Keywords

Introduction

Reptiles play important roles in ecosystems , as prey and predators, grazers, agents for seed dispersal, commensal species , and their often specific microhabitat associations may be used to illustrate evolutionary processes of speciation (Raxworthy et al. 2008; Read 1998). Due to its ecological relevance, the declines of reptile populations may cause negative impact on the natural systems. In order to maintain healthy ecosystems, biodiversity studies are crucial as they provide the knowledge to prioritize conservation areas and habitats, and to model sustainable use of resources (Sohdi et al. 2004). Species richness data for instance are vital so that the responsible authorities are aware of the wildlife present in an area. Mitigation measures that need to be included in the development plans considering the plight of the animals can be developed using the data, thus ensuring the continued existence of the species in their natural habitat . Without substantial amount of biodiversity publications, species will be prone to extermination as no action taken on threats faced by a particular species.

In Malaysia , most of the reptile studies were focusing on species richness (Sumarli et al. 2015, 2016; Voris 2015; Shahriza and Ibrahim 2014; Nurulhuda et al. 2014; Amirah et al. 2013; Quah et al. 2013; Shahriza et al. 2012; Chan et al. 2010a, b; Ibrahim et al. 2008, 2012, 2013; Grismer et al. 2004, 2006, 2014a, b, c) and only a single study have been published on the estimation of species richness (van Rooijen et al. 2011). It has been reported that 397 species of reptiles have been recorded around Malaysia and among them, an approximate of 256 species (65%) were identified to be present in Peninsular Malaysia (Das and Norsham 2007). Since then, many new species have been discovered along with the rediscovery of rare species (Grismer et al. 2008a, b, c, 2009, 2010a, b, 2011, 2014a, b, c, 2016a, b, c, d; Sumarli et al. 2016; Grismer and Quah 2015; Johnson et al. 2012; Grismer 2008, 2011; Chan et al. 2010a; Wood et al. 2009). These discoveries clearly show that Malaysian forests are very rich in reptile assemblage, which underlines the need for more studies and surveys to be carried out.

Reptiles in Tasik Kenyir , Hulu Terengganu are still understudied although this place is a home to a significant number of flora and fauna (Faizah et al. 2015). Therefore, this study was conducted to examine the species richness of reptiles in selected sites surrounding Tasik Kenyir, Terengganu. It is hoped that this study can be useful for future reptile studies, and for the conservation and management purposes at Tasik Kenyir and other similar habitats particularly in Terengganu.

The survey was conducted from April 2015 to February 2016 at four sampling sites located at and around Tasik Kenyir , Terengganu , namely Sungai Buweh, Belukar Bukit , Sekayu and Saok , (Table 1, Fig. 1). These four sampling sites are recreational areas surrounded by lowland dipterocarp forests. They were chosen as the study sites because there were no or very limited information on reptilian fauna of these areas which may harbour a diverse set of species .

Table 1 List of sampling sites, dates and methods used
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Fig. 1
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Map showing the four sampling sites around Tasik Kenyir , Hulu Terengganu. (Source: Google Maps)

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In this study, pitfall trapping method was used to collect samples at all sites but not in all occasions. In order to increase the probability of reptiles to fall into the traps , drift fences from aluminium sheets, wire nets or fallen logs were used. The numbers of pitfall traps used were unequal between sampling sites due to geographical constraint and manpower limitations. Visual Encounter Surveys (VES) was also conducted to search and to collect reptiles. Active searching were carried out for three sessions per day (in the morning, evening and at night time) along an approximately 1 km transect, for 2–3 h per session. All observed reptile species were recorded and captured, when possible, using sweep nets, hand-picking device, or simply by hand grabbing.

The specimens were placed inside an individual plastic or cloth bag and were taken back to the laboratory for sample processing. Voucher specimens were preserved in 10% formalin and stored in 70% ethanol and deposited in laboratory situated in Centre of Kenyir Ecosystems Research, Kenyir Research Institute , Universiti Malaysia Terengganu (UMT) for future reference. Taxonomy of reptiles or species identification was based on Das (2004, 2007, 2010). The conservation status of the reptile species was assessed based on IUCN Red List of Threatened Species (IUCN 2016) and Wildlife Conservation Act 2010.

To estimate the species richness of reptiles in the study area, the data were analysed using non-parametric richness estimators calculated in EstimateS version 9.1 (Colwell 2013) Chao 1 and Chao 2 (Chao 1984). Chao 1 uses abundance -based data while Chao 2 uses incidence-based data. These estimators use information on the frequency of rare species in a sample to estimate the number of undetected species in an assemblage (Gotelli and Chao 2013; Gotelli and Colwell 2011).

