Li Lian WONG1, Siti Raudah ABDUL KADIR2, Rabi Atun ADAWIAH ABDULLAH1, Charlie Albert LASUIN3, Kok Onn KWONG4, and Takaomi ARAI5*
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ACTA ICHTHYOLOGICA ET PISCATORIA (2017) 47 (1): 73–79 DOI: 10.3750/AIEP/02072 EVIDENCE SUPPORTING THE OCCURRENCE AND THE ECOLOGICAL IMPLICATION OF GIANT MOTTLED EEL, ANGUILLA MARMORATA (ACTINOPTERYGII: ANGUILLIFORMES: ANGUILLIDAE), FROM SABAH, BORNEO ISLAND Li Lian WONG1, Siti Raudah ABDUL KADIR2, Rabi Atun ADAWIAH ABDULLAH1, Charlie Albert LASUIN3, Kok Onn KWONG4, and Takaomi ARAI5* 1Institute of Tropical Aquaculture, Universiti Malaysia Terengganu, Kuala Terengganu, Terengganu, Malaysia 2Institute of Oceanography and Environment, Universiti Malaysia Terengganu, Kuala Terengganu, Terengganu, Malaysia 3Faculty of Business, Economics and Accountancy, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia 4School of Biological Sciences, Universiti Sains Malaysia, Minden, Penang, Malaysia 5Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei Darussalam, Brunei Darussalam Wong L.L., Abdul Kadir S.R., Adawiah Abdullah R.A., Lasuin C.A., Kwong K.O., Arai T. 2017. Evidence supporting the occurrence and the ecological implication of giant mottled eel, Anguilla marmorata (Actinopterygii: Anguilliformes: Anguillidae), from Sabah, Borneo Island. Acta Ichthyol. Piscat. 47 (1): 73–79. Abstract. Although tropical anguillid eels account for two-thirds of all species in the genus Anguilla, the information on the species diversity, geographic distribution, and life histories of the tropical eels is very limited. Recent studies suggested that accurate species identification in the tropical anguillid eels needs a validation by molecular genetic analysis after morphological observation. Two anguillid eels found in Sabah, Borneo Island, were firstly identified as Anguilla marmorata Quoy et Gaimard, 1824 using morphological analysis and further analysis of mitochondrial 16S ribosomal RNA (16S rRNA) sequences confirmed the morphological species identification. The presently reported study represents the first description of A. marmorata in Sabah, Borneo Island. One-year survey suggests that representatives of A. marmorata found in the region might belong to the North Pacific population in the westernmost distribution. Keywords: tropical anguillid eel, diadromous fish, geographical distribution, marbled eel, Madagascar mottled eel, giant long-finned eel, tropical biodiversity The anguillid eels of the genus Anguilla Schrank, 1798 related to the ancestral form than their temperate-climate are widely distributed throughout the world. These eels counterparts. Thus, studying the biological aspects of have a catadromous life history, migrate between inland tropical eels provide clues for understanding the nature of waters and coastal growth habitats, and have offshore primitive forms of catadromous migration in freshwater spawning. Nineteen species/subspecies of freshwater eels eels and how the large-scale migration of temperate have been reported worldwide, including 13 from tropical species became established. regions (Ege 1939, Watanabe et al. 2013, Arai 2016). Of the The recent drastic decline of glass eel recruitment latter, seven species occur in the western Pacific around in Europe and East Asia has caused serious problems in Indonesia and Malaysia (Ege 1939, Arai 2016). Molecular eel stock to sustainable levels of adult abundance (Arai phylogenetic research on freshwater eels has revealed that 2014a). Tropical eels are considered a major target species tropical eels are the most basal species originating in the to compensate the high demand of eel resources. Recently, Borneo Island and that freshwater eels radiated out from freshwater eel biology such as species composition, the tropics to colonize the temperate regions (Minegishi et distribution and life history has been gradually al. 2005). Tropical freshwater eels must be more closely accumulated in tropical eel species in Peninsular Malaysia * Correspondence: Prof. Takaomi Arai, Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei Darussalam, Jalan Tungku Link, Gadong, BE 1410, Brunei Darussalam, phone: +673-2463001, fax: +673 2461502, e-mail: (TA) [email protected], (LLW) [email protected], (SRAK) [email protected], (RAAA) [email protected], (CAL) [email protected], (KOK) [email protected]. 74 Wong et al. (West Malaysia) (Arai et al. 2012, 2015, Arai and Chino 2013, Arai 2014b, Abdul Kadir et al. 2015, Arai and Sabah Wong 2016). The identification of eels at the species level using solely visual observation is suggested to be difficult South China because of the similarities and overlapping morphological Sea characteristics in eels, particularly tropical anguillids (Arai et al. 2015, Arai 2016, Arai and Wong 2016). Furthermore, such information about the geographical distribution, species composition, and life history is available in the limited area and little information is still available for Papar River many tropical eels across the Indo-Pacific region. In the presently reported study, we surveyed and collected two anguillid eels during a one-year sampling in Sabah, Borneo Island. These eels