Bull. Natn. Sci. Mus., Tokyo, Ser. B, 30(4), pp. 135–149, December 22, 2004

Studies on Planktonic Blue-green Algae 10. Classification of
Planktonic Anabaena with Coiled Trichomes Maintainedin the National Science Museum, Tokyo
Masayuki Watanabe, Yuko Niiyama and Akihiro Tuji
Department of Botany, National Science Museum, Amakubo 4–1–1, Tsukuba, 305–0005 Japan
E-mail: watanabe@kahaku.go.jp; y-niiya@gw2.u-netsurf.ne.jp; tuji@kahaku.go.jp

Abstract Twenty seven strains of planktonic Anabaena with regularly coiled trichomes fromtwenty one localities in Japan were cultured under the same conditions. The form and dimensionsof cells, heterocytes, akinetes and coils of all the strains were examined under a microscope. They
were classified into nine species, A. akankoensis, A. circinalis, A. crassa, A. mucosa, A. oumiana,
A. pseudocompacta, A. reniformis, A. spiroides and A. ucrainica. Of morphological characteristics,
coil form is the most changeable within several years of culture, but the form and dimensions ofcells, heterocytes and akinetes are stable enough to identify at the species level. Some taxonomic
notes are given.
Key words : morphology, taxonomy, planktonic, Anabaena, strains, culture, blue-green algae,
Japan.

Since Professor Okamura recorded planktonic
Anabaena, A. flos-aquae and A. spiroides var.
crassa from Japanese waters for the first time
(Okamura 1916), eleven Anabaena species withcoiled trichomes have been reported up to today.
These are Anabaena akankoensis M. Watan., A.
circinalis Rabenh. ex Born. et Flah., A. crassa(Lemm.) Kom.-Legn. et Cronb., A. eucompacta
Li et M.M. Watan., A. minispora M. Watan., A.
mucosa Kom.-Legn. et Elor., A. oumiana M.
Watan., A. pseudocompacta M. Watan., A. reniformis Lemm. emend. Aptek., A. spiroides Kleb.
and A. ucrainica (Schkorb.) M. Watan.
In order to examine morphological variations
among Anabaena strains under the same controlled conditions, we have collected manyplankton samples from different localities inJapan, and obtained a hundred strains from twenty water bodies. For the present study we used 27
strains from 21 different collecting sites andcompared dimensions of vegetative cells, heterocytes, akinetes and trichome coils. After a longculture many strains lose the natural forms which
they had when they lived in nature, but thestrains keep the necessary characteristics to identify them at the species level.
Materials and Methods
The strains used in this study are shown in
Table 1. They were maintained in the stock roomof the Department of Botany, National Science
Museum in Tsukuba, Ibaraki prefecture (TAC,
Tsukuba Algal Collection). Most of the strainsused in this study were isolated in 2001 and 2002
from eutrophic lakes and ponds in Japan (Fig. 1).
Samples were collected with a plankton net andcarried in small vials to our laboratory within a
few days. Isolation was done by the pipette washing method under a binocular. Throughout thisstudy, 10 ml of NaCB medium (Ichimura and
Watanabe 1977) contained in a screw cap test
tube (18 mm150 mm) was used. The cultures
were illuminated by cool-white fluorescentlamps; photon flux density was about
20 m mol/m2/sec and the photoperiod was 12hours light and 12 hours dark. The temperature
was kept at 20°C.

136

Masayuki Watanabe, Yuko Niiyama and Akihiro Tuji
Table 1. Anabaena strains with regularly coiled trichomes used in this study.

TAC No.

Collecting site

Date of collection

Collector

Isolator

425
449
455
464
473
477
478
481
482
484
486
490
492
497
501
504
505
509
518
520
522
529
539
541
543
551
553

