Phycological Research 2004; 52: 224–234
Phylogenetic study of the Nemaliales (Rhodophyta) based on
large-subunit ribosomal DNA sequences supports segregation
of the Scinaiaceae fam. nov. and resurrection of Dichotomaria
Lamarck
John M. Huisman,1* James T. Harper2,3 and Gary W. Saunders2
School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia 6150, Australia,
Centre for Environmental and Molecular Algal Research, Department of Biology, University of New Brunswick, Fredericton,
New Brunswick, E3B 6E1, and 3Canadian Institute for Advanced Research, Department of Botany, University of British
Columbia, Vancouver, British Columbia, V6T 1Z4, Canada
1
2
INTRODUCTION
SUMMARY
Gene sequence data have been newly obtained for 18
species in 13 genera of the order Nemaliales (Rhodophyta), allowing for the first time a relatively comprehensive molecular phylogenetic appraisal of the order.
The phylogenetic trees generated from these data support
the recognition of three families: (i) the Liagoraceae as
presently constituted; (ii) a reduced Galaxauraceae
including Actinotrichia, Galaxaura (sensu lato), and
Tricleocarpa; and (iii) a new family, Scinaiaceae,
segregated from the Galaxauraceae and including the
genera Scinaia, Gloiophloea, Nothogenia, and probably
Whidbeyella. The four genera of the Scinaiaceae differ
from the newly circumscribed Galaxauraceae in being
uncalcified, and having heteromorphic life histories in
which the tetrasporophyte is much reduced and filamentous or crustose. This type of life history is found
in only Tricleocarpa of the Galaxauraceae. The results
also show Galaxaura to be para/polyphyletic if Actinotrichia and Tricleocarpa are recognized. To remedy this,
the Galaxaura marginata species complex, Galaxaura
diesingiana, and Galaxaura obtusata are removed from
the genus and placed in the resurrected Dichotomaria
Lamarck. Galaxaura marginata, presently thought to be
wide-ranging and morphologically variable, is shown to
comprise several species. As a consequence, Galaxaura
tenera Kjellman and Brachycladia australis Sonder are
removed from the synonymy of G. marginata and
restored as independent species in Dichotomaria for
South African and Australian isolates, respectively. The
Liagoraceae is shown to encompass genera previously
placed in the segregate families Nemaliaceae and
Dermonemataceae, and the value of the reproductive
characters used to define those taxa is discussed.
Key words: Dichotomaria, Galaxauraceae, Galaxaura
marginata, Liagoraceae, Nemaliales, phylogeny, Scinaiaceae fam. nov.
The order Nemaliales (as Nemalionales) was erected by
Schmitz (1892) as one of the original four orders of the
subclass Florideophycidae (the higher red algae), the
others being the Gigartinales, Cryptonemiales, and Rhodymeniales. The order was characterized by relatively
simple postfertilization development in which the gonimoblast phase developed directly from the zygote
(postfertilization carpogonium), in contrast to the other
orders in which the zygote nucleus was first transferred
to an auxiliary cell (a specialized cell unique to the red
algae) from which the gonimoblast then arose. From
this relatively simple beginning, the Nemaliales has
subsequently experienced a taxonomic history that ‘has
been a complex series of proposals, counter-proposals,
and vigorous arguments, with various taxonomists
holding wildly differing views’ (Maggs 2002). The various
circumscriptions of the Nemaliales since Fritsch (1945)
are shown in Figure 1.
Initially, the Nemaliales included both uniaxial and
multiaxial taxa, the former within the families Acrochaetiaceae, Gelidiaceae, Bonnemaisoniaceae and Naccariaceae. The first three of these families are now
generally accorded ordinal status, as Acrochaetiales,
Gelidiales, and Bonnemaisoniales, respectively. The
ordinal placement of the Naccariaceae is still questionable. Most treatments place it in the Bonnemaisoniales
(e.g. Womersley 1996), but some authors (e.g. Abbott
1999) include it in the Gigartinales. Schils et al.
(2003) suggest that the family is not monophyletic and
its ordinal placement is yet to be resolved.
As presently constituted, the Nemaliales is restricted
to multiaxial taxa, which have been variously distributed into families. Those with a cohesive cortex and
*To whom correspondence should be addressed.
Email: [email protected]
Communicating editor: G. C. Zuccarello.
Received 1 May 2003; accepted 15 March 2004.
Phylogeny of the Nemaliales
225
Fig. 1. Major changes to the composition of the Nemaliales since Fritsch (1945), proposed by Kylin (1956), Dixon (1973), Dixon (1982)
and Garbary and Gabrielson (1990). Shaded taxa are excluded from the order. 1Orthography discussed by Nicolson and Norris (1983).
Elevated to ordinal status by Desikachary (1964), a move largely ignored. 3Name proposed by Parkinson (1983: 608) to replace Chaetangiaceae. 4Proposed by Feldmann (1953: 12). 5Proposed by Harper & Saunders (2002: 471). 6Proposed by Pueschel & Cole (1982: 717).
7Not mentioned, but presumably recognized. 8Proposed by Müller et al. (2002: 819). 9Proposed by Feldmann and Feldmann (1942: 163).
10According to Schils et al. (2003: 54) the Naccariaceae is not monophyletic and its ordinal placement is yet to be resolved. 11Proposed by
Kylin (1923: 132).
