Bull. Natl. Mus. Nat. Sci., Ser. B, 41(4), pp. 147–153, November 20, 2015

First Record of Callithamniella tingitana (Schousboe ex Bornet)
Feldmann-Mazoyer (Ceramiaceae, Rhodophyta) from Japan
Taiju Kitayama
Department of Botany, National Museum of Nature and Science,
Amakubo 4–1–1, Tsukuba, Ibaraki 305–0005, Japan
E-mail: kitayama@kahaku.go.jp(Received 24 August 2015; accepted 24 September 2015)

Abstract A marine red alga, Callithamniella tingitana (Schousboe ex Bornet) FeldmannMazoyer (Ceramiaceae, Ceramiales, Rhodophyta) was collected from the coast of Chichi-jimaIsland, Ogasawara Islands, Japan. This species is the type species of the genus Callithamniella anddiffers from all other members of the genus in having determinate axes, laterals branched dichotomously from the third proximal cells on indeterminate axes and ellipsoidal tetrasporangia borne on
unicelled pedicels on indeterminate axes. This is the ﬁrst record of the genera and species fromJapan and also the ﬁrst report on this species from the Paciﬁc Ocean.
Key words : Callithamniella tingitana, Ceramiaceae, Japan, Ogasawara Islands, red alga.

The red algal genus Callithamniella (Ceramiaceae, Ceramiales, Rhodophyta) was establishedby Feldmann-Mazoyer (1938) on the basis of“Callithamnion tingitana” Schousboe ex Bornet(Bornet, 1892) as a new genus having minutedorsiventral thalli, which are composed of simple
erect determinate axes and Callithamnion-likeerect indeterminate axes arising from prostrateindeterminate axes. In this genus, there are ﬁvecurrent species in the world (Guiry and Guiry,2015): C. tingitana (Schousboe ex Bornet) Feldmann-Mazoyer (Feldmann-Mazoyer, 1938) (typespecies), C. capensis Simons (Simons, 1970), C.
ﬂexilis Baardseth (Baardseth, 1941), C. paciﬁca
Abbott et R.E. Norris (Abbott and Norris, 1993),
C. silvae Searles in Searles et Schneider (Searlesand Schneider, 1989). Most species of them, C.
tingitana, C. capensis, C. ﬂexilis and C. silvae,
were recorded from the Atlantic Ocean and theneighboring waters, while in Paciﬁc Ocean only
one species, C. paciﬁca, was found by Abbottand Norris (1993), who described this as anendemic species to Hawaii. Although Kim andLee (1991) described a new species, “C. koreana

H.-S.Kim et I.K.Lee” based on the alga from
Korea, it was synonymized into C. paciﬁca laterby Kim and Lee (2012) because of their similarity in morphology. Thus the distribution of Callithamniella had been regarded as separating into
the four atlantic species and one paciﬁc species
so far. However, information about the paciﬁcspecies is few because of its difﬁculty of collecting and identiﬁcation and is insufﬁcient for discussing about the distribution of this genus.
Ogasawara Islands (＝Bonin Islands) are oceanic islands located ca. 1,000 km south of TokyoMetr., Japan. In the investigations of algal ﬂora
around the Islands, several rare algae were foundfrom the deep sublittoral zone using dredge: forexample, Aneurianna ogasawaraensis Kitayama(Kitayama, 2014), Zosterocarpus ogasawaraensis Kitayama (Kitayama, 2013). There is apossibility that the Ogasawara Islands has aunique algal ﬂora different from any area of theJapanese Archipelago. Recently, in addition, asmall alga referable to Callithamniella was collected from Chichi-jima island, main island ofOgasawara Islands. In this study, to conﬁrm the148

