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Morphological and Molecular Identifcation of Sea Cucumber Pertanika J. Trop. Agric. Sci. 40 (1): 161 - 172 (2017) TROPICAL AGRICULTURAL SCIENCE Journal homepage: http://www.pertanika.upm.edu.my/ Morphological and Molecular Identification of Sea Cucumber species Holothuria scabra, Stichopus horrens and Stichopus ocellatus from Kudat, Sabah, Malaysia Kamarul Rahim Kamarudin*, Maryam Mohamed Rehan and Nur Aliah Bahaman Food Biotechnology, Faculty of Science and Technology, Universiti Sains Islam Malaysia, 71800 USIM, Nilai, Negeri Sembilan, Malaysia ABSTRACT The abundance of sea cucumbers (Phylum Echinodermata: Class Holothuroidea) in Malaysian waters has been gradually declining in past decades. Due to the lack of recent studies on the status of sea cucumber populations in Kudat, Sabah, Malaysia, this study was conducted. This study aimed to identify the species of a timun laut morphospecies i.e. Holothuria (Metriatyla) scabra and two gamat morphospecies i.e. Stichopus horrens and Stichopus ocellatus that were collected from Limau Limawan based on ossicle shapes and non-protein-coding 12S mitochondrial rRNA gene sequences. A number of five main ossicle shapes were microscopically identified without microscopic size measurement i.e. rod, plate, rosette, button and table. However, a number of ossicle shapes for S. horrens and S. ocellatus recorded in the previous studies were not observed in this study and this could be due to the body deformation of the specimens. Interestingly, five specimens of H. scabra exhibited additional ossicle shapes other than the smooth button and the table. Despite the absence of common ossicles and the presence of additional ossicle shapes, 12S mitochondrial rRNA gene sequences analysed using the Basic Local Alignment Search Tool programme for Nucleotide (blastn) resulted in the species identification of the specimens of morphospecies H. scabra and S. horrens as H. scabra and S. horrens; however, the specimen of morphospecies S. ocellatus was identified only up to the genus level i.e. genus Stichopus, showing the lack of 12S mitochondrial rRNA gene sequences of S. ocellatus in the GenBank until 15 September, 2016. ARTICLE INFO In total, 31 partial sequences of 12S Article history: Received: 28 April 2016 mitochondrial rRNA gene were registered Accepted: 10 November 2016 with the GenBank (Accession No.: E-mail addresses: KX913672-KX913702). The findings also [email protected] (Kamarul Rahim Kamarudin), [email protected] (Maryam Mohamed Rehan), suggested that species identification based [email protected] (Nur Aliah Bahaman) * Corresponding author on 12S mitochondrial rRNA gene sequence ISSN: 1511-3701 © Universiti Putra Malaysia Press Kamarul Rahim Kamarudin, Maryam Mohamed Rehan and Nur Aliah Bahaman showed better inference than the ossicle making the country the fourth top producer shape identification. In summary, the three of sea cucumber products in the world after morphospecies were morphologically and Indonesia (35 commercial species), China genetically verified asH. scabra, S. horrens (27 commercial species) and the Philippines and S. ocellatus. Despite the fact that more (26 commercial species). specimens and more molecular techniques Holothuria (Metriatyla) scabra (Jaeger, are required to generate better conclusive 1833) is a timun laut species. However, in outcomes, the current findings give better Malaysia, some also regard it as a gamat insight into the importance of morphological species. It is locally known in Malaysia as and molecular approaches and the present bat putih (Kamarudin et al., 2015) or balat status of the timun laut species and gamat harimau putih (Abdullah, 2016). Its English species in Kudat. name is sandfish. It has a brackish grey dorsal part, dark wrinkle lines (upper side) Keywords: 12S mitochondrial rRNA gene, gamat, and a light grey ventral part (underside). The Holothuria scabra, Kudat, ossicle shape, Stichopus sandfish is one of Malaysia’s commercial horrens, Stichopus ocellatus, timun laut species of sea cucumber that are exploited as food (Choo, 2008). However, the species is INTRODUCTION regarded as “endangered, or at a high risk of In Malaysia, sea cucumber (Phylum extinction” based on the International Union Echinodermata: Class Holothuroidea) for Conservation of Nature (IUCN) Red List species can be categorised into two groups for aspidochirotid holothuroids (Conand i.e. gamat species and timun laut species et al., 2014). In order to restore the sea (Kamarudin et al., 2015). Gamat species cucumber species in Langkawi, sea ranching refers to all species of sea cucumber from of H. scabra is being carried out by the the family Stichopodidae including the Langkawi Development Authority (LADA) genus Stichopus and the genus Thelenota. in Teluk Yu, Temoyong, Langkawi and