First Report of the Microgastropod Ammonicera Japonica

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Journal of Asia-Paciﬁc Biodiversity xxx (2016) 1e3

55 HOSTED BY Contents lists available at ScienceDirect 56 57 Journal of Asia-Pacific Biodiversity 58 59 60 journal homepage: http://www.elsevier.com/locate/japb 61 62 63 Original Article 64 65 1 Q1 First report of the microgastropod Ammonicera japonica 66 2 67 3 (Omalogyridae Habe, 1972) in Korea 68 4 69 a,b a a c c 5 Q13 Tsukasa Waki , Hee-Jung Lee , Sang-Rul Park , Jinsoon Park , Hyuck Joon Kwun , 70 6 Kwang-Sik Choi a,* 71 7 72 8 a School of Marine Biomedical Science (BK21 PLUS), Jeju National University, 102 Jejudaehakno, Jeju, 63243 South Korea b 73 9 Q2 Meguro Parasitological Museum, 4-1-1 Shimomeguro Meguro-ku, Tokyo, Japan c Biodiversity Dynamics Team, National Marine Biodiversity Institute of Korea, 75, 101 Jangsan-ro, Janghang-eup, Seocheon-gun, Chungcheongnam-do, 325- 74 10 902, South Korea 75 11 76 12 77 13 article info abstract 78 14 79 15 Article history: The intertidal zone of Jeju Island, Korea, is characterized by well-developed volcanic rocks with high 80 16 Received 27 January 2016 wave action. During low tide, numerous small tidal pools are formed on the rocky intertidal zone, which 81 17 Received in revised form provide shelter and habitats for benthic organisms. Previous investigation indicated that many species of 82 12 March 2016 18 micromolluscans inhabit the tidal pools, however, only a few studies have reported the ecology and Accepted 14 March 2016 83 identification of these microshells. In this study, we have identified a microgastropod, Ammonicera 19 Available online xxx 84 20 japonica Habe, 1972 (Omalogyridae), from a tidal pool on the southern coast of Jeju Island. Morphological 85 identification of the species was based on scanning electron microscopy (SEM) of the protoconch and 21 Keywords: 86 teleoconch. A. japonica was found to be associated with encrusting coralline algae distributed on the 22 Ammonicera japonica fi 87 23 coralline algae bottom of the tidal pools. This is the rst report of A. japonica from Korea, and the specimen was registered at the National Marine Biodiversity Institute of Korea (MABIK MO00157413). 88 24 microgastropod Omalogyridae Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). 89 25 SEM Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// 90 26 creativecommons.org/licenses/by-nc-nd/4.0/). 91 27 92 28 93 29 94 30 Introduction Members of the Omalogyridae family are typical micro- 95 31 gastropods, with a shell length of a few millimeters. Okutani (2000) 96 32 Microshells are the adult stage of small sized gastropods or bi- reported approximately 40 species of these family members from 97 33 valves with a shell length (i.e. the longest axis) smaller than a few Japanese waters and some of them are found within the benthic 98 34 millimeters (Sasaki 2000). Additionally, the early juvenile stage of macro algae community, although their ecological role is still un- 99 35 large mollusk species is often called a microshell. In the coastal known. Among the Omalogyridae family, the genus Ammonicera is 100 36 marine ecosystem, these micromollusks are often associated with characterized by an ammonite-like shell, although the shell size is 101 37 benthic algal tufts, especially coralline algae, and they play a key extremely small, with a shell length < 2 mm. In Japan, Okutani 102 38 Q3 role as secondary producers (Akioka et al 1999; Kelaher 2002; (2000) reported two species of Ammonicera, including Ammoni- 103 39 Olabarria 2002). In Korea, Min (2004) reported 247 species of cera japonica (Habe 1972) and Ammonicera angulate (Sleurs 1985). Q4,5 104 40 micromollusks, mostly from coastal Jeju Island. Despite their In the present study we collected the first specimens of 105 41 abundance and ecological importance, few studies have reported A. japonica associated with coralline algae in tidal pools on the 106 42 the distribution pattern and life history of these micromollusks to south coast of Jeju Island, Korea. Accordingly, the present study first 107 43 date. According to Sasaki (2000), numerous species of micro- reports A. japonica in Korea. 