Oceanogr. Mar . Biol. A111111. Rev.

1992, 30, I 148

Margaret Barnes, A . D . nsell and R . N . Gib on, £di1ors
UCL Pres

231029
THE RHODOPHYTA : SOME ASPECTS
OF THEIR BIOLOGY. III

STEVE . M RRAY 1 and PETERS . DIXO

1
Depar1me111 of Biological Science, California S1a1e UniversilJ'. Fullerion , California ,
USA 92634
2
Depar1me111 of Ecology and £volu1io11ary Biology, Universi1y of California, Irvine,
California, USA 9271 7

ABSTRACT Red algal biology is reviewed with emphasis on cellular bio logy,
morphology, genetics, reproduction, life hi tories, and systematics. Red a lgal cell
walls, calcification , pit plug , chloroplast , cell and tissue adhesions and fusion ,
protoplasts, specialised cells and stru ctures, and chromosomes, nuclei, and cell
division features are discussed . The limited information on red a lga l genetics and
molecular biology, including hybridi ation studies, is reviewed . Principles of thallus
con truction and development arc evaluated together with the data available on cell
division, cell enlargement and cell differentiation , and the adhesion a nd integration
of filaments in pseudoparenchymatous floridcophycids . The mechani m of
wound-healing and regeneration are described. The wide variety of asexual and
sexual reproductive structures are detailed and evaluated . In forma ti on on asexua l
reproduction by spo res and vegetative propagation is summari ed . Sexual repro-
duction i reviewed a nd the variou type of red algal life history are enumerated
and discussed . Informa ti on on th e life his tory is provided for 345 florideophycid
taxa. Proposa ls for the evolution of red alga l life histories are presented and research
on the enviro nm ental contro l of life-history events, with emphasi on photoperiodic
respon es, is a nalysed . A to ta l of 46 photoperiodic re ponses (43 short-day, 2
long-day, and I dual day-length), mos t (38) of which invo lve the development or
relea e of reproductive bodies, are identified for 42 red algal species. Views o n red
alga l sys tema tics have cha nged dramatically during the pa t decade. Remark on th e
criteria used for taxonomic discrimination a nd eva lu atio ns of the status of the 17
(4 bangiophycid and 13 florideophycid) order recognised in this review are presented.

TRODUCT!O

The present contribution represent a re-evaluatio n of topics considered

previou ly (Dixon, I 963a, l 970a) in the first two review of thi eries,
together with a urvey of advances made during the past two decades.
Since the la st review (Dixon, l 970a), there has been a phenomenal surge
in publication s co ncerning the biology of red a lgae. Two books (Di xon,
1973; Cole & Sheath , 1990) have provided summ a rie a nd a na lyses of
advance in the understa ndin g of red a lga l biology. Tn addition, four major
treatment of the cora lline group of red a lgae (Johan en, 1974, 198 1; Littler,
1972; Woelkerling, 1988) and two introductory surveys of red a lgal biology
(Dixon & Irvine, 1977; Desi kachary , Krishnam urth y & Ba lakrishnan, 1990)
2 STEVE N . M U RRAY AND PET E RS . DIXO

have been publi shed. These work s have been supplemented by discussions
of the red algae appearing in several genera l alga l texts a nd edited algal
volumes (e.g., Prescott, 1968; Kum ar & Singh , 1971 ; Tokida & Hirose, 1975;
Bold & Wynne, 1978, 1985; v.d . H oek & Jahns, 1978; Trainor, 1978; Christen en ,
1980; Lee, 1980, 1989; C layton & K ing, 198 l , 1990; Dawes, 198 l ; Lobban
& Wynne, 198 l ; Dixon . l 982a ; Sze, 1986; South & Whittick , 1987; Gabrielson.
et al., 1990) and more than 7000 original research articles that have appeared
in the literature during the past two decade . Thi large amount of published
material is due partly to an increase in the number of investigators intere ted
in the red algae a nd a concomitant increase in their research activity . It is
a lso due, however, to a significa nt increa e in outlets for publication . For
example, there has been an expan ion in the number of serial publications
that frequently contain phycologica l articles and in specia l aggregate
publications such as symposia proceedings and dedicated vo lumes during
the past decade. Thi tremendou growth in red algal literature i particularly
noticeable to the second author, who wrote the first two reviews (Dixon,
l 963a, l 970a) in thi s series and an early comprehensive text on red a lgal
biology (Dixon, 1973). lt is not intended that the present con tribution should
be based on, or provide, a total comprehensive bibliography of articles
published o n the red algae during the past 20 year ; indeed, thi would be
nearly impossible . We have elected to focu this review on the cellular biology,
morphology, reproduction, life histories, a nd ystematic of the red a lgae.
In particular, this review is intended to draw attention to developments in
those areas of red algal biology where ideas have changed a nd where new
critical information has become avai lable .

TABL E [
Orders of Rh odop hyta recogni ed in thi review . All taxa are co nsidered to
belong to the single cla Rh odophyceae (after Woelkerling, 1990)

Order

Ba ngiop hycid red a lgae

Bangia les
Compsopogona les
Porphyndi ales
Rh o d oc h ac ta l~s

Flondeophyc1d red algae

Acrochactialcs
Ahnfolualcs
Bal rachospcrmales
Bo nnema is on 1a !es
Ccramia lcs
orallinalcs
Gchdialcs
G1 ga rtinalcs
Graciianalcs
I illdcnbrandialcs
cmalialcs
Palma n ales (1nclud1ng Rh odophyscmataccac)
Rh odymc males
 ........................................
._.

RHODOPHYTA. I ll 3

As suggested by Woelkerling ( I 990), we have accepted a total of I 7 red

alga l orders (4 bangiophycid and I 3 florideophycids) , including the proposal
that taxa historica lly a signed to the Cryptonemia les (excluding the
Cora llin aceae and Hildenbrandiaceae) be included in the Gigartinales , in
preparing this review (Table I). We a lso agree wit h the proposal (see
Gabrielson , Garba ry & Scagel, I 985; Garbary & Gabrielson , I 990) that the
formal division of t he red a lgae into classes or subclasses Bangiophyceae
and Bangiophycidae and F lorideophyceae and F lorideophycidae cannot be
supported.

CELLULA R BIOLOGY

Great progress in understanding the cellular biology of red algae has been
achieved during the past two decades, particularly at the ultrastructural level
due partially to refi nements in fixation and embedding procedure . As
summarised by Pue chel ( 1990), red algae possess various cellular features
that are unequaled a mong eukaryotes, including: chloroplasts characterised
by unstacked and even ly spaced thylakoids and phycobilisome pigment
granules; deposition of s tarch granules in the cytosol; unusual pattern s of
as ociation of cis-Golgi with other cellul a r organelles; presence of pit plugs
formed at the co mpletion of cleavage; and the complete absence of centrioles
and flagella . Red alga l cells are believed (Pueschel, 1990) to be generally
typical of eukaryotes in terms of the structure of the plasmalemma, rough
and mooth endoplasmic reticulum , mitochondria , and nuclear features (i.e.,
nuclear envelope, pores , and nucleoli) ; the ize of non-polyploid interphase
nuclei of most red algal cells is, however, extremely small (3- 5 µm). During
the past two decade , red a lga l cytology has been the topic of reviews by
Duckett & Peel (1978), Brawley & Wetherbee (1981), and Pue chel (1990).
The ensuing discussion will focus on selected features of red algal cytology,
including the composition of the cell wall, the phenomenon of calcification,
pit plug and chloroplast st ructure, cell and tissue adhesions and fusions,
protoplast formation, the function of pecialised cells a nd structures, and
chromosomes, nuclei , and selected aspects of cell division .

THE CELL WA LL

The organisation and chemical composition of red algal cell wall are unique
among all other a lgae and plant (Craigie, I 990). All red algal cell wal ls
which have been examined o far how a similar ba ic tructure: they are
composed mainly of poly accharide and can be divided into an inner layer
which is not (or only ery slightly) extractable with boiling water and an
outer layer which i more readily soluble. The inner portion of the red algal
cell ' all i made up of cr) talline polysaccharide, including mall amount
of cellulose in mo t pecie , but i replaced by polysaccharide containing
o-xylo e. o-galacto e and o-mannose in certain bangiophycid (Frei &
Preston. I 961: Pre ton. 1974). Previous)) , it had been thought that cellulo e
wa absent from the cell walls of all bangiophycid red algae (Preston , 1974)
and that thi · chemical di tinction wa of major y tematic ignificance . We
nO\\ kno''· howe\er, that cellulo e can be a con tituent of the cell wall of
4 STEVEN N . MURRAY AND PETERS . DIXON

the conchocelis phase but be ab ent from the larger, 'leafy' and
parenchymatous phases of bangiophycids such as Bangia and Porphyra
(Gretz, Aaronson & Sommerfeld, 1980, 1984, 1986; Mukai. Craigie & Brown ,
1981; Gretz, Sommerfeld & Aaronson, 1982; Gretz & Vollmer, 1989) . It is
now believed that cellulose is present in sma ll amounts in the walls of all
red algal species with the possible exception of members of the Porphyridiales ·
(Gretz & Vollmer, 1989). When present, the cellulosic content appears to be
less than 12% of purified fractions of red algal ce ll walls (Pre ton, 1974;
Gretz et al., 1980, 1986; Mukai et al., 1981), an amount much le s than that
found in other algal and plant groups (Craigie, 1990).
The water-soluble carbohydrates, which form from 30- 70% of the dry
weight of red algal cell walls (McCandless, 1978) and which have been
described very aptly as " mucilages", have been used commercia ll y for many
years. As a consequence of their economic importance, these water-soluble
components are relatively well-known in terms of chemica l tructure and
occurrence and their systematic significance has recently been a matter of
considerable interest. Essentially, the water-soluble components are complex
ulphated galactans which can be divided into two major categories, the
agarocolloids and the carrageenans. The agarocolloids con ist of both
gel-forming agars such as agaro e and non-gelling or weakly gelling forms
called agaroids (Craigie, 1990). The specific biochemistry and the resultant
gelling and other properties of the agarocolloids produced by a particular
red alga are quite variable because agarocolloids are often heterogeneous in
composition. Considerable variation also occurs in carrageenan biochemistry
among red algal species and it is unusual for any red seaweed to contain
only one carrageenan type (Craigie, 1990). The different carrageenan forms
are based upon the sulphation patterns and the di tribution of 3,6
anhydro-o-galactose in the repeating structura l units (McCandless, 1978) .
Craigie ( 1990) distinguishe three families of carrageenans based on these
chemica l variations: the kappa family including kappa and iota carrageenan,
the beta family, and the lambda family including lambda and omega
carrageenan.
In addition to the various carbohydrate constituents, red a lga l cell walls
contain small amounts of protein . The structural characteristic a nd
functions of these proteins are poorly understood, although it is probable
that in addition to playing a structural role, wall proteins are involved in
transport of ions and organic molecules and the synthesis, modification a nd
degradation of wall polymers, and also may be important in cell-to-cell
adhesion, function in detoxification, and provide physical protection
(Craigie, 1990).
Two interesting components of red algal wall structure are the essentially
proteinaceous cytoplasmic trand s, which are said to permeate the wall. and
the so-called "cuticle" which forms an outer boundary layer of the wall.
Considering first the former, the walls of many red algae have been hown
by electron microscopy (e.g., Cottier, 1971; Duckett & Peel, 1978; Young,
1978, 1980; Goff, 1979; Young & West , 1979) to contain extensio ns of the
plasma lemma ranging in breadth from 30 to 50 nm and in length to I µm
or more. The functions of these strands have been tated to be in wall
construction (Cottier, 1971 ; Duckett & Peel , 1978) or nutrient tran fer
between host and para ite cells (Goff, 1979). At the same time there have
 RHODOPHYTA . Ill 5

been questions as to whether these structures are real (see Gordon &
McCandless, 1973; Brawley & Wetherbee, 1981) and Pueschel (I 980a) states
quite emphatically that in Pa/maria palmata the supposed extensions or
plasmalemma-villi are fixation artifacts.
The outermost region of many red algal cell walls is often conspicuous in
sections examined either by light or transmission electron microscopy (e.g.,
Hanic & Craigie, 1969; Chamberlain & Evans, 1973 ; Scott & Dixon , I 973a,b;
Gerwick & Lang, 1977; Young, 1980) and can contain up to as many as 20
layers in Chondrus crispus (Cottier, 1971 ). This multilayered region of the
wall has been referred to as a "cuticle" and has been shown to consist of
as much as 80% protein in Porphyra umbilicalis (Hanic & Craigie, 1969)
and 50% protein in lridaea (Gerwick & Lang, 1977). Such a proteinaceous
layer also occurs in green and brown algae (Hanic & Craigie, 1969). This
outermo t layer ha been associated with the iridescence found frequently
in Chondrus crispus (Cottier, 1971) and lridaea (Gerwick & Lang, 1977), as
supported by the observations of Pedersen , Roomans & Hofsten (1980) who
found that in iridescent Chondrus crispus, a multilayered outermost region
of the wall occurred whereas multilayering was absent in non-iridescent
individual . Although the term "cuticle" is often applied to this outermost
region of the wall in red and other algae, this structure is very different
chemically from that to which this term is applied in higher plants where
4-hydroxyproline i a constant feature . Hence, the u age of the term "cuticle"
needs to be applied with caution to algal cells and thalli (Dixon, 1973).

ALCIFICATION

Deposition of calcium alt is common to some organisms of almost all algal

group . Calcium carbonate is by far the most common calcium salt to be
depo ited and in the algae, the anhydrous salt exists in two crystalline forms,
calcite and aragonite, which differ not only in form but also in specific gravity,
hardne , and olubility. In addition, calcium ion can be replaced by
magnesium and other cation of smaller radii in calcite and strontium and
other cations of larger radii in aragonite (see Dixon , 1973 ; Craigie, 1990) .
Calcite i rhomboidal while aragonite is orthorhombic and although most
animals deposit a mixture of these two forms this does not appear to occur
in any algal species.
Calcification within the red algae ha been observed only in ftorideophycid
and i a primary characteristic of the Corallinales. Calcification also occur
among certain members of the emaliales, Batrachospermales, and the
Peys onneliaceae of the Gigartinales . Members of the Corallinales are unique
among calcified rhodophyte and other algae a they deposit calcite wherea
in all other calcified algae aragonite is the principal deposited form
(Penteco t, 19 0; Johansen, 1981; abioch & Giraud, 19 6).
In calcified red algae, the calcifying crystal of calcite and aragonite are
ob erved in the cell wall within an organic matrix (Borowitzka, 1977,
19 2a,b: Borowitzka & e k, 1979; Penteco t, 19 0), although the calcified
deposits may be either intra- or extraparietal or may be imultaneou ly both
intra- and e traparietal in location . Little is known of the preci e structural
or phy iological mechani m for calcium carbonate depo ition (Craigie,
1990). etwork of organic fibre have been demon trated in the wall of
6 STEVE N MURRAY A D PETERS . DIXO

decalcified coralline algae (Giraud & Cabioch, 1979) and it is believed that
the calcification process in crustose Corallinale is omehow controlled by
a polysaccharide matrix (Cabioch & Giraud, 1986). Jn addition, the process
of calcification is in some manner believed to be either re ultant from as yet
unexplained cellular metabolic event or due to removal of carbon dioxide
and bicarbonate during photosynth sis (Littler, 1976). Calcification is known·
to be energy dependent (Okazaki, 1977), can proceed in the light at a rate
ten times that occurring in .the dark (Borowitzka, 1982a), and is inhibited.
at lea t in the green seaweed Halimeda, by chemical that also inhibit
photosynthesis (Borowitzka & Lark um , 1976). Pear e ( 1972). studying
calcification in Bossie/la orhigniana. collected data upporting the hypo-
thesis that calcium carbonate depo ition was related to carbon dioxide with-
drawal and hydroxyl production taking place during photo ynthesis. Very
occasionally, calcareous deposit occur in specimens of the fre hwater
Batrachospermum or, particularly, in the marine pecies ema/ion
helminthoides containing a heavy endophytic infestation of the cyanobacterium
Ca/othrix . These deposits are of unknown chemical composition but they
are probably in the form of hydrated calcium carbonate (CaC0 3 ·6H 20)
resulting from the excessive uptake of C0 2 . Although photosynthesis and
the calcification process are clearly clo ely linked (Borowitzka, 1986). CaC0 3
depo ition can occur in darkness (when photosynthesis doe not occur) and
even in killed cells (Borowitzka. 1982a). If calcification were only linked to
C0 2 extraction then , a empha i ed by Littler ( 1976). the que lion rai ed
originally by Lewin ( 1962) remains unanswered : why do not all marine algae
calcify? As noted by Craigie (1990) in hi recent review. the mechani m
initiating CaC0 3 depo ition in red and other marine algae yet needs to be
elucidated .

