First Record of the Blue-banded Sea Krait (Laticauda laticaudata, Reptilia: Squamata: Elapidae: Laticaudinae) on Jeju Island, South Korea

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1 Asian Herpetological Research 2017, 8(2): DOI: /j.cnki.ahr ORIGINAL ARTICLE First Record of the Blue-banded Sea Krait (Laticauda laticaudata, Reptilia: Squamata: Elapidae: Laticaudinae) on Jeju Island, South Korea Jaejin PARK 1#, Kyo-Soung KOO 1#, Il-Hun KIM 1,2, Woo-Jin CHOI 1 and Daesik PARK 3* 1 Department of Biology, Kangwon National University, Chuncheon, Kangwon 24341, South Korea 2 National Marine Biodiversity Institute of Korea, Seocheon, Chungnam 33662, South Korea 3 Division of Science Education, Kangwon National University, Chuncheon, Kangwon 24341, South Korea Abstract We report the first recorded capture of a blue-banded sea snake (Laticauda laticaudata Linnaeus, 1758, Jobeuntti KunBadabam in Korean) in South Korea based on one male specimen collected from Marado-ri, Seogwiposi, Jeju-do on 20 October The morphological features of the lateral nostrils, the much wider ventrals than adjacent dorsals, the horizontally undivided rostral, the two prefrontals, and the uniform black bands on the body indicate that the specimen is L. laticaudata. An analysis of the partial mitochondrial cytochrome b gene sequence indicated that the specimen fits well into the known L. laticaudata phylogenetic group, which confirms that the sea krait is L. laticaudata. Including this report, five species of sea snakes (L. laticaudata, L. semifasciata, Hydrophis platurus, H. cyanocinctus, and H. melanocephalus) have now been reported in Korean waters. Keywords sea snake, Hydrophiinae, Laticaudinae, blue-banded sea snake, Laticauda laticaudata 1. Introduction Marine (Hamann et al., 2007; Rasmussen et al., 2011a; Wallace et al., 2016) and terrestrial reptiles (Reading et al., 2010) are declining globally, and the major factors underlying the decline in marine reptiles include climate change, coastal development, water pollution, and overexploitation (GBRMPA, 2012; Cao et al., 2014). Sea snakes are a representative marine reptile that is vital to marine ecosystems because of their roles as top predators and their use of relatively wide habitats (Brischoux et al., 2007; Ineich et al., 2007). Similar to marine turtles (GBRMPA, 2012; Wallace et al., 2016), sea snakes are also declining (Hamann et al., 2007; Goiran and Shine, 2013; Lukoschek et al., 2013). To understand the declining trends and develop mitigation # Both authors contributed equally to this paper. * Corresponding author: Prof. Daesik Park, from Division of Science Education, Kangwon National University, Chuncheon, South Korea, with his research focusing on basic and conservation ecology of amphibians and reptiles. parkda@kangwon.ac.kr Received: 20 November 2016 Accepted: 14 April 2017 approaches, studies to determine the species distributions and biological and ecological characteristics are necessary (Hamann et al., 2007; GBRMPA, 2012). In particular, new records of sea snake species beyond their typical sea snake distribution ranges must be reported. Globally, 70 sea snakes (aquatic elapids) are distributed in the two subfamilies Hydrophiinae (true sea snakes) and Laticaudinae (sea kraits), and these snakes primarily inhabit the tropical and subtropical waters of the Indian and Pacific oceans (hppt:// In East Asia, which includes China, Japan, and Korea, a total of 16 sea snake species have been reported, with 13 in the Hydrophiinae and 3 in the Laticaudinae (Kang and Yoon, 1975; Mao and Chen, 1980; Zhao and Adler, 1993; Toriba, 1994; Kim and Han, 2009). Recently, several sea snake have been captured outside of typical sea snake distribution ranges. For example, H. platurus was found in Ventura County, California, USA (Gordon, 2015), L. semifasciata and L. laticaudata were found on the east and west coasts of mainland Japan (Tandavanitj et al., 2013a), and three L. semifasciata specimens were reported at Jeju Island, Korea in 2016 (Park et al.,

