DEAR EDITOR,
Species of Xenophrys are conserved morphologically and live primarily in forests.
In Thailand, the genus harbors many cryptic species. Herein we report the collection
of specimens from Doi Inthanon, Chiang Mai Province, northern Thailand, which were
identified previously as X. minor. Molecular and morphological analyses find that
these specimens differ significantly from other known congeners, and therefore we
describe a new species. Further, our phylogenetic analyses indicate that X. latidactyla
is a junior synonym of X. palpebralespinosa.
The Indo-Burma and Sundaland biodiversity hotspots span Thailand and host a high diversity
of amphibian species (Myers et al., 2000). In Thailand, at least 32 of 193 species
of amphibians appear to be endemic (Frost, 2019). Some recent studies of Megophrys
sensu lato, Leptobrachella and Fejervarya have shown that the diversity of amphibians
in Thailand is underestimated (Chen et al., 2017, 2018; Suwannapoom et al., 2016).
Further, 10 new species of amphibians have been discovered in the past three years
alone (Frost, 2019; Pawangkhanant et al., 2018; Poyarkov et al., 2018; Suwannapoom
et al., 2018). Thus, the extensively rich amphibian diversity in Thailand appears
to remain underestimated. Like many other regions, high rates of deforestation owe
to increased development (Royal Forest Department, 2006) and this drives a high risk
of extinction even before the discovery of new species.
GenusXenophrysGünther, 1864 (family Megophryidae) occurs in the southern and eastern
Himalayas, Indochina, and northward to the Qinling and Huangshan mountains of mainland
China (Chen et al., 2017). Of the 66 species, Thailand has seven species only: X.
aceras, X. lekaguli, X. longipes, X. major, X. minor, X. parva and X. takensis(Chan-ard,
2003; Mahony, 2011; Nutphund, 2001; Stuart et al., 2006). Xenophrys minor Stejneger
was described originally from Kwanghsien (now Guan Xian, Dujiangyan City), 55 kilometers
northwest of Chengtu (Chengdu), Szechwan (Sichuan), China. Several researchers recorded
it for montane areas of northern Thailand (Chan-ard, 2003; Chuaynkern & Chuaynkern,
2012; Nabhitabhata et al., 2000; Nabhitabhata and Chan-ard, 2005). Several recent
publications revised the X. minor complex (Li et al., 2014; Mahony et al., 2013; Wang
et al., 2012). Further, the type locality occurs in Sichuan, China and a distance
of over 1 500 km separates them from the known localities in northern Thailand. Thus,
the taxonomic status of Thai populations previously referred to as X. minor requires
further investigations.
Our recent fieldwork in Thailand resulted in the collection of specimens of Xenophrys
cf. “minor” from Chiang Mai Province (Doi Inthanon). Further phylogenetic analyses
of mtDNA sequences and morphological examinations showed that this species is distantly
related to X. minor from China and can be distinguished from all known congeners
both by molecular and morphological characters. Based on an integrative taxonomic
approach, we describe this population as a new species of the genus Xenophrys.
Six individuals were collected from Doi Inthanon, Chiang Mai Province, Thailand in
August 2017 (Figure 1). After specimens were euthanized using benzocaine, liver tissue
was taken and preserved in 95% alcohol. The specimens were fixed with 10% formalin
for 24 hours and subsequently transferred to 70% ethanol. All specimens were deposited
in the herpetological collection of the Museum of the Kunming Institute of Zoology
(KIZ), Chinese Academy of Sciences (CAS) and University of Phayao (AUP). Six preserved
adult specimens were examined and measured to the nearest 0.1 mm using digital calipers.
Morphological terminology followed Fei et al. (2009) and Poyarkov et al. (2017) (Supplementary
Methods).
Figure 1
Known distribution of Xenophrys angka sp. nov. from Doi Inthanon, Chiang Mai Province,
Thailand
A: Map of Thailand; B: Inset map of northern Thailand. Star shows the type locality
of the new species. Photo by N.A. Poyarkov.
Whole genomic DNA was extracted, and a partial fragment of the mitochondrial 16S rRNA
were amplified and sequencing. DNA extraction, primers and PCR cycle protocols are
in Supplementary Methods. Matrilineal genealogies were reconstructed to study the
phylogenetic relationships among Xenophrys based on the partial mitochondrial 16S
rRNA gene. Homologous sequences of related species of Xenophrys, and those of the
outgroups Leptobrachella oshanensis, L. ventripunctata, Leptobrachium boringii, Megophrys
nasuta, and M. baluensis, were downloaded from GenBank (Supplementary Table S1).
Trees were reconstructed using maximum likelihood (ML) and Bayesian inference (BI)
(Supplementary Methods). Apart from tree-based methods, we also calculated row pairwise
sequence divergence using uncorrected p-distances implemented in MEGA v6.0.6 (Tamura
et al., 2013).
The results of the ML and BI analyses yielded essentially identical topologies with
relatively high nodal support values for most terminal nodes (Figure 2). The tree
resolved monophyly of Xenophrys with two major lineages, corresponding to the subgenera
Xenophrys sensu stricto and Panophrys (Figure 2). Xenophrys cf.“minor” from Chiang
Mai Province assigned to Panophrys and phylogenetic relationships within which remained
essentially unresolved. The Chiang Mai population ofXenophrys cf.“minor” was a strongly
supported lineage (BPP=1, BS=100; Figure 2), which different notably from X. minor
sensu stricto from China (Figure 2). Genetic distance between the Chiang Mai population
and other species of Xenophrys ranged from 4.5% (X. rubrimera, subgenus Panophrys)
to 14.4% (X. mangshanensis, subgenus Xenophrys) (Supplementary Table S2). The tree
nested X. latidactyla within the radiation of X. palpebralespinosa with high support
(BPP=1.0, BS=94) (Figure 2). The genetic divergence between X. latidactyla and X.
palpebralespinosa was 0.9%.