Taiju Kitayama

identity of this present alga from the Island andreconsideration on the distribution of Callithamniella in the Paciﬁc Ocean, the author made anatomical observations on the material using amicroscope.
Materials and Methods
The red algal material referable to the genus
Callithamniella was collected from the subtidal
zone (1–2 m in depth) of the coast of Futami Bay,
Chichi-jima Island in the Ogasawara Islands(＝Bonin Islands), Japan by snorkeling on 13
July 2013. For preservation, the material wasﬁxed in 10% formalin-seawater. Specimens weremounted in glycerine jelly after staining by 1%
aniline blue solution. Anatomical observations
were made on the material using a microscope.
Voucher specimens were deposited in the algal
herbarium of the National Museum of Natureand Science (TNS).
Results
Order Ceramiales Oltmanns, 1904
Family Ceramiaceae Dumortier, 1822
Tribe Dohrnielleae Feldmann-Mazoyer, 1941
Callithamniella tingitana (Schousboe ex Bornet) Feldmann-Mazoyer
Comptes Rendus Hebdomadaires des Séancesde lʼAcadémie des Science, Paris 207: 1119 (1938)[Figs. 1–11]
Basionym: Callithamnion tingitana Schousboe
ex Bornet, 1892: 329 [Type locality: Tangier,Morocco (Schneider and Searles, 1997). Holotype: PC (Schneider, 1984: 458)]
Synonym: Callithamnion aegagrophila Funk,
1922: 236, table V, f. 15, 16.
Callithamniella capensis sensu Stegenga, 1988:
376.
Grallatoria tingitana (Schousboe ex Bornet)
Abbott, 1976: 148.
Habitat: Grew on other benthic marine algae(e.g., Champia, Dictyota, Padina) in the subtidal
zone (1–2 m in depth).

Vegetative morphology: Plants are epiphytic,
minute, up to 2 mm in height, ﬁlamentous andbright red in color. The thalli are dorsiventral,organized with prostrate axes and erect indeterminate and determinate axes arising irregularly
from the prostrate axes (Fig. 1). All axes are uniseriate and ecorticate (Figs. 2–4). Prostrate axes
are cylindrical, 30–55 μm in diameter. Each cellof the prostrate axes is straight, 60–320 μm in
length, producing an erect axes and a ventral rhizoid or a hapteron from a basal cell. Rhizoids arecolorless, uniseriate, unicellular or multicellular,elongate, up to 400 μm in length, 16–24 μm in
diameter (Fig. 3, arrow). Haptera are colorless,unicellular, discoidal to digitate (Figs. 1, 4,arrowheads, 11 h). Erect determinate axes areshort, 11–13 celled, branched dichotomously
once or twice from the 3rd proximal cells, curved
slightly toward axes. Erect inderminate axes areelongate, issuing alternately determinate laterals
in spiral and few indeterminate laterals, terminated an apical cell (Fig. 5). Cells of the erect
indeterminate axes are cylindrical, 45–84 μm in
length, 18–40 μm in diameter in the lower portion, tapering to the top, 6–15 μm in length,
4–10 μm in diameter in the terminal portion.
Determinate laterals are similar to erect determinate axes, 10–13 celled, curved slightly towardaxes, branched dichotomous, once or twice fromthe 3rd proximal cells (Fig. 6).
Reproductive morphology: Tetrasporangia areformed on one celled pedicels on erect indeterminate axes, adjacent to the basal cells of determinate laterals (Figs. 2, 6). Immature tetrasporangia
are long ovate (Figs. 7, 8). Mature tetrasporangia
are ovate or ellipsoidal, 30–54 μm in diameter,
48–72 μm in length, devided cruciately (Figs. 6, 9,10). Sexual organs were not observed.
Specimens examined: “Koyo-walls” in front of
the Ogasawara Fisheries Center, Futami Bay,Chichi-jima Island, Ogasawara Islands, Japan(27°5′50″N, 142°11′56″E); 13 July 2013; leg. T.
Kitayama (TNS-AL 198288–198290).
Japanese name: Hai-kinu-ito (nom. nov.).
Distribution: Atlantic Ocean and Mediterranean Sea: Europe, Africa, Atlantic Islands, North

Callithamniella tingitana New to Japan149Figs. 1–4. Callithamniella tingitana from Chichi-jima Island, Ogasawara Islands, Japan. 1. Habit showing a dorsiventral thallus composing of an erect determinate axis (d) and indeterminate axis (i) arising from the prostrate axis with a holdfast (arrowhead). 2. Erect indeterminate axis with mature tetrasporangia. 3. Erect indeterminate axis showing a rhizoid (arrow) from the basal cell of determinate lateral. 4. Prostrate indeterminate
axis with erect determinate axes (d) and a holdfast (arrowhead) on the surface of Champia.

