Taxonomic studies in the Schizymeniaceae (Nemastomatales, Rhodophyta): on the

identity of Schizymenia sp. in the Azores and the generic placement of

Nemastoma confusum

DANIELA GABRIEL1,3*, TOM SCHILS

4, MANUELA I. PARENTE2,5, STEFANO G.A. DRAISMA

6,7, ANA I. NETO2,8

AND SUZANNE FREDERICQ3

1CIBIO-Acores, 2Departamento de Biologia, Universidade dos Acores, 9501-801 Ponta Delgada, Acores, Portugal3Department of Biology, University of Louisiana at Lafayette, Lafayette, LA 70504-2451, USA

4Marine Laboratory, University of Guam, Mangilao, GU 96923, USA5Departamento de Ciencias e Engenharia do Ambiente, Instituto do Mar – IMAR, Faculdade de Ciencias e Tecnologia,

Universidade Nova de Lisboa, Quinta da Torre, 2829-516 Caparica, Portugal6Nationaal Herbarium Nederland – Universiteit Leiden, 2333 CC Leiden, The Netherlands

7Institute of Ocean & Earth Sciences, University of Malaya, Kuala Lumpur 50603, Malaysia8CIIMAR (Centro Interdisciplinar de Investigacao Marinha e Ambiental), Universidade do Porto, Rua dos Bragas,

289-4050-123 Porto, Portugal

GABRIEL D., SCHILS T., PARENTE M.I., DRAISMA S.G.A., NETO A.I. AND FREDERICQ S. 2011. Taxonomic studies in theSchizymeniaceae (Nemastomatales, Rhodophyta): on the identity of Schizymenia sp. in the Azores and the genericplacement of Nemastoma confusum. Phycologia 50: 109–121. DOI: 10.2216/09-67.1

Comparative rbcL sequence analysis indicates that the species going under the name Schizymenia dubyi in the Azoresshould be referred to as S. apoda. Sequences of Schizymenia specimens from China and Namibia were also identified asS. apoda, of which the type locality is the Cape Province in South Africa. Schizymenia dubyi, described from AtlanticFrance, is clearly a distinct species that we here report for Japan and Sicily in the Mediterranean Sea. Both Schizymenia

species, along with an unreported species from Japan, are distinct from S. pacifica described from Washington, in thePacific Coast of North America. Secondary pit connections were observed in gametophytes of S. apoda from the Azores,a previously unknown character for the Nemastomatales. Examination of type material of Nemastoma confusum

indicates that this species, currently placed in the Nemastomataceae, should be transferred to the genus Platoma in theSchizymeniaceae. A morphological comparison between Platoma confusum (Kraft & John) comb. nov. with descriptionsof P. cyclocolpum and P. chrysymenioides suggests that the three species are closely related.

KEY WORDS: Azores, Nemastoma, Nemastomatales, Platoma, rbcL, Rhodophyta, Schizymenia, Schizymeniaceae,Systematics, Taxonomy

INTRODUCTION

Schizymenia J. Agardh (Schizymeniaceae) has the largest

geographical distribution of all nemastomatalean genera.

The 10 species of Schizymenia that are currently recognised

are found in temperate, subtropical and tropical waters,

ranging from the subantarctic islands to Alaska (Guiry &

Guiry 2009). The genus Schizymenia is distinguished from

other genera in the Schizymeniaceae by the presence of

diagnostic gland cells resembling large, inverted tears,

located terminally on cortical filaments (Dixon & Irvine

1977).

The type of the genus, Schizymenia dubyi (Chauvin ex

Duby) J. Agardh, was established by Agardh based on

Halymenia dubyi Chauvin ex Duby from Atlantic France,

and it is the most studied and best-characterised member of

the Schizymeniaceae. The genus also contains the only

known tetrasporophyte of Schizymeniaceae found in nature

(Masuda & Guiry 1994). Extensive culture studies per-

formed on S. dubyi (Ardre 1977, 1980) and S. pacifica

(Kylin) Kylin (DeCew et al. 1992) revealed a heteromorphic

life history where the tetraspophytic phase was identified as

a crustose species originally attributed to the generitype of

Haematocelis, H. rubens J. Agardh.

Kylin (1956) circumscribed the genus Schizymenia as

follows: ‘with blade-like thalli that bear gland cells in the

cortex, produce carpospores towards the exterior of the

thallus, with the base of the carposporophyte lying deep

inside the medulla, and in which nearly all cells of the

gonimoblasts become carpospores. Additional characters

include weakly developed sterile filaments, or lack thereof,

surrounding the carposporophyte, and a weakly defined

but distinct ostiole located above the slightly raised

carposporangial mass’. The shape and size of the blades,

along with vegetative features such as short cortical branch

systems with subspherical inner cells, may also serve to

distinguish species (Abbott 1967; Womersley 1994).

The species of Schizymenia occurring in the Azores were

originally reported by Trelease (1897) as S. undulata J.

Agardh (Terceira Island) and S. obovata J. Agardh (Corvo

Island), both species currently regarded as synonyms of S.

dubyi, described from Atlantic France, and S. apoda (J.

Agardh) J. Agardh described from Atlantic South Africa,* Corresponding author (danielalgabriel@gmail.com).

Phycologia (2011) Volume 50 (2), 109–121 Published 3 March 2011

109

respectively (Guiry & Guiry 2009). After extensive studies

on the Azorean marine flora, Neto (1994) reported that

only S. dubyi occurred in this archipelago.

The macroalgal communities of the Azores have been

studied since the mid-1800s (Seubert 1844), but early

publications were restricted to species inventories. Since

Feldmann (1942), more attention has been given to the

ecology of Azorean macroalgae, and several papers have

been published by Neto and coauthors over the past

15 years (see Tittley et al. 2001, 2009; Tittley & Neto 2005).

Life history studies and morphological information (Par-

ente et al. 2003a, b; Toste et al. 2003a, b; Gabriel et al. 2009,

2010) are scanty. The floristic studies reveal a mixed flora

with a strong component of cold-water species together

with a few tropical and subtropical taxa (Neto 1997).

The recently resurrected order Nemastomatales (Kylin)

Saunders & Kraft comprises two families, the Nemasto-

mataceae and Schizymeniaceae (Masuda & Guiry 1995;

Saunders & Kraft 2002; Gavio et al. 2005), both

represented in the marine flora of the Azores. Nemastoma

confusum Kraft & John (Fredericq et al. 1992; Neto 1994),

Itonoa marginifera (J. Agardh) Masuda & Guiry (Larkum

1960; Neto 1994) and Predaea feldmanii Børgesen (Freder-

icq et al. 1992; Neto 1994; Tittley & Neto 1994) are the

three reported species of the Nemastomataceae. Platoma

cyclocolpum (Montagne) F. Schmitz (South & Tittley 1986;

Neto 1991, 1994) and S. dubyi (Schmidt 1929; Palminha

1957; South & Tittley 1986; Neto 1994; Tittley & Neto

1994) are the listed species of the Schizymeniaceae.

