Bull. Natn. Sci. Mus., Tokyo, Ser. B, 22(1), pp. 1- 10, March 22, 1996

Studies on Planktonic Blue-green Algae 6.
Bloom-forming Species in Lake Biwa (Japan)
in the Summer of 1994
By

Masayuki WATANABE
Department of Botany, National Science Museum,4- 1- 1 Amakubo, Tsukuba, lbaraki 305, Japan
Abstract Eight species of bloom-forming cyanophytes were recognized in five samples collected from Lake Biwa, Shiga Prefecture, Japan. The algae include one newspecies, Anabaena oumiana M. Watanabe, and one alga which was proposed for a newrank, Anabaena ucrainica (Schkorbatow) M. Watanabe for A. spiroides var. ucrainica
Schkorbatow. The alga which was previously recorded in the lake as Oscillatoria tenuis
Ag. was thought to be Planktothrix raciborskii (Wolosz.) Anagn. & Kom.

In 1994 Y. MATSUOKA and S. lcHISE of the Shiga Prefectural Institute of
Public Health and Environmental Science brought some plankton samples collected at four sites in Lake Biwa to the author to identify bloom-forming species ofcyanophytes. Lake Biwa is the largest lake in Japan and it plays very importantrole in the local economy. Due to increasing population around the lake,especially in the southern part, eutrophication of the lake water has been accelerating and noxious phytoplankton is increasing year by year. Information onclassification, behaviour and productivity of harmful substances for such algal
speci~s has been of interest to local lake water managers. Lake Biwa has become
one of the most well-known lakes in Japan regarding phytoplankton taxonomy
due to the work of Dr. NEGORO (1968, 1991, etc.) . In the summer of 1994, theclimate of Japan was unusually hot and dry, thus the water level of the lake waslower than that of an ordinary summer. This abnormal climate brought somechanges to the phytoplankton flora of Lake Biwa, namely, abnormal growth ofMicrocystis species and the appearance of new Anabaena species. In this paper theauthor will discuss the state and species of blue-green algal bloom in Lake Biwa
under abnormal climatic conditions.
Materials and Methods
Samples were collected by the staff of the Shiga Prefectural Institute of
Public Health and Environmental Science and brought to the author. The

2

Masayuki WATANABE
Table l.
Sample no.
53658
5365953660
53661
53662

Localities of the materials studied.

Locality
Akanoi harbor, southeast part of the lake
Nagahama harbor, northeast part of the lake
Okoto harbor, southwest part of the lake
Akanoi harbor
Off Konohama, southeast part of the lake

Date of collection
August 22nd, 1994
August 24th, 1994
September 9th, 1994
September 13th, 1994
September 13th, 1994

specimens were fixed with formalin and preserved in the herbarium of theNational Science Museum, Tokyo (TNS) . Table 1 shows the sources of thematerials used in this study.
Results and discussion

Out of the five samples, five species of Anabaena, two species of Microcystis,and one species each of Oscillatoria and Planktothrix were detected. Descriptions
and taxonomic notes are given below.
Anabaena affinis Lemm.
(Figs. 1, 2, 11)
In the samples from Akanoi harbor a small number was of trichomes ofAnabaena affinis observed. Among the single trichomes, only a few bundleforming trichomes were seen. Two other species of Anabaena with straighttrichomes have been known in Lake Biwa, namely A. planctonica Brunth. and A.
smithii (Kom.) M. Watan. A solitary trichome of A. affinis is distinguished fromthe other species by its smaller dimensions and by attenuation at the trichomeends (WATANABE 1971, 1992; NEGORO 1991).
1.

Anabaena crassa (Lemm.) Kom.-Legn. & Cronb.
(Fig. 12)This alga was originally described as a variety of Anabaena spiroides by
LEMMERMANN (1898) and was raised to species rank by KoMARKovALEGNEROVA & CRONBERG (1992) . The alga is characterized by regularly
twisted spring-like coils, elliptical akinetes and larger dimensions than those of A.
spiroides, and is commonly found in the southern part of Lake Biwa (NEGORO1968, 1991). A small number of this alga was found in a sample from Akanoi
harbor (no. 53658), and it became rare after three weeks at the same location (no.
53661; akinetes 16-18 ,urn broad, 18- 20 ,urn long).
2.