2 132 Asian Herpetological Research Vol ). To evaluate the effects of recent climate change on sea snake population dynamics and potential range expansions, records of sea snake captures beyond the limits of their distribution range are critical. In this study, we report for the first time the capture of the blue banded sea krait Laticauda laticaudata (Linnaeus, 1758) in Korea based on a specimen collected from Jeju Island on 20 October In addition, we update the identification keys for species of Laticaudinae and Hydrophiinae in Korea and discuss the meaning of recent sea krait captures in Korea. 2. Materials and Methods 2.1 Collecting the specimen and the morphological study The sea snake reported in this study was collected approximately 30 km south of Marado-ri, Seogwipo-si, Jeju-do, South Korea (N , E ) by a fisherman (Kang Y. N.) on 20 October When caught by a hand net, the sea snake was swimming on the water surface near a cutlassfish ship. The dead snake due to keeping it in a freezing storage on the ship was donated to the Herpetology Laboratory of the Kangwon National University (KNU). On arrival at the lab, we determined its sex by gonadal observation and measured its snout vent and tail lengths to 0.1 cm using a tape ruler and its body weight to 0.1 g using a digital balance (ELT 4001, Sartorius-Korea, Seoul, South Korea). Subsequently, we investigated the key morphological and classification features, such as the number of scale rows and bands on the head and body, photographed the snake, collected 2-3 mm tail tissues for later molecular study, preserved it in 95% ETOH, and finally deposited it in the herpetological collection of the KNU (G535LL). We identified the specimen on the basis of previous morphological studies (Mao and Chen, 1980; Toriba, 1994; Rasmussen et al., 2011b). 2.2 DNA extraction, PCR, and phylogenetic analysis of the mitochondrial cytochrome b gene We extracted whole genomic DNA from the tail muscle tissues using the QIAGEN DNeasy Blood and Tissue kit (QIAGEN, Hilden, Germany) following the manufacturer s instruction and then amplified the partial mitochondrial cytochrome b (mt-cyt b) gene using the forward primer L14910 and the reverse primer H16064 (Burbrink et al., 2000). We conducted the PCR using a SimpliAmp Thermal Cycler (Life Technologies, Carlsbad, CA, USA) under the following conditions: 94ºC for 4 min; 35 cycles of 94ºC for 30 s, 57ºC for 30 s, and 72ºC for 1 min; and a final extension of 72ºC for 7 min. The PCR products were sequenced at the Macrogen Sequencing facility (Macrogen, Seoul, South Korea). To construct the phylogenetic tree, we additionally downloaded 14 sea snake mt-cyt b sequences from GenBank (Slowinski and Keogh, 2000; Lukoschek and Keogh, 2006; Sanders et al., 2008, Sanders et al., 2013a, b; Tandavanitj et al., 2013b) and aligned the all sequences using Clustal X2 (Thompson et al., 2002). Uniform sequences were edited using the Bioedit software package (Hall, 2011) and then analyzed by the maximum likelihood (ML) method using PAUP 4.0b10 (Swofford, 2002) and ModelTest (Posada and Crandall, 1998) and the Bayesian method using MrBayes 3.1 (Ronquist and Huelsenbeck, 2003). In addition, we determined the haplotype of the mt-cyt b sequence of the specimen by comparing the known mt-cyt b haplotypes of L. laticaudata collected by Tandavanitj et al. (2013b) on the Taiwan-Ryukyu archipelagos. 3. Results and Discussion The male snake specimen had a prominent, vertically flattened, paddle-like tail, which is a representative feature of typical sea snakes (Figure 1 A, B). The ground body color was blue, the ventral color was yellowish, the upper lip was pale blue, the dorsal bands were black, and the ventral bands were yellowish black (Figure 1 A, B). The width of the uniform black cylindrical bands on the trunk and tail was between three and four dorsal scales (Figure 1 A). The specimen had 49 bands on the trunk and five on the tail (Figure 1 A). The rostral visible from above was not divided into two (Figure 2 A, B). The snake had two prefrontals, two internasals, one frontal, and two parietals (Figure 2B). In addition, we identified seven supralabials (the 3rd and 4th touched the eye), one supraocular, one preocular, two postoculars, and 1+2 temporals on each dorsal side of the head (Figure 2 C) and one mental, four inframaxillaries and seven infralabials on each ventral side of the head (Figure 2 C, D). The snake had 239 ventrals, 42 subcaudals and 2 anals (Figure 1 B). The number of scale rows around the neck, on the mid-body, and near the anus was 19, 19, and 18, respectively. The snout-vent length was cm, the tail length was 12.4 cm, and the body weight was g. In the phylogenetic analysis of the partial mt-cyt b gene sequences, the specimen fit well into a previously known L. laticaudata group (Figure 3). The specimen had a unique mt-cyt b haplotype (GenBank accession No. KY114891) that had not been previously reported; however, the haplotype sequence differed by only one

3 No. 2 Jaejin PARK et al. First Record of Laticauda laticaudata in Korea 133 Figure 1 Male Laticauda laticaudata caught at Marado-ri, Seogwipo-si, Jeju-do, South Korea on 20 October Dorsal (A) and ventral (B) surfaces. Figure 2 Male Laticauda laticaudata caught at Marado-ri, Seogwipo-si, Jeju-do, South Korea on 20 October Frontal (A), dorsal (B), lateral (C), and ventral surfaces of head (D). bp from the Lati-1 haplotype, which has been identified throughout Taiwan and the Ryukyu Islands (Tandavanitj et al., 2013b). Based on the above morphological features, we identified the sea krait collected in Korea as a blue-banded sea krait (L. laticaudata). In northeast Asia, three sea krait species (L. colubrina, L. laticaudata, and L. semifasciata) have been reported (Kang and Yoon, 1975; Mao and