PIT PLUGS

The term " pit plug" is now u ed exten ively for the structure which until
very recently were referred to as " pit connections". although it had been
indicated earlier by Dixon (1973) that the term pit connection was ""most
inappropriate in that the structure wa neither a ' pit ' nor a 'connection ' " .
Since the application of transmission electron micro copy to algal cytology
more than 30 years ago there has been considerable interest in the red algal
pit plug. The basic structure of the pit plug established by Ramus (1969a,b)
ha been confirmed repeatedly by later inve tigators (e .g .. Aghajanian &
Hommersand, 1978; Scott, Bosco, Schornstein & Thomas. 1980; Pueschel
& Cole, 1982; Davis & Scott, 1986). As a consequence of the incomplete
centripetal furrowing of the plasmalemma during cellular division, the
aperture which remains is occupied fir t by cisternae and then filled by
granular, proteinaceous material referred to as the plug core; after core
deposition . the tubular membranes disappear leaving behind the
membrane-lined plug (Pue chel. 1990). Thus, cytoplasmic continuity between
daughter-cells formed by the cell division is severed, although the original
plasma membrane remains on the periphery of the plug core . ing
freeze-fracture techniques, Pue chel (1977) was able to how that in most
red algae, additional membranes called cap membrane occur on the upper
and lower sides of the plug core. In these cases. the plug core is complete!
 Rl-IODOPHYTA . Ill 7

membrane-bound and lie outside the cytoplasmic contents of either

daughter-cell.
Many minor structural variations have been described for pit plug . They
may change in hape a nd size with cell maturation a nd between different
pha es in the life histo ry of a ingle taxo n (D uckett, Buc hana n, Peel &
Martin, 1974; Wetherbee, 1979, 1980; Wet herbee & Scott, 1980; Wetherbee
& Kraft, 198 1). Major variations in pit plug structure occur, however. among
rhodophytes and these have been found ( ee Pueschel & Cole, 1982) to have
sy tematic significance. These variations include the pre ence or absence of
the cap membranes a sociated with the plug core and whether, in addition
to the cap membra nes, a cap consisting of one or two outer layers of material
i a l o present. In addition, if there are two cap layers, the outer cap layer
may either form a thin plate or appear as a large dome-like structure. When
two-layered, the cap membrane lies between the two cap layer (Pue chel,
1989). According to Pueschel ( I 980b, 1990), the outer cap layer is formed
by the Go lgi apparatus and endoplasmic reticulum and, at least in five red
a lgal orders (Trick & Pueschel, 1990, 199 1), is composed of glycoprotein.
To date, little information appear to be available concerning the chemical
composition or origin of the inner cap layer.
The detailed structure of the pit plug appears to be conserved among
related taxa and, a a con equence, thi feature has recently acquired
considerable importance in discriminating between red algal orders (Pueschel
& ole, 1982; Pueschel , 1987 , 1989). For example, cap membrane are ab ent
in the bangiophycid red algae, the Ahnfeltiale (a delineated by Magg &
Pue chel, 1989) and member of the Corallinale (Pue chel. 1987, 1990) and
the e obser ation appear to be valid and not merely due to fixation artifact
(Pue chel & Magne, 19 7; colt, Thomas & aunders, 1988). Other variation
in pit plug tructure that appear to characteri e red algal order are the
number of cap layer and the morphology of the outer cap la yer (Table fl) .
One controver \ hich i till unre olved concern the po ible role of the
pit plug with re pect to tran location of material between cells. lt ha e en
been ugge ted that the pit plug in the carpo poroph) te of Polysipho111a
11ovae-a11gliae are tructurally peciali ed for nutrient transfer (Wetherbee,
1979. 1980) although thi interpretation has been que ·tioned (Pue chel.
19 Oc) . nother problem regarding the role of the pit plug concern the
apparent re-opening of the aperture between cell \\h1ch occur during the
m1grat1on of nu lei through the po 1tion prenousl) occupied b) the pn plug.
This has been obse ned (01\.on. 1973) during porang1al. spermatangial or
\egetall\e regeneration. de\elopmental e\ents \\h1ch lll\oh·e the tran fer
between cells of con · iderable quant1lle of C)topla m.
It ha been 1..nO\\n for more than a centur) that pit plugs can al o form
between adJUcent thallus celb that are not of 1..mdred origin Pn plug
formation can occur secondaril) through the producuon of a pec1al lateral
cell \\ h1ch then fuses \\ nh an adjacent thallus cell re ult mg m the recel\ mg
cell becommg mulunucleate This mode of econdar) pit plug formauon is
\\ 1Jespread among members of the eram1.1ks. ther reports. part1cularl)
111 pec1e l)f Hildc11/>ra11dw and member of the Coralhnale ( ab1och. 19 I).
uggest that secondar) pll plugs al. o can be formed b) means other than
cell ru swns \\1th the recel\ mg cell remL11ning unmueleate. ltra trm.:tural
1mes11g,uwns ( abwch & 1raud. 19 I. 19, 2. Pueschel, 19 ) ha\e
8 STEVEN MU RRAY A D P ETE RS . DIXO

TABLE II
Variatio ns in pit plug structu re amo ng red a lga l orders (a fter Pue chel, 1_9~0) .
TL= outer cap layer co nsisting of a thin line; TP =o uter cap layer con 1sting
of a thin plate; LD =outer cap layer consisting o f a la rge dome; na =
character not found in group; +=character present; - =character absent

Cap la yers

Plu g Cap Number of Outer cap

Order core membrane layers la yer

Bang1ophyc1d red algae

Bangiales + I TL
Compsopogonales + 0 na
Po rph yndiales na na na na
Rhodochaetales + 0 na

Florideophyc1d red algae

Acrochaetiales + + 2 TP or LD
Ahnfcltialcs + 0 na
Batrachospermales + 2 LD
Bonnema1so111ales + + 0 na
Ceramiales + + 0 na
Coralhnalcs + 2 LD
Gelid1ales + + I TL
G1garl1nales + + 0 na
Gracilariales + + 0 na
1-hldcn bra ndia Jes + + I TL
emalialcs + + 2 TP
Palmanales + + 2 TP
Rh odymernales + + 0 na

confirmed that such secondary pit plugs are produced directly, pre uma bl y
by the perforation of a common wa ll (Cabioch, 197 1).

C HLOROPLASTS

Algal chloroplasts are highl y di ver e in their structure, shapes a nd size , a nd

the photosynthetic pigments that they contain. The chloroplas ts of members
of the Rh odophyta are unique from other photosynthetic algae a nd plants
in many ways and are an important feature used to define the division .
The crucia l difference in the tructure of the chloropla t of red a nd
o ther algae occurs at the ultrastructural level where it ha s been demon trated
that red alga l chloroplasts are characterised by: single, unstacked a nd even ly
spaced thylakoids which are encircled by usuall y one (or in certai n taxa more
than one) peripheral thylakoid, an envelope consisting of two membranes:
and the absence of an a sociated urrounding shea th of endoplasmic
reticulum . In addition, the characterist ic photo ynthetic pigments.
phycoer) thrin , phycocyanin and allophycocyani n, occur in electron den e
granule called phycobilisomes that are attached to the stromal urface of
the photosynthetic membranes (Duckett & Peel. 1978; Brawley & Wetherbee,
1981; Pueschel, 1990). The phycobilisomes are knov. n to have a definitive
tructure and have been characteri ed as a macromolecular complex of
______________________ ...................
RHODOPHYTA . Ill 9

phycobiliproteins. which absorb light energy of variou wavelengths, bound

together by linker polypeptides in such a manner a to orientate the
phycobiliprotein chromophore units (Gantt, 1989, 1990). In Rhode/la vio/acea
(Moer chel & Rhiel, 1987) and Porphyridium purpureum (Redlinger & Gantt,
1981) the phycobilisomes consist of a core containing allophycocyanin
connected to peripheral rods composed ofphycocyanin, nearer the core, and
ultimately phycoerythrin. The actual size and shape of the phycobilisomes
vary among specie (Gantt, 1980, 1986, 1990), but the two mo t common
structural types are hemi-discoidal and hemi-ellipsoidal (MacColl &
Guard-Friar, 1987).
The number, shape, and disposition of chloroplasts within red algal cells
are variable, particularly among the Acrochaetiales and bangiophycids
(Gabrielson et al., 1990). Chloroplast morphology is also known to vary in
different life-history phases of the same pecies in cases where thallu
morphologies also differ (Pueschel & Cole, 1985). Red algal chloroplasts
vary in the presence or ab ence of pyrenoids and the presence or absence
and, when present, the disposition of internal thylakoid features. Based on
these structural characteristics, Hara & Chi hara ( 1974) prepared a
preliminary grouping of the chloroplasts of red algae consisting of nine
categories as shown in Table TIT. They ob erved that the chloroplasts of
most bangiophycid belong to their Nema/ion-type and that their
Po/ysiphonia-type chloropla t is characteri tic of most florideophycids.
Pyrenoids appear to be confined to the bangiophycids and certain member
of the emaliales sensu /ato and to be lacking in more advanced florideo-
phycids. Additional research on more red algal species needs to be performed
before the significance of Hara & Chihara's (1974) chloroplast groups can be
fully appreciated.

CELL AND TISSUE ADHESIO SA D FUSIONS

Contact between cells, filaments or axes resulting in adhesion or fusion

occur much more frequently in red algae than one might appreciate from the
literature, as di cussed by Dixon ( 1973) and, more recently, by Maggs &
Cheney (1990). In the latter paper which deals with competition studies,
Magg & Cheney ( 1990) indicate that "cooperation, rather than competition,
is the most significant feature of intraspecific interactions" in cases where
sporelings and crusts of a single species occur together in coalesced
masses. An examination of mature florideophycid thalli reveals that, other
than in those ca e where the morphology consists of simple, branched
filaments, the form of the pseudoparenchymatous thallu is brought about
by the adhesion · of filaments into complex aggregations. Under certain
circumstances, particularly in culture, the adhesion of filaments can break
down so that the complex thallus is reduced to a simple system of isolated
'acrochaetioid-like' filaments. othing is known of the cause for either
adhesion between filaments to produce florideophycid pseudoparenchyma
or the breakdown in culture of these adhesions into their imple filamentous
constituents.
Contact between independent multicellular thalli may also result in the
adhesion of axes (Rueness. I978a: Maggs & Pueschel, 1989) and, in general,
it would appear that such attachment is formed as a result of a contact
 0

TABL E III
Types of chloroplasts in the red algae (after H ara & Chihara, 1974). +=characteristic is present; - =characteri stic is a bsent;
n/a =characteristic is not applicable
en
-I
Modified tT1
Characteristic Nema/ion-type Nemalion-t ype He/mi111hoc/adia-type Liagora-type Rhode/la- type Polysiphonia-ty pe Batrachosperm11m-typc <
tT1
z
Pyrenoids + + + + + - - z
Outermost
lamellae - -
s::
- - + + c
Bundles of ;o
tubular lamellae - - - ;o
- + >
Shape Stellate Parietal Highly Highly Hi ghly Di scoid Di scoi d -<
lobed and lobed and lobed and or or >
stellate stella te stellate parietal pariet al z
Numbers per cell
Site within cell
Single
Axile
Single
Peripheral
Single
Axile
Single
Axile
Single
Axile
Ma ny
Peri pheral
Many
Periph eral
.,,
0
tT1
Floridean starch -I
grains covering tT1
;o
pyrenoid matrix - + + + n/a n/a en
Thylakoids
surrounding the 0
pyrenoid matrix + + + - n/a n/a x
0
Patterns of
thylakoid
sys tem wi thin a
pyrenoid matrix Irregular Througho ut Irregular Throughout Free n/a n/a
 RHODOPHYTA . 111 II

stimulu . Rhizoids may develop from both participating axes a lthough it

has been claimed (Fritsch , I 945) th a t such development occur o nl y when
both axes a re of the sa me species.
In addition to adhesion , there are also various types of cell fusion that
occur in red a lgae making these organisms model systems for stud ying cell
fusion processes. Fu ion s resultin g in the formation of seco nd a ry pit plugs
a re proba bl y those for which the red a lgae a re best known. [n most cases,
the development of a seco ndary pit plug involves the formation of a latera l
cell (the so-called "conjunctor cell'', sepa rated from its mother-cell by a pit
connection) and its subsequent fu sio n with a nother adj acent ce ll. Thi s type
of seco ndary pit plug formation res ults in the receiving cell becoming
binucleate through the transfer of the nucle us from the co njuncto r cell. Tn
addition to their formation between cell s within the sa me thallus, seconda ry
pit plugs can also form between a so-ca lled "parasite" and its host species
(Peyriere, I 98 I ; Goff & Coleman , I 985) , with a nuclea r transfer effected so
that the recipient cell co nta in s th e nuclei of two different species ho used
together within a common cyto pla sm . Th ere is a lso evid ence that fusions
ca n occur between so ma tic cell s in the Corallina les and other cru tose red
algae without the production of a conj unctor cell, in which case the fused
cells belon g to the sa me ge netic individu a l (Cabioch, 1970; Cod omie r, 1973;
Han sen, I 977; Saunders, M aggs & Mc l ac hl an, I 989). Fusions ca n, however,
a lso occur between cell s of genetica ll y distinct individuals as reported to
take place between cells of ma le a nd female filaments in Griffithsia tenuis
(Waa la nd , 1978).
Another type of cell fusion a nd ad hesion can occur in connection with
the in situ germination of spo res wit hin a tetrasporangium . fn any
tetrasporangium, from o ne to fo ur spores may fail to be released and each
may germin ate within the spo ra ngium to give rise to a new individual which
thereby remai ns a ttached to the parent tetrasporophyte thal lus. Although a
tetra pore germling formed in this manner may eventua ll y detach, in some
cases it may bind permanently to the tetrasporophyte and, should thi s
happe n, it is often difficult to di tinguish between the parent thallus,
presumably dipl oid, a nd the tetraspore germling, presumably haploid .
G ametangia may be formed on the tetraspore germling which has the
appea ra nce of an adventitious latera l axis of the tetrasporangial thallus. Tt
i possible that some of the many reports of the occurrence of different types
of gametangia and tetrasporangia on the same tha ll us may result from such
in situ development of tetraspore instead of other mean such as mutations
in a ll ele regulating sex differentiation a apparently occurs (Van der Meer,
I 986a. I 990a) in Graci/aria tihahiae and other pecies. A slightly different
phenomenon has been known for many year where the four products of a
tetrasporangium germinate, coalesce and fuse to produce a single product
which i obviously of compound genetic origin . This mode of sporeling
production ha been termed "syntagmatic germination" by Tokida &
Ya mama to (I 965). who ob erved that in Pachymeniopsis yendoi the
"compound" tetrasporeling remained fused with the parent tetra porangial
thallu .
Yet another adhe ion phenomenon involve coale cence of germinated
pore at the poreling tage . Thi wa first de cribed for Graci/aria 1·errucosa
by Jone (1956) who showed that clu tered spore coale ced and that thi
12 STEVEN N. MURRAY AND PETERS. DIXON

led to accelerated growth and development. There have been numerous other
investigations of sporeling coalescence in related red algae such as Chondrus
crispus (Chen & Taylor, 1976; Tveter & Mathieson , 1976; Tveter-Gallagher
& Mathieson , 1980), Mastocarpus (as Gigartina) stellatus (Tveter & Mathie-
son, 1976; Rueness, l 978a), and Gymnogongrus pat ens and Phyllophora
trail/ii (Maggs & Cheney, 1990). Following coalescence, the original
individual sporelings may be indistinguishable if the process is initiated at a
sufficiently early stage altho_ugh a furrow due to cellular damage at the
junction between two sporelings may be apparent if initiation begins when
the sporelings are more mature. Secondary pit plug formation can take place
between adjacent sporelings and , as noted by Maggs & Cheney (1990),
probably occurs much more frequently than noted in the literature.
Obviously, fusion and adhesion could have significant genetic consequences
although little is known apart from a few particular examples. Hence,
the phenomena of sporeling coalescence and fusion and syntagmatic
germination may be of ecological and evolutionary significance, particularly
if these processes result in what Maggs & Cheney ( 1990) refer to as a
" super-organism ". Genetic investigations of all types of red algae are still
in the earliest stages but the possibilities of chimeras produced by the cellular
fusions of different individuals may well be the explanation for many
apparently anomalous situations. This topic clearly deserves further and
more detailed investigation.

PROTOPLASTS

Although the production of isolated protoplasts from higher plants has been
achieved relatively frequently and protoplasts have been used extensively for
various physiological, cytological and genetic purposes, protoplast research
in seaweeds is still relatively new. For the red algae, the genetic manipulation
of protoplasts is a particularly promising field for future research as it is
possible using protoplasts to produce hybrid genomes from species that are
otherwise not sexually compatible. Methods for isolating and culturing
protoplasts have been developed for only a few red algae. Protoplasts have
been isolated in several laboratories from several species of Porphyra (Zhao
& Zhan, 1981 ; Tang, 1982; Polne-Fuller & Gibor, 1984, 1986; Polne-Fuller,
Biniaminov & Gibor, 1984; Saga & Sakai , 1984; Fujita & Migita , 1985, 1987;
Polne-Fuller, 3aga & Gibor, 1986; Saga , Polne-Fuller & Gibor, 1986; Chen,
1986, 1987, 1989; Chen , Hong & Craigie, 1988; Araki & Morishita , 1990;
Fujita & Saito, 1990; Waaland, Dickson & Watson , 1990). Protoplast
isolations have been reported for only a few other genera , e.g., Porphyridium
(Lee & Tan , 1987), Chondrus (Smith & Bidwell, 1989; Le Gall, Braud &
Kloareg, 1990), and Graci/aria (Cheney, 1984; Cheney, Mar, Saga & Van
der Meer, 1986).
Fusion of isolated protoplasts and subsequent cell division in resultant
protoplast-derived cells have been demonstrated but their regeneration into
whole thalli has been accomplished only rarely in seaweeds (Evans & Butler,
1988). Similarly, only a few red algal genera (five species of Porphyra , and
single species each of Chondrus, Gelidium , and Agardhiella) have been
reported to regenerate whole thalli from either cell or tissue culture (Cheney,
1986). Although the reasons for the low success in regenerating red algal
thalli from protoplast-derived cell masses are unknown , Cheney et al.
----------------------------------·
RHODOPHYTA . Ill 13

( 1986) suggest that a lack of "morphologically competent cells" in the

protoplast-derived tissue or the absence of a crucial morphogenetic substance
in the culture medium (which is necessarily free or nearly free of bacteria)
may be responsible.
fnterestingly , no investigator has yet made any connection between
protoplasts and the wall-le monospores that occur in certain species of red
algae. Of the types of sporangia reported in bangiophycid red algae, Drew
(1956) distinguished three types of which her Type 2 represented wall-less
monospores produced from undifferentiated vegetative cells. The occurrence
of such monospores has al o been detected in culture in ftorideophycid red
algae even when they have not been reported in the field . In certain cases,
monosporangia producing these monospores have been described (Dixon ,
1973) as "little-differentiated and the process appears to consist of little more
than the release from a cell of its contents". The relationship between such
simple, wall-less monospores and protoplasts is another topic worthy of
further investigation .