Checklist of Reptiles

From 46 sampling days, 118 individuals of reptiles from nine families, 19 genera and 26 species were recorded from study sites at and around Tasik Kenyir , Terengganu (Table 2). The most abundant family was Gekkonidae (42%) followed by Agamidae (23%), Scincidae (11%), and the other six families, Geoemydidae, Trionychidae, Varanidae, Colubridae, Elapidae and Viperidae each contributed 4% for the total number of species (Fig. 2). The most diverse reptile genus recorded were Hemidactylus with three species followed by two species for Draco, Gonocephalus, Cyrtodactylus, Gekko and Eutropis each. Only one species was recorded for the genus Cyclemys, Dogania, Aphaniotis, Calotes, Cnemaspis, Gehyra, Hemiphyllodactylus, Luperosaurus, Lipinia, Varanus, Calamaria, Naja and Tropidolaemus. The proportion of species that have been assessed for their conservation status was 54%. Based on IUCN 2016, only nine out of the 26 species were categorised as Least Concern and the rest were not yet assessed. In Wildlife Conservation Act 2010, 11 of the total species recorded were protected , mostly in the Agamidae family .

Table 2 Checklist of reptiles in selected sites of Tasik Kenyir , Terengganu
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Fig. 2
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Composition of reptile in each family in selected sites of Tasik Kenyir , Terengganu

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The numbers of reptile species estimated by Chao 1 and Chao 2 estimators were all higher than the number of observed species, 26 (Table 3, Fig. 3). The percentage of observed richness based on the estimated richness of Chao 1 and Chao 2 was 74% and 67% respectively.

Table 3 Number of estimated species from abundance - and incidence-based richness estimators, and the percentage of predicted richness actually observed of reptiles in the study area
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Fig. 3
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Observed species , S(obs), Chao 1 and Chao 2 estimator curves for number of reptile species

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In this study, Belukar Bukit and Sekayu have the highest number of reptile species , mainly because the sampling duration in these study sites were longer, 14 and 15 days respectively, compared to Sungai Buweh (10 days) and Saok (seven days). Restricted time allows limited coverage area for sampling activities, thus contributes to limited finding of species (Ibrahim et al. 2012; Shahriza et al. 2012). Herpetological surveys especially require longer periods of sampling due to the elusive and secretive nature of amphibians and reptiles (Ibrahim et al. 2013) therefore additional surveys in the study sites are necessary to increase the chances of species detection. Gekkonidae was found to be the most dominant family at Tasik Kenyir with almost half of the total species recorded (42%) were from this family . This is because most of the species in this family such as Gehyra mutilata, Gekko monarchus, G. smithii, Hemidactylus frenatus and H. garnotii were considered as commensal species and were easily spotted around human residences. Some of these species may come from nearby forested habitats to forage in human habitations where the food source is available.

Eutropis multifasciata from family Scincidae (Fig. 4) was the most abundant species (23.7%) recorded in this study, found at all study sites except Saok . This commensal species is known to be common in forest edges and around human settlements. The specimens of this species were found around buildings, along forest trails, and on rocky outcrops near water bodies. Two individuals of E. multifasciata, one in Sekayu and one in Belukar Bukit were caught in cage traps that were used by other zoological team members to catch small mammals . Two individuals of Cyclemys sp. were also caught in cage traps placed along the river banks in Belukar Bukit.

Fig. 4
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Eutropis multifasciata was observed basking on a rock at Taman Pertanian Sekayu, Kenyir, Terengganu . (Photograph by Fathihi Hakimi Rosmidi)

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In this study, only three snake species managed to be recorded. Calamaria pavimentata was observed on the ground near rocky area of Sungai Buweh waterfall while Naja kaouthia and Tropidolaemus wagleri (Fig. 5) were both found along the river at Sekayu. The low number of snakes spotted may be due to their highly elusive and cryptic behaviour. Longer sampling duration may not necessarily produce a higher number of snake species encountered. For instance, only three species of snakes were documented by Ibrahim et al. (2012) in Bukit Perangin Forest Reserve , Kedah from January 2009 till end of May 2010.

Fig. 5
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Tropidolaemus wagleri, Wagler’s keeled green pit viper (female)

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One of the interesting species encountered in the study area was Luperosaurus browni (Fig. 6), which was found tangled in a mist nest deployed for bird survey at Saok . This species is highly elusive as it dwells in the canopy , and the grey-brown colouration of this small gecko enables it to camouflage well on tree trunks.

Fig. 6
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Luperosaurus browni (Brown camouflage gecko) found in Saok , Tasik Kenyir , Terengganu

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The Chao 1 and Chao 2 species richness estimator showed a completeness of 74% and 67% respectively. Although this result revealed an acceptable estimate based on the sampling efforts (Shazali et al. 2016), additional surveys with standardised sampling methods are highly recommended to better estimate the reptile species composition at Tasik Kenyir . The duration of sampling of this study ranged from seven to 15 days per study site, which was not enough to cover the entire forests, rivers and waterfalls, especially with limited manpower.

Conclusion

Based on this study, Tasik Kenyir is expected to hold a higher number of reptile species , as suggested by the estimators (up to 39 species), and the opportunities to discover rare and new species are infinite. Extensive surveys covering areas deep in the forest that are more pristine should be conducted to establish a better picture of its reptile diversity . All of the study sites are always frequented by visitors from time to time therefore it is hoped that this study would be useful for the management purposes of Tasik Kenyir. The composition of reptiles and other taxa should be taken into account before any changes to the habitat is made in order to avoid species loss especially for species that are sensitive to environmental changes.