ngo Luong NR (Hoa Binh Province).
This index is measured by the following formula:
djk = 2M / (2M+N)
in which M is the number of species occurring in
both regions and N is the total number of species with
presence in just one region.
Results
Ranidae
Babina chapaensis (Bourret 1937)
Chapa Frog / Chang sa pa (Fig. 2B)
Specimens examined. Two adult males (VFU
A.2009.12-13) collected on 27 April 2009 by VQL et
al. in Doi Thung 1 forest, Quy Hoa Commune, Tan Lac
District (N 20o36.995’, E 105o29.256’), at an elevation
of ca. 680 m a.s.l.
Morphological characters. SVL 47.2-48.2 mm;
head longer than wide (HL18.1-18.7 mm, HW 16.617.0 mm); canthus rostralis distinct; nostril directed
laterally; loreal region concave; tympanum visible,
rounded; supratympanic fold distinct; vomerine
teeth present; tongue notched posteriorly; vocal sacs
present in males. Forelimbs: relative length of fingers:
II<I=IV<III; fingers free of webbing; tips of fingers
rounded, without discs; dermal fringe along outer finger
absent; palmar tubercles distinct; nuptial pad present in
males. Hindlimbs: toes long and thin, relative length of
toes: I<II<V<III<IV; toes less than half webbed; tips
of toes rounded; dermal fringe along outer toe absent;
subarticular tubercles present; inner metatarsal tubercle
present, outer metatarsal tubercle indistinct. Skin: dorsal
New records of amphibians from Thuong Tien Nature Reserve, Vietnam
53
Figure 2. A) Habitat of evergreen forest in Thuong Tien Nature Reserve; B) Chapa Frog Babina chapaensis; C) Taylor’s
Treefrog Kurixalus bisacculus; D) Thao Whipping Frog Rhacophorus feae; E) Black-webbed Treefrog Rhacophorus kio; F)
Hill Garden Bug-eyed Frog Theloderma asperum. Photos: V. Q. Luu.
surface of head and body smooth; dorsolateral fold
distinct; lateral head and flanks smooth; a small fold
present along arm; ventral surface smooth. Coloration
in life: head and dorsum light brown with a cream
vertebral stripe, edged in dark brown, running from
between the eye to vent; posterior part of dorsum with
some dark spots; upper jaw with a cream stripe, from
below the nostril to axilla; dorsolateral fold yellowish
brown, edged in black laterally; upper part of tibia and
thigh with dark bars; venter cream (determination after
Bourret, 1942; Chuaynkern et al., 2010).
Distribution. In Vietnam, this species has been known
from Lao Cai, Bac Giang, Ha Tinh, Kon Tum, Gia Lai,
Dak Lak provinces. Elsewhere, this species has been
54
reported from Laos and Thailand (Nguyen, Ho and
Nguyen, 2009). This is the first record of B. chapaensis
from Thuong Tien NR as well as from Hoa Binh
Province.
Natural history notes. Specimens were collected
between 21:00 and 21:30 while sitting on a stone in a
rocky stream. The surrounding habitat was evergreen
forest at elevation of ca. 680 m a.s.l.
Rhacophoridae
Kurixalus bisacculus (Taylor 1962)
Taylor’s Treefrog / Ech cay tay-lo (Fig. 2C)
Specimens examined. Two adult males (VFU
A.2009.14-15) collected on 27 April 2009 by VQL et
al. in Doi Thung 1 forest, Quy Hoa Commune, Tan Lac
District (N 20o36.360’, E 105o29.353’, at an elevation
of ca. 750 m a.s.l.).
Morphological characters. SVL 32.7-33.7 mm; head
as long as wide (HL 10.9-11.3 mm, HW 11.9-12.2 mm);
snout pointed at tip; loreal region concave; tympanum
enlarged, rounded; supratympanic fold distinct;
vomerine teeth present; tongue notched posteriorly;
vocal sacs present in males. Forelimbs: relative length
of fingers: I<II<IV<III; tip of fingers enlarged into large
discs; webbing basal; dermal fringe along outer finger
and palmar tubercles present; nuptial pad enlarged.
Hindlimbs: toes with enlarged discs; relative length of
toes: I<II<III=V<IV; toes three-fourths webbed, first
and second toes less than half webbed; dermal fringe
along outer toe present; subarticular tubercles visible;
inner metatarsal tubercle present; outer metatarsal
tubercle absent. Skin: dorsal surface of head, occiput,
eyelids, and dorsum with several tubercles; flanks
with bigger tubercles; ventral skin, upper part of thigh,
and cloacal region granular. Coloration in life: Dorsal
surface brown with large moss green regions; dorsal
limbs with dark bars; ventral surface cream with brown
dots on belly; underside of limbs brown with small light
dots (determination after Taylor, 1962).