Lake Toro-ko, Hokkaido Pref.
Lake Sagami-ko, Kanagawa Pref.
Lake Tsukui-ko, Kanagawa Pref.
Lake Inba-numa, Chiba Pref.
Nigo-ike pond, Hyogo Pref.
Nigo-ike pond, Hyogo Pref.
Shin-ike pond, Hyogo Pref.
Tatsugaya-ike pond, Hyogo Pref.
Lake Inba-numa, Chiba Pref.
Lake Tega-numa, Chiba Pref.
Lake Biwa-ko (Akanoi), Shiga Pref.
Lake Yogo-ko, Shiga Pref.
a pond, Niigata Pref.
Lake Shiroyama-ko, Kanagawa Pref.
Lake Shiroyama-ko, Kanagawa Pref.
Soe-ike-nishi pond, Hyogo Pref.
Lake Akan-ko, Hokkaido Pref.
Funada-ike pond, Chiba Pref.
a pond in Fujiidera City, Osaka Pref.
Lake Suwa-ko, Nagano Pref.
a pond in Mannou town, Kagawa Pref.
Lake Biwa-ko (Otsu), Shiga Pref.
Lake Hachiro-gata, Akita Pref.
Lake Hachiro-gata, Akita Pref.
a pond in Fujiidera City, Osaka Pref.
Mishima-ike pond, Shiga Pref.
Lake Hachiro-gata, Akita Pref.

Aug. 1990
Aug. 1991—
Aug. 1996
Jul. 2001
Jul. 2001
Jul. 2001
Jul. 2001
Sept. 2001
Sept. 2001
Oct. 2001
Oct. 2001
Oct. 2001
Nov. 2001
Nov. 2001
Nov. 2001
Sept. 2002
Aug. 2002
Oct. 2002
Oct. 2002
Oct. 2002
Oct. 2002
Jul. 2002
Aug. 2002
Oct. 2002—
Sept. 2002

Watanabe M.
Watanabe M.
Watanabe M.
Watanabe M.
Nakagawa M.
Nakagawa M.
Nakagawa M.
Nakagawa M.
Watanabe M.
Watanabe M.
Watanabe M.
Watanabe M.
M. Dai Naw
Arii S.
Arii S.
Nakagawa M.
Tuji A.
Nakaike T.
Tuji A.
Tuji A.
Tuji A.
Tuji A.
Sasaki S.
Sasaki S.
Tuji A.
Tsujimura S.
Sasaki S.

Niiyama Y.
Niiyama Y.
Watanabe M.
Watanabe M.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Niiyama Y.
Tsujimura S.
Niiyama Y.

Observations and Discussions
Morphological observations such as the forms
and dimensions of vegetative cells, heterocytes,
akinetes and trichomes as well as the relative location of the akinetes to the heterocytes havebeen performed for the twenty seven strains. All
the strains were classified into the following ninespecies. The species are arranged approximatelyfrom small to large in vegetative cell diameter(Table 2).
1.

Anabaena reniformis Lemm. emend. Aptek.
Figs. 3–10
Cells spherical to slightly elongated, 3.0–6.0
m m wide, 2.5–10.0 m m long.; l/w ratios 0.67–
2.50. Heterocytes spherial to slightly elongated,
4.5–7.5 m m wide, 5.5–10.0 m m long. Akinetes
spherical, one to three in series, attaching usuallyat both sides of heterocytes, 8.0–12.5 m m wide.
Trichomes regularly coiled, closely contracted,

coils 20.0–50.0 m m wide, 5.0–25.0 apart.
The strains examined were TAC 478, 481, 484
and 543.
Lemmermann (1898) described Anabaena
reniformis nov. spec. from Steinhuder Meer. The
new species was characterized by kidney formed
vegetative cells, though he could not observeakinetes. Aptekar reported the same alga developing akinetes richly from around DnieproPetrovsk in 1927. Elenkin (1938) cited Aptekar’s
figures in his monograph. Measuring the original
figures (Fig. 2) cited by Elenkin (l.c.) l/w ratios
in vegetative cells are 0.8–1.8. These measurements are comparable with those of our algae.
Anabaena reniformis was recorded by Niiyama(1996) for the first time in Japan from Sikata-futago-ike pond, Hyogo prefecture and succeedingly recorded by Watanabe (1998) from Lake
Koya-ike, Oosaka prefecture. According to Professor Yukio Kimura of Mukogawa Women’s
University, this alga caused heavy water bloom inClassification of Planktonic Anabaena with Coiled Trichomes

Fig. 1.

137

Localities of strains isolated and used in this study.