SPECIALISED C ELLS AND STRUCTURES

Certain red algae have an iridescent appearance that may or may not be
associated with specialised cells which have variously been termed "gland",
"vesicle", or "secretory" cell . Although iridescent structures have not always
been localised within such specialised cells, at least in some species iridescence
can be associated with the occurrence of special intracellular iridescent bodies
(Pellegrini , Gaillard & L'Hardy-Halos, 1989). As discussed previously,
iridescence in Chondrus crispus and lridaea is associated with a laminated
"cuticle" whereas in Fauchea laciniata some property of the cytopla m itself
is the cau e for the marked blue cast characteristic of this species (Dixon,
1973). The ecological significance of iridescence is unknown .
In past year there has been much controversy regarding the function of
gland or vesicle cells, but it is now obvious that these specialised cells are
of several different types and have divergent functions (Feldman:i, l 970a,b;
Feldmann & Feldmann, 1975; Young, 1978, 1979a,b; Young & West , 1979;
Young, Howard & Fenical, 1980). For example, in certain members of the
Bonnemaisoniale and Ceramiales, ve icle cells appear to be involved in the
accumulation of halogenated products (Pueschel, 1990). The gland cell
located in the inner cortex of Botryocladia apparently ecrete mucilage into
the in1erior space in the thallus (Young, 1978) and , in Opuntiel/a, special
colourless cortical cells appear to be involved in the storage of protein
(Young, 1979b) . It is apparent that many more chemical and fine structural
investigations of these specialised cells and ve icles are needed before any
general conclusion can be reached regarding their structura l relationship
to torage, secretion or iridescence. For many red algal species, the structure
and function of refringent and apparently specialised cells remain completely
unstudied and ince 1980 little research has been published on this interesting
topic .

CHROMO OME , N C L E !, A • D CE LL DIVISIO

Earlier tudies of chromosome number and morphology, and mitosis and

meio is in red algae, summari ed pre iou ly by Magne (1964a) and Dixon
14 STEVE . MURRAY AND PETERS . DIXON

( 1966a), were obviou ly limited by the resolution of the available optical

equipment due to the small ize of the nuclei and the even mailer dimen ions
of the chromosomes. As a re ult, co nts of red algal chromosome were not
easy to o btain (a si tuat ion that still exists) and severa l publi hed value are
suspect a nd probably inaccurate. Knowled ge of chromosome structure and
chromosome numbers ha , however. increased during the past two decade ·
but by no mea ns a much a~ the understa nding of other a pect of red algal
cell bio logy.

Chromosomes
Con idering fir t the number of chromosomes, the recent summary of counts
provided by Cole ( 1990) includes data for a pproxima tel y twice the number
of species listed previo usly by M ag ne ( l 964a) and Dixon ( l 966a), or reported
by Desikacha ry, Krishna murth y & Ba lakri shnan ( 1990). Even o, counts are
avai lable for only about 5% of the total number of red algal specie and
provide a very non-representative coverage of taxa, although data are now
available for a ll red alga l orders with the exception of the Hildenbrandiale
(Cole, 1990). Cole ( 1990) reports that the haploid chromo ome number in
red algae ranges from 2 to 68 72, with lowest numbers recorded for species
in the Porphy ridia les and Ba ngia les and hi ghest number for tho e in the
Ceramiales and Gigartinales. With respect to chromoso me number, Porphy ra
is the most thoroughly tudied rhodophyte genu a nd counts are now
available for about 56 of the 65 + species (Cole, 1990).
Secondly, a ignificant adva nce made si nce the last review of this series
(Di xon, l 970a) relates to the increa ed understa nding of the tructure of
individual chromo o mes in a particular complement. The be t that could be
said previou ly was that chromo omes were spherical, sli ghtl y elongate, or
elongate, and occurred in different sizes or were all of the sa me ize. It is
now clear th at unlike the ca e in terrestrial plant a nd other algae, red algal
chromo omes are extremely sma ll (see Di xo n, l 963b, l 966a) and range in
length from 0.25 µm to abo ut 3.5 µm (Co le, 1990). Knowl edge of karyotypes
in red algae is beginning to become avai lable, together with knowledge of
chromosome number and chromo ome morphology a nd event uch as
chia mata and chromosome pairing in meio tic situatio ns. The amount of
information is still ve ry small, a nd i limited to on ly a very few genera such
a Bangia (C:)le, Hymes & heath, 1983), Porphyra (Yabu, 1969a; Ka pra un
& Fre hwater, 1987), Furce!laria (A u tin , 1960a,b), a nd Polysiphonia
(Kapraun, unpubl. in Cole, 1990). Centromere and their po itions have
now been observed in P . jlexicau/is (R avanko, 1987), Wrangelia tay /oriana
(as W. argus) (R ao. 1970, 1974), Bangia 1•ermicularis (Co le et al., 1983),
Porphyra papenfussii (Conway & ole, 1973), and Harveye!la mirabilis
and Odo111ha/ia jloccosa (Goff & Cole, 1973). This repre ent a conside-
rable improvement over information available previously, but tudie have
till been limited to only a minute fraction of the red algae. An additio nal
observation of intere t i the ugge ted occurrence of sex-dete rmining
chromosomes in Wrangelia rayloriana (as W . argus) (R ao. 197 1). On the
ba i of tetraspore germination producing equal, or approximately equal,
number of male and female gametangial thalli in Antithamnion
spirograp/;idis. Drew ( l 955a) uggested that ex determination was due to
 RHODOPHYTA . III 15

the segregation of sex chromosomes during meiosis . Apart from the report
of Rao (1971), there have, however, been no other identifications on
structural grounds of sex chromosomes in the red a lgae . Evidence
contradicting the existence of separate sex chromosome in Graci/aria
tikvahiae ha s been obtained by Van der Meer ( l 986a, l 990a). For G. tik vahiae
it has been demonstrated that sex determination is controlled by the
regulation of a single pair of Mendelian factors or alleles found in a limited
region of one of the chromosomes, and that gametophytic or tetrasporophytic
characteristics are controlled by the homozygous or heterozygous condition
of these alleles refuting the concept of separate sex chroma omes (Van der
Meer & Todd, 1977; Van der Meer, 198la , 1986a) . Knowledge concerning
the chromosomal or genetic ba is of sex determination in red algae is a n
area in need of much additional stud y.

Nuclei and cell division

Ultrastructural investigations of the proces of red algal cell division have
provided significa nt advancements in knowledge which recently have
contributed greatly to the development of hypot heses concerning red algal
evolution. Unfortunately, cell divi ion feature are known for only a few
red algal genera. As summarised by Scott & Broadwater ( 1990), mo t
inve tigations have concerned members of the Ceramiales (Peyriere, 1971 ;
McDonald , 1972; Scott et al., 1980; Phillips & Scott, 1981 ; Dave & Godward ,
1982; Broadwater, Scott & Pobiner, 1986a,b; Sheath, Cole & H ymes, 1987)
and Porphyridiales (Bronchart & Demoulin , 1977; Schornstei n & Scott, 1980,
1982; Scott, 1986) with only single studie available for Batrachospermales
(Scott, 1983) and Rhodymeniales (Davis & Scott, 1986). Cell division in the
Ceramiales appears to be quite uniform and, because members of this order
received the greatest attention during the earlier periods of fine structural
investigation, it was thought that the ceramialean mode of cell division might
be characteristic of all red algae. It is, however, now appreciated that cell
division varie among red algal species and that this variation appears to be
conserved a nd indicative of evolutionary patterns (Scott & Broadwater,
1990).
Certain aspects o f nuclear divi sion and cytokinesis appear to be similar
in the limited number of pecies inve tigated . As outlined by Scott &
Broadwater ( 1990), dividing nuclei have typical eukaryotic pindles. These
are enclosed within a nuclear envelope that remain intact throughout mitosis
except at the pole where there are gaps of various sizes. A nucleu -associated
organelle ( AO), unique to the red algae, occur at each pole with a typica lly
ring-shaped configuration . All specie produce a per i tent interzonal
midpiece or pindle that remains until nuclear division re ults m the
production of two distinct daughter-nuclei . Among the principa l variation
in red algal nuclear di i ion deemed to be of sy tematic importance (Scott
& Broadwater, J 990) are the morphology and behaviour of the A Os, the
presence or ab ence of a perinuclear endopla mic reticulum (PER), and the
characteri tic of the prometapha e-anapha e polar a rea . ing the e
features. cott & Broadwater ( 1990) ha e identified a working categori ation
of five type of red algal cell di i ion . The e are: the Porphyridium-.
Ba1rachosper11111111- . F/i11tiel!a-. Po/ysip/1011ia- . and Lomentaria-type (T able IV).
 °'

TABLE IV
Types of nuclear division i11 the Rhodoph yta based on ultrastructural features (after Scott & Broadwater, 1990)

Characteristic Porphyridium-type F/i111ie/la-type Botrachospermum-type Lomentaria-type Polysiphonia-type "'...,rn

<
Nucleus associated Bipartite: Bipartite: Bipartite: Bipartite: Bipartite: rn
orga nelle (NAO) large proximal small ring upon smal ring within large ring upon large ring upon
z
granule and small a ring a larger ring a ring a ring z
distal cylinder s:
Late prophase poles One nuclear pocket Two nuclear pockets Two nuclear pockets at Two nuclear pockets One nuclear envelope c:
;o
at each pole at each pole each pole at each pole protrusion at each pole ;;o
Pro me ta phase Absent Present Present Absent Absent >
m1crotubule filled -<
tunnels traversing the >
nucleus z
0
Metaphase nuclear Intact, except for one Intact except for Intact except for one Intact except for Intact except for many "O
envelope condition small gap at each pole one large gap at intermediate-sized gap two small gaps and fenestrations at rn
...,
each pole at each pole many fcnesrations each pole rn
at each pole ;;o
Pennuclear endoplasmic Absent Absent Present Present and Present and very abundant
reticulum (PER ) moderately
"'0
abundant x
K1netochore structure Small in size and simple Small in size ? Medium in size Large in size and layered 0
and simple and layered
Organelle associated with Enlarged, central Enlarged, cen tral Central vacuole Central vacuole Central vacuole
cytokinesis chloroplast chloroplast
 RHODOPHYTA . Ill 17

Much more work is needed, particularly on members of those red algal

orders where cell division has yet to be described at the ultrastructural level ,
before the full significance of the variable features of cell division in
determining systematic relationships amo ng the red a lgae can be appreciated.
One peculiarity of the mitotic process in certain red a lgae referred to the
Gigartinale was described from light microscopic investigations by Magne
( l 964a,b, 1978). Most obvious in Calliblepharis, the term "ca lliblepharidian
divi ion" was employed for this situation in which the nucleu in prophase
possessed a supposedly characteristic spind le shape. Unfortunately, little new
information has been obtained on this divisio n process during the past
decade, alt ho ugh o ne detailed examination of Chondrus crispus (Hanic, 1973)
wa unable to verify the occurrence of the "ca lliblepharidian" process
de cribed and figured by Magne (1964a,b, 1978) .
The genera l aspects of the process of meiosis observable with a light
microscope have been outlined by Magne (1964a) and Dixon (1966a) and
transmission electron microscopy has added relatively li ttle information that
would modify these genera lised patterns. The occurrence of synaptomena l
complexes indicative of meio is was first demonstrated for red algae with
the aid of the electron microscope by Kugrens & West (1972a). At the
ultrastructural level, meiotic cell division appears to resemble mitosi s with
only minor differences (Scott & Broadwater, 1990) although there has been
but a single detailed investigation of the entire process, in Dasya baillouviana
(Broadwater e l al., l 986a,b). Other investigation of meio i (Kugrens &
We t, l 972a; Scott & Thomas, 1975; Pue chel, 1979; Vesk & Borowitzka,
1984; heath el al., 1987) are not complete in all respects but ag ree in general
with the more detailed account of D. baillouviana . An exception is the earlier,
apparently erroneous, interpretation by Scott & Thomas ( 1975) that both
meiotic division apparently took place in a common nuclear envelope
without an intervening interkinesis. Accounts by Broadwate r el al. (1986b)
of the movements and position occupied by meiotic nuclei in Dasya have
now pro ided better understanding of nuclear behaviour during meio i .
The e indicate that the nuclear envelopes of the four po t-division nuclei
can become quite closely appre ed and in ome pecie their separation is
obvious, wherea in others ( ee cott & Thomas, 1975) distinct inter-
connection between nuclear envelopes can be ob erved .
It i now appreciated that almo tall red algal cell . unlike those of virtually
all other eukaryotes, spend the major portion of the cell cycle in G 2 , where
replicated copie of the nuclear genome are pre ent (Goff & Coleman , 1984,
19 7. 1990). Thi mean that a haploid red algal cell in G ~ ha the ame
total quantity of D as a diploid cell in G 1• and that the minimum D
level found in a particular organi m can only be encountered in G 1 haploid
cells.
The variation in nuclear size in different part of the ame red algal thallu
wa · de cribed b} Magne (1964a) and Dixon (1966a) and i al o empha i ed
b) off oleman ( 1990) in their recent re>1e\\. of red algal D . In nearly
all bangiophycid red algae. a ·ingle nucleu occur in each cell and thi
nu leu · doe not become pol} genomic (Goff & oleman , 1990). In
llorideophy td ·. howeYer, both uninucleate and multtnucleate cell often
oc ur. and 111terpha e nu let common!) ext t 111 a polygenomic tate. In
llondeophyctd red algae where the principa l apical cell 1 uninucleate. the
18 STEVE . MURRAY AND PETERS. DIXON

nucleus is often much larger than the nuclei of the derivative cells which are
produced by mitosis and cell division . Mito is occurs frequently in apical
cells (and also in germinating spores) during active growth and , using
DNA-specific fluorochrome and microspectrophotometric analy is, it has
become possible to learn much about nuclear behaviour in florideophycids
during cell division and growth .
Tn florideophycids, growth of thalli or spore germlings is al mo t exclu ively
accompli hed by mitotic divisions of apical cells and the en uing enlargement
of their derivative cells (Dixon, l 963a, l 970a 1973). As ummarised by Goff
& Coleman ( 1990), a florideophycid apical cell may have: ( 1) a single,
non-polyploid nucleus; (2) a single, highly endopolyploid nucleu ; or (3)
many, non-polyploid nuclei . The pa tterns of nuclear number and nuclear
ploidy level that arise as a con equence of mitotic divisions in florideophycids
have been shown to be reflections of the nuclear condition of the generating
apical cells (Goff & Coleman , 1984, 1986, 1987, 1990). Tn florideophycids
with uninucleate and non-polyploid apical cells, mitotic divi ions may
produce either uni nucleate or multi nucleate cell derivative (Goff & Coleman,
1990). the uninucleate cell derivatives may be either polygenomic or
non-polygenomic. Tn the former ca e, both polyploid (multiple chromosome
complements) and polytene (replicated genome without an increase in
chromosome number) conditions are possible; multinucleate cell deri atives
are generally non-polyploid (Goff & Coleman , 1990). When florideophycid
apical cells, such as tho e occurring in Polysiphonia, contain ingle , highly
endopolyploid nuclei, it appear that mitotic division ultimately produce
cell within which the number of nuclei increase during development but
where the ploidy level of each individual nucleu decreases (Goff & Coleman ,
1986). Thus, in this ca e, nuclear divisions within the derivative cells are not
accompanied by DNA replication. Where apical cells have multiple, non-
polyploid , nuclei such as in Griffithsia pacijica, it appears that during
cell division they produce derivative cells also containing multiple nuclei.
most of which are non-polyploid (Goff & Coleman. 1987).
In contrast to the decrease in nuclear size that can occur a cells become
more distant from their apical cell origins, in certain red algae there are case
where relatively large nuclei can be found in older, inactive cells that occup
location remote from thallus apice . Previously, attention was drawn
(Dixon , l 966a) to the occurrence of such large nuclei in cells for which both
cell division and nuclear divi ion had ceased . These are frequently figured.
without comment, as in the case of Plocamium cartilagi11e11111 . Here, the nuclei
are as large as 30 µm in diameter, and with age, migrate against the curved
wall of a vacuolate cell so that they are highly flattened and extremely
difficult to quantify volumetrically . If, however. measured carefully, nuclear
volume can be calculated and by comparing cells ofincrea ing age the volume
of the nucleus in the oldest cells can be shown to have increased in size by
value far exceeding error attributable to accuracy in quantification . The
cau e and functional repercu sions of uch apparent increases in nuclear size
are unknown .
Mea surements of nuclear ize using light microscopy have no\ gi en wa
to m1crosp.ectrophotometry in order lo determine the relationship between
the genomic content of a cell, it age and its size. It has long been reported
that there is a strong correlation between genome size and cell volume in
-------------------------------- ......
RHODOPHYTA . III 19

eukaryotic cells, i.e., larger cells have greater DNA content and larger nuclei
(Goff & Coleman , 1987, 1990). Florideophycid red algae are well known for
the enormous growth in cell volume that occurs with age, increases reported
by Dixon (1970a , 1973) to be as great as 44 000 times the volume at formation .
Consequently, red algae are ideal for research focusing on the relationship
between genomic content and cell size , an area still in need of much critical
study. Recently, Goff & Coleman ( 1987) established the existence of a
correlation between nuclear content and cell ize in Griffithsia pacifica, a
multinucleate ftorideophycid red alga with isomorphic free-living tctraspor-
angial and ganetangial phases. They explored the paradox that homologous
cells in the diploid and haploid generations of ' isomorphic' algae theoretically
should show twofold differences in their DNA contents and cell volumes,
but observations in upport of such differences appear to be unreported.
Goff & Coleman ( 1987) found that cell size did not differ between
homologous cells of the isomorphic gametangial and tetrasporangial thalli
of Griffithsia and that, despite ploidy level , homologous cells have the same
total quantity of nuclear DNA due to the fact that each diploid nucleus is
urrounded by a cytoplasmic domain that is nearly twice the size of that
surrounding a haploid nucleus. Although Goff & Coleman (1987) studied
homologous cells of species with isomorphic gametangial and tetrasporangial
life history phases, it is probable that a similar relationship between DNA
quantity and cytopla mic volume is a feature of all red algal cells. Jn support
of this premise, Garbary & MacPherson (in prep .) have recently demon-
rrated that an increase in nuclear length and at least some increase in
DNA content are associated with an increase in cell length in at least one
species of uniseriate and uninucleate red algae.