Figure 2
BI tree resulting from 541 bp length fragment of mitochondrial 16S rRNA gene for
Xenophrys species and outgroups
Bayesian posterior probabilities (BPP)>95%/ML inferences (ML-BS)>70% are shown for
each node. Hyphen (“-”) denotes a Bayesian posterior probabilities<95% and bootstrap
support<70%.
The Chiang Mai population ofXenophrys cf.“minor” differs in a number of taxonomically
important diagnostic characters from other congeners, including X. minor from China.
Thus, both mtDNA and morphological analyses clearly indicate that this population
represents a separately evolving lineage and an undescribed species, which we describe
below.
Xenophrys angka
sp. nov.
Figures 3–4; Table 1.
Chresonymy:
Xenophrys minor (partim) — Chan-ard, 2003; Nabhitabhata and Chan-ard, 2005; Nabhitabhata
et al., 2000; Chuaynkern and Chuaynkern, 2012.
Figure 3
Holotype Xenophrys angka sp. nov. (KIZ040591, field number AUP-00074, female) in life
A: Dorsal view; B: Ventral view; C: Head, lateral view; D: Volar view of the left
hand; E: Plantar view of the left foot. Photos by N.A. Poyarkov.
Figure 4
Type series of Xenophrys angka sp. nov. in life
A: Holotype KIZ040591, female; B: Paratype AUP-00055, female; C: Paratype AUP-00077,
male. Photos by N.A. Poyarkov and C. Suwannapoom.
Table 1
Measurements (in mm) of type series of Xenophrys angkasp. nov.
KIZ
040591*
KIZ
040592
AUP-00076
AUP-00055
KIZ
040595
AUP-00077
Sex
F
F
F
F
M
M
SVL
38.2
37.5
38.2
39.2
32.1
31.2
HDL
12.9
12.8
12.7
13.0
11.3
11.5
HDW
12.3
12.6
12.4
12.6
10.5
11.0
SNT
4.2
4.4
4.0
4.1
3.5
3.7
DNE
1.8
1.7
1.7
1.8
1.4
1.5
IND
3.4
3.2
3.7
3.7
3.1
3.3
IOD
3.3
3.2
3.2
3.5
3.0
2.7
UEW
3.4
3.1
3.2
3.2
2.5
2.9
ED
4.1
4.0
4.2
4.1
3.9
3.7
TD
2.3
1.8
1.8
2.3
1.7
1.8
TED
2.0
1.4
1.4
2.1
1.5
1.3
SN
2.1
2.5
2.4
2.2
2.0
2.1
IFE
6.2
6.4
6.6
6.6
5.3
5.3
IBE
10.4
10.1
10.0
9.6
9.0
9.2
FAL
7.8
8.0
7.4
8.6
6.4
6.4
HL
9.4
9.7
9.7
9.3
8.7
8.6
THL
17.6
18.5
18.1
17.6
14.8
14.0
TL
18.7
18.8
18.7
18.6
16.0
15.5
FL
15.7
16.8
17.2
16.5
15.6
14.3
IMTL
1.6
2.4
1.9
1.7
1.4
1.7
FLI
3.6
3.5
3.6
3.8
3.5
3.9
FLII
4.1
4.1
4.1
4.2
3.8
4.1
FLIII
6.2
6.3
6.4
6.5
6.0
6.5
FLIV
4.4
4.2
4.2
4.4
4.1
4.3
TLI
2.1
2.3
2.2
2.2
2.4
2.3
TLII
4.2
4.4
5.0
4.6
4.2
3.9
TLIII
7.0
6.1
6.9
7.0
6.0
5.6
TLIV
9.8
10.1
10.4
10.4
8.7
8.2
TLV
5.3
5.5
5.6
5.1
4.7
4.0
For abbreviations, see text and Supplementary Methods. Asterisk (*) indicates holotype.
F: Female; M: Male.
Holotype:KIZ040591, an adult female collected from Kiew Mae Pan nature trail in Doi
Inthanon, Chiang Mai Province, Thailand (N18.556187°, E98.482229°; elevation 2 190
m a.s.l.), collected by Chatmongkon Suwannapoom, Parinya Pawangkhanant and Nikolay
A. Poyarkov on 29, August, 2017.
Paratypes:Two males KIZ040595 and AUP-00077, three females KIZ040592, AUP-00076 and
AUP-00055; collected at the same locality and same collection information as the holotype.
