Distribution of Batillaria Multiformis and B. Attramentaria (Batillariidae) in Southern Kyushu

Plankton Benthos Res 13(1): 10–16, 2018 Plankton & Benthos Research © The Japanese Association of Benthology

Distribution of Batillaria multiformis and B. attramentaria (Batillariidae) in Southern Kyushu

1, 1 1 2 Tomoko Yamamoto *, Takafumi Kagohara , Kousei Yamamoto , Satomi Kamimura & 3 Masami Hamaguchi

1 Faculty of Fisheries, Kagoshima University, 4–50–20 Shimoarata, Kagoshima 890–0056, Japan 2 Graduate School of Engineering, Osaka City University, 3–3–138 Sugimoto, Sumiyoshi-ku, Osaka 558–8585, Japan 3 National Research Institute of Fisheries and Environment of Inland Sea, 2–17–5 Maruishi, Hatsukaichi-shi, Hiroshima 739– 0452, Japan Received 15 May 2017; Accepted 11 January 2018 Responsible Editor: Shigeaki Kojima

Abstract: The present study investigated the distribution of Batillaria multiformis and B. attramentaria in the tidal flats of Southern Kyushu. These two species are the dominant inhabitants of tidal flats and play an important role in conserving the environmental condition of the coastal area. Since it is difficult to distinguish between the two species based on shell morphology, the polymerase chain reaction restriction fragment length polymorphism (PCR-RFLP) technique was used for identification. Among the 55 tidal flats surveyed, Batillaria species were found in 32, mainly along the coasts of Kagoshima Bay and East China Sea. Furthermore, these species were not observed in certain tidal flats, although their presence in these tidal flats was confirmed from 1999 to 2003. The reason for their absence or decline has been discussed here. Batillaria multiformis was distributed along the neighboring tidal flats of inner Kagoshima Bay and around Nagashima Island, whereas B. attramentaria was isolated along a few scattered tidal flats facing to the Pacific Ocean or East China Sea. The difference in the distribution of two species might be attributed to their developmental system̶B. multiformis and B. attramentaria employ planktonic and direct developmental systems, respectively.

Key words: Batillaria, developmental system, dispersal, tidal ﬂat, PCR-RFLP technique

dominant group in the tidal flats. They play an important Introduction role in the tidal flats, because of their feeding habit ̶de- A tidal flat is an important transition zone with eco- posit feeders and grazers of benthic diatoms (Kamimura logical processes that functionally link terrestrial, fresh- & Tsuchiya 2004, 2006). Batillaria multiformis and B. at- water, and marine ecosystems (Levin et al. 2001, Wall et tramentaria (or B. cumingi) are ubiquitously distributed in al. 2001). This type of habitat provides valuable ecosystem Japan, except in the Ryukyu Islands, and often co-occur services, including regulation of disturbance, waste treat- in Central and Western Japan (Hasegawa 2000). Howev- ment, and food production (Costanza et al. 1997, Sasaki er, recent surveys have revealed that the local population 2003). Benthic organisms are the dominant inhabitants of these two species exhibit contrary patterns of abun- of tidal flats and support the above-mentioned ecological dance and distribution, particularly in Central Japan. For functions via their food web (Levin et al. 2001). How- instance, the distribution of B. multiformis has decreased ever, many species in the tidal flats are threatened, because during the 1990s. Furthermore, the population of B. mul- of the decreasing tidal flat area and habitat degradation tiformis along the coast of inner Tokyo Bay is extinct or caused by coastal developments (Wada et al. 1996, Japa- are restricted to certain tidal flats, while a large popula- nese Association of Benthology 2012). tion of B. attramentaria has remained stable (Furota 2000, In Japan, the gastropods of the genus Batillaria are a Yuhara et al. 2013). Furota et al. (2002) suggested that this difference is due to the difference in the developmental * Corresponding author: Tomoko Yamamoto; E-mail, yamamoto@fish. system of the two species. Batillaria multiformis produc- kagoshima-u.ac.jp es planktonic larvae, whereas B. attramentaria produces Distribution of Batillaria 11 juveniles through direct