Red Algal Taxonomy

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American Journal of Botany 91(10): 1494–1507. 2004.

ASSESSING RED ALGAL SUPRAORDINAL DIVERSITY AND


TAXONOMY IN THE CONTEXT OF CONTEMPORARY
SYSTEMATIC DATA1

GARY W. SAUNDERS2,4 AND MAX H. HOMMERSAND3


2
Centre for Environmental & Molecular Algal Research, Department of Biology, University of New Brunswick, Fredericton, New
Brunswick, Canada, E3B 6E1; and 3Department of Biology, University of North Carolina, Chapel Hill,
North Carolina 27599-3280 USA

The wondrously diverse eukaryotes that constitute the red algae have been the focus of numerous recent molecular surveys and
remain a rich source of undescribed and little known species for the traditional taxonomist. Molecular studies place the red algae in
the kingdom Plantae; however, supraordinal classification has been largely confined to debate on subclass vs. class level status for the
two recognized subgroups, one of which is widely acknowledged as paraphyletic. This narrow focus has generally masked the extent
to which red algal classification needs modification. We provide a comprehensive review of the literature pertaining to the antiquity,
diversity, and systematics of the red algae and propose a contemporary classification based on recent and traditional evidence.

Key words: Bangiophyceae; Compsopogonophyceae; Cyanidiophyta; Eurhodophytina; Florideophyceae; Metarhodophytina; Rho-


dophyta; Rhodoplantae.

The biological significance of red algae is only beginning to be including a wide diversity of lineages distributed among some
appreciated. Even among professional biologists, knowledge of 15 classes (cf. Andersen, 2004). The Rhodophyta have not
these organisms is often minimal and based on cursory informa- experienced a similar explosion in taxonomic breadth with our
tion contained in general botany textbooks (Woelkerling, 1990, p. current perspective on supraordinal relationships virtually un-
1). changed since ca. 1900 and confined to a continuing debate
Macroalgal systematics traces its ‘‘modern’’ era to rather as to whether the two constituent lineages, Bangiophyceae and
humble beginnings, the multitude of diverse species assigned Florideophyceae, should be recognized as distinct classes or
to a few genera in a subdivision (Algae) of the class Crypto- subsumed as subclasses within a single class Rhodophyceae
gamia, which also included the ferns, mosses and fungi, po- (cf. Dixon, 1973).
sitioned among 23 classes of cone-bearing and flowering The current system of red algal classification creates the
plants in the plant kingdom (Linnaeus, 1753). This early clas- illusion that this lineage is relatively limited in its diversity
sification clearly underrepresented macroalgal diversity and when compared to chlorophytes and chromophytes; this de-
substantial taxonomic refinements inevitably followed. La- spite the wide range of morphology observed among red algae
mouroux (1813) was the first to use color to segregate algal and a wealth of contemporary ultrastructural and molecular
assemblages when he removed certain red algae from their data that speak to the antiquity and diversity within Rhodo-
respective associations with species of like morphology to the phyta. This review sets as its aim to amass the available in-
Floridées. Harvey (1836) took the ‘‘biochemical’’ marker fur- formation on red algal phylogeny, diversity, and antiquity and
ther and established the Chlorospermae, Melanospermae, and to use this to reform red algal taxonomy. It is not our intent
Rhodospermae for green, brown, and red algae, respectively; to deal with the broader issue of red algal affinities relative to
in essence establishing the three major groups of macroalgae the other major eukaryotic lines. The reader is directed to an
that are recognized today. overview of that topic by Keeling (2004) in this issue.
Numerous taxonomic changes were implemented in the en-
suing decades, but the relatively recent advent of ultrastruc- FOSSILS AND ANTIQUITY OF THE RED ALGAE
tural and molecular systematic data in particular have uncov-
ered the bewildering diversity, as well as evolutionary affini- The red algae are a study in extremes. Morphologically more di-
ties of the chlorophytic and chromophytic lineages. Recent verse than any other group of algae, they range from single cells
taxonomic treatments vary, but schemes including as many as to large ornate multicellular plants . . . Uniquely among (nonfun-
10 classes in two phyla are now presented for the chlorophytic gal) eukaryotes they lack both flagella and centrioles . . . and ex-
line (cf. Lewis and McCourt, 2004). The brown algae are in- hibit a remarkable, often bizarre range of reproductive strategies
cluded in a larger chromophytic lineage, Heterokontophyta, (Butterfield, 2000, p. 386).

1
Manuscript received 15 January 2004; revision accepted 17 June 2004. The earliest putative red algal fossils date to ca. 2 billion
During preparation of this review, GWS was supported by funds from the years before present and are superficially similar to the extant
Natural Sciences and Engineering Research Council of Canada and the Can- taxa of the Porphyridiales, Bangiophyceae (Tappan, 1976). Al-
ada Research Chair Program and MHH was supported by NSF PEET grant though the evolutionary scenario presented by Tappan, in
DEB-0328491. We are indebted to P. Silva and M. J. Wynne for helpful which the red algae represent a direct link between the pro-
discussions regarding the ICBN, as well as P. Silva for drawing the work of
Doweld to our attention. We thank R. Moe for Latin translations. Comments
karyotic cyanophytes and other eukaryotes, is widely rejected
from J. D. Palmer and two anonymous reviewers were genuinely appreciated in light of recent phylogenetic hypotheses (e.g., Ragan and
and served to improve the clarity of this manuscript. Gutell, 1995), the possibility that unicellular red algae did exist
4
E-mail: gws@unb.ca. at such an early stage (Fig. 1) is compatible with the fossils
1494
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1495

Fig. 1. Geological time scale from a general biology text (Campbell and Reece, 2002), modified to place red algal fossils in context with other major
evolutionary events.