Diagnosis:
Xenophrys angka
sp. nov. is a member of genus Xenophrys based on the following combination of morphological
characters: head large, somewhat narrow and comparatively non-compressed, angular;
tympanum distinct; vertical pupil; transverse skin fold at head basis absent; no large
horny spines on dorsum; and two narrow glandular mid-dorsal ridges present, forming
X, H or Y-shaped figure (Chen et al., 2017). The following combination of characters
diagnoses the new species: (1) small body size, adult snout-vent length (SVL) 31.2–32.1
mm in males (n=2), 37.5–39.2 mm in females (n=4); (2) tympanum distinct and circular;
(3) vomerine ridges indistinct and vomerine teeth absent; (4) maxillary teeth present;
(5) tongue heart-shaped, not notched posteriorly; (6) supratympanic fold distinct,
extending from the posterior corner of eye to shoulder; (7) webbing between toes rudimentary;
(8) lateral fringes on toes absent; (9) tibio-tarsal articulation reaching the area
between eye and snout tip; (10) nuptial pads present on finger I; (11) subarticular
tubercles present on the base of fingers I–II, but absent on fingers III–IV; (12)
subarticular tubercle present at base of toes I, absent on toes II–IV; (13) heels
meeting or overlapping when tibias positioned at right angle to body axis; (14) inner
metatarsal tubercle big, outer metatarsal tubercle absent; (15) protruding projection
posterior to cloaca of males present; (16) dorsal surface with a complete dark brown
interorbital triangle with light blotch in the middle and two distinct thin opposing
“V”-shaped reddish glandular ridges with ridge on dorsum; (17) orange coloration of
groin contrasting with surrounding regions on males; and (18) inner metacarpal tubercle
and outer metatarsal tubercles distinct reddish color.
Description of holotype (measurements in Table 1) : KIZ040591, sexually mature female,
body habitus stocky (Figure 3), body size small (SVL=38.2 mm); head large (head length
(HDL)/SVL 33.8%, maximum head width (HDW)/SVL 32.2%), slightly longer than wide (HDW/HDL
95.3%); triangular in dorsal view; top of head flat; snout short (snout length (SNT)/HDL
32.6%) and wide (the distance between anterior orbital borders (IFE)/HDW 50.4%), snout
obtusely pointed in dorsal view (Figure 3A), sharply protruding in profile, without
rostral appendage, notably projecting beyond lower jaw ( Figure 3C); loreal region
vertical and concave; canthus rostralis distinct, sharp; dorsal region of snout flattened;
eyes large (eye diameter (ED)/HDL 31.8%); slightly protuberant in dorsal view and
notably protruding in profile (Figure 3), eye less than twice as long as maximum tympanum
diameter (tympanum diameter (TD)/ED 56.1%) and subequal to snout length (ED/SNT 97.6%);
eye-tympanum distance less than maximum tympanum diameter (tympanum–eye distance (TED)/TD
87.0%); tympanum distinct, circular in shape, relatively small (TD/HDL 17.8%), eye
diameter notably larger than tympanum diameter (ED/TD 178.3%); nostril rounded, laterally
orientated, nostril closer to anterior corner of eye than to tip of snout (distance
from nostril to eye (DNE)/snout–nostril distance (SN) 85.7%); internarial distance
equal to width of upper eyelid (internarial distance (IND)/width of upper eyelid (UEW)
100.0%), slightly larger than interorbital distance (IND/interorbital distance (IOD)
103.0%); pineal ocellus not visible externally (Figure 3A); tongue heart-shaped, not
notched posteriorly; vomerine ridges indistinct and vomerine teeth absent; maxillary
teeth present; pupil diamond-shaped (Figure 3C), vertical.
Forelimbs moderately long and robust; forearm not enlarged, length shorter than hand
length (forearm length (FAL)/hand length (HL) 83.0%); fingers long and narrow, not
flattened dorsoventrally, lateral fringes on fingers absent, relative finger lengths:
I<II<IV<III; tips of all fingers rounded, slightly dilated relative to digit widths,
with circular pads, terminal grooves absent; no webbing between fingers; a large subarticular
tubercle present at base of fingers I–II, absent on fingers III–IV; more distal subarticular
tubercles absent, replaced by low callous dermal ridges; supernumerary tubercles absent;
inner metacarpal tubercle big, oval, outer metacarpal tubercle small, flattened (Figure
3D).
Hindlimbs long and robust, thigh length shorter than tibia length (thigh length (THL)/tibia
length (TL) 94.1%), but greater than foot length (THL/foot length (FL) 112.1%); tibio-tarsal
articulation of straightened limb reaching eye level; heels slightly overlapping when
tibias positioned at right angles to body axis; toes long and slightly dorsoventrally
flattened, relative toes lengths: I<II<V<III<IV; tips of all toes rounded, slightly
dilated, terminal grooves absent; notably expanded relative to digit widths forming
circular pads; terminal grooves absent; lateral dermal fringes on absent; rudimentary
webbing present between all toes; tarsal fold absent; subarticular tubercle present
at base of toes I, absent on toes II–IV, replaced by indistinct callous dermal ridges;
inner metatarsal tubercle large, ca. 1.5x longer than wide, oval-shaped; and outer
metatarsal tubercle absent (Figure 3E).
Dorsal surface of body and both dorsal and lateral surfaces of head weakly granular;
several large distinct warts scattered on flanks; horn-like tubercle and several smaller
tubercles at edge of eyelids present; and supratympanic fold distinct, glandular,
starting immediately at posterior corner of upper eyelid (palpebrum) and running posteriorly
towards dorsal edge of tympanum, where it sharply curves ventrally becoming more prominent
and swollen and gently continues towards axilla. Dorsolateral folds well-developed,
glandular, almost straight, running from scapular region posteriorly towards sacral
region becoming less distinct and interrupted posteriorly; two opposing “V”-shaped
glandular skin folds present on dorsum joined by a ca. 10 mm long dorsomedial fold
in a hourglass-shape (Figure 3A); dorsal surfaces of limbs with small tubercles forming
distinct transverse skin folds on hindlimbs and irregular reticulate folds on forelimbs;
ventral surfaces of limbs, chest, abdomen and throat smooth; pectoral glands prominent,
rounded, located closely to axilla (Figure 3D); femoral glands small, oval-shaped,
positioned on posterior surface of thighs closer to groin than to the knee.