development (Adachi & Wada Materials and Methods 1999). Further, Furota (2000) suggested that the planktonic larvae might be unable to reach a suitable habitat, because The following are the differences in shell morphology the tidal flat area has been severely limited by coastal de- between the two species: B. multiformis has an expanding velopments. On the contrary, the direct development of B. outer lip, low spiral ribs and a distinct white callus on up- attramentaria can maintain its population locally in the per margin, while B. attramentaria does not have any of remaining and isolated habitats, since the offspring can those; and B. multiformis is stouter than B. attramentaria migrate to the habitats of their parents. (Okutani 2017). However, exceptions have been observed Yamamoto et al. (2009) reported that Batillaria spp. in the populations of Batillaria in Southern Kyushu (Kago- dominated the Shigetomi-higata tidal flat in the northern hara 2010) and Aomori in Tohoku area (Kanaya et al. part of Kagoshima Bay in 2005, whereas they were very 2011). Since molecular phylogenetic analysis using mtDNA rare in 1994. Since the snails of the genus Batillaria in confirmed that they are two distinct species (Ozawa 1996), Kagoshima Bay were identified as B. multiformis by a mo- the polymerase chain reaction restriction fragment length lecular genetic method using mitochondrial deoxyribonu- polymorphism (PCR-RFLP) technique was used to distin- cleic acid (mtDNA) (Kagoshima Prefecture 2003), it can guish the two species in the samples from most tidal flats. be presumed that the statuses of B. multiformis population The samples were stored at −20°C after collection. The in Southern Kyushu is different from that in Central Japan. soft tissue was separated from the shell after subjecting the To conserve these two Batillaria species, it is important sample to slight boiling. DNA was extracted from colu- to understand their distribution and the size of the local mellar muscle of each individual by immersing in 50 µm population in Southern Kyushu, which is almost the south- of 5% chelex and heating at 98°C for 20 min. After cen- ernmost distribution limit of B. multiformis. A few studies trifugation for 3 min at 15,000 rpm, the supernatant was have investigated the distribution of B. multiformis and collected. B. attramentaria in Southern Kyushu, focusing mainly on The mitochondrial cytochrome c oxidase subunit I gene either the benthic or molluscan fauna of certain tidal flats (COI) was amplified using a Takara Taq TM with primers in Kagoshima (Wakamatsu & Tomiyama 2000, Maki et HCO2198; 5′-TAA ACT TCA GGG TGA CCA AAA AAT al. 2002, Yamamoto et al. 2009) and Miyazaki prefecture CA-3′ and LCO1490; 5′-GGT CAA CAA ATC ATA AAG (Umemoto & Miura 2009). ATA TTG G-3′ (Folmer et al. 1994). The conditions for The present study surveyed the distribution of B. multi- polymerase chain reaction (PCR) were: 94°C for 60 s; then formis and B. attramentaria in as many as accessible tid- 35 cycles at 94°C for 30 s, 40°C for 30 s and 72°C for 60 s; al flats of Southern Kyushu as possible. Among the three and 72°C for 7 min. species of Batillaria̶B. multiformis, B. attramentaria, NlaIII, a restriction enzyme, was used to cut the PCR and B. zonalis in Kyushu Island (Kojima et al. 2003) ̶B. products according to Kamimura (unpublished) and Kanaya zonalis can be distinguished from the other two species et al. (2011). After incubation at 37°C for 90 min, the di- based on shell morphology. Since it is very difficult to rec- gested product was separated by electrophoresis in 3% aga- ognize B. multiformis and B. attramentaria by their shell rose gel at 100 V for 30 min, and then stained with ethidium morphology, each species was identified by using a mo- bromide. The bands of DNA fragment were analyzed under lecular genetic method. ultra violet illumination. It is known that the DNA of B. attramentaria and B. multiformis is digested into two and three fragments, respectively, by NlaIII (Fig. 1).

Fig. 1. Electrophoretic patterns of Batillaria multiformis and B. attramentaria by using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) technique. Both ends show molecular-weight markers. 12 T. Yamamoto et al.

