Review Article |
Corresponding author: Amirrudin B. Ahmad ( amirrudin@umt.edu.my ) Academic editor: Thomas Ziegler
© 2023 Baizul Hafsyam Badli-Sham, Muhamad Fatihah Syafiq, Mohd Shahrizan Azrul Aziz, Natrah Rafiqah Mohd Jalil, Muhammad Taufik Awang, Muhammad Nouril Ammin Othman, Anis Azira Abdul Aziz, Khunirah Dzu, Nurul Asyikin Abdol Wahab, Nor Liyana Jamil, Murni Azima Ismail, Wan Ahmad Aidil Wan Azman, Ooi Xin Wei, Nur Ain Nabilah Jamaha, Mohamad Aqmal-Naser, Muhammad Fahmi-Ahmad, Noor Shahirah-Ibrahim, Syed Ahmad Rizal, Daicus M. Belabut, Chan Kin Onn, Evan Seng Huat Quah, Larry Lee Grismer, Amirrudin B. Ahmad.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Badli-Sham BH, Syafiq MF, Aziz MSA, Mohd Jalil NR, Awang MT, Othman MNA, Abdul Aziz AA, Dzu K, Abdol Wahab NA, Jamil NL, Ismail MA, Wan Azman WAA, Xin Wei O, Jamaha NAN, Aqmal-Naser M, Fahmi-Ahmad M, Shahirah-Ibrahim N, Rizal SA, Belabut DM, Kin Onn C, Quah ESH, Grismer LL, Ahmad AB (2023) A decade of amphibian studies (Animalia, Amphibia) at Sekayu lowland forest, Hulu Terengganu, Peninsular Malaysia. ZooKeys 1157: 43-93. https://doi.org/10.3897/zookeys.1157.95873
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Amphibians of Sekayu lowland forest have been studied more than a decade, with discoveries of new records of species showing no sign of abating between the years 2003 to 2020, indicating the remarkably rich diversity of anurans in this forest. Despite ceaseless anthropogenic activities in this area, this study successfully recorded 52 species of amphibians from 32 genera in the lowland forest of Sekayu. The species composition consisted of a single species from the family Ichthyophiidae and 51 species of anurans of 31 genera and six families. The number of species recorded has steadily increased especially during more recent surveys from 2015 to 2020. This study augments the total number of amphibian species recorded from Hulu Terengganu by ten additional species, increasing the total to 70 species for the district.
Biodiversity conservation, herpetofauna, lowland forest, Malaysia, protected areas
The earliest herpetological surveys conducted by
From 2011 to the present, extensive efforts have been made to document the herpetofauna diversity in Terengganu, including lowland to upland areas (Gunung Gagau:
As part of the Hulu Terengganu Forest Reserve that is adorned with beautiful streams and intact forests, Sekayu lowland forest (SLF) has become the most popular picnic spot in Terengganu amongst locals and tourists alike with nearly 203,000 visitors reported in the year 2010 (
Furthermore, the actual diversity of amphibians in SLF remains uncertain as the checklists were not properly reviewed and updated in the latest taxonomy, may contain several erroneous records or misidentifications of specimens, and the existing areas have not been exhaustively surveyed. The objectives of this paper are to: (1) properly compile and update the information from previous and recent fieldwork to produce a comprehensive checklist of amphibians, (2) to examine the previously and recently collected specimens in SLF for accurate species accounts, and (3) to assess the trend of long-term surveys conducted on amphibians throughout the past decade in SLF. In addition, this paper also provides a compiled checklist based on published records on the amphibian fauna in Hulu Terengganu District (
Sekayu lowland forest (SLF) is located within the Hulu Terengganu Forest Reserve (Annex) near Kuala Berang to the east, and Taman Negara (= National Park) to the west and south-west (Fig.
Map A shows the location of Sekayu lowland forest (SLF) indicated by red box in Peninsular Malaysia. The detailed location of SLF and several localities with published checklist on amphibians in Hulu Terengganu were displayed on Map B and indicated by the red circles for respective localities.
In SLF, fieldworks were conducted at various locations within SRF and SAP. The Sekayu Recreational Forest area (SRF) (entrance at 4°58'01.1"N, 102°57'35.4"E) contains substantial landscape changes to accommodate facilities for Forestry staff and visitors, such as huts, toilets, changing rooms, chalets, and camping sites. SRF is drained by a stream channel of the Peres River, which remains the main attraction for this area for recreational activities such as picnics and camping (
Sekayu Agricultural Park (SAP) (entry point at 4°58'01.8"N, 102°57'28.4"E) is comprised of mostly agricultural lands growing various species of fruits such as Lansium domesticum, Nephelium lappaceum, Gracia mangostana, Durio zibethinus, and garden plants. Most of the landscape of this area is significantly altered and surrounded by the forest edge and drained by a stream channel of the Bubu River (
Surveys were conducted using standard methods of visual encounter surveys (VES) and acoustic surveys, together with drift-fenced pitfall traps in SLF. VES is a time-constrained technique that is frequently employed in herpetological surveys, in which the observers walk along a in standardised route at a standard pace to visually search the entire area for amphibians (Crump and Scott 1994;
Additional information of species from SLF was obtained from the compilation of amphibian checklists conducted by previous undergraduate fieldwork from 2003, 2004, 2006, 2013, 2014 and early 2015. Voucher specimens collected from previous and more recent fieldwork were examined to confirm species identifications based on
The checklist of amphibians from previous studies (2003–2015) were tabulated and compiled together with the most recent studies (October 2015-December 2020) to obtain the accumulated number of amphibian species that have been recorded in SLF. Species accumulation curve and estimated number of duplicates (species with two samples) and unique species (species represented by one sample) (
Fifty-two species of amphibians were recorded in total, consisting of one caecilian from the family Ichthyophiidae and 51 anurans from 31 genera and six families in SLF (Table
Checklist of amphibians of Sekayu lowland forest, Hulu Terengganu, Terengganu.