America, Western Atlantic, South America(Guiry and Guiry, 2015); Paciﬁc Ocean: Japan(Ogasawara Islands, the present study).
The four speciﬁc characters that distinguished
C. tingitana from other members of the genus areshown in Table 1. The material from the Ogasawara Isls. agrees well with C. tingitana, except
the range of branching position in erect determinate laterals: Schneider and Searles (1991, p. 735)
stated that C. tingitana has the branching occurringfrom the 3rd–5th proximal cells of the laterals.
Discussion
The red alga collected from the Ogasawara
Islands possesses completely generic characteristics of Callithamniella Feldmann-Mazoyer: thedorsiventral thalli composed of erect indeterminate and determinate axes arising from prostrateaxes; determinate laterals issued alternately or
spirally from the erect indeterminate axes; tetrasporangia borne on pedicels adjacent to thedeterminate laterals. In Japan, this is the ﬁrst
record for this genus, which may have been mistaken for juvenile plants of Callithamnion before.
Furthermore, it is not easy to carry out species
identiﬁcation within the genus because there arefew considerable differences among the ﬁve current species in the world. Comparisons of a few
characteristics of determinate axes and laterals
and tetrasporangia among them (Table 1)
resulted barely in the key to the species of thegenus (see below), in which the present algafrom Ogasawara Islands can be treated as Cal-150
Table 1.

Taiju Kitayama
Comparisons of the four characteristics among the species of the Callithamniella
Branching positionof determinate erectaxes and laterals

C. capensis(Simons, 1970)
C. ﬂexilis(Secilla, 2012)
C. paciﬁca(Abbott and Norris, 1993)
C. paciﬁca(Kim and Lee, 2012)
C. silvae(Searles and Schneider,1989)
C. tingitana(Schneider, 1984; Searles
and Schneider, 1989)
C. tingitana(the present study)

Unbranched*

Tetrasporangia
Position

Pedicels

Shape and lenght

1–2 cells

From the 3rd
proximal cells**
From the 3rd
proximal cells***“In upper portion”(from the 6–7th
proximal cells****)
From the 3rd–5th
proximal cells

On the indeterminate
erect axes
On the indeterminate
erect axes
On the indeterminate
erect axes
On the indeterminate
erect axes
On the proximal cellsof determinate
laterals
On the indeterminate
erect axes

A single cell

Ellipsoidal,38–55 μm

From the 3rd
proximal cells

On the indeterminate
erect axes

A single cell

Ellipsoidal, ovate,
48–72 μm

Unbranched

Ellipsoidal,
up to 75 μm*
1–2 (3) cells
Ellipsoidal,
27–43 μm
1–3 cellsLong ovate,
up to 90 μm
1–2 (3) cells*** Ellipsoidal,
60–65 μm
1 (2) cells
Ellipsoidal,
27–45 μm

* Judging from ﬁg. 6 in Simons (1970). ** Judging from ﬁg. 17 in Abbott and Norris (1993). *** Judging from ﬁg. 47
in Kim and Lee (2012). **** Judging from ﬁgs. 5 and 6 in Searles and Schneider (1989).