THALLUS MORPHOGENESIS

The simplest red algal thalli consist of free-living unicells, as in the case of
Porphyridium and Rhode/la, or unicells surrounded by a mucilaginou sheath
and indiscriminately organised into what Garbary, Hansen & Scagel
(I 980b) refer to as amorphous or pseudofilamentous colonies, as occur
in Goniotrichum . Red algal thalli can also be composed of cells arranged to
form one- or two-layered parenchymatous sheets, as for example occurs in
Porphy ra; however, most red algae and specifically the ftorideophycids are
filamentous or composed of packed aggregations of filament , which in the
latter case can produce thalli of considerable morphological complexity.
The need for a concise survey of the variou vegetative anatomies and
morphologie exhibited by Rhodophyta has been indicated in each preceding
review of this series (Dixon , l 963a, l 970a); it still exists . There have been
many descriptions of general vegetative structure provided during the pa t
two decade , but the e have merely expanded the bank of descriptive data
on individual taxa and generally have not led to the development of new
principles or interpretations of red algal morphogene is . As stressed during
previou discussions (see Dixon, 1973), the absence of a morphoge-
netic approach to the analysis of red algal morphologies can lead to
mi interpretations , ome of which have important systematic implications.
Other recent summaries of research contributing to the understanding of the
20 STEVE N MURRAY AND PETERS . DIXO

vegetative morphology and development of red algae have been provided

by Gabrielson & Garbary (1986), Coomans & Hommer and (1990), and
Waaland ( 1990). In this section, we shall focus on certain topics of importance
to developing an understanding of morphogenesis in the red algae. To date,
virtually all of the limited progres made in this area ha been obtained with
florideophycids and we still know very little about morphogenetic events iri
the generally less complex. multicellular bangiophycids.

SPORE GERMI ATIO

Various patterns of pore germination have previously been de cribed for

red algae and categori ed by various authors (e.g., Killian. 1914; Kylin, 1917;
Chemin, 1937; Inoh , 1947) as ummarised by Dixon (1973) . In his recent
review of sporangia and spore , Guiry (I 990a) describe five major modes
of spore germination in Rhodophyta : (I) ema!ion-type; (2) accaria-type;
(3) Ge/idiwn-type; (4) Dumontia-type; and (5) Cera111ium-type. A discu sed
by Guiry ( l 990a), despite the observation that general patterns exist, spore
germination is quite variable, particularly among the bangiophycids, and
there are many examples of pore germination pattern that fail to fit within
the confines of these five or other proposed categorie .
One major dichotomy in the mode of spore germination that ha been
emphasised previously involve the earliest stages of development.
Representatives of most florideophycid orders exhibit a unipolar pattern
of spore germination which often result in the production of a cru to e or
filamentous basal system prior to the development of erect thallus parts. In
contrast, a bipolar pattern of spore germination. referred to as the
Ceramium-type by Guiry (1990a) , result in the essentially imultaneous
development of basal attachment and erect thallus parts. This pattern of
development occurs throughout the Ceramiales, but also appear in members
of other red algal orders such as the Bonnemaisoniales and Bangiales. The
ecological significance of the e early developmental pattern remains
unexplored . Hypothetically unipolar germlings, which direct resources
towards the production of basal y tern , have, however. de elopmental
patterns that favour the advantage of secure attachment and perhaps
resi tance to dislodgement by wave action or grazers o er the presumably
greater productivity and growth rate of bipolar germlings that allocate more
energy, during early development, to the production of erect photosynthetic
thallu parts and less to ecure attachment.

LATER DEVELOPMENT

Historically, studies of red algal thallus development were confined to only

the earlie t stages due largely to problems encountered in su taining cultures
in the laboratory . The resultant reports of red algal morphogene i usually
failed to account fully for how the filamentous axes of florideophycid red
algae become aggregated to produce the mature thallus form and ho\
pattern of cell divi ion and cell enlargement are controlled v ithin this
developmental framework .
Gross aspects of thallus variation in any red algal taxon can be clarified
by gaining an understanding of the processes of axi formation and growth.
 RHODOPHYTA . Ill 21

This can be learned through sequential observation of individual th a lli

growing under different environmental conditions, as has been performed
for British pecies of Gelidium (Dixon, l 966b; Dixon & Irvine, 1977), a red
algal tax on once regarded as " un genre diabolique" because of its tremendous
morphological variability. Unfortunately, such studies are understandably
unpopular as they are laborious, exceedingly time-consuming and because
they are often regarded as of little importance other than to the taxonomic
specialist. As a consequence, there remains an immense amount of research
to be done on growth under differing environmental conditions before the
full extent of morphological variation within recognised red algal taxa can
be adequately understood even in those geographic regions considered to be
'well known ', uch as the British Isles.
Field observations of morphological variation must be interpreted on the
basis of the developmental patterns by which the thallus of a given taxon
achieves its final form. Despite the enormous differences in appearance
among about 2500 to 6000 species (see Woelkerling, 1990), the thalli of all
red algae are characterised by certain distinctive features . For example, the
florideophycid red algae all are filamentous or are formed by the aggregation
of filaments produced by the divisions of apical cells. There is some
intercalary cell division but from the evidence available (see Dixon, 1973),
such divisions appear to be a regular feature only in members of the
Delesseriaceae of the Ceramiales and the Corallinales. Following its
formation by apical division , a cell undergoes enlargement which frequently
i of considerable magnitude . The resultant file of enlarging cells derived
from active apical cell division often produce lateral branches by means of
the initiation of lateral apical cells. Branching, to a greater or lesser extent,
occurs in all the filaments making up fleshy florideophycid thalli, producing
a three-dimensional structure often of great complexity.
Of the red algae, the florideophycids offer more challenges and
opportunitie for morphogenetic analysis because, almost without exception,
patterns of symmetry are present involving control of cell division and cell
enlargement, the formation of lateral branches, apical dominance, and
interaction between filaments of different orders. By comparison, thalli of
multicellular bangiophycid red algae (with the possible exception of
Compsopogon) are relatively simple and generally fail to exhibit the degree
of symmetry characteristic of most florideophycid . Even in some
morphologically-simple bangiophycids, form variation can, however, be
quite considerable, as in the case of Asterocytis where a marine isolate
changed its morphology from filamentous to a uni- or bi-cellular form
resembling Chroothece when grown in pure culture in sea-water medium of
reduced alinity (Lewin & Robertson, 1971 ). The effects of alinity cannot
be the only factor involved in the determination of thallu form in these
poorly understood taxa as Chroothece has been reported from saline soils
and AsteroC) 11is has been collected from freshwater habitats .
The lack of a ynthetic understanding of morphogenesis in red algal thalli
i probably mo t ignificant in relation to the interpretation of the nature
of filamentous aggregation. This point ha s been uccinctly noted by
Gabrielson & Garbary ( 1986) who commented about "compariso ns made
u ing only feature of mature tructure " without consideration of
"developmental pathways leading to their formation" . This deficiency is
22 STEVEN . MURRAY AND PETERS . DIXON

most significant with regard to two generally accepted concepts which need
to be reconsidered critically not only with regard to their importance in
understanding morphogenesis of red algal thalli but also for evaluation of
their systematic implications. These are the concepts of "heterotrichy" and
the "uniaxial" or "multiaxial" nature of erect red algal thalli.

HETEROTRICHY

It has been appreciated for many years that algal thalli of many different
types have a heterotrichous organisation, i.e., they are differentiated into
filaments that are prostrate and adherent to the substratum and filaments
that are erect. The categorisation of red algal thalli into these two types of
filaments is most obviously applied to those ftorideophycids exhibiting
unipolar spore germination , such as members of the Gigartinales and
Corallinales, where an initial basal layer is first formed which then gives rise
to filaments that form erect axes if such occur. One critical feature that can
confuse interpretations of heterotrichous thallus development has been
indicated earlier by Dixon ( 1973); whether or not a thallus demonstrates a
primary heterotrichous organisation , the thallus as a whole may be
differentiated secondarily into axes which are prostrate and axes which are
erect. In Cryptopleura ramosa or Plocamium carti/agineum, the particular
mode of erect or prostrate growth appears to be determined by external
conditions and, although experimental verification is lacking, it would appear
that the realised developmental pathway is correlated with irradiance (Dixon,
1973). A convenient term for this developmental phenomenon is "secondary
heterotrichy " although there are obvious objections to the use of this
terminology . While in some red algal species secondary heterotrichy may be
a means of increasing opportunities for perennation under certain conditions,
in other red algae this mode of growth appears to be the sole form
characteristic of the taxon . For example, the crustose thallus of Rhizophyllis
squamariae resembles closely an erect axis of R. divaricata laid upon its side
but is of different construction than would be anticipated of a prostrate
system arising from a simple heterotrichous arrangement of filaments (Dixon,
1973). Although a complete morphogenetic analysis of thallus development
is unavailable, it appears that there may be a primary heterotrichous
arrangement of filaments in R . squamariae, with the erect filamentous axes
ultimately becoming prostrate to produce a secondary heterotrichous thallus .
In the Ceramiales, an initial primary heterotrichous arrangement of
filaments is always lacking because of the bipolar nature of spore
germination ; however, secondary heterotrichy often results in the production
of prostrate filamentous axes. Dixon ( 1973) has sugge ted that the
interpretation of thallus construction in the encrusting members of the
Corallinales is also complicated by the possibility of secondary heterotrichy.
In some genera of crustose corallines the prostrate thallus can be interpreted
as an elaboration of a primary heterotrichous basal system, whereas in other
such as certain species of Lithothamnion, the thallus resembles an erect axis
of Amphiroa laid upon its side and appears to be secondarily heterotrichous
in construction . Unfortunately, real morphogenetic studies of crusto e and
other Corallinales have been hampered by technical problems in maintaining
natural growth of these calcified plants in laboratory culture and a
 RHODOPHYTA . Ill 23

morphogenetic understanding of the development of coralline thalli is not

well under tood. Woelkerling ( 1988) has devised a descriptive system for
categorising thallus structure in coralline algae which fails to take into
account the pathway by which thallus development occurs. Studies designed
to follow the complete development of a mature thallus from a pore are
required before existing anatomical syntheses can be interpreted morpho-
genetically. Such interpretations will also lead to the elimination of terms
that contradict a morphogenetic concept of thallus development. An examj)le
is the use of the term "terminal initial" which has been applied inap-
propriately in Lithophy llum orbicu/atum (Chamberlain, Irvine & Walker, 1991)
to describe a meristematic apical cell.

AXIAL CONST RU C TIO

It has been customary to regard the basic organisation of the axes of erect
ftorideoph ycid thalli as being uniaxial, developing supposedly from the
activity of a single meristematic apical cell, or multiaxial involving a cluster
of actively dividing apical cells. Mo t past descriptive treatments of the
organi ational nature of the erect axes of ftorideophycid thalli have been
based on static anatomical analyses of mature apices and have not been
derived from sequential morphogenetic studies of axis development
commencing with spo re germination. In addition, the actual term uniaxial
and multiaxial have a confused history if one trace their origin and
ubsequent use . Consequently, misinterpretations a nd miscommunication of
the true nature ofaxi organi ation and development have been made because
of the failure to understand thallus morphogenesis and confusion in the
application of the terms uniaxial and multiaxial.
The origin of these terms to descri be the ax ial organi ation of erect
ftorideophycid axes traces to Oltmanns ( 1904) who was the first to de cribe
the st ructure of mature ftorideoph ycid thalli as being either " Zentralfaden-
typus" or " Springbrunnentypus". Hence, Oltmanns (1904), who wrote in
German , is credited with introducing the concepts of uniaxial and multi-
axial organisation. Although "Zentralfadentypus" is, however, synonymous
with the English " uniaxial' ', st rictly peaking "Sp ringbrunnentypus" i not
directly translatable to "multiaxia l". In stead, "Springbru nnentypus" is
interpretable as "fo untain type", a description that differ, although subtly,
from the generally accepted application of multiaxial. It appears that the
English conversion of Oltmanns' ( 1904) original terminology were made by
Frit ch ( 1945). Becau e thi translation was not strictly parallel in the case
ofmultiaxial, differences in interpretation can occur depending upon whether
or not one strictly adheres to Oltmanns· original usage or employs the term
sensu Frit ch.
Regardle of terminology. in certain red algae problem also occur in
clearly di criminating between uniaxial and multiaxial thalli . These were
rai ed and di cu ed many years ago by Frit ch ( 1945) and there are many
ca e \\here an a\is is referred to one type b) one inve tigator and the
opposite type b) another. One difficulty in interpretation involves certain
pecie of Dele eriaceae where the aggregation of what could be considered
individuall) to be uniaxial axes produce a webbed thallu by lateral
adhe ion: thus. no ingle. central filamentou ax1 ma) be distingui hable.
24 STEVEN N . MURRAY A D PETERS . DIXO

In other taxa, the degree of webbing varies during the life of a thallu and
appears to depend upon the rates of formation and growth of the lateral
axes. When formation and growth are slow, the central major axis is clearly
a uniaxial structure. When the formation of lateral axes occurs rapidly, they,
however, become aggregated and indistinguishable so that the apical
meristem of the main axis appears to contain not one but everal, virtually
identical apical cells. One of these 1s the apical cell of the principal filament
of unlimited growth that forms the body of the major axis, wherea the
others represent apical cells of the filaments of unlimited growth that
eventually will peel off laterally to form lateral axes. The first description of
this developmental phenomenon was provided for Gelidium by Dixon ( 1958);
more recently, Rodriguez & Santelices ( 1987) have described a similar
situation for Gelidium and other closely related gelidialean taxa. An
analogous situation occurs in Weeksia (Norri , 1971 ), where the thallus,
which is flattened and foliose, had been regarded as multiaxial. By observing
the events leading to thallu development, orris ( 1971) was, however, able
to show that the initial uniaxial thallu becomes multiaxial in appearance
through the webbing of the initial filament of unlimited growth with what
are, in actuality, lateral filaments of unlimited growth that comprise the
lateral axes . Analyse of the organisation of filaments comprising the erect
axes of Schi::.ymenia (Ardre, 1980) have revealed that the thallus is initially
uniaxial and then adopts a multiaxial appearance in a manner similar to
that described for Weeksia by orris (1971) . In D11111ol1fia. recent re earch
(Rietema, 1984; Wilce & Davi , 1984) has revealed with regard to axial
construction, a converse situation to that described for Weeksia. Here, the
thallus primordium is initially multiaxial, and then fragment into axes which
are ultimately uniaxial as the lateral filaments peel off from the central core.

FILAMENTO S ORGA ISATION

As described previou ly (Dixon, 1973), the thalli of all complex ftorideo-

phycid red algae consist of an aggregate of filaments so that they are
essentially of a pseudoparenchymatous nature. Some thalli are composed
of filaments that rarely branch whereas others consist of aggregates of richly
branched filaments . Variou terminologies have been u ed to describe the
latter, much-branched filamentous systems, where obviously several order
of filament:; exist. Surprisingly little attention ha been paid to the details
of development in such cases. One such study, however, is that of Aghajanian
& Hommer and ( 1980) on Ba1rachospennw11 sirodotii where patterns of
development were compared between different filaments and cell types and
three distinct types of apical cell were demonstrated based on nuclear and
cell division characteristics. A similar, but le s complete. investigation by
L' Hardy Halos (1971a ,b) on members of the Ceramiaceae g<n·e similar but
less detailed results . More invc tigation uch as these arc needed to improve
understanding of thallus morphogenesis in ftorideophycids .