observed by Tappan and other scientists. Most notable in this (Saunders and Kraft, 1997; Fig. 2), were established and dif-
regard is the old (1.2 billion years) and relatively advanced ferentiated by 600–550 Ma, at the end of the Proterozoic Eon
fossil taxon Bangiomorpha (Butterfield, 2000). Bangiomorpha and prior to the Cambrian explosion. In further support of the
pubescens Butterfield (2000) was described from the 1200- antiquity of these various groups, Campbell (1980) reported
million-year-old Hunting Formation in the Canadian Arctic on a 425-million-year-old endolithic microfossil from Poland
and represents the earliest putative record for sex and taxo- clearly identifiable as a Conchocelis stage of the Bangiales,
nomically resolvable complex multicellularity among eukary- for which pit plugs (proteinaceous plugs deposited in the pores
otes. Thus its likeness to taxa currently included in the red resulting from incomplete furrowing following cell division in
algal order Bangiales is truly remarkable (Butterfield et al., red algae) were clearly documented. This same formation also
1990; Butterfield, 2000). contained red solenoporacean algae, considered to be the stem
Zhang et al. (1998) considered that at least eight of the fossil lineage from which the Corallinales evolved (Campbell, 1980),
species described from the terminal Proterozoic (600–550 mil- which differ from the earlier Thallophyca in being calcified.
lion years ago [Ma]) Doushantuo Formation, China, were red In fact, the calcareous Solenoporaceae first appear in the fossil
algae (also see Xiao et al., 1998), and their observations may record ca. 550 Ma and disappear around 60 Ma (Johnson,
provide a unique window into the vegetative and reproductive 1960; Wray, 1977). Fossil red algae directly assignable to ex-
diversity of red algae prior to the Paleozoic (Fig. 1). In addi- tant genera of the Corallinales (lineage 2, Fig. 2) show up in
tion to a variety of parenchymatous species, the fountain-type the Cretaceous (130 Ma), whereas fossils identifiable with gen-
filamentous construction with differentiated medullary and era of the Peyssonneliaceae, Gigartinales (lineage 4, Fig. 2),
cortical filaments was reported for some species. This pattern are recovered from the late Jurassic (160 Ma) providing solid
is characteristic of some extant Florideophyceae. Tetrads noted evidence (Wray, 1977) for a relatively early divergence among
for Paratetraphycus are reminiscent of carposporangial pro- orders within the major florideophyte lineages.
duction in Porphyra, Bangiales, whereas cavities and clusters Naturally, the more recent the fossil, the more easily as-
of spheroidal cells in Thallophyca were considered as a link signable to extant taxa, whereas the earliest records (e.g., Tap-
between this taxon and later fossil Solenoporaceae, which are pan, 1976) are the most difficult to assign unambiguously to
considered a stem group to extant Corallinales (lineage 2, Fig. taxonomic lineages. Perhaps the unexpected antiquity of the
2). Moreover, Thallophyca lacked calcification (Zhang et al., earliest putative red algal unicells is sufficient to cause con-
1998), indicating that this attribute derived relatively recently troversy over their identification. However, when all of the
within lineage 2, a result consistent with the SSU (small sub- fossil evidence is considered in combination, both the relative
unit ribosomal DNA) molecular trees for florideophyte taxa and absolute chronological series of events is logical and con-
(Saunders and Kraft, 1997). In this same formation were other sistent with molecular data on both the antiquity and phylo-
fossil algae, e.g., Paramecia, with embedded clusters of car- genetic relationships of red algae (Figs. 1 and 2).
posporophyte-like structures considered similar to those in lin-
eage 4 orders (Fig. 2) such as the Ceramiales and Gigartinales MOLECULAR SYSTEMATICS AND DIVERSITY
(Zhang et al., 1998).
If the interpretations of these fossils are correct, then the Red algae clearly constitute one of the major radiations of eu-
Bangiales, as well as the four major lineages of florideophytes karyotes. Measured by divergence of SSU rDNA sequences within
1496 AMERICAN JOURNAL OF BOTANY [Vol. 91

Fig. 2. Phylogenetic hypothesis for the red algae based on a compilation of molecular results from Saunders and Bailey (1997, 1999), Oliveira and
Bhattacharya (2000), Müller et al. (2001), and Yoon et al. (2002b). The black arrow indicates an association (albeit not supported) for an alliance of the
Compsopogonales et al. with the Bangiales/Florideophyceae lineage. For orders with more than one family (excepting Porphyridiales), the familial composition
is provided (* indicates a family of equivocal taxonomic affinity). Lineages 1–4 of the Florideophyceae follow Saunders and Kraft (1997). Putative evolutionary
scenarios for the type of Golgi association (ER 5 exclusively ER; ERm 5 ER and mitochondrial; NU 5 nuclear) and presence vs. absence (PT, NPT, respectively,
or Mix for both) of peripheral encircling thylakoids are provided. Only those porphyridialean genera included in molecular systematic studies are listed.

the most conservative regions, Rhodophyta are more divergent the red and green lines diverged ca. 1500 Ma; the Cyanidiales
among themselves than are (i) fungi or (ii) green algae and green diverged soon after, ca. 1370 Ma, and prior to the secondary
plants together (Ragan et al., 1994, p. 7278). endosymbiosis event (ca. 1270 Ma) that seeded the chromo-
Although it is known that homologous genes can evolve at phytic line; the remaining bangiophycean lines had largely di-
unequal rates in different lineages and, therefore, that direct verged by the time the chlorophytes had separated from the
comparisons of levels of divergence can be misleading as to charophycean-land plant line (ca. 1200 Ma); the Florideophy-
the relative age of a group, the red algae display consistently ceae and Bangiales diverged prior to the split between the
high diversity across a variety of genes including actin and charophytes and land plants (ca. 800 Ma); and the major flor-
the nuclear and plastid small subunit ribosomal (SSU) genes ideophycean groups had diverged prior to the first appearance
(cf. Ragan et al., 1994; Medlin et al., 1997). of land plants (ca. 460 Ma; Yoon et al., 2004).
Lim et al. (1986) published the first study to consider red Clearly, the molecular data are consistent with the fossil
algae in a broader eukaryotic context and to estimate their record in recognizing the red algae as a relatively early lineage
divergence dates from molecular data. They used the 5S ri- of eukaryotes, with the component lineages also the result of
bosomal RNA and concluded: red algae diverged from other early divergence events. However, the task of resolving ade-
eukaryotes at an early stage, ca. 1400 Ma; the split between quately the composition and relative relationships among these
the Bangiales and Florideophyceae was relatively early in red same red algal lineages receives limited support from the fossil
algal evolution (ca. 1000 Ma); and, the florideophytes included record. Molecules, on the other hand, have provided consid-
in their analyses (representatives of the contemporary lineages erable insight in this regard. The first molecular investigations
2 and 4, Fig. 2) were phylogenetically remote from one an- to consider red algal phylogeny at and above the ordinal level
other relative to taxa within other eukaryote lines. The brown were published back-to-back in 1994 and used the nuclear
algae, in contrast, were considered a recent divergence, only SSU (Ragan et al., 1994) and the plastid rbcL (Freshwater et
ca. 200 Ma, consistent with later estimates based on additional al., 1994). These studies suffered the inevitable consequence
molecular data (Saunders and Druehl, 1992) but in strong con- of being first viz. low, and underrepresentative taxon sampling
trast to their putative fossil record and taxonomic framework (cf. Saunders and Kraft, 1997). This was particularly true for
(cf. Saunders et al., 1992). the Bangiophyceae, which were represented by only four to
Yoon et al. (2004) used a six-gene data set to generate the six genera in these reports. Regardless, both studies set the
most robust molecular clock estimates to date for the diver- foundations for future molecular phylogenetic research in the
gence of photosynthetic lineages. Their results echo the find- Rhodophyta and were consistent in resolving the Bangiophy-
ings of earlier studies that used single molecules and inferred ceae as paraphyletic to the Florideophyceae.
great antiquity for the red algae (e.g., Lim et al., 1986; Ragan The paucity of published molecular data for the Bangio-
et al., 1994). According to the estimates of Yoon et al. (2004), phyceae was soon remedied by a series of ordinal-level taxo-
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1497