Lake Koya-ike every year. In this paper, four localities, Shin-ike pond, Tatsugaya-ike pond in
Hyogo prefecture, a pond in Fujiidera city, Oosaka prefecture and Lake Tega-numa, Chiba prefecture are newly added to distribution records inJapan.
Some strains lose their original form during along culture year by year. TAC 481 isolated in
July, 2001 from Tatsugaya-ike pond has now lostits regularly spiral form. The trichomes of thealga are almost straight these days. Measurements of cells, heterocytes and akinetes in strainsshow a more or less wider range than those innatural populations.

Fig. 2. Anabaena reniformis
Aptekar after Elenkin.

Lemm.

emend.

138

Masayuki Watanabe, Yuko Niiyama and Akihiro Tuji

Table 2. Dimensions of vegetative cells, heterocytes, akinetes and coils among strains used in this study.
Species

TAC
No.

Vegetative Cells
Width m m

Length m m

Heterocytes
Width m m

L/W

A. reniformis

481 3.0–4.8 (3.87)
2.5–6.5 (4.48) 0.67–1.63 (1.16)
484 3.0–5.5 (4.16)
3.0–10.0 (5.17) 1.00–2.00 (1.25)
478 3.0–5.3 (4.40)
3.0–8.0 (5.16) 0.67–2.50 (1.21)
543 3.8–6.0 (4.58)
3.8–7.5 (5.40) 0.84–1.40 (1.18)
A. pseudocompacta 539 3.0–5.0 (4.24)
3.5–7.5 (5.29) 0.73–2.50 (1.30)
541 3.0–5.0 (4.43)
2.5–7.5 (4.93) 0.50–1.80 (1.13)
477 4.0–6.0 (4.77)
2.5–7.5 (5.41) 0.50–1.88 (1.14)
A. oumiana
464 5.0–7.0 (5.96)
5.0–7.5 (6.35) 0.79–1.50 (1.09)
509 5.5–7.5 (6.13)
3.8–6.8 (5.08) 0.53–1.13 (0.84)
A. spiroides
551 5.0–7.3 (5.90)
3.5–7.5 (5.63) 0.70–1.22 (0.95)
504 7.5–9.5 (8.33)
5.5–8.0 (6.55) 0.66–1.00 (0.79)
A. akankoensis
505 6.3–8.8 (7.40)
5.0–11.5 (7.95) 0.64–1.53 (1.08)
A. crassa
518 7.0–10.0 (8.08) 5.0–8.5 (6.62) 0.50–1.00 (0.83)
529 8.0–11.0 (9.93) 5.0–10.0 (6.97) 0.49–1.00 (0.70)
486 9.0–11.3 (9.99) 4.5–7.5 (5.95) 0.45–0.75 (0.59)
490 8.0–11.8 (10.01) 4.5–10.0 (7.41) 0.47–1.00 (0.74)
473 8.5–12.5 (10.21) 4.8–10.5 (7.08) 0.48–1.00 (0.70)
492 8.5–12.3 (10.31) 5.0–10.0 (7.85) 0.49–1.00 (0.77)
522 9.3–13.0 (11.79) 6.3–12.5 (8.70) 0.50–0.96 (0.74)
520 10.0–13.0 (12.03) 5.0–10.0 (7.51) 0.40–0.95 (0.63)
A. ucrainica
449 9.5–12.0 (10.43) 4.5–10.0 (7.33) 0.47–0.95 (0.70)
455 10.0–12.5 (11.03) 4.5–8.0 (6.29) 0.40–0.76 (0.57)
A. mucosa
425 10.0–13.0 (11.94) 6.3–12.5 (9.54) 0.53–1.00 (0.79)
A. circinalis
482 7.5–10.5 (9.08) 5.0–12.5 (7.81) 0.53–1.33 (0.86)
497 9.3–13.0 (10.72) 4.5–12.5 (7.14) 0.45–1.00 (0.65)
553 10.0–12.5 (11.00) 6.3–10.0 (9.15) 0.63–1.00 (0.83)
501 9.5–13.3 (11.48) 7.0–10.0 (8.49) 0.59–1.00 (0.75)

SpeciesA. reniformis

A. pseudocompacta
A. oumiana
A. spiroides
A. akankoensis
A. crassa

A. ucrainica
A. mucosa
A. circinalis

TAC
No.
481
484
478
543
539
541
477
464
509
551
504
505
518
529
486
490
473
492
522
520
449
455
425
482
497
553
501

