Botanica Marina Vol. 46, 2003, pp. 2–8 © 2003 by Walter de Gruyter · Berlin · New York
Chamaebotrys erectus sp. nov. (Rhodymeniales, Rhodophyta)
from the Socotra Archipelago, Yemen
T. Schilsa*, J. M. Huismanb and E. Coppejansa
a
Phycology Research Group, Biology Department, Ghent University, Krijgslaan 281 (S8), 9000 Ghent, Belgium
of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia 6150, Australia
b School
* Corresponding author: tom.schils@rug.ac.be
A third species of Chamaebotrys, C. erectus, is described from an upwelling region off Socotra Island, Yemen.
The new species clearly displays one of the defining features of the genus, viz. terminal tetrasporangia in nemathecial sori. The nemathecia become diffuse when mature and produce secondary tetrasporangia.
Tetraspores can apparently germinate in situ, resulting in compound thalli with tetrasporic and cystocarpic
parts. Carpogonial branches are four-celled and cystocarps are protuberant, both of which features illustrate
the affinities of Chamaebotrys with the closely related Coelarthrum.
Introduction
The genus Chamaebotrys was recently erected by
Huisman (1996) for Coelarthrum boergesenii Webervan Bosse, the two features distinguishing it from the
type species of Coelarthrum, C. cliftonii (Harvey)
Kylin, being the terminal, rather than intercalary
tetrasporangia and the nemathecial sori in which
they occur (Huisman 1996). A second species of
Chamaebotrys is C. lomentariae (Tanaka et K. Nozawa in Tanaka) Huisman, which is very imperfectly
known only from the type collection. Both it and the
type species have low-growing, decumbent thalli of
small stature. It was therefore of interest when several relatively large, upright thalli referable to Chamaebotrys were collected from an upwelling area off Socotra (Fig. 1). These specimens are herein described
as the new species C. erectus.
13 January –20 February 1999 and 26 March –7 May
2000, respectively. The subtidal habitats around the
island were sampled while snorkelling or SCUBA
diving. Specimens were pressed on herbarium sheets
and preserved in a 5% Formalin-seawater solution.
Herbarium sheets, liquid-preserved specimens and
microscope slides are deposited in GENT. Material
for microscopical examination was stained with aniline blue. The anatomical and reproductive characteristics were observed by studying transverse sections (made by hand or with a freezing microtome set
at 40 µm) and squashed preparations (whole-mounts
in a mixture of corn syrup and phenol, 50:1) under a
standard light microscope (Leitz Diaplan, Wetzlar,
Germany). Line drawings were prepared with a camera lucida, and photographs were taken with a digital
camera (Olympus DP10, Melville, U.S.A.).
Results
Material and Methods
Specimens were collected during two field trips to
Socotra Island (Yemen; 12.47 N, 53.87 E) from
Chamaebotrys erectus Schils et Huisman, sp. nov.
Diagnosis: Ad Chamaebotrydem boergesenii (Weber-
Fig. 1. Sampling stations around Socotra where Chamaebotrys erectus was collected: IT-059 (a); IT-103, type locality (b);
Alg-40 (c). Scale bar: 20 km.
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Chamaebotrys erectus sp. nov
3
Figs 2–7. Chamaebotrys erectus sp. nov.
Fig. 2. Habit of holotype. Fig. 3. Apical region showing the narrow and short connections between the segments. Fig. 4. Section of cortex. Fig. 5. Cortical section showing gland cells attached to a medullary cell. Fig. 6. Surface view of cortex. Fig. 7.
Compound thallus: cystocarpic axes (C) developing from tetrasporic segments (T). Scale bars: Fig. 2, 1 cm; Fig. 3, 1 mm;
Figs 4–6, 10 µm; Fig. 7, 1 mm.
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T. Schils et al.
van Bosse) Huisman similis sed characteribus sequentibus distinguitur. Planta recta, ad 20 cm alta, sine
anastomosibus inter ramos. Tetrasporangia decussate
divisa, in nematheciis irregulariter formatis portata.
Tetrasporae interdum in situ germinantes, thallum
compositum facientes ex partis tetrasporicis gametophyticis et cystocarpicis constantes. Spermatangia ignota.