Table 1. Position of the surveyed tidal flats and presence of Batillaria multiformis or B. attramentaria. ○; either B. multiformis or B. attramentaria was found. ̶; None of the species were found. Numbers in the extreme-left column indicate the number assigned for each tidal flat represented in Fig. 2. Presence of No. Name of Coast or River Area Ocean area Latitude/Logitude Batillaria 1 Kushitsu Mudfat the Pacific coast of Miyazaki Pref. the Paciffic 32°30′14.8″N/131°40′52.2″E ○ 2 Hitotsuse River the Pacific coast of Miyazaki Pref. the Paciffic 32°3′10.0″N/131°30′10.5″E ̶ 3 Hitotsuba Lagoon the Pacific coast of Miyazaki Pref. the Paciffic 31°55′07.7″N/131°27′34.0″E ̶ 4 Honjou River (Miyazaki) Osumi Pen. (Miyazaki Pref.) Shibushi Bay 31°25′22.2″N/131°14′47.8″E ○ 5 Anraku River Osumi Pen. Shibushi Bay 31°27′39.2″N/131°04′34.2″E ̶ 6 Hishida River Osumi Pen. Shibushi Bay 31°26′49.4″N/131°03′10.5″E ̶ 7 Kimotsuki River Osumi Pen. Shibushi Bay 31°21′24.8″N/131°00′29.3″E ̶ 8 Oda River Osumi Pen. Shibushi Bay 31°16′23.3″N/131°04′49.1″E ○ 9 Kubota River Osumi Pen. the Paciffic 31°13′39.4″N/131°00′45.8″E ̶ 10 Hetsuka River Osumi Pen. the Paciffic 31°05′31.4″N/130°49′39.8″E ̶ 11 Ogawa River Osumi Pen. Kagoshima Bay 31°13′05.0″N/130°45′48.1″E ̶ 12 Kaminokawa River Osumi Pen. Kagoshima Bay 31°16′16.0″N/130°47′28.5″E ̶ 13 Takasu River Osumi Pen. Kagoshima Bay 31°21′02.5″N/130°47′45.0″E ○ 14 Matsuzaki River Osumi Pen. Kagoshima Bay 31°25′47.4″N/130°45′05.0″E ̶ 15 Honjou River (Kagoshima) Osumi Pen. Kagoshima Bay 31°29′12.2″N/130°41′49.3″E ○ 16 Kenkou River inner Kagoshima Bay Kagoshima Bay 31°42′15.7″N/130°47′02.4″E ○ 17 Amori River inner Kagoshima Bay Kagoshima Bay 31°42′29.7″N/130°44′26.9″E ○ 18 Shimizu River inner Kagoshima Bay Kagoshima Bay 31°43′35.2″N/130°42′59.4″E ○ 19 Obamama Beach inner Kagoshima Bay Kagoshima Bay 31°44′36.6″N/130°41′30.4″E ○ 20 Hikiyama River inner Kagoshima Bay Kagoshima Bay 31°43′46.7″N/130°40′11.5″E ○ 21 Amikake River inner Kagoshima Bay Kagoshima Bay 31°43′42.6″N/130°39′36.5″E ○ 22 Beppu River inner Kagoshima Bay Kagoshima Bay 31°43′14.4″N/130°38′46.8″E ○ 23 Shigetomi Mudflat inner Kagoshima Bay Kagoshima Bay 31°42′30.1″N/130°37′21.3″E ○ 24 Inari River inner Kagoshima Bay Kagoshima Bay 31°36′22.0″N/130°34′26.0″E ○ 25 Nagata River Satsuma Pen. Kagoshima Bay 31°31′32.0″N/130°31′39.2″E ○ 26 Atago River Satsuma Pen. Kagoshima Bay 31°22′49.9″N/130°32′42.1″E ○ 27 Hachiman River Satsuma Pen. Kagoshima Bay 31°22′44.2″N/130°32′47.6″E ○ 28 Yamagawa Satsuma Pen. Kagoshima Bay 31°12′34.4″N/130°38′14.5″E ̶ 29 Shinkawa Satsuma Pen. the East China Sea 31°10′43.7″N/130°33′17.8″E ̶ 30 Mawatari River Satsuma Pen. the East China Sea 31°14′51.7″N/130°28′16.1″E ̶ 31 Ishigaki River Satsuma Pen. the East China Sea 31°15′10.3″N/130°26′39.9″E ̶ 32 Mizunari River Satsuma Pen. the East China Sea 31°15′11.6″N/130°26′07.2″E ̶ 33 Kajisa River Satsuma Pen. the East China Sea 31°15′20.4″N/130°24′41.2″E ̶ 34 Takesako River Satsuma Pen. the East China Sea 31°15′20.6″N/130°23′22.6″E ̶ 35 Nagasawa River Satsuma Pen. the East China Sea 31°15′13.5″N/130°22′06.3″E ̶ 36 Shirasawa Satsuma Pen. the East China Sea 31°15′20.1″N/130°21′41.3″E ̶ 37 Hanawatari River Satsuma Pen. the East China Sea 31°16′09.4″N/130°17′12.7″E ̶ 38 Kushi River Satsuma Pen. the East China Sea 31°18′39.3″N/130°13′23.9″E ̶ 39 Ohatari River Satsuma Pen. the East China Sea 31°24′48.1″N/130°08′08.6″E ○ 40 Harai River Satsuma Pen. the East China Sea 31°24′31.7″N/130°11′16.8″E ○ 41 Oura Satsuma Pen. the East China Sea 31°23′55.4″N/130°13′35.6″E ○ 42 Manose River Satsuma Pen. the East China Sea 31°26′22.0″N/130°17′47.9″E ○ 43 Ohsato River Satsuma Pen. the East China Sea 31°41′14.9″N/130°17′31.4″E ○ 44 Yafusa River Satsuma Pen. the East China Sea 31°41′51.5″N/130°17′11.1″E ○ 45 Sendai River northern Satsuma the East China Sea 31°50′21.5″N/130°12′27.3″E ̶ 46 Wakimoto northern Satsuma the East China Sea 32°05′03.7″N/130°11′28.8″E ○ 47 Shiomi River Nagashima Isl. the East China Sea 32°06′32.1″N/130°08′31.8″E ○ 48 Sashie River Nagashima Isl. the East China Sea 32°10′10.3″N/130°06′33.1″E ○ 49 Kohama River Nagashima Isl. the East China Sea 32°11′20.4″N/130°06′09.5″E ○ 50 Urazoko River Nagashima Isl. the East China Sea 32°11′49.5″N/130°09′28.9″E ○ 51 Kasedo Bay Nagashima Isl. Yatsushiro Sea 32°08′11.4″N/130°10′26.0″E ○ 52 Euchi River northern Satsuma Yatsushiro Sea 32°07′11.9″N/130°15′53.2″E ̶ 53 Noda River northern Satsuma Yatsushiro Sea 32°05′44.4″N/130°16′41.8″E ○ 54 Jyabuchi River northern Satsuma Yatsushiro Sea 32°06′25.9″N/130°18′20.9″E ○ 55 Komenotsu River northern Satsuma Yatsushiro Sea 32°07′00.3″N/130°20′18.0″E ○ Distribution of Batillaria 13

Samples of B. attramentaria and B. multiformis were collected from the tidal flats of Kagoshima Prefecture on Kyushu Island and the southern part of Miyazaki Prefec- ture. Using a 1 : 50,000 map, a catalog of all rivers along the coast in this area was created. Along the mouths of these rivers, certain areas containing soft sediment (from sand to silt) were selected using aerial satellite photographs. We traveled along the coastline by car, and selected tidal flats to survey based on the ease of accession by foot from the main road. The selected areas have been presented in Table 1. The tidal flats were surveyed during low tide of spring tide from May 2008 to August 2009. Usually two inves- tigators searched for the Batillaria snails throughout the tidal flats from lower intertidal to upper intertidal for at least 15 min at each tidal flat. Where Batillaria snails were found, the tidal flat was divided into three survey areas, each containing sets of one to three quadrats (15 cm×15 cm). The two Batillaria species found within the quadrats were sampled. When snails with morphological characteristic different from those in the quadrats were found, they were sampled even outside the quadrats. Approximately 30 snails were sampled from the tidal flat where snail density was too low to collect using quadrats. Fig. 2. Distributions of Batillaria multiformis and B. attramentaria in Southern Kyushu. The presence of these two species and Results location of each surveyed tidal flat and the number assigned for Four and 51 tidal flats in Miyazaki and Kagoshima pre- each tidal flat (as shown in Table 1) are shown. Black triangles, surveyed