C ELL DIVISIO AND CFLL FNL ARGFMFNT

Because florideophycid axes are polar and arise as a product of the di vi ions
of the apical cells of their filaments and the enlargements of the derivative
------------------------------------im
RHODOPHYTA . 111 25

cells produced by these apica l cells, factor affecti ng cell division or

enlargement rate play an important role in the development oftha llu s form.
Waaland (1990) has recently reviewed the small amount of information
available on cell divisio n, enlargement, and differentiation in red a lgae and
only a brief con ideration of these processes and how they relate to the
overall morphology of red algal thalli will be presented here. The influence
of the magnitude of irradiance and photoperiod on the rates of division of
apical cell s has been investigated in several florideophycids of relatively
simple filamentous construction (see Waaland , 1990) . In the case of
Pleonosporium squarrulosum, photoperiod and the quantity of irradiance
both influenced the rate of apical cell division , which was shown to increase
with the total dose of daily irradiance received up to a point of saturation
(Murray & Dixon , 1973) . Garbary (I 979a) found similar results for four
other Ceramiaceae, whereas Waaland & Cleland ( 1972) reported in Griffithsia
pacifica, that the rate of division of apica l cells require light, but is not
influenced by the quantity of daily irradiance received .
Cells formed by apical cell division characteristically undergo enlargement
of varying degrees as they mature. The magnitude of this enlargement can
be very slight, as is the case in members of the Acrochaetiales, or very large
such as occur in Ceramium echionotum and Lemanea fluviatilis where
100- and 1000-fold increases in cell length and 14000- and 44000-fold
increases in cell volume have been documented , respectively (Dixon, 1971 ,
1973). Several investigators (Murray & Dixon , 1975; Garbary, Grund &
McLachlan , 1978; Garbary, l 979b) have reported that the total dosage of
daily irradiance affects enlargement rates in ome florideophycids whereas
in others (Waa land & Cleland, 1972; Garbary, l 979b) no effect of the amount
of irradiance received appears to occur. It is now known that in the
florideophycids, cell enlargement involves the deposition of new wall material
rather than expansion of the pre-existing wall. In growing apical cells, new
wall material is deposited at the growing tips (Garbary & Belliveau, 1990).
In enlarging cells cleaved off by apical cell division, deposition may be in
the form of a band (see Waaland , 1990) or, as shown recentl y by Garbary
& Belliveau ( 1990), in certain Acrochaetiales and Ceramiaceae may be diffuse
throughout the wall .

POLARITY AND I TEGRATION OF THALLI

If easonal and environmental modifications of thallus form a re ever to be

fully appreciated in p eudoparenchymatou florideophycid s, the factors
governing adhe ion and integration of the composite filament must be
establi hed . At the pre ent time, little is known abo ut how the multi tudes
of individual branched filaments integrate to produce a characteristic thallus
form .
The development of complex red algal thalli is based upon cellular
adhesion to produce filament a nd filamentous adhesion to yield the axes
that form the integrated thallus . A indicated previou ly, in thalli of
multifilamentou florideophycid , increase in cell number occurs through
divi ions of the polar apical cell of each filament except in members of the
Deles eriaceae and Corallinale , where growth proceed by intercalary cell
divi ion instead of being exclu ively apical. In some genera of the
26 STEVE N . MURRAY AND PETERS . DIXO

Dele seriaceae, certain cells produced by the division of an apical cell initiate
what might be co nsidered as 'internal apical cells'. Once formed, these
internal apical cells behave imilarly to ordinary terminal apical cells in that
they cut off segments from their basipetal pole. Therefore, the p rincipal
thallus filaments initially consi t of a few cells formed by the division of
termina l apical cells, and then increase in cell number due to the divisioH
activity of the internal apical cells. A different type ofintercalary cell divi ion,
most readily demonstrated _in the genus Melobesia, occur in ome members
of the Corallinale . In these forms, short, erect and unbranched filaments
ari e from the cells of the prostrate basal system but their formation is
preceded first by the production of a terminal cap cell who e function is
related to calcium carbonate depo ition. Once formed, the cap cell does not
divide again, leaving the production of new cells forming the upright filament
to the meristematic activity of the subterminal cell. Thu , although the locus
of cell division in these two ca e differ from that where apical cells are the
exclusive means of increa ing cell number, the actual division process closely
resembles the apical activity characteristic of virtually all ftorideophycids.
In the multicellular bangiophycid , cell division is not localised in apical
cells, but instead is generally diffuse and occurs throughout the thallus with
the single exception of Compsopogon, where meristematic activity occurs in
the apical cell of the initial filament formed by the germinating spore.
The phenomenon of polarity of meristematic activity i matched by the
polarity displayed in ftorideophycid thalli during regeneration, where a cell
isolated from a filament will produce a new apical cell from what was
previou ly the acropetal pole and new rhizoid from what wa previously
the basipetal pole. This phenomenon of regeneration, whereby a single-celled
fragment can regenerate a complete thallus, obviously has profound
ecological significance and is one of the means by which red algae can be
i olated and grown in laboratory culture.
When a cell in a filament dies but without causing filament breakage,
regeneration can occur internally, apparently by ingrowths through adjacent
pit plug , although the evidence for this process is not explicit. s described
by Waaland ( 1990) and Kim, Kim & Lee ( 1988), this 'healing' process
involve the formation ofa new living fusion cell from adjacent 'repair cells' .
The living cell on the acropetal side of the empty. dead cell cuts off an
ingrowing rhizoidal regenerate, while the living cell on the basipetal side cuts
off an ingrowing apical axis . Upon meeting within the remnant walls of the
dead cell, the rhizoidal and apical repair cells fuse to form a new living cell.
This method , rt.ferred to a the "Fusion Type", was the most common
process encountered by Kim et al. ( 1988) among the 16 pecie of filamentous
Ceramiale that were employed in their studies of wound hea ling. A second.
les common process identified (Kim et al., 1988) as the "Non-fusion Type",
al o involves the production of new rhizoidal and apical repair cells from
supra- and ~ub-tending cell , but in lead of fusing, these develop a secondar
pit connection when they come into contact with one another. In the third
method of wound healing ob erved in filamentous eramiale . de cribed a
the " Elonga_tion Type" ?Y Kim et al. (1988), the adjacent living cell do not
cut off repair cells, but instead imply elongate filling up the ca it left b
the dead ce!l and then connect with one another by developing a secondar
pit connectton .
--------------------------------~·
RH O D O PHY TA . Ill 27

Besid es the si mple un iseri a te Cera mi a les tha t have se rved as ma teri a l fo r
most studies o f wou nd- hea ling a nd regenera ti o n, these processes have a l o
been o bserved in mo re complex fl o rid eo ph ycid . Fo r exa mple, Waa la nd
( 1990) reviews Perrone & Felicini ( 1972, 1974) a nd Perrone- Peso la &
Fel ici ni's ( 198 1) wo rk describin g the po la r regenera ti o n o f excised fragments
of Scho ttera nicaeensis (as Petrog/ossum nicaeense). Additi o na l evidence o f
po la r regenera ti o n a nd a pica l d o mina nce in fl orideoph ycid has been
obtai ned by Abela rd & L 'H a rd y-H a los ( 1975) fo r Apoglossum ruscifo /ium
where, despi te a rela ti vel y complex fl attened morph o logy, the principa l
fil a ment o f unlimited growth toge ther with the fi la ments o f firs t, seco nd ,
third , a nd ub equent o rders ca n readil y be identified . Excisio n of the a pex
o f the principa l a pica l cell resul ts in the fi r t order a pices co nver ting fro m
determinate to ac ti vely growing indeterminate modes, thus ta king over the
a ttribu tes of the principa l fi la ment o f unl imited grow th which had been
elimina ted .
Tn higher pl ants, pola rity, regenera ti o n, a nd a pica l d o mina nce a re as pects
o f mo rp hogenesis tha t in vo lve a n interactio n o f hormo na l a nd nutriti o na l
fac to r . D espi te the ava ila bili ty o f evidence for co ntro l o f a t least certa in
a lga l develo pmenta l p rocesses by ho rm o nes o r pla nt growth substa nces
(PGSs) tha t a re a lso acti ve in hi gher pla nts (see Augier, 1978; Buggeln , 198 1;
Jacobs, 1986) , there a re conflicting views o n the ro le pl ayed by these
substa nces in red a nd o ther a lgae (see Bradley, 199 1; Eva ns & Trewavas,
199 1). One example o f a develo pmenta l system th a t occurs in red a lgae
a ppea rs to be co nt ro lled by a ho rmo ne th a t has no a na log in hi gher pla nts.
Thi s is rhod omorphin , a substa nce tha t coo rdin a tes the cell repa ir p rocess
in severa l pecies o f Griffithsia (see Waa la nd , 1990). Rh od o mo rphins a ppea r
to be species specific glyco proteins o f a bo ut 15 000 kd that a re produced by
ingrowing rhi zoida l porti o ns o f cell s during injury; rh od o mo rph ins a re
kn own to induce di visions in cell s subtending inj ured cells a nd to mai nta in
the gro wth pa ttern o f the re ulta nt re pa ir cells (Waa la nd , 1990).
In fl o rideo ph ycid , where correla ti ons between the pola r developmenta l
processes o f indi vidua l cell s a nd who le fil a ments is hi ghl y suggesti ve o f
some tran sfer o r tra nsloca tio n behavio ur, the o nl y mea ns o f sympl as tic
co mmunica ti o n a ppea r to be via the co nnectio ns fo rmed between adjacent
cells durin g cyto kinesis. These a re, however, closed with in a sho rt time by
the pit plug which is sur ro unded in most red a lga l taxa by ca p memb ra nes,
producin g wha t wo uld seem to constitute a ba rrier to intercellula r
communica tio n. Therefo re, a n impo rta nt to pic for in ves tiga ti o n is the mea ns
of intercellula r co mmunica ti o n required to suppo rt the rigidl y co nt ro lled
developmenta l processes tha t produce the con i tent a nd complex pa ttern s
cha racteristic o f mature red a lga l tha lli . N o t o nl y the specific ho rm one o r
PGSs, if pre ent, bu t a lso the co rrid o rs fo r their tra nspo rta ti o n a nd d ispersa l
within red a lga l th alli need to be id entified . W ith rega rd to the la tter iss ue,
as Pue chel ( 1990) has stated the ro le o f pi t plugs in tra nspo rtat io n between
cell " has bee n the subject o f much specula ti o n, b ut p roof has been elusive" .

GE E T! CS
Ad va nces in understa nd ing the genetics of m ulticellul ar ea weeds have lagged
fa r behind the p rogre s made wit h unicellul ar green a lgae a nd most ot her
28 STEVEN N . MURRAY AND PETERS . DIXON

groups of organ isms (Van der Meer, l 986b, l 990a). For example, fifteen
years ago the extent of our knowledge of multicellular marine algae was
covered in only one (Fjeld & L¢vlie, 1976) of thirteen chapters of a compiled
volume on algal genetics (Lewin, 1976a); in comparison, eleven chapters
were devoted to unicellular green (six to Chlamydomonas) and one to the
blue-green algae. Various reasons have been offered for this lack of progreS'S,
most of which concern the facility with which multicellular marine algae
could be grown , maintained and bred in the laboratory. Many of the
problems in culturing seaweeds in the laboratory have, however, been solved
and today genetic studies of many species are highly practical.
Historically, most research on the genetics of multicellular marine algae
has been done by a limited number of investigators working on only a few
select species. For the red algae, this lack of attention is unfortunate given
the many interesting and important genetic problems in need of research
and the attributes exhibited by most red algae that make them appealing can-
didates for genetic study. These attributes were recognised by Lewin (1976b)
who indicated that red algae would make ideal subjects for studies of the
genetic basis of, for example: ( 1) nucleo-cytoplasmic relations in developing
cystocarps where in many species both haploid and diploid nuclei can be
found sharing a common cytoplasm; (2) fertilisation and compatibility
mechanisms where non-motile male gametes or spermatia appear to adhere
to and fuse only with the trichogynes of conspecific females; (3) the
development and function ofphycobiliproteins, the accessory photosynthetic
pigments; (4) differences in cell-wall biochemistry which in certain red algae
differ between morphological phases; and (5) morphological differentiation
of heteromorphic phases such as haploid gametophytes and diploid tetra-
sporophytes or diploid carposporophytes and diploid tetrasporophytes.
Furthermore, as emphasised by Van der Meer ( l 986b, l 990a), the reproduc-
tive modes of red algae, and specifically most florideophycids, present
advantages for genetic study , including: (1) the availability of haploid
individuals for genetic analysis; (2) the facility with which the individual
spores of meiotic tetrads can be isolated and their germination products
followed ; (3) zygote amplification which results in the production of hundreds
to thousands of genetically identical offspring from carpospores; and (4) the
availability of monoecious species to provide insurance against self crossing
during hybridisation studies .
Fjeld & L¢vlie ( 1976), in an earlier review of the genetics of multicellular
algae, summarised the totality of our knowledge of red algal genetics by
referring to a mere three studies compared with multiple references and
several pages devoted to describe the genetics of other seaweeds, particularly
the green algae Viva and Enteromopha . Since Fjeld & L¢vlie's ( 1976) review,
the Rhodophyta have, however, replaced the Chlorophyta as the most
prominent subjects of seaweed genetic research (Yan der Meer, l 986b) . This
has been largely due to the contributions of John Van der Meer and his
colleagues who have pioneered genetic studies on multicellular red algae and
specifically Graci/aria tikvahiae. Since the treatment of Fjeld & L¢vlie ( 1976),
review containing information on red algal genetics have been provided by
Yan der Meer (1986b, 1990a), and the interested reader is referred to these
contributions for a more complete coverage of the current state of knowledge
of red algal genetics.
--------------------------------~ ..
RH O D OP H Y T A . Ill 29

P A T TE R NS OF C H A R ACTE R I H ERI TANCE

G enetic resea rch invo lves not o nl y the tracing of pa ttern s of inhe rita nce o f
differen tia l characteristics fr o m o ne genera ti o n to the nex t, th e goa l o f
virt ua lly a ll of t he ea rli er genetic resea rc h reviewed by Fjeld & L¢v li e ( 1976)
a nd Va n d er M eer ( I 986b. I 990a), bu t a lso investigatio ns of th e m o lecula r
mecha nisms unde rl yin g suc h inh eri ta nce pa tte rns ( Lewin , 1976b). In the case
of th e Rh odo ph yta, most resea rc h to da te has focused o n a few, select
pheno typic c ha racterist ics (e.g., th a llu s pi gmentatio n a nd colo ur, ex a nd
phase de termina ti o n, a nd vario us morp ho logica l att ributes) that a re most ly
inherited in a M endeli a n fas hi o n . M o re a nd m o re investigators a re, however,
pursuing genetic q uesti o ns in the Rh odo phyta al th e m o lecul a r level a nd
soo n t he re will be dra m a tic inc reases in knowledge of red a lga l nuclea r,
chl oro pl a t a nd mi toc hon dr ia l genome and the nat ure a nd va riabi lity of
the pro tein p roducts (e.g., isozymes) that they p rod uce.
In sight into the ge ne tics o f red a lgae is ofte n gai ned by o bservi ng
mu tationa l phenotypes a nd fo ll owi ng the pa tte rn s of inheri ta nce ex hibited
by ind ividua ls ex p ressing these p heno types unde r co nt ro lled breeding a nd
growth co nditio ns. In vestigators have occasio na ll y identi fied a nd isola ted
spo ntaneo us red a lga l muta nts g ro win g in the fie ld a nd arising in la bora tory
c ultures. M utagen ic age nts, suc h as c hem ica ls o r UV rad ia ti o n , have a lso been
empl oyed to induce mu tat io na l event for genetic study (Va n der M eer,
I 986b , l 990a). M ost kn own red a lga l muta nts in vo lve phe no typic varia tions
in pi gmenta ti o n; seve ral a ffect th a llu s mo rph o logy . Va n de r M eer ( 1990a)
li sts 124 ide ntified genes tha t have been c haracterised by fo ll owing inheri ta nce
patte rns of id entified muta nts for Graci/aria tikvahiae, the most thoroug hl y
st udied red a lga. Thi s exceed s the genetic kn owled ge that has acc um ulated
(Va n de r M ee r, I 990a) fr o m gene ti c c ha racterisa Lio ns of a ll o th er red a lga l
species co m bi ned (55 muta nts occurrin g in a tota l of o nl y 12 othe r red a lga l
taxa).
Pa rtic ul a rl y useful fo r stud yin g M endelian in he ri ta nce patte rns in red a lgae
have been co lo ur muta nts whi ch ca n rea dil y be ide ntified when th ey ap pea r
in the fie ld o r in la bo ra to ry c ultu re. Co lo u r m uta n ts are known to arise
po nta neo usly in red a lgae a nd to occu r in vario us frequencies in nat ura l
a nd labora to ry po pul atio ns (Va n der M eer, I 986b, l 990a) . Fo r exam ple,
colo ur muta nts a ri se rela tively fre quentl y in G. tikvahiae c ul tures a nd in fie ld
pop ul at io ns of Chondrus crispus, but appear to occur Jes freque n tly in ot her
red a lgae whe re they have been recorded, e.g., Pa/maria pa/mata, De1•aleraea
ramentacea, Champia parvula, Gelidium vagum , and Porphy ra umbilicalis
(Va n de r M eer. 1990a.b; Kehoe & Van de r M eer, 1990) . Tn most cases
colo ur muta nt ex hi bit cla sica l M endelia n inheritance patte rn s but, in select
case , they d isp lay non-n uclear inheritance and deviate from Mendelian
inherita nce mod els. In t he case of no n-nuclear inherita nce, the co lour m utants
often result from mu tations in c hl orop last D A and the co lo ur mutations
are tra nsmi tted. o nl y by the maternal parent, which in most exually
reproduci ng red a lgae appear to be the exclusive cont ributor to the
chl o ro pl a t genome. Va n der M eer ( I 990a) lists 36 examp les in Graci/aria
tikvahiae a nd 34 in other pecies of red algae of colour mutations showing
nuclear inheritance and M endelian transmis ion patterns; thi compares with
o nl y 11 ca e in G. tikvahiae and 10 in all other red algal species where
30 STEVEN N . M U RRAY AN D P ETERS . DIXON

inherita nce is no n- nuclea r a nd a ppa rentl y maternally transmitted. Because

of their di stinctiveness a nd pigmentation characte ri stics, colo ur mutants have
been used not on ly for genetic studies but a lso , for exam ple, to work out
life-hi sto ry events (Va n der M eer & Todd, 1977 , 1980; Van der Meer &
Chen, 1979; Van der Meer, 198 1b,c) a nd to exami ne physiological processes
(Ramus, 1983; Ramu s & Van der Meer, 1983) .