Anabaena flos-aquae Breb. in Born. & Flab.
(Figs. 3, 4, 13)
Trichomes free-floating, irregularly twisted, forming floccose colonies, sometimes forming somewhat irregular coils, without a mucilaginous sheath. Cells
spherial or barrel-shaped, with gas vesicles, 5-6 .urn broad. Heterocytes spherical,
3.

Studies on planktonic blue-green algae 6. Bloom-forming species in Lake Biwa

35- 6.5 11m broad. Akinetes remote from heterocytes, cylindrical, with rounded
ends, sometimes slightly curved, 9 f1m broad, 18 flm long.
Authorities from the Shiga Prefectural Institute of Public Health and Environmental Sciences were especially interested in the toxicity of A. jlos-aquae,
which has been known as a toxic alga (GORHAM et al. 1964, CARMICHAEL 1988,PARK et al. 1993). The Biwa alga differs taxonomically from the famous toxic
strains NRC-44-1 and NRC-525-17 from Canadian lakes, at least as indicated by
the two scanning electron micrographs published by CARMICHAEL (1988) . Anabaena jlos-aquae has spherical cells, while, the Canadian strains have cylindricalcells which are characteristic of A. mendotae Trelease (Syn.: A. jlos-aquae var.
treleasii Born. & Flab.), which was originally described from Lake Mendota,Wisconsin. One of the common properties of the two species is the formation offloccose aggregations. In Japan A. jlos-aquae is distributed mainly in the centraldistricts, while, A. mendotae is found in the northern districts, especially in
Hokkaido.
4.

Anabaena oumiana M. Watanabe, sp. nov.
(Figs. 5-7, 14, 15, 19, 21)
Trichomata libere natantia, solitaria, plus minusve regulariter circinata,vaginis crassis mucosis circumcincta. Spirae 28- 46 f1m in diametro, 1G-20 f1m
distantes. Cellulae vacuolis gaseosis includentes, sphaeroideae vel cupiformes,
6.G-7.1 f1m latae, 3.G-6.5 flm longae. Heterocytae sphaerica, 6.8-8.5 f1m latae,
6.4- 8.0 longae. Akineta sphaerica, 1G-12 flm lata, solitaria vel binata, ad heterocytas unilaterale vel utrirnque affixa.
Iconotypus: Figurae 5-7.
Locus typicus: in lacu Biwa, Shiga, Japoniae.
Trichomes free-floating, solitary, more or less regularly coiled, covered withthick mucilage. Coils 28- 46 flm broad, 1G-20 flm apart. Cells with gas vesicles,
subspherical or barrel-shaped, 6.G-7.1 flm broad, 3.G-6.5 flm long. Heterocytesspherical, 6.8-8.5/lm broad, 6.4-8.0/lm long. Akinetes spherical, 1G-12f.1m
broad, solitary or in pairs, attaching at one or both sides of the heterocytes.
The new species resembles Anabaena spiroides Kleb. superficially, but differs
in producing spherical akinetes. Although the alga approaches A. ucrainica inakinete form, it differs in the dimensions of its cells and in the relative location of
the akinetes to the heterocytes. In A. ucrainica, akinetes develop away from theheterocytes. The new species is closest in many aspects to A. kisseleviana (Kissel.)
Elenk. except the latter species has straight trichomes.
Etymology: Oumi is the old name of Lake Biwa and means "large lake."
5.

Anabaena ucrainica (Schkorb.) M. Watanabe, stat. nov.
(Figs. 8, 16-18)
Syn. Anabaena spiroides var. ucrainica Schkorbatow, Not. Syst. Inst. Crypt.
Hort. Bot. Petropol. 2(6) : 88 (1923) .

Masayuki W ATANABE

4068
1
Figs. 1- 7. 1, 2. Anabaena affinis.
nov. All: X 1000.

