Jpn. J. Limnol., 53, 1, 47-54, 1992

Morphology and Variation of galeata SARS from Lake Biwa and Lake Kizaki in Japan

Susumu TANAKA

Abstract

In Japan SARS has been confused for a long time with Daphnia hyalina or due to the confusion in Europe where the three species originally described. In this paper, the Daphnia species from Lake Biwa and Lake Kizaki, which has been assigned various scientific names, are confirmed as Daphnia galeata SARS, 1863, based on the determinative key proposed by FLOBNERand KRAUS (1986), and their morphology and morphological variations are described.

Key words: Daphnia galeata, , Lake Biwa, Lake Kizaki

KRAUS (1986), these taxonomic complications 1. Introduction were caused by the occurrence of numerous Since the excellent classical works by UENO different morphological races or forms, and the (1927, 1937), few contributions has been made presence of many intermediate forms among to the of Japanese Cladocera. Even different populations. in Lake Biwa and Lake Kizaki where many Recently the populations of hyaline limnetic limnological investigations were conducted, the species of Daphnia in various European waters cladoceran fauna has not been thoroughly stud- have been successfully divided into separate ied. The populations of limnetic species of the species by careful analysis (CHRISTIE, 1983, genus Daphnia in these lakes, which are inter- FLOSNERand KRAUS,1986; HRBACEK,1987; HUDEC, esting as being dominant in zooplankton com- 1991).In the European literature, D. hyalina munities, are also confused with regard to their LEYDIG was defined as a species with pointed taxonomic status and assignment. Therefore rostrum, long and low antennula mound, and a these populations has long been recorded under relatively low and always evenly rounded hel- various names such as D. longispina (NARITA met. The frons is usually convex or straight. and OKAMOTO, 1984), D. longispina hyalina These characteristics are fundamentally identi- (UENO, 1934a, b, 1937), D. hyalina (UENO, 1973, cal to LEYDIG'S (1860) original description, MIZUNO, 1977), D. longispina galeata (UENO, whereas D. galeata SARS was defined as a 1937) and D. galeata (UENO;1973, MIZUNO,1977). species with blunt rostrum, short and high It was also uncertain whether the populations in antennula mound, and high angulated or typi- these lakes were monotaxic. cally pointed helmet. The frons is distinctly Many species of Daphnia including D. galeata concave or nearly straight and directed back- SARS were described originally in Europe, and wards. the confusion as to taxonomic status or nomen- After the taxonomic criteria proposed, the clature of hyaline limnetic species of Daphnia Daphnia populations of L. Biwa and L. Kizaki (D. hyalina-galeata complex) has continued collected in several years were definitely even in Europe until quite recently. The confu- identified as Daphnia galeata SARS. In the pres- sion in Japan undoubtedly relates to the situa- ent paper the author describe the precise tion in Europe. As pointed out by FLOBNERand morphology of Daphnia galeata SARS from two 48 TANAKA

Japanese lakes and discusses some taxonomic problems.

2. Materials and methods

Lake Biwa is the largest and the most ancient

lake in Japan. It is located in the western part

of Honshu Island (35•‹15'N, 136•‹05'E) with a

surface area of 674.4 km2 and a maximum depth

of 104.0 m, and Lake Kizaki is a small lake

located in the central part of Honshu (36•‹33'N,

137•‹50'E) with a surface area of 1.4 km2 and a

maximum depth of 29.5 m (HORIE, 1962). Sam-

ples were collected from the North Basin of L.

Biwa (near Station D in KAWABATA, 1987) on 27

October 1989 and the deepest point of L. Kizaki

on 23 August 1984 and 29 August 1990. The

samples were obtained by the zooplankton net

of 94 ƒÊm in mesh size (Nitex) which were

vertically hauled from about 30 m depth (L.

Biwa) and from near lake bottom (L. Kizaki)

to the surface. The were fixed with

4% formalin or 95% ethyl alcohol immediately

at collection and preserved in 4% formalin or

70% ethyl alcohol for laboratory use. For Fig.1. Total length frequency distributions of observations, complete individuals and isolated parthenogenetic female of Daphnia galeata parts of the body were mounted on slides with SARS from L. Biwa and L. Kizaki. Total 50% glycerol. Measurements of sizes and line length indicates the length from top of drawings were made on a compound micro- head to base of shell-spine.