The red algal genus Nemastoma J. Agardh (1842)

currently comprises nine species predominantly inhabiting

tropical to subtropical waters worldwide (Huisman 1999;

Rodriguez-Prieto et al. 2004). Despite its wide distribution

range, representatives of the genus are not abundantly

present in the respective floras, and most of the species are

known only from their original description (Kraft & John

1976). The reproductive features of Nemastoma species

other than those described in N. dichotomum J. Agardh

have been poorly studied and require re-examination

(Masuda & Guiry 1994). Nemastoma confusum was

described by Kraft & John (1976) based on gelatinous

specimens from Ghana. The specific epithet alludes to

initial misidentification of the species as Predaea feldmannii

when cystocarps could not be observed.

As part of a revision of the Schizymeniaceae, the present

paper reports on a molecular-based reappraisal of Schizy-

menia species and provides morphological and ecological

observations of the Azorean Schizymenia species. We also

present reasons for transferring N. confusum to the genus

Platoma.

MATERIAL AND METHODS

Algal material used in the present study was collected since

1990 at different sites of the Archipelago of the Azores.

Collections were made from April to September, in the

intertidal. Reference collections were made by storing

samples in a 5% formalin/seawater solution, pressed as

herbarium sheets or dried in silica gel. Collections are

deposited in the Herbarium of the Department of Biology,

University of the Azores. Additional samples of Nemasto-

matales from the Ghent University Herbarium (GENT,

Belgium) and the Herbarium of the University of Louisiana

at Lafayette (LAF, USA) were used for comparison.

The observations of N. confusum presented in this work

are based on five well-preserved slides of the isotype from

Ghana (John no. 7260) used for the original description of

this species (Kraft & John 1976, p. 332). The material was

obtained through the kindness of Dr Gerry Kraft

(University of Melbourne Herbarium – MELU) as a loan

to Dr Willem Prud’homme van Reine from the National

Herbarium of the Netherlands, Leiden (L).

A combination of stereo- and compound microscopes

was used to describe morphological and anatomical

characters and reproductive structures for the diagnosis.

Species identifications were based on the original descrip-

tions and on a critical analysis of the literature. Represen-

tative collections of microscope slides and photomicro-

graphs were made. Microscope slides of squash mounts

were prepared from liquid-preserved material, stained with

1% aniline blue with HCL acidification, and mounted in

50% Karo corn syrup–water solution (containing a few

drops of 2% phenol). Photomicrographs were taken using

various digital cameras connected to light microscopes.

Measurements of cells and other structures were made

using a micrometer eye piece (presented in the text as length

per width).

DNA samples were prepared using the DNAeasy Plant

Minikit (Qiagen, Valencia, CA). Silica gel dried specimens

and extracted DNA samples are deposited at LAF and

stored at 220uC. Plastid-encoded rbcL was selected to infer

a phylogeny of Schizymenia and related nemastomatalean

genera. Protocols for DNA extraction, gene amplification

and sequencing are described in Gavio & Fredericq (2002).

PCR primers (F7-R753, F57-R557, F645-R1150, F993-

RrbcSstart) and sequencing primers (F7, F57, F645, F993,

R376, R557, R753, R1150, RrbcSstart) are listed in Lin et

al. (2001) and Gavio & Fredericq (2002).

A total of 24 rbcL sequences were used in this study,

including newly generated sequences of which the vouchers

are located at LAF, and of sequences downloaded from

GenBank. A data set of available members of Schizymenia

was assembled, and two other taxa in the Schizymeniaceae,

P. cyclocolpum and Titanophora pikeana (Dickie) Feld-

mann, were added as the out-group based on a global

phylogenetic analyses of the Nemastomatales (Gavio et al.

2005). The information about the taxa, collection sites and

collectors is listed in Table 1.

The generated rbcL sequences were compiled, edited and

aligned using Sequencher software (Gene Codes Corp.,

Ann Arbor, MI, USA) and exported for phylogenetic

analysis in PAUP* v.4.0 beta 10 (Swofford 2003) and

MacClade v.4 (Maddison & Maddison 2000).

Phylogenetic analyses were conducted with the maximum

parsimony (MP) and maximum likelihood (ML) algorithms

as implemented in PAUP and PhyML v2.4.4 (Guindon &

Gascuel 2003), respectively, and the Bayesian inference as

implemented in MrBayes 3.0 (Hall 2001; Huelsenbeck &

Ronquist 2001). Parsimony trees obtained under the Fitch

criterion of equal weights for all substitutions (Fitch 1971)

110 Phycologia, Vol. 50 (2), 2011

Table

1.

Lis

to

fsp

ecie

su

sed

inth

erb

cLse

qu

ence

an

aly

sis

wit

hco

llec

tio

nin

form

ati

on

an

dG

enB

an

kacc

essi

on

nu

mb

er.

Sp

ecie

sC

oll

ecti

on

iden

tifi

cati

on

Co

llec

tio

nlo

cali

tyC

oll

ecti

on

data

Gen

Ban

kacc

essi

on

nu

mb

er

Pla

tom

acyclo

colp

um

(Mo

nta

gn

e)S

chm

itz

SM

G-0

4-2

02

Po

nta

Garc

a,

Vil

aF

ran

ca,

Sao

Mig

uel

,A

zore

s(8

-md

epth

)D

.G

ab

riel

&P

.M

ad

eira

,20

Au

g.

2004

FJ8

68809

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hL

AF

-7-6

-93-1

-1S

wak

op

mu

nd

,N

am

ibia

M.H

.H

om

mer

san

d,

6Ju

l.1993

AY

294401

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hL

AF

-6-9

4-1

-1T

aip

ing

Cap

e,S

han

do

ng

pro

v.,

Ch

ina

M.H

.H

om

mer

san

d,

Jun

.1994

AY

294392

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hG

RW

-04-8

7B

arr

oV

erm

elh

o,

Gra

cio

sa,

Azo

res

D.

Gab

riel

,10

Jun

.2004

FJ8

78860

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hG

RW

-04-8

8B

arr

oV

erm

elh

o,

Gra

cio

sa,

Azo

res

D.

Gab

riel

,10

Jun

.2004

FJ8

78861

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hG

RW

-06-7

86

Baıa

da

Fo

nte

,G

raci

osa

,A

zore

s9

Jul.

2006

FJ8

78862

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-04-1

64

Pra

iad

oP

op

ulo

,S

ao

Mig

uel

,A

zore

sM

.I.

Pare

nte

,14

Jun

.2004

FJ8

78863

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-04-1

65

Pra

iad

oP

op

ulo

,S

ao

Mig

uel

,A

zore

sM

.I.

Pare

nte

,14

Jun

.2004

FJ8

78864

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-05-1

45

Sao

Ro

qu

e,S

ao

Mig

uel

,A

zore

sD

.G

ab

riel

,9

Au

g.

2005

FJ8

78865

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-05-2

26

Mo

stei

ros,

Sao

Mig

uel

,A

zore

sD

.G

ab

riel

&M

.I.