108 44 gastropods are associated with benthic macro-algae including 109 45 coralline algae and large brown algae such as Sargassum spp. 110 Materials and methods 46 111 47 112 In July 2015, we installed a 10 cm 10-cm microquadrat in a 48 113 tidal pool, to collect microgastropods associated with benthic algae 49 * Corresponding author. Tel.: þ82 64754 3422; fax: þ82 64756 3493. 114 (Figure 1). The sampling area was a rocky intertidal area on the 50 E-mail address: [email protected] (K.-S. Choi). 115 south coast of Jeju Island, Korea. The removed algal tuft was iden- 51 Peer review under responsibility of National Science Museum of Korea (NSMK) and 116 Korea National Arboretum (KNA). tified as coralline algae, Collallina pilulifera and Collallina officinalis. 52 117 53 http://dx.doi.org/10.1016/j.japb.2016.03.009 118 54 pISSN2287-884X eISSN2287-9544/Copyright Ó 2016, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. 119 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Waki T, et al., First report of the microgastropod Ammonicera japonica (Omalogyridae Habe, 1972) in Korea, Journal of Asia-Paciﬁc Biodiversity (2016), http://dx.doi.org/10.1016/j.japb.2016.03.009 JAPB139_proof ■ 4 April 2016 ■ 2/3

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1 photomicrographs, the microgastropods isolated from the quadrat 66 2 were identified as A. japonica Habe (1972) (Figure 2), and this 67 3 species is new to Korean waters. A total of 40 A. japonica were 68 4 counted from the quadrat, suggesting that A. japonica is densely 69 5 associated with the coralline algae, C. pilulifera and C. officinalis in 70 6 the tidal pool. Of the 40 individuals, most of them were found to be 71 7 live specimens, with the operculum. Malacological features of 72 8 A. japonica can be summarized as follows: 73 9 74 10 Order Heterostropha Ponder and Warén, 1988 75 11 Family Omalogyridae G. O. Sars, 1878 76 12 Genus Ammonicera Vayssière, 1893 77 13 78 Ammonicera japonica (Habe, 1972) 14 79 Ammonicera japonica Habe, 1972: p115, Figures 1e4 (type locality: 15 80 Yamaguchi Pref., Japan); Okutani, 2000: p700e701, 16 81 Figure Omaligyridae-1. 17 82 18 83 Description. Protoconch: 185 mm in shell diameter. Shell with 19 84 two spiral ridges extending to the first three quarters of the whorl; 20 85 transition to teleoconch indistinct (Figure 2B). Obsolete axial 21 86 growth lines. Teleoconch: shell extremely small (476 mm in shell 22 87 diameter), red-brown color, planispiral, opaque, translucent 23 88 (Figure 2A). Obsolete axial growth lines between axial ribs. 24 89 The microstructure of the shell surface of A. japonica demon- 25 90 strated in this study using SEM corresponds very well with the 26 91 description of the shell surface by Habe (1972) and Okutani (2000). 27 92 Bieler and Mikkelsen (1998) reported that the surface structure of 28 93 the protoconch and teleoconch of Ammonicera minortalis is 29 94 Figure 1. Sampling site of specimens of Ammonicera japonica Habe, 1972. extremely similar to that of A. japonica, although A. minortalis is 30 95 limited in distribution in the Atlantic Ocean (i.e. Florida coast). It is 31 96 unlikely that the microgastropod identified in this study is 32 After transportation to the laboratory, the algae-microshell com- 97 A. minortalis, because this species has not been reported from the 33 plexes were immersed in 70% ethanol for 15 minutes and sieved 98 west Pacific region. Chernyshev (2003) reported a new species of 34 through a 2-mm mesh to isolate the associated microorganisms. 