nomic studies. Oliveira et al. (1995) enhanced representation further investigation will the validity of this interesting asso-
for the Bangiales in SSU trees, while Holton et al. (1998) ciation be evaluated.
added the first representatives of the freshwater family Bol- For the Florideophyceae, ordinal-level investigations by
diaceae, Compsopogonales. Rintoul et al. (1999) expanded Saunders and Kraft (1994, 1996) provided the first molecular
representation for the Compsopogonales in the SSU and rbcL advances on the initial studies of Freshwater et al. (1994) and
alignments and uncovered support for a monophyletic lineage Ragan et al. (1994). Saunders and Bailey (1997) published a
including the freshwater families Boldiaceae and Compsopo- comprehensive ordinal representation for the Florideophyceae
gonaceae, as well as the marine Erythrotrichiaceae (assigned in which four lineages were clearly identified (Fig. 2), defined,
to a segregate order in some treatments; cf. Silva, 1996). The in part, by pit-plug ultrastructure. Saunders and Kraft (1997)
following year, the Rhodochaetales were added to the molec- imparted some degree of informal recognition for these groups
ular framework (Zuccarello et al., 2000). This monogeneric as lineages 1 through 4. Following these works, a series of
order was considered by many to be of pivotal importance in papers used SSU, rbcL, or a combination of these genes, as
understanding red algal evolution (e.g., Chadefaud, 1965; well as anatomical observations, to recognize a number of new
Pueschel and Magne, 1987; Garbary and Gabrielson, 1990), orders in the Florideophyceae: Balbianiales (Sheath and Müll-
but they were later shown to be a close ally of the Erythro- er, 1999); Balliales (Choi et al., 2000); Colaconematales
trichiaceae (as Erythropeltidaceae; Zuccarello et al., 2000) and (Harper and Saunders, 2002); Thoreales (Müller et al., 2002);
not the immediate ancestor to the florideophyte algae or the a resurrected Nemastomatales (Saunders and Kraft, 2002); and
earliest red algal lineage. Consistent with the molecular results, the Pihiellales (Huisman et al., 2003). In addition, Harper and
Rhodochaete shares many of the diagnostic features that ally Saunders (2001) used the large-subunit rDNA to assess ordinal
the three families of the Compsopogonales sensu lato (dis- relationships among the Florideophyceae, and Saunders et al.
cussed later). Nonetheless, Zuccarello et al. (2000) considered (2004) have completed a comprehensive SSU investigation of
that Rhodochaete warranted recognition at the ordinal level, lineage 4.
as did the Erythrotrichiaceae in their system, leaving the Although a number of unresolved issues remain in red algal
Compsopogonales sensu stricto with only the two freshwater taxonomy (discussed later), a phylogenetic consensus at and
families. above the ordinal level is starting to emerge (Fig. 2).
The studies discussed generally had low representation for
the Porphyridiales sensu lato (i.e., including Cyanidiales), the VEGETATIVE, REPRODUCTIVE AND
order containing the many unicellular and pseudofilamentous ULTRASTRUCTURAL DIVERSITY
members of the Rhodophyta. Oliveira and Bhattacharya Being an ancient lineage, the red algae have undergone a broad
(2000) filled the gap and provided the most comprehensive range of modifications in cellular organization. Even the spectrum
bangiophyte trees published to that date. Their study used the of morphological possibilities, from unicellular forms . . . to com-
plastid SSU and, consistent with earlier reports, resolved the plex . . . parenchymatous thalli, fails to convey the degree of cel-
Bangiophyceae as paraphyletic in positioning the Florideophy- lular diversity (Pueschel, 1990, p. 8).
ceae as sister to the Bangiales. They resolved three distinct
The morphological and ultrastructural diversity of the red
lineages of a polyphyletic Porphyridiales sensu lato: one weak- algae is as striking as their genetic variation revealed in the
ly allied to the Compsopogonales; a second sister to that as- molecular studies. Even a cursory survey of the chapters in
semblage; and the third equivalent to the Cyanidiales as rec- Biology of the Red Algae by Cole and Sheath (1990) provides
ognized by some workers (e.g., Ott and Seckbach, 1994). ample evidence. Pueschel (1990) noted that among the red
Müller et al. (2001) provided a nuclear SSU rDNA phyloge- algae, there are at least three patterns of Golgi association,
netic hypothesis the following year, containing even more taxa, three methods by which cells achieve multinuclearity in de-
but essentially inferring the same relationships as the earlier velopment, and several methods of establishing intercellular
plastid-based investigation. The studies of Oliveira and Bhat- connections through cellular fusions and pit-plug formation.
tacharya (2000) and Müller et al. (2001) are unquestionably Scott and Broadwater (1990) described five distinct patterns
the most substantial in contributing to our understanding of of mitosis, differing in details of microtubule number and
relationships among the lineages of the Bangiophyceae. In an mode and location of formation, number and disposition of
effort to understand better the evolution of secondary plastids, gaps in the nuclear envelope, shape and size of the nuclear-
Yoon et al. (2002a, b) combined from two to five plastid genes associated organelles, and the mode of cytokinesis. Coomans
and provided further insights into red algal phylogeny. Their and Hommersand (1990) described three patterns of cytoki-
results echoed many aspects of the earlier studies, viz., an early nesis, whereas Hommersand and Fredericq (1990) recognized
divergence for the Cyanidiales, an association for the Bangiales three distinct patterns by which the various reproductive struc-
and Florideophyceae, and a strongly resolved Compsopogonales/ tures are formed in red algae, these clearly associated with
Erythropeltidales/Rhodochaetales clade. Yoon et al. reported that different evolutionary lineages. The following section outlines
the divergence of the Cyanidiales from the remaining red algae the key anatomical features and the fluctuating taxonomic sys-
predates the origin of the entire kingdom Chromista sensu lato, tems dependent on them for each of the lineages observed in
an event they estimated at ca. 1.3 billion years ago. Yoon et the molecular analyses (Fig. 2).
al. also resolved an association between the Bangiales/Flori-
deophyceae and the Compsopogonales and its allies (Fig. 2), Cyanidiales—Taxa in this lineage consistently resolve as
albeit with no support. We find some satisfaction in such an sister to the rest of the red algae (Fig. 2). Chapman et al.
association because a single origin for complex multicellular- (1968) concluded that these algae were not only distinct at the
ity and pit plugs (unique to, and almost always associated family level, but that they warranted a distinct order, Cyani-
with, complex multicellular development in red algae) would diales (first proposed in Christensen, 1962), based on their
characterize a common ancestor to this lineage. Only through biliprotein composition. Chapman (1974) reversed his earlier
1498 AMERICAN JOURNAL OF BOTANY [Vol. 91