Length m m

L/W

4.5–6.3 (5.53)
5.5–7.5 (6.48) 1.10–1.27 (1.17)***
5.0–7.5 (6.33)
5.5–10.0 (7.31) 1.00–1.67 (1.18)
5.8–6.0 (5.90)
6.5–7.5 (7.00) 1.08–1.29 (1.18)
5.0–7.5 (6.25)
6.3–8.0 (7.15) 1.07–1.26 (1.16)
5.0–5.5 (5.16)
5.0–6.5 (5.52) 1.00–1.30 (1.07)
5.0–6.3 (5.41)
5.0–7.5 (6.80) 1.00–1.42 (1.26)
7.5
7.5
1.00
7.5–8.8 (8.08)
7.5–8.8 (8.08) 1.00
5.8–7.5 (6.93)
7.5–9.5 (8.17) 1.00–1.29 (1.19)
7.5–9.5 (8.78)
7.5–9.3 (8.28) 0.86–1.06 (0.94)
7.5–10.0 (9.06) 7.5–10.0 (9.37) 1.00–1.11 (1.04)
7.5–9.5 (8.00)
7.3–9.5 (8.10) 0.97–1.10 (1.01)
*
*
*
*
*
*
*
*
*
*
*
*
10.0–12.5 (10.92) 9.3–11.3 (10.28) 0.90–1.03 (0.94)
12.5
12.5
1.00
12.5–13.8 (13.10) 12.5–13.8 (13.10) 1.00
*
*
*
*
*
*
11.3–13.3 (12.57) 13.0–15.0 (14.02) 1.08–1.16 (1.12)
8.0–10.0 (9.43) 7.5–11.3 (9.66) 0.93–1.13 (1.02)
10.0–12.5 (11.32) 10.0–13.0 (11.06) 0.93–1.07 (0.98)
10.0–12.5 (10.55) 10.0–12.5 (10.80) 0.97–1.14 (1.02)
12.5–13.3 (12.80) 12.0–13.0 (12.42) 0.90–1.00 (0.97)

Akinetes

Coils

Width m m

Length m m

L/W

Width m m

Distance m m

8.0–10.0 (9.41)
8.0–12.5 (10.50)
8.8–12.0 (9.91)
8.8–12.5 (10.48)
7.5–7.5 (7.50)
6.3–7.5 (6.90)
5.0–8.0 (7.18)
10.0–12.5 (11.28)
9.5–10.5 (10.21)
8.0–10.0 (9.62)
8.0–11.3 (9.78)
12.0
12.5–15.8 (13.83)
15.5–20.0 (18.21)
15.0–18.8 (16.88)
16.3–20.0 (17.87)
15.0–18.8 (16.41)
14.5–17.5 (16.08)
17.5–22.5 (20.04)
17.5–20.0 (18.23)
20.0–22.5 (20.38)
17.5–22.5 (20.14)
17.8–22.5 (19.99)
12.5–16.3 (14.42)
12.5–17.5 (15.67)
13.0–20.0 (16.12)
15.0–22.5 (17.93)

8.8–11.3 (9.96)
8.0–12.5 (10.53)
8.0–12.5 (10.48)
8.8–12.5 (10.48)
20.5–26.3 (23.10)
16.0–17.5 (16.75)
10.0–15.0 (12.39)
10.0–12.8 (11.37)
9.5–10.5 (10.21)
18.0–25.0 (20.31)
19.5–28.5 (22.66)
27.5
15.0–20.0 (17.05)
20.3–27.5 (24.48)
20.0–26.3 (22.60)
20.0–27.5 (22.43)
17.0–21.3 (19.12)
17.0–22.5 (19.90)
22.5–27.5 (25.02)
20.0–25.5 (23.71)
20.0–23.0 (21.19)
18.0–22.5 (20.07)
21.3–27.5 (23.39)
21.3–30.0 (27.52)
29.5–46.0 (37.05)
22.5–31.5 (27.65)
25.5–38.0 (31.97)

