Studies on Taxonomy and Distribution of the Freshwater Snails, Genus Semisulcospira in the Three Islands Inside Lake Biwa

Jap. J. Limnol. 45, 3, 194-203, 1984.

Studies on Taxonomy and Distribution of the Freshwater Snails, Genus Semisulcospira in the Three Islands inside Lake Biwa

Naoshi C. WATANABE

Abstract

A freshwater snail, genus Semisulcospira was studied in the three islands inside Lake Biwa, Japan. A large and pronouncedly nodulated form of S. niponica was found off Takeshima and Shiraishijima Islands as well as off Chikubujima Island from which this form was described. Among the three islands, the snails become larger and nodes on the whorls become more intense with the decreasing area of the islands. A new species, S. morii, is described from Chikubujima and Takeshima Islands. This species coexists with S. niponica, and is abundant on a rather deeper bottom according to the monthly survey of vertical distribution. Three unknown types of Semisulcospira were also found off Takeshima and Shiraishijima Islands. All of the types live on the rocky bottom there, but in adult and embryonic shell characteristics they resemble the decipiens group which live on the sandy or muddy bottom of the coastal zone of Lake Biwa. From the above survey, several ecological and evolutionary problems are presented on Semisulcospira in these islands.

1. Introduction 2. Materials and Methods A freshwater snail, genus Semisulcospira There are four islands inside Lake Biwa; is classified into nine species in Japan Okinoshima, Chikubujima, Takeshima and (DAvis, 1969), and six among them are Shiraishi jima (Fig. 1). All of them are endemic to Lake Biwa and the River Yodo Water System. In the littoral zone of Lake Biwa, four species predominate S. niponica, S. d eci piens, S. multigranosa and S. reticulata. S. ni ponica exclusively occupies the rocky and stony bottom. On the sandy or muddy bottom the other three species live, and their habitats differ from each other in relation to depth and partly substratum (WATANABE, 1970, 1980). Semisulcospira in the islands inside Lake Biwa has not been sufficiently studied yet. A large and pronouncedly nodulated form of S. niponica is only known from Chiku- bu jima Island; it was described as S. biwae by KOBELT (1879). In this study, the same form of S. niponica is reported from Takeshima and Shiraishijima as from Chikubujima, and their shell characteristics are compared. In addition, a new species and three unknown types of Semisulcospira from the three islands are described. Finally, several ecological and evolutionary problems about Semisulcospira in these Fig. 1. Map of Lake Biwa showing the locations islands are discussed. of the islands. WATANABE 195 composed of igneous rock. Okinoshima 0.05 mm. Also, the snails per 0.25 m2 were Island is only about 2 km off the east shore counted at different depths in Chikubujima and in a relatively shallow area, but the every month from 28 April to 18 November other three islands, which are dealt with 1966, in order to study the seasonal change here, rise abruptly from the deep bottom. of vertical distribution. Water depths around both Chikubujima and Shiraishijima are 70 m, and that around 3. A comparison of S. niponica among Takeshima is 40 m. The distance around Chikubujima, Takeshima and Shira- Chikubujima and Takeshima is about 1.9 ishijima Islands km and 0.4 km, respectively. Shiraishijima The adult and embryonic shells collected consists of four cays whose circumference off Chikubujima, Takeshima and Shira- ranges from several to about 30 m. ishi jima are shown in Fig. 3. These spec- Snails were gathered by scuba diving imens are the largest snails collected in each off the three islands on 31 August 1965, 6 island on 29 May 1983 and their embryos. August 1966 and 29 May 1983. The S, niponica from Izaki, Ohmihachiman specimens collected on 1983 were mainly City on the east shore of the lake, is also used for measurements of shell character- shown in the figure; this specimen is a istics and descriptions of new species. The relatively large type among those from the others were referred to when necessary. coastal zone of the lake. As shown in the The measured characteristics of the shells figure, the adult S. niponica in the three are shown in Fig. 2. The measurements islands is larger than in Izaki and have of the adult shells are made by a caliper more noticeable nodes. Moreover, among which can be read to 0.1 mm. The embryos the three islands, the adult snails become in the brood pouches of females were larger and more intensely nodulated in the studied under a dissecting microscope, island order of Chikubujima, Takeshima and measurements were made with an and Shiraishi jima. The embryos in the objective micrometer and were accurate to females from every locality are generally globose and have pronounced nodes along the mid-whorl. The embryonic shells are light brown in colour and have distinct dark brown bands; a sutural and a basal band, and a slight one at mid-whorl in some cases. These are the characteristic features of the embryos of S, niponica (DAVIS, 1969). Statistics on the adult and embryonic shells are shown in Table 1. The measured specimens are the largest ten or eleven adults collected on 29 May 1983 and their embryos. The measurements of specimens from Otsu described by DAvis (1969) are also shown in the table. The adult shells of S. niponica in all of the three islands are larger than those in Otsu City, although the size varied among the islands; the largest in Shiraishijima and the smallest Fig. 2. Diagram illustrating the methods of in Chikubujima. On the other hand, there making shell measurements of Semi- sulcospira. L; shell length, W; shell are generally two basal cords and nearly width, BWL; body whorl length, AL; twelve longitudinal ribs on the penultimate aperture length, BW; body whorl, PW; whorl. The females of the three islands penultimate whorl. have generally more embryos than those 196 Taxonomy and Distribution of the I'resh"atet Snail-