Similar to Chamaebotrys boergesenii (Weber-van
Bosse) Huisman but with the following distinguishing characters: plants erect, to 20 cm tall, lacking
anastomoses between branches. Tetrasporangia decussately divided, in irregularly shaped nemathecia.
Tetraspores occasionally germinating in situ, resulting in a compound thallus comprised of tetrasporic,
gametophytic and cystocarpic parts. Spermatangia
unknown.
Holotype: SOC 265 (GENT).
Etymology: The specific epithet (L. erectus = upright)
alludes to the upright habit of the species.
Type locality and specimens examined: Yemen, Socotra Island (Fig. 1): 5 February 1999, 10 km east of
Rhiy di-Qatanhin (IT-059: 12.308 N, 53.658 E), shallow subtidal, leg. F. Leliaert (SOC 028: tetrasporophyte and female gametophyte); 3 March 1999, 1 km
southeast of Ghubbah di-Net (IT-103: 12.425 N,
53.475 E; type locality), shallow subtidal, leg. F. Leliaert (SOC 265: tetrasporophyte and female gametophyte); 30 April 2000, west of Bidholih (ALG-40:
12.303 N, 53.843 E), subtidal: –20 m, leg. T. Schils
(SMM 456: female gametophyte).
Habit and vegetative structure: Plants are upright, to
20 cm tall (Fig. 2), segmented, and branch dichotomously or have a percurrent primary axis and verticillate laterals. Several thalli, each with a short solid
stipe (to 7 mm long and 1.5 mm wide), can arise from
a single discoid holdfast (to 3 mm diameter). Young
branches and apical regions are bright red in colour
and older parts of the thallus are brownish red. Thalli
are soft in texture and composed of hollow, mucusfilled segments that are joined by narrow connections (Fig. 3). The shape of the segments varies from
subcylindrical near the apex to thick, elongate and
barrel-shaped in older thallus parts. The inner medulla is composed of 1 or 2 layers of large, colourless
cells (22.5–125 µm [l] × 27–160 µm [w]; Fig. 4). Gland
cells (6.5–20.5 µm in diameter) are borne singly or in
pairs on the inner surface of medullary cells (Fig. 5)
or on stellate cells attached to the medullary cells.
Secondary internal filaments occasionally are initiated from the medullary cells. The cortex is composed
of 2–3 layers of subspherical pigmented cells
(4.5–18 µm in diameter), these gradually decreasing
in size towards the thallus surface. Outer cortical cells
regularly bear hairs. Cortical cells in surface view are
irregularly arranged (Fig. 6) and variable in diameter.
Reproductive thalli: The larger plants (e.g. SOC 265)
are compound, composed of tetrasporic and gametophytic/cystocarpic individuals (Fig. 7), the latter oc-
Figs 8–9. Chamaebotrys erectus sp. nov.
Fig. 8. Four-celled carpogonial branch. Fig. 9. Initiation of a
cystocarp: auxiliary mother cell (am), auxiliary cell (aux)
and carpogonial branch remnants (arrow). Scale bars:
10 µm.
curring distally on the tetrasporophyte. Hence, it is
suspected that the tetrasporangia germinate in situ
and give rise to gametophytic thalli. The process of
tetraspore germination, singly or syntagmatically,
was not observed. Smaller, to 7 cm tall, entirely cystocarpic thalli also occur, indicating that the tetraspores
can also disperse from the mother plant and produce
free-living gametophytes.
Carpogonial branch and cystocarps: Carpogonial
branches are 4-celled and slightly curved (Fig. 8). A
cortical cell, attached to the supporting cell and with
secondary pit connections with adjacent cortical
cells, acts as the auxiliary mother cell and initiates an
obovoid auxiliary cell (Fig. 9). Immediate post-fertilisation events have not been observed. Upon presumed diploidisation of the auxiliary cell, the latter
produces a stalked gonimoblast (Fig. 10). Basal to the
gonimoblast, nutritive cells are formed from the cells
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Chamaebotrys erectus sp. nov
5
Figs 10–13. Chamaebotrys erectus sp. nov.