3, 4. Anabaena jlos-aquae.

5- 7. Anabaena oumiana sp.

Studies on planktonic blue-green algae 6. Bloom-forming species in Lake Biwa~·-­t-\ 10
Figs. 8- 10.

8. Anabaena ucrainica. 9, 10. Planktothrix raciborskii. All: X 1000.

5

6Masayuki WATANABE

1617Figs. 11- 19. 11. Anabaena affinis. 12. Anabaena crassa. 13. Anabaenajlos-aquae. 14, 15.
Anabaena oumiana sp. nov. 16, 17. Anabaena ucrainica with spherical akinetes. 18. a:Anabaena ucrainica, b: Microcystis aeruginosa treated with ink. 19. Anabaena oumianatreated with ink. 11- 14, 16-19: X 200, 15: X 100.

Studies on planktonic blue-green algae 6. Bloom-forming species in Lake Biwa

7Trichomes solitary, free-floating, forming regular coils, with a thick mucilaginous sheath. Coils about 60 ttm in diameter, so-70 ttm apart. Cells spherical orshort barrel-shaped, about 10 ttm broad. Heterocytes spherical, about the same
size with the cells. Ak.inetes spherical, 18-23 ttm broad, remote from theheterocytes.
This alga was originally described by ScHKORBATOW from Ukraina as a newvariety of Anabaena spiroides, distinguishing from A. spiroides var. crassa byspherical akinetes. The present author proposes to give the species rank for thealga, because the relation between var. crassa and var. ucrainica is comparablewith that of A. planctonica andA. smithii (WATANABE 1992) and var. crassa waschanged to the species rank by KOMARKOVA-LEGNEROVA & CRONBERG (1992).
Anabaena spiroides var. crassa has been recorded from many places in Japan
without any information of akinetes in most cases (UMEZAKI & WATANABE
1994), but at least some of those algae should be identified as A. ucrainica. The
present author previously noted the presence of "A. ucrainica" in Lake Sagami(WATANABE 1994).
6.

Microcystis aeruginosa (Ktitz.) Ktitz.
(Figs. 20a, 21 b)
Outline of colonial mucilage not visible under a microscope. Cells irregularlyarranged, spherical, with gas vesicles, S.o-6. 7 ttm broad.
This alga was the most abundant of all the samples examined.

7.

Microcystis wesenbergii (Kom.) Kom. in Kondr.
(Fig. 20b)
Colonies soft, spherical or irregularly lobated, composed of refractive envelopes and filling mucilage. Cells attached to inside of the envelope in single layer.
Among this species, two different types of cell dimensions were observed. Most ofthe colonies examined had smaller cells about 6 ttm broad while the larger ones
were 6.9-7.2ttm broad.

8.

Oscillatoria kawamurae Negoro(Fig. 22)
This species was originally described from Manchuria, northwest China by
NEGORO (1943), and appeared in Lake Biwa recently (NEGORO 1991). The alga
is characterized by very wide trichomes of a maximum breadth of over 70 ttm andregularly arranged large gas vesicles. Each discoid cell contains 3 or 4 gas vesicles
at periphery which gradually change positions with respect to adjacent cells.
Consequently regulary and loosely twisted lines are visible from the surface of thetrichomes.

9.

Planktotbrix raciborskii (Wolosz.) Anagn. & Kom.
(Figs. 9, 10, 21c, 23, 24a)Syn. Oscillatoria raciborskii W olosz.

8Masayuki WATANABE

J4(ua~'~ U.tdihl.

tNtt• ,,, .. n,... ..

du*'•'!fllf!

* ~,~ ,•'".

122~ •.Jl~!:.. cFigs. 2G-24. 20. a: Microcystis aeruginos, b: M. wesenbergii. 21. a: Anabaena oumian, b:Microcystis aeruginosa, c: Planktothrix raciborski. 22. Oscillatoria kawamurae. 23.
Planktothrix raciborskii.
24. a: Planktothrix raciborskii, b: Anabaena oumiana, c:Microcystis aeruginosa. 20, 21: X 60, 22, 23: X 100, 24: X 200.