SEX AND PHASE DETERMi ATIO

The genetic mechanisms underlying sex a nd phase determination in red algae

long have been a mystery. In addition, the rare occurrence of both ga metangia
a nd tetrasporangia on the same tha llus, o r what has been referred to as
" mixed phase" reproduction (Van der Meer & Todd, 1977), has intrigued
phyco logists for years. As indicated previously (Di xo n, l 970a, 1973),
occurrence of mixed phases appears more commo nl y in the Ceramiaceae
than in any other red a lga l gro up . Although studies delineating the ge netic
mechanisms resulting in ex and phase determination or the producti o n of
mixed phases have yet to be performed for most red a lgae including the
Ceramiaceae, some understanding of the genetic mechanisms for these
processes has been developed for Graci/aria tikl'ahiae a nd at leas t fo ur other
taxa . The limited genetic data o n sex and phase determination in red algae
have been reviewed by Van der M eer ( 1986b, 1990a) a nd also di scussed
briefly by Maggs ( 1988); only a brief summa ry will be provided here.
For G. tikl'ahiae, a sin gle pair of factors ap pea rs to exert prima ry control
over sex and phase determintion. These fac tors o r all eles a re inherited in
M endelia n fashion a nd have been shown by recombination st udies to be
located on a single chromosome (Va n der M eer & T odd , 1977; Va n der
M eer, 198 la). It is unclear whether the two factors represent a lterna tives of
a si ngle gene or if grea te r ge netic complexity exists. The ex pression of male
characteristics results when cell s of the haploid tha llus co ntain o nl y the male
allele and female characteristics occur when o nl y the female a llele is present.
A recessive mutation at a second locus, a lso inherited in Me ndeli a n fashion,
ca n, however, result in the expressio n of female charac teristics even on male
tha lli when the female a llele is no t present (Va n der M eer, Patwary & Bird,
1984; Yan der Meer 1986b). In addi tio n, diploid tetrasporo phytes of
G. tikvahiae, which have two reces ive a lleles a t the seco nd locus o r which a re
homozygous with either two ma le or two fem a le all eles, become mixed ph ase
thalli by for min g both gameta ngia a nd tetras pora ngia on the sa me individua l
(Va n der Meer & Todd, 1977; Van der M ee r, 198 1a, l 986b). H ence, dipl oid
tetrasporophytes that form o nl y tetrasporangia a re heterozygo us for the
male and female a lleles. It is now known that it is this heterozygosity in tead
of diploidy that in G. tikvahiae determines whether a tetrasporangial or a
gametangia l m orphology develops. Unfortunately, in Pa/m aria pal111ata,
Devaleraea ramentacea, Chondrus crispus, a nd Champia parl'tda, the other
red a lgae where some genetic in fo rma ti o n is ava il a ble. sex a nd phase
determination appear to be caused by different mecha ni sms. Of particular
interest, in light of the ob ervat ion for many red algal po pulati o ns th a t male
plants are rare or absent in the field, is a n unusua l repo rt for the normall y
dioecious Champia parvula out lined by Yan der M ee r (1990a). In C. parl'llla,
a life history can be perpetuated where gene tic female clones can develop
--------------------------------~im
RHODOPHYTA . 111 31

occasiona l pa tch es of functional sperma tangia . Following fertili sa tion ,

carposporophytes produced o n these genetic females develop carpospo res
which germinate into viab le tetrasporop hytes tha t a re homozygo us for the
fem a le a llele a nd whose tetra spores germinate exclusively into female plants.

HYBRIDISATI ON STUD I ES

Hybridi ation studies, where fertile pl a nts are brought toge ther to test for
their abi lity to cross, have been pe rformed on a growi ng number of red a lgae
to determine breeding relationships within a nd a mo ng recogni sed species
populations. H ybridi sation research has been umm a ri sed and di scussed
previously by Rue ness ( I 978a), Polanshek & West ( 1980), Mathieso n, orton
& Neushul ( 198 1), Van der Meer ( 1986b), and Hawkes ( 1990) .
H ybridisation studies have been useful in identifying ecotypes a nd
delimiting species boundaries, a centra l goa l of systema tics. Also , hybrid-
isa tion studies are va luab le in establ-ishing co nnection s between hetero-
morphic erect gametophyte a nd c ru tose tetrasporophyte pha ses, a nd
in dete rmining the genetic structure of po pula ti ons where either no n-sex ua l
direct development or heteromorphic sex ua l life hi stories ca n occur as is
known for Gigartina a nd Mastocarpus. Results of cross-fertili satio n tests to
delimit pecies have been repo rted for severa l Cera miales that are relatively
easy to maintain a nd breed in labo ra to ry culture, including species of
Antithamnion (S undene, 1959 , 1975; Rueness & Ruene s, 1975; Rueness,
I 978a), Ceram ium ( Rueness, I 978a), Aglaothamnion (l' H ardy- Halos &
Rueness, 1990) , Callithamnion (l'Hardy-Ha los & Rueness, 1990), a nd
Polysiphonia (Edwards, I 970a; Rue nes , I 973b; Ka p rau n, I 977a; Koch,
1986). H ybridisatio n st udies performed o n more co mplex a nd genera ll y
slower growin g red a lgae include bi o ys tem atic work o n strai ns a nd popu-
la ti o ns o f Chondrus crispus (C hen & T ay lo r, 1980; Guiry & C unnin gham,
1989), Graci/aria (Va n der M eer & T odd, 1977; Mclachlan , Van der Meer
& Bi rd, 1977; Bird & M c l achla n, 1982; Bird , Van der Meer & Mc l ach lan,
1982; Guiry & Freamhainn, 1985; Ya ma moto & Sasaki , 1987, 1988; Pl astino
& Oli veira, I 988a ; Bird & Rice, 1990; R ice & Bird , 1990), and Pa/maria
(Va n der Mee r & Bird, 1985) to establish interbreeding potential. Also,
hybridisa tion st udies have been employed to delineate species boundaries
a nd to es tabli sh life- history relationships in vario usly related strains and
populations of Gigartina, Mastocarpus, and Petrocelis (Polanshek & West,
1975, 1977; West. Polan hek & Guiry. 1977; West, Polanshek & Shevlin .
1978: Guiry & W e t, 1983; West , Guiry & Ma uda, 1983; Guiry, l 984b;
Masuda, West. Ohno & Ku rogi, 1984: Guiry, Tripodi & li.ining, l 987b;
Masuda, West & Ku rogi, 1987).

MOLE ULAR GENET I CS

t the molecular level , little i known to date about red algal genomes which
u ually number three (nuclear. chloroplast. and mitochondrial) in mo t cells.
In ome species of Graci/aria. Gy111nogongrus. and Porphyra small (2 to 8 kb).
circular, A+ T rich plasmid D As have. however. also been reported (Goff
& Coleman. 198 ; Villemur. 1990a. b: Bird et al .. 1990). As with our
knowledge of the tran mission of phenol) pie characters. this lack of progre s
32 STEVEN MURRAY A D PETERS . DIXON

has been due to the shortage of attention given to the red algae by molecular
geneticists, in part becau e red and other a lgae have properties that make
the extraction and purification of nucleic acids and their protein products
procedurally difficult (Olsen, 1990; R oell & Morse, 199 1). As outlined by
Olsen ( 1990), molecular studies on alga l geno mes are frequently challenging
to perform because: ( I) sufficient quantities of cellu lar m ateria l ca n be
difficult to obtain; (2) algae generally have low D A to bioma s ratios; (3)
multicellular forms are often heavily epiphytised and, therefore, co nta mi-
nated by other organi ms . and are hard to clean; (4) tough a lga l cell walls
can make D A extraction difficult and laborious; (5) the large amo unts of
polysaccharide occurring in many species interfere with extractio n a nd purifi-
cation procedures; and (6) many algal cells contain significant amo unts of
interfering nucleases, polyphenols, and other chemical substances.
For the red algae, mo t research has concentrated on the sma ller genomes
of chloroplasts , which generally have more copies in each cell th an nuclear
genomes, but together with mitochondrial D A represent on ly 0.1 to 5.0%
of total cellular DNA (Li & Cattolico, 1987). Little information is avai la ble
at this time on either mitochondrial DNAs, which in Griffithsia pacifica
appear to range in size from 27 to 350 kb (Li & Cattolico, 1987), or the
much larger nuclear genomes of red a lgae (see Van der Meer, 1990a).
Li & Cattolico ( 1987) provided the fir t portrayal of the composition of
a red algal chloroplast genome. They determined that the ize of the
chloroplast DNA of G. pacifica was 178 kb. This value is near the size ( 150 kb)
generally reported for the plastid DNA of terrestrial plants (Li & Cattolico,
1987; Goff & Coleman, 1988), but in G. pacifica, the chloropla t genome
contained only one instead of two copies of the genes for ribo omal R A
characteri tic of green algae and mo t terrestrial plants. Van der Meer ( l 990a)
indicates that preliminary data for the ch loroplast DNA of a Porphyra species
a lso reveal a single ribosomal RNA gene whereas for Pa/maria palmata, two
copies of the genes exist and these are arranged as in green algae a nd most
terre trial plants in the form of an inverted repeat. The ch loropla t genomes
of Pa/maria, Porphyra ye::oe11sis, another but unidentified Porphyra species,
and seven other red algae appear to be comparable in size to that of Griffithsia,
whereas slightly smaller genome size have been estimated for two other red
algal pecies (Shivji & Cattolico, 1987; Goff & Coleman, 1988; Van der
Meer, l 990a) . Among other , gene for the synthe i of the photosynthetic
enzyme ribulose-1,5-bisphosphate carboxylase ( Ru BPCase), phycobili-
proteins, and thylakoid protein also appear to be part of the red algal
chloroplast genome (Gantt, 1990; Van der Meer, l 990a) .
Recently, analyses of nucleic acids and proteins have added to the under-
standing of red alga l evolution and systematics and to know ledge of the
genetic make-up of individual algal population . At the time of this review,
however, these studies arc few in number and their real impact on red alga l
phylogeny and systematic is yet to come. The phylogenetic relation hips of
the red algae to other eukaryote have been ana ly ed using ribosomal R A
sequence data (Hori, Lim & 0 awa, 1985; Lim, Kawai, Hori & Osawa, 1986;
Ho~i & Osawa: 1987; Peras o et al., 1989; Bhattacharya , \wood. Goff &
Sog111, 1990) with variable re ult . In addition, plastid ribosomal R As of
red and other algae have been sequenced and studied (Yan den Eynde et al.,
1988) to gain insight into their evolutionary origins.
--------------------------------....im
RHODOPHYTA . 111 33

The use of restriction end o nuclease a nd gel electrop horesis to cut,

separate, and compare the D A of individual orga ni sm has eno rm o us
potential to contribute to red algal systematics, particularly in those taxa
where consistent morpho logical criteria are often difficult to recognise and
employ . For example, using three species of Graci/aria a nd six othe r red
algae, Goff & Co leman ( 1988) showed that plastid DNA restriction fragment
pattern differed between red algal genera and between species of the same
genus. Analysis of these patterns a lso a ll owed the authors to identify a
Graci/aria population of previously uncertain taxonomic affinity. Other
workers have used plastid D A re triction patterns for species recognition
in the taxonomically difficult Gracilariaceae (Bird & Rice, 1990; R ice & Bird,
1990; Bi rd et al., 1990) and to approach taxonomic problems and link
heteromorphic phases in a non-sexua l population of the morphologically
variable genus Gymnogongrus (Parson , Magg & Dougla , 1990).
The separation of o luble protein , cu tomarily performed by tarch-gel
electrophoresis, has been employed succe fully to a sess the genetic relation-
hips within and among terrestrial plant populations, but to date this
technique has been u ed in only a few select cases for red algae . For example,
protein polymorphisms have been used to assess the taxonomic status of
orth Atlantic and orth Pacific Pa lm ariaceae (Lindstrom & South, 1989),
British species of Callithamnion (Price, Pettitt & Ru ssell, 1987; Ru ssell , 1989),
Florida population of Eucheuma (Cheney & Babbel, 1978), and a lso to
determine species relationships in British Co lumbi an and Wa hington
members of morphologically sim ilar members of the Porphyra pe1forata
comp lex (Lindstrom & Cole, 1990). Importa nt future studies of red alga l
population genetics await the development of workable protocols for
extracting, separating, and identifying protein species for a broader pectrum
of red a lgal taxa.

REPROD UCT ION A D LI FE HISTORY

REPRODUCTION

Reproduction in red a lgae occurs by both sexual and asexual processes, but
in all ca e reproductive bodies share the uniqu e feat ure of being devoid of
flagella . A claim for the occurrence of a structure suggestive of ftagellar
organisation ("appareil cinetique" ) in spermatangia has been made by
Simon-Bichard-Breaud ( 1971, 1972) based on ultrastructural observations,
but thi s has not been substantiated by other investigators working with
various red a lgal genera (e.g., Kugrens & West, I 972b; Scott & Dixon, 1973b;
Ku grens, 1974; Peyriere, 1974; Peel & Duckett , 1975; Young, 1977). No
exp lan ation for the report by Simon-Bichard-Breaud was presented by these
aut hor but simi lar structures detected in spermatangia of Po/ysiphonia
haneyi and tetrasporangia of Dasya haillou1'iana were interpreted
( Broadwater & Scott, 1983) as fibrou vacuole as ociated organelles.
Unice llular forms depend upon asexual fission to produce new individuals
whereas multicellular red a lgae reproduce by a diverse array of sexual and
asexual mechanisms and are well known for the complexity of their exual
reproductive processes. Most multicellular red algae have extraordinary
34 STEVEN . MURRAY A D PETERS . DIXO

capacity to reproduce asexually by regrowth from detached thallus

fragments, a me ·hanism that may be the principal means of sustaining
populations in certain environments or geographic area . evertheless,
reproduction of many red algal populations probably occurs through the
release of sexually or asexually produced spores which are borne in sporangia.
At least ten different categories o f sporangia and pores occur in the red
algae (Guiry, 1990a). and the form and function of thee variou sporangia
and spore have been the subject of several thorough reviews (Drew. 1956;
Dixon, 1973; Dixon & Irvine, 1977; Guiry, 1978, 1990a; Magg, 1988; Guiry
& Irvine, 1989). As advocated by Guiry (1990a), the classification of red
algal sporangia is best ba ed upon morphological attribute rather than on
whether or not the resultant pore is produced as a con equence of meiosis
because the process of reduction division i not obligately linked to sporangial
type.
A di cussed by San tel ices ( 1990), algae reproducing primarily by asexual
means produce offspring believed to be genetically identical to parent thalli
re ulting in less genetic heterogeneity in succeeding generations. Asexually
reproducing populations, therefore, are well suited to ituations where
environmental change are few and where the population is well established
and presumably well adapted . In contrast, reproduction by sexual processes
potentially increase genetic variability within a population and. hence, the
opportunities for at lea t ome individual to survi e en ironmental changes.
Sexual reproduction, however, also involves greater resource expenditure
and offers greater risk of failure than reproduction by a exual means
(Santelices, 1990). In the present section. sexual and asexual mechanisms of
reproduction are reviewed with emphasis on the diversity of reproductive
bodies found in the Rhodophyta. The reader is referred to an tel ices ( 1990)
for discussions focu ing on ecological aspects of the reproduction of red and
other seaweeds.

