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Botanica Marina 54 (2011): 135–145 2011 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2011.015
2010/014
Article in press - uncorrected proof
Morphology and taxonomy of Anadyomene species
(Cladophorales, Chlorophyta) from Bahia, Brazil
Aigara M. Alves
1,
*, Lı´sia M. De Souza Gestinari
2
and Carlos W. Do Nascimento Moura
1
1
Universidade Estadual de Feira de Santana, DCBIO,
PPGBOT, LAFICO, Av. Transnordestina s/n, Novo
Horizonte, CEP 44036-900, Feira de Santana, Bahia,
Brazil, e-mail: aigarama@yahoo.com.br
2
Nu´cleo em Ecologia e Desenvolvimento So´cio-Ambiental
de Macae´/UFRJ, CEP 27910-970, Macae´, Rio de Janeiro,
RJ, Brazil
* Corresponding author
Abstract
We made a taxonomic study of representatives of Anadyo-
mene occurring off the coast of Bahia State, Brazil. Six spe-
cies were identified: A. lacerata, A. linkiana, A. pavonina,
A. rhizoidifera, A. saldanhae and A. stellata. This is the first
report of A. rhizoidifera since the original description of the
species. Non-birefringent proteinaceous crystalline inclu-
sions in the form of tetrahedrons were recorded for the first
time in the genus. Fertile thalli of A. saldanhae and A. stel-
lata were also encountered for the first time along the Bra-
zilian coast. A. stellata has the widest distribution along the
coast of Bahia State; it was found from the intertidal region
to depths of 100 m. A. rhizoidifera occurred in only a single,
intertidal collection. A. lacerata, A. linkiana, A. pavonina
and A. saldanhae occurred only in the near-shore zone at a
minimum depth of 20 m. Detailed descriptions, illustrations
and comparisons with related taxa are provided.
Keywords: Anadyomene; Cladophorales; crystalline
inclusions; Siphonocladales; taxonomy.
Introduction
The seaweed genus Anadyomene (Ulvophyceae, Chlorophy-
ta) was established by Lamouroux (1812) based on A. fla-
bellata J.V. Lamour. wsA. stellata (Wulfen in Jacq.) C.
Agardhx. This genus is characterized by attached, mono- or
polystromatic blade-like thalli composed of large, elongated,
polychotomously branching cells (veins) and interstitial
spaces that are completely or partially filled by smaller inter-
stitial cells (Littler and Littler 1991).
Anadyomene can be distinguished from the genus Micro-
dictyon Decne. (the other genus in the family Anadyome-
naceae) by its entire blade; the blade of Microdictyon has a
reticulate structure and its terminal filaments are generally
free. Lateral filaments of Microdictyon, principally at the
extremities, are anastomosed and irregular (Littler and Littler
1991). Two species of Anadyomene have perforated blades
that are clearly different from the reticulate blades found in
Microdictyon.
According to Leliaert et al. (2007a), the type of thallus
seen in Anadyomene (i.e., with a network completely filled
with small interstitial cells) may be derived from a reticular
thallus. Also, the lateral union of the branches appears to
have evolved as a special form of the tenacular cells found
in Microdictyon. Cell unions in Microdictyon only occur at
the extremities of the apical cells, while the cells grow next
to one another in Anadyomene, resulting in a lateral union.
Similarities between the ways in which cells of the two gen-
era unite is evident in the immature thallus of Anadyomene,
which has an open reticulate structure with anastomoses
occurring at the cell apices, as seen in Microdictyon (Littler
and Littler 1991, Leliaert et al. 2003).
The genus Anadyomene is exclusively marine and found
in tropical and temperate regions of the Atlantic, Indian and
Pacific Oceans, as well as in the Mediterranean and Adriatic
Seas. Though typically a shallow-water reef flat alga, it has
been collected from depths greater than 90 m and is believed
to be an important part of very deep water communities.
Twelve species are currently recognized within the genus
(Guiry and Guiry 2010), with eight occurring in the western
Atlantic (Wynne 2005) and six along the coast of Brazil
(Horta 2000, Yoneshigue-Valentin et al. 2006).
The large majority of references to Anadyomene species
in Brazil are in check-lists of local and regional floras, or in
species lists from ecological investigations. Joly and Oliveira
Filho (1969) and Joly and Pereira (1973) were the only
authors to have published papers dealing exclusively with
the genus Anadyomene in Brazil; these works provided
descriptions of new species.