were subjected to identification using both morphological analyses and mitochondrial 16S ribosomal RNA (16S rRNA) sequence analyses. This paper describes the first confirmed record of a tropical anguillid eel, Anguilla marmorata Quoy et 5 km Gaimard, 1824, from Borneo Island. We also discussed the Sabah ecological implication and importance of the occurrence South 5 N° Brunei of A. marmorata in the region. Malaysia China Malaysia Eels and morphological analysis. During one-year (west) Sea survey between August 2015 and July 2016, two anguillid (east) eels were caught by a fishing rod and line, using sago Borneo 0 ° Indonesia worms as bait by local people in the Papar River, Papar Indonesia District, Sabah, Borneo Island, East Malaysia on 23 March and 2 May 2016 (Fig. 1, Table 1). The Papar River with a total flow length of approximately 60 km originates from 100 °E 105 °E 110 °E 115 °E the Crocker Range and flows towards a large floodplain and discharges into the South China Sea (Fig. 1). The Fig. 1. Eel sampling site in the Papar River, Manggis, Papar River has several tributaries, particularly in the Sabah, Borneo Island (East Malaysia) middle and upper reaches and approximately 85% of the floodplain area is flat alluvial, with the remainder either index (GSI; percent relative gonad weight to BW) was sandy ground or mangrove swamp (Chai et al. 2012). subsequently calculated. The Papar River floodplain is an important area for paddy Histology analysis. The histology of all specimens was growing and agriculture plantation, however its potential examined. Fragments from the middle region of one is limited by the loss of arable land caused by accelerated gonad were fixed in formalin for histological analysis. flooding and sedimentation (Chai et al. 2012). There are Tissue fragments were prepared for resin and routine two monsoon regimes, the southwest monsoon (May to paraffin embedding. Resin blocks were processed September) and the northeast monsoon (November to routinely and paraffin blocks were sectioned at 5 µm March). The northeast monsoon brings heavy rainfall and and stained with haematoxylin-eosin for histological the southwest monsoon normally signifies relatively drier observation. Histology classifications in female and male weather. Two eels were collected in the freshwater area were according to Arai (2014c) and Arai et al. (2016). where the eel inhabits were in deep and dark holes covered Molecular species identification. DNA was extracted with wilted leaves from the trees surrounding the area of from dorsal fin clip of each specimen using Gentra the river. Puregene Tissue Kit (QIAGEN, USA), according to the The external morphometric characteristics were manufacturer’s instruction. Total DNA concentration measured following Ege (1939) and Watanabe et al. and quality was quantified using BioPhotometer (2004), and the data are shown in Table 1. The fin Plus spectrophotometer (Eppendorf, Germany). difference index (FDI), which is the distance between the PCR amplification for 16S rRNA gene using verticals from beginning of the dorsal fin (Z) to the anus primer sets from Palumbi et al. (1991); L2510: (ano-dorsal length) relative to the total length (TL) (Ege 5′CGC CTG TTT ATC AAA AAC AT 3′ and H3080: 5′ 1939), was calculated as follows: CCG GTC TGA ACT CAG ATC ACG T 3′ was conducted according to Arai and Wong (2016). PCR amplicons FDI = 100Z · T L –1 were purified using QIAquick® PCR Purification Kit (QIAGEN, USA), labelled with BigDye Terminator The sex of each eel was determined by visual v.3.1 Cycle Sequencing Kit (Applied Biosystems and histological observations of the gonads. Whole Inc., USA) and sequenced bi-directionally on an gonad weight was measured, and gonadosomatic ABI PRISM 3730xl Genetic Analyzer. Generated Occurrence of Anguilla marmorata in Borneo 75 Table 1 Morphometric characters of Anguilla marmorata collected in Sabah, Borneo Island Specimen Parameter SB-1 SB-2 Total length (TL) [mm] 1309.0 688.0 Body weight [g] 6500.0 817.0 Gonad weight [g] 190.7 0.32 Head length (HL) [mm] 172.0 100.0 Predorsal length (PD) [mm] 368.0 200.0 Preanal length (PA) [mm] 570.0 324.0 Distance between verticals through anus and origin of dorsal fin (AD) [mm] 202.0 124.0 Predorsal length without head length (PDH) [mm] 196.0 100.0 Preanal length without head length (TR) [mm] 398.0 224.0 Distance from tip of lower jaw to corner of mouth (LG) [mm] 63.7 26.0 Distance from perpendicular through eye centre (DEG) [mm] 20.7 6.5 Length of intermaxillary-vomerine band (LV) [mm] 33.1 19.3 Length of left maxillary band (LM) [mm] 44.5 23.4 Number of teeth of mid part of maxillary band (NMM) [mm] 2.0 2.0 Width of mid part of maxillary band (WMM) [mm] 2.8 1.4 Fin difference index (FDI) [%] 15.0 18.0 PA ÷ TL [%] 43.5 47.1 HL ÷ TL [%] 13.0 15.0 TR ÷ TL [%] 30.0 33.0 PDH ÷ TL [%] 15.0 15.0 Patten of colour marking of skin Variegated Variegated Sex Female Female Gonadosomatic index [%] 2.93 0.04 Gonad maturity stage V I sequence tracefiles were manually edited and assembled occur in the mid-south-eastern region of Africa and using SeqMan Pro application in DNASTAR version eastern Australia and Tasmania, respectively (Ege 1939).