No | Family/Species | Year | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
2003 | 2004 | 2006 | 2008 | 2013 | 2014 | 2015 | 2016 | 2017 | 2018 | 2020 | ||
Family Ichthyophiidae | ||||||||||||
1 | Ichthyophis cf. asplenius | – | – | – | – | – | – | – | – | + | – | – |
Family Bufonidae | ||||||||||||
2 | Ansonia latiffi | – | – | – | – | + | + | + | + | – | + | – |
3 | Ansonia lumut | – | – | – | – | – | – | – | + | + | + | – |
4 |
Duttaphrynus bengalensis
(Duttaphrynus sp. 1) |
– | – | – | + | + | – | – | + | – | + | + |
5 | Ingerophrynus parvus | + | + | + | – | + | + | + | + | + | + | + |
6 | Leptophryne borbonica | – | – | – | – | – | – | – | + | – | – | + |
7 | Phrynoidis asper | + | + | + | + | + | + | + | + | + | + | + |
8 | Rentapia flavomaculata | – | – | – | – | – | – | + | + | – | – | – |
Family Dicroglossidae | ||||||||||||
9 | Fejervarya limnocharis | + | + | + | + | + | + | + | + | + | + | + |
10 | Limnonectes blythii | + | + | + | + | + | – | + | + | + | + | + |
11 | Limnonectes hascheanus | – | – | – | – | – | – | – | + | + | + | + |
12 | Limnonectes deinodon | – | – | – | – | – | – | + | + | + | + | + |
13 | Limnonectes malesianus | + | + | – | – | – | – | + | + | + | + | + |
14 | Limnonectes plicatellus | – | – | – | – | – | – | – | + | + | + | + |
15 | Limnonectes utara | – | – | – | – | – | – | – | – | – | + | – |
16 | Occidozyga sumatrana | – | – | – | – | – | – | – | + | – | + | + |
17 | Occidozyga martensii | – | – | – | – | – | – | – | + | + | + | + |
Family Megophryidae | ||||||||||||
18 | Leptobrachium hendricksoni | + | – | + | + | + | + | + | + | + | + | + |
19 | Leptobrachella sola | – | – | – | – | – | – | + | + | + | + | – |
20 | Pelobatrachus nasutus | – | – | + | – | + | + | – | + | + | + | + |
Family Microhylidae | ||||||||||||
21 | Kalophrynus kiewi | – | – | – | – | – | – | + | + | + | + | + |
22 | Kalophrynus palmatissimus | – | – | – | – | – | – | – | + | – | – | – |
23 | Kaloula latidisca | – | – | – | – | – | – | + | + | – | + | + |
24 | Kaloula pulchra | – | – | – | – | + | + | + | + | + | – | + |
25 | Microhyla bedmorei | – | – | – | – | – | – | + | + | – | – | – |
26 | Microhyla butleri | – | – | – | + | + | + | + | + | + | + | + |
27 | Microhyla cf. heymonsi | + | + | + | + | + | + | + | + | + | + | + |
28 | Microhyla superciliaris | – | – | – | – | + | – | – | + | – | + | + |
29 | Micryletta dissimulans | – | – | – | – | – | – | – | + | + | + | + |
30 | Phrynella pulchra | – | – | – | – | – | + | – | – | – | – | – |
Family Ranidae | ||||||||||||
31 | Amolops gerutu | + | – | + | + | + | + | + | + | + | + | + |
32 | Chalcorana labialis | – | – | + | + | + | + | + | + | + | + | + |
33 | Humerana miopus | – | – | – | – | + | – | + | + | + | + | + |
34 | Hylarana erythraea | + | + | + | + | + | + | + | + | + | + | – |
35 | Indosylvirana nicobariensis | + | – | – | – | + | – | + | + | + | + | + |
36 | Odorrana hosii | + | – | + | + | + | + | + | + | + | + | + |
37 | Pulchrana glandulosa | – | – | – | – | + | + | + | + | + | + | + |
38 | Pulchrana laterimaculata | – | – | – | – | – | – | – | – | – | + | + |
39 | Pulchrana sundabarat | + | – | + | – | – | – | + | + | + | + | – |
40 | Sylvirana malayana | + | – | + | – | + | + | + | + | + | – | – |
Family Rhacophoridae | ||||||||||||
41 | Kurixalus chaseni | – | – | – | – | – | + | – | + | + | + | + |
42 | Nyctixalus pictus | – | – | – | – | – | + | + | + | + | + | + |
43 | Polypedates colletti | – | – | – | – | – | – | – | – | – | – | + |
44 | Polypedates discantus | – | – | – | – | – | – | + | + | + | + | + |
45 | Polypedates leucomystax | + | + | + | + | + | + | + | + | + | + | + |
46 | Polypedates macrotis | – | – | – | – | + | + | + | + | + | + | + |
47 | Rhacophorus nigropalmatus | – | – | – | – | + | – | – | – | – | + | – |
48 | Rhacophorus pardalis | – | – | – | – | + | – | – | – | – | – | – |
49 | Theloderma horridum | – | – | – | – | + | – | – | – | – | – | – |
50 | Theloderma licin | – | – | – | – | – | – | – | + | – | – | – |
51 | Zhangixalus prominanus | – | – | – | – | + | – | – | + | + | + | – |
52 | Zhangixalus tunkui | – | – | – | – | + | – | – | – | – | – | – |
Total number of species | 14 | 8 | 14 | 12 | 28 | 20 | 29 | 43 | 34 | 38 | 34 |
Class Amphibia
Order Gymnophiona
One specimen was collected from SRF (UMTZC1792, SVL = 198 mm).
The specimen had elongated and cylindrical body with SVL 198 mm; head as wide as body; snout round; small eyes; body darkish purple with pale yellowish lateral band. Specimen tentatively recognised as Ichthyophis cf. asplenius as suggested by
Eight specimens were collected from SRF consisted of four males (UMTZC1319, UMTZC1400, UMTZC1461, and UMTZC1575, SVL = 38–60 mm) and four females (UMTZC1318, UMTZC1353, UMTZC1401, and UMTZC1553, SVL = 41–59 mm).