Pare

nte

,07

Sep

.2005

FJ8

78866

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-05-2

59

Sao

Vic

ente

,S

ao

Mig

uel

,A

zore

sD

.G

ab

riel

,21

Sep

.2005

FJ8

78867

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hS

MG

-06-8

4S

ao

Mig

uel

,A

zore

sD

.G

ab

riel

,2006

FJ8

78868

Sch

izym

enia

apoda

(J.

Agard

h)

J.A

gard

hP

G07220

Pra

iad

oP

op

ulo

,S

ao

Mig

uel

,A

zore

sD

.G

ab

riel

&M

.P

are

nte

2007

GQ

495983

Sch

izym

enia

dubyi

(Ch

au

vin

exD

ub

y)

J.A

gard

hL

AF

-6-2

2-9

3-1

-1P

igh

et,

Bri

ttan

y,

Fra

nce

J.C

ab

ioch

,22

Jun

.1993

AY

294389

Sch

izym

enia

dubyi

(Ch

au

vin

exD

ub

y)

J.A

gard

hL

AF

-7-1

0-9

4-1

-1Jo

do

gah

am

a,

Miy

ak

o,

Iwate

-ken

,Ja

pan

M.H

.H

om

mer

san

d&

M.

Yo

shiz

ak

i,10

Jul.

1994

AY

294388

Sch

izym

enia

dubyi

(Ch

au

vin

exD

ub

y)

J.A

gard

hL

AF

-7-1

0-9

4-1

-2Jo

do

gah

am

a,

Miy

ak

o,

Iwate

-ken

,Ja

pan

M.H

.H

om

mer

san

d&

M.

Yo

shiz

ak

i,10

Jul.

1994

FJ8

78869

Sch

izym

enia

dubyi

h(C

hau

vin

exD

ub

y)

J.A

gard

PG

08865

Mo

nd

ello

,S

icil

y,

Italy

M.

Pare

nte

&R

.S

ou

sa2008

GQ

495984

Sch

izym

enia

dubyi

(Ch

au

vin

exD

ub

y)

J.A

gard

hP

G08887

Mo

nd

ello

,S

icil

y,

Italy

M.

Pare

nte

&R

.S

ou

sa2008

GQ

495985

Sch

izym

enia

paci

fica

(Kyli

n)

Kyli

nL

AF

-7-2

6-9

5-1

-1K

an

ah

aB

ay,

W.

Juan

Isla

nd

,W

A,

US

AM

.J.

Wyn

ne,

26

Jul.

1995

AY

294393

Sch

izym

enia

paci

fica

(Kyli

n)

Kyli

nL

AF

-4-1

5-9

4-1

-1V

an

cou

ver

,B

riti

shC

olu

mb

ia,

Can

ad

a(d

rift

)S

.C.

Lin

dst

rom

,15

Ap

r.1994

AY

294394

Sch

izym

enia

paci

fica

(Kyli

n)

Kyli

nL

AF

-7-2

4-9

8-1

-1(T

C101)

No

rth

Bo

ard

man

St.

Park

,O

R,

US

AT

.O.

Ch

o&

G.I

.G

ayle

,24

Jul.

1998

FJ8

78870

Sch

izym

enia

paci

fica

(Kyli

n)

Kyli

nL

AF

-7-2

4-9

8-1

-2(T

C130)

No

rth

Bo

ard

man

St.

Park

,O

R,

US

AT

.O.

Ch

o&

G.I

.G

ayle

,24

Jul.

1998

FJ8

78871

Sch

izym

enia

sp.

cf.

novae-z

elandia

eJ.

Agard

hL

AF

-9-5

-93-1

-1T

ok

aw

a,

Ch

osh

i,C

hib

aP

ref.

,Ja

pan

S.

Fre

der

icq

&M

.Y

osh

izak

i,2

Sep

.1993

AY

294391

Tit

anophora

pik

eana

(Dic

kie

)J.

Fel

dm

an

nL

AF

-2-1

1-0

1-1

-1D

eep

Sp

on

ge

Ree

f,S

od

wan

aB

ay,

Kw

aZ

ulu

-Nata

l,S

ou

thA

fric

a(2

7-m

dep

th)

S.

Fre

der

icq

&O

.D

eCle

rck

,11

Feb

.2001

AY

294364

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 111

were inferred from a heuristic search, excluding uninfor-

mative characters consisting of 1000 random sequence

additions holding 10 trees at each step, MULPARS and

tree-bisection-reconnection (TBR) algorithms with the

MULTREES (saving multiple trees) and STEEPEST

DESCENT option. Support for nodes in the MP and ML

analyses were assessed by calculating bootstrap proportion

values (Felsenstein 1985) based on 1000 and 100 resam-

plings, respectively, retaining groups with a frequency

greater than 50%, MULPARS and TBR algorithms.

The optimal models of sequence evolution to fit the data

alignment estimated by hierarchical likelihood ratio tests

performed by Modeltest v.3.6 (Posada & Crandall 1998)

was the GTR + I + G (general time reversible model with a

proportion of invariable sites and gamma distribution split

into four categories) for the data set. The Akaike

information criterion parameters applied in the likelihood

analysis were as follows: assumed nucleotide frequencies

A 5 0.3045; C 5 0.1632; G 5 0.2103; T 5 0.3220;

substitution rate matrix A–C substitutions 5 0.0, A–G 5

6.0541, A–T 5 2.3094, C–G 5 0.8317, C–T5 17.2925, G–T

5 1.0; proportion of sites assumed to be invariable 5 0.485;

and rates for variable sites assumed to follow a gamma

distribution with shape parameter 5 0.625.

For the Bayesian analysis, four chains of the Markov

chain Monte Carlo were run, sampling one tree every 100

generations for 2,000,000 generations starting with a

random tree for the rbcL data sets, with the following

parameters applied: nst 5 6 and Rates 5 invgamma. The

first 20,000 generations were discarded as the ‘burn-in’

period to reach equilibrium. A 50% consensus tree

(majority rule as implemented by PAUP) was computed

from the trees saved after the burn-in point. Reliability of

the Bayesian consensus tree is given by the frequency at

which each node appears among all saved trees after the

burn-in generation. This frequency corresponds to the

posterior probability of the clades (Hall 2001).

RESULTS

Schizymenia ‘dubyi’ (Chauvin ex Duby) J. Agardh (1851,

p. 171) from the Azores

HABIT AND VEGETATIVE STRUCTURE: Plants foliose, liver-

red to brownish-red in colour, simple or broadly lanceolate

with irregular lobes and proliferations from the margins,

sometimes undulate, soft fleshy, and slippery (Figs 1–4), up

to 20 cm tall. The occasionally perforated blades are

attached with a short stipe to the substratum by a small

discoid holdfast, from which other blades can emerge,

usually growing within dense assemblages of geniculate

Corallinaceae (Fig. 4). Cystocarps on the blade surface are

easily distinguished by visible ostioles.