Color of the holotype in life:Coloration of holotype in life shown in Figure 3 and
Figure 4A. In life, dorsal surface light brown with olive green tint, with a complete
dark brown inverted triangle with light-ochre central blotch present between eyes;
all small tubercles and glandular ridges on dorsal surfaces of head and body reddish-brown,
hourglass-shaped dorsal glandular skin ridges also reddish brown surrounded with darker
grey-brown “X”-shaped marking with indistinct borders; flanks with irregular dark
brown spots and reddish mottling getting denser ventrally (Figure 4A); lateral surfaces
of head light brownish-gray to beige, upper lips with 3 to 4 dark reddish-brown vertical
bars, the one below eye largest and most distinct; tympanum entirely dark brown; white
supratympanic fold with black to dark-brown lower margin; loreal region dark-brown;
the edge of upper eyelid (palpebrum) with 3 distinct reddish palpebral tubercles,
the medial one largest forming horn-like projection; dorsally palpebral tubercles
edged with dark brown; dorsal parts of limbs reddish-brown with dark brown crossbars
and reddish mottling; dorsal surface of the fingers with dark brown crossbars; ventral
surfaces of body and limbs primarily off-white to grey, mottled with dense black and
white blotches and flecks on belly; black and white marbling getting denser anteriorly;
gular and chest dark grey and mottled with white; posterior part of belly off-white
with large grey blotches; ventral surfaces of hindlimbs with contrasting black and
white marbling; groin area, anterior surfaces of thighs and posterior surfaces of
heels bright reddish-orange in life; pectoral and femoral glands small, cream-white
in color; iris golden-bronze with dense black mottling; pupil edged with thin golden
line; thenar and palmar surface of limbs dark grey; and inner metacarpal tubercle,
outer metacarpal tubercle, and inner metatarsal tubercle bright pink.
Color of the holotype in preservative:For coloration see Supplementary Figure S1.
After 2 years in preservative, dorsum faded to dark brown; a complete dark brown inverted
triangle between eyes and crossbars on dorsal limbs and fingers still clear; two opposing
“V”-shaped skin folds present on dorsum becoming less distinct; throat and chest turns
dark brown; abdomen and ventral surface of limbs dark brown mottled with whitish-grey
marbling; inner metacarpal tubercle and inner metatarsal tubercle become off-white,
outer metacarpal tubercle brown; dark brown vertical bars present upper lips still
clear; supratympanic folds dark brown; pectoral glands and femoral glands still distinct,
cream; ventral side of the hands and toes brown and digit tips brown or cream.
Variation:Morphometric variation of types reported in Table 1. All 5 paratypes are
very similar in morphology the holotype, but also show variation in color in life.
Dorsal surface of holotype and paratype AUP-00055 light brown, but paratype AUP-00077
orange (Figure 4).
Male secondary sexual characteristics:The new species shows slight differences in
body size between the sexes: females have slightly larger SVL (37.5–39.2 mm, mean
38.3 mm; n=4) than males (31.2–32.1 mm, mean 31.7 mm; n=2). All adult males have nuptial
pads pinkish-red in life covering the dorsal surface of the base of FI. Male has external,
single subgular vocal sac with slit-like openings at posterior corners of jaws and
a prominent protruding projection posterior to cloaca (Figure 4).
Distribution and ecology:
Xenophrys angka
sp. nov.is currently known only from Doi Inthanon, Chiang Mai province, Thailand (Figure
1) at elevations from 1800 to 2200 m a.s.l. along forest cascade streams and waterfalls.
Most males were located by calls made while sitting on vegetation 1–2 m from the stream;
females were recorded in forest litter along the streams. Xenophrys angka
sp. nov.appears to be a strict forest specialist, restricted to patches of undisturbed
montane evergreen forests and is likely endemic to the Doi Inthanon – Thanon Thong
Chai Range. It inhabits forest floor, leaf litter and the nearby undergrowth rocky
mountainous surrounded by moist evergreen broadleaved forests. The new species was
found in sympatry with Leptobrachium huashen Fei et Ye and Limnonectes tayloriMatsui,
Panha, Khonsue et Kuraishi.
Comparisons:We compared Xenophrys angka
sp. nov. with their 66 known congeners on the basis of morphology. Comparisons with
each subgenus are discussed separately below.
SubgenusPanophrys: Xenophrys angka
sp. nov. differs from the following large-sized species by having a smaller adult
male size, SVL 31.2–32.1 mm (vs. adult-male 42.0–45.0 mm, n=5, in X. baolongensis,
Ye et al., 2007; 45.0–51.0 mm, n=3, in X. binlingensis, Fei et al., 2009; 81.3 mm,
n=1, in X. caudoprocta, Fei et al., 2009; 53.0–56.5 mm, n=2, in X. jingdongensis,
Fei et al., 2009; 56.0–59.5 mm, n=10, in X. omeimontis, Fei et al., 2009; 54.7 mm,
n=1, in X. sangzhiensis, Jiang et al., 2008; 99.8–115.6 mm, n=6, in X. shuichengensis,
Tian et al., 2000; and 47.2–54.4, n=18, in X. spinata, Fei et al., 2009); from X.