Morphological characters of the specimens from SLF agreed well with the description by Wood et al. (2008b). Size (SVL: 38–60 mm, n = 4 males; 41–59 mm, n = 4 females); snout projecting beyond lower jaw; tympanum distinct; interorbital ridges absent; small warts at jaw; head narrow in females, but wide in males; inner and outer metatarsal tubercles present; first finger reaching tip of second finger; single mandibular asperities in UMTZC1400 and double for other specimens; dorsal tubercles distinct; spotting at gular region, obscured in UMTZC1353 and UMTZC1553; abdomen finely granular; no dorsolateral row of tubercles;
All observed and collected A. latiffi were found along the banks of the small streams of the Peres River within the areas of SRF. Ansonia latiffi is typically found on rocky substrate or the ground of sloping terrain, and sometimes found perched on low vegetation below 1 m from the ground.
Three males were collected from SRF (UMTZC1527 and UMTZC1991, SVL = 15–24 mm) and SAP (UMTZC1615, SVL = 26 mm).
Morphological characters of the specimens agreed well with the description by
Ansonia lumut was first collected from the Bubu River in SAP by
Four males were collected from SRF (UMTZC1147, UMTZC1148, and UMTZC1149, SVL = 47–68 mm) and SAP (UMTZC1065, SVL = 59 mm).
Morphological characters of the specimens agreed well with the former description by
This species was more frequently observed at SAP compared to SRF, probably due to the more disturbed and man-made environment that is favoured by this commensal anuran (
Ten specimens were previously collected from SRF consisted of seven males (UMTZC1021, UMTZC1025, UMTZC1026, UMTZC1033, UMTZC1255, UMTZC1339, and UMTZC1398, SVL = 33–37 mm) and three females (UMTZC1023, UMTZC1158, and UMTZC1625, SVL = 42–45 mm).
Morphological characters of the specimens agreed well with the description by
Most of the individuals were collected and observed near the stream areas. This species is also common in open recreational areas. Ingerophrynus parvus was commonly found on the leaf litter, in rocky crevices and rotten logs, but rarely found on low vegetation.
Two male specimens were collected from SRF (UMTZC1500 and UMTZC1733, SVL = 22–24 mm).
Morphological characters of the specimens agreed well with the description by
Leptophryne borbonica is so far known to occur at the small streams of SRF with the first collected specimen UMTZC1500 from the Peres small stream and UMTZC1733 from the Bubu small stream. This forest-dwelling species was sighted amongst the piles of dead leaves on the forest floor and the banks of the streams.
Nineteen specimens were collected from SLF consisted of 17 specimens from SRF (Juvenile: UMTZC1136, SVL = 17 mm; Males: UMTZC1020, UMTZC1022, UMTZC1031, UMTZC1083, UMTZC1112, UMTZC1129, UMTZC1135, UMTZC1399, UMTZC1483, UMTZC1508, UMTZC1511, UMTZC1575, UMTZC1576, and UMTZC1577, SVL = 24–111 mm; Females: UMTZC1321 and UMTZC1800, SVL = 93–150 mm) and two specimens from SAP (Males: UMTZC1152 and UMTZC1153, 32–34 mm).
Morphological characters of the specimens agreed well with the description by
Phrynoidis asper is common at the stream areas of SLF. This species was typically observed in rocky crevices and the ground near the stream bank. This toad is also amongst the largest species of anuran recorded in this area with a maximum SVL reaching 150 mm.
Two adult females were collected from SRF (UMTZC1404 and UMTZC1495, SVL = 102–104 mm).
Morphological characters of the specimens agreed well with the description of
The first collected specimen UMTZC1404 (Fig.
Twenty-four specimens were previously collected from SAP (Males: UMTZC1391, UMTZC1396, UMTZC1397, and UMTZC1598, SVL = 14–40 mm; Female: UMTZC1497, SVL = 50 mm), and SRF (Males: UMTZC1002, UMTZC1019, UMTZC1048, UMTZC1049, UMTZC1088, UMTZC1089, UMTZC1150, UMTZC1215, UMTZC1216, UMTZC1229, UMTZC1230, UMTZC1239, and UMTZC1259, SVL = 23–45 mm; Females: UMTZC1003, UMTZC1058, UMTZC1087, UMTZC1122, UMTZC1151, and UMTZC1324, SVL = 49–58 mm).
Morphological characters of the specimens agreed well with the description of
This species was ubiquitous in cleared and disturbed areas of SLF and is considered as commensal species of frog in this area. Most of the collected specimens were found on the grassy fields and in puddles. Active calling can be heard after the rains.
Seven specimens were collected from SRF consisted of juveniles (UMTZC1390 and UMTZC1599, SVL = 31–38 mm), males (UMTZC1004 and UMTZC1394, SVL = 84 to 87 mm), and females (UMTZC1393, UMTZC1459, and UMTZC1491, SVL = 48–68 mm).
Morphological characters of the specimens agreed well with the description by
All specimens were collected from the recreational zones of SLF and the small streams of the Peres and Bubu Rivers. This species is usually found on the ground at stream banks.
Two male specimens were collected from SAP (UMTZC1516, SVL = 29 mm) and SRF (UMTZC1529, SVL = 19 mm).
Morphological characters of the specimens agreed well with the description by
UMTZC1516 was collected from hilly terrain at SAP and they are usually seen quietly perched amongst piles of dead leaves. UMTZC1529 was found at the Herbal Park within SRF on similar substrate as the preceding specimen.
Seventeen specimens were collected from SRF consisted of juveniles (UMTZC1386, UMTZC1388, UMTZC1548, and UMTZC1549, SVL = 20–30 mm), males (UMTZC1392, UMTZC1395, UMTZC1458, UMTZC1547, and UMTZC1557, SVL = 43–55 mm) and females (UMTZC1125, UMTZC1370, UMTZC1371, UMTZC1374, UMTZC1387, UMTZC1389, UMTZC1470, and UMTZC1471, SVL = 31 to 53 mm).
Morphological characters of the specimens agreed well with the description by
The species was ubiquitous at stream areas of SRF and can be found at various microhabitats such as in rocky crevices, dead leaves, rotten logs, or intermittent pools near the streams.
Two male specimens were collected from SRF (UMTZC1123 and UMTZC1628, SVL= 74–81 mm).
Morphological characters of the specimens agreed well with the description by
All specimens were collected from a small stream of the Peres River at SRF. Additional individuals of this species can be found on forest floors and stream banks of the small streams and recreational zones in SRF.
Two adult specimens were collected from SRF for male (UMTZC1460, SVL = 35 mm) and female (UMTZC1512, SVL = 35 mm).