2
distinct pericarp (the genus Galaxaura and close relatives) are placed in the Galaxauraceae (previously
Chaetangiaceae). Members of this family share the
seemingly apomorphic character of the production of
nutritive cells from the hypogynous cell of the carpogonial branch, and have been regarded as clearly delineated (Kraft 1989). The subdivision of the remainder of
the Nemaliales is controversial, with various authors
recognizing either one family (the Liagoraceae, e.g.
Kraft 1989) or up to three (the Nemaliaceae, Liagoraceae, and Dermonemataceae, e.g. Abbott 1976; Dixon
1982; Abbott 1999). As yet there is no consensus.
Members of the Nemaliales occur almost worldwide,
from the sub-Antarctic waters of Macquarie Island
(Nothogenia Montagne, see Ricker 1987) to all tropical
seas. The order is at its most diverse in warmer waters,
however, where numerous species of Galaxaura Lamouroux, Liagora Lamouroux and Ganonema Fan et
Wang can be found. A wide variety of pre and postfertilization processes has resulted in the descriptions of
numerous genera based on very precise reproductive
events (e.g. Abbott & Doty 1960; Abbott 1970,1976;
Yoshizaki 1987; Kraft 1989; Huisman & Borowitzka
1990; Huisman & Kraft 1994; Huisman & Schils
2002), and many genera have been recently monographed (Huisman 1986, 2002; Huisman et al. 2004).
Despite the abundance of morphological information
regarding the Nemaliales, there is still some disagreement regarding both what is encompassed by the order
and the arrangement of its constituent families.
Our objective in the present study was to use
sequence data to provide the first molecular examination of phylogenetic relationships within the Nemaliales.
MATERIALS AND METHODS
Collection information for specimens used in the
present study is provided in Table 1. Samples were
field-dried in silica gel and DNA was subsequently
extracted as outlined previously (Saunders 1993). The
large subunit (LSU) ribosomal DNA (rDNA) was
polymerase chain reaction (PCR)-amplified using the
primer combinations outlined in Harper and Saunders
(2001) with the following exceptions. The 3′ region of the
LSU (Z fragment of Harper and Saunders) was difficult
to amplify for most members of the Galaxauraceae and
the resulting data were usually incorrect (sequence
from liagoracean taxa and marine invertebrates generally resulted). We therefore designed a specific primer
Nem1 (5′-GTTGGCTCTAGTGGAGCGGG-3′) to replace
T05 of Harper and Saunders (2001) for amplification
of this region. More remarkably, six members of the
Galaxauraceae sequenced here (see Results) had large
(approximately 2 kb) inserts in the 3′ region of the
LSU, rendering amplification and sequencing of this
region difficult for these taxa. The following primers
were therefore established within the insert to amplify,
and in a few cases sequence, this region for the problem
taxa: forward Scin1 (5′-AGGTTCATCGACTTGACGG-3′)
and Tricleo1 (5′-TGCTGCAATGGGGTTCAAGG-3′); and
226
Table 1.
J. M. Huisman et al.
Collection information and voucher number for the samples newly sequenced in the present study
Taxon name
Voucher number Collection information
GenBank
Galaxauraceae
Actinotrichia fragilis (Forsskål) Børgesen
GWS000151
AY570363
Galaxaura diesingiana Zanardini
KZN 2291
Galaxaura marginata (Ellis et Solander)
Lamouroux
Galaxaura marginata South Africa
DLB 5987
GWS001052
Ningaloo Reef, Western Australia, Australia.
17.viii.1995. JMH
The Bluff (Treasure Beach), Durban, South Africa.
15.vi.2003. O. De Clerck & F. Leliaert.
Turrumote Reef, La Parguera, Puerto Rico
11 m; 20.x.2003. Hector Ruiz.
Isipingo, South Africa. 16.vi.2003. O. De Clerck &
F. Leliaert.
Rupert’s Reef, Lord Howe, Australia. 13.iii.2001. GWS
AY570366
GWS000143
Barrow I., Western Australia, Australia. 28.xi.1995. JMH
AY570368
GWS001463
GWS001659
IA 30099
Bicheno, Tasmania, Australia. 25.xi.2002. GWS
Bamfield, British Columbia, Canada. 16.v.2003. GWS
Ma’ili, O’ahu, Hawaiian Islands, USA. 2.iv.2003. JMH
AY570379
AY570380
AY570369
Liagoraceae
Dotyophycus abbottiae Kraft
G0404
Ganonema borowitzkae Huisman
GWS000148
Helminthocladia australis Harvey
G0039
Helminthora australis J. Agardh ex.Levring
MURU JB 629
Anemone Mound, Easter Group, Abrolhos I., Western
AY570370
Australia, Australia. 10.xi.1995. G.T. Kraft & GWS.
Surf Pt., Barrow I., Western Australia, Australia. 10.ii.1997. AY570371
JMH.
Port MacDonnell, South Australia, Australia. 30.xi.1991.
AY570372
G.T. Kraft & GWS.
South of Cervantes, Western Australia, Australia. 29.x.2000. AY570373
JMH
Anemone Lump, Abrolhos I., Western Australia, Australia. AY570374
2.ii.1997. JMH.