decision, retaining the lineage at the family level within the plex (cf. Dixon, 1973; Silva, 1996), and for the most part, the
Porphyridiales. Garbary et al. (1980) reevaluated bangiophyte three lineages identified in the molecular trees are at odds with
taxonomy and considered that Cyanidium and its allies were all previous taxonomic proposals. Generic concepts and spe-
best included in the Phragmonemataceae, Porphyridiales, cies complements have changed markedly through the various
largely owing to an absence of pyrenoids and the presence of schemes (Garbary et al., 1980, Table 1), resulting in a bewil-
endospores. In contrast, Merola et al. (1981) treated these al- dering variety of taxonomic systems in the literature for these
gae as distinct at the class level, Cyanidiophyceae, which was algae. Garbary et al. (1980) provided a major step forward in
part of a larger thesis to consider Cyanidium and its allies as removing an earlier emphasis on unicells vs. pseudofilaments
a ‘‘phylogenetic bridge’’ between the prokaryotic cyanobac- (e.g., Dixon, 1973; Chapman, 1974), but their proposed tax-
teria and the eukaryotic red algae. However, the key support- onomic groupings are strongly at odds with the subsequent
ing character, plastids bounded by a single membrane (Merola molecular data (Fig. 2). It is timely to reconsider these organ-
et al., 1981), was later shown to be erroneous. Gabrielson et isms in light of the molecular trees (cf. Müller et al., 2001).
al. (1985) advocated that the new class be rejected because it Porphyridiales 1, represented in the molecular trees to date
lacked defining synapomorphies and continued to include by Dixoniella, Glaucosphaera, and Rhodella, are primarily a
these taxa in the Porphyridiales. Seckbach (1987) continued lineage of unicellular taxa (Müller et al., 2001), which have
the trend of taxonomic elevation for the Cyanidiales and pro- contrasting states for many of the characters traditionally con-
posed phylum status, Prerhodophyta, for this unusual lineage sidered to be taxonomically useful (Fig. 2). Dixoniella and
of eukaryotes. Seckbach et al. (1992, p. 100) subsequently Glaucosphaera have their Golgi associated with the nucleus
reversed the earlier elevation and recognized this lineage as a and an encircling thylakoid in the plastid, whereas Rhodella
distinct subclass of the Bangiophyceae. Seckbach and Ott has a Golgi–ER association and lacks an encircling thylakoid
(1994, p. 141) reconsidered the attributes of the cyanidioph- (Scott et al., 1992). Rhodella is more similar to Dixoniella in
ytes and, despite generally referring to them as a class through- having a stellate plastid with a central pyrenoid, whereas Glau-
out their publication, concluded that the system of Chapman cosphaera has a parietal reticulate plastid lacking a pyrenoid
(1974; family of the Porphyridiales) was best supported from (Broadwater and Scott, 1994). In addition to the molecular
the available evidence, whereas Ott and Seckbach (1994, p. data, structural data may prove this lineage distinct from the
149) in the same volume supported ordinal status within the other two porphyridialean groups in the types of Golgi asso-
Bangiophycidae. Seckbach (1999) revived the class-level des- ciation.
ignation, and researchers working directly with these organ- In Porphyridiales 2 (Müller et al., 2001), the unicellular ge-
isms have generally accepted this system (e.g., Muravenko et nus Rhodosorus is sister to a host of pseudofilamentous genera
al., 2001). Other red algal systematists have tended to retain (and allies, e.g., unicell Chroothece and pseudofilament
the group as an order, Cyanidiales, of the Bangiophyceae (e.g., Chroodactylon; Lewin and Robertson, 1971). Members of this
Müller et al., 2001). group are similarly variable in plastid morphology and pyre-
Although the main argument of Gabrielson et al. (1985) for noid disposition, as well as the presence or absence of an en-
rejecting the Cyanidiophyceae, viz., the absence of a defining circling thylakoid (Fig. 2). The last feature is absent from the
synapomorphy, may be considered valid by some phycolo- unicellular Rhodosorus (Broadwater and Scott, 1994), sup-
gists, this does not change the reality of the molecular data, porting other plastid differences and molecular data in recog-
which consistently place them as sister to the remaining Rho- nizing this genus as distinct within Porphyridiales 2. Members
dophyta. Further, Gross et al. (2001) have uncovered levels of of this group are, where known, characterized by a Golgi–ER/
SSU divergence among strains of cyanidiophytes equivalent mitochondrial association, a feature shared with Porphyridiales
to ordinal and lineage level divergence among florideophytes 3 (Broadwater and Scott, 1994) and the Bangiales and Flori-
(Fig. 2). In support of the molecular data, Cyanidium and its deophyceae (Pueschel, 1990).
allies have a Golgi–ER association, as is common in other Porphyridiales 3 include, thus far, the unicells Flintiella and
eukaryotes, but rare among red algae; thick proteinaceous cell Porphyridium. Again, these two genera are distinct in features
walls; endospores; heterotrophic capacity; and the ability, per- of plastid morphology and possibly pyrenoid disposition
haps unique among eukaryotes, to live in extreme acidophilic/ (Broadwater and Scott, 1994), but alike in lacking the periph-
thermophilic environments (cf. Chapman, 1974; Gross et al., eral encircling thylakoid. The presence of a peripheral thyla-
2001). Muravenko et al. (2001) further provided evidence that koid is generally considered primitive rather than derived
the cyanidiophytes have the smallest known genomes of any (Pueschel and Magne, 1987), a hypothesis consistent with the
phototrophic eukaryotes. Many putative synapomorphies have distribution of this feature on the molecular trees (Fig. 2), and
been listed here, but more importantly the unique attributes of thus the absence of this attribute may ultimately prove a syn-
these organisms provide a sense that the Cyanidiales are as apomorphy for this lineage.
distinct from other red algae as are phyla in the plant and We can conclude that the emphasis on plastid morphology
animal kingdoms relative to one another. and pyrenoid occurrence at familial and ordinal taxonomic lev-
els among red algae (e.g., Garbary et al., 1980) is not justified,
Porphyridiales—Even with removal of the anomalous although these features may prove useful for taxonomy within
Cyanidiaceae from Porphyridiales, molecular analyses gener- the major lineages of the Porphyridiales. Similarly, these two
ally have indicated that this order is paraphyletic (Oliveira and features failed to resolve higher-level taxa within the florideo-
Bhattacharya, 2000; Müller et al., 2001), although Yoon et al. phyte order Acrochaetiales sensu lato, but were nonetheless
(2002a, b) provided the first results consistent with monophyly useful in distinguishing among closely related genera (Harper
for this order. Regardless, it is clear from all of the previous and Saunders, 2002).
studies that there are three distinct and highly divergent lines
in this order as currently circumscribed. The nomenclatural Compsopogonales, Erythropeltidales, and Rhodochaeta-
history surrounding this lineage has been convoluted and com- les—Garbary et al. (1980) united the families Boldiaceae,
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1499