Morphological characters of the specimens agreed well with the description by
UMTZC1460 was collected from a small stream of Peres River, and UMTZC1512 from the recreational zone within SRF. Both were found on the forest litter.
One male specimen was collected from SLF (UMTZC1964, SVL = 49 mm).
Morphological character of the specimen agreed well with the description by
Information of L. utara from SLF is limited to a specimen and photograph of a dead specimen, as it was contributed through recent undergraduate sampling. This species was previously reported as Limnonectes cf. kuhlii in SRF.
Seven adult male specimens were collected from SRF (UMTZC1507, UMTZC1561, UMTZC1562, UMTZC1610, UMTZC1629, UMTZC1631, and UMTZC1734SVL, SVL = 22–35 mm).
Morphological characters of the specimens agreed well with the description by
All specimens were found in temporary stagnant water bodies near the Peres River at SRF, such as puddles or intermittent pools that developed after heavy rains on the forest floor and near stream areas. The species is typically observed with its body partially submerged in water with eyes exposed.
No specimen was collected for this species, but it was recorded by field observation and photographs of two individuals at an artificial pond at Herbal Park in SRF (UMTZCP040519–122).
All observed individuals had stocky body; flattened heads; tympanum covered by skin; supratympanic fold distinct; first finger longer than second; inner and outer metacarpal tubercles distinct; toes completely webbed; dorsum paler brown with numerous dark blotches and indistinct blackish dorsolateral stripe; venter smooth and yellowish white. Morphological features of these individuals closely resemble Occidozyga martensii based on photographic material illustrated in
Both individuals were observed perched on a leaf overhanging the pond, and they quickly escaped into the water when approached.
Three specimens were collected from SRF consisted of males (UMTZC1484 and UMTZC1563, SVL 29–36 mm) and female (UMTZC1614, SVL = 43 mm).
All specimens were previously identified as Kalophrynus cf. pleurostigma and were re-examined following the description of populations from Peninsular Malaysia by
All specimens were collected from the trekking trails and artificial pond within the Herbal Park at SRF. No calling was heard, but K. kiewi was frequently found on the forest litter and generally towards the monsoon season. This species is a new record for the amphibians in Hulu Terengganu.
Two male specimens were collected from SRF (UMTZC1486 and UMTZC1632 = 35–38 mm).
Morphological characters of the specimens agreed well with the description by
Specimens of this species were collected from the open areas of the camping site, and trekking trail of the Herbal Park at SRF, among leaf litter and rotten logs. Brief calling was heard from a specimen found at the camping site in mid-November. This species is a new record for the amphibians in Hulu Terengganu.
Five specimens (formerly identified as K. baleata) were collected from SRF consisted of juvenile (UMTZC1011, SVL = 20 mm) and adult males (UMTZC1310, UMTZC1316, UMTZC1464, and UMTZC1482, SVL = 35–64 mm).
Morphological characters of the specimens agreed well with the description of northern populations from Peninsular Malaysia by
Kaloula latidisca was frequently spotted on tree trunks around the open and recreational areas, and occasionally at the small streams of the Peres River at SRF. No calling was heard, but K. latidisca was typically found in mid-November and possibly until the end of the monsoon season. This species is a new record for the amphibians in Hulu Terengganu.
Four specimens were collected from SRF (Juvenile: UMTZC1414, SVL = 15 mm; Males: UMTZC1082 and UMTZC1415, SVL = 57–62 mm) and SAP (Male: UMTZC1056 = 45 mm).
Morphological characters of the specimens agreed well with the description by
Kaloula pulchra was ubiquitous in open and recreational areas in SLF, with a tendency to be encountered hiding in irrigation ditches, drains, and toilets. The calls of adult males were heard during and after the heavy rains.
Three male specimens were collected from SRF (UMTZC1457, SVL = 12 mm) and SAP (UMTZC1062 and UMTZC1063, SVL 13–14 mm).
Morphological characters of the specimens agreed well with the description by
UMTZC1457 was collected from the recreational zone within SRF in leaf litter, UMTZC1062 and UMTZC1063 were found at the roadside within SAP, also in leaf litter. Additional individuals were observed inside the artificial ponds at the Herbal Park within SRF during the mid-monsoon season.
Eight male specimens were collected from SAP (UMTZC1064, UMTZC1217, UMTZC1218, UMTZC1219, UMTZC1220, UMTZC1221, UMTZC1222, and UMTZC1223, SVL = 21–25 mm).
Morphological characters of the specimens agreed well with the description by
Microhyla butleri was usually found beneath piles of leaf litter and occurs throughout SLF. Despite the fact that all collected specimens were from SAP, many individuals of this species were observed on leaf litter, mostly along roadsides and trekking trails within SRF.
Nine specimens were collected from SRF (Males: UMTZC1028, UMTZC1067, UMTZC1224, and UMTZC1226, SVL = 17–24 mm; Females: UMTZC1008 and UMTZC1066, SVL = 25–27 mm) and SAP (Males: UMTZC1320 and UMTZC1489, SVL = 17–20 mm; Female: UMTZC1343, SVL = 29 mm).
Morphological characters of the specimens agreed well with the description by
Microhyla cf. heymonsi was commonly found beneath piles of leaf litter and in rock crevices throughout SLF. This species was also found to occur in similar man-made ponds as with other species of Microhyla. Active and loud calling could be heard from this species after rains. The species is considered a commensal species that is tolerant of habitat alteration (
One specimen was collected from SRF (UMTZC1761, SVL = 18 mm).
Morphological characters of the specimen agreed well with the description by
Microhyla superciliaris can be easily mistaken for M. butleri that occurs syntopically in the leaf litter at SLF. This species is a new record for the amphibians in Hulu Terengganu.
Five specimens were collected from SRF consisted of males (UMTZC1519, UMTZC1521 and UMTZC1573, SVL = 18–23 mm) and females (UMTZC1520 and UMTZC1523, SVL = 23–26 mm).
Morphological characters of the specimens closely resembled the newly described Micryletta dissimulans from Saba Yoi District, Songkhla Province, Southern Thailand (
Micryletta dissimulans was commonly found at open areas with grass or places with piles of dead leaves. This species is typically found in early November of each year until the end of the monsoon season. This species is a new record for the amphibians in Hulu Terengganu.