The cortex is composed of anticlinal fascicles of

dichotomously branched moniliform filaments (Figs 5–8,

10), with occasionally darkly staining elongated gland cells

(Fig. 6, arrow) reaching the thallus surface. Innermost

cortical cells are spherical, surface cells are more elongated

(Figs 5–8). Inner cortical cells laterally produce primordia

that extend into medullary rhizoidal filaments (Figs 6, 7).

Occasionally, inner cortical cells are linked by secondary pit

connections (Fig. 8, arrow). The medulla is composed of

primary filiform filaments as well as secondarily formed

rhizoidal filaments that are laxly to densely interwoven with

one another and that may undergo localised swellings

(Fig. 9).

PRE- AND EARLY POSTFERTILISATION STRUCTURES: Thalli

are monoecious. Carpogonial branches (Figs 10, 11)

develop outwards from an inner cortical cell bearing

subdichotomies of cortical filaments. The generative

cortical cell becomes the supporting cell of a three-celled

carpogonial branch (Fig. 10). With maturation, a straight

trichogyne develops from the carpogonium growing to-

wards the thallus surface (Fig. 11). Simultaneously, the

cortical cells linked to the supporting cell expand in size and

become dark staining subsidiary auxiliary cells (a.k.a.

nutritive auxiliary cells; Fig. 11).

POSTFERTILISATION STRUCTURES: The formation of con-

necting filaments was not observed. The generative auxiliary

cell cuts off same-sized gonimoblast cells that are surround-

ed by a loose network of vegetative filaments linked to the

auxiliary cell that form an involucrum-like structure around

the carposporophyte (Fig. 12, arrows). A surface ostiole

develops at the distal end of the gonimoblast (Fig. 13).

MOLECULAR EVIDENCE: All Schizymenia vouchers from the

Azores belong to a single species, nested in a clade that is

distinct from, but sister to, S. dubyi from Atlantic France

and Japan (Fig. 14). The Azorean samples are conspecific

with Schizymenia apoda from Namibia and China. An

unreported Schizymenia species from Japan is sister to S.

dubyi and S. apoda. A fourth species is S. pacifica (Kylin)

Kylin occurring along the North American West Coast

(Washington and Oregon, USA, and Canada). The

uncorrected pairwise difference between S. dubyi and S.

apoda is 0.015, between S. dubyi and S. sp. is 0.034, between

S. apoda and S. sp. is 0.033, between S. pacifica and S.

dubyi is 0.050, between S. pacifica and S. apoda is 0.046 and

between S. pacifica and S. sp. 0.048.

Nemastoma confusum Kraft & John (1976, p. 332) from

Ghana (based on isotype J-7260)

VEGETATIVE STRUCTURE: The thallus consists of narrow

medullary filaments that are sparsely branched and loosely

aggregated, sometimes comprising X- and Y-shaped cells,

and pseudodichotomously branched cortical filaments, with

cells decreasing in size and becoming more darkly stained

with aniline blue closer to the surface (Fig. 15). Occasion-

ally, adventitious rhizoidal filaments are formed in the inner

cortex, growing inward where they intertwine with the

medullary filaments. Gland cells are subspherical and

intercalary on cortical filaments (Fig. 15), occurring singly

at different densities throughout the blade.

PRE- AND EARLY POSTFERTILISATION STRUCTURES: Mature

three-celled carpogonial branches develop at the distal end

of an inner cortical cell (supporting cell), in an intercalary

position at the dichotomy of a cortical fascicle (Figs 16, 17).

112 Phycologia, Vol. 50 (2), 2011

Figs 1–7. Habit of Schizymenia apoda from the Azores.Fig. 1. Cystocarpic specimen from Sao Miguel, SMG-01-30; bar 5 1 cm.Fig. 2. Cystocarpic specimen from Sao Miguel, SMG-04-170; bar 5 1 cm.Fig. 3. Cystocarpic specimen from Graciosa, GRW-04-87; bar 5 1 cm.Fig. 4. Cystocarpic specimen from Sao Miguel growing on Corallina elongata.Fig. 5. Vegetative morphology showing regularly branched cortical fascicles subtending a medullary filament; bar 5 100 mm. GRW-04-88.Fig. 6. Cortical branches with elongated gland cell (arrow) and filiform medullary filaments; bar 5 40 mm. SMG-06-84.Fig. 7. Primary medullary (m) and secondary rhizoidal filament (r) connected to base of cortical fascicle; bar 5 40 mm. SMG-06-84.

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 113

Figs 8–13. Schizymenia apoda from the Azores.Fig. 8. Secondary pit connection (arrow) linking inner cortical cell with cell in neighboring cell file; bar 5 25 mm. GRW-04.88.Fig. 9. Filiform rhizoidal filaments and medullary cells connected by secondary pit connections (arrow); bar 5 100 mm. GRW-04.88.Fig. 10. Immature carpogonial branch (icb) borne on supporting cell (arrow) cut off laterally from inner cortical cell; bar 5 25 mm. GRW-04.88.Fig. 11. Squashed three-celled carpogonial branch consisting of rounded basal cell, flat hypogenous cell and carpogonium withtrichogyne (t). Note that neighboring cortical cells have expanded and started to stain darkly, which marks their transformation intosubsidiary auxiliary cells (sac); bar 5 25 mm. GRW-04.88.Fig. 12. Young gonimoblasts (g) borne on auxiliary cell (aux), and incoming connecting filament (cf). Note that the basal cells of corticalfilaments surrounding the gonimoblasts have elongated (arrows), forming a ‘rudimentary’ pericarp; bar 5 25 mm. GRW-04.88.Fig. 13. Surface ostiole of the carposporophyte showing carposporangia; bar 5 100 mm. SMG-04-164.

114 Phycologia, Vol. 50 (2), 2011

The carpogonial branches consist of an oval to rectangular

basal cell, an oval hypogynous cell and a distal conical

carpogonium with a straight trichogyne (Fig. 16). Immedi-

ately before putative fertilisation, the two distal cells

connected to the supporting cell and their subtending

cortical fascicles become darkly staining (Fig. 17). These

cells become swollen, produce bulges on the cell’s sides and

become irregular in shape (Fig. 18) and act as subsidiary

auxiliary cells upon their fusion with the fertilised

carpogonium (stage not seen). The connecting filament

initials originating from the subsidiary auxiliary cells were

not observed. Connecting filaments traverse the thallus,

and each fuses with a generative auxiliary cell located in an

intercalary position, similar to the position of the support-

ing cell bearing a carpogonial branch, on another cortical

fascicle (Fig. 19).

LATE POSTFERTILISATION STRUCTURES: Upon diploidisa-

tion, the auxiliary cell enlarges, and a gonimoblast initial is

cut off distally, in the same manner as a carpogonial branch

initial (Fig. 20). The gonimoblast initial continues to divide

forming a single gonimolobe (Figs 21, 23). All gonimoblast

Fig. 14. One of 276 equally most parsimonious trees based on rbcL sequences showing the position of species of Schizymenia in theSchizymeniaceae, using Platoma cyclocolpum and Titanophora pikeana as the out-group. Branch lengths are proportional to sequencechange. The three tiers of numbers at a node, namely represent maximum parsimony and maximum likelihood bootstrap values andBayesian posterior probabilities, respectively (top to bottom).