The present study aimed to investigate the diversity of
Anadyomene along the coast of Bahia State and to provide
detailed descriptions of the morphology, reproduction and
cellular inclusions of the different species. This study con-
tributes to our knowledge of the chlorophyte flora of Bahia
State and of Brazil in general.
Materials and methods
Bahia State, Brazil (088209070 to 188209070S and 308209370
to 468369590W), which has the longest state coastline in the
country (1103 km), contains a large variety of habitats
including sandy beaches, coral reefs, sandstone formations,
136 A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil
Article in press - uncorrected proof
rocky coastal formations, and mangrove swamps (Nunes and
Guimara˜es 2008).
The specimens examined were collected along the Bahia
State coast between 2005 and 2008; others were collected in
1994 and 1995. These collections are deposited in the Her-
barium of the Universidade Estadual de Feira de Santana
(HUEFS). In addition, specimens from various Brazilian her-
baria (ALCB, SP, SPF, RB and RFA) were examined. The
herbarium abbreviations used in this study follow Holmgren
and Holmgren (1998).
Morphological and anatomical characteristics of the spec-
imens were examined using stereo and compound micro-
scopes equipped with ocular micrometers and digital cameras
(Sony model Cyber-shot DSC-W7, Tokyo, Japan). The
dimensions (diameters and lengths) of all of the structures
were established from 10 to 20 measurements from each
specimen.
The chemical nature of the crystalline inclusions was
determined by testing solubilities in 1
N
hydrochloric acid,
5% sodium hypochlorite, 67% aqueous acetic acid (Yasue
1969, Leliaert and Coppejans 2004, Alves et al. 2009, 2010)
and 40% hydrofluoric acid, using protocols from Faegri and
Iversen (1975). The presence or absence of birefringence was
evaluated using phase contrast interference (Nomarski)
microscopy.
Results
Six Anadyomene species that occur along the coast of Bahia
can be identified with the following key:
1. Thallus perforate
2. Thallus with distinct stipe; interstitial cells randomly
arranged, oval in transverse section ........... A. linkiana
29. Thallus without a stipe; interstitial cells regularly
arranged and perpendicular to the veins, H-shaped in
transverse section ...................................... A. pavonina
19. Thallus eperforate
3. Rhizoids originating in the basal portion of the blade
and in any part of the thallus
4. Interstitial cells in pinnate arrangement, appearing
as lateral or transverse bars tightly parallel to one
another ............................................... A. rhizoidifera
49. Interstitial cells polychotomously branched, ran-
domly arranged ................................... A. saldanhae
39. Rhizoids originating only in the basal region of the
blade
5. Margin smooth or lobed, formed by multiple layers
of rounded or oval interstitial cells ........... A. stellata
59. Margin lacerated, formed by a single layer of vein
cells ....................................................... A. lacerata
Anadyomene lacerata D.S. Littler et Littler (Littler
and Littler 1991, p. 105, figs 6–14) (Figures 1– 11)
Description
Blade light green, erect, up to 4 cm. Stipe
formed by the union of basal rhizoidal cells; attached to the
substratum by numerous rhizoids that extend from the fila-
ments of the stipe. Blade monostromatic, eperforate, heart-
shaped, with margin undulated, lacerated or dentate, formed
by vein cells. Blades composed of 1–3 elongated, clavate
cells, 200-(1740)-2820
mm long=160-(230)-320 mm in dia-
meter, forming veins that branch polychotomously, with 3–7
cells at the apex, with blunt connections end-to-end, occa-
sionally forked. Interstitial cells small, regularly arranged,
perpendicular to main vein, 67.5-(165)-440
mm long=52.5-
(77.5)-110
mm in diameter, generally in the form of a dumb-
bell or ‘‘H’’ arrangement in lateral view or in transverse
section. Cortical rhizoids arising from the base of the basal
vein cells. Proteinaceous crystalline cell inclusions tetrahe-
dral, non-birefringent, present in the protoplasm between the
chloroplasts. No fertile material was observed.