Fig. 10. Section of cystocarp: broken-off gonimoblast (gb), pericarp (pc), nutritive tissue (nt). Fig. 11. Protuberant cystocarp
with a prominent ostiole. Fig. 12. Surface view of irregularly contoured tetrasporangial nemathecia. Fig. 13. Section of
tetrasporial nemathecium showing medullary cells (mc), nemathecial filaments (nf) and tetrasporangial initials (ti). Scale
bars: Fig. 10, 50 µm; Fig. 11, 0.5 mm; Fig. 12, 50 µm; Fig. 13, 20 µm.
that surround the supporting cell. Simultaneously,
a protuberant pericarp surrounds the gonimoblast
(Fig. 11).
Spermatangia: Not observed.
Tetrasporangia: Tetrasporangia occur in nemathecial
sori (Fig. 12). During maturation the sori spread into
irregular diffuse patches that can cover the greater
part of the thallus. The nemathecia are composed of
slender filaments (Fig. 13) that arise from outer cortical cells and cut off distal tetrasporangia. Sterile filaments occur among the tetrasporangial filaments. After releasing the first order of tetrasporangia,
secondary nemathecial filaments can be produced
which give rise to secondary tetrasporangia in more
elevated sori. Tetrasporangia develop from darkly
staining elliptical initials 13.5–25 µm [l] × 6.5–14 µm
[w] (Fig. 13). The first division is transverse and
oblique, with subsequent divisions splitting the two
halves longitudinally at right angles to one another,
resulting in decussately divided tetrasporangia
27–41 µm × 20–25 µm.
Habitat: Plants are epilithic on bare or sand inundated
rocks.The associated subtidal macroalgal flora is com-
posed of Asteromenia peltata (W. R. Taylor) Huisman
et Millar, Botryocladia leptopoda (J. Agardh) Kylin,
Carpopeltis maillardii (Montagne et Millardet) Chiang, Champia indica Børgesen, Chondria armata
(Kützing) Okamura, Dictyota cervicornis Kützing,
Euptilota fergusonii Cotton, Hypnea boergesenii
Tanaka, Lobophora variegata (Lamouroux) Womersley ex Oliveira, Sarcodia montagneana (J. Hooker et
Harvey) J. Agardh, Scinaia moniliformis J. Agardh,
Sebdenia flabellata (J. Agardh) Parkinson, and Udotea
indica A. Gepp et E. Gepp.
Discussion
Chamaebotrys erectus clearly displays the key characteristic of the genus, viz. terminal tetrasporangia in
nemathecial sori. The new species has morphological
and anatomical features similar to the other Chamaebotrys species and also to species of the closely related Coelarthrum (Table I). It can readily be distinguished from Chamaebotrys boergesenii and C.
lomentariae by its erect thallus, large size and compound thalli comprising tetrasporic, gametophytic
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Chamaebotrys erectus
Schils et Huisman,
sp. nov.
Chamaebotrys boergesenii
(Weber-van Bosse)
Huisman
Coelarthrum cliftonii
(Harvey) Kylin
Coelarthrum decumbens
Huisman
Coelarthrum opuntia
(Endlicher) Børgesen
Grouping of
tetrasporangia
Discrete nemathecial sori that
diffuse while maturing and
develop secondary tetrasporangia
Discrete nemathecial sori
that remain discrete
Scattered, not in sori
Indistinct sori
Scattered, not in sori
Carpogonial branch
4-celled
?
4-celled
4-celled
4-celled
Tetrasporangia
Terminal, decussately
divided
Terminal, cruciately
divided
Intercalary, cruciately
divided
Intercalary, cruciately
divided
Intercalary, cruciately
to decussately divided
Habit
Erect
Decumbent
Erect
Decumbent
Erect
Secondary lateral
anastomoses
Absent
Present
Present
Present
Absent
Constrictions
between the segments
Narrow
Broad
Broad
Broad
Stalk-like
Cystocarps
Protuberant
Protuberant
Immersed
Protuberant
Protuberant
Additional
peculiarities
In situ germination of
tetraspores: female
gametophytes epiphytic on
tetrasporophytes, also free-living
female gametophytes
Elongate processes at apical
regions of the thallus
Monostromatic septa
Outer cortex in a
rosette-like formation in
surface view
Cartilaginous stipe
Size (cm)