Distribution. Yu et al. (2010) stated that previous
records of Kurixalus verrucosus in Vietnam should be
referred to K. bisacculus. In Vietnam, K. bisacculus
has been recorded from Lao Cai and Ha Giang in the
North southwards to Thua Thien-Hue and Gia Lai
provinces (Nguyen, Ho and Nguyen, 2009). Elsewhere,
this species is known from China, Laos, Thailand, and
Cambodia (Yu et al., 2010). This is a new record for
Thuong Tien NR as well as for Hoa Binh Province.
Vinh Quang Luu et al.
Natural history notes. Specimens were found between
21:20 and 21:30 on tree leaves, approximately 1 m
above the forest floor, at an elevation of ca. 750 m a.s.l.
Rhacophorus feae Boulenger 1893
Thao Whipping Frog / Ech cay phe (Figs. 2D)
Specimen examined. One adult male VFU A.2009.1
collected by VQL et al. on 25 April 2009 in evergreen
forest near Doi Thung 1 area, Quy Hoa Commune,
Lac Son District (N 20o35.702’, E 105o29.619’), at an
elevation of ca. 650 m a.s.l.
Morphological characters. SVL 75.4 mm; head
longer than wide (HL 26.3 mm, HW 25.2 mm); canthus
rostralis distinct; loreal region concave; tympanum
visible, supratympanic fold distinct; vomerine teeth
present; tongue rounded posteriorly; vocal sac present
in the male. Forelimbs: relative length of fingers:
I<II<IV<III; tip of fingers enlarged into large discs,
rounded; webbing completed; dermal fringe along outer
finger well developed; palmar tubercles present; nuptial
pad present. Hindlimbs: toes with enlarged discs; relative
length of toes: I<II<III=V<IV; toes fully webbed; dermal
fringe along outer toe present; subarticular tubercles
indistinct; inner metatarsal tubercle present. Skin: dorsal
surface of head, body and limbs smooth; ventral surface
of belly and thighs granular. Coloration in life: dorsal
surface of head, body, and limbs green; lateral head with
a yellow stripe on each side, from nostril through above
orbit and tympanum to axilla; webbing greenish yellow;
belly and lower thighs purplish brown; lower lip, throat,
chest, and ventral surface of limbs white (determination
after Boulenger, 1893; Orlov, Nguyen and Ho, 2008).
Distribution. In Vietnam, R. feae has been recorded
from Lai Chau, Lao Cai, Kon Tum, Dak Lak, Lam
Dong, and Dong Nai provinces. Elsewhere, this species
is known from China, Myanmar, Laos, and Thailand
(Nguyen, Ho and Nguyen, 2009; Frost, 2013). Our
finding represents the first record for Thuong Tien NR
as well as for Hoa Binh Province.
Natural history notes. The specimen was collected
at 22:00 on a banana leaf, ca. 1 m above a stream in
evergreen forest, at an elevation of ca. 650 m a.s.l.
Rhacophorus kio Ohler and Delorme 2006
Black-webbed Treefrog / Ech cay ki-o (Fig. 2E)
Specimens examined. One adult male and one adult
female (VFU A.2009.2 and VFU 2009.3) collected by
VQL et al. on 27 April 2009 in evergreen forest near Doi
Thung 1 area, Quy Hoa Commune, Lac Son District (N
New records of amphibians from Thuong Tien Nature Reserve, Vietnam
20o41.230’, E 105o28.812’), at an elevation of 580 m
a.s.l.
Morphological characters. SVL 68.7-74.3 mm; head
longer than wide (HL 24.7-25.2 mm, HW 21.4-24.5
mm); snout acute; canthus rostralis circular; loreal
region moderately convex; nostrils rounded, closer to
the tip of snout than to the orbit (SN 4.1-5.0 mm, EN
5.4-6.6mm); tympanum rounded, visible; vomerine
teeth present; tongue rounded posteriorly; vocal sac
present in the male. Forelimbs: relative length of fingers:
I<II<IV<III; tips of fingers enlarged into rounded discs;
webbing well developed; dermal fringe along outer
finger present; palmar tubercles indistinct; nuptial pad
present. Hindlimbs: tibia longer than femur and foot
length; relative length of toes: I<II<III<V<IV; toes fully
webbed; dermal fringe along outer toe well developed;
subarticular tubercles present, rounded; inner metatarsal
tubercle indistinct. Skin: dorsal and ventral skin smooth.