4 134 Asian Herpetological Research Vol. 8 Figure 3 Maximum likelihood (ML) tree based on the partial mitochondrial cytochrome b gene of Laticauda laticaudata collected at Jeju Island, South Korea. Three Hydrophis species, which previously known in Korea, and 11 Laticauda sequences were downloaded from GenBank (the accession number is listed after each scientific name) and used in the analysis. The phylogenetic tree was constructed with PAUP* v4.0b10 (Sowfford, 2002). On each branch, the Bayesian posterior probabilities are denoted. Chen, 1980; Zhao and Adler, 1993; Toriba, 1994; Kim and Han, 2009). Among them, only L. semifasciata has a horizontally divided rostral and evident V-shaped bands on the body, while L. colubrina has a unique yellow to white upper lip, which is the source of its English name yellow-lipped sea krait, and three prefrontals (Mao and Chen, 1980; Rasmussen et al., 2011b; Park et al., 2016). Compared with L. colubrina and L. semifasciata, L. laticaudata has two prefrontals and the rostral is visible from above (Mao and Chen, 1980; Rasmussen et al., 2011b). The features of the horizontally undivided rostral, two prefrontals, and uniform black bands on the body of the specimen are all consistent with L. laticaudata. In addition, the number of bands, ventrals, subcaudals, and scale rows on the body are all within the known range of L. laticaudata (Mao and Chen, 1980; Toriba, 1994; Rasmussen et al., 2011b). These features all indicate that the specimen collected at Jeju Island is L. laticaudata. In the phylogenetic analysis of the partial mt-cyt b gene sequences, the specimen was well matched to the known L. laticaudata group. This finding clearly shows that the specimen is L. laticaudata. Unfortunately, we could not determine the origin of the specimen from the haplotype of the partial mt-cyt b sequence. The haplotypes of the mt-cyt b gene of L. laticaudata are not highly differentiated throughout Taiwan- Ryukyu archipelagos. Throughout the regions, only four haplotypes have been identified from 136 samples (Tandavanitj et al., 2013b). Although the haplotype of the mt-cyt b gene of the L. laticaudata subject in this study was unique, it differed by only one bp from previously reported Lati-1 haplotype from specimens in Taiwan and the southern and northern Ryukyu Islands. The morphological and molecular data obtained here consistently indicate that the sea krait collected at Jeju Island is L. laticaudata; therefore, this paper represents the first official report of L. laticaudata in Korea. To date, five species of sea snakes (L. laticaudata, L.

5 No. 2 Jaejin PARK et al. First Record of Laticauda laticaudata in Korea 135 semifasciata, Hydrophis platurus, H. cyanocinctus, and H. melanocephalus have been reported in Korean waters. Our first capture of L. laticaudata at Jeju Island is particularly meaningful because another sea krait species, L. semifasciata, was newly reported in Korea within the last year (Park et al., 2016). Despite the capture of two different sea krait species at Jeju Island, the L. laticaudata specimen in this study might represent a simple accidental drifter via the Taiwan Warm or Kuroshio currents (Su, 2001; Xu et al., 2009; Zhou et al., 2015) because it is unlikely that a sea krait population has been established at Jeju Island. Nevertheless, this specimen indicates that sea kraits have newly or recently entered Korean waters (Lee et al., 2013; Kim et al., 2016; Park et al., 2016). Jeju Island where we caught both sea kraits is geographically located just outside the typical distribution range of sea kraits (Mao and Chen, 1980; Heatwole et al., 2016; Gherghel et al., 2016). In recent decades ( ), the oceanic temperature at Jeju Island has rapidly increased at a rate of C/year (increase of C/ year in winter), which is likely because of recent climate changes (Jang et al., 2006; Jung et al., 2013). If climate changes and oceanic warming continue in the area, the influx of sea kraits might continue and their survival period in the area should extend. Therefore, further monitoring of sea kraits at Jeju Island as well as at other boundary areas of global sea snake distributions should be encouraged to evaluate potential effects of recent climate changes on sea snake populations. Key to the Laticaudinae and Hydrophiinae species in Korean waters: Laticaudinae. Ventrals much wider than the adjacent dorsals, with the width approximately 4 times greater than the length. 1. Rostral divided in two horizontally; three prefrontals....laticauda semifasciata 2. Rostral not divided; two prefrontals...laticauda laticaudata Hydrophiinae. Small ventrals that are less than twice as wide as the adjacent dorsals or similar in size. 1a. Head elongated and dorsoventrally slightly flattened; black dorsal and yellowish ventral; no cross bands...hydrophis platurus 1b. Not as above a. Head small; eye larger than the preocular, one anterior temporal...hydrophis melanocephalus 2b. 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