Compsopogonaceae, and Erythrotrichiaceae (as Erythropelti- attributes are generally regarded as ancestral, they are more
daceae) together in the Compsopogonales (as Erythropeltida- probably derived character states for this order.
les; cf. Wynne, 1986) based on a similar pattern of monospo-
rangial production. Monosporangia are produced from an un- Florideophyceae—Red algal species in the class Florideo-
differentiated vegetative cell following the formation of an phyceae have been subjected to nearly a century of taxonomic
oblique curved wall, which divides the cell into two, the small- thought dominated by unwavering emphasis on female repro-
er differentiating as a sporangium. A Golgi–ER association, ductive anatomy and postfertilization development. In turn,
encircling thylakoids in the plastid, and a thylakoid-free cen- this taxonomic framework has shaped the way that taxono-
tral region of the plastid further define this lineage (cf. Rintoul mists view all aspects of red algal evolution; e.g., life history
et al., 1999), as well as the order Rhodochaetales. Silva (1996) patterns, reproductive structures, and vegetative anatomy, with
argued that the members of the Compsopogonaceae are more regards to ancestral vs. derived character states. Recent ultra-
complex than those of the Erythrotrichiaceae and that the latter structural and molecular investigations have challenged the
should form the basis of an emended Erythropeltidales. This foundation of the dominant assumptions on which red algal
proposal is supported by recent molecular analyses (e.g., Zuc- classification is constructed, directing the taxonomic structure
carello et al., 2000; Müller et al., 2001), a freshwater vs. ma- for these organisms down a new and often unexpected path.
rine habitat, and aspects of the plastid ultrastructure and nu- Over a century ago, Schmitz (1892) started red algal sys-
clear-associated organelle structure (Scott and Broadwater, tematics along a new course by placing emphasis on aspects
1989), which also serve to unite the Boldiaceae and Comp- of the female reproductive system and postfertilization devel-
sopogonaceae at the ordinal level, to the exclusion of the Er- opment. In retrospect, it is a testament to Schmitz’s intuition
ythrotrichiaceae. In addition to the features noted, the Rho- and appreciation of red algal species that he took this path,
dochaetales possess pit plugs without caps or membranes sim- although the sheer wonder of red algal life histories alone
ilar to those in the Compsopogonaceae (Pueschel and Magne, could justify such an approach. In red algae, there are no mo-
1987). Nonetheless, the Rhodochaetales have generally been tile stages in the life history, and this, in turn, manifests itself
treated as a separate order owing to their apical rather than in an unusual complement of reproductive structures (Fig. 3).
diffuse growth (Gabrielson et al., 1985). In phylogenetic stud- The full dynamics of this life history were realized through
ies by Zuccarello et al. (2000), the Rhodochaetales were a the cytological work of Yamanouchi (1906) while investigat-
close sister to the Erythropeltidales, with this combined line- ing the genus Polysiphonia. In short, male gametophytes pro-
age only a relatively distant sister to the Compsopogonales, duce spermatia that are released into the water column to con-
which includes two freshwater families, Boldiaceae and tact passively trichogynes (long receptive extensions of the
Compsopogonaceae (Fig. 2). oogonia, termed carpogonia) that extend beyond the surface
Rhodochaete parvula Thuret is an alga that has been con- of the female gametophyte (Fig. 3). The male nucleus makes
sidered as a likely sister to the Florideophyceae (cf. Gabrielson its way down the central channel of the trichogyne to fuse
and Garbary, 1986) owing to branched uniseriate filaments with the haploid nucleus of the carpogonium, the fusion prod-
with apical growth, naked pit-plugs (i.e., no caps or mem- uct of which develops on the female gametophyte into a dip-
branes; Pueschel and Magne, 1987), intercalary reproductive loid generation termed the carposporophyte. In some species,
structures (Magne, 1960), and a putatively triphasic life history the carposporophyte can develop directly from the carpogo-
(Guiry, 1987) that incorporates a ‘‘proto-carposporophyte’’ nium, but it is common for the fertilized carpogonium to trans-
generation consisting of two cells, one of which forms a car- fer the diploid nucleus (directly or indirectly) to a ‘‘vegeta-
posporangium that releases a single carpospore. However, this tive’’ cell of the thallus, termed an auxiliary cell, from which
evolutionary hypothesis is more likely an artifact of Rhodo- carposporophyte development initiates. The carposporophyte
chaete similarities to the Acrochaetiales, an order of Florideo- remains dependent on the female gametophyte and produces
phyceae long, albeit incorrectly (Saunders and Bailey, 1997), a number of carposporangia, each of which releases a diploid
considered the ancestral lineage of florideophytes. Indeed, the carpospore (Fig. 3). This nonflagellate spore attaches to suit-
interpretation of a triphasic life history for Rhodochaete (cf. able substrate and initiates vegetative development to yield the
Gabrielson and Garbary, 1986; Guiry, 1987) is probably more sporophyte generation. The florideophycean sporophyte is
an overinterpretation based on the assumption of a close alli- called a tetrasporophyte because meiosis characteristically re-
ance to the Florideophyceae than an accurate interpretation of sults in sporangia with four spores; these in turn release to
the postfertilization events. develop into the gametophyte generation (Fig. 3). We would
argue that this is truly the most elaborate sexual life history
Bangiales—This bangiophyte order is the most closely al- among the macrophytic algae.
lied to the Florideophyceae (Fig. 2) in all recent molecular Schmitz was not alone in changing the tide of red algal
systematic analyses (e.g., Müller et al., 2001). This relation- taxonomy; his work was accepted and embellished by key
ship is supported by the Golgi–ER/mitochondrion association players in red algal systematics, notably Oltmanns (1904–
and similarities between the Conchocelis (diploid stage in sex- 1905) and Kylin (1932, 1956). Kylin, in particular, codified
ual cycles) phase of the Bangiales and the florideophytes (Cole red algal taxonomy based on his interpretation of comparative
and Conway, 1975). The Conchocelis phase has an encircling red algal morphology. Kylin’s scheme recognized the Acro-
peripheral thylakoid in the plastid, apical growth, and pit plugs chaetiaceae with their sessile carpogonia as basal to other
with a single cap layer (cf. Cole and Conway, 1975; Gabriel- members of the Nemaliales, which produce distinct carpogo-
son et al., 1985), whereas the bangialean gametophyte is par- nia-bearing branches, but for which carposporophytes still de-
enchymatous and unique (exceptions discussed later) among veloped directly from the fertilized carpogonium. In more ‘‘ad-
red algae in producing carposporangia and spermatangia in vanced’’ systems, the fertilization nucleus is transferred to a
distinct packages via a series of successive divisions (cf. Hom- remote (nonprocarpy) or nearby (procarpy) auxiliary cell from
mersand and Fredericq, 1990). Although these gametophytic which the carposporophyte develops. Kylin (1956) further dis-
1500 AMERICAN JOURNAL OF BOTANY [Vol. 91

Fig. 3. A generic look at the ‘‘typical,’’ albeit remarkable, florideophyte life history. Blue and purple text and arrows represent haploid and diploid stages,
respectively. Consult text for a description of the structures.

tinguished between the case in which the auxiliary cell is pre- tiated a controversial split with the existing paradigm by erect-
sent before or in the absence of fertilization vs. production ing the Palmariales for certain members of the Rhodymeniales
only following fertilization (Fig. 4), a condition he considered based on aspects of tetrasporangial development rather than
the peak in red algal evolution. Fritsch (1945) and Feldmann female reproductive anatomy and postfertilization develop-
(1952) also had much influence in establishing the Acrochae- ment (unknown for these species at that time). Pueschel and
tiaceae as ancestral among the Florideophyceae. Cole (1982) dramatically challenged the traditional classifica-
The first break with the Schmitz/Kylin system came with tion on the basis of pit plug ultrastructure and provided support
the establishment of the Bonnemaisoniales (cf. Feldmann, for some earlier contentious ordinal proposals including the
1952) based on life history studies that established that mem- Bonnemaisoniales, Corallinales (formally proposed later by
bers of the Naccariaceae and Bonnemaisoniaceae possessed Silva and Johansen, 1986), Gelidiales, and Palmariales, as well
heteromorphic life histories in which a conspicuous gameto- as for the new orders Batrachospermales and Hildenbrandiales.
phyte was followed by a microscopic filamentous or crustose Hommersand and Fredericq (1988) later formally reinstated
tetrasporophyte (cf. West and Hommersand, 1981), in contrast the Gelidiales following detailed anatomical investigations,
to the isomorphic life history found in Polysiphonia and most whereas Fredericq and Hommersand (1989) proposed the Gra-
red algae. Subsequent life history studies of a variety of red cilariales on the basis that the carposporophyte developed di-
algae grown in culture demonstrated that many unrelated red rectly from a carpogonial fusion cell rather than an auxiliary
algal species had heteromorphic life histories (cf. West and cell as had previously been thought. In the same year, Maggs
Hommersand, 1981). For this and other reasons, Dixon (1973) and Pueschel (1989) established the Ahnfeltiales based on the
downgraded the significance of life history in classification of presence of naked pit plugs that lacked caps and membranes
red algae and subsumed the Bonnemaisoniales and the Geli- and a carposporophyte that developed outwardly directly from
diales under an emended order Nemaliales. Guiry (1978) ini- the terminal fertilized carpogonium. Molecular data were com-
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1501

(Figs. 2 and 4). Harper and Saunders (2004) and Saunders et


al. (2004) provided detailed reviews of the orders, and com-
ponent families of the four florideophyte lineages (summarized
in Fig. 2). We consider that the time for formal taxonomic
recognition of these lineages is overdue. Prior to taxonomic
designation for these ordinal assemblages, however, it is nec-
essary to consider red algal supraordinal taxonomy.