tidal flats where neither of the two species was found; fectures, respectively, were surveyed. Batillaria multifor- Black circles, tidal flats where both the species were identified by mis and/or B. attramentaria were observed in 32 tidal flats using polymerase chain reaction-restriction fragment length poly- (Table 1, Fig. 2). Neither species was found at Sendai River morphism (PCR-RFLP) technique; Open circles, tidal flats where (45 in Fig. 2; hereinafter, the sampling site number (shown only B. multiformis was identified by PCR-RFLP technique; Grey in Fig. 2) will be shown immediately after the area name) circles, tidal flats where B. multiformis and/or B. attramentaria and Euchi River (52) along the northern coast of Satsuma were found (PCR-RFLP technique was not applied). Peninsula, along the southern coast of Satsuma Peninsula (28–38), both sides of Osumi peninsula (5–7, 9–12, 14), (1), which is the only tidal flat located further north of Shi- and the Pacific coastal areas of Miyazaki (2, 3). In contrast, bushi Bay containing Batillaria species. most of tidal flats of Kagoshima Bay and the East China The ratio of B. multiformis and B. attramentaria identi- Sea contained populations of Batillaria. fied by PCR-RFLP differed among the tidal flats (Table The mtDNA of samples collected from 23 of 32 tidal 2), with the latter being the dominant species at Kushitsu flats was analyzed by PCR-RFLP technique to identify the Tidal Flat (1) in Miyazaki Prefecture (more than 98%; 46 species. The samples from the other 9 tidal flats could not out of 47 samples) and Kohama River (49) along the north- be identified. The sample numbers were small from the 9 ern coast of Nagashima Island (81%; 13 out of 16 samples). tidal flats, and then not enough PCR and/or digested prod- Furthermore, both the species were equally abundant at ucts were obtained. Batillaria multiformis was found along Oura (41), along the western coast of Satsuma Peninsula 23 tidal flats, and its coexistence with B. attramentaria (B. attramentaria accounted for 45% of the two species; was found along six tidal flats (Table 2, Fig. 2). Further, 5 out of 11 samples), and at Shiomi River (47) along the B. attramentaria alone was not observed in any tidal flat. southern coast of Nagashima Island (40%; 10 out of 25 The surveyed tidal flats in Kagoshima Bay were inhab- samples). Batillaria multiformis dominated within the Wa- ited by only B. multiformis. Batillaria attramentaria was kimoto (46) and Jabuchi River (54), near Nagashima Island found only around Nagashima Island, including the coastal (B. multiformis accountd for more than 90% of the two areas of Yatsushiro Sea (46, 47, 49, 54), the East China species). Sea (Oura; 41), and the northern part of Miyazaki Prefec- ture (Kushitsu Tidal Flat; 1). Oura was the only tidal flat Discussion where B. attramentaria was found in the Satsuma Penin- sula. Among the surveyed tidal flats along the Pacific side, The distribution of B. multiformis and B. attramentaria B. attramentaria was found only in Kushitsu Tidal Flat was investigated along 55 tidal flats in Southern Kyushu. 14 T. Yamamoto et al.