1.00–1.19 (1.06)
0.95–1.05 (1.00)
0.91–1.19 (1.06)
1.00–1.00 (1.00)
2.73–3.51 (3.08)
2.33–2.54 (2.43)
1.33–3.00 (1.76)
1.00–1.05 (1.01)
1.00–1.00 (1.00)
1.80–2.50 (2.11)
2.00–2.64 (2.32)
2.29
1.14–1.37 (1.23)
1.27–1.43 (1.34)
1.17–1.45 (1.34)
1.14–1.46 (1.26)
1.13–1.33 (1.17)
1.17–1.32 (1.24)
1.13–1.57 (1.25)
1.14–1.41 (1.30)
1.00–1.13 (1.04)
0.90–1.09 (1.00)
1.13–1.25 (1.17)
1.31–2.07 (1.94)
1.84–2.71 (2.38)
1.42–2.33 (1.74)
1.38–2.50 (1.81)

20.0–35.7
20.0–30.0
25.0–50.0
20.0–30.0
17.5–30.0
15.0–20.0
17.5–30.0
20.0–40.0
30.0–37.5
12.5–25.0
30.0–35.0
37.7–75.0
32.5–40.0
45.0–50.0
42.5–45.0
50.0–60.0
30.0–40.0
30.0–50.0
50.0–62.5
32.5–50.0
50.0–70.0
50.0–62.5
160.0–175.0
120.0–150.0
62.5–87.5
110.0–145.0
45.0–75.0**
7.5–10.0
10.0–25.0
5.0–10.0
7.5–10.0
5.0–10.0
5.0–10.0
ca. 20.0
10.0–30.0
5.0–7.5
ca. 30.0
30.0–90.0
30.0–40.0
55.0–62.5**
50.0–60.0
ca. 50.0
ca. 50.0
67.5–82.5
30.0–50.0
20.0–30.0
37.5–50.0****
ca. 50.0**
ca. 50.0*: not developed; **: not be measured because of fragmentation; ( ): mean value.

Classification of Planktonic Anabaena with Coiled Trichomes

Figs. 3–10. Anabaena reniformis, 3–4: TAC 481, 5–6: TAC 484, 7–8: TAC 478, 9–10: TAC 543.
Scale bar100 m m.

139

140

Masayuki Watanabe, Yuko Niiyama and Akihiro TujiFigs. 11–16. Anabaena pseudocompacta, 11–12: TAC 539, 13–14: TAC 541, 15–16: TAC 477.
Scale bar100 m m.

2.

Anabaena pseudocompacta M. Watan.
Figs. 11–16
Cells spherical to slightly elongated, 3.0–6.0
m m wide, 2.5–7.5 m m long; l/w ratios 0.50–2.50.
Heterocytes spherial to slightly elongated, 5.0–
7.5 m m wide, 5.0-8.0 m m long. Akinetes long ellipsoidal, remote from heterocytes, 6.3–8.0 m mwide, 10.0–26.3 m m long; 1/w ratios 1.33–3.51.
Trichomes regularly coiled, coils 15.0–30.0 m mwide, 5.0–10.0 m m apart.
Strains examined were TAC 477, 539 and 541.
This alga from Lake Kasumigaura was first re-ported as Anabaena spiroides (Watanabe andChihara 1980) and afterwards it was described asa new species based on natural samples from
Lake Tega-numa and Lake Inba-numa, Chiba
prefecture (Watanabe 1996a). In this paper two
localities, Nigo-ike pond, Hyogo prefecture andLake Hachirougata, Akita prefecture are newly
added to distribution records in Japan. This alga
resembles A. reniformis in sterile conditions, but
clearly differs in akinete form and in relative location of akinetes to heterocytes.
Measurements of cells in the strains used in

Classification of Planktonic Anabaena with Coiled Trichomes

141

Figs. 17–20. Anabaena oumiana, 17–18: TAC 464, 19–20: TAC 509. Scale bar100 m m.

this study are slightly smaller than those in a natural population from Lake Teganuma (Watanabe
1996a).
3.

Anabaena oumiana M. Watan.