C a b

Hit. .t. Adult and embryonic shells of Semisulrospira niponira in the three islands and Izaki: a d: adult shetls, e h; embryonic shells . a,e: Izaki. b.f: Chikubujinui , c. .¢: Takeshima. d, h: Shiraishijima.

of Otsu City. a straight line on the full-logarithmic scale , Among the three islands, the females of although their sizes differ . The regression Takeshima have fewer embryos than off equation is S PV 0. 5 3B14'L' ° where S W Chikubujima in spite of their larger adult is shell width and BIJVL is body whorl size. The largest embryo in a female length, in nun. becomes larger in both shell length and Figure 5 shows the relationship between width in the order Otsu, Chikubujima , shell length and shell width of the largest Takeshima and Shiraishijima, although the embryo in each female. As to the embryos data of Otsu seem to be somewhat over- of Otsu, the average value of every whorl valued because DAVIS reported the average count is given in the figure. The plots of of the embryos having the greatest whorl the three islands and Otsu give a straight counts (15) froth all of the females exam- line whose regression equation is SW ined. 1. 01SL°•", where S W is shell width and Figure 4 shows the relationship between SL is shell length, in tun. The average body whorl length and shell width of the sizes of the embryos differ from each other, same adult specimens as in Table 1. As although the ranges overlap. shown in the figure, the specimens from As seen above, the prominence of nodes the three islands and Otsu give essentially and the average size of the adultt shells WATANABE 197

Table 1. A comparison of the adult and embryonic shell features of Semisulcospira niponica among the four localities.

* The values of Otsu are obtained from DAvis (1969) . The parentheses indicate the rare cases. differ among the localities. However, the Semisulcospira morii sp, nov. embryos of the three islands and Otsu are (Figs. 6-7) the same in morphology and colour pattern, Description The shell is sturdy and has and their length•width relationship gives a pronounced longitudinal ribs. On the body straight line with overlapping size ranges. and penultimate whorls, each of the ribs Therefore, it is reasonable that specimens has pustulate nodes which are not distinct in Takeshima and Shiraishijima be regarded as the same geographical form of S, ni- in some cases. The penultimate whorl has ponica as on Chikubujima. 10 to 12 ribs, and each rib has four or five (common) nodes when distinct. The 4. A new species of Semisulcospira shell is eroded at the apex and only four from chikubujima and Takeshima to five whorls remain. The sides of whorls Islands are slightly convex. The basal cords on "1' 198 axonomv and Distribution of the Freshwater Snails

Fig. 5. Relationship between shell length and shell width in embryos of S. niponica Fig. 4. Relationship between body whorl length from the four localities. In the three and shell width of adult specimens of islands, the value of the largest embryo S. niponica in Chikubujima, Takeshima in each female is shown in the figure. and Shiraishijima Islands, and Otsu. The value of Otsu, however, is the The data of Otsu are obtained from average of embryos having each whorl DAVIS (1969). count obtained from DAVIS (1969).