Abrolhos I., Western Australia, Australia. 3.x.1995. JMH. AY570375
Bamfield, British Columbia, Canada. A. Henderson
AY570376
Galaxaura obtusata (Ellis et Solander)
Lamouroux
Galaxaura rugosa (Ellis et Solander)
Lamouroux
Nothogenia fastigiata (Bory) Parkinson
Scinaia confusa (Setchell) Huisman
Tricleocarpa cylindrica (Ellis et Solander)
Huisman et Borowitzka
KZN 2317
Liagora mannarensis Krishnamurthy et
GWS000147
Sundararajan
Liagora valida Harvey
GWS000149
Nemalion helminthoides (Velley in Withering)
Batters
Patenocarpus paraphysiferus Yoshizaki
Yamadaella caenomyce (Decaisne) Abbott
GWS000152
AY570364
AY570365
AY570367
Malus I., Dampier Archipelago, Western Australia, Australia AY570377
27.viii.1999. JMH
Eagles Nest, Barrow I., Western Australia, Australia.
AY570378
26.xi.1995. JMH.
JMH, John M. Huisman; GWS, Gary W. Saunders.
reverse Scin2 (5′-TGTGCGCGGGATTGCAGCAC-3′), Scin3
(5′-AGCTTACGCTGCGGCCTGACT-3′) and Tricleo2 (5′CGACGGATCGAACGCGGTTC-3′).
The PCR products were agarose gel-purified with the
WizardTM PCR Preps DNA Purification System (Promega,
Madison, WI, USA) following the manufacturer’s protocol. DNA Sequencing was completed with the dRhodamine Terminator Cycle Sequencing Ready Reaction
Kit (PE Applied Biosytems (ABI), Foster City, CA) and
data were collected with the ABI PRISM 3100 Genetic
Analyzer.
The LSU sequences determined here were added to
an alignment of 13 previously published sequences
representing orders of the florideophyte ANP (Acrochaetiales/Nemaliales/Palmariales) complex (Saunders et al.
1995; Harper & Saunders 2002). The taxa included:
Acrochaetiales – Acrochaetium secundatum (Lyngbye)
Nägeli (AF528044), Audouinella hermanii (Roth) Duby
(AF419102), Rhodochorton purpureum (Lightfoot)
Rosenvinge (AF419103) and Rhodochorton tenue Kylin
(AF421126); Colaconematales – Colaconema dasyae
(Collins) Stegenga, I. Mol, Prudhomme van Reine et
Lokhorst (AF419100), Colaconema daviesii (Dillwyn)
Stegenga (AF528047), Colaconema endophyticum
(Batters) J.T. Harper et G.W. Saunders (AF419101)
and Colaconema rhizoideum (K.M. Drew) P.W. Gabrielson
(AF528050); Palmariales – Halosaccion glandiforme
(Gmelin) Ruprecht (AF528052), Palmaria palmata
(Linnaeus) Küntze (Y11506) and Rhodophysema elegans
(P. et H. Crouan ex J. Agardh) Dixon (AF419140); and
Nemaliales – Cumagloia andersonii (Farlow) Setchell et
Gardner (AF419137) and Galaxaura marginata (Ellis
et Solander) Lamouroux (AF419138).
The resulting alignment contained 31 taxa and
2892 sites (excluding the large inserts in six of the
Galaxauraceae) of which 222 were excluded. Modeltest
(v 3.06; Posada & Crandall 1998) was used to determine that a general time reversible model with a
gamma distribution and invariant sites was most appropriate for these data. The program MrBayes (v. 2.01;
Huelsenbeck & Ronquist 2001) was used to complete
Bayesian inference of phylogeny under this model.
Phylogeny of the Nemaliales
227
Fig. 2. Phylogenetic tree produced by Bayesian inference including posterior probabilities (top value), as well as bootstrap support under
minimum evolution (middle value) and unweighted parsimony (lower value). Asterisk indicates branches with 100% support in all analyses;
branches with a single value lacked bootstrap support under distance and parsimony; value in bold indicates that in distance analyses
Nothogenia and Scinaia were a sister group to the other included Nemaliales with 79% support.
Four Markov chains were used, the temperature was set
to 0.2 and 106 generations were run with sampling
every 100 generations. Log-likelihood values stabilized
around 22 000 generations and we used the final
6000 trees (4000 burn-in) to calculate the posterior
probabilities. Distance analyses used the parameters
determined in Modeltest and trees were constructed
under minimum evolution (100 random additions) in
the computer program PAUP 4.0b10 for the Macintosh
(Swofford 2001). Parsimony analyses were completed
under a heuristic search with 100 random additions,
all characters equally weighted, gaps treated as
missing data, and the Tree Bisection-Reconnection
branch swapping option in effect. Distance and parsimony analyses were subjected to bootstrap resampling
(2000 replicates with random additions set to 10 in
both cases) to estimate robustness of branches
(Felsenstein 1985).
228
RESULTS
The LSU region amplified herein for members of the
Nemaliales generally ranged from 2681 bp in Yamadaella to 2806 bp in Galaxaura obtusata. Exceptions
occurred for six galaxauracean taxa, which contained a
large (approximately 2 kb) insert in the 3′ region of the
LSU: G. marginata (Puerto Rico; insert not sequenced
(INS)), G. marginata (South Africa; INS), G. diesingiana
(INS); Nothogenia (INS); Scinaia (1968 bp); and Tricleocarpa (2070 bp). These inserts are likely Group I
introns and it is interesting to note that Nothogenia is
to our knowledge only the second florideophyte genus
(Saunders, unpubl. data 2003) for which this type of
intron is reported in the small subunit (SSU) (Hildenbrandia is the other; cf. Müller et al. 2001). Hildenbrandia also contains a putative Group I intron in its
LSU (Harper & Saunders 2001), suggesting that there
is a correlation in red algae for occurrence of Group I
introns in the SSU and LSU, a hypothesis that may be
best tested in the Galaxauraceae.