Specimens examined Brazil, Bahia State (138389550S,
388459400W), Estaca˜o-2C, 50 m depth on 14 October, 1997,
¸
leg. REVIZEE (RFA 29077); (148569480S, 388509570W),
Estaca˜o-4C, 45 m depth on 21 October, 1997, leg. REVIZEE
¸
(RFA 29078); (168479140S, 388419330W), Estaca˜o-13C, 40 m
¸
depth on 26 October, 1997, REVIZEE (RFA 29076);
(188359370S, 378549450W), 65 m depth on 29 June, 2001,
REVIZEE (RFA 30981), pro parte.
Type locality Puerto Rico, on the west side of Isla Moni-
to, northwest of Isla de Mona (18809.509N, 67859.969W).
Remarks Anadyomene lacerata is morphologically dis-
tinct from congeners because it has a lacerated or dentate
margin formed by a single cell layer. According to Littler
and Littler (1991), the species is present as isolated individ-
uals, generally restricted to depths of 15–60 m on flat, sandy
sea floors.
Littler and Littler (1991) reported that Anadyomene lace-
rata differs from other Indo-Pacific eperforate and from oth-
er Atlantic species by the presences of leaves with lacerate
margins composed of elongated vein cells.
The material analyzed, which was dredged from depths of
40–65 m, matches the descriptions and illustrations of spec-
imens from Puerto Rico and Brazil published by Littler and
Littler (1991).
The distribution of Anadyomene lacerata along the coast
of Brazil is restricted to the states of Pernambuco, Bahia,
Espı´rito Santo and to the Martin Vaz archipelago (Littler and
Littler 1991, Bravin et al. 1999, Yoneshigue-Valentin et al.
2006).
Anadyomene linkiana D.S. Littler et Littler (Littler
and Littler 1991, p. 106, figs 15–21) (Figures 12– 19)
Description
Blades light green, erect, with stipe, up to
5 cm tall. Stipe short, but distinct; fixed to the substratum
by extensions of stipe filaments that develop in rhizoids.
Blade monostromatic with large numbers of perforations of
various shapes and sizes, from 280 to 1140
mm in diameter,
which are delineated by a membrane and by vein cells, while
the margin is entire. Margins of young thalli are formed by
A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil 137
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Figures 1–11 Anadyomene lacerata.
(1) General habit. (2, 3) Branching pattern of blade. (4) Margin lacerated. (5) Elongated vein cells forming a lacerated margin. (6–9) Detail
of elongated vein cells and small interstitial cells (perpendicular to vein cells). (10) Cross section of blade showing H-shaped interstitial
cells. (11) Tetrahedral proteinaceous crystals (arrow).
interstitial cells and margins of developed thalli are formed
by vein cells. Blade formed anatomically by longitudinally
elongate cells, uniseriate, cylindrical to oval, 500-(964)-2000
mm long=110-(175)-230 mm in diameter, constituting poly-
tomically ramified veins, with 2–5 cells at the apex, united
by slight depressions. Interstitial cells small, polychoto-
mously branched, elliptical or irregularly shaped, arranged
randomly, attached by forked prongs wedged between adja-
cent cells, 150-(205)-270
mm long=50-(79)-97 mm in diam-
eter, oval in transverse section. Crystalline proteinaceous
inclusions non-birefringent, tetrahedral, visible in the proto-
plasm between the chloroplasts. No fertile material was
observed.
Specimens examined Brazil, Bahia State (158489010S,
378469220W), 58 m depth on 11 November, 1997, leg. REVI-
ZEE (RFA 29083); (158499400S, 388369260W) on 21 June,
2002, leg. REVIZEE (RFA 31005); (168199550S,
388149390W), 58 m depth on 26 October, 1997, Estaca˜o 7-
¸
C, leg. REVIZEE (RFA 29082); (188049210S, 378199390W),
82 m depth, on 23 October, 1997, leg. REVIZEE (RFA
28113), (188229560S, 378359190W), 103 m depth on 12 June,
2002, leg. REVIZEE (RFA 31006).
Type locality Bahamas, San Salvador Island, Fernandez
Bay (2481.69N, 74832.59W).
Remarks Anadyomene linkiana is morphologically simi-
lar to Anadyomene pavonina (C. Agardh) Wille in having a
perforated blade; it differs from A. pavonina by its smaller
stipe, more numerous perforations, interstitial cells arranged
polytomically and randomly dispersed.