Table 2. Distribution of Batillaria multiformis or B. attramen- to a change in the local population in these tidal flats dur- taria. Numbers in the two right columns indicate the number of ing the early 2000s. samples identified by polymerase chain reaction-restriction frag- Furthermore, the tidal flats where the two species were ment length polymorphism (PCR-RFLP) technique. Furthermore, not distributed or their local population has changed often the data of samples collected only from the quadrates have been were facing to the open ocean (the Pacific Ocean or East shown. Numbers in the extreme-left column indicate the number China Sea) (Fig. 2) or located at the edge of peninsulas. assigned for each tidal flat represented in Fig. 2. Studies should focus not only on the habitat conditions No. Name of Coast or River B. multiformis B. attramentaria for adults, but also on larval dispersal and their biogeo- graphical distribution, in order to understand the distribu- 1 Kushitsu Mudflat 1 46 tion pattern of benthic organisms in tidal flats. Though 4 Honjou River (Miyazaki) 10 0 B. multiformis and B. attramentaria are related species, 8 Oda River 34 0 they employ contrast developmental systems, with B. mul- 13 Takasu River 18 0 tiformis employing planktonic development and B. attra- 15 Honjou River (Kagoshima) 18 0 mentaria employing direct development (Adachi & Wada 16 Kenkou River 20 0 1999). Along the southern coast of Satsuma Peninsula, the 17 Amori River 10 0 probability of larvae being carried away by the flow of 18 Shimizu River 7 0 ocean water is high. Because there is a southward-flow 19 Obamama Beach 13 0 off the southern coast of Satsuma Peninsula and south- 20 Hikiyama River 7 0 eastward-flow off the top of Osumi Peninsula, probably 21 Amikake River 7 0 affected by the Kuroshio Current (Nakamura et al. 2003, 22 Beppu River 13 0 2004). The population of B. multiformis further south of 23 Shigetomi Mudflat 3 0 the Satsuma Peninsula was found only at a few tidal flats 24 Inari River 4 0 of Amami-Oshima (Kojima et al. 2003), and the recruit- 26 Atago River 13 0 ment of larvae appeared to be relatively low. It is possible 39 Ohatari River 21 0 that tidal flats along the edge of the Satsuma and Osumi 40 Harai River 6 0 peninsulas were unfavorable for the recruitment of B. mul- 41 Oura 6 5 tiformis with marginal changes in flow causing a sharp 44 Yafusa River 36 0 reduction in their population, and even their extinction. 46 Wakimoto 18 1 Batillaria multiformis was found in all the 22 tidal flat 47 Shiomi River 15 10 samples that were identified by PCR-RFLP, whereas B. at- 49 Kohama River 3 13 tramentaria was found in only six tidal flats (Fig. 2). The 54 Jyabuchi River 38 4 ratio of coexisting of B. attramentaria and B. multiformis varied among the tidal flats. The population of B. attramentaria ranged from 5% at Jabuchi River (54) near Nagshima Island to more than 98% at Kushitsu Tidal Flat These species were not found along the northern coast of (1) in Miyazaki Prefecture. It is important to understand if Satsuma Peninsula (Sendai River, 45; Euchi River, 55), the this difference was caused by a difference in environment southern coast of Satsuma Peninsula (28–38), and in some condition in the tidal flats. It has been reported that B. at- tidal flats of the Osumi Peninsula (5–7, 9–12, 14). Further, tramentaria prefer a lower area of the intertidal zone when the presence of both the species from 1999 to 2003 was compared with B. multiformis. Further, B. attramentaria confirmed at Sendai River (45), certain tidal flats of the is distributed in muddy-sandy sediment, whereas B. mul- southern coast of Satsuma Peninsula (Mizunari River (32), tiformis has a wide preference, from sandy to muddy sub- Kajisa River (33), Takesako River (34), and Hanawatari strates (Adach & Wada 1997, 1998). However, there is no River (37)), and certain tidal flats of the Osumi Peninsula evidence to suggest that these preferences determine their (Anraku River (5), Hishida River (6), and Kimotsuki River distribution among different tidal flats. (7)) (Kagoshima Prefecture 2003). It was unclear whether In the present study, Batillaria attramentaria was dis- the two species have disappeared along these coastal areas tributed in scattered tidal flats, i.e., Kushitsu Tidal Flat or whether they were overlooked during the present study. (1) of Miyazaki Prefecture (open to the Pacific Ocean), The entire stretch of tidal flats̶from upper intertidal to Oura (41) in the western coast of Satsuma Peninsula (opens lower intertidal flats and from the river to the end of the to the East China Sea), and some tidal flats around Na- tidal flat̶was surveyed; therefore, the species could not gashima Island. Since B. attramentaria does not have a have been overlooked. Neither species was recorded at Ma- planktonic stage, this species has been reported to be dis- nose River (42) in the