liboensis by having a smaller adult female body size, SVL 37.5–39.2 mm (vs. 60.8–70.6
mm, n=8, in X. liboensis, Zhang et al., 2017); further from X. acuta by meeting or
overlapping when tibias positioned at right angle to body axis (vs. not meeting in
X. acuta, Li et al., 2014), and head slightly longer than wide (vs. head length slightly
shorter than head width in X. acuta, Li et al., 2014); fromX. binchuanensis by lateral
dermal fringes on toes absent (vs. lateral dermal fringes on toes wide in X. binchuanensis,
Fei et al., 2009), and horn-like tubercle above eyelids present (vs. absent in X.
binchuanensis, Fei et al., 2009); from X. boettgeri by tongue not notched behind
(vs. tongue notched behind in X. boettgeri, Fei et al., 2009), lateral dermal fringes
on absent (vs. present in X. boettgeri, Fei et al., 2009), and male with external
single subgular vocal sac (vs. male with internal single subgular vocal sac in X.
boettgeri, Fei et al., 2009); from X. brachykolos by head slightly longer than wide
(vs. head width larger than head length in X. brachykolos, Fei et al., 2009), male
with external single subgular vocal sac (vs. male with internal single subgular vocal
sac in X. brachykolos, Fei et al., 2009), and heels meeting or overlapping (vs. not
meeting in X. brachykolos, Fei et al., 2009); from X. cheni by lateral fringes on
fingers and toes absent (vs. lateral fringes on figures and toes wide in X. cheni,
Wang et al., 2014), a large subarticular tubercle present at base of fingers I–II,
absent on fingers III–IV (vs. subarticular tubercles indistinct in X. cheni, Wang
et al., 2014), golden-bronze (vs. iris dark brown in X. cheni, Wang et al., 2014),
and tongue not notched behind (vs. margin of tongue notched behind in X. cheni, Wang
et al., 2014); from X. daweimontis by vomerine ridges indistinct and vomerine teeth
absent (vs. present in X. daweimontis, Rao & Yang, 1997), and male with external single
subgular vocal sac (vs. male with internal vocal sac in X. daweimontis, Rao & Yang,
1997); from X. dongguanensis and X. nankunensis by vomerine ridges indistinct and
vomerine teeth absent (vs. strong vomerine ridge bearing vomerine teeth in X. dongguanensis
and X. nankunensis, Wang et al., 2019), subarticular tubercle present at base of toes
I, absent on toe II–IV (vs. subarticular tubercles only present at base of each toe
in X. dongguanensis and X. nankunensis, Wang et al., 2019), and heels meeting or
overlapping (vs. heels not meeting in X. dongguanensis and X. nankunensis, Wang et
al., 2019); from X. fansipanensis and X. hoanglienensis by vomerine ridges indistinct
and vomerine teeth absent (vs. present in X. fansipanensisandX. hoanglienensis, Tapley
et al., 2018), inner and outer metacarpal tubercles present (vs. absent in X. fansipanensisandX.
hoanglienensis, Tapley et al., 2018), a large subarticular tubercle present at base
of fingers I–II, absent on fingers III–IV (vs. absent in X. fansipanensisandX. hoanglienensis,
Tapley et al., 2018), inner metatarsal tubercle large (vs. inner metatarsal tubercle
very weakly in X. fansipanensis and X. hoanglienensis, Tapley et al., 2018), and
protruding projection posterior to cloaca of males present (vs. absent in X. fansipanensisandX.
hoanglienensis, Tapley et al., 2018); from X. huangshanensis by tympanum distinct
(vs. indistinct in X. huangshanensis, Fei et al., 2009), male with external single
subgular vocal sac (vs. male with internal single subgular vocal sac in X. huangshanensis,
Fei et al., 2009), subarticular tubercle present at base of toes I, absent on toe
II–IV (vs. present in X. huangshanensis, Fei et al., 2009), and heels meeting or overlapping
(vs. heels not meeting in X. huangshanensis, Fei et al., 2009); from X. insularis
by vomerine ridges indistinct and vomerine teeth absent (vs. vomerine ridge strong
with vomerine teeth in X. insularis, Wang et al., 2017), subarticular tubercle present
at base of toes I, absent on toe II–IV (vs. subarticular tubercle only present at
base of each toe in X. insularis, Wang et al., 2017), heels meeting or overlapping
(vs. not meeting in X. insularis, Wang et al., 2017), and tibio-tarsal articulation
reaching area between eye and snout tip (vs. reaching forward to posterior edge of
tympanum in X. insularis, Wang et al., 2017); from X. jinggangensis by subarticular
tubercle present at base of toes I, absent on toe II–IV (vs. a large subarticular
tubercle at base of each toe in X. jinggangensis, Wang et al., 2012), relative finger
lengths: I<II<IV<III (vs. II<I<IV<III in X. jinggangensis, Wang et al., 2012), and
lateral fringes on fingers absent (vs. present in X. jinggangensis, Wang et al., 2012);
from X. jiulianensis by tongue not notched posteriorly (vs. tongue weakly notched
posteriorly in X. jiulianensis, Wang et al., 2019), subarticular tubercle present
at base of toes I, absent on toe II–IV (vs. subarticular tubercles only present at
base of toe I and II in X. jiulianensis, Wang et al., 2019); from X. kuatunensis by
male with external single subgular vocal sac (vs. male with internal single subgular
vocal sac in X. kuatunensis, Fei et al., 2009), and heels meeting or overlapping (vs.