scope with phase optics, a sliding stage and a

drawing tube. long and high, developing crest; helmet variable in size and shape, either elongate triangular 3. Description with sharply pointed apex on the top (most 3-1. Parthenogenetic female (Figs. 2-4) materials in L. Biwa, Fig.2 A-F, a few mate- Size: a medium-sized species; longest axis rials in L. Kizaki,Fig.2 K) or uniformly (exclusive of shell-spine) of egg-carrying rounded or bluntly tapering (most materials in female 0.8-2.0 mm (Fig.1). Carapace color- L. Kizaki, Fig. 2 G-J, L); ventral margin bulged less and hyaline; oval shape in lateral view, in front of the eye, slightly or distinctly concave maximum height about 4/5 of length; ventral between eye and rostrum. Rostrum acute, margin curved and dorsal margin slightly moderately long, distinctly projecting beyond curved; spinulation on ventral margin extend- the sensory hair of the antennules (Fig.3). ing anteriorly about half of the edge and on Antennula mound short and high. Fornix dorsal margin restricted posterior one-third; extending to the edge of the optic vesicle. spinules widely spaced and so minute that they Abdominal processes moderately developed, are difficult to discern. Shell-spine long but first process longest and about two and half highly variable up to half as long as carapace, times as long as second (Fig.4 A, C, D). arising in or slightly dorsally from the longitu- Postabdomen weakly tapering distally, with 8- dinal body axis, slightly directed dorso-poster- 13, usually 10-12 anal teeth which strongly and iorly or straight backwards. Head moderately uniformly decrease in length proximally (Fig.4 49 Daphnia galeata SARS in L. Biwa and L. Kizaki

Fig.2. Daphnia galeata SARS, parthenogenetic females: A-F, L. Biwa; G-L., L. Kizaki; F and L, young individuals with eggs. Scales indicate 1 mm. 50 TANAKA

Fig.3. Daphnia galeata SARS, variation of female rostrum, A-D, L. Biwa; E-H, L. Kizaki .

A). Postabdominal claws long and slender, with three pectens of fine teeth and with two incisions on ventral margin (Fig.4 B, E). 3-2. Male (Fig. 5) Samples from both lakes contained a few immature males. The longest axes of mate- rials were up to 1.3 mm in L. Kizaki and 1.0 mm in L. Biwa. Head in the material of L. Kizaki with low rounded crest or sharply pointed apex (Fig.5 C, D), and in L. Biwa almost all males with thornlike vertex (Fig.5 A, B) . Ventral margin between rostrum and eye slightly con- cave. Rostrum directed ventrally, with apex rounded. Antennules two to three times as long as broad, a lateral sensory hair found subapically and near base of flagellum; flagel- lum shorter than apical sensory hairs (Fig .5 E). First thoracic appendage with a stout hook and a long seta as in Daphnia longispina (Fig.5 F). Carapace oblong, dorsal margin slightly con- vex; maximum width middle anterior border of ventral margin forming thickened rim , bearing no spines or hairs (unlike males of most species Fig.4. Daphnia galeata SARS, A, postabdomen, L. Biwa; B, post abdominal claw, L. Biwa; C, of Daphnia). Posterior half of ventral margin abdominal processes, L. Biwa; D, abdomi- with about 24 wide-spaced spinules. Dorsal nal processes, L. Kizaki; E, post abdominal margin without spinulation. Shell-spine long. claw, L. Kizaki. Abdominal processes rudimentary, second the Daphnia galeata SARS in L. Biwa and L. Kizaki 51

Daphnia, he frequently moved the taxonomic status of particular taxa from species to vari- eties or vice versa in his successive published and unpublished lists (FREY, 1982). D. hyalina, on the other hand, was described by LEYDIG (1860) based on the specimens with low rounded helmets from Lake Constance. According to BROOKS (1957), RICHARD (1896) definitely divided D. galeata as a separate species from D. hyalina, but he included the specimens with taller helmet from L. Constance in D. hyalina. Since then taxonomic complica- tions on both species have continued until quite recently. The historical sketches on the change of taxonomic status or nomenclatures of D. hyalina-galeata complex were shown in CHRISTIE (1983) and FLOSNERand KRAUS (1986). BROOKS(1957) indicated precisely the points of morphological differences between D. hyalina and D. galeata in the assignment of specimens belonging to D. galeata distributed in North America. FLOSNER (1972) and HERBST (1976) followed BROOKS(1957) criteria in their Fig.5. Daphnia galeata SARS, Male: A and B, L. studies of European Daphnia and gave keys for Biwa; C and D, L. Kizaki; E, antennule, L. identification. Most recent publications in Biwa; F, first appendage, L. Biwa. Japan, however, still continue to confuse. It is known that D. galeata distributed widely longest. 9-13 anal teeth. in Holarctic (HRBACEK,1987). Most varieties in D. galeata might be described on the basis of 4. Discussion variation of head shape or different stages of