Fig. 6. Adult shells of S. morti. a; Mo-31131 (holotvpe), b; Mo 31132, c; Mo 31135.

the body whorl are generally two and is straw-yellow to light brown and an rarely one. The outer lip of the shell obscure dark brown hand occurs around undulates where the basal cords reach the the colunellar lip. The length-width margin. The shell is uniformly light brown relationship of the embryonic shells is linear in colour and no handing occurs. A full- on the full-logarithmic scale, and the grown female has embryos less than some regression equation is S W 1. 18SLo-11, thirty in the brood pouch. The embryonic where S W is shell width and SL is shell shells are comparatively large and elongate, length, in nun. The chromosome number and has distinct longitudinal ribs. The of the species is n-16; ten metacentric, largest embryo in a female has 3. 5 to 4. 5 four submetacentric and two subtelocentric whorls. The colour of the embryonic shells chromosomes. W NFAN A III 199

Pig. r t?nibrvunic shells of S. morn: a; Mu 31131 (holotvpe) . h: Mo-31132, c: Mo 311:13, d : Mo 311H.

Meusnrenie nts Holotype tOMNH Mo specimens Mo 31132-x31141) and four 31131 shell length, 31.6 min; shell width, from Takeshima (Mo 31142--.31145). The 12.2111111; body whorl length, 19 ,0111111; specimen Mo 31140 is male and the others aperture length, 11.3111111; two basal cords are female. The measurements of paratypes on the hods whorl, ten ribs on the pe- are as follows:

Adult shells

nultimate whorl and five nodes on each rib. L, shell length; W, shell width; BWL, Four and one half whorls remain. There body whorl length; AL, aperture length; arc eleven shelled embryos in the brood ribs, the number of ribs on the penultimate pouch. The shell length, shell width and whorl; nodes, the number of nodes on each whorl count of the largest embryo is 4.35 rib; *, nodes are not distinct. Every mm, 2. 75 min and 4. 5 whorl, respectively. specimen has two basal cords except the The pal atypes are ten from Chikubujitna specimen Mo 31142 which has only one. 200 Taxonomy and Distribution of the Freshwater Snails

Embryos in each female

SL, shell length; SW, shell width; WC, species is named after Dr. Syuiti MORI, whorl count. the President of Shiga University, who Type locality Chikubujima Island in Lake made the pioneering ecological works on Biwa, Shiga Prefecture, Japan. Semisulcospira, and advised me to study Distribution The species is found on piled this genus in Lake Biwa. rock bottom covered in some places with thin mud at the depth of 3-12 m off 5. Vertical distribution of S. niponica Chikubujima (abundant) and Takeshima and S. morii in Chikubujima Island (sparse) Islands of Lake Biwa. Figure 8 shows the vertical distribution This species is apparently similar to co- of. S, niponica and S. morii in Chikubu- existing S. niponica, but the longitudinal jima Island surveyed monthly from 28 ribs on the whorls are not so clearly April to 18 November 1966. In the study separated into nodes by spiral cords as area, a cliff falls into the water about 3 m those of S. niponica. The embryos in deep. The bottom gently slopes from 3 m females of the new species are easily dis- to 10-12 m in depth, then becomes abruptly tinguished from those of S. niponica steep and falls vertically again 25-30 m because they are fewer, larger and more deep. The point of 1 m in depth in the elongate, and have no colour band on mid- figure is the surface of vertical base rock, whorl. In some areas of the lake, e, g., and the substrata of the other points are the rocky shore across from Chikubujima the piled rocks of diameter 0.5-2 m. On (Tsuzuraozaki), there is a type of S. the points deeper than 10-12 m, both S. niponica which has also pronounced ribs. niponica and S. morii were sparse, and From the embryos, however, this type not collected by the quadrat samplings. evidently belongs to S, niponica and differs The figure shows that S. niponica occurs from S, morii. Further comparisons with in the whole depth range from May to other Semisulcospira species are made in October, and increases in summer at the the last section. depth of 1 m, where no snail was collected The holotype and paratypes are deposited after and before the winter (April and in Osaka Museum of Natural History. This November) ; this suggests the seasonal WATANABE 201