Trichomes straight, several hundreds micrometers long, solitary, freefloating, with gas vesicles, without constriction at the cross-walls, 9.5-11 (-12) f..lm
broad, usually attenuated and sometimes bent at the apex.
This species is common in eutrophic lakes in central Japan (WATANABE
1994) and has been recorded as Oscillatoria tenuis Ag. in Lake Biwa (NEGORO
1968, 1991). Oscillatoria tenuis does not form gas vesicles and is fundamentallya benthic species.
The distribution and appearance of the algal species in the specimens
examined are summarized in Table 2. Algae were most at Akanoi harbor andpoorest at Nagahama harbor in both quality and quantity. MATSUOKA andICHISE told the first findings of Anabaena ftos-aquae and A. oumiana in Lake Biwa(in personal comm.).

Studies on planktonic blue-green algae 6. Bloom-forming species in Lake Biwa

9Table 2. Distribution and appearance of the species in the specimens.
Locality
SpeciesAnabaena affinis
Anabaena crassa
Anabaena jlos-aquae
Anabaena oumiana
Anabaena ucrainica
Microcystis aeroginosa
Microcystis wesenbergii
Oscillatoria kawamurae
Planktothrix raciborskii

AkanoiAug. 22nd

Nagahama
Aug. 24th

Okoto
Sept. 9thfew
few
abundant
few
manycommon

many
few

few
many
few

Akanoi
Sept. 13th
few
rare
few
few
few
many

off Konohama
Sept. 13th

few
many
few
few

common- : not detected.

Acknowledgements
The author expresses his sincere thanks to Mr. Yasutsune MATSUOKA andMr. Satoshi lCHISE of the Shiga Prefectural Institute of Public Health andEnvironmental Science for presenting the materials and to Dr. Ken KATSUMOTO
for his help in the preparation of the Latin descriptions.

References
Carmichael, W. W., 1988. Toxins of Freshwater Algae. In A. T. Tu (ed.), Handbook of NaturalToxins 3: 121-147. Marcel Dekker, New York.
Gorham, P. R., J. McLachlan, U. T. Hammer & W. K . Kim., 1964. Isolation and culture of toxic
strains of Anabaenajlos-aquae (Lyngb.) de Breb. Verb. Internat. Verein Limnol. 15: 796-804.
Komiukova-Legnerova, J. & G . Cronberg, 1992. New and recombined filamentous cyanophytes
from 6 lakes in South Scania, Sweden. Algol. Stud. 67 : 21- 32.
Negoro, K ., 1943. Untersuchungen iiber die Planktoncyanophyceen der Binnengewiisser derMandschurei. I. Se. Rep. Tokyo Bunrika Daigaku, Sect. B 6(94): 69- 85, Taf. I, 11.
Negoro, K. , 1968. Phytoplankton of Lake Biwa. InS. Kitamura (ed.) , Flora Ohmiensis, pp. 275330, pis. 14- 31. Hoikusha, Osaka (in Japanese).
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1993. Hepatotoxin (microcystin) and neurotoxin (anatoxin-a) contained in natural blooms andstrains of cyanobacteria from Japanese freshwaters. Natural Toxins 1: 353- 360.
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Nostocales and Stigonematales. Jpn. J. Phycol. 42: 301- 324.
Watanabe, M. , 1971. The species of Anabaena from Hokkaido. J. Jap. Bot. 46: 263- 277 (inJapanese) .
Watanabe, M., 1992. Studies on planktonic blue-green algae 4. Some Anabaena species with straighttrichomes in Japan. Bull. Natn. Sci. Mus. , Tokyo, Ser. B. 18: 123- 137.

10Masayuki WATANABE

Watanabe, M., 1994. Bloom-forming cyanophytes in Japan. In M. F . Watanabe, K.-1. Harada & H.
Fujii (eds.), Waterbloom of Blue-green algae and Their Toxins, pp. 25- 54. Univ. Tokyo Press,Tokyo (in Japanese) .