The hyaline limnetic species of Daphnia from cyclomorphosis. These morphological varia-

Lake Biwa and Lake Kizaki was identified as tions may also indicate a possibility of hybridi-

D. galeata SARS, 1863 emend. FLOBNER and zation of two species or forms (BROOKS,1957,

KRAUS, 1986. The figures of D. hyalina by WOLF, 1987). Investigating numerous popula-

UENO (1973) and MIZUNO (1977) also indicated tions, FLOSNERand KRAUS(1986) suggested that the characteristics of D. galeata SARS. Accord- many local races of D. galeata maybe classified ing to the studies made in Europe, D. galeata into two groups, the typical form with pointed

SARS is distinguished from the closely related helmet and f. gracilis with high but rounded species, Daphnia hyalina LEYDIG, and the hybrid, helmet. They also observed that many inter-

D. galeata •~D. cucullata, which are character- mediate forms between the typical and f. ized by the high and short antennula mound, gracilis appeared in some localities. sharp lateral edges of rostrum and large ocellus Most individuals in the population occurring

(FLOBNER and KRAUS, 1986). in L. Biwa were identical to the typical form,

D. galeata SARS is a highly variable species, and those from L. Kizaki were similar to the and many local races, forms or varieties were varieties of f. gracilis or the inter-mediates described under the name D. galeata since SARS between the typical and the gracilis form. This

(1863) original description. Although SARS coincides with the tendency that the pointed described many species and/or varieties in helmets are more developed in large stratified 52 TANAKA lakes (FLOSNERand KRAUS,1986). But various glaciated areas of Europe, except the Tetras, intermediate forms between acute and round Pyrenees, and Balkans, and the eastern limit helmets occurred also in both lakes. The dif- remains uncertain (HRBACEK,1987). Under the ferences between the two lakes in terms of the key proposed (FLOENERand KRAUS,1986, HUDEC, head shape were also shown in the relationship 1991), neither populations of D. hyalina nor the between head length and total length (Fig.6), hybrids between the two related species has and between head depth and carapace length been recorded in Japan so far. The records of (Fig.7). D. hyalina LEYDIGin much of the literature of The distribution of D. hyalina, on the other Japan may need to be revised to D. galeata hand, is restricted to water bodies of formerly SARS.

Fig.6. Comparison of the relationship between total length (TL) and head length (HL) .

Fig.7. Comparison of the relationship between carapace length (CL) and head depth (HD) . 53 Daphnia galeata SAGS in L. Biwa and L. Kizaki

It is still undetermined how many varieties of tacea: Cladocera). Hydrobiologia, 137: 97-115. D. galeata are present in Japanese lakes and FREY, D. G. (1982): G. O. SARS and the Norwegian reservoirs, and also whether the D. hyalina Cladocera: a continuing frustration. Hydrobiologia 96: 267-293. LEYDIGdistributed in Japan. HERBST, H. V. (1976): Erganzungen zu den "Blatt- fussbreksen" Deutschlands. Limnologische Acknowledgements Schr. Gewass. Abwass. No. 60/61: 7-26. The author is indebted to Drs. T. NARITA and HORIE, S. (1962): Morphometric features and the K. KAWABATA for their field assistance in L. classification of all the lakes in Japan. Mem. Biwa. Thanks are also due to Dr. S. Coll. Sci., Kyoto Univ., Ser. B, 29: 191-262. WATANABE and two anonymous referees for HRBACEK, J. (1987): Systematics and biogeography of Daphnia species in the northern temperate their valuable comments on the manuscript. region. Mem. Ist. Ital. Idrobiol., 45: 37-76. In R. H. PETERS and R. DE BERNARDI (eds.), Daphnia. 摘 要 HUDEC, I. (1991): Occurrence and biology of the