Phylogenetic trees determined here were largely
congruent for all three methods of analyses used and
only the result from Bayesian inference is presented
(Fig. 2). The Nemaliales was solidly monophyletic relative to the three outgroup orders included, and resolved
as three strongly supported lineages; that is, the
Liagoraceae (including Nemalion), a Nothogenia/Scinaia
clade, and the Galaxauraceae sensu stricto. Unweighted
parsimony resulted in 35 trees (length = 851 steps;
consistency index = 0.572; retention index = 0.784)
and differed only in failing to resolve relationships
among most included members of the Liagoraceae, and
in failing to resolve relationships among the three
major lineages of the Nemaliales (Fig. 2). Within the
Liagoraceae the genus Nemalion resolved as an early
divergence relative to the other included genera, and
Liagora mannarensis failed to join its congener Liagora
valida. Otherwise, relationships were weakly resolved
within this family. Galaxaura, Galaxauraceae, also failed
to form a monophyletic group. Galaxaura rugosa was a
close sister to Actinotrichia, this lineage a sister to
Tricleocarpa, whereas the remaining isolates of Galaxaura formed a monophyletic sister lineage to the former
group. Within this latter lineage, however, the three
isolates of G. marginata from different geographic locations failed to form a lineage and had relatively high
levels of LSU divergence, indicating that they are
probably not a single species.
DISCUSSION
The trees generated by our analyses clearly indicate
that the Nemaliales forms a strongly supported, monophyletic clade. Within the order, three lineages can be
recognized: the Liagoraceae (sensu lato, including the
Dermonemataceae and probably the Nemaliaceae), and
J. M. Huisman et al.
two lineages including the genera previously comprising the Galaxauraceae. One of these, the Galaxauraceae sensu stricto, includes Galaxaura, Actinotrichia
and Tricleocarpa; although the first-mentioned genus
was not monophyletic. The second lineage includes
Scinaia and Nothogenia, which are essentially the
uncalcified members of the family (Huisman 1985;
Huisman 1986; Huisman & Womersley 1992). Therefore, we propose recognition of this second lineage at
the familial level, as the Scinaiaceae fam. nov.
Scinaiaceae Huisman, J.T. Harper et G.W.
Saunders, fam. nov.
Thalli recti, non-calcarii, dichotome vel subdichotome
(raro irregulariter) ramosi. Axes teretes vel compressi.
Structura multiaxialis; medulla filamentibus longitudinalibus, filamenta assimilantia anticlinalia subdichotome
ramosa gerentibus corticem formantia composita; cortex
filamentosus, vel pseudoparenchymatus remanens.
Spermatangia in cellulis exterioribus vel in cavitatibus
gerentia. Rami carpogoniales in filamentibus interioribus corticalibus portati, 3-cellulosi; cellula hypogyna
cellulis nutritoriis praedita. Gonimoblasta ab carpogonio statim evoluta. Cystocarpi in medulla exteriori
portati,-non-protrusi, filamentibus gonimoblastis et
carposporangiis terminalibus instructi, maturitate pericarpio distincto e filamentibus ab cellula basali ramosi
carpogonialis formato. Tetrasporophyta (ubi cognita) vel
filamentosa (Scinaia, Gloiophoea) vel crustosa (Nothogenia), tetrasporangiis cruciatim divisis instructa.
Thalli erect, uncalcified, dichotomously or subdichotomously branched, rarely irregular. Axes terete or compressed. Structure multiaxial; medulla of longitudinal
filaments bearing anticlinal, subdichotomously branched
assimilatory filaments forming a cortex; cortex remaining filamentous or becoming pseudoparenchymatous.
Spermatangia borne on outer cortical cells or within
cavities. Carpogonial branches on inner cortical filaments,
3-celled, hypogynous cell bearing nutritive cells. Gonimoblast developing directly from carpogonium. Cystocarps within outer medulla, not protuberant, with
branched gonimoblast filaments and terminal carposporangia, when mature with a distinct pericarp formed from
filaments arising from the basal cell of the carpogonial
branch, ostiolate. Tetrasporophytes (where known) either
filamentous (Scinaia, Gloiophloea) or crustose (Nothogenia), with cruciately divided tetrasporangia.
Type genus: Scinaia Bivona-Bernardi
In addition to Scinaia and Nothogenia we also
tentatively include Gloiophloea and Whidbeyella, the
uncalcified genera not examined in the present study.
The morphology, reproduction and life history of Gloiophloea were examined by Huisman (1985, 1987) and
based on those studies the genus is clearly aligned
with the new family. Whidbeyella is in need of a critical
Phylogeny of the Nemaliales
re-examination, but for the moment placement in the
Scinaiaceae appears to be the most appropriate.
Within the Nemaliales, the Scinaiaceae are characterized by an uncalcified thallus with a consolidated
cortex, production of distinct pericarp, and spermatangia arising in surface sori (Scinaia, Gloiophloea) or
in small surface pits (Nothogenia). However, spermatangial characteristics have not been recorded for
Nothogenia fastigiata (Bory) Parkinson, the type of the
genus and the species used in the present study.
Descriptions of spermatangia for Nothogenia are mostly
derived from the study of Martin (1936), who examined Nothogenia ovalis (Suhr) Parkinson (as Chaetangium saccatum J. Agardh).