western coast of Satsuma Peninsula persed by floating for a short distance during the juvenile (Nature Conservation Bureau & Biodiversity Center of Ja- stage (Adachi & Wada 1997), rafting on the floating al- pan 2007) around 2004; however, both species were found gae (Highsmith 1985), or transported by migratory birds at this site in the present study. This might possibly be due (Malone 1965). The latter mode of dispersal can disperse Distribution of Batillaria 15 the species to isolated tidal flats (Kojima et al. 2004) along idae) at a co-occurring area. Venus 57: 115–120. the western coast of Satsuma Peninsula and around Na- Adachi N, Wada K (1999) Distribution in relation to life history gashima Island. Because the tidal flats from the East China in the direct-developing gastropod Batillaria cumingi (Batil- Sea to Yatsushiro Sea are thought to be stop-over points lariidae) on two shores of contrasting substrata. J Mollus Stud for migratory birds of the East Asian-Australasian flyway 65: 275–287. (Amano 2006). When transported to a new habitat with a Amano I (2006) Higata wo riyou suru wataridori no gennjy- favorable environment, B. attramentaria can quickly in- ou [Current status of migratory birds that use the tidal flats]. crease in population size. Chikyu Kankyo 11: 215–226. (in Japanese) On the contrary, B. multiformis is distributed in the Association of Wildlife Research (2015) Search system of Japa- nese red data. Available at: http://www.jpnrdb.com/search. neighboring tidal flats, particularly in the closed-off sec- php?mode=region (accessed on 14 May 2017) tion of Kagoshima Bay. This species has been listed as a Costanza R, d’Arge R, de Groot R, Farber S, Grasso M, Hannon near-threatened species in the Red List of Japan, and has B, Limburg K, Naeem S, O’Neill RV, Paruelo J, Raskin RG, also been included in the Red List of some prefectures (As- Sutton P, van den Belt M (1997) The value of the world’s eco- sociation of Wildlife Research 2015). Furota et al. (2002) system services and natural capital. Nature 387: 253–260. suggested that the species employing planktonic develop- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA ment have a disadvantage in regions where suitable habi- primers for amplification of mitochondrial cytochrome c oxi- tat is scarce and highly fragmented, and are therefore are dase subunit I from diverse metazoan invertebrates. Mol Mar vulnerable. The present study revealed that B. multiformis Biol Biotechnol 3: 294–299. has maintained stable populations along the coastal regions Furota T (2000) Naiwan no kairui zetsumesu to hozen: Touky- of Kagoshima Bay. This suggests that the planktonic dis- ou-wan no umininarui suitai karano kousatu [Extinction and persal strategy of this species is still active. However, this conservation of mollusks in en-closed waters, a consideration strategy did not appear to be active in the species along from population decline in the batillariid snails in Tokyo Bay]. some coastal regions in Southern Kyushu. Further, the dis- Kaiyo Monthly (Suppl) 20: 74–82. (in Japanese) tribution of B. attramentaria also appears to be changing Furota T, Sunobe T, Arita S (2002) Contrasting population sta- drastically, which is indicated by its absence within the in- tus between the Planktonic and direct-development Batillariid ner Kagoshima Bay in the present study, although its pres- snails Batillaria multiformis (Lischke) and B. cumingi (Crosse) ence was reported in 2014 (Itoh personal communication). on an isolated tidal flat in Tokyo bay. Venus 61: 15–23. In the present study, the distributions of B. multifor- Hasegawa K (2000) Batillariidae. In: Marine Mollusks in Japan mis and B. attramentaria was investigated in Southern Ky- (eds Okutani T). Tokai University Press, Tokyo, pp. 130–133. ushu. Batillaria multiformis was distributed in neighbor- Highsmith RC (1985) Florting and algal rafting as potential dis- ing tidal flats and B. attramentaria exhibited a scattered persal mechanisms in brooding invertebrates. Mar Ecol Prog distribution pattern. 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(in Japanese) Kamimura S, Tsuchiya M (2004) The effect of feeding behavior We are grateful to Dr. Osamu Miura (Kochi Univer- of the gastropods Batillaria zonalis and Cerithideopsilla cin- sity) and Dr. Hajime Itoh (University of Tokyo) for provid- gulata on their ambient environment. Mar Biol 144: 705–712. ing valuable information on the Batillaria snails. We also Kamimura S, Tsuchiya M (2006) Effects of opportunistic feed- thank Ms. Sasaki and students of Education and Research ing by the intertidal gastropods Batillaria zonalis and B. flec- Center for Marine Environment and Resources, Kagoshi- tosiphonata on material flux on a tidal flat. Mar Ecol Prog Ser ma University for supporting the laboratory experiments 318: 203–211. and field survey. 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