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 115

cells transform sequentially into carposporangia, with the

more immature ones observed at the base of the gonimo-

lobe. Concomitantly, vegetative cells adjacent to the

auxiliary cell elongate forming a primordial involucrum

surrounding the carposporophyte (Figs 22, 23).

DISCUSSION

As inferred from the rbcL sequence data analysis, the

Azorean vouchers of Schizymenia are conspecific with S.

apoda from Namibia, a species described from Table Bay,

Cape Province, along the west coast of South Africa, and

are different from S. dubyi, described from Brittany,

Atlantic France. Consequently, S. apoda can be added as

a second Schizymenia species to the algal flora of the North

Atlantic. Published records of the species under the name S.

dubyi from Iceland (Caram & Jonsson 1972), Ireland

(Cotton 1912; Newton 1931; Guiry 1978; Morton 1994),

Great Britain (Newton 1931; Dixon & Irvine 1977; Hardy

& Guiry 2003), the north coast of Atlantic Spain (Veiga et

al. 1998) and Portugal (Ardre 1970) need to be critically re-

examined to ascertain their correct identity. Schizymenia

dubyi has also been reported from China, but our results

newly record S. apoda for the region, and it is likely that

many or all of the Chinese S. dubyi records are in fact S.

apoda. Thus, an in-depth morphological and molecular

study to differentiate the worldwide species of Schizymenia

is called for. Only then will the biogeographic patterns

among the Azorean, Namibian and Chinese populations of

S. apoda and those of S. dubyi from Atlantic France, the

Mediterranean Sea and Japan be understood.

Although Ardre (1980) considered gland cells to be

generally present in Australian specimens of S. dubyi, it is

likely that gland cells are not consistently present in

Australia, as is the case for European specimens of the

same species (Womersley 1994). As reported in the present

study, young gland cells are initially subspherical and

elongate when maturing to become ovoid and finally

longitudinally elongate when reaching the surface.

DeCew et al.’s (1992) suggestion that North American S.

pacifica is probably not distinct from S. dubyi has proved to

be incorrect (Womersley 1994; Fredericq et al. 1996). The

sequences of a second Schizymenia species from Japan

(Fig. 14) fits the morphological and anatomical description

of Schizymenia novae-zelandiae J. Agardh 1878 (p. 677)

from New Zealand as was reported and illustrated in

Adams (1994). However, as we have not examined type

Figs 15–19. Platoma confusum from Ghana.Fig. 15. Pseudodichotomously branched cortical filaments, intercalary gland cell, X-shaped medullary cell and thin medullary filaments;bar 5 40 mm. J-7260.Fig. 16. Three-celled carpogonial branch borne on inner cortical supporting cell (su), consisting of rectangular basal cell (bs), ovalhypogynous cell (hc) and conical carpogonium (c); bar 5 40 mm. J-7260.Fig. 17. Three-celled carpogonial branch with swollen subsidiary auxiliary cells (arrows); bar 5 40 mm. J-7260.Fig. 18. Subsidiary auxiliary cell producing a bulge (arrow); bar 5 40 mm. J-7260.Fig. 19. Cortical fascicles bearing an intercalary pyriform generative auxiliary cell; bar 5 40 mm. J-7260.

116 Phycologia, Vol. 50 (2), 2011

material of S. novae-zelandiae, the Japanese specimen is

here referred to as Schizymenia sp. Figure 24 presents an

updated overview of Schizymenia distributions in the world.

In detailed studies of S. dubyi, Ardre (1977, 1980)

discovered that the species is actually heteromorphic in

which the life cycle comprises an erect gametophyte

alternating with a crustose tetrasporophyte that bears

zonate tetrasporangia and resembles Haematocelis rubens

J. Agardh (Hansen 1989). Until the present study,

secondary pit connections have been reported only from

the crustose ‘Haematocelis’ tetrasporophyte in Nemasto-

matales; it is herein newly reported that they occasionally

occur in the gametophyte of S. apoda, linking cells of

adjacent inner cortical branches and between medullary X-

cells.

In the course of a revision of the Nemastomatales, we

examined the vegetative and reproductive morphology of

the red alga N. confusum, a species whose taxonomic status

should be reinvestigated (e.g. Masuda & Guiry 1994; Gavio

et al. 2005). When this species was erected, all nemastoma-

talean taxa were placed in the Nemastomataceae; the

morphologically similar genera Nemastoma, Platoma and

Predaea were separated based on a combination of features.

The presence of nutritive cell clusters on cells adjacent to

the auxiliary cell, a diagnostic character of the genus

Predaea, separates Predaea huismanii from N. confusum

(Sanson et al. 1991). Although N. confusum shares features

with both Nemastoma and Platoma, the species was placed

in the former genus mainly on the basis of the presence of

gland cells (Itono & Tsuda 1980).

Kajimura (1997) suggested that N. confusum was

probably a member of Platoma lacking a stipe and noticed

its resemblance to some specimens of Platoma izunosimense

Segawa. Masuda & Guiry (1994) noted that N. confusum

was closely related to P. cyclocolpum based on the following

morphological similarities: supporting cells and auxiliary

cells originate from the basal cells of cortical fascicles, the

gonimoblast develops directly from the auxiliary cell and

gland cells are formed in an intercalary position on cortical

fascicles.

Based on the illustrations and original description of N.

confusum, Gavio et al. (2005) also concluded that the

species should be transferred to a related genus once the

mode of connecting filament initiation has been clarified.

Gavio et al. (2005) contended that most species placed in

Nemastoma may in fact be species of Predaea because the

Figs 20–23. Platoma confusum from Ghana.Fig. 20. Auxiliary cell borne intercalary in inner cortex bearing a gonimoblast initial; bar 5 40 mm. J-7260.Fig. 21. Young gonimoblast develops distally from the opposite side of the incoming connecting filament (cf); bar 5 4.5 mm. J-7260.Fig. 22. Young gonimolobe on an inflated auxiliary cell (ac); bar 5 100 mm. J-7260.Fig. 23. Close-up of Figure 22 showing a connecting filament (cf) and elongated cortical cells surrounding the gonimolobe (arrows); bar5 40 mm. J-7260.

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 117

original drawings by Berthold (1884) of the type N.

dichotomum from the Bay of Naples depict auxiliary cells

encompassing one or two swollen cells toward the ends of

filaments. Such rhizoidal auxiliary filaments were the basis

for the recognition of the monotypic Adelophycus (as

Adelophyton) Kraft, a genus that thus may have to be

merged with Nemastoma (Gavio et al. 2005).

Nemastoma confusum had been considered a ‘male’ plant

of P. feldmannii described by Børgesen from Saint Helena

(Kraft & John 1976) or perhaps a species of Predaea lacking

auxiliary nutritive cells (Gavio et al. 2005). Upon examina-

tion of type material of N. confusum, we conclude that this

species belongs to the Schizymeniaceae instead of the

Nemastomataceae based on the early prefertilisation events

in which the subsidiary auxiliary cells inflate, become darkly

staining, produce bulges and become irregular in outline, the

diagnostic feature of this family (Gavio et al. 2005).