PREVIOUS TAXONOMIC PROPOSALS


Once a system of classification becomes widely adopted, it takes
on many of the attributes of a creed. Not only does it constitute
the framework about which the botanist does his thinking but it
rapidly becomes a substitute for it . . . To function properly, all
systems must be kept in a fluid and flexible state (Arnold, 1948,
pp. 3–4).
Dixon (1973) provided a summary of red algal supraordinal
taxonomy until that time. By the early 1900s, red algal sys-
tematists had generally settled on a single class, Rhodophy-
ceae, with the two subclasses Bangiophycidae and Florideo-
phycidae. Dixon (1973) discussed a trend during the 1900s to
raise the status of all major algal groups and treat them as
phyla, in this case the Rhodophyta, with the two major groups
now recognized at the class level. Dixon considered the issue
of whether the two major divisions should be recognized at
the subclass or class level and concluded, based largely on
differences in vegetative development (intercalary vs. apical),
that two classes were justified. Gabrielson et al. (1985) sub-
sequently argued that the Bangiophyceae are paraphyletic and
lack a distinguishing synapomorphy and therefore only a sin-
gle class, Rhodophyceae, with two subclasses is warranted.
This argument clearly lacks validity—the Bangiophycidae are
Fig. 4. Schematic representation of red algal evolution from traditional equally paraphyletic and wanting of a unifying synapomorphy
(Kylin, 1956) and contemporary (Pueschel, 1994; Saunders and Bailey, 1997) regardless of taxonomic rank. Clearly, all of the information
perspectives. Dotted and dash/dot lines lead to extant members of lineages 2
and 4, respectively (cf. Fig. 2). IC 5 gain (– indicates loss of this same
must be considered in trying to frame a contemporary system
feature) of single (inner in later taxa) cap layers; M 5 gain of cap membranes; of taxonomy for red algae, not only the monophyly of con-
DOC and TOC represent gain of domed and thin (plate) outer cap layers in stituent lineages, but also the antiquity and diversity of these
lineage 2; * highlight the putatively primitive Acrochaetiales and advanced same lineages.
Ceramiales. Magne (1989) has provided the only substantive ‘‘bottom-
up’’ attempt at reforming supraordinal classification among the
red algae. He specifically challenged the lack of monophyletic
bined with anatomical studies by Saunders and Kraft (1994) groupings and proposed three subclasses: Archaeorhodophy-
to propose the Plocamiales and later, the Halymeniales (Saun- cidae for those red algae lacking sporangia (in essence the
ders and Kraft, 1996). Subsequent investigations have contrib- Porphyridiales sensu lato); Metarhodophycidae for those or-
uted to the recognition of six additional orders (discussed ear- ders in which members converted only a portion of the parent
lier). cell to a sporangium (Compsopogonales, Erythropeltidales,
On the phylogenetic front, Pueschel (1994) presented a de- Rhodochaetales); and the Eurhodophycidae for those taxa that
tailed hypothesis in which naked pit plugs (lacking covering he considered to have true sporangia (complete protoplasm
membranes and caps at their cytoplasmic faces) were regarded converted to sporangia) including the Bangiales and Florideo-
as ancestral and all taxa with two cap layers were derived from phyceae. Although Magne’s system comes closer to recogniz-
a common ancestor. Pueschel argued for the latter taxa that ing monophyletic lineages (Archaeorhodophycidae are the ex-
the domed outer cap was ancestral to the thin outer plate (Fig. ception), the recognition of these major units at the subclass
4) and that the presence of cap membranes was a derived state. level fails to acknowledge the substantial diversity within and
Molecular studies using SSU (Saunders and Bailey, 1997) between the various lineages. Nonetheless, Magne’s contri-
have confirmed Pueschel’s hypothesis and clarified relation- bution is significant in recognizing the need for more than two
ships among the many other florideophyte orders for which upper-level groups, in acknowledging a relationship between
plug features fail to provide a distinguishing character (cf. Fig. the Bangiales and Florideophyceae and opening the door for
2). A significant result has been the recognition that the Ac- new proposals on red algal supraordinal taxonomy. Silva
rochaetiales are a recently derived order and that the Cera- (1996, p. 912) rejected Magne’s proposals, noting that ‘‘de-
miales are not the pinnacle of red algal evolution (Fig. 4). spite significant differences, there is sufficient common ground
Saunders and Kraft (1997) designated the four major florideo- among the Archaeorhodophycidae, Metarhodophycidae, and
phyte groupings resolved in the previous study as lineages 1 Bangiales to warrant the traditional recognition of the Bangio-
through 4 and defined them on the basis of pit plug attributes phycidae . . . at least for pedagogical purposes.’’ Although we
1502 AMERICAN JOURNAL OF BOTANY [Vol. 91

are sympathetic with this point, the weight of evidence dictates at the supraordinal level. Here we merge the recently acquired
that the previous taxonomic entities are not closely allied and phylogenetic knowledge with the fossil and molecular evi-
thus the taxonomic system currently in place needs revision. dence on the antiquity of the red algal lineages to provide a
Ironically, at the highest levels of eukaryote taxonomy new and comprehensive system of classification. In so doing,
(‘‘top–down approach’’) the significance and antiquity of the we have attempted to use available, particularly typified,
red algae is recognized, and the group is granted, along with names as discussed in the International Code of Botanical No-
the Glaucophyta, kingdom or subkingdom status in some sys- menclature (hereafter ICBN; Greuter et al., 2000).
tems (e.g., Cavalier-Smith, 1981, 1998). In his 1998 summary,
Cavalier-Smith included infrakingdom rankings for the Glau- Kingdom Plantae
cophyta and Rhodophyta in his subkingdom Biliphyta, which Subkingdom Rhodoplantae G.W. Saunders et Hommer-
was considered as probably a paraphyletic assemblage. Cav- sand subregnum nov.
alier-Smith (1998) further considered that the Bangiophyceae
were so diverse that two classes were warranted: Bangiophy- Plantae sine flagellis omnino; materia photosynthetica in
ceae sensu stricto for the Bangiales and Rhodochaetales, which cytoplasmate condita; lamellae chloroplasti non-aggregati;
have pit connections; and Rhodellophyceae for the Porphyri- pigmenta accessoria (incl. ‘‘phycoerythrin’’ et ‘‘phycocya-
diales, Cyanidiales, and Compsopogonales, which he consid- nin’’) in corporibus in pagina lamellae chloroplasti dictis
ered lacked pit plugs. Unfortunately for this system, the Comp- ‘‘phycobilisome.’’
sopogonales have members with pit plugs, and neither of his Eukaryotic organisms lacking flagella in all life history
two groupings was monophyletic based on analyses of any of stages; photosynthetic reserve stored in the cytoplasm; plas-
the available anatomical or molecular evidence (Fig. 2). At the tids with non-aggregated thylakoids; accessory pigments in-
same time, Cavalier-Smith established the subphylum Rhodel- cluding phycoerythrin and phycocyanin in phycobilisomes
lophytina for his new class and united his Bangiophyceae sen- on the thylakoid surfaces.
su stricto with the Florideophyceae as a new subphylum
Macrorhodophytina. Again, neither of these groupings is Comments—Although we concur with Cavalier-Smith
monophyletic, and the status of the Erythropeltidales was left (1998) that the red algae deserve subkingdom status within
equivocal. Doweld (2001) established the kingdom Rhody- kingdom Plantae, we agree with Doweld (2001) that they
meniobiota including the subkingdoms Cryptomonadobiotina, should not be included in the same subkingdom as Glauco-
Glaucobiotina, and Rhodymeniobiotina. This kingdom is not phyta. We restrict subkingdom Biliphyta Cavalier-Smith
monophyletic, but the recognition of distinct subkingdoms for (1998; originally proposed as a kingdom, Cavalier-Smith,
the glaucophytes and rhodophytes, although they should be 1981) to the Glaucophyta and establish a separate subkingdom
included within the kingdom Plantae, represents an improve- for red algae in the kingdom Plantae. In our opinion, the de-
ment to Cavalier-Smith’s (1998) system. A further advance- scriptive (i.e., nontypified) name Rhodoplantae is the best
ment in Doweld’s classification is recognition of a distinct choice for the red algae because Thuret (1855) was first to
phylum for cyanidiophytes (Cyanidiophyta) relative to the re- unite the bangiophycean and florideophycean algae together
maining rhodophytes. into a taxonomic construct for which he used the name Rho-
Within the Florideophyceae themselves, the biggest revi- dophyceae Ruprecht (cf. Ragan and Gutell, 1995). We thus
sionist attempt was provided by Chadefaud (1960). In this reject the typified name Rhodymeniobiotina Doweld, as is per-
work, we find an attempt at supraordinal taxonomy in the Flor- mitted under the ICBN (Art. 11.9).
ideophyceae in which he recognized the Eo-floridées (Acro- Phylum 1: Cyanidiophyta Moehn ex Doweld 2001
chaetiales, Eu-Nemaliales), Meso-floridées (remaining Nem-
aliales, Gigartinales, Rhodymeniales, etc.), and the Meta-flor- Unicellular red algae inhabiting extreme environments;
idées (Bonnemaisoniales, Ceramiales). We now know that this Golgi associated with endoplasmic reticulum, cell walls
perspective of the ‘‘primitive’’ Acrochaetiales leading to the thick and proteinaceous; production of endospores; hetero-
‘‘advanced’’ Ceramiales is erroneous, so that Chadefaud’s sys- trophic capacity.
tem is not natural (Fig. 4).
Class Cyanidiophyceae Merola et al., 1981
A CONTEMPORARY TAXONOMIC PERSPECTIVE Characters as for phylum.
Order Cyanidiales T. Christensen 1962
Our understanding of the phylogeny of red algae, and hence their
classification, is presently in a period of major upheaval unprec- Comments—It is clear that the Bangiophyceae are paraphy-
edented since the end of the nineteenth century . . . revisions are letic to the Florideophyceae (Freshwater et al., 1994; Ragan
potentially as far-reaching as those that occurred in the Chloro- et al., 1994; Saunders and Kraft, 1997) and that the Cyanidi-
phyta in the 1970s and early 1980s (Garbary and Gabrielson, 1990,
ales are more evolutionarily divergent from the remaining red
p. 478).
algae as are phyla and classes of organisms in other kingdoms
It is obvious from the previous discussion that red algae are relative to one another (discussed earlier). We consider that
an old and diverse lineage of organisms at all levels (mor- this lineage warrants distinction at the level of phylum, which
phology to molecules). Any revisionist attempt at red algal was advocated also by Doweld (2001). Seckbach (1987) es-
classification must incorporate this richness, as well as strive tablished the phylum Prerhodophyta for this lineage, which has
to recognize monophyletic groupings. Much work has been unfortunate evolutionary connotations. To the best of our
completed over the past decade, particularly for the Florideo- knowledge, this name has not been validly published because
phyceae and more recently for the Bangiophyceae, to resolve Seckbach (1987) failed to provide a Latin diagnosis and we
monophyletic lineages, but there has been general (exceptions were unable to identify subsequent validation in the literature.
noted previously) hesitation to implement taxonomic changes Further, it is a descriptive name, and its use is thus not required
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1503