琵 琶 湖 と木 崎 湖 の カ ブ ト ミジ ン コ genus Daphnia, subgenus Daphnia (Cladocera, ) in Slovakia. 3rd part: D. galeata, Daphnia galeata SARSの 形 態 と変 異 D. cucullata. Biologia (Brastislava), 46: 129- カ ブ ト ミ ジ ン コDaphnia galeata Snxsは 形 態 の 138. 変 異 が 大 き く,古 くか ら多 くの 変 種(variety)が KAWABATA,K. (1987): Abundance and distribution of Eodiaptomus japonicus (Copepoda: 記 載 さ れ る な ど,分 類 学 的 に混 乱 した 状 態 に あ っ Calanoida) in Lake Biwa. Bull. Plankton Soc. た が,最 近 ヨー ロ ッパ に お い て,近 縁 の ウス カ ワ ハ リナ ガ ミ ジ ン コDaphnia hyalina LEYDIGと 区 別 Japan, 34: 173-183. LEYDIG, F. (1860): Naturgeschichte der Daphniden. され る は っ き り と した 種 で あ る こ とが 明 らか に さ Tiibingen. れ た。 し か しわ が 国 で は,ハ リナ ガ ミ ジ ン コD. MIZUNo, T. (1977): Illustrations of the freshwater longispina O.F.MULLERま た はD.hyalinaの シ plankton of Japan. Hoikusha Publishing Co. (in ノ ニ ム か 亜 種 と し て あ つ か わ れ て き て お り,D. Japanese) galeataの 分 類 上 の 位 置 が確 定 さ れ な い で きた 。 特 NARITA, T. and K. OKAMOTO (1984): Zooplankton, p. にD.hyalinaと は 明 瞭 に 区 別 され て い な い 。 本 報 313-321. In S. HORIE (ed.), Lake Biwa. Dr. W. Junk Publishers. で は,D.galeataとD.hyalinaの 両 種 が 分 布 す る RICHARD, J. (1896): Revision des Cladoceres, 2. Ann. 湖 と され て きた 琵 琶 湖 と木 崎 湖 のDaphniaを 調 べ Sci. nat. Zool. 8. Ser. 2: 187-363. た と こ ろ,出 現 した 種 は どち ら もD.galeataだ け SARS, G. O. (1863): Berwtning om en i Sommeren で あ る こ と が 明 らか とな っ た 。 ど ち らの 湖 と も出 1862 foretagen zoologisk Reise i Christianias 現 したD.galeataに は大 き な 形 態 の 変 異 が あ り, og Trondhjems Stifter. Nyt Mag. Naturviden- 変 異 は二 つ の 湖 で 異 な っ て い る が,こ の 二 つ の湖 sk. 12: 193-252. の標 本 に も とづ き単 為 生 殖 雌 と雄 の 形 態 の 記 載 と UENO, M. (1927): The freshwater of 若 干 の 考 察 を 行 っ た。 Japan. I. Mem. Coll. Sci., Kyoto Univ., Ser. B, 2: 259-311. References UENO, M. (1934a): The freshwater Branchiopoda of Japan. III. Genus Daphnia of Japan. 1. Seasonal BROOKS, J. L. (1957): The systematics of North succession, cyclomorphosis and reproduction. American Daphnia. Mem. Connect. Acad. Arts Mem. Coll. Sci., Kyoto Univ., Ser. B, 9: 289- Sci.13: 1-180. 320. CHRISTIE, P. (1983): A taxonomic reappraisal of the U>NO, M. (1934b): The freshwater Branchiopoda of Daphnia hyalina complex (Crustacea: Japan. IV. Genus Daphnia of Japan. 2. Local Cladocera): an experimental and ecological races of Japanese Daphnia. Mem. Coll. Sci., approach. J. Zool. Lond. 199: 75-100. Kyoto Univ., Ser. B, 9: 321-342. FLOSNER, D. (1972): Krebstiere, Crustacea. Kiemen- UENO M. (1937): Class Crustacea, Order Bran- und BlattfUsser, Branchiopoda. Fischlause, chiopoda, Fauna Nipponica. 9.135 pp. Sanseido Branchiura. Tierwelt Dtl. 60: 1-501. (in Japanese). FLOSNER, D. and K. KRAUS (1986): On the taxonomy U>NO, M. (1973): Branchiopoda, p. 405-430. In M. of the Daphnia hyalina-galeata complex (Crus- 54 TANAKA

UENO (ed.), The late TAMIJIKAWAmuRA Fresh- (著 者:田 中 晋,富 山 大 学 教 育 学 部 生 物 学 教 室, water Biology of Japan, Enlarged and revised 〒930富 山 市 五 福3190;Susumu TANAKA, Depart- edition. Hokuryukan Publishing Co. (in ment of Biology, Faculty of Education, Toyama Japanese) University, 3190 Gofuku, 930 Toyama) WOLF, H. G. (1987): Interspecific hybridization between Daphnia hyalina, D. galeata and D. Received: 31 May 1991 cucullata and seasonal abundances of these Accepted: 5 October 1991 species and their hybrids. Hydrobiologia, 145: 213-217.