Tuba The term gamat also refers to sea cucumber Island, Langkawi (Sharif & Osman, 2016). species that are believed traditionally or Langkawi and Pangkor Islands are well proven scientifically to contain medicinal known in the sea cucumber-based traditional properties e.g. Stichopus horrens (Selenka, medicine industry in Peninsular Malaysia 1867) or the dragonfish. The timun laut or for the production of body fluid extracts (air non-gamat species refers to all species of gamat) and lipid extracts (minyak gamat). sea cucumber from other than the family S. horrens and Stichopus ocellatus Stichopodidae. Timun laut species are (Massin, et al., 2002) are among the gamat usually exploited as food in the beche-de- species in Malaysia. The total number of mer or trepang industry in Sabah, Malaysia. Malaysia’s gamat species to date is 10, Choo (2008) reported that 19 sea cucumber including eight Stichopus species and two species are commercialised by Malaysia, Thelenota species (Kamarudin et al., 2015). 162 Pertanika J. Trop. Agric. Sci. 40 (1) 162 - 172 (2017) Identification of three sea cucumber species from Kudat, Sabah S. horrens or dragonfish is locally known of the Sunda Platform area. Furthermore, as gamat emas or golden sea cucumber in Sabah is the most significant sea cucumber Malaysia due to its grey-brown colour and its fishery in Malaysia and the Sabah Fisheries use as the main ingredient in the production Department reported that about 139 tonnes of of air gamat and minyak gamat. Its old sea cucumber was landed in Sabah between scientific name was Stichopus variegatus 2000 and 2005 (DOF, 2000-2005). Kudat, a because its body is often variegated with town in the state of Sabah, is geographically dark patches; however; the scientific name located near the northernmost point of is no longer accepted. Meanwhile, a living Borneo Island in East Malaysia. Due to the specimen of S. ocellatus is yellow-orange lack of recent studies on sea cucumber in mottled with a green-grey colour and has Kudat, this town was chosen as the study eye-like, large papillae in its dorsal part site for this study. (Massin et al., 2002). The dragonfish is also In general, the aims of this study were one of Malaysia’s commercial species of to identify the species of a timun laut sea cucumber but S. ocellatus was not listed morphospecies i.e. Holothuria (Metriatyla) by Choo (2008). Moreover, S. horrens and scabra and two gamat morphospecies i.e. S. ocellatus are not included in the IUCN Stichopus horrens and Stichopus ocellatus Red List for aspidochirotid holothuroids as that were collected from Limau Limawan endangered or at risk of extinction and by based on ossicle shapes and non-protein- Conand et al. (2014) as vulnerable or at risk coding 12S mitochondrial rRNA gene of extinction; however Thelenota ananas sequences. Ossicles are small parts of and Stichopus herrmanni from the gamat calcified materials from sea cucumber. Their species group are in their lists. shapes, in fact, have continued to be an There are a lot of sea cucumber studies important characteristic for morphological focussing on Sabah, Malaysia as the main identification of sea cucumber (Kamarudin study site (Kamarudin et al., 2015). The & Mohamed Rehan, 2015). Furthermore, report by Ridzwan and Che Bashah (1985) mitochondrial DNA containing the 12S on the distribution of sea cucumbers in mitochondrial rRNA gene has been the Sabah and their use as a food resource is main subject of interest in zoological believed to be the first documentation of genetic studies due to its considerably the sea cucumber. According to Kamarudin effective maternal inheritance, continuous et al. (2009), at least three factors have replication, non-recombination, haploid contributed to the unique level of richness genome and greater rate of substitution as of the sea cucumber species in Sabah i.e. compared to ‘single-copy’ nuclear cells the extensive distribution of coral reefs, low (Nabholz et al., 2008). Therefore, ossicle level marine pollution and the possibility and non-protein-coding 12S mitochondrial of biogeographical factors within and out rRNA genes were used in this study for Pertanika J. Trop. Agric. Sci. 40 (1): 163 - 172 (2017) 163 Figure 1. The collection site of Holothuria (Metriatyla) scabra, Stichopus horrens and Stichopus ocellatus in Kudat, Sabah, Malaysia highlighted in red. [Adapted from Google earth Version 7.1.5.1557 (December 14, 2015)]. Kamarul Rahim Kamarudin, Maryam Mohamed Rehan and Nur Aliah Bahaman morphological and molecular sea cucumber species identification and verification. MATERIALS AND METHODS Study Site and Sampling A number of 30 specimens of H. scabra (PKS 1-PKS 30), one specimen of S. horrens (PKSH1) and one specimen of S. ocellatus (PKSO1) were collected fromFigure Figure2.
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