The only female specimen ever collected (UMTZC1302, SVL = 38 mm) which deposited as voucher without much associated information of habitat or site, but with a date of 2014 from SLF.
Morphological characters of the specimens agreed well with the description by
The available information of this species is limited to a description and photograph of a preserved specimen; however, it is presumed to be found within SRF.
Fourteen specimens were collected from SRF (Juvenile: UMTZC1406, SVL = 28 mm; Males: UMTZC1051, UMTZC1052, UMTZC1091, UMTZC1159, and UMTZC1256, SVL = 40–54 mm; Females: UMTZC1127, UMTZC1160, UMTZC1161, UMTZC1166, and UMTZC1192, SVL = 60–70 mm) and SAP (Juvenile: UMTZC1468, SVL = 35 mm; Males: UMTZC1455 and UMTZC1603, SVL = 40–48 mm).
Morphological characters of the specimens agreed well with the description by
Leptobrachium hendricksoni was common along small streams, cleared areas and man-made ponds in SLF. This species is usually found hiding among grass, on the ground or leaf litter. The tadpoles of L. hendricksoni can be found in the small streams, throughout the year.
Eight male specimens were collected from SLF (UMTZC1378, UMTZC1379, UMTZC1408, UMTZC1409, UMTZC1410, UMTZC1411, UMTZC1473, and UMTZC1521, SVL = 20 to 27 mm).
Morphological characters of the specimens agreed well with the description of L. sola by
Leptobrachella sola is commonly found near the stream banks, and is usually sighted sitting on low vegetation, bare ground, or piles of dead leaves. This species can be hard to spot during the night as they usually hide amongst the leaf litter and quickly hides beneath the litter when approached.
Three specimens were collected from SLF (Juveniles: UMTZC1103 and UMTZC1187, SVL = 36–38 mm; Male: UMTZC1494, SVL = 94 mm).
Morphological characters of the specimens agreed well with the description by
Pelobatrachus nasutus were found on the forest floor at various locations: UMTZC1494, UMTZC1103 and UMTZC1187 were collected from the small stream of Peres Rivers where it was sighted on the forest floor. Afterwards, two individuals were observed on the forest floor beside the recreational trail at SRF, and three individuals were observed amongst the dead leaves at the banks of the small stream of the Peres River. Loud callings can be heard typically near the monsoon season.
Thirteen specimens were collected from the SLF consisted of adult males (UMTZC1030, UMTZC1032, UMTZC1036, UMTZC1041, UMTZC1043, UMTZC1045, UMTZC1046, UMTZC1106, UMTZC1137, UMTZC1378, and UMTZC1505, SVL = 30–38 mm) and females (UMTZC1297 and UMTZC1377, SVL = 48–53 mm).
Morphological characters of the specimens agreed well with the description by
A Amolops gerutu B Chalcorana labialis (pale yellow colouration) C C. labialis (brown colouration) D Humerana miopus E Hylarana erythraea F Indosylvirana nicobariensis G Odorrana hosii H Pulchrana glandulosa I P. laterimaculata J P. sundabarat (orange dorsolateral stripe) K P. sundabarat (yellow dorsolateral stripe) and L Sylvirana malayana.
This species can only be found along the torrential zones of the Peres and Bubu Rivers in SLF. The species can be observed perched on the surfaces of boulder stacks along the streams, and occasionally on adjacent low vegetation. Tadpoles of A. gerutu can found clinging to boulders below the waterline.
Twelve specimens were collected from SRF consisted of one juvenile (UMTZC1032, SVL = 20 mm), males (UMTZC1029, UMTZC1090, UMTZC1235, UMTZC1236, UMTZC1237, UMTZC1383, and UMTZC1384, SVL = 29–36 mm) and females (UMTZC1132, UMTZC1297, UMTZC1317, and UMTZC1622, SVL = 49–55 mm).
Morphological characters of the specimens agreed well with the description by
This species can be found at many swampy locations and flowing streams within SLF. Chalcorana labialis was usually observed perched on the surface of low vegetation along the streams and swampy areas, and was occasionally found at artificial ponds. All collected and observed individuals were found lower than 2 metres from the ground.
Four specimens were collected from SRF consisted of juvenile (UMTZC1682, SVL = 23 mm), males (UMTZC1007 and UMTZC1379, SVL = 62–65 mm) and female (UMTZC1472, SVL = 70 mm).
Morphological characters of the specimens agreed well with the description by
Humerana miopus was common at the artificial ponds of the Herbal Park in SRF. The species was frequently observed perched on low vegetation beside the artificial ponds, and quickly leapt into the water when disturbed.
Eight specimens were collected from SAP consisted of juvenile (UMTZC1264, SVL = 25 mm), males (UMTZC1182, UMTZC1183, UMTZC1184, and UMTZC1186, SVL = 30–40 mm) and females (UMTZC1050, UMTZC1055, and UMTZC1165, SVL = 42–73 mm).
Morphological characters of the specimens agreed well with the description by
Hylarana erythraea was common in the swampy areas in SAP. The species was also observed by drains, artificial ponds, and sometimes on grassy areas.
Three specimens were collected from SRF consisted of one male (UMTZC1571, SVL = 50 mm) and two females (UMTZC1563 and UMTZC1676, SVL = 42–43 mm).
Morphological characters of the specimens agreed well with the description by
This species was common at the Herbal Park in SRF. The species can be observed perching on rock surfaces at artificial ponds and is abundant at the start of monsoon season. Indosylvirana nicobariensis is a pond-breeding frog and can inhabit both natural and altered habitats (
Twenty adult specimens were collected from SRF (Males: UMTZC1164, UMTZC1170, UMTZC1171, UMTZC1172, UMTZC1173, UMTZC1174, UMTZC1233, UMTZC1299, and UMTZC1304, SVL = 32–66 mm; Females: UMTZC1009, UMTZC1044, and UMTZC1063, SVL = 54–96 mm) and SAP (Males: UMTZC1348, UMTZC1351, UMTZC1385, and UMTZC1504, SVL = 32–50 mm; Females: UMTZC1306, UMTZC1323, UMTZC1380, and UMTZC1481, SVL = 48–98 mm).