Coloration in life: Dorsal surface of head, body and
upper zone of flank green with white dots, lower lateral
part dark brown with yellow spots; forearm proximately
green and yellowish with small white dots; thigh orange
yellow posteriorly; dermal fringes on toes and fingers
yellowish white; ventral surface yellow, webbing
orange with an ink black spot at base; nuptial pad yellow
(determination after Ohler and Delorme, 2006).
Distribution. In Vietnam, R. kio has been known from
Lao Cai and Cao Bang in the North southwards to Kon
Tum and Gia Lai provinces. Elsewhere, this species has
been recorded from eastern India, China, Laos, Thailand,
and Cambodia (Nguyen, Ho and Nguyen, 2009; Frost,
2013). This is the first record of the species from Thuong
Tien NR as well as for Hoa Binh Province.
Natural history notes. Specimens were found at 14:00
on tree leaves, ca. 5-6 m above a small pond, at an
elevation of 580 m a.s.l.
Theloderma asperum (Boulenger 1886)
Hill Garden Bug-eyed Frog / Ech cay san a-x-po (Fig.
2F)
Specimens examined. One adult male VFU A.2009.11
collected on 21 July 2009 by VQL et al. in Suoi Doi
forest, Quy Hoa Commune, Lac Son District (N
20o36.242’, E 105o29.003’), at an elevation of ca. 650
m a.s.l.
Morphological characters. SVL 34.5 mm; head wider
than long (HW 13.1 mm, HL 12.1 mm); canthus rostralis
indistinct; loreal region concave; tympanum enlarged,
supratypanic fold absent; vomerine teeth present;
tongue notched posteriorly; vocal sacs present in the
55
male. Forelimbs: relative length of fingers: I<II<IV<III;
tips of fingers enlarged into large discs; webbing basal;
dermal fringe along outer finger absent; palmar tubercles
present; nuptial pad present. Hindlimbs: toes with
enlarged discs; relative length of toes: I<II<III=V<IV;
toes about three-fourths webbed; dermal fringe along
outer toe absent; subarticular tubercles distinct; inner
metatarsal tubercle present. Skin: dorsal and lateral skin
covered by tubercles with whitish granular asperities;
chin nearly smooth; ventral surface with large granules;
under thighs smooth. Coloration in life: dorsal surface
of head and body bluish grey with a small brown
line between eyes; posterior part of body with a large
chocolate area; dorsal surface of forelimbs chocolate
with small light dots; dorsal surface of hindlimbs
brown with cream markings; ventral surface cream
(determination after Taylor, 1962; Inger, Orlov and
Darevsky, 1999; Bain and Nguyen, 2004).
Distribution. T. asperum has been reported from Lai
Chau and Ha Giang provinces in the North southwards
to Lam Dong and Dong Nai provinces in the South of
Vietnam (Nguyen, Ho and Nguyen, 2009; Frost, 2013).
Elsewhere, this species is known from India, China,
Myanmar, Laos, Thailand, Cambodia, and Malaysia
(Nguyen, Ho and Nguyen, 2009). This is a new record
for Thuong Tien NR as well as for Hoa Binh Province.
Natural history notes. The specimen was collected at
22:00 while jumping on the forest floor in evergreen
forest at an elevation of 720 m a.s.l.
Salamandridae
Tylototriton asperrimus Unterstein 1930
Granular Newt / Ca coc san (Figs. 3A, B)
Specimen examined. One adult male (VFU A.2009.25)
and one adult female (VFU A.2009.8) collected on 24
July 2009 in Cot Ca forest, Quy Hoa Commune, Lac Son
District (N 20o37.059’, E 105o29.300’), at an elevation
of 720 m a.s.l.
Morphological characters. SVL 61.2-71.3 mm, tail
length TaL 67.7-71.7 mm; head wider than long (HL
14.3-17.0 mm, HW 16.9-20.4 mm); snout short, blunt,
projecting anteriorly beyond lower jaw; glandular ridge
on midline of crown from above anterior edge of eye
to middle of head; glandular ridge on outer margin of
crown from above eye to base of parotoid gland; parotoid
glands enlarged, projecting posteriorly; vertebral
tubercular ridge well-developed, from posterior end of
crown to base of tail; a dorsolateral row of 15-17 large
glandular warts present on each side from axilla to
56
Vinh Quang Luu et al.
Natural history notes. The specimens were found
between 15:00 and 17:00 in a pond (ca. 3-4 m in diameter
and water level about 0.3 m in depth) in evergreen
forest. Several juveniles were seen in the pond in July,
at an elevation of 720 m a.s.l.