One of the more surprising outcomes of the present
study is the indication that the Scinaiaceae is an early
divergence in the Nemaliales, and possibly sister to the
Liagoraceae. Kraft (1989, p. 300) suggested that the
Galaxauraceae (which, at the time, included the genera
of the Scinaiaceae) displayed a: ‘suite of shared unique
characters … that seem highly unlikely as plesiomorphic
conditions’. He then postulated that the Galaxauraceae
might be: ‘derived from, rather than a sister family to,
the Liagoraceae’ (Kraft 1989, p. 300). Perhaps the
most distinctive feature of the Galaxauraceae (sensu
lato) is the production of 3-celled carpogonial branches
bearing sterile laterals on the hypogynous and basal
cells, with those on the hypogynous cell seemingly with
the uniform function of providing nutrition to the developing carposporophyte. Carpogonial branches in the
Liagoraceae, however, display a variety of morphologies,
with some being very simply constructed and unbranched.
Kraft’s proposals were, therefore, intuitively agreeable as
the condition in the Galaxauraceae was both uniform
and seemingly derived; that of the Liagoraceae, at least
in part, simple and seemingly primitive. The results of
the present study, however, indicate that this might not
be the case.
The genera of the Galaxauraceae
Within the Galaxauraceae, G. rugosa (Ellis et Solander)
Lamouroux (the type of the genus) forms a clade with
Actinotrichia (represented by the type, A. fragilis (Forsskål) Børgesen). This is not a surprising result, as the
two taxa share many character states, including terete
thalli and tetrasporangia borne on elongate surface
filaments (Huisman & Borowitzka 1990; Wang &
Chiang 2001). Although clearly closely related, Actinotrichia and Galaxaura should be maintained as separate genera based on the structural differences
between the tetrasporophyte and gametophyte phases
of Galaxaura, as opposed to the isomorphic life history
of Actinotrichia. In addition, the morphology of the
cystocarp in the two genera differs (Wang & Chiang
2001, table 1). The clade formed by G. rugosa and
229
A. fragilis is sister to Tricleocarpa cylindrica (Ellis et
Solander) Huisman et Borowitzka, again the type of the
genus.
Galaxaura marginata (Ellis et Solander) Lamouroux,
G. obtusata (Ellis et Solander) Lamouroux, and
G. diesingiana Zanardini, however, lie on a separate
branch from that containing G. rugosa, Actinotrichia
and Tricleocarpa, resulting in Galaxaura being para/
polyphyletic as presently constituted. To remedy this,
we advocate the segregation of these three species at
the generic level. Reproductive features of these
species that have not been emphasized at this level
include the production of tetrasporangia laterally or
terminally on stalk cells of epidermal cells, rather than
on elongate filaments as in G. rugosa. In addition,
these species have a tetrasporophyte cortex with
stalked epidermal cells, as opposed to the filamentous
sporophyte cortex of G. rugosa.
Several names are potentially available for this
segregate genus, for which we are selecting
G. marginata as the type. Corallina marginata (Ellis &
Solander 1786, p. 115, pl. 22, fig 6) has been placed
in five different legitimate genera in addition to Galaxaura (Dichotomaria Lamarck, Alysium C. Agardh, Holonema Areschoug, Brachycladia Sonder, and Microthoe
(Decaisne) Harvey). The earliest available name is
Dichotomaria (Lamarck 1816). As neither it nor Galaxaura (Lamouroux 1812) were originally typified, both
names remain legitimate regardless of lectotypification. Galaxaura was lectotypified with G. rugosa (Ellis
et Solander (Lamouroux 1816)) (Corallina rugosa (Ellis
& Solander 1786, 1786, p. 115, pl. 22, fig 3)) by
Schmitz (1889). Dichotomaria has remained untypified. Therefore, we lectotypify the name Dichotomaria
with D. marginata (Ellis et Solander) Lamarck, rendering it the correct name for the genus that includes
Corallina marginata.
In line with this, we also propose the following
corrected generic description:
Dichotomaria Lamarck
Thalli calcified, subdichotomously branched, occasionally with proliferations. Axes terete or flattened, occasionally with a terete, hirsute, basal portion. Medulla
filamentous. Cortex of gametophyte mostly three layered, inner 1–2 of large hyaline cells that often fuse
laterally, outer of smaller, pigmented cells; cortex of
tetrasporophyte pseudoparenchymatous, 3–6 layered,
inner 1–3 of large hyaline cells, outer borne on
pigmented stalk cells. Spermatangia in cavities. Carpogonial branches arising in place of a normal vegetative
filament. Pre-fertilization hypogynous cell with 3–4
nutritive branches and basal cell with 3–4 small-celled
sterile branches. Gonimoblast initials arise from the
carpogonium and radiate outwards, some growing laterally then distally, forming the wall of the cystocarp.
230
Table 2.
J. M. Huisman et al.
New taxa and nomenclatural changes resulting from the present study
Scinaiaceae Huisman, J.T. Harper et G.W. Saunders, fam. nov.
Type Genus: Scinaia. Other genera included: Gloiophloea, Nothogenia, Whidbeyella
Dichotomaria australis (Sonder) Huisman, J.T. Harper et G.W. Saunders, comb. nov.
Basionym: Brachycladia australis Sonder (1855) (Plantae Muellerianae). Algae annis 1852 et 1853 collectae. Linnaea 26: 514.
Type: Wilson’s Promontory, Victoria, Australia, May 1853.
Dichotomaria diesingiana (Zanardini) Huisman, J.T. Harper et G.W. Saunders, comb. nov.