briefly described below. The adult and embryonic shells are shown in Fig. 9. The first type from Takeshima resembles the smooth type of S. multigranosa described by DAvls (1969) in adult features; the shell is very smooth and longitudinal ribs are not distinct. The females, however, have more embryos which are far smaller and more constricted on the suture, than S. multigranosa. Six different specimens were found together with the first type in Takeshima. This second type has sculptured longitudinal ribs and spiral cords on the whorls, and resembles the flat sided type of S. reticulata (type 2 by DAVIS, 1969). However, the body whorl is more elongate and the ratio of the body whorl length to shell width is greater than S. reticulata. The sculpture on the shell surface is coarser and ribs on the whorl are generally fewer than S. reticulata. The embryos in the brood pouch are comparatively few and large among Semisulcospira species, but more and smaller than S. reticulata. The third type was found off Shirai- Fig. 8. Vertical distribution of S. niponica and shi jima. This type resembles the second S. morii in Chikubujima Island surveyed type and also S. reticulata, in adult shell from 28 April to 18 November 1966. features except in several respects, e. g., Each of the bars indicates the number of snails per 0.25 m2. the darker shell colour. The embryonic shells, however, are quite different; a greater number, more elongate and more vertical migration. On the other hand, only constricted on the suture than the second a few specimens of S. morii were collected type and S, reticulata. at the depth of 1 m. This species is It is noticeable that these three new types abundant at 3 m to 10-12 m depth, the resemble S. multigranosa or S. reticulata, gently sloping area, especially its deeper both of which live on the sandy or muddy part. As a whole, the habitats of S. bottom in the littoral zone of the lake. niponica and S, morii overlap, but the latter is slightly deeper. 7. Problems on Semisulcospira in 6. New types of Semisulcospira from the three islands Takeshima and Shiraishijima Islands Several interesting questions arise on Three new types other than S, morii Semisulcospira in Chikubu jima, Takeshima were found on the piled rocks covered and Shiraishijima Islands. with thin mud in some places at the depth These islands are composed of the same of 5-10 iii; two from Takeshima and one igneous rocks, but are fairly distant and from Shiraishiji ma. The detailed descrip- isolated by deep water from each other. tions and the taxonomical decision will be The same form of S. niponica, however, made in another report after further exam- was found off the three islands as mentioned inations. Their major characteristics are above. This large and pronouncedly nodu- 202 Taxonomy and Distribution of the Freshwater Snail=

a b C

Fig. 9. Adult and embryonic shells of the three new types in Takeshima and Slut ai shijirna Islands: a e: adult shells, rl t: embryonic shells. a,d: the first type from Takeshima, b,et the second type front Takeshima, r. l: the third type from Shiraishijima.