The arrangement of the interstitial cells in Anadyomene
linkiana is similar to those in the thallus of A. saldanhae
(which has randomly dispersed cells, with non-overlapping
interstitial cells); however, unlike A. linkiana, A. saldanhae
has an eperforate blade, an indistinct stipe, vein cells that do
not decrease in size distally and rhizoids that are dispersed
over the entire thallus.
The specimens we analyzed and identified as Anadyomene
linkiana clearly match the material originally described by
Littler and Littler (1991) from specimens collected at 61 m
on San Salvador, Bahamas and the material described for
Brazil by Bravin et al. (1999), which was collected at 110 m
depth along the northern coast of Rio de Janeiro State.
Anadyomene linkiana has thus far been reported only
along the Brazilian coast in the states of Bahia, Espı´rito San-
138 A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil
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Figures 12–19 Anadyomene linkiana.
(12) General habit. (13) Detail of perforate blade. (14, 16) Branching pattern of blade. (15) Outer margin formed from small interstitial
cells (arrow). (17) Cross section of blade. (18) Detail of perforations delineated by membrane and vein cells (arrow). (19) Tetrahedral
proteinaceous crystals (arrows).
to and Rio de Janeiro (Bravin et al. 1999, Yoneshigue-Valen-
tin et al. 2006).
Anadyomene pavonina (C. Agardh) Wille (Wille 1910,
p. 114) (Figures 20–30)
Description
Blades dark green, prostrate, up to 5 cm in
diameter by width; fixed to the substratum by rhizoids that
originate on the ventral face of the blade, distributed over
all of the thallus. Blade flattened, monostromatic, perforate,
with perforations irregularly shaped and of diverse sizes,
310–2600
mm in diameter by width, delineated by vein cells.
Anatomically formed by longitudinally elongate cells, uni-
seriate, cylindrical, 450-(1390)-3900
mm long=70-(113)-
150
mm in diameter, forming veins with polytomic
ramifications, giving rise to 2–8 cells at the apex, with fur-
cate connections at the base, arranged irregularly within the
blade. Interstitial spaces filled with elongated cells 72.5-
(129)-210
mm long=52.5-(58)-65 mm in diameter, in a pin-
nate arrangement, aligned perpendicularly to the vein cells,
partially overlapping or overlapping at the extremities of
adjacent cells, occasionally united by small lobes but fre-
quently smooth in the shape of an ‘‘H’’ or a dumb-bell in
the lateral view or in the transverse section. External margin
of the thallus is delimited by a layer of vein cells. Crystalline
proteinaceous inclusions non-birefringent, tetrahedral in
shape, visible in the protoplasm between the chloroplasts. No
fertile material was observed.
Specimens examined Brazil, Bahia State (158499400S,
388269200W), 83 m depth on 21 June, 2002, leg. REVIZEE
(RFA 31009); (198489470S, 378539130W), 60 m depth on 18
June, 2001, leg. REVIZEE (RFA 28114); (198489010S,
A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil 139
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Figures 20–30 Anadyomene pavonina.
(20) General habit. (21, 25–27) Arrangement of vein cells and interstitial cells. (22–24) Detail of perforate blade. (28, 29) Cross section
showing H-shaped interstitial cells (arrows). (30) Tetrahedral proteinaceous crystals (arrows).
378469220W), 58 m depth on 16 November, 1997, leg. REVI-
ZEE (RFA 28115); (198489470S, 378569330W), 60 m depth
on 12 July, 2001, leg. REVIZEE (RFA 31010); (198489010S,
378469220W), 58 m depth on 16 November, 1997, leg. REVI-
ZEE (RFA 31008).
Type locality Florida, USA.
Additional specimens examined Brazil, Rio de Janeiro
State (228239160S, 378359500W), 107–105 m depth on 08
February, 1996, leg. REVIZEE (RFA 31007).
Remarks Anadyomene pavonina has a perforate thallus,
similar to A. linkiana, but can be distinguished by its pros-
trate blade with rhizoids distributed over the entire surface,
with large perforations, and interstitial cells in a pinnate
arrangement that are disposed perpendicularly to the vein cells.
The blade margin of Anadyomene pavonina is similar to
that of A. lacerata. Both are formed from elongate vein cells,
although in A. pavonina, the margins are smooth and the
blade is perforated, while in A. lacerata the margins are lac-
erated, and there are no perforations.