not meeting inX. kuatunensis, Fei et al., 2009); from X. leishanensis by male with
external single subgular vocal sac (vs. male with internal single subgular vocal sac
in X. leishanensis, Li et al., 2018), relative finger lengths: I<II<IV<III (vs. II<I<V<III
in X. leishanensis, Li et al., 2018), and head slightly longer than wide (vs. head
width slightly larger than head length in X. leishanensis, Li et al., 2018); from
X. lini by subarticular tubercle present at base of toes I, absent on toe II–IV (vs.
subarticular tubercle distinct at base of each toe in X. lini, Wang et al., 2014),
and lateral dermal fringes on fingers and toes absent (vs. wide in X. lini, Wang et
al., 2014); from X. lishuiensis by male with external single subgular vocal sac (vs.
male with internal single subgular vocal sac inX. lishuiensis, Wang et al., 2017);
from X. minor by a large subarticular tubercle present at base of fingers I–II,
absent on fingers III–IV (vs. absent in X. minor, Fei et al., 2009), subarticular
tubercle present at base of toes I, absent on toe II–IV (vs. absent in X. minor, Fei
et al., 2009), lateral dermal fringes on toes absent (vs. absent in X. minor, Fei
et al., 2009), male with external single subgular vocal sac (vs. male with internal
single subgular vocal sac inX. minor, Fei et al., 2009), and horn-like tubercle above
eyelids present (vs. absent in X. minor, Fei et al., 2009); from X. mufumontana by
relative finger lengths: I<II<IV<III (vs. II=IV<I<III in X. mufumontana, Wang et al.,
2019), subarticular tubercle present at base of toes I, absent on toe II–IV (vs. subarticular
tubercles only present at base of each toe in X. mufumontana, Wang et al., 2019),
a large subarticular tubercle present at base of fingers I–II, absent on fingers III–IV
(vs. presence of a subarticular tubercle at base of each finger in X. mufumontana,
Wang et al., 2019), and outer metacarpal tubercle small, flattened (vs. indistinct
in X. mufumontana, Wang et al., 2019); fromX. nanlingensis by vomerine ridges indistinct
and vomerine teeth absent (vs. vomerine ridge and vomerine teeth present in X. nanlingensis,
Wang et al., 2019), tongue not notched posteriorly (vs. tongue notched posteriorly
in X.nanlingensis, Wang et al., 2019), a large subarticular tubercle present at base
of fingers I–II, absent on fingers III–IV (vs. presence of a subarticular tubercle
at base of each finger in X. nanlingensis, Wang et al., 2019), subarticular tubercle
present at base of toes I, absent on toe II–IV (vs. presence of a subarticular tubercle
at base of each toe in X. nanlingensis, Wang et al., 2019), and adult males have nuptial
pads pinkish-red in life covering dorsal surface of base of FI (vs. nuptial pads and
nuptial spines invisible in males during breeding season in X. nanlingensis, Wang
et al., 2019); from X. obesa by vomerine ridges indistinct (vs. two vomerine ridges
moderately developed in X. obesa, Li et al., 2014), heels meeting or overlapping (vs.
not meeting in X. obesa, Li et al., 2014), and head slightly longer than wide (vs.
head width slightly larger than head length inX. obesa, Li et al., 2014); from X.
ombrophila by heels meeting or overlapping (vs. not meeting in X. ombrophila, Messenger
et al., 2019), and tibio-tarsal articulation reaching area between eye and snout tip
(vs. reaching posterior corner of eye in X. ombrophila, Messenger et al., 2019);
from X. palpebralespinosa by vomerine teeth absent (vs. present in X. palpebralespinosa,
Fei et al., 2009), lateral dermal fringes on fingers and toes absent (vs. slight lateral
fringes on fingers, lateral fringes wide on toes in X. palpebralespinosa, Fei et al.,
2009), and male with external single subgular vocal sac (vs. male with internal single
subgular vocal sac in X. palpebralespinosa, Fei et al., 2009); from X. rubrimera by
vomerine teeth absent (vs. present in X. rubrimera, Tapley et al., 2017), a large
subarticular tubercle present at base of fingers I–II, absent on fingers III–IV (vs.
absence of subarticular tubercles on fingers in X. rubrimera, Tapley et al., 2017),
and head slightly longer than wide (vs. head width slightly larger than head length
inX. rubrimera, Tapley et al., 2017); from X. tuberogranulata by male with external
single subgular vocal sac (vs. male with internal single subgular vocal sac in X.
tuberogranulata, Mo et al., 2010), a large subarticular tubercle present at base of
fingers I–II, absent on fingers III–IV (vs. indistinct in X. tuberogranulata, Mo
et al., 2010), and relative finger lengths: I<II<IV<III (vs. II<IV=I<III in X. tuberogranulata,
Mo et al., 2010); from X. wugongensis by heels meeting or overlapping (vs. not meeting
in X. wugongensis, Wang et al., 2019), a large subarticular tubercle present at base
of fingers I–II, absent on fingers III–IV (vs. presence of a subarticular tubercle
at base of each finger in X. wugongensis, Wang et al., 2019), subarticular tubercle
present at base of toes I, absent on toe II–IV (vs. presence of a subarticular tubercle
at base of each toe in X. wugongensis, Wang et al., 2019); from X. wuliangshanensis
by a large subarticular tubercle present at base of fingers I–II, absent on fingers
III–IV (vs. indistinct in X. wuliangshanensis, Fei et al., 2009), male with external
single subgular vocal sac (vs. male with internal single subgular vocal sac in X.
wuliangshanensis, Fei et al., 2009), horn-like tubercle at edge of eyelids present
(vs. absent in X. wuliangshanensis, Fei et al., 2009), and relative finger lengths:
I<II<IV<III (vs. IV<III<II=I in wuliangshanensis, Fei et al., 2009); from X. wushanensis
by horn-like tubercle and some smaller tubercles at edge of eyelids present (vs. absent
in X. wushanensis, Fei et al., 2009), male with external single subgular vocal sac
(vs. male with internal single subgular vocal sac in X. wushanensis, Fei et al., 2009),
and lateral dermal fringes on toes absent (vs. male with wide lateral fringes in X.
wushanensis, Fei et al., 2009).