99 Ammonicera from Korean water as Ammonicera chosenica. This 35 Microscopic examination of the filtrate revealed numerous small 100 species was discovered from the coastal East Sea, near Pohang, 36 organisms including several species of gastropods. A scanning 101 suggesting that A. chosenica distributes in rather cold water. 37 Q6 electron microscope (SEM: Carl Zeiss AG - SUPRA 55VP) was used to 102 A. japonica can be distinguished from A. chosenica, because 38 identify the microgastropods by examining the microstructure of 103 A. japonica has two spiral ridges extending to the teleoconch, and 39 the shell surface. The specimens were stored in 70% ethanol and 104 large axial ribs on the teleoconch. 40 registered at the National Marine Biodiversity Institute of Korea 105 Material examined. A tidal pool in the south coast of Jeju Island, 41 (MABIK MO00157413). 106 3314’23.42“N, 12623’49.22”E. July 18, 2015, one adult (476 mmin 42 107 shell diameter). 43 108 Results and discussion Distribution. From the Indian Ocean to Southern Hokkaido, Japan 44 109 (West Pacific Ocean). A. japonica reported in this study was found 45 110 Numerous benthic organisms were found within the 10 mm from turfs of coralline algae. Several studies have reported that 46 Q8 111 10-mm microquadrat, mostly small molluscans. Based upon SEM micromollusks use turfs of coralline algae as a shelter, which 47 Q7 112 48 113 49 114 50 115 51 116 52 117 53 118 54 119 55 120 56 121 57 122 58 123 59 124 60 125 61 126 62 127 63 128 64 Figure 2. Ammonicera japonica shells by scanning electron microscopy. A, Apical view. Arrows represent axial ribs on the teleoconch and two ridges on the protoconch. B, Pro- 129 65 toconch from apical view (detail of A). Arrows represent two ridges. 130

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1 protects them from strong wave or water flow and predators Bieler R, Mikkelsen PM. 1998. Ammonicera in Florida: notes on the smallest living 21 2 (Uchiba et al 1982; Hayakawa et al 2013). Accordingly, we believe gastropod in the United States and comments on other species of Omalogyridae 22 (Heterobranchia). Nautilus-Paper Edition 111:1e12. 3 that A. japonica also utilizes the turfs of coralline algae, C. pilulifera Chernyshev AV. 2003. Three new species of the genus Ammonicera Vayssière, 1893 23 4 and C. officinalis, as shelter for protection from predators and strong (Gastropoda, Omalogyridae) from the Japan Sea. Ruthenica 13 (2):107e112 [In 24 5 wave actions. Russian]. 25 Habe T. 1972. The Japan’s smallest gastropod, Ammonicera japonica, sp. nov. Venus 6 31:115e116. 26 7 Hayakawa J, Kawamura T, Kurogi H, et al. 2013. Shelter effects of coralline algal 27 8 Acknowledgments turfs: protection for Turbo cornutus juveniles from predation by a predatory 28 gastropod and wrasse. Fishery Science 79:15e20. 9 Kelaher BP. 2002. Influence of physical characteristics of coralline turf on associated 29 10 This study was supported by the monitoring of biodiversity macrofaunal assemblages. Marine Ecology Progressive Series 232:141e148. 30 11 dynamics on diverse coastal habitats (2015M00200) of the National Min DK. 2004. Mollusks in Korea. Busan, Korea: Hangul Graphics. pp. 1e566. Q9 31 12 Marine Biodiversity Institute of Korea. Olabarria C. 2002. Role of colonization in spatio-temporal patchiness of micro- 32 gastropods in coralline turf habitat. Journal of Experimental Marine Biology and 13 Ecology 274:121e140. 33 14 Okutani T. 2000. Marine mollusks in Japan. Tokai University Press. Q10 34 References 15 Sasaki T. 2000. Taxonomy of micro mollusk. Ourobors 9. The University Museum, The 35 University of Tokyo. Q11 16 Akioka H, Baba M, Masaki, et al. 1999. Rocky shore turfs dominated by Corallina Uchiba S, Nishima K, Yamamoto T, et al. 1982. Research about inhabitation and 36 17 (Corallinales, Rhodophyta) in northern Japan. Phycological Research 47:199e ecology of top shell 1: the factors affecting habitats of top shell juvenile. Bulletin 37 e 18 206. of Fukuoka Prefecture Fisheries Experiment Station; 1982:157 165 [In Japanese]. Q12 38 19 39 20 40