The study material identified as Anadyomene pavonina
clearly matches the original descriptions of material collected
in Florida, USA by Littler and Littler (1991) and specimens
collected along the coast of Rio de Janeiro State described
by Bravin et al. (1999). In Brazil, A. pavonina has been
reported to occur off the coasts of the states of Bahia, Espı´-
rito Santo and Rio de Janeiro (Bravin et al. 1999, Yones-
higue-Valentin et al. 2006).
Anadyomene rhizoidifera A.B. Joly et S.M.B. Pereira
(Joly and Pereira 1973, p. 70, figs 1–7) (Figures
31–42)
Description
Blades dark green, erect, up to 2 cm tall,
growing in small tufts, fixed to the substratum by rhizoids
that are interwoven to form a short stipe. Blade polystro-
matic, eperforate, fan-shaped, with an entire, undulate or
140 A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil
Article in press - uncorrected proof
Figures 31–42 Anadyomene rhizoidifera.
(31) General habit. (32) Detail of blade with rhizoids (arrow). (33) Entire outer margin of interstitial cells. (34) Branching pattern of blade.
(35–37) Detail of rhizoids (arrows). (38) Base of vein cell forked, with one side soon elongating to form rhizoid (arrow). (39–41) Cross
section. (39) Blade showing cells layers are several rhizoids thick (arrow). (40) Interstitial H-shaped cells (arrow). (41) Blade with two cell
layers and H-shaped interstitial cell. (42) Tetrahedral proteinaceous crystals among the chloroplasts (arrow).
lobate margin delineated by interstitial cells. Blade composed
of 1–3 longitudinally elongated cells, 490-(1362)-3400
mm
long=130-(120)-250
mm in diameter, forming veins that are
polychotomously branched, giving rise to 2–4 cells at the
apex that diminish in size towards the distal region of the
thallus; vein cells have furcate bases, with one of the extrem-
ities elongated to form cortical rhizoids. Interstitial cells
small, spherical or oval, 60-(120)-250
mm long=47.5-
(71)105
mm in diameter, with a pinnate arrangement, appear-
ing as lateral or transverse bars tightly parallel to one another
and with their extremities partly overlapping or straddling
vein cells; in lateral view or in transverse section, they have
an ‘‘H’’ or dumb-bell shape. Cortical rhizoids originate from
the proximal extremities of the vein cells, covering the infe-
rior surface of the blade (except in young thalli). Crystalline
proteinaceous inclusions non-birefringent, tetrahedral, visible
in the protoplasm. No fertile material was observed.
Specimens examined Brazil, Bahia State, Ilhe´us, Praia
do Aeroporto on 08 November, 2006, leg. A.M. Alves et al.
(HUEFS 136247).
Additional specimens examined Holotype Brazil, Per-
nambuco State, Municı´pio de Cabo, Praia do Gaibu´ 25 July,
1968, leg. S. Pereira and Veloso (SPF 2636).
Type locality Praia de Gaibu´, Municı´pio de Cabo, Per-
nambuco, Brazil.
Remarks This is the first report of Anadyomene rhizoi-
difera since its original description and thus the first record
outside the type locality. This species was encountered at
only one of the collecting stations, growing in the form of
small tufts in the intertidal region, on a rocky substratum.
A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil 141
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Figures 43–49 Anadyomene saldanhae.
(43) General habit. (44) Young thallus. (45) Detail of the blade with rhizoids extending from basal portions of vein cells (arrows). (46)
Branching pattern of blade showing the random arrangement of interstitial cells (arrows); the outer layer is composed of small spherical
cells (arrow). (47) Cross section of vein. (48) Tetrahedral proteinaceous crystals (arrow). (49) Fertile cell with conical projection on the
lateral side of the cell (arrow).
The presence of rhizoids on the entire blade is a trait
shared by Anadyomene rhizoidifera and A. saldanhae; how-
ever, the latter species differs in that it has a random arrange-
ment of interstitial cells following repeated polychotomous
divisions and overlapping cells are absent within the eper-
forate blade.
In the original description of Anadyomene rhizoidifera,
Joly and Pereira (1973) mentioned the presence of rhizoids
on both sides of the blade. In our material, rhizoids were
observed only on the ventral sides of the blade, similar to
the observations made by Littler and Littler (1991).