Morphological characters of the specimens agreed well with the description by
Odorrana hosii was ubiquitous at the rocky sections of streams with many boulders. All individuals were collected at night but specimens could be observed in the day hiding in the roots of large trees at the stream bank.
Four male specimens were collected from SRF (UMTZC1301, UMTZC1350, UMTZC1576, and UMTZC1608, SVL = 43–74 mm).
Morphological characters of the specimens agreed well with the description by
Pulchrana glandulosa was found in the small streams and recreational areas of SLF. The species was commonly observed hidden amongst piles of dead leaves and rotten logs.
One specimen of adult female specimen was collected from SLF (UMTZC1699, SVL = 50 mm).
Morphological characters of the specimen agreed well with the description by
Pulchrana laterimaculata can be found in areas similar to P. glandulosa in SLF. The species was commonly observed hidden among piles of dead leaves and rotten logs.
Four specimens were collected from SRF consisted of three males (UMTZC1376, UMTZC1377, and UMTZC1387, SVL = 40 mm) and one female (UMTZC1375, SVL = 57 mm).
Morphological characters of the specimens agreed well with the description by
Seven specimens were collected from SRF (Males: UMTZC1013, UMTZC1014, UMTZC1107, and UMTZC1382, SVL = 43–47 mm; Females: UMTZC1093 and UMTZC1381, SVL = 51–58 mm) and SAP (Males: UMTZC1308, SVL = 45 mm).
Morphological characters of the specimens agreed well with the description by
Sylvirana malayana can be found in the disturbed areas of SLF. This species was commonly observed hiding between rock crevices within the Herbal Park.
Ten adult specimens were collected from SRF (Males: UMTZC1095, UMTZC1345, UMTZC1360, UMTZC1361, UMTZC1463, UMTZC1465, UMTZC1574, and UMTZC1627, SVL = 30–41 mm; Female: UMTZC1359, SVL = 44 mm) and SAP (Male: UMTZC1502, SVL = 22 mm).
Morphological characters of the specimens agreed well with the description by
Kurixalus chaseni can be found perched on low vegetation within artificial ponds of the Herbal Park. Active calls of males can be heard from this place during the monsoon season in SLF.
Three adult male specimens were collected from SRF (UMTZC1425 and UMTZC1426, SVL = 29–30 mm) and SAP (UMTZC1601, SVL = 35 mm).
Morphological characters of the specimens agreed well with the description by
UMTZC1601 was found on low vegetation, less than 1 m from the ground near the suspension bridge at SAP, and UMTZC1426 and UMTZC1425 were found at bushy areas within a small stream off the Peres River in SRF. This species is a new record for the amphibians in Hulu Terengganu.
One adult male specimen was collected from SAP (UMTZC1871, SVL = 67 mm).
Morphological characters of the specimen agreed well with the description by
This species was found at the waterfall of SAP, perched on low vegetation less than 2 m from the ground.
Twenty-seven specimens were collected from SLF consisted of males (UMTZC1012, UMTZC1015, UMTZC1016, UMTZC1024, UMTZC1081, UMTZC1094, UMTZC1096, UMTZC1113, UMTZC1115, UMTZC1185, UMTZC1240, UMTZC1273, UMTZC1421, UMTZC1509, UMTZC1510, UMTZC1589, and UMTZC1592, SVL = 40–53 mm) and females (UMTZC1006, UMTZC1027, UMTZC1157, UMTZC1179, UMTZC1241, UMTZC1423, UMTZC1424, UMTZC1496, UMTZC1590, and UMTZC1591, SVL = 60–71 mm).
Based on description by
This species was common in both natural and man-made habitats of SLF. Most of the collected and observed individuals were found clinging to shrubs or leaves of low vegetation less than 2 m from the ground. This species is a new record for the amphibians in Hulu Terengganu.
Twenty-seven specimens were collected from SLF consisted of males (UMTZC1010, UMTZC1114, UMTZC1128, UMTZC1131, UMTZC1180, UMTZC1181, UMTZC1243, UMTZC1244, UMTZC1246, UMTZC1328, UMTZC1329, UMTZC1422, UMTZC1485, UMTZC1624, and UMTZC1417, SVL = 40–52 mm) and females (UMTZC1125, UMTZC1130, UMTZC1154, UMTZC1155, UMTZC1156, UMTZC1178, UMTZC1245, UMTZC1263, UMTZC1272, UMTZC1344, UMTZC1347, and UMTZC1444, SVL = 44–67 mm).
Morphological characters of the specimens agreed well with the description by
Polypedates leucomystax can be distinguished from P. discantus by having the skin of the head fused with the skull, distinct white spots or reticulations on a dark background on the rear thigh, and the absence of a tubercle at the heel. This species known as a commensal species and inhabits all manner of human-made and natural habitats in SLF. This species can be observed clinging onto shrubs or the leaves of low vegetation up to 2.5 m off the ground.
Nine specimens were collected from SRF consisted of males (UMTZC1327, UMTZC1346, UMTZC1418, UMTZC1419, and UMTZC1497, SVL = 60–68 mm) and females (UMTZC1030, UMTZC1097, UMTZC1416, and UMTZC1454, SVL= 62 to 102 mm).
Morphological characters of the specimens agreed well with the description by
Polypedates macrotis is restricted to natural or man-made stagnant water bodies closer to the forested areas. This species can also be observed perched on low vegetation near the ponds in syntopy with other species of Polypedates.
Two specimens were collected from SRF consisted of subadult male (UMTZC1732, SVL = 60 mm) and adult male (UMTZC1057, SVL = 95 mm).
Morphological characters of the specimens agreed well with the description by
UMTZC1057 was collected from a fallen large tree at the Herbal Park within SRF while the second individual UMTZC1732 was found perched on low vegetation at the same location. This species was only encountered during the monsoon season in SLF.
Two male specimens were collected from SRF (UMTZC1111 and UMTZC1110, SVL = 49–53 mm).
Morphological characters of the specimens agreed well with the description by
Both UMTZC1111 and UMTZC1110 were collected from the large trees beside the artificial pond of the camping site in SRF.
One male specimen was collected from SAP (UMTZC1490, SVL = 28 mm).