lithamniella tingitana (Schousboe ex Bornet)
Feldmann-Mazoyer. In particular, the present algafrom Ogasawara Islands is similar strikingly inmorphology to the Feldmann-Mazoyer (1940)ʼsalga and Schneider (1984)ʼs alga of C. tingitana
from North Carolina, U.S.A.; on the other hand, it
differs from the Schneider and Searles (1997)ʼsalga of C. tingitana from Bermuda in having
many unbranched determinate laterals.
The alga from the Ogasawara Islands alsodoesnʼt agree with C. paciﬁca, which is known as
the only species distributed to the Paciﬁc Ocean(Abbott and Norris, 1993) in morphology ofreproductive organs. Abbott and Norris (1993, p.
459) noted “C. paciﬁca sp. nov. is widely separated geographically (from the Atrantic species),
but this should not be the basis for describing
new species”. As a strong characteristic for the
new species, they featured “very large tetrasporangia, up to 90 μm long” (Abbott and Norris,1993) and “to 22 by 90 μm including wall layers”(Abbott, 1999), which are surely different fromany species of the genus including the present
alga from Ogasawara Islands. Additionally, tetrasporangia of C. paciﬁca have “1–3 cells long”
pedicles (Abbott and Norris, 1993), while ones inmost of other species have unicelled or 1–2

celled pedicels except C. ﬂexilis (Secilla, 2012).
Kim and Lee (2012) also observed Korean algaof C. paciﬁca, which was identical to “C. koreana” described informally by Kim and Lee(1991), and observed 1–2 (3) celled pedicels(they illustrated three celled pedicel in ﬁg. 47B).
According to their description, however, teterasporangia of the Korean alga are not so longovate and under 65 μm in length. It is probablethat this size exclude wall layers, for most of theones showed in their illustration (ﬁg. 47A–E) are
mesurable as 50–120 (150) μm in lengh.
Although reality of the species endemic to thePaciﬁc Ocean is an unresolved problem becauseof morphological variation in the Atlantic species, the alga from Ogasawara Islands is identiﬁed with C. tingitana at the present time. As aresult, it is considered that the two species ofCallithamniella, C. paciﬁca (Hawaii and Korea)
and C. tingitana (Japan), are distributed to thePaciﬁc Ocean. To clarify the relationship among
the Callithamniella tingitana and other species of
the genus Callithamniella, and to redeﬁne its
generic circumscription, obervations of sexual
reproductive organs and molecular analyses on
the new materials from Ogasawara Islands arerequired.

Callithamniella tingitana New to Japan151

Figs. 5–11. Callithamniella tingitana from Chichi-jima Island, Ogasawara Islands, Japan. 5. Apex of erect indeterminate axis with apical cell (a), issuing alternately determinate laterals. 6. Erect indeterminate axis withdeterminate laterals and tetrasporangia. 7–10. Various stages of tetrasporangia on unicellular pedicels (p). 7–8.
Immature terasporangia. 9. Side view of mature tetrasporangium. 10. Front view of mature tetrasporangium.
11. Prostrate indeterminate axis bearing an erect indeterminate axes (i), three erect determinate axes (d) andthree holdfasts with haptera (h).

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Taiju Kitayama

Key to the species of Callithamniella
1a. Determinate axes and laterals unbranched ........................................................................................2
1b. Determinate axes and laterals often branched dichotomous .............................................................32a. Tetrasporangia 27–43 μm in length ..................................................................................... C. ﬂexilis
2a. Tetrasporangia up to 75 μm in length ............................................................................... C. capensis
3a. Branching of determinate axes occurring from the 6–7th proximal cells; tetrasporangia on theproximal cells of determinate laterals ...................................................................................C. silvae
3b. Branching of determinate axes occurring from the 3rd–5th proximal cells; tetrasporangia on theindeterminate axes ............................................................................................................................44a. Tetrasporangia long ovate, 22–90 μm in length, borne on 1–3 celled pedicels ................. C. paciﬁca
4b. Tetrasporangia ovate or ellipsoidal, 38–72 μm in length, borne on 1 celled pedicels ..... C. tingitana
Acknowledgments
I am grateful to Mr. Yuji Aoki and Mr. Yuhei
Tanaka, the Ogasawara Fisheries Center, Tokyo
Metropolitan for providing me the facilities toprocessing the specimens. I thank Drs. ToshihikoFujita, Hiroshi Namikawa, Kazunori Hasegawa,Hironori Komatsu, Department of Zoology,
National Museum of Nature and Science for theirkind help in the ﬁeld study in the island. This
study was supported by Grants-in-Aid for Scientiﬁc Research (no. 25440225) from the Ministryof Education, Culture, Sports, Science and Technology, Japan.
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