According to Littler and Littler (1991), Anadyomene stel-
lata may, under certain environmental conditions, also form
rhizoids on one side of the blade. According to them (op.
cit.), only the largest cell of the vein at the base of the thallus
of A. stellata usually forms rhizoid extensions, which con-
tinue adjacent and parallel to the vein proximally, giving rise
to small and inconspicuous stipes in young thalli or to var-
ious fixation points in older thalli. Littler and Littler (1991)
also noted that the presence of rhizoids over the entire blade
is a relatively stable characteristic in A. rhizoidifera, but
occurs sporadically in A. stellata.
The specimens analyzed here differ from those studied by
Joly and Pereira (1973) in having fewer cell layers (three)
and lacking of rhizoids located internally to the vein cells.
Littler and Littler (1991) reported specimens with only a sin-
gle cell layer, excluding the rhizoids.
Anadyomene saldanhae A.B. Joly et E.C. Oliveira
Filho (Joly and Oliveira Filho 1969, p. 30, figs 1–3)
(Figures 43–49)
Description
Blades light green, erect, up to 2 cm tall,
without a conspicuous stipe, or prostrate, growing in dense
tufts; fixed to the substratum by rhizoids that grow from vein
142 A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil
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cells in the basal region of the blade. Blade monostromatic,
eperforate, fan-shaped, margin entire, smooth, bordered by
small, oval cells. Blade composed of 2–6 elongated, cylin-
drical to swollen cells, 350-(808)-1540
mm long=90-(123)-
310
mm in diameter, forming veins dividing polychoto-
mously into 2–3 cells at the apex. Interstitial cells small,
elliptical or irregularly shape, attached by a pointed or fur-
cate extremity, 80-(124)-180
mm long=70-(85)-100 mmin
diameter, polychotomously branched, randomly arranged,
with little or no overlapping of adjacent cells. Cortical rhi-
zoids absent, rhizoids extending from the basal portion of
the basal vein cells, generally suspended free or adhering to
the substratum. Crystalline proteinaceous inclusions non-
birefringent and tetrahedral shape visible in the protoplasm
between the chloroplasts. Fertile thalli were encountered dur-
ing the months of February and July.
Specimens selected Brazil, Bahia State (138049180S,
388239380W), 91 m depth on 23 July, 2002, leg. REVIZEE
(RFA 30990); (148489300S, 388559000W), 20 m depth on 01
July, 2001, leg. REVIZEE (RFA 31012); (168079300S,
388109520W), 40 m depth on 30 June, 2001, leg. REVIZEE
Central (RFA 28141); (188019220S, 358539280W), 60 m depth
on 13 November, 2001, leg. REVIZEE Central (RFA 28142);
(208219100S, 368389040W), 55 m depth on 13 July, 2001, leg.
Projeto REVIZEE Central (RFA 28135).
Additional specimens selected Holotype Brazil, Espı´-
rito Santo State, Dragagem no banco ‘‘Dogareza’’, 85 m
depth on 16 May, 1967 (SPF 60).
Type locality Banco Dogareza, off the coast of Vito´ria,
Espı´rito Santo State, Brazil.
Remarks The thalli of Anadyomene saldanhae are mor-
phologically similar to those of A. howei D.S. Littler et Lit-
tler, but they differ in the shape of the external margin of
the thallus, which in A. saldanhae is bordered by small and
spherical cells, whereas in A. howei, it is bordered by various
layers of large vein cells.
According to Littler and Littler (1991), the diagnostic
characteristics of Anadyomene saldanhae are the absence of
overlapping cells within the eperforate blade, the random
arrangement of interstitial cells following repeated polycho-
tomous divisions and the presence of an outer margin com-
posed of small spherical cells.
The material analyzed and identified as Anadyomene sal-
danhae from the coast of Bahia State matches the type mate-
rial and the descriptions and illustrations provided by Joly
and Oliveira Filho (1969), Bucher et al. (1990), Schneider
and Searles (1991) and Littler and Littler (1991, 1997, 2000).
Although this material was collected at 85 m depth, it was
similar to the descriptions of Schnetter and Bula Meyer
(1982) and Bucher et al. (1990) of material collected in shal-
low waters (3 and 9 m) in the Caribbean Sea off Colombia
and from Florida, respectively. Littler and Littler (1991,
1997, 2000) made reference to the occurrence of this species
growing on rocky substrata, on sponges, mangrove roots and
other hard substrata.