Among the Schizymeniaceae (i.e. Platoma, Schizymenia,

Titanophora and Wetherbeella), N. confusum is readily

distinguished from species of Titanophora by a lack of

calcified thallus incrustation and from Schizymenia by a

lack of a compact cortex bearing elongate gland cells

terminally on cortical fascicles. The genus Wetherbeella was

erected on the basis of DNA sequence analysis to

accommodate two ‘Platomas’ from Australia that lacked

gland cells and formed a sister lineage to the other three

genera in the family (Saunders & Kraft 2002). Since we did

not have access to suitable material of N. confusum for

molecular phylogenetic studies, we were not able to

compare it with Wetherbeella using rbcL sequences.

A comparison between N. confusum and descriptions of

Platoma suggests that this species is closely related to P.

cyclocolpum and P. chrysymenioides Gavio, Hickerson &

Fredericq (Gabriel et al. 2010). Platoma cyclocolpum has a

great morphological plasticity covering apparently distinct

morphotypes even when environmental conditions did not

vary between specimens (Huisman 1999). Phylogenetic

studies showed that specimens going under the name P.

cyclocolpum worldwide are often misidentified members of

P. chrysymenioides (Gabriel et al. 2010). The distinction

between P. cyclocolpum, P. heteromorphum, P. izunosimense

and P. chrysymenioides lies in the behaviour of the fertilised

carpogonium before fusion with the subsidiary auxiliary

cells and the origin of the connecting filament (Schils &

Coppejans 2002; Gavio et al. 2005; Gabriel et al. 2010).

Since we were unable to observe this ephemeral stage in the

slides we had access to, we suggest the new combination

Platoma confusum, transferring the species to the genus

Platoma while keeping the specific epithet.

Taxonomic conclusions

Schizymenia apoda (J. Agardh) J. Agardh 1851, p. 175

Figs 2–9

TYPE LOCALITY: Table Bay, Cape Province, South Africa.

BASIONYM: Platymenia apoda J. Agardh 1848, p. 47.

SYNONYMS: Platymenia undulata var. obovata J. Agardh

1848, p. 47 (fide Silva 1980; Silva et al. 1996).

Schizymenia obovata J. Agardh 1851, p. 175 (fide Silva

1980, Silva et al. 1996).

DISTRIBUTION: South Africa, Tristan da Cunha (Stegenga

et al. 1997), Namibia (Fredericq et al. 1996), (as S. dubyi):

Fig. 24. Global distribution patterns of Schizymenia species.

118 Phycologia, Vol. 50 (2), 2011

The Azores (Neto 1994; Tittley & Neto 1994), Madeira

(Levring 1974).

Schizymenia dubyi (Chauvin ex Duby) J. Agardh 1851, p. 169

TYPE LOCALITY: Cherbourg, Manche, Atlantic France.

BASIONYM: Halymenia dubyi Chauvin ex Duby 1830,

p. 944.

SYNONYMS: Haematocelis rubens J. Agardh 1851, pp. 496–

497 (fide Ardre 1980).

Turnerella atlantica Kylin 1930: 40 (fide Womersley &

Kraft in Womersley 1994).

Schizymenia minor (J. Agardh) J. Agardh 1851: 172 (fide

Guiry & Guiry 1990).

Haematophloea crouaniorum P.L. Crouan & H.M.

Crouan 1858, pp. 5–6 (fide Guiry & Guiry 1990).

DISTRIBUTION: Atlantic France (Feldmann 1954; Ardre

1977, 1980), Japan (Fredericq et al. 1996), Mediterranean

Sea (this paper).

Platoma confusum (Kraft & John) Gabriel & Fredericq,

comb. nov.

BASIONYM: Nemastoma confusum Kraft & John, British

Phycological Journal 11, pp. 332–335, figs. 1–9, 1976.

TYPE LOCALITY: Vernon Bank, Ghana.

DISTRIBUTION: Ghana (Lawson & John 1987; John et al.

2003, 2004).

ACKNOWLEDGEMENTS

We thank the Fundacao para a Ciencia e Tecnologia (FCT)

for PhD grant SFRH/BD/12541/2003, the SYNTHESYS

Program from the European Union for the Research Grant

NL-TAF-4691, Centro de Investigacao de Recursos Na-

turais da Universidade dos Acores (CIRN/UA) and

Direccao Regional da Ciencia e da Tecnologia (DRCT/

Acores) for the travel grants M3.2.1/I/133/2007 and M3.2.1/

I/062/2008. The National Science Foundation grants DEB-

0315995, DEB-0328491, DEB 0743024, DEB-0919508 and

DEB-0937978 are thanked for financial support. We also

would like to thank Joao Brum, Nuno Alvaro, Patrıcia

Madeira and Sandra Monteiro for their help in collecting

Azorean specimens and Ian Tittley (Herbarium NHM,

London), Willem Prud’homme van Reine (NHN, Leiden),

Olivier de Clerck (Herbarium Ghent) and other collectors

listed in Table 1 for providing vouchers used in this study.

REFERENCES

ABBOTT I.A. 1967. Studies in some foliose red algae of the Pacificcoast II. Schizymenia. Bulletin of the Japanese Society forPhycology 66: 161–174.

ADAMS N.M. 1994. Seaweeds of New Zealand. An Illustrated Guide.Canterbury University Press, Canterbury. 360 pp.

AGARDH J.G. 1842. Algae maris Mediterranei et Adriatici,observationes in diagnosin specierum et dispositionem generum.Fortin, Masson et Cie, Paris. 164 pp.

AGARDH J.G. 1848. Om de Kapska artena af slagtet Iridaea.Ofversigt af Kongelige Vetenskaps-Akademiens Forhandlingar,Stockholm 5: 46–49.

AGARDH J.G. 1851. Species genera et ordines algarum, seudescriptiones succinctae specierum, generum et ordinum, quibusalgarum regnum constituitur. Volumen secundum: algas flor-ideas complectens. Part 1. Lundae [Lund]. XII + 351 pp.

AGARDH J.G. 1878. De algis Novae Zelandiae marinis ActaUniversitatis Lundensis. Lunds Universitets Arsskrift. Afdelningenfor Mathematik och Naturvetenskap 14: 1–32.

ARDRE F. 1970. Contribution a l’etude des algues marines duPortugal. I. La flore. Portugalia Acta Biologica Series B 10:137–555.

ARDRE F. 1977. Sur le cycle du Schizymenia dubyi (Chauvin exDuby) J. Agardh (Nemastomacee, Gigartinale). Revue Algologi-que, Nouvelle Serie 12: 73–86.

ARDRE F. 1980. Observations sur le cycle de developpement duSchizymenia dubyi (Rhodophycee, Gigartinale) en culture, etremarques sur certains genres de Nemastomacees. Cryptogamie,Algologie 1: 111–140.