Discussion
Figure 3. Granular Newt Tylototriton asperrimus A) dorsal
view and B) ventral view. Photos: V. Q. Luu.
base of tail, smaller posteriorly; dorsal skin with small
tubercles; throat and chest granular; belly with striations
perpendicular to body axis; fingers free of webbing; toes
with a web-remnant at base; tail laterally compressed,
tail tip pointed. Coloration in life: Body dark brown;
dorsal margin of tail, outer margin of upper and lower
surface of finger and toe tips, upper surface of fingers
and toes, cloacal region continuing to ventral ridge of
tail yellowish orange (determination after Nguyen et al.,
2009; Nishikawa, Matsui and Nguyen, 2013).
Distribution. Nishikawa, Matsui and Nguyen (2013)
referred the populations of Tylototriton from Cao Bang
and Ha Giang in northern Vietnam to a newly described
species, namely T. ziegleri. Elsewhere, this species is
known only from China (Nguyen, Ho and Nguyen,
2009). This is the first record of the species for Thuong
Tien NR and for Hoa Binh Province.
1
The new records bring the total number of amphibian
species to 33 in Thuong Tien NR, comprising 5
species of Megophryidae, 3 species of Bufonidae,
1 species of Hylidae, 9 species of Microhylidae, 8
species of Dicroglossidae, 9 species of Ranidae, and
15 species Rhacophoridae (Fig. 4). Nguyen, Ho and
Nguyen (2009) reported 27 anuran species from Hoa
Binh Province, including Microhyla berdmorei (Blyth
1856) from Thuong Tien NR and Odorrana andersonii
Boulenger 1882 and Chiromantis vittatus Boulenger
1887 from adjacent areas. However, voucher specimens
of these species have not been found during our field
surveys in Thuong Tien NR in 2008 and 2009. Statistic
analyses showed that the species composition of the
amphibian fauna of Thuong Tien NR is most similar to
that of Hang Kia – Pa Co NR (djk = 0.750) with 21
species recorded in both areas whereas it is only 0.593
between Cuc Phuong NP and Ngoc Son – Ngo Luong
NR (see Table 1). It is expected that additional new
records and even new species will be discovered from
Hoa Binh Province in future. Sterling, Hurley and Le
(2006) indicated that a wild range of elevations and the
complexity of landforms have given the northwestern
region of Vietnam a great diversity of natural habitats
and a high level of biodiversity potential. For instance,
north of the Hoa Binh Province, the Hoang Lien
National Park (Lao Cai Province) harbours a total of 63
species of amphibians, including one newly recorded
genus and five new species have been described since
2000 (Nguyen, Ho and Nguyen, 2009; Nguyen et al.,
2013).
Table 1. Similarity (Sorensen coefficient index) of the species composition of the amphibian
Table 1. Similarity (Sorensen coefficient index) of the species composition of the amphibian fauna between Thuong Tien NR and
2 fauna between Thuong Tien NR and nearby protected areas in northwestern Vietnam.
nearby protected areas in northwestern Vietnam.
Thuong Tien
Cuc Phuong Hang Kia - Pa Co
Ngoc Son (Hoang and
(Nguyen et
(Nguyen et al.,
Ngo Luong
Luu, 2009;
al., 2003)
2000)
(Le et al., 2008)
this study)
Thuong Tien
1
Cuc Phuong
0.688
1
Hang Kia - Pa Co
0.750
0.593
1
Ngoc Son - Ngo Luong
1
0.746
0.738
0.632
Protected area
3
New records of amphibians from Thuong Tien Nature Reserve, Vietnam
57
Figure 4. Species richness of amphibian families from Thuong Tien Nature Reserve (new records marked in red).
Acknowledgements. We are grateful to the directorates and staffs
of Thuong Tien NR for support of our field work. We thank L. D.
Phan, L. X. Tran, H. K. Can, T. Bui, T. H. Nguyen, T. V. Ninh,
and C. H. Nguyen (Hanoi) for their assistance in the field. Many
thanks to A. Ohler (Paris) for commenting on our manuscript, and
E. Sterling (New York) and K. Koy (Berkeley) for providing the
map. Field work in Thuong Tien NR was funded by IDEAWILD
for V. Q. Luu. Research of V. Q. Luu in Germany is funded by the
Ministry of Education and Training of Vietnam (MOET, Project
911) and the German Academic Exchange Service (DAAD).
Research of T.Q. Nguyen in Germany is funded by the Alexander
von Humboldt Stiftung/Foundation (VIE 114344).
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Accepted by Diogo Provete