Among the Anadyomene species, A. saldanhae has the
second widest distribution along the Brazilian coast, occur-
ring in the states of Pernambuco, Bahia, Espı´rito Santo, and
Rio de Janeiro, on the Abrolhos archipelago, and near the
island complex of Trinidad and Martin Vaz (Joly and Oli-
veira Filho 1969, Nassar 1994, Horta 2000, Yoneshigue-
Valentin et al. 2005, 2006, Figueiredo 2006a,b).
Anadyomene stellata (Wulfen in Jacq.) C. Agardh
1823 (Agardh 1822–1823, p. 400) (Figures 50–68)
Description
Blades light to dark green, sometimes yel-
lowish, erect, forming tufts up to 6 cm tall; fixed to the
substratum by ramified aseptate rhizoids that are interwoven
to form a short stipe. Blade rigid, eperforate, with smooth
margins in young thalli and lobed or undulate margins in
older thalli. Blade formed by longitudinally elongate cells,
that are cylindrical to clavate, 120-(1183)-4000
mm
long=100-(143)-210
mm in diameter, forming veins with
polytomic ramifications, with 3–7 apical cells, entire or
divided into 2–11 transversally septate cells and united by
furcate extremities. Interstitial cells are small and perpendic-
ular to the principal cells, 55-(182)-410
mm long=50-(76)-
130
mm in diameter, pinnate in arrangement, forming a layer
of parallel lateral cells; interstitial cells dumb-bell shaped (H-
shaped) in lateral view or in transverse section. External mar-
gin smooth, formed by small, spherical cells. Cortical
rhizoids arise from the bases of the vein cells. Crystalline
proteinaceous inclusions non-birefringent, tetrahedral shape,
present in the protoplasm between the chloroplasts. Fertile
cells present at the thallus apex, with reproductive structures
liberated by terminal papillae. Fertile thalli were encountered
in June.
Specimens selected Brazil, Bahia State, (138049180S,
388239380W), Estaca˜o 7C, 91 m depth on 23 June, 2002, leg.
¸
REVIZEE (RFA 31000); Conde, Sı´tio do Conde on 20 April,
2007, leg. A.M. Alves and C.S. Santana (HUEFS 136248);
Salvador, Praia de Itapua˜ on 12 August, 2006, leg. A.M.
Alves et al. (HUEFS 136259); Itacare´, Praia da Concha on
09 November, 2006, leg. A.M. Alves et al. (HUEFS
136277); Prado, Corumbau on 14 June, 2007, arrival, leg.
A.M. Alves and C.S. Santana (HUEFS 136288).
Type locality Adriatic Sea
Remarks Anadyomene stellata is the most common spe-
cies along the coast of Bahia State, and was encountered
growing in the intertidal zone, pools and areas exposed to
surf, where they formed small, dense tufts. In shaded and
protected sites along reef edges, the thalli were larger and
formed loose tufts. Dredged material from 20 to 100 m deep
was collected in association with Rhizoclonium riparium
(Roth) Ku¨tz. ex Harv.
Anadyomene stellata is widely distributed along the Bra-
zilian coast, occurring in the states of Ceara´, Rio Grande do
A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil 143
Article in press - uncorrected proof
Figures 50–68 Anadyomene stellata.
(50) Habit. (51, 52) General view. (53) Detail of branching pattern of blade. (54, 55) Outer margin consisting of small interstitial cells.
(56–58) Vein branches highly variable. (56) Vein branch composed of one elongate cell. (57, 58) Vein branch composed of 3–4 successive
cells. (59) Vein branch composed of 10 short cells. (60, 61) Base of vein cell forked. (62) Vein cell ending in a lobed base (arrow).
(63) Cross section of monostromatic blade with interstitial H-shaped cells (arrow). (64) Cross section of blade showing various layers of
rhizoids (arrow). (65) Detail of chloroplast morphology. (66) H-shaped interstitial cell. (67, 68) Tetrahedral proteinaceous crystals (arrow).