Subgenus Xenophrys: Xenophrys angka
sp. nov. differs from the following large-sized specie by having a smaller adult male
size, SVL 31.2–32.1 mm (vs. adult-male 55.8–62.4 mm, n=6, in X. aceras, Wang et al.,
2017; 39.1–45.0 mm, n=8, in X. ancrae, Mahony et al., 2013; 76.7 mm, n=20, in X. auralensis,
Ohler., 2002; 57.1 mm, n=1, in X. damrei, Mahony, 2011; 56.9–68.4 mm, n=4, in X. flavipunctata,
Mahony et al., 2018; 76.3–81.0 mm, n=10, in X. glandulosa, Fei et al., 2009; 68.0–73.5
mm, n=7, in X. himalayana, Mahony et al., 2018; 55.6–66.6 mm, n=8, in X. lekaguli,
Stuart et al., 2006; 47.0 mm, n=1, in X. longipes, Wang et al., 2017; 65.5 mm, n=1,
in X. major, Fei et al., 2009; 62.5 mm, n=1, in X. mangshanensis, Fei et al., 2009;
58.0–76.0 mm, n=6, in X. maosonensis, Yang et al., 2018; 57.2–68.0 mm, n=16, in X.
medogensis, Fei et al., 2009; 71.3–93.8 mm, n=12, in X. periosa, Mahony et al., 2018;
73.5–83.1 mm, n=6, in X. robusta, Mahony et al., 2018; 45.9–53.4 mm, n=7, in X. megacephala,
Mahony et al., 2011; 47.4–53.0 mm, n=33, in X. takensis, Mahony, 2011); from X. oreocrypta
by having a smaller adult female body size, SVL 37.5–39.2 mm (vs. 94.9 mm, n=1, in
X. oreocrypta, Mahony et al., 2018); further from X. monticola by vomerine ridges
indistinct (vs. distinct in X. monticola, Mahony et al., 2018), a large subarticular
tubercle present at base of fingers I–II, absent on fingers III–IV (vs. absent in
X. monticola, Mahony et al., 2018), inner and outer metacarpal tubercles distinct
(vs. absent in X. monticola, Mahony et al., 2018), and inner metatarsal tubercle large
(vs. indistinct in X. monticola, Mahony et al., 2018); from X. oropedion by vomerine
ridges indistinct and vomerine teeth absent (vs. present in X. oropedion, Mahony et
al., 2013), a large subarticular tubercle present at base of fingers I–II, absent
on fingers III–IV (vs. absent in X. oropedion, Mahony et al., 2013), protruding projection
posterior to cloaca of males present (vs. absent in X. oropedion, Mahony et al., 2013),
and inner and outer metacarpal tubercles distinct (vs. absent in X. oropedion, Mahony
et al., 2013); from X. pachyproctus and X. parva by vomerine ridges indistinct and
vomerine teeth absent (vs. present in X. pachyproctus and X. parva, Fei et al., 2009),
a large subarticular tubercle present at base of fingers I–II, absent on fingers III–IV
(vs. absent in X. pachyproctusandX. parva, Fei et al., 2009), and male with external
single subgular vocal sac (vs. male with internal single subgular vocal sac in X.
pachyproctus and X. parva, Fei et al., 2009); from X. serchhipii by toes with rudimentary
webbing (vs. at least one-fourth webbing in X. serchhipii, Mathew & Sen, 2007), relative
finger lengths: I<II<IV<III (vs. 2nd and 4th fingers subequal in length in X. serchhipii,
Mathew & Sen, 2007), and vomerine teeth absent (vs. present in X. serchhipii, Mathew
& Sen, 2007); from X. vegrandis by a large subarticular tubercle present at base of
fingers I–II, absent on fingers III–IV (vs. absent in X. serchhipii, Mathew & Sen,
2007), protruding projection posterior to cloaca of males present (vs. absent in X.
serchhipii, Mathew & Sen, 2007), and pupil vertical, iris golden-bronze (vs. pupil
horizontally orientated, iris metallic yellowish-orange in X. serchhipii, Mathew &
Sen, 2007); from X. zhangiby vomerine ridges indistinct and vomerine teeth absent
(vs. present in X. zhangi, Fei et al., 2009), a large subarticular tubercle present
at base of fingers I–II, absent on fingers III–IV (vs. absent in X. zhangi, Fei et
al., 2009), lateral dermal fringes on toes absent (vs. present in X. zhangi, Fei et
al., 2009), and male with external single subgular vocal sac (vs. male with internal
single subgular vocal sac in X. zhangi, Fei et al., 2009); from X. zunhebotoensis
by horn-like tubercle and a number of smaller tubercles at edge of eyelids present
(vs. absent in X. zunhebotoensis, Mathew & Sen, 2007), tongue not notched behind (vs.
tongue notched behind in X. zunhebotoensis, Mathew & Sen, 2007), and vomerine teeth
absent (vs. present in X. zunhebotoensis, Mathew & Sen, 2007).