under the ICBN. Doweld (2001) has provided a typified des- Metarhodophycidae Magne Cryptogamie Algologie 10: 112
ignation to this lineage at the phylum level, which we accept (1989).
here. At the current time, only the single order, Cyanidiales T. The characters of subphylum Metarhodophytina are consis-
Christensen, and family, Cyanidiaceae Geitler, are recognized tent with the subclass Metarhodophycidae Magne (1989);
in this phylum. Considering the substantial genetic diversity the former is validated by citation of the latter taxon. The
among the isolates studied thus far (Gross et al., 2001; Pinto characters are essentially as outlined next for the single
et al., 2003), future taxonomic divisions within this group are class included in this lineage.
likely.
Class Compsopogonophyceae G.W. Saunders et Hommer-
Phylum 2: Rhodophyta Wettstein 1901 sand classis nov.
Rhodophyta cum monosporangiis et spermatangiis separatis
Comments—This name has long been associated with red ex cellulis usitatis per parietes curvatos; corpus dictus
algae at the phylum level. The application of a typified name, ‘‘Golgi’’ cum reticulo endoplasmatico consociatus; lamella
Rhodymeniophyta, by Doweld (2001) is a superfluous act that cingens in chloroplasto adest; historia vitae (ubi cognita)
will only add unnecessary confusion to the taxonomic litera- generationibus duobus.
ture. We thus retain the original descriptive name. Red algae with monosporangia and spermatangia usually
cut out by curved walls from ordinary vegetative cells; Gol-
Subphylum 1: Rhodellophytina Cavalier-Smith 1998 gi–ER association; encircling thylakoids in the plastid; life
Unicellular or pseudofilamentous red algae with variable history biphasic if known.
plastid morphologies and organellar associations; sexual re- Order 1 Compsopogonales Skuja 1939: 34. (includes Boldi-
production unknown. aceae Herndon and Compsopogonaceae Schmitz)
Order 2 Erythropeltidales Garbary et al. 1980 (includes Ery-
Class Rhodellophyceae Cavalier-Smith 1998 throtrichiaceae G.M. Smith [cf. Silva, 1996])
Order 3 Rhodochaetales Bessey 1907 (includes Rhodochae-
Characters as for subphylum. taceae Schmitz)
Order 1 ‘‘Porphyridiales 1’’ (in Fig. 2; including Rhodella, on
which the class and subphylum are based)
Order 2 Stylonematales K. Drew 1956 (Porphyridiales 2 in Comments—The new subphylum is an elevation in rank of
Fig. 2, includes Stylonemataceae K. Drew) Magne’s (1989) Metarhodophycidae. Although it could be ar-
Order 3 Porphyridiales Kylin ex Skuja 1939 (Porphyridiales 3 gued that the Erythropeltidales be subsumed into the Rhodo-
in Fig. 2, includes Porphyridiaceae Skuja) chaetales, the two orders are distinct in a number of regards
(Zuccarello et al., 2000) and are as divergent at the molecular
level as are some of the florideophyte orders relative to one
Comments—Although we would prefer a taxonomic eleva- another. We thus continue to recognize these orders as distinct.
tion of the Archaeorhodophycidae Magne (1989; his group There is considerable confusion regarding the authorities to
was largely monophyletic, and use of this taxon would be many of the taxa in this subphylum, and particularly the Er-
consistent with proposals for other subphyla discussed later), ythropeltidales; the reader is directed to Silva (1996) in this
we use a restricted (remove Cyanidiales and Compsopogon- regard. A recent study by Nelson et al. (2003) indicated that
ales) concept of Cavalier-Smith’s (1998) subphylum Rhodel- at least some of the taxa now included in this lineage have
lophytina, which is presumably based on Rhodella, i.e., a typ- lost the diagnostic pattern of sporangial and spermatangial de-
ified name, and can be unambiguously assigned to this group. velopment and converged on the mode of division more typ-
We similarly emend his class Rhodellophyceae. Cavalier- ical of the Bangiales. This is an interesting discovery, one that
Smith’s taxa are problematic in that they are not based on a requires considerably greater investigation by red algal sys-
‘‘legitimate name of an included family based on a generic tematists, but not one that would alter the overall taxonomic
name’’ (ICBN Art. 16.1) and are not, as we understand the hierarchy presented here.
code, automatically typified. This presumably could be reme-
died when necessary taxonomic proposals are applied to Por- Subphylum 3: Eurhodophytina G.W. Saunders et Hom-
phyridiales 1 (Fig. 2), which include Rhodella and currently mersand subphylum nov.
lack familial or ordinal level classification. We have refrained
from presenting formal taxonomic proposals for Porphyridi- Eurhodophycidae Magne Cryptogamie Algologie 10: 112
ales 1 pending inclusion of Phragmonema, type of the family (1989).
Phragmonemataceae, in overall phylogenetic analyses among The characters of subphylum Eurhodophytina are consistent
porphyridialean algae. Classification for this subphylum is thus with the subclass Eurhodophycidae Magne (1989); the for-
an interim recommendation to reduce unnecessary taxonomic mer is validated by citation of the latter taxon. General
congestion in the literature. This class is likely paraphyletic characteristics include: Golgi in an endoplasmic reticulum/
and, as was the case for the Cyanidiophyceae, will need con- mitochondrial association; life histories where known bi-
siderable taxonomic restructuring in light of the exceptional phasic or triphasic; pit plugs present in at least one stage
levels of divergence noted among and within the three com- of sexual life histories.
ponent lineages. Silva (1996) provides an excellent summary
of the nomenclature pertaining to this group, particularly with Comments—Macrorhodophytina Cavalier-Smith (1998) was
regards to the ordinal designations. a subphylum erected to contain all of the Eurhodophytina as
defined here, as well as the Rhodochaetales. As circumscribed,
Subphylum 2: Metarhodophytina G.W. Saunders et Hom- it is too broad to be applied to any of our groups, and because
mersand subphylum nov. it is a descriptive, rather than typified name, it cannot be un-
1504 AMERICAN JOURNAL OF BOTANY [Vol. 91