Norte, Paraı´ba, Pernambuco, Bahia, Espı´rito Santo, and Rio
de Janeiro as well as in Atol das Rocas, Trinidad Island and
the Martin Vaz archipelago (Horta 2000, Yoneshigue-Valen-
tin et al. 2006, Figueiredo 2006a,b).
A pronounced variation in the number of successive vein
cells in the blade was observed. Some contained 1–3 suc-
cessive cells and were very long, whereas others had 3–7
cells. Still others contained up to 11 short cells. Multiple
patterns were sometimes observed in a single thallus.
Littler and Littler (1991) suggested that these variations
reflect the age of the thallus or, to a lesser extent, the envi-
ronmental conditions to which the plant has been exposed.
Thalli with 1–3 successive cells are young, those with 3–7
cells are of intermediate age; old thalli have more than seven
cells and their apical portions are often destroyed. Gray
(1866) and De Toni (1889) described two varieties of the
species based on variations of the nerve cells: var. floridana
(Gray) has 3–7 long successive cells, and var. luxurians
(Toni) has up to 12 short successive cells. These varieties
are now considered synonyms of A. stellata (Littler and Lit-
tler 1991).
The arrangement of the blade cells of Anadyomene stellata
is similar to that of A. lacerata; both have elongated vein
cells, with polytomic ramifications to the apex of the thallus
and interstitial cells arranged in series parallel to the vein
cells. They differ, however, in formations of their blade mar-
gins; the margin of A. stellata is formed by small, oval inter-
stitial cells, whereas the margin of A. lacerata is formed by
vein cells.
Anadyomene stellata is also similar to A. rhizoidifera in
the ramification patterns of vein cells, although the latter
species differs by having a polystromatic thallus, with up to
144 A.M. Alves et al.: The genus Anadyomene from Bahia, Brazil
Article in press - uncorrected proof
five layers, as well as having rhizoids on the base of the vein
cells in all areas of the thallus.
Discussion
Marked differences in distribution along the Brazilian coast
were found among different Anadyomene species. A. stellata,
however, is the only species with a broad distribution. In
contrast, A. rhizoidifera was found at only a single collecting
station, in the intertidal region off the southern coast of
Bahia. The other species (A. lacerata, A. linkiana, A. pavo-
nina and A. saldanhae) only occurred along the infralittoral
zone at a minimum depth of 20 m.
The morphological characteristics related to the ramifica-
tion patterns and the disposition of thallus cells, the types of
cells that bordered the external margin, and the presence and
point of origin of the rhizoids were diagnostic for the sepa-
ration of the species in the study area. However, most of the
characters used for species delimitation are known to be
extremely variable. This variation reflects either the age of
the thallus or, to a lesser extent, environmental conditions,
and, hence, intermediate morphologies are expected to be
common, leading to difficulties in identification.
Non-birefringent crystalline proteinaceous, tetrahedral
inclusions are reported here for the first time for the genus
Anadyomene; they are comparable to the proteinaceous crys-
tals encountered in Haplogloia kuckuckii Kylin (Phaeophy-
ceae), in Antithamnion kylinii (Ceramiales) by Pueschel
(1994, 1995), and in various cladophoralean taxa by Leliaert
and Coppejans (2004) and Leliaert et al. (2007b). Some
authors have suggested that proteinaceous crystals may have
a storage function (Jo´nsson 1962, Wetherbee et al. 1984,
Pueschel 1992, 1994). This hypothesis was supported by
Pueschel and Korb (2001), who demonstrated that protein
bands were present in thalli supplied with nitrogen but were
absent in nitrogen-starved thalli.
Acknowledgements
The authors would like to thank the Coordenaca˜o de Aperfeicoa-
¸¸
mento de Pessoal de Nı´vel Superior (CAPES) for a research grant
to the first author, the Fundaca˜o de Amparo a` Pesquisa do Estado
¸
da Bahia (FAPESB) (Proc. PPP 0011/2006) for partially financing
the project, the Universidade Estadual de Feira de Santana (UEFS)
and the team of the Laborato´rio de Ficologia (LAFICO) for the use
of their infra-structure and for their invaluable help, the Programa
de Po´s-Graduaca˜o em Botaˆnica of UEFS for financial aid to visit
¸
national herbaria and the curators of those herbaria for providing
access to their material.
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Received 19 February, 2010; accepted 20 December, 2010; online
first 25 February, 2011
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