Basionym: Galaxaura diesingiana Zanardini (1846) Del vero posto che alle Galaxaure si compete nella serie dei vegetabili marini.
Giornale Botanico Italiano, Anno 2, 1(1): 51. Type: Port Natal, South Africa.
Dichotomaria lenta (Kjellman) Huisman, J.T. Harper et G.W. Saunders, comb. nov.
Basionym: Galaxaura lenta Kjellman (1900). Om Floridé-släget Galaxaura, dess organografi och systematik. Kongl. Svenska
Vetenskaps-Akademiens Handlingar [ser. 4] 33 (1): 70, pl. 19, figs 28–30, pl. 20, fig. 43. Type: Sri Lanka, fragment in University of
California Herbarium, Berkeley (UC) (fide Papenfuss et al. 1982). Dichotomaria lenta has a cortical and tetrasporangial arrangement
similar to that of Dichotomaria marginata (Papenfuss et al. 1982), but has terete branches.
Dichotomaria tenera (Kjellman) Huisman, J.T. Harper et G.W. Saunders, comb. nov.
Basionym: Galaxaura tenera Kjellman (1900). Om Floridé-släget Galaxaura, dess organografi och systematik. Kongl. Svenska
Vetenskaps-Akademiens Handlingar [ser. 4] 33 (1): 77–78, pl. 14, figs 10–19, pl. 20, fig. 32. Lectotype: Mombasa, Kenya
(fide Papenfuss and Chiang 1969).
Mature cystocarps with a central fusion cell. Carposporangia terminal on gonimoblast filaments that project
towards the center of the cavity. Tetrasporangia lateral
on stalk cells of epidermal cells or terminal on epidermal cells, cruciately divided.
Type: Dichotomaria marginata (Ellis et Solander)
Lamarck
Heterotypic synonym: Brachycladia (Sonder, 1855)
Type species: Brachycladia australis Sonder
A possible type specimen of Brachycladia australis
was referred to G. marginata by Huisman and Borowitzka (1990), but the present study has shown it to be
an independent species (see below).
Of the species originally included by Lamarck in
Dichotomaria, we include Dichotomaria marginata and
Dichotomaria obtusata (Ellis et Solander) Lamarck, and
exclude Dichotomaria rugosa (= G. rugosa), Dichotomaria
lapidescens (probably also = G. rugosa) and D. fragilis
(= Tricleocarpa fragilis) (Linnaeus) Huisman et Townsend.
Additional species not included by Lamarck but referred
to Dichotomaria herein are: Dichotomaria australis
(Sonder) comb. nov., Dichotomaria diesingiana (Zanardini) comb. nov., Dichotomaria lenta (Kjellman) comb.
nov., and Dichotomaria tenera (Kjellman) comb. nov.
(see Table 2).
As our sequence data represent only a small sample
of the species presently included in Galaxaura, we have
a limited data set to establish the morphological
features that might characterize Dichotomaria. Given
the close association of G. rugosa and Actinotrichia,
two taxa in which tetrasporangia are borne laterally or
terminally on relatively long cortical filaments, and the
production of tetrasporangia on much reduced epidermal cells in all species herein referred to Dichotomaria,
we are proposing that this be the defining feature of
the genus. The Dichotomaria sporangial arrangements
were described by Svedelius (1942) as pleurosporangiataetypus (where the sporangia are lateral) and acrosporangiatae-
typus (where the sporangia are terminal), and are found
in many species. Given this, it is likely that the majority
of species presently included in Galaxaura are more
appropriately referred to Dichotomaria. In line with this
we are proposing several new combinations, but have
restricted ourselves to species that we have either
examined personally or for which the type description
is sufficiently detailed to allow unequivocal placement
in Dichotomaria. We have also only proposed nomenclatural changes for currently recognized species. Our
results with G. marginata, however, indicate that many
names presently in synonymy might be resurrected
after further study.
The Galaxaura marginata complex
Initiated by Papenfuss et al. (1982), and followed by
subsequent authors (e.g. Huisman & Borowitzka 1990),
was the move to regard G. marginata as a widespread,
pan-tropical species with a broad range of external
morphologies and internal structure. That this is an
artificial arrangement is shown by the position of the
G. marginata specimens included in our analysis. We
have generated new sequences from specimens referable to this species from Puerto Rico and South Africa,
and these are compared to existing sequences from
Australian material. As shown in Figure 2, Australian
G. marginata forms a strongly supported clade with
South African G. diesingiana, the latter also a flattened
species but clearly demarcated with a distinctive morphology (epidermal cells are borne singly on stalk cells,
as opposed to the paired cells in G. marginata). South
African G. marginata forms a clade with Puerto Rican
G. marginata, but with relatively high levels of LSU
divergence, indicating that they might not be conspecific.
So what, then, is true G. marginata? Unfortunately
the type specimen of Corallina marginata Ellis et
Solander is lost, and the species is lectotypified by an
Phylogeny of the Nemaliales
illustration that shows a flattened habit, but no further
detail. The type locality of the species is in the
Bahamas and, fortunately, there appears to be only one
flattened species recorded from the region. Børgesen
(1915) gives a detailed account of the morphology of
G. marginata from the West Indies, based on tetrasporophyte specimens. In the same publication he
describes a new species, G. occidentalis, but this
species clearly represents the gametophyte phase of
G. marginata (as suggested by Howe 1918). Littler and
Littler (2000) depict the cortical structures of gametophytes and tetrasporophytes of G. marginata, with the
latter agreeing precisely with Børgesen’s description of
G. occidentalis. Kjellman (1900) reported several flattened species from the region and these were subsequently also included in Taylor’s marine flora (1960);
all have been referred to G. marginata by Wynne
(1998). Schneider (2003) also records only G. marginata
from the Bermuda Islands. From these accounts it
seems reasonable to conclude that only one flattened
species, G. marginata, occurs in the Caribbean region.