From species not yet assigned to a subgenus: Xenophrys angka
sp. nov. differs from X. feii by lateral dermal fringes on toes absent (vs. lateral
fringes on toes moderate to wide in X. feii, Yang et al., 2018), lateral fringes on
fingers absent (vs. moderate lateral fringes present on outer most three fingers in
X. feii, Yang et al., 2018), groin coloration in life contrasting with surrounding
regions on males (vs. groin coloration not contrasting with surrounding regions on
males in X. feii, Yang et al., 2018), and nuptial pads present on finger I (vs. absent
in X. feii, Yang et al., 2018).
The diversity of Xenophrys is underestimated greatly (Chen et al., 2017; Liu et al.,
2018). In the last three years, 19 new species were described mostly from China, Vietnam
and India (Li et al., 2018; Mahony et al., 2018; Messenger et al., 2019; Tapley et
al., 2017, 2018Wang et al., 2017; Wang et al., 2017; Wang et al., 2019; Yang et al.,
2018; Zhang et al., 2017). Compared to other countries in the Indochinese region,
the diversity of Xenophrys in Thailand attracted less attention and no new species
were described for the country within the last seven years. Herein, we describe a
new species of Xenophrysfrom northern Thailand based on morphological and molecular
analyses. Our discovery increases the number of amphibian species recorded in Thailand
to 194, and the species number of Xenophrys to 27. The diversity of amphibians known
from Thailand has increased remarkably from 125 (Khonsue and Thirakhupt, 2001) to
193 (Frost, 2019) and the diversity remains underestimated (Chan et al., 2018; Chen
et al., 2017, 2018
Grismer et al., 2016; Laopichienpong et al., 2016; Matsui et al., 2018; Pawangkhanant
et al., 2018; Poyarkov et al., 2018; Sheridan & Stuart, 2018; Suwannapoom et al.,
2017; Suwannapoom et al., 2018). Further field surveys and taxonomic studies on the
Thai herpetofauna will likely result in further discoveries of yet unknown lineages
and species of amphibians.
Our study also elucidates taxonomic status of Xenophrys latidactyla(Orlov et al.,
2015), whicha recently described from northern Vietnam. It was described as a member
of Megophrys sensu lato based on a single male specimen collected from Pu Mat National
Park in south-western Nghe An Province. Orlov et al. (2015) indicated that this species
is most closely resembles X. palpebralespinosa, inhabiting montane areas of northern
Vietnam (recorded from provinces Lao Cai, He Giang, Cao Bang, Vinh Phuc, Son La, Thanh
Hoa, Nge An) and northern Laos, eastern part of Yunnan and the westernmost part of
Guangxi, China (Bourret, 1937, 1942; Fei et al., 2009, 2010Orlov et al., 2015; Tapley
et al., 2017). The main morphological differences of these two species were the presence
of very wide dermal fringes along all length of the toes in X. latidactyla (vs. broad
dermal fringes absent in X. palpebralespinosa), presence of prominent subarticular
tubercles in X. latidactyla (vs. absent), and differences in tympanum size. Our mtDNA
genealogy unambiguously places two specimens of X. latidactyla, including the type
specimen ZISP 12182, within radiation of X. palpebralespinosa from northern Vietnam
and Laos. The genetic divergence between X. latidactyla and X. palpebralespinosa
is small, ranging from 0.3%–1.4%, suggesting that these two taxa might be conspecific.
Morphological differences that were used by Orlov et al. (2015) to diagnose these
species might be subject to significant variation, which was not assessed due to small
sample size (n=1): feet webbing and dermal fringes on toes in X. palpebralespinosaare
normally significantly reduced out of the breeding season and get enlarged during
the reproduction (personal observation); the reported distinct subarticular tubercles
in X. latidactylamight be the result of partial dehydration of limbs due to preservation
in ethanol. Thus, no unambiguous morphological or molecular characters distinguishing
these two species. Therefore, we transfer X. latidactyla to the synonymy of X. palpebralespinosa
as a subjective junior synonym. Further, this result indicates that molecular analyses
are essential in assessing species diversity of Xenophrys,and megophryids in general.
NOMENCLATURAL ACTS REGISTRATION
The electronic version of this article in portable document format represents a published
work according to the International Commission on Zoological Nomenclature (ICZN),
and hence the new names contained in the electronic version are effectively published
under that Code from the electronic edition alone (see Articles 8.5–8.6 of the Code).
This published work and the nomenclatural acts it contains have been registered in
ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science
Identifiers) can be resolved and the associated information can be viewed through
any standard web browser by appending the LSID to the prefix http://zoobank.org/.
Publication LSID:
urn:lsid:zoobank.org:pub:599B00C7-BCD7-4C24-ACB6-0AC2B508BADA.
Xenophrys angka LSID:
urn: lsid:zoobank.org:act:44272F1C-0019-4EE5-83E9-28C3286BCA4F.
SCIENTIFIC FIELD SURVEY PERMISSION INFORMATION
Specimen collection protocols were approved by the Institutional Ethical Committee
of Animal Experimentation of the University of Phayao (certificate number UP-AE59-01-04-0022
issued to Chatmongkon Suwannapoom) and the Institute of Animal for Scientific Purposes
Development Thailand (No. U1-01205-2558).
SUPPLEMENTARY DATA
Supplementary data to this article can be found online.
Click here for additional data file.
Click here for additional data file.
Click here for additional data file.