Morphological characters of the specimen agreed well with the description by
Theloderma licin was found resting on the ground within piles of dead leaves. This species is a new record for the amphibians in Hulu Terengganu.
No specimen was collected, but photographs of this species from from previous fieldwork in 2014 in SRF (UMTZCP070614-392, Fig.
Examined photographs show similar characteristics as described by
This species was found among the dense vegetation on steep terrain in the forested areas in SRF. Theloderma horridum was spotted clinging to the side of a tree trunk facing upwards.
Two male specimens were collected from SRF (UMTZC1469 and UMTZC1299, SVL = 56–57 mm).
Morphological characters of the specimens agreed well with the description by
Two specimens of Zhangixalus prominanus were collected from the flooded rock pools within the recreational zones of SRF. Another observed individual was also seen perched on low vegetation or rock surfaces in the same area, only found during the monsoon season. This species is a new record for the amphibians in Hulu Terengganu.
UMTZCP110414-419.
One individual of Zhangixalus tunkui was previously recorded in SRF. However, it was only photographed (UMTZCP110414-419, Fig.
The individual of this species was found at the flooded rock pools in SRF. This species is a new record for the amphibians in Hulu Terengganu.
From 14 species recorded in the first survey in 2003, the number of species had steadily increased to 18 species in 2008. The surveys continued in 2013 and recorded more species, with a total of 38 species in 2015. This trend of species discoveries kept increasing during the surveys up to the end of 2020. The results shown by the species accumulation curve generated from the list of species recorded between 2003 and 2018 show a constantly increasing trend (Fig.
Compilation of updated and revised checklist of amphibian fauna from published materials and this study in Hulu Terengganu, Terengganu. Note: DD = Data Deficient, NE = Not Evaluated, LC = Least Concerned, NT = Near Threatened, EN = Endangered, NP = Not Protected, and P = Protected. Symbol * = represents the additional record of species in Hulu Terengganu, 1 = Sekayu (This study), 2 = Gunung Lawit (
No | Species | IUCN Status | WCA 2010 | 1 | 2 | 3 | 4 |
---|---|---|---|---|---|---|---|
Family Ichthyophiidae | |||||||
1 | Ichthyophis cf. asplenius* | DD | NP | + | – | – | – |
2 | Ichthyophis glutinosus | VU | NP | – | – | + | – |
3 | Ichthyophis sp. | DD | NP | – | + | + | – |
Family Bufonidae | |||||||
4 | Ansonia latiffi | NT | NP | + | + | – | + |
5 | Ansonia lumut | NE | NP | + | + | – | – |
6 |
Duttaphrynus bengalensis
(Duttaphrynus sp.1) |
LC | NP | + | – | + | – |
7 | Ingerophrynus parvus | LC | NP | + | + | + | + |
8 | Ingerophrynus quadriporcatus | LC | NP | – | + | + | – |
9 | Leptophryne borbonica | NE | NP | + | + | + | + |
10 | Phrynoidis asper | LC | NP | + | + | + | + |
11 | Rentapia flavomaculata | NE | NP | + | + | + | – |
Family Dicroglossidae | |||||||
12 | Fejervarya cancrivora | LC | NP | – | – | + | – |
13 | Fejervarya limnocharis | LC | NP | + | + | + | + |
14 | Ingerana tenasserimensis | LC | NP | – | – | + | – |
15 | Limnonectes blythii | NT | P | + | + | + | + |
16 | Limnonectes hascheanus | LC | NP | + | – | – | + |
17 | Limnonectes utara | NE | NP | + | + | + | + |
18 | Limnonectes deinodon | NE | NP | + | + | + | – |
19 | Limnonectes malesianus | NT | P | + | – | + | – |
20 | Limnonectes tweediei | LC | P | – | + | – | – |
21 | Limnonectes paramacrodon | NT | P | – | + | – | + |
22 | Limnonectes plicatellus | LC | NP | + | + | + | – |
23 | Occidozyga sumatrana | LC | NP | + | + | + | – |
24 | Occidozyga martensii | LC | NP | + | + | – | – |
Family Megophryidae | |||||||
25 | Leptobrachium hendricksoni | LC | NP | + | + | + | + |
26 | Leptobrachella heteropus | LC | NP | – | – | + | + |
27 | Leptobrachella sola | EN | NP | + | + | – | – |
28 | Pelobatrachus nasutus | LC | P | + | + | + | + |
29 | Xenophrys aceras | LC | P | – | + | – | – |
Family Microhylidae | |||||||
30 | Chaperina fusca | LC | NP | – | – | + | – |
31 | Kalophrynus kiewi | NE | NP | + | + | + | – |
32 | Kalophrynus palmatissimus* | EN | P | + | – | – | – |
33 | Kaloula latidisca* | DD | NP | + | – | – | – |
34 | Kaloula pulchra | LC | NP | + | – | + | – |
35 | Microhyla bedmorei | LC | NP | + | + | + | – |
36 | Microhyla butleri | LC | NP | + | + | + | – |
37 | Microhyla heymonsi | LC | NP | + | + | + | – |
38 | Microhyla superciliaris* | LC | NP | + | – | – | – |
39 | Microhyla mantheyi | LC | NP | – | + | – | – |
40 | Micryletta dissimulans* | LC | NP | + | – | – | – |
41 | Metaphrynella pollicaris | LC | NP | – | + | – | – |
42 | Phrynella pulchra | LC | NP | + | – | + | – |
Family Ranidae | |||||||
43 | Abavorana luctuosa | LC | NP | – | + | – | – |
44 | Amolops gerutu | NE | NP | + | + | + | + |
45 | Chalcorana labialis | NE | P | + | + | + | + |
46 | Humerana miopus | LC | NP | + | – | + | – |
47 | Hylarana erythraea | LC | P | + | – | + | + |
48 | Indosylvirana nicobariensis | NE | NP | + | – | + | – |
49 | Odorrana hosii | LC | P | + | + | + | + |
50 | Pulchrana baramica | LC | NP | – | – | + | – |
51 | Pulchrana glandulosa | LC | NP | + | – | + | – |
52 | Pulchrana laterimaculata | LC | NP | + | + | + | – |
53 | Pulchrana sundabarat | LC | P | + | + | + | + |
54 | Sylvirana malayana | NE | NP | + | – | + | + |
Family Rhacophoridae | |||||||
55 | Kurixalus chaseni | NE | NP | + | + | – | – |
56 | Nyctixalus pictus* | NT | P | + | – | – | – |
57 | Philautus vermiculatus | LC | NP | – | + | – | – |
58 | Polypedates colletti | LC | P | + | + | + | – |
59 | Polypedates discantus* | NE | NP | + | – | – | – |
60 | Polypedates leucomystax | LC | NP | + | + | + | – |
61 | Polypedates macrotis | LC | NP | + | + | + | – |
62 | Rhacophorus rhodopus | LC | NP | – | + | – | – |
63 | Rhacophorus nigropalmatus | LC | P | + | + | – | – |
64 | Rhacophorus pardalis | LC | P | + | + | – | – |
65 | Rhacophorus norhayatiae | NE | NP | – | + | – | – |
66 | Theloderma leprosum | NE | NP | – | + | – | – |
67 | Theloderma horridum | LC | NP | + | + | – | – |
68 | Theloderma licin* | LC | NP | + | – | – | – |
69 | Zhangixalus prominanus* | LC | P | + | – | – | – |
70 | Zhangixalus tunkui* | NE | NP | + | – | – | – |
Total numbers of species | 52 | 44 | 41 | 18 |
The cumulative species discovery curve of the species (dotted line), species accumulation curve of replicated samples of the amphibians from previous and recent surveys (black line). Red line shows the estimated number of unique, and duplicate species (blue line) of amphibians from long term surveys in Sekayu lowland forest, Hulu Terengganu.