All descriptions of G. marginata (some admittedly,
seemingly rehashing that of Børgesen) highlight several
features that can probably be used to distinguish the
species: (i) not all plants are distinctly flattened, some
are terete (Børgesen 1915); and (ii) the outer epidermal cells in tetrasporophytes are often apiculate
(Børgesen 1915, p. 107, fig. 116; Littler & Littler
2000). Our Puerto Rican G. marginata agrees with
descriptions of this species in the Caribbean region
(including the possession of apiculate epidermal cells);
therefore, we feel confidant that what we have used in
the present study is true G. marginata.
With regard to G. marginata from other locations,
the Australian specimen does not group with Puerto
Rican G. marginata and is clearly a different species.
This specimen was collected from south-eastern Australia in Victoria, type locality of B. australis (Sonder
1855), a species usually synonymized with G. marginata.
This would appear to be the earliest name available for
this entity (and probably also includes Galaxaura laxa)
(Kjellman (1900)). This species can be distinguished
morphologically from G. marginata in its typically flattened thallus and lack of apiculate epidermal cells.
Therefore, we herein resurrect Sonder’s name and
propose the combination D. australis (Sonder) Huisman, J.T. Harper et G.W. Saunders, comb. nov. (see
Table 2).
The situation regarding the South African G. marginata
is less clear. The entity forms a clade with Puerto
Rican G. marginata and has terete lower branches, but
differs from G. marginata in lacking apiculate epidermal cells. In addition, there are some differences in
LSU sequences between the South African and Puerto
Rican specimens, which suggests that they are separate species. While our results do not unequivocally
prove that the African entity is an independent species,
231
we feel that the sequence differences, plus some
morphological features, provide support for its recognition. The specimen used in the present study was
collected from the east coast of South Africa, at Natal.
Presently regarded as synonymous with G. marginata
are four flattened species described by Kjellman
(1900) with type localities in eastern Africa and
Madagascar: Galaxaura clavigera (Kjellman 1900),
Galaxaura tenera (Kjellman 1900), Galaxaura ventricosa
(Kjellman 1900) and Galaxaura veprecula (Kjellman
(1900). It is likely that these species are synonymous
with one another (Papenfuss et al. 1982). Since all of
the Kjellman names have equal priority, herein we
adopt the most widely used, G. tenera. Prior to Papenfuss et al. (1982) synonymizing all four species with
G. marginata, Papenfuss and Chiang (1969) stopped
just short of doing so and regarded them all as
representing Kjellman’s G. tenera. Interestingly, in
neither the descriptions by Kjellman of these species,
nor the description provided by Papenfuss and Chiang
(1969) of G. tenera, is there mention of apiculate
epidermal cells, considered herein to be characteristic
of G. marginata. Therefore, we regard the east African
entity as a separate species for which the name
G. tenera appears to be the most appropriate. In line
with this we propose the combination D. tenera (Kjellman) Huisman, J.T. Harper et G.W. Saunders, comb.
nov. (see Table 2). A detailed examination of a range of
African specimens is desirable, however, to test the
validity of our scheme and to establish the exact
application of Kjellman’s names.
The Liagoraceae
The separation of the genera in the Liagoraceae clade
is less immediately obvious. The family has, in the past
and also presently by some authors (Abbott 1976,
1999), been divided into three families: the Dermonemataceae, the Liagoraceae, and the Nemaliaceae,
based on features of the carpogonial branch and
mature cystocarp. The Nemaliaceae is characterized by
compact gonimoblasts and carpogonial branches being
modified vegetative filaments, the Liagoraceae by
accessory carpogonial branches, and the Dermonemataceae by diffuse gonimoblasts (Abbott 1976).
These families were discussed by Kraft (1989), who
felt it was not possible to satisfactorily subdivide the
group and suggested that a broadly defined Liagoraceae was more appropriate.
Genera from the three families are represented in
the present tree, but do not cluster along familial lines.
Cumagloia Setchell et Gardner, Dotyophycus Abbott,
Patenocarpus Yoshizaki, and Yamadaella Abbott are
regarded as members of the Dermonemataceae; Nemalion Duby is a member of the Nemaliaceae, and the
remaining genera are included in the Liagoraceae. The
recognition of the Dermonemataceae is clearly not
232
supported by the sequence data, as its four genera
arise in separate branches of the tree and are closely
aligned with genera with compact gonimoblasts. Evidence for the Nemaliaceae is equivocal, as only one of
the included genera is representative of that family. It
occupies a separate branch, but further data are
required before any clear divisions can be inferred.
Therefore, the sequence data suggest, as did Kraft
(1989), that the recognition of three families cannot
be supported and only the single family Liagoraceae is
warranted at this stage.