Sexual reproduction
In exually reproducing red algae, reproduction ha been known to be
oogamou since the cla sical tudics of Bornet & Thuret (I 67. 1 76. 1880).
Sexual reproduction in the Rhodophyta has been summarised pre' iously by
Dixon (1973) and addressed in recent reviews by Hommer and & Fredericq
( 1990) and Hawkes ( 1990). Where documented , fertilisation involves the
fu ion of a non-flagellated male gamete, the spermatium. ' ith a sessile,
egg-containing cell , the carpogonium . The frequency of fusion between a
non-motile male gamete released into an aquatic medium and a static female
gamete is hypothetically low, particularly in calm water, a premise that has
been viewed by some authors (e.g., caries, 1980; Guiry, 1987) as the basis
for life-history evolution in the Rhodophyta. Paradoxically, however, in
extant populations field collections suggest that fertilisation is common and
often occurs with a high degree of uccess . Attempts to consider this enigma
statistically led to a theoretical estimate of red algal fertili ·at ion success that
was several orders of magnitude lower than that apparently occurring in
~ature (Dixon, unpubl. data) . Hence, sexual fusions in red algae appear to
111volve more than the mere random meeting of gametes. Two mechanisms
may help explain why realised fertili ation frequencies in the Rhodophyta
_____________.................................
RHODOPHYTA . III 35

are much higher than those expected in a breeding system consi ting of
passively dispersed , non-motile male a nd sessile female gametes . The first
involves the ch emo-attraction of spermatia to either the carpogonium
directly, or to the female gametangial thallus as a whole and is based on
the poorly explored premise that the non-Aagellated spermatia are capable
of significant amoeboid movement. It is known that permatia may first
attach to vegetative cell and later bind to a carpogonium a nd it has been
hypothesised that, in some species, permatia may secrete a chemical
substance directing growth of nearby trichogyncs towards themselves thereby
facilitating fertilisation (Hommersand & Fredericq, 1990). A econd
mechanism involves morphological adaptations, uch as external appendages
on male spermatia or the release of spermatangial clusters in mucilaginous
strands. For example, rigid spine-like appendages have been reported to occur
on spermatia of Spy ridiafilamentosa (Broadwater, Scott & West, 1991) and
Callithamnion (Aglaothamnion) neg/ectum (Magruder, l 984a), and elongate
(up to 600 µm) mucilaginous " spermatia strand " have been found in
Pleonosporium vancouverianum ( eushul , 1972) and Tiffanie/la snyderae
(Fetter & eushul, 1981) and suggested (Grubb, 1925) for several other red
algae. Neither mechanism ha been carefully investigated and only through
more study and the investigation of new hypotheses will it be possible
to reconcile the apparent discrepancies between theoretical and actual
fertilisation frequencies in the Rhodophyta .
The female gametangium or carpogonium generally develops among
vegetative thallus cells either as a sessile structure or at the apex of a short
filament (often consisting of three or four cells) referred to as the carpogonial
branch . The carpogonium may be indistinguishable from a vegetative cell
as occurs in certain sexually reproducing bangiophycids or, more typically,
is characterised by an inflated base that terminates distally into an elon-
gate process. This process, the trichogyne or protrichogyne, receives the
non-motile, passively dispersed male gametes. Whereas sexual reproduction
is well documented for score of species in Aorideophycid red algae, uch is
not the case for bangiophycids. In the past, this has led to considerable
controversy concerning the existence of sexual reproduction in the bangio-
phycids. Lengthy discussions challenging the historical evidence for alleged
gametic cell fusion and meiosis in bangiophycids have been provided
previously (Dixon , I 963a , l 970a , 1973) and will not be repeated here. It is,
however, now clear that at least in some bangiophycids, sexual reproduction
indeed take place (Magne, l 960a ,b, 1990; Boillot, 1975; Hawkes, 1978;
Kornmann , 1984, 1987).
In most Aorideophycid red algae, meiosis is thought to take place in the
tetrasporangium (Guiry, I 990a), a specialised structure that yield four
tetraspore or meiospores . Also, meiospores may be limited to two or
exceed four. In the former case, the sporangium is referred to as a
bisporangium whereas in the latter, the sporangium is termed a polyspor-
angium . Bisporangia occur in everal species of Corallinales and also have
been reported, although less commonly, for members of the Gelidiales ,
Gigartinales, and Ceramiales (Dixon , 1973; Guiry, 1978, l 990a ; Guiry &
Irvine, 1989). Bisporangia also occur in Audouinella occult a (Stegenga, 1985),
a pecie currently a igned to the Acrochaetiale , however, Guiry ( l 990a)
ugge ts that this taxon may instead belong to the Gigartinales.
36 ST EVE N M U RRAY A D P ET E R S. DIX ON

Polys po rangia appea r to be limited to the Rhod ymeni a les (Cha mpi aceae)
a nd Cera mi ales and occur in a t lea t eleven genera o f Ceramiaceae (Dixon ,
1973; Guiry, 1978, 1990a ; Gu iry & Irv ine, 1989) . M eiosis also ca n occur in
cell s o ther th a n spo ra ngia in some fl o rideo phyci d red algae. Aspo rangi a te
o r so ma tic meio is ha been d ocumented for Lemanea (M ag ne, 1967a ,b;
Th irb & Benso n-Evans, 1982) a nd Batrachospermum (Hurdelbrink &
Schwa ntes, 1972; Ba la krish na n & C ha ugule, 1980), a nd i suspected in certain
o ther red a lgae incl ud ing. Bonnemaisonia asparagoides (Rueness & Asen,
1982) a nd Hummbre/la hydra ( Haw ke , 1983) .
In ba ngio phycid red algae, tetras po ra ngia a re lacking. M eiosis in sex uall y-
rep rod ucing membe rs of the Bangia les has been fo und to occur in the
conchocelis phase in pecia lised co nchospora ngia ( Mi gita, 1967; Gira ud &
Magne, 1968 ; Kito, 1978) . It wa recently repo rted fo r va ri o us species o f
Porphyra (M a & M iura, 1984; Burzycki & Waa la nd , 19 7; T eng & Sun ,
1989) that meiosis also may , however, occur in the co ncho po res fo ll o win g
their release instead o f dur ing their fo rma ti o n in the conchospo rangium .
An interesti ng res ult o f this positio n fo r meiosis in th e life history of
Porphyra is tha t the lea fy phase th a t develo ps fr o m co ncho po re germlings
is a com posi te of genetica lly d ifferent cell lines as dem o nstra ted by Ohme,
Kun ifuji & M iura ( 1986) fo r colo ur muta nt o f P. ye:oensis. The occurrence
of meiosis du ri ng co nchospo re germ ina tio n was acco rded majo r systema tic
importa nce by G ab rielso n & G a rba ry ( 1986), who indica ted tha t, o n this
basis, the meiospora ngia of ex ually reproducing ba ngio phycid may no t be
ho mo logo us to the te tras pora ngia of fl o rideo phycid red a lgae. Interes tingly,
it has recentl y been lea rned th a t meiosis in fl o rideo ph ycid red algae a lso ca n
occur fo llowing tetra po re release ra ther tha n durin g tetras porogenesis (G off
& Colema n, 1990) , suggesting th a t, in a t least some fl o rid eoph ycid s,
indi vi dual ga meta ngia l th a ll i co nsist o f genetica ll y di stinct cell lines. Much
mo re research need to be performed to de termine: ( I) the frequency of
post- release meiosis in co ncho po res a nd te tras po res in species where thi s
eve nt occurs; a nd (2) how wides prea d pos t-release meiosis is a mo ng red a lga l
genera a nd species .
A unique a nd impo rta nt charac teri stic o f virtua lly a ll exua ll y reproducing
fl o rideo ph ycid red algae is tha t fo llo wing fertili sa ti o n the zygo te is no t
released directl y, but is reta ined o n the fema le ga meta ngial tha llus ' here it
develo ps int o a third genera ti o n, the ca rpospo roph yte. The ca rpospo roph yte
co nsists mostl y o f co lo urless cell tha t form wha t Schmitz ( I 3) ca lled the
go nim o blas t fil a me nts. The cell s o f the ca rpospo roph yte a re believed to
receive no urishment fr o m the ho t ti ssues o f the female gameto ph yte.
Depending upo n the taxo n, the go nim o blas t fil a ments may develo p directl y
fr o m the zygo te o r after cell fu io ns a nd nuclea r tra n fers involvin g
the co nnecti o n o f the fertilised ca rpogo nium with a n auxilia ry cell.
Rega rdless o f the deta il o f their develo pme nt , ca rposporo phyte fil a ment s
typica ll y termina te in carpo pora ngia a nd relea se ca rpo po re which serve
as th e age nts o f recruitment fo r the te tras poroph yte genera ti o n. The
ca rpos poro ph yte genera ti o n is usua ll y multicellul a r ( ee Dixo n, 1973;
Ho mmersa nd & Fredericq , 1990), but ca n be reduced to a ingle cell
( = " porozygo te") , as occurs in A11doui11el/a simplex ( = Acrochaeri11111
pecrinarwn) (Abdel- Ra hma n & M ag ne, 1983) . The ca rposporophyte
 R II ODOPIIYTA Il l J7

generauon may also be eliminated enurely. a . in Rhodopln .11! 1110 e/ef!.£111.1

( f)e(ew & West. 1982) and members of the Palmanale ( an der M eer
hen . 1979. an der eer & Todd. 1980. Deshmukhe & TatC\\ak1 . 1990)
M agne ( 1987). however. pro•1des an alternauve interpretation for these ta\a
whereb y instead of the e rect. d1plo1d thallus represenung the tetrasporophyte.
as outlined by an der cer and colleague . he suggests that this generauon
may be a free-living carposporophytc .
In sexually-reproducing bang1ophyc1ds. the /ygote can d1\1de internally
b) m1tos1s forming several carpospores as in Porphrra ( Ha1\ kes. 197 ). di\ 1de
d1rectl} to produce a single spore as in Rhodoclwele (M agne . 1960a . b. Boillot .
1975) and probabl} P orph1·ros1ro111111111 ( Kornmann. 19 4. 1987). or can be
retained on the gametophyte thallus forming a linear -,enes of cell'> as in
f n 1hro1richia rnmea ( M agnc. 1990) Gu1ry ( 1990a) has created the term
.. /}gotospor,1ng1.1 " to d1..,tingu1'>h thc\C bang1ophyc1d structures from tho ... e
found 111 flondeoph1c1d red algae 11 here carposporang1a ame as modificauons
o l apical cells of the gonimoblast filament\
l hree maJor patterns of carposporophyte dc1elopment in tlomlcophyc1d..,
ha1e been outlined by I lommcrsand I rcdcm:q ( 1990) based on 1n111al po..,t-
li:nilisation c1 cnt.., fhcsc arc described a ... those case., 11 here the fir-,t cell
38 STEVEN . M U RR AY A D P ET E R S. D IXO

spo ra ngia give rise to pro tra te pl a nts tha t fo rm tetras po rangia suggesting
tha t the ca rpo tetraspo res are no t meiospo res (Guiry & C unnin gha m, 1989;
Guiry, l 990a, b).

Asex ual reproduction

D espite their potentia l eco logical impo rta nce as fac ulta ti ve o r o bli ga tory
a lte rna ti ve to a sex ual . life hi to ry, asexua l reproductive processes in
Rh odophyta have not been well st udied o r received the degree of a ttenti o n
th a t they meri t (D ixon, l 963b, 1965 ; H aw ke , 1990). Asex ua l reproducti o n
occurs in un icell ula r red a lgae by cell fiss io n a nd th is reproducti ve mode
appea rs to be the o nl y one o perative in the ' uni pha ic' Po rph yridi ales . In
multicellul a r red algae, the age nts of asex ual reproduc ti o n ca n be spo res o r
un pecia lised or specia li sed vegetative structures, fr agments o r o utgro wth s.

Asexual reproduction by spores In multicellul a r Rh odo ph yta, asex ual

re p roductio n is often med iated by mi to tica lly- produced spo res whic h ca n be
produced in large nu m ber a nd rea dil y d is persed . E nd ospora ngia,
mo nosporangia , bin uclea te bispo ra ngia a nd para po ra ngia a re believed to
be excl usively asex ua l mito pora ngia a nd to p rov ide re producti ve a lter-
natives in additio n to or instead of th ose occurring in the sex ua l life hi sto ry.
In cont rast, meiospore-prod uci ng te tras pora ngia , q uadrinuclea te bispo-
ra ngia , po lyspora ngia, ca rpotetraspora ngia, a nd co nchos pora ngia a re
genera ll y invo lved in the sex ua l life histo ry, as a re zygo to pora ngia a nd
ca rpo pora ngia which a re genera ll y fo rmed as a res ult o f ga mete fu io n
(Gui ry, 1990a) . T he ass ump tio n tha t a ny pa rticula r ca tego ry o f pora ngium
i evidence fo r a sex ua l process ca nno t, ho wever, be made beca use a
no n-sex ual ro le a lso is kn own for spo res p roduced by virtua lly each type o f
red a lga l spora ngium ( ee Guiry, 1978) .
As described by G uiry ( 1990a), end ospo ra ngia p roduce va ria ble number
o f irregula rl y ar ranged spores by mi tosis a nd a re co nfi ned to o nl y a few
taxa . End ospo res occur on ly in th e Phrag mo nema taceae ( Po rph yridia les).
where they a re comm o n (G uiry , 1990a), a nd in the Eryth ro peltidaceae o f
the Co mp o pogo na le (Ga rgiul o , D e M asi & T ripod i, 1987) .
M o nospora ngia are variable in their mode of develo pment a nd a re of
wid espread occurrence a mo ng the ba ngio ph ycid red a lgae (Guiry, l 990a;
Haw ke , 1990) , where in ma ny taxa they e rve as the principa l o r so le mea ns
of po re-medi a ted reprod uc ti o n. In the fl orideo phycids. differenti a ted
mo no pora ngia a re usua ll y o blo ng a nd fo rmed fro m te rmina l cells o f
bra nched fil a me nts, genera ll y o n loosely fil a me nto us th alli o r o n the basa l,
pros tra te o r a ttac hm ent pa rts o f the erect phases of specie in the
Acrochae ti ales, N erna li ale , Ba trac hosperrn ales a nd , le s co mm o nl y, the
Gi ga rtina le (Guiry & Irvi ne, 1989 ; Guiry, l 990a; Hawkes. 1990) a nd
A hnfelti ales (M aggs & Pue chel, 1989) . M o no po ra ngia al o occur o n two
pecies in the Rhodymenia lc ba ed o n wo rk perfo rmed by Di xo n (unpubl. )
who o bserved d ifferentia ted rno nospo ra ngia in Rliody111e11ia par[fica a nd
Ba lla ntine ( 1989) who fo und und ifferentia ted mo no pora ngia in Botryocladia
py riformis. M o nospora ngi a a re of ques ti o na ble occurre nce in the era mia les,
a nd ha ve no t been de tected in the Pa lrna ria les, Cora llina les, G elidia les,
G raci laria les, Hilde nbra nd ia le , a nd Bo nnernaiso nia les (Guiry. 1990a) .
-----------------------------------..
RHODOPHYTA . III 39

For ma ny species in the Acrochaeti a les (Stegenga, 1979, 1985; Woelkerling,

1983; Guiry, l 990a) and certain growth forms of Ba trachosperm a les (Shea th ,
1984; Guiry & Irvine, 1989), reproduction is mediated exclusively by asex ual
monospo res a nd a life history involving the sex ua l processes of ga mete fusion
and meiosi s is unknown. In the Acrochaeti a les, monospora ngia are sessile
and occur either singl y or in clusters at the end s of filaments a nd can produce
in sequence as man y as 11 to 14 spores per spo ra ngiu m (Di xo n, 1973). In
the freshwater Batrachospermales, mo nospora ngia can be produced o n both
the prostra te, basa l " Chantransia stage" as well as on the erect ga meta ngia l
thallus (Dixon , 1973). For species in the Nema li a les, asex ua l reproduction
by monospores appears widespread. Investiga to rs have identified mono-
sporangia on both the filamentou s tetra sporo phyte (Stosch , 1965; Fries,
1967; Martin , 1969; R a mus, I 969c; Boillo t, I 972a; Umezaki , I 972a; Chen ,
Edelstein , Bird & Yabu , 1978; Guiry, 1990b) and prostrate o r erect ga m-
etophyte (Svedelius, 1917; Ramus, 1969c; Dixo n, 1973; M aggs & Guiry,
1982a; Hui sma n, 1985) phases. Most knowledge of the po tenti a l roles a nd
fates of monospores in nem ali a lea n taxa has come fr o m culture studies of
the poorl y known tetrasporophyte and yo un g, prostrate gametophyte stages;
relatively little is known of the role of mo no po res produced on the erect
ga metoph ytic thalli . Asex ua l reproducti o n mediated by monospores
may, however, be of grea t ecological significa nce, particularly in temperate
Nemaliales where the filamento us tetrasporophyte o r the prostrate,
filamentou s ga metophyte stages may represe nt th e 'o verwintering' phase o f
the life hi sto ry. Monosporangia have been repo rted for o nl y a few taxa in
the Gi ga rtina les, mostly in members of the Dum o ntiaceae a nd H a lymen i-
aceae. Mon osporangia occur o n bot h the crustose tetrasporangial a nd the
erect gametangial phases of Thuretellopsis (Di xo n & Richardson, 1969;
Richardso n & Dixon , 1970), the cru tose tetrasporo ph ytes o f Pikea ca!ifornica
(Scott & Di xo n, 197 1), a nd the basa l filamentous a nd erect ga meto ph yte
tage o f Ha!y menia floresia (v.d . H oek & Cortel-Breema n, 1970a).
In the Cera miales, evid ence for asex ua l rep rod uctio n by mono pores is not
a b olute. Dixon ( 1973) considers the "seiro porangia" (see Guiry, 1978)
characteri stic of certai n genera in the Ceramia les (i.e., Seirospora and
Dohrniella) a nd Gigartinales (Gibsmithia ) to be monosporangia that are
formed in termin a l chains. In S eirospora , Di xo n ( 1973) indicated that
reproductio n by mea ns of these spo rangia can occur either through the
release of the pore contents from the wa lled sporangium or by
the detachment a nd s ubsequent germi nation of the entire sporangium cell.
De pite st udi es of eirospore release a nd germination ( Pl attner & ichols,
1978) a nd developmental fate ( Bird & Johnson , 1984) in S . seirosperma, the
details of thi s reproductive mechanism still require clarification . If the spore
content are indeed shed from walled sporangia, then so-called seirosporangia
differ in their development and function from typical monosporangia only
by their formation in terminal chains and are definable a monosporangia .
If entire wa lled 'sporangial units' are hed , then these structure a re, however,
be t referred to as "vegetative propagula", i.e., organised and walled asexual
reproductive un its of one or more cells that are released from the parent
plant in their entirety. In the latter case, the eirosporangia of
eirospora are more a nalogo us to the o-called multinucleate mono porangia
of the ceramiacean red algae Ma::.oyerella arachnoidea (Gordon-Mills &
40 ST EVE N M U RR A Y A D P ET E R S. DI XO