Figs. 17–20
Cells spherical, 5.0–7.5 m m wide, 3.8–7.5 m mlong: l/w ratios 0.53–1.50. Heterocytes spherical,
7.5–8.8 m m wide. Akinetes spherical, attaching at
both sides of heterocytes, 9.5–12.5 m m wide.
Coils slightly irregular, 20.0–40.0 m m wide,
10.0–30.0 m m apart.
The strains examined were TAC 464 and 509.
This alga was originally described by Watanabe (1996) studying natural samples from Lake
Biwa-ko, Shiga prefecture. In this paper, two localities, Lake Inba-numa and Funada-ike pond in
Chiba prefecture, are newly added to distribution
records in Japan. Measurements of cells instrains examined in this study show a slightly
wider range than those in the natural population(Watanabe l.c.).

This alga seems to be most identifiable with A.
spiroides sensu auct. (Klebahn 1895), because
both algae have spherical akinetes attaching at
one or both sides of heterocytes, and they also
show similar forms and dimensions in cells, heterocytes, akinetes and coils. The concept of Anabaena spiroides, especially on akinetes, waschanged after original publication. Lemmermann(1910) defined akinete form as “Akinetes at first
spherical, later slightly curved, almost hexagonalin optical longitudinal section”. Lemmermann(l.c.) did not mention the relative location of
akinetes to heterocytes, but Geitler (1932) added
a new concept “next to heterocysts or remotefrom heterocysts”. Thus the current concept of
Anabaena spiroides has been established.
According to Klebahn (l.c.) A. spiroides has
cells 6.5–8 m m in diam. and a young akinete
14 m m in diam. When this akinete develops into
elliptic form, the akinete also attains a wider diameter than 14 m m. Few planktonic species ofAnabaena have an akinete in which width gains

142

Masayuki Watanabe, Yuko Niiyama and Akihiro Tujimore than two times more than vegetative cells.
A rare case can be seen in Anabaeba macrospora
Kleb. (Kleb. 1895, akinete w./cell w. ratio is morethan 2.6; Watanabe, Kiyosawa and Hayashi 1985,
Watanabe 1992, akinete w./cell w. latio is 2.4).
To his shame Watanabe (1996) passed at least
the following three papers unmarked. Frémy(1930) recorded Anabaena spiroides from Victoria-Nyanza, Africa with a figure of sphericalakinetes attaching to both side of herocytes.
Tiffany and Britton (1952) recorded the samealga with a figure after Frémy (l.c.) from Illinois,
USA. Baker (1991) also recorded the same algafrom several water bodies in Australia. After
Klebahn published the original description we
can not fined very many records on Anabaena
spiroides in an original sense in Europe or in theUSA, regrettably.
4.

Anabaena spiroides Kleb.
Figs. 21–26
Cells spherical, 5.0–9.5 m m wide, 3.5–8.0 m m
long; l/w ratios 0.66–1.22. Heterocytes spherical,
5.8–9.5 m m wide, 7.5–9.5 m m long. Akinetes
long ellipsoidal, remote from heterocytes, 8.0–
11.3 m m wide, 18.0–28.5 m m long; l/w ratios
1.80–2.64. Coils slightly irregular, 12.5–35.0 m mwide, ca 5.0–30.0 m m apart.
The strains examined were TAC 504 and 551.
As seen in Finland (Kom.-Legn. and Elor.
1992) Anabaena spiroides does not distribute so
widely in Japanese waters as A. crassa. and A.
circinalis do. Most records of A. spiroides lacking akinete information were possibly of A.
oumiana, A. crassa or A. circinalis. The forms
and dimensions of akinetes in this species are thesame as those in A. pseudocompacta, but thecells in the former are larger and relatively shorter than those of the latter.
Measurements of cells and akinetes in strains
examined in this study show a slightly wider
range than those in a natural population at Lake
Koyama-ike (Watanabe 1998).
5.

Anabaena akankoensis M. Watan.
Figs. 27–28
Cells almost spherical, sometimes somewhat