BERTHOLD G. 1884. Die Cryptonemiaceen des Golfes von Neapel.Fauna und Flora des Golfes von Neapel 12: 1–127.

CARAM B. & JONSSON S. 1972. Nouvelle inventaire des alguesmarines de l’Islande. Acta Botanica Islandica 1: 5–31.

COTTON A.D. 1912. Clare Island Survey. Marine algae. Proceedingsof the Royal Irish Academy 31B(15): 1–178.

CROUAN P.L. & CROUAN H.M. 1858. Note sur quelques alguesmarines nouvelles de la rade de Brest. Annales des SciencesNaturelles, Botanique 4: 69–75.

DECEW T.C., SILVA P.C. & WEST J.A. 1992. Culture studies on therelationship between Schizymenia and Haematocelis (Gigar-tinales, Rhodophyceae) from the Pacific coast of North America.Journal of Phycology 28: 558–566.

DIXON P.S. & IRVINE L.M. 1977. Seaweeds of the BritishIsles. Volume 1. Rhodophyta. Part 1. Introduction, Nemaliales,Gigartinales. British Museum (Natural History), London. 252pp.

DUBY J.E. 1830. Aug. Pyrami de Candolle Botanicon gallicum seuSynopsis plantarum in Flora gallica descriptarum. Editio secunda.Ex herbariis et schedis Candollianis propriisque digestum. Parssecunda plantas cellulares continens. Desray, Paris. 1068 pp.

FELDMANN J. 1942. Remarque sur les Nemastomacees. Bulletin dela Societe Botanique de France 89: 104–113.

FELDMANN J. 1954. Inventaire de la flore marine de Roscoff.Algues, champignons, lichens et spermatophytes. TravauxStation Biologique de Roscoff, Nouvelle Serie 6, supplement:152.

FELSENSTEIN J. 1985. Confidence limits on phylogenies: anapproach using the bootstrap. Evolution 39: 783–791.

FITCH W.M. 1971. Toward defining the course of evolution:minimal change for a specific tree topology. Systematic Zoology20: 406–416.

FREDERICQ S., SERRAO E. & NORRIS J.N. 1992. New records of redalgae from the Azores. Arquipelago 10A: 1–4.

FREDERICQ S., HOMMERSAND M.H. & FRESHWATER D.W. 1996.The molecular systematics of some agar-and carrageenan-containing marine red algae based on rbcL sequence analysis.Hydrobiologia 326/327: 125–135.

GABRIEL D., SCHILS T., NETO A.I., PARAMIO L. & FREDERICQ S.2009. Predaea feldmannii subsp. azorica (Nemastomataceae,Nemastomatales), a new subspecies of red algae from the Azores.Cryptogamie, Algologie 30: 251–270.

GABRIEL D., PARENTE M.I., NETO A.I., RAPOSO M., SCHILS T.,PARAMIO L. & FREDERICQ S. 2010. A phylogenetic appraisal ofthe genus Platoma (Nemastomatales, Rhodophyta), includinglife history and morphological observations on P. cyclocolpumfrom the Azores. Phycologia 49: 2–21.

GAVIO B. & FREDERICQ S. 2002. Grateloupia turuturu (Halymenia-ceae, Rhodophyta) is the correct name of the non-native speciesin the Atlantic known as Grateloupia doryphora. EuropeanJournal of Phycology 37: 349–360.

GAVIO B., HICKERSON E. & FREDERICQ S. 2005. Platomachrysymenioides sp. nov. (Schizymeniaceae), and Sebdenia integrasp. nov. (Sebdeniaceae), two new red algal pecies from the

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 119

northwestern Gulf of Mexico, with a phylogenetic assessment ofthe Cryptonemiales-complex (Rhodophyta). Gulf of MexicoScience 23: 38–57.

GUINDON S. & GASCUEL O. 2003. A simple, fast, and accuratealgorithm to estimate large phylogenies by maximum likelihood.Systematic Biology 52: 696–704.

GUIRY M.D. 1978. An appraisal of the Irish benthic marine algalflora. British Phycological Journal 13: 1–200.

GUIRY M.D. & GUIRY G.M. 2009. AlgaeBase. Worldwideelectronic publication, National University of Ireland, Galway.http://www.algaebase.org (11 August 2009).

HALL B.G. 2001. Phylogenetic trees made easy. Sinauer Associates,Sunderland, Massachusetts. 179 pp.

HANSEN G.I. 1989. Schizymenia dawsonii and its relation tothe genus Sebdenia (Sebdeniaceae, Rhodophyta). Taxon 38:54–59.

HARDY F.G. & GUIRY M.D. 2003. A check-list and atlas of theseaweeds of Britain and Ireland. British Phycological Society,London. 435 pp.

HUELSENBECK J.P. & RONQUIST F.R. 2001. MrBayes. Bayesianinference of phylogeny. Biometrics 17: 754–755.

HUISMAN J.M. 1999. Vegetative and reproductive morphologyof Nemastoma damaecorne (Gigartinales, Rhodophyta)from Western Australia. Australian Systematic Botany 11:721–728.

ITONO H. & TSUDA R.T. 1980. Titanophora marianensis sp. nov.(Nemastomataceae, Rhodophyta) from the Sea of Japan.Phycologia 26: 419–428.

JOHN D.M., LAWSON G.W. & AMEKA G.K. 2003. The marinemacroalgae of the Tropical West Africa Subregion. Beihefte zurNova Hedwigia 125: 1–217.

JOHN D.M., PRUD’HOMME VAN REINE W.F., LAWSON G.W.,KOSTERMANS T.B. & PRICE J.H. 2004. A taxonomic andgeographical catalogue of the seaweeds of the western coast ofAfrica and adjacent islands. Beihefte zur Nova Hedwigia 127:1–339.

KAJIMURA M. 1997. The morphology of Platoma izunosimense(Shizymeniaceae, Rhodophyta). Botanica Marina 40: 477–485.

KRAFT G.T. & JOHN D.M. 1976. The morphology and ecologyof Nemastoma and Predaea species (Nemastomataceae,Rhodophyta) from Ghana. British Phycological Journal 11:331–344.

KYLIN H. 1930. Uber die Entwicklungsgeschichte der Florideen.Lunds Universitets Arsskrift, Ny Foljd, Andra Afdelningen.26(6): 103 pp.

KYLIN H. 1956. Die Gattungen der Rhodophyceen. C.W.K.Gleerups Forlag, Lund. 673 pp.

LARKUM A.W. 1960. Botany (Algae). Azores Expedition 1959,Final Report. The Exploration Board, Imperial College ofScience and Technology, London.

LAWSON G.W. & JOHN D.W. 1987. The marine algae and coastalenvironment of tropical West Africa (second edition). Beiheftezur Nova Hedwigia 93: 1–415.

LEVRING T. 1974. The marine algae of the Archipelago of Madeira.Boletim do Museu Municipal do Funchal 28: 5–111.