This extensive survey on amphibian fauna in SLF highlights the immense biodiversity that can be found on a local scale through long-term inventory study, hence demonstrating the potential of Hulu Terengganu forests as one of the nation’s important biodiversity spots. The approach also affirms the importance of long-term and comprehensive surveys, regardless of substantial time, cost and effort are needed, especially in tropical countries. The long-term surveys in SLF have successfully captured the variation in abundance and composition of amphibians between habitats and the temporal patterns that are apparently impossible in short-term or rapid surveys. In addition, continuous, standardised sampling efforts and multi-habitat surveys could provide the most useful baseline information on the status and trends of amphibian communities in tropical lowland forest for biodiversity monitoring.
Amphibian community particularly in tropical forests are closely related to seasonal factors (
Expanding the survey areas that have been overlooked before, such as hilly areas of forests and small streams, has been rewarding as additional species were added to the list. Hilly forested areas and small streams in fact serve as the better ground for foraging and breeding areas for many species of anurans (
However, certain species such as Phrynella pulchra, Theloderma horridum, and Zhangixalus tunkui remained undetected since their initial discoveries in 2013–2014, even though continuous surveys have been made since 2015. This might indicate that these secretive species cannot be detected by a simple method such as visual surveys alone and may require alternative techniques that effective on arboreal amphibians. Several studies noted that T. licin and P. pulchra occupied smaller tree holes closer to the ground, generally in the less disturbed areas (
The compilation of amphibian records from established inventories in Hulu Terengganu have demonstrated a great diversity of amphibians so far, with a total of 70 species compared to another studied area in Terengganu like Gunung Tebu and adjacent forests in Besut, which have a total of 50 amphibian species (
To date, there are 17 protected species of amphibians under the Wildlife Conservation Act 2010 (Act 716). Five species of ‘Near Threatened’, two species of ‘Endangered’ and one species of ‘Vulnerable’ amphibians found in Hulu Terengganu are listed on the IUCN Red List (IUCN, 2021). This area deserves attention for better protection of the species, especially for the endemic and threatened species in this area. More alarming, frequent changes in taxonomy and the description of many new species has put these species into a vulnerable state as most of them are not evaluated under the IUCN Red List. The problem with the Wildlife Conservation Act 2010 appears to be not comprehensive enough, and is outdated as there are only 17 species listed as protected, while many of the unique and newly described species such as Rhacophorus norhayatiae, Ansonia lumut, Limnonectes utara, and many others are not listed. This legislation requires immediate revision to offer better protection of these species from illegal trade and wildlife trafficking. Furthermore, many areas within Hulu Terengganu, even in SLF, are vulnerable to further deforestation if conservation action is not taken seriously. The benefits of this long-term data collection could be utilised to spread public awareness on the importance of biodiversity conservation and be extended for ecotourism benefits of this forest reserve.
Fifty-two amphibian species from 32 genera were recorded from SLF, making up a total of 70 species recorded in Hulu Terengganu District. Data such as this are a clear indication that extensive study and monitoring is the cogent approach in attempting to reveal the true diversity of a forest reserve. Working repeatedly and systematically in this locality during different months of the years from 2003 to 2020 has resulted in revealing the ecological complexity and high species richness within this area. This finding also denotes that varying sampling efforts influence the knowledge on species diversity of the studied area. This study emphasised that continuous efforts of documenting species diversity is crucial to ensuring the reliability and validity of species diversity harboured by any area or habitat. The available information on amphibian diversity in SLF and Hulu Terengganu can hopefully be used to assist conservation programmes and long-term monitoring of biodiversity. In another way, remarkable species diversity of recreational forests and other areas should be preserved as it can be used to nurture conservation awareness and promote scientific citizenship amongst the local folks to work together to protect the biodiversity at this recreational forest.
We wish to thank, Department of Forestry Terengganu for granting permission to conduct research at Sekayu lowland forest and to Faculty of Science and Marine Environment, Universiti Malaysia Terengganu for providing facility and equipment to conduct the field survey and laboratory works. We would like to thank Mr Mazrul Aswady, Izzat Husna, Izwan Anas and Najwa Sawawi for assistances during the fieldwork. We are also deeply grateful to the Department of Wildlife and National Parks Malaysia (DWNP) (research permit: T-00563-16-17), Department of Forestry Peninsular Malaysia (JPSM), Forestry Department of Terengganu, Sekayu Recreational Forest staffs, Agriculture Department of Terengganu, and Sekayu Agricultural Park’s authorities for permission to conduct the study. Anuar McAfee (Universiti Sultan Zainal Abidin, UniSZA, Terengganu) reviewed the English language.