Wo mersley, 1974· Huisma n & Kra ft, 1982) M . pedicel/atus ( = M onosporus

pedicellatus) (Bornet & Thuret, 1876; Feldma nn -M azoye r, 1941 ; L' Hard y-
H a los, 1970; Hui sma n & K raft, 1982), a nd M onosporus indicus (Kim & Lee,
1989) which also a re released fr o m pare nt tha lli in their entire ty. Other
repo rts (e.g., Y a ma no uchi , 1906a ,b; Lewi s, 1909 ; Svedelius, 19 14; R osen-
vinge, 1923- 24; Jaasund, 1965) o f m o nospo ra ngia in Cera miales are
q uesti o nable. In add iti o n to single-cell ed vegeta ti ve pro pag ula, co nfu sion
ex ists as to the functi o n ofla rge o r gia nt mo nos po res p roduced , fo r example,
in Nemalion vermiculare (M a ud a & U meza ki , 1977) a nd Helminthocladia
macrocephala (Umeza ki , 196 1). Guiry ( l 990a) believes tha t in the fo rmer
ca e, the gia nt m o nospora ngia rep rese nt undi vided tetraspora ngia. Guiry's
hypot hesis is based o n M as ud a & Umeza ki's ( 1977) o b erva ti o n th a t the
gia nt mo nospo res produced by tetrasporoph ytic pla nts o f Nema!ion
vermiculare gave rise in c ulture to what we re interpreted to be ga meto ph ytic
pla nt instead of tet ras porophytes as wo uld be ex pected if these spo res
functio ned as m o nospores.
Parasporangia a re defi ned by D rew ( 1937, 1939) as spo ra ngia tha t produce
mo re t ha n fo ur spo res by m itosis a nd whic h a re no t ho mologous with a nd
do not replace the occurrence of te tras po ra ngia. Pa ras po rangia a ppea r to
be restricted to the Ceramia le a nd have been repo rted fo r Plumaria elegans
( D rew, 1939; Rueness, 1968), Ceramium strictwn ( Ruenes, 1973a),
Antithamnion plwnula (Schiller, 19 13), Callithmanion hookeri ( Rueness &
Rueness, 1978), a nd C. decompositum (Guiry, 1990a). Deta iled studies o f
pa ras po ra ngia are few a nd m uc h co nfusio n still ex ists co ncernin g
paras pora ngial develo pme nt a nd fun c ti o n. Ea rli er, Di xo n ( 1973) pointed
o ut that stro ng si mil a rities exist between pa ras po ra ngia a nd the ga ll-like
pro liferatio ns fo und co mm o nl y in Ceramium. Al so. Guiry ( I 990a) has no ted
tha t, based o n their mo rpho logy, pa ras po ra ngia stro ngly resemble the
cera miacea n carpospora ngia l genera ti o n, suggesting the possibilit y tha t
paras po ra ngia ca n be co nfu ed with ca rpospora ngia. eve rtheless, de pite
the limited informatio n ava il a ble o n these structures, G uiry & Irvine ( 1989)
a nd G uiry ( l 990a) propose th a t para po ra ngia a re fo und o nl y o n triploid
tha ll i, a a pparently is the ca e in C. strictu111 ( Rueness, 1973a)
a nd Plumaria elegans (Drew, 1939) . Based o n the suppositi o n tha t the
fo rmation o f pa ras pora ngia req uire a triplo id pl oidy level, Guiry & Irvine
( 1989) pecu la te tha t the mecha ni sm for pa ras po ra ngial develo pm ent in the
Cera m iaceae in vo lves the ex pressio n in th e tripl oid co nditi o n o f the a lleles
co ntroll ing sex ua lity a nd tetras po ra ngia l fo rma tio n.
Asex ual reproducti o n a lso ca n occur by mea ns of spo res relea ed by mito tic
bi po ra ngia, tetraspora ngia o r po lys po ra ngia, struc ture genera ll y,a)sumed
to fun cti o n as meios pora ngia in the fl o rideo ph ycid red a lgae. Spo res
produced within structure where meios is is no rm all y believed to occur a re
aid to be produced a pomeio tica ll y. Wh en fun cti o ning asex ually,
apo meiotica ll y-prod uced spores recycle the ph ase upo n which they a re bo rne.
Bi po ra ngia (=two-spored spora ngia) ca n occur bo th o n tha lli th a t a lso bea r
tetras porangia, or ca n be the exc lu sive for m of spora ngia l reproductio n
(D ixo n, 1973). When functio ning as meiospora ngia, it a ppear tha t
bi pora ngia are q uadri nucleate a nd th a t th eir bis po res a re binuclea te,
whereas when bispores a re prod uced mito tica lly, they a re un inuclea te a nd
come fro m binuclea te bispora ngia ( Ba uch, 1937; Suneso n, 1950; G o ff, 198 1).
---------------------------------- ..
~
RHODOPHYTA . Ill 41

Bi porangia have been ob erved in the Acrochaetiales, Gelidiales,

Corallinales, Gigarti na les, and Ceramiales (G uiry & Irvine, 1989; Guiry,
1990a) but have received greatest attenti on in the Cora llina les, where asexual
reproduction by uninucleate bispores appears to be relatively common in
both crustose (Suneso n, 1950; C ha mberlain , 1977, 1983, 1987) and articu lated
(Gittins & Dixon, 1976; Johansen , 198 1) species.
Apomeiotic tetrasporangia , re ul ting in a life history where new
tetrasporophytes develop directly from tetraspores, have been reported in
the Acrochaetiales, Bon nemaisonia les, Ceramia les, Cora llina lcs, Gigarti-
na les, Hild enbrandia les, a nd in the Palmariales (Rh odophysemataceae)
(Tables V, VI) . Interesti ngly, in Antithamnionella sarniensis (L'Hardy-
Ha los, 1985; Magne, I 986a) and Gloeophycus koreanum (Notoya, I 984a),
apomeiotic a nd meiotic tetrasporangia appear to develop on the
ame thallus resulti ng in the production of both tetrasporangial and
gametangial progeny. This phenomenon is known as " mixed tetrasporop hyte
recycling" (see Maggs , 1988). Polysporangia , defined by Drew ( 1937, 1939)
as sporangia that produce more than four spores by divisions involving
meiosis and that are homologous with and repl ace tetrasporangia , are known
on ly for members of the Rh odymeniales and Ceramiales (Guiry, 1990a).
Polysporangia were thought to be exclusively meiotic. Guiry & Irvine ( 1989)
suggest, however, that apomeiotic polysporangia may occur in eastern North
Pacific populations of Gastroclonium subarticulatum (Rhodymeni ales)
where only poly porangial a nd tetrasporangial plants are known from the
field and Goff & Co lema n ( 1990) have reported apomeiotic polysporangia
in Gonimophy llum skottsbergii specimens from central California .
Cyto logica l tudie indicate that in many bangiophycids concho porangia
and zygotospora ngia produce spores that function outside the sexua l cycle.
In these cases, it is virtually impossible to determine whether or not a sexua l
cycle exists without obtaini ng chromosome numbers of the various phases
or evidence of either gamete fusion or meio i . In ftorideophycid red algae,
carposporangia are produced terminally on the gonimoblast filaments
comprising the diploid carposporophyte and are pa rt of the ftorideophycid
ex ua l cycle. In numerous ftorideophycids , carpospore can, however,
germinate to produce directly new gametophytic thalli , particularly in
certain members of the Nemaliales, Bonnemaisoniales, Gigartinales, and
Ceram ia les (Tables V, VI) . Thi direct development of gametophytic tha ll i
from carpospores can occur where the carposporophyte and carposporangia
develop without the involvement of either the male or female gamete
(apogamou ly) or witho ut gamete fusion (apomictical ly).

Vegetative propagation Vegetative propagation is a particularly wide-

spread means of achieving a exual reproduction in red algae. It can be achieved
in everal way , reflecting various level s of thallu speciali ation and
differentiation .
A common method of a exual reproduction exhibited , for example, by
certain populations of Gelidium and Pterocladia is the production of new
erect axe from a spreading array of pro trate, stoloniferous outgrowths
(Yamada, 1976) . The simple t mode of vegetative propagation in red algae,
howe er, involves the detachment a nd ubsequent re-attachment of
vegetative axe . As indicated previously, a cut portion of a ftorideophycid
 ~
N

TABL E V
Life-histo ry ty pes o fftorideoph ycid red algae: summary of morphological phases and reproductive bodies. Hetero = Heteromorphic
with respect to a ppearance of gamet:rngial and tetra sporangial phases; !so= Isomorphic with respect to appearance of gametangial
and tetrasporangial phases; (T) =ultimately independent of other phases; (P) = pa rasitic or not independent of other phases . VJ
-l
GP = gametangial ph ase; TP = tetrasporangial phase; CP = carposporangial phase; X = phase or spore type is present; [11

n/a =category is no t applicable <

[11
z
Phases in life history Spore types z
Gametangial and --- ::::
Life-h istory type tetrasporang1al phases GP CP TP Carpospores Tetraspores Carpotetraspores c
;i;
;i;
Sexual life histories
I. Audoumella simplex
>
-<
l'irgatu/a-type Hetero x x x x x absen t >
( I) (P) (I) z
x x x 0
2. Polys1phonia-type lso x x absen t
-0
( I) (P) ( I) [11
3. Bonnemaisonia hamifera- -l
[11
type Hetero x x x x x absen t ;i;
(I) (P) ( I) !"'
4. Ltagora tetr.asporifera-type n 'a x x absent absen t absen t x 0
(I) (P)
5. Pa/maria-type lso (J) x absent' x absent x absen t
><
0
Hetero (; ) (I) ( I) z
6. Rhodophysema e/egan.Hy pe Hetero x absent x• absent x absen t
( I) (P)
7. Audouinel/a purpurea
jloridu/a-type Hetero x X' x absen t x a bsen t
(I) (P) ( I)
8. Lemanea-type n/a x x absent x abse nt a bse nt
{I ) (P)
Non-sex ua l li fe histori es
9. Direct development
tet raspora ngia l ph ase n/a a bsent a bsent x absent x a bsent
(I)
10. Direct development
ga meta ngia l phase n/a x x a bse nt x a bse nt absent
(I) (P)

• Magne ( 1987) considers the tetrasporophyte lo be reduced to o nl y a stalk cell a nd a tetraspo ra ng1um as occurs in Rhodophysema, and the independent d iploi d
ph ase lo be the ca rposporo ph yte.
b Tetraspora ngia l phase is reduced to two cell s (stalk cell a nd tetraspo ra ngium ).
' In certa in cases , the tetrasporangial ph ase ca n develo p directl y fr om the zygo te, thereby by- pass ing the ca rpospora ngia l genera ti o n.

;:o
J:
0
0
0
-0
J:
-<
...,
)>

.,,.
w
44 STEVE N . MURRAY AND PETERS . DIXON

thallus usually gives rise to one or more new apices from cells
comprising the ac1 o petal pole of the fragment while one or more rhizoidal
attachments develop from the basipetal pole. The ability to regenerate in
this way reflects the strong polar organisation of thalli in florideophycid red
algae and is relatively rare in the much less polar thalli of the bangiophycids.
Researchers have long taken advantage of the prolific regenerative properties
of florideophycid thalli by using excised apical tips as standard material for
initiating laboratory cultu(es. Many years ago, Chemin (1928) described
vegetative propagation through fragmentation in various florideophycid red
algae although little attention was given at the time to the potential
significance of this phenomenon. It is now appreciated that vegetative
propagation by fragmentation can have particularly significant ecological
consequences. For example, vegetative propagation is believed to be the
principal method of reproduction in several populations of Audouinella
purpurea (as Rhodochorton purpureum) (Knaggs, 1966, 1967; Pearlmutter &
Vadas, 1978; Breeman & Hoeksema, 1987), and has been shown (Dixon,
1965) to be important in sustaining populations of Bornetia secundifiora in
the English Channel. Also , in populations of Asparagopsis armata living at
their northern limit in the British Isles, the sexual cycle has been replaced
by the independent vegetative propagation of the gametangial Asparagopsis-
phase and the tetrasporangial Falkenbergia-phase (Dixon, 1965; Martin,
1969). Vegetative propagation can be a particularly important mode of
reproduction in sedimentary habitats, where Santelices & Doty (1989) found
populations of Graci/aria to be sustained by the regrowth of detached and
buried thallus fragments .
Where propagation by fragmentation occurs, the fragments may not always
become re-attached and the result is a free-living population, often termed
"loose-lying", which occurs most often (but not always) in sheltered waters
at a depth below effective wave disturbance (Burrows, 1958; Norton &
Mathieson, 1983). Massive quantities of algae can be produced in this way
and following a storm , these detached populations often contribute significant
amounts of biomass to the beach drift. One particular red seaweed that
commonly maintains loose-lying populations by the vegetative propagation
of detached lateral axes is Furcel/aria lumbricalis ( = F. fastigiata). Because
of the relative ease with which unattached seaweed thalli can be harvested,
populations of Furcellaria suspended in the water column and cast ashore
on the beach at one time made an especially attractive source of "Danish agar"
(Austin , 1960c; Lund & Christensen , 1969; Norton & Mathieson , 1983).
The release of unspecialised cells for the purpose of asexual reproduction
has been reported on only one occasion for red algae other than the
bangiophycids where this means of propagation appears to be quite common .
Ballantine (1989) observed that undifferentiated vegetative cells can be
released singly from the cortex urface of the florideophycid Botryocladia
py riformis and germinate into new thalli. f n function and mode of production,
these cortical cells are comparable to the Type Tl bangiophycid monospores
of Drew ( 1956) which are widespread among bangiophycids. Ballan-
tine's ( 1989) report is the first for florideophycids whereby asexual repro-
duction is achieved by means of the release of single, undifferentiated
vegetative cells . An unanswered question regarding asexual mechanisms of
florideophycid reproduction concerns how important the release of
_____________............................
RHODOPHYTA . Ill 45

undifferentiated single cell s i to the recruitment of new individuals in the

field .
Another method by which undifferentiated cells and thallus part can
function in vegetative propagation is known from studies of the digestive
abi lities of herbivorous a nima ls. It ha been known for some time (e.g.,
Atkinson, 1970, 197 1, 1972, 1980) that con umed living cells of certain kinds
of freshwater a lgae co uld sur vive passage through the dige tive tracts of
anima l but it has been appreciated only recently that fragments of red a lgae
are capab le of survivi ng passage through the guts of both vertebrates and
invertebrates. Breeman & H oeksema ( 1987) demonstrated that tufts
of Audouinella purpurea (as Rhodochorton purpureum) can grow from
fragment fou nd in sticky aggregate considered to be faecal pellets. An even
more interesting recent discovery (Santelices & Ugarte, 1987) was that
digested bangiophycid red algae were capable of releasing protopla sts with
reproductive potential. This is particularly interesting because a common
laboratory procedure for obtaining free-living protoplasts from Porphyra
involves the in vitro use of herbi vore dige tive enzymes (Po lne-Fu ller &
Gibor, 1984).
In Furcellaria lumbricalis (as F. fastigiata), the portion of the thallus that
is shed i a pecialised axis (Austin, l 960c) instead of unspecialised cells or
portions of the vegetative thallus . Similar 'specia li sed' struct ures that function
in vegetative reprod uction have been reported in various florideophycid red
a lgae, such as Polysiphonia (La urel, 1970), Antithamnionella (as Antitham-
nion) sarniensis (Stosch, 1969), Solieria chordalis (Floc'h, Deslandes & Le
Gall , 1987), Centroceras clavulatum (Lipkin, 1977) and Spyridia jilamentosa
(West & Ca lumpo ng, 1989). In the case of Spyridia, short latera l axes of
determinate growth, ca lled " brachyblasts", are deciduous in the field a nd
under culture co nditi o ns have been show n to grow readily into new thalli
upon release. An a nalogo us ' mi ssi le-shaped' specia li sed axis was reported
to function in the vegetative propagation of a natural population of Centro-
ceras (Lipki n, 1977).
An eve n higher degree of specia lisation occurs in the vegetative
reproductive bodies of members of the Rh odomelaceae (Ceramiales) whe re
in certain pecies trichoblast-like axes can play a reproductive ro le.
Trichobla t are branched filamentou structures made up of e entia ll y
co lourle s cell s a nd are highly ephemera l (except in Brongniartella where the
cell co ntain chl oroplasts a nd the trichoblasts are persistent) . Vegetative
late ra l axes form either in the ax il of a trichoblast and its initiating axis, o r
from the sa me basal cell as the trichoblast, or in place of the
trichobla t filament. Ro envinge ( 1904) described an interesting condition
whe re the initial development of an axi had the characteristics of a
trichoblast but , ubsequently, assumed the cellul ar characteristics of a
normal vegetative axis, suggesting that trichoblasts may be capable of
regenerating vegetative tha lli . This observation has been largely ignored
alth ough considerable interest ha now developed in the phenomenon of
asexua l vegetative reproduction by means of specialised structures.
Kaprau n ( l 977a) described asex ual trichoblast-like tructures in Polysiphonia
ferulacea as " developmentally and morphologically resembling spermatangial
branches but appearing o n male, female , and tetrasporangial plants".
Spermatangial axes do arise in