ambiguously allied to a specific group of taxa. Use of priority sistent with the order Hildenbrandiales Pueschel and Cole
is not mandatory for taxa above the rank of family (ICBN Art. (1982); the former is validated by citation of the latter tax-
11.9) and is only recommended (ICBN Art. 16B) for typified on. Diagnostic features include: red algae that are crustose
taxa (i.e., descriptive taxa are not included), and thus we reject and smooth to tubercular or with erect branches; composed
Macrorhodophytina here in favor of an elevated status for of a basal layer of laterally adhering branched filaments and
Magne’s Eurhodophycidae, which was a monophyletic group- laterally adhering simple or branched erect filaments; te-
ing and is thus unambiguously assignable to this lineage. We trasporangia zonately or irregularly divided, apomeiotic,
consider that the two distinct lineages in this subphylum borne in ostiolate conceptacles; sexual reproduction un-
should be recognized at the class level. known; pit plugs with a single cap layer and membrane.
Order Hildenbrandiales Pueschel et K.M. Cole 1982: 718.
Class 1: Bangiophyceae A. Wettstein 1901
Life history biphasic, heteromorphic, gametophyte macro- Comments—Hildenbrandiales have not changed in familial
scopic, initially uniseriate, becoming pluriseriate or foliose composition since granted ordinal designation (cf. Pueschel
by diffuse growth; carposporangia and spermatangia pro- and Cole, 1982).
duced in packets by successive perpendicular divisions;
sporophyte filamentous, with pit plugs, a single cap layer Subclass 2: Nemaliophycidae Christensen 1978
present but lacking membranes; typically forming concho- Pit plugs characterized by two cap layers.
spores in fertile cell rows. Order Nemaliales Schmitz in Engler 1892
Order Bangiales Nägeli 1847 Other orders listed in Fig. 2 (lineage 2)
Comments—Although monophyly of Bangiales is beyond Comments—Nemaliophycidae have been the subject of a re-
dispute (cf. Müller et al., 2001), the component genera are not cent taxonomic review (as lineage 2), and the reader is directed
natural entities (cf. Müller et al., 2003; and references therein) to Harper and Saunders (2002) for an updated perspective of
and are characterized by SSU divergence levels among species the included orders and their constituent families (summarized
that dwarf some ordinal level distances among florideophytes in Fig. 2).
(Oliveira et al., 1995). A considerable amount of taxonomic
work is required in this group, which will undoubtedly lead Subclass 3: Ahnfeltiophycidae G.W. Saunders et Hommer-
to the recognition of many more genera and families (currently sand subclassis nov.
a single family, Bangiaceae) among these morphologically
conservative species. Carpogonia terminalia sessiliaque; carposporophytum ex-
trorsus exoriens; obturamenta intercellularia nuda, opercula
Class 2: Florideophyceae Cronquist 1960 et membrans carens.
Growth by means of apical cells and lateral initials forming Carpogonia terminal and sessile; carposporophyte devel-
branched filaments in which the cells are linked throughout oping outward; pit plugs naked, lacking caps and mem-
by pit connections; life history fundamentally triphasic con- branes.
sisting of gametophytic, carposporophytic, and tetrasporo- Order 1 Ahnfeltiales Maggs et Pueschel 1989: 349.
phytic phases; reproductive cells (monosporangia, sperma- Order 2 Pihiellales Huisman et al. 2003
tangia, carposporangia, tetrasporangia) generally terminal
or lateral on the filaments; carpogonia terminal or lateral, Comments—Huisman et al. (2003) have recently established
bearing an apical extension, the trichogyne, to which the the order Pihiellales and should be consulted along with
spermatangia attach; carposporophyte developing directly Maggs and Pueschel (1989) for a discussion of diagnostic fea-
from the carpogonium or its derivative. tures, as well as family–level taxonomy.

Comments—Doweld (2001) introduced the typified name Subclass 4: Rhodymeniophycidae G.W. Saunders et Hom-
Rhodymeniophyceae for this class. Although some may argue mersand subclassis nov.
that it would be better to use a typified name for this taxo- Rhodophyta cum historis vitae generaliter generationibus
nomic entity (i.e., move away from descriptive names, cf. Sil- tribus; carposporophytum ex carpogonio vel cellula fusioni
va, 1996), the Florideophyceae trace back to the Floridées La- statim exoriens, vel cellula auxiliari indirecte exoriens; ob-
mouroux (1813)—the first time red algae were grouped to- turamenta intercellularia cum membranis solum (Gelidiales
gether as a distinct lineage. It has also been applied for over cum operculo intrinseco unico).
a century to an unambiguous taxonomic construct. We thus Red algae with sexual life histories generally triphasic; car-
reject Rhodymeniophyceae as an unnecessary name that will posporophyte developing directly from the carpogonium or
only add confusion to the taxonomic literature. The included carpogonial fusion cell, or indirectly from an auxiliary cell
subclasses (discussed next) constitute the traditional Florideo- that has received the postfertilization diploid nucleus; pit
phyceae and are derived from the four lineages of Saunders plugs with membranes only (single inner cap in Gelidiales).
and Kraft (1997). Order Rhodymeniales Schmitz in Engler 1892: 19.
Other orders listed in Fig. 2 (lineage 4).
Subclass 1: Hildenbrandiophycidae G.W. Saunders et
Hommersand subclassis nov. Comments—Saunders et al. (2004) have recently completed
Hildenbrandiales Pueschel et K.M. Cole American Journal for Rhodymeniophycidae (as lineage 4) a comprehensive mo-
of Botany 69: 718 (1982). lecular systematic survey, which includes a listing of orders
The characters of subclass Hildenbrandiophycidae are con- with their recognized families (summarized in Fig. 2).
October 2004] SAUNDERS AND HOMMERSAND—RED ALGAL SYSTEMATICS 1505

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