LIN S.M., FREDERICQ S. & HOMMERSAND M.H. 2001. Systematicsof the Delesseriaceae (Ceramiales, Rhodophyta) based on thelarge subunit rDNA and rbcL sequences, including the Phyco-dryoideae, subfam. nov. Journal of Phycology 37: 881–899.

MADDISON D.R. & MADDISON W.P. 2000. MacClade 4: Analysis ofphylogeny and character evolution. Version 4.0. Sinauer Associ-ates, Sunderland, Massachusetts.

MASUDA M. & GUIRY M.D. 1994. The reproductive morphologyof Platoma cyclocolpum (Nemastomataceae, Gigartinales) fromGran Canaria, Canary Islands. Cryptogamie, Algologie 15:191–212.

MASUDA M. & GUIRY M.D. 1995. Reproductive morphologyof Itonoa marginifera (J. Agardh) gen. et comb. nov. (Nemas-tomataceae, Rhodophyta). European Journal of Phycology 30:57–67.

MORTON O. 1994. Marine algae of Northern Ireland. UlsterMuseum, Belfast. 123 pp.

NETO A.I. 1991. Estudo da vegetacao macrofitobentonica da costade Sao Roque, ilha de Sao Miguel, Acores. 1u Encontro Nacionalde Macroalgas Marinhas, LNETI, Lisboa 13–14 de Dezembro1990: 73–90.

NETO A.I. 1994. Checklist of the benthic marine macro algae of theAzores. Arquipelago 12A: 15–34.

NETO A.I. 1997. Studies on algal communities of Sao Miguel,Azores. PhD thesis. Universidade dos Acores, Ponta Delgada.309 pp.

NEWTON L. 1931. A handbook of the British seaweeds. BritishMuseum (Natural History), London. 478 pp.

PALMINHA F.P. 1957. Contribuicoes para o estudo das algasmarinhas portuguesas. II. (Litoral Algarvio). Boletim daSociedade Portuguesa de Ciencias Naturais Series 2 22: 68–74.

PARENTE M.I., NETO A.I. & FLETCHER R.L. 2003a. Morphologyand life history studies of Endarachne binghamiae (Scytosipho-naceae, Phaeophycota) from the Azores. Aquatic Botany 76:109–116.

PARENTE M.I., NETO A.I. & FLETCHER R.L. 2003b. Morphologyand life history studies of Scytosiphon lomentaria (Scytosipho-naceae, Phaeophyceae) from the Azores. Journal of Phycology39: 353–359.

POSADA D. & CRANDALL K.A. 1998. Modeltest: testing the modelof DNA substitution. Bioinformatics 14: 817–818.

RODRIGUEZ-PRIETO C., VERGES A., SANCHEZ N., POLO L. &VERLAQUE M. 2004. The morphology and reproductive struc-tures of Mediterranean species of the genus Nemastoma J.Agardh, nom. cons. (Nemastomataceae, Nemasomatales): Ne-mastoma dichotomum and N. dumontioides. Botanica Marina 47:38–52.

SANSON M., REYES J. & AFONSO-CARRILLO J. 1991. Contributionto the seaweed flora of the Canary Islands: new records ofFlorideophyceae. Botanica Marina 34: 527–536.

SAUNDERS G.W. & KRAFT G.T. 2002. Two new Australianspecies of Predaea (Nemastomataceae, Rhodophyta) withtaxonomic recommendations for an emended Nemastomatalesand expanded Halymeniales. Journal of Phycology 38:1245–1260.

SCHILS T. & COPPEJANS E. 2002. Gelatinous red algae of theArabian Sea, including Platoma heteromorphum sp. nov.(Gigartinales, Rhodophyta). Phycologia 41: 254–267.

SCHMIDT O.C. 1929. Beitrage zur Kenntnis der Meeresalgen derAzoren. I. Hedwigia 69: 95–113.

SEUBERT M. 1844. Flora Azorica. Adolph Marcus, Bonn.50 pp.

SILVA P.C. 1980. Remarks on algal nomenclature. VI. Taxon 29:121–145.

SILVA P.C., BASSON P.W. & MOE R.L. 1996. Catalogue of thebenthic marine algae of the Indian Ocean. University ofCalifornia Publications in Botany 79: 1–1259.

SOUTH G.R. & TITTLEY I. 1986. A checklist and distributionalindex of the benthic marine algae of the North Atlantic Ocean.British Museum (Natural History) and Huntsman MarineLaboratory, London and St. Andrews, New Brunswick, Canada.76 pp.

STEGENGA H., BOLTON J.J. & ANDERSON R.J. 1997. Seaweeds of theSouth African West Coast. Contributions from the BolusHerbarium No 18, Cape Town. 655 pp.

SWOFFORD D.L. 2003. PAUP*: phylogenetic analysis usingparsimony (and other methods). Version 4.0. Sinauer Associates,Sunderland, Massachusetts.

TITTLEY I. & NETO A.I. 1994. ‘Expedition Azores 1989’: benthicmarine algae (seaweeds) recorded from Faial and Pico.Arquipelago 12A: 1–13.

TITTLEY I. & NETO A.I. 2005. The marine algal (seaweed) flora ofthe Azores: additions and amendments. Botanica Marina 48:248–255.

TITTLEY I., NETO A.I., FARNHAM W.F. & PARENTE M.I. 2001.Additions to the marine algal (seaweed) flora of the Azores.Botanica Marina 44: 215–220.

TITTLEY I., NETO A.I. & PARENTE M.I. 2009. The marine algal(seaweed) flora of the Azores: additions and amendments 3.Botanica Marina 52: 7–14.

120 Phycologia, Vol. 50 (2), 2011

TOSTE M.F., PARENTE M.I., NETO A.I. & FLETCHER R.L. 2003a.Life history and phenology of Hydroclathrus clathratus (Scyto-siphonaceae, Phaeophyceae) in the Azores. Cryptogamie Algolo-gie 24: 209–218.

TOSTE M.F., PARENTE M.I., NETO A.I. & FLETCHER R.L. 2003b.Life history of Colpomenia sinuosa (Scytosiphonaceae,Phaeophyceae) in the Azores. Journal of Phycology 39:1268–1274.

TRELEASE W. 1897. Botanical observations on the Azores. AnnualReport of the Michigan Botanical Garden 8: 77–220.

VEIGA A.J., CREMADES J. & BARBARA I. 1998. A catalogue of themarine benthic algae of the Sisargas Islands (N.W. Iberian

Peninsula, Spain). Boletim Museu Municipal do Funchal 5,supplement: 481–493.

WOMERSLEY H.B.S. 1994. The marine benthic flora of southernAustralia – Part IIIA – Bangiophyceae and Florideophyceae(Acrochaetiales, Nemaliales, Gelidiales, Hildenbrandiales andGigartinales sensu lato). Australian Biological Resources Study,Canberra. 508 pp.

Received 20 August 2009; Accepted 7 June 2010

Associate editor: Juliet Brodie

Gabriel et al.: Schizymenia sp. in the Azores and ‘Nemastoma’ confusum 121