lated form was not found in the other area Takeshima. of the lake through the whole lake surveys The second question is what it means in 1965 and 1966. The first question is this; that the smaller the area of the island, the what do the facts imply? Did the three larger and the more intensely nodulated islands connect geographically with each S. niponica becomes; the difference in other in the past? Did the same charac- growth or longevity by environmental con- teristics evolve independently in similar ditions ? or the difference fixed genetically' environments of the islands? Did the The third question is what the origin of population in any one of the islands invade S. morii is. DAVIS (1969) divided genus and settle in the other islands ? The Semisulcospira into S. libertina species similar questions arise also on S. morii complex and S. niponica complex. The which was found in Chikubujima and former is characterized by high chrotno- WATANABE 203 some numbers (n=18 or 20), many basal 採集された.3島の間では,竹生島・多景島・白石島 cords and many embryos per female, and の順に面積が小さくなるが,それにつれてヤマトカワ the latter by low chromosome numbers ニナのサイズは大きくなり,イボもより顕著になる. (n = 7 to 14), few basal cords and few 一方 ,竹生島と多景島から新種モリカワニナを記載し embryos. S. moyii is intermediate in た-この種は上記のヤマトカワニナと共存し,成殻の chromosome numbers (n=16), although it 形態も類似するが,胎殻の形態や数はまったく異なり, falls into the category of S, niponica 垂直分布からみてもヤマトカワニナよりも深い場所に complex by low numbers of basal cords 多く生息する傾向がみられた.多景島と白石島からは and comparatively few embryos. This new さらにカワニナ属の新しい3タイプが発見された.こ species resembles S, ni ponica in adult shell れらのタイプはいずれも水深5～10mの積み重なった characters, but the embryonic features are 巨岩上に生息するが,成殻と胎殻の形態はびわ湖沿岸 quite different. 部の砂あるいは泥底にすむイボカワニナ類と似ている. The fourth question is where the three 上記の結果にもとついて,3島のカワニナ属をめぐる new types in Takeshima and Shiraishi jima 生態学的および進化学的な幾つかの間題を提出した. come from. S, decipiens, S, multigyanosa References and S. Yeticulata all of which inhabit the sandy or muddy bottom resemble each DAVIS, G. M. (1969) : A taxonomic study of some species of Semisulcospira in Japan (Mesogas- other morphologically and they were once tropoda: Pleuroceridae). Malacologia, 7: united into a single species (KURODA, 211-294. 1963); I called them decipiens group KOBELT, W. (1879) : Fauna Molluscorum Extra- (WATANABE, 1970). All of the new types marionorum Japoniae. Abhandl. Senkenberg. obviously belong to the decipiens group natur. Ges. XI. Bd., Christian Winter, in adult and embryonic features. Never- Frankfurt am Main. theless, they live on the generally rocky KURODA, T. (1963) : A catalogue of the non- bottom together with S. ni ponica in the marine mollusks of Japan including the Oki- islands. nawa and Ogasawara Islands. Malac. Soc. Further ecological and paleogeographical Japan, Tokyo. (in Japanese). WATANABE, N. C. (1970) : Studies on three investigations on the three islands are species of Semisulcospira in Lake Biwa. I) needed to solve the questions presented Comparative studies of shell form and above. habitat. Venus, 29: 13-30. (in Japanese with English abstract). Acknowledgments WATANABE, N. C. (1980) : Some factors affecting I am indebted to Dr. Tetsuo SUNAGA,Kagawa the distribution and abundance of the two University, Dr. Tetsuya NARITA, Kyoto Uni- melanian snails, Semisulcospira decipiens and versity, and Dr. Yasunobu YANAGISAWA,Ehime S. reticulata, in Lake Biwa. Jap. J. University, for their assistance in scuba diving Limnol., 41: 212-224. (in Japanese with to collect the specimens. Thanks are also given English abstract). to Mr. Hiroshi NAKAMURA,Kyoto University, who taught me how to examine the chromosomes. (著者:渡辺直,香川大学教育学部環境科学研究室,〒760 高松市幸町1-1; Naoshi C. WATANABE, 摘要 Department of Environmental Science, Faculty びわ湖内の3つの島におけるカワニナ属の分布と分 of Education, Kagawa University, Saiwai-cho, Takamatsu 760) 類について調べた.ヤマトカワニナの大型でイボの強い型が竹生島に生息することは従来から知られていた Accepted: 29 March 1984 が,今回の調査では同様の型が多景島と白石島からも