What conclusions, if any, can be drawn from the
topology of the tree? The first is that many of the
characters used in the delineation of genera (accessory
vs nonaccessory carpogonial branches, compact vs
spreading gonimoblasts) are of little use in characterizing higher-level relationships. If one regards nonaccessory carpogonial branches as the ancestral state, then
accessory carpogonial branches have arisen on several
occasions. The formation of diffuse gonimoblasts
appears to have arisen at least three times, as it is a
feature of Cumagloia, Dotyophycus (Abbott 1976;
Kraft 1988), Patenocarpus (Yoshizaki 1987) and
Yamadaella (Abbott 1970; Wynne & Huisman 1998),
and slightly diffuse gonimoblasts are characteristic of
some species of Liagora (Huisman & Wynne 1999;
Huisman 2002).
The second is that the included species of Liagora
only form a monophyletic clade if Patenocarpus and
Helminthora J. Agardh are included. This is unacceptable as these genera differ substantially from each
other in vegetative and reproductive features. The
alternative argument, that Liagora is poorly defined and
should probably be subdivided into several smaller
genera, seems the more acceptable solution. All
studies on a range of species of Liagora show that a
number of carpogonial branch and cystocarp morphologies are presently accommodated in the genus (Huisman 2002). The continued inclusion of these species
with differing morphologies in Liagora is probably
based on tradition rather than being a true reflection of
their relatedness. The two species included in our
analyses, Liagora valida and Liagora mannarensis,
display substantial differences in cortical structure,
postfertilization development, and ontogeny of spermatangia (see Huisman 2002), characteristics probably
worthy of generic level recognition. Subdivision of
Liagora was initially suggested by Kraft (1989), was
implemented in part by Huisman and Kraft (1994)
when they resurrected Ganonema, and has been further
supported by Huisman and Wynne (1999) and
Huisman and Schils (2002), the latter resurrecting
Izziella for Liagora orientalis. Separation of Ganonema
is supported by the trees, with the recently described
Ganonema borowitzkae (Huisman 2002) occupying a
position distant from the species of Liagora. Huisman
et al. (2004) presented a morphological and sequence
J. M. Huisman et al.
study of several Hawaiian Ganonema species that also
clearly indicated monophyly in that group. Unfortunately, the two species of Liagora included in our
analyses did not include the type (Liagora viscida
(Forsskål) C.Agardh), so further taxonomic revisions
must only be flagged.
While there seems ample support for further subdivision of Liagora, this does little to enhance our
understanding of morphological and reproductive characteristics that might be of use in higher-level separation of the Liagoraceae. Kraft (1989) postulated that
the ancestral Liagoraceae might have produced carpogonial branches with a few modified cells terminating
an otherwise normal cortical filament. The sequence
data seem to support this hypothesis, as this type of
carpogonial branch is found in Nemalion, the sister
group of the included genera. Further sequences from
genera such as Trichogloea (included in the Nemaliaceae by Abbott 1976; but in the Liagoraceae by
Abbott 1999) will be of great interest in assessing
the validity of these hypotheses. Trichogloea produces
carpogonial branches that are long and terminate
seemingly normal vegetative filaments, but also produces specialized short laterals from lower cells of the
carpogonial branch. It therefore displays features that
might indicate a connection with the Scinaiaceae.
The present study represents a first step towards an
understanding of the phylogenetic relationships of the
members of the Nemaliales. The results demonstrate
that many of the morphological features used to
characterize genera are of little use in delineating
higher-level relationships. There is a clear need, however, for additional sequence data from a wider variety
of taxa (including type species of the relevant genera)
before any taxonomic schemes (particularly in the
Liagoraceae) can be proposed with confidence.
The families of the Nemaliales recognized herein
can be separated using the following key:
1 Thallus with terete or slightly compressed branches,
structurally with a cortex composed of loosely arranged
filaments; carpogonial branch of various forms, 3- to
many-celled, the hypogynous cell generally naked or
rarely with short filaments; carposporophyte naked
or with a loose involucre of subsidiary filaments ...
Liagoraceae.
1 Thallus with flattened or terete branches, structurally with a distinct cortex composed of laterally
coherent or fused cells or utricles; carpogonial
branch 3-celled, the hypogynous cell bearing nutritive cells; carposporophyte with a distinct pericarp
and ostiole ...2.
2 Thallus calcified, with distinctly flattened or terete
axes, life history isomorphic or involving slightly
dissimilar gametophytes and tetrasporophytes (differing in cortical structure), or with a filamentous
tetrasporophytes (Tricleocarpa); spermatangia in
conceptacle-like cavities ... Galaxauraceae.
Phylogeny of the Nemaliales
2 Thallus uncalcified, with terete axes or slightly compressed axes, life history phases markedly heteromorphic with a filamentous or crustose tetrasporophytes;
spermatangia in surface nemathecia or in cortical
pits (Nothogenia) ... Scinaiaceae.
ACKNOWLEDGMENTS
We gratefully acknowledge the nomenclatural advice of
Dr Paul Silva (University of California). Dr Dave Ballantine (University of Puerto Rico) and Dr Olivier De Clerck
(Ghent University, Belgium) kindly provided several key
collections of, respectively, Caribbean and South
African algae. Monique Surette is thanked for technical
assistance, as is Alex George for the Latin translation.
J. M. Huisman thanks the Australian Biological Resources
Study for financial support. Part of the present study
was completed while J. M. Huisman was undertaking
research at the Botany Department, University of
Hawaii at Manoa, and he thanks his host, Dr Isabella
Abbott, and (for financial support) the David and Lucile
Packard Foundation. This research was supported by
Natural Sciences & Engineering Council of Canada
grants and Canada Research Chair funds to G. W.
Saunders.
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