protruding at both ends, 6.3–8.8 m m wide, 5.0–
11.5 m m long: l/w ratios 0.64–1.53. Heterocytes
spherical, 7.5–10.0 m m wide, 7.5–10.0 m m long.
The strain examined was TAC 505.
Only one immature akinete was observed during the present study. The akinete is elongated,12.0 m m wide and 27.5 m m long. This alga wasreported from Lake Akan-ko by the first authorof this paper for the first time as Anabaena circinalis (Watanabe 1971) and described as a new
species after examinations on enough natural
samples with mature akinetes by the same author(Watanabe 2003). Akinetes of A. akankoensis develop at both sides of and one or two cells remotefrom heterocytes. The strain TAC 505 was isolated from the same natural sample with a preserved specimen, no. 54054 (TNS).
Measurements of cells in this study show awider range than those in a natural populationfrom Lake Akan-ko, sample no. 54054 in TNS(Watanabe l.c.).
This species resembles A. fusuca Hill (1976)
described from a Minnesota lake in the forms ofcells, heterocytes and akinetes, but clearly differs
in dimensions (Watanabe l.c.).
6. Anabaena crassa (Lemm.) Kom.-Legn. andCronb.
Figs. 29–42
Cells spherical, 7.0–13.0 m m wide, 4.5–12.5
m m long; l/w ratios 0.40–1.00. Heterocytes
spherical, 7.5–13.8 m m wide, 7.3–13.8 m m long.
Akinetes ellipsoidal, remote from heterocytes,
12.5–22.5 m m wide, 15.0–27.5 m m long; l/w ratios 1.13–1.57. Coils regular, 30.0–62.5 m mwide, 30.0–82.5 m m apart.
The strains examined were TAC 473, 486, 490,
492, 518, 520, 522 and 529.
This alga shows the widest distribution
throughout Japan and inter strainal variations arealso wide. Four strains did not form heterocytes
under the present culture condition. Measurments of cells, heterocytes, akinetes and coils of
the strains used in this study show a wider range
than those in natural populations (Watanabe1998).

Classification of Planktonic Anabaena with Coiled Trichomes

Figs. 21–26. Anabaena spiroides, 21–23: TAC 551, 24–26: TAC 504.
Figs. 27–28. Anabaena akankoensis, TAC 505. Scale bar100 m m.

143

144

Masayuki Watanabe, Yuko Niiyama and Akihiro TujiFigs. 29–34. Anabaena crassa, 29–30: TAC 518, 31–33: TAC 529, 34: TAC 486. Scale bar100 m m.

7.

Anabaena ucrainica (Schkorb.) M. Watan.
Figs. 43–46
Cells spherical, 9.5–12.5 m m wide, 4.5–10.0
m m long; l/w ratios 0.40–0.95. Heterocytes notobserved. Akinetes spherical, 17.5–22.5 m mwide, 18.0–23.0 m m long; l/w ratios 1.00–1.04.
Coils regular, 50.0–70.0 m m wide, 20.0–50.0 m mapart.
The strains examined were TAC 449 and 455.
This alga was recorded from Lake Sagami-ko
by the present author for the first time in Japan(Watanabe 1994, as A. spiroides var. ucrainica
Schkorb.), and was second recorded from Lake

Biwa-ko (Watanabe 1996). Measurements ofcells and akinetes in the strains used in this study
show a slightly wider range than those in natural
populations from Lake Sagami-ko and Lake
Biwa-ko (Watanabe 1998).
Morphological characters except the akinete
form of this species almost resemble those of A.
crassa. The length width ratios of akinetes deviate from each other. Li et al (2000) measured oneof the strains (TAC 449) used in this study andpresented the dimensions of the heterocytes as
10.8–15.4 m m in diameter, and of the akinetes as
16.5–31.0 m m in diameter.

Classification of Planktonic Anabaena with Coiled Trichomes

145

Figs. 35–42. Anabaena crassa, 35–36: TAC 490, 37–38: TAC 473, 39: TAC 492, 40–41: TAC 522, 42: TAC 520.
Scale bar100 m m.

146

Masayuki Watanabe, Yuko Niiyama and Akihiro TujiFigs. 43–46. Anabaena ucrainica, 43–44: TAC 449, 45–46: TAC 455.
Figs. 47–48. Anabaena mucosa, TAC 425. Scale bar100 m m.

8.