To 20
2–3
To 20
3–4
To 30
Distribution
Upwelling area of Socotra
Island, Yemen
Warmer waters of the IndoPacific and upwelling area of
Hallaniyat Islands, Oman
Indo-Pacific
Great Barrier Reef and
Lord Howe Island,
Australia
Indo-Pacific
T. Schils et al.
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Feature
6
Table I. Comparison of Chamaebotrys erectus to other Chamaebotrys and Coelarthrum species (Mshigeni and Papenfuss 1981, Huisman 1996, 2000, Wynne 2001, this paper).
Chamaebotrys lomentariae is excluded as the species is insufficiently known (Huisman 1996).
Chamaebotrys erectus sp. nov
and cystocarpic parts (non-compound thalli also occur). In addition, C. erectus produces occasional internal filaments, these being secondarily produced
and not comparable to longitudinal filaments of the
Champiaceae (Ricker and Kraft 1979, Huisman
1995) and Lomentariaceae (Lee 1978). Adventitious
filaments have also been observed in Coelarthrum
species and not accorded taxonomic significance
(Huisman 1996). The latter feature, however, might
prove to be of taxonomic importance in other
Rhodymeniaceae genera, viz. the absence of internal
rhizoids in Chrysymenia and their presence in
Cryptarachne (generally lumped in Chrysymenia, e.g.
Abbott and Littler 1969) might support the molecular separation of both genera (Saunders et al. 1999, p.
38).
In light of the recent molecular findings on the
Rhodymeniales (Saunders et al. 1999), the observation of a 4-celled carpogonial branch in Chamaebotrys erectus supports maintaining the genus (which
was not sequenced by Saunders et al. 1999) within
the Rhodymeniaceae. The genus is unusual in the
Rhodymeniaceae, however, in producing terminal
tetrasporangia in nemathecia. This has been hypothesised as a reversion to the ancestral condition by
Saunders et al. (1999). Further molecular studies may
elucidate the phylogenetic placement of Chamaebotrys in relation to other Rhodymeniaceae.
Some tetrasporangia in C. erectus appear to be
tetrahedrally divided, a result of the oblique first division in combination with the decussate arrangement of the tetraspores. Nevertheless, the divisions
are always successive, a distinctive feature of cruciately (decussately) divided tetrasporangia (Guiry
1978, 1990).
In comparison to the reported sizes of the other
Chamaebotrys species (Mshigeni and Papenfuss
7
1981, Huisman 1996), C. erectus is markedly larger.
All material was collected from the south coast of Socotra, which is subject to upwelling of cold water.
This phenomenon is beneficial for algal growth (constant nutrient flow and stable temperature regime),
as the south coast harbours the most luxuriant and
species-rich algal flora of the Island (Schils et al.
2001). Analogous discoveries of large representatives
of certain genera from this upwelling region include
Champia gigantea Wynne (1998), another member of
the Rhodymeniales. These findings suggest that the
Arabian Sea harbours a distinctive and interesting
marine flora.
Acknowledgements
We appreciated constructive comments from Gerry
Kraft and an anonymous reviewer. Sincere thanks
are expressed to the Senckenberg Research Institute,
Germany (Michael Apel, Uwe Zajonz and Fareed
Krupp), for the excellent field trip preparations to
the Socotra Archipelago. Frederik Leliaert is gratefully acknowledged for making his exquisite collection of Socotran algae available. Tom Schils is indebted to the Fund for Scientific Research Flanders
(Belgium) for a research assistant grant and a travel
grant to Murdoch University (Western Australia).
John Huisman thanks Associate Professor Michael
Borowitzka (Murdoch University) for hosting his research and Alex George (Four Gables, Barclay St.,
Kardinya) for kindly supplying the Latin translations. Financial support was provided by grants from
the ‘Australian Biological Resources Study’ and the
‘Western Australian Department of Commerce and
Trade’.
Accepted 10 October 2002.
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