Anabaena mucosa Kom.-Legn. and Elor.
Figs. 47–48
Cells spherical, 10.0–13.0 m m wide, 6.3–12.5
m m long; l/w ratios 0.53–1.00. Heterocytes
spherical or slightly elongated, 11.3–13.3 m mwide, 13.0–15.0 m m long. Akinetes slightly
longer than wide, remote from heterocytes, 17.8–
22.5 m m wide, 21.3–27.5 m m long; l/w ratios
1.16–1.25.
The strain examined was TAC 425.
Morphological characters except the akinete
form of this species almost resemble those of A.

circinalis, but the length width ratios of akinetes
markedly deviate from each other. This species
was recorded from Lake Hime-numa and Lake
Toro-ko in Hokkaido, Lake Higurashi-ike in Aomori prefecture and Lake Sagami-ko in Kanagawa prefecture (Watanabe 1998).
9. Anabaena circinalis Rabenh. ex Born. andFlah.
Figs. 49–56
Cells spherical, 7.5–13.3 m m wide, 4.5–12.5
m m long; l/w ratios 0.45–1.33. heterocytes spherical, 8.0–13.3 m m wide, 7.5–13.0 m m long.

Classification of Planktonic Anabaena with Coiled Trichomes

Figs. 49–56. Anabaena circinalis, 49–50: TAC 482, 51–52: TAC 497, 53–54: TAC 553, 55–56: TAC 501.
Scale bar100 m m.

147

148

Masayuki Watanabe, Yuko Niiyama and Akihiro Tuji

Akinetes elongated or cylindrial, remote fromheterocytes, 12.5–22.5 m m wide, 21.3–46.0 m m
long; l/w ratios 1.31–2.71. Coils more or lessregular, 45–150 m m wide, about 50 m m apart.
The strains examined were TAC 482, 497, 501
and 553.
Those four strains show comparatively wide
variations in dimensions of vegetative cells, hetercytes and coils but the form and dimensions of
the akinetes are largely overlapped, thus all of thestrains are identified with A. circinalis. Dimensions of vegetative cells among strains belonging
to A. crassa, A. ucrainica and A. circinalis arecontinuously overlapped, but length/width ratiosof akinetes among three species clearly deviate
from each other. They are 1.2–1.3, 1.0 and 1.7–
2.4 respectively.
Key to the species of planktonic Anabaenawith regularly coiled trichomes recorded inJapan. Two species affixed with an asterisk were
not treated in this study.
1. Akinetes spherical . . . . . . . . . . . . . . . . . . . . . 2
2. Akinetes attaching at both side of heterocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
3. Mean value of cell width about 4 m m. . . . . . . . . . . . . . . . . . . . . . A. reniformis
3. Mean value of cell width about . . . . . .
5–6 m m. . . . . . . . . . . . . . . . . A. oumiana
2. Akinetes remote from heterocytes . . . . . . 4
4. Mean value of cell width about 11 m m. . . . . . . . . . . . . . . . . . . . . . A. ucrainica
4. Mean value of cell width about 7 m m .....
. . . . . . . . . . . . . . . . . . . . . A. minispora*
1. Akinetes longer than wide. . . . . . . . . . . . . . . 5
5. Akinetes attaching at both side of heterocytes . . . . . . . . . . . . . . . . A. eucompacta*
5. Akinetes remote from heterocytes . . . . . . 6
6. Akinetes one or two cells remote fromheterocytes . . . . . . . . . . . A. akankoensis
6. Akinetes more than three cells remotefrom hetercytes . . . . . . . . . . . . . . . . . . 7
7. Mean value of cell width about
4–5 m m. . . . . . . . A. pseudocompacta
7. Mean value of cell width about
8–12 m m . . . . . . . . . . . . . . . . . . . . . 8

8. Mean value of l/w ratios of
akinetes 1.7–2.4 . . . . A. circinalis
8. Mean value of l/w ratios of
akinetes 1.2–1.3 . . . . . . . . . . . . . 9
9. Coil width 30–60 m m. . . . . . . .
. . . . . . . . . . . . . . . . . A. crassa
9. Coil width 160–175 m m. . . . . .
. . . . . . . . . . . . . . . . A. mucosa
Acknowledgments
We are indebted to Ms. Suzue Arii, Dr. M. Dai
Naw, Ms. Megumi Nakagawa, Dr. Toshiyuki
Nakaike and Mr. Shun-ichi Sasaki for collecting
plankton samples used in this study and to Dr.
Shigeo Tsujimura for offering his Anabaena
strain isolated from Mishima-ike pond, Siga prefecture.
This work was partly supported by the Ministry of Education, Culture, Sports, Science andTechnology, Grant-in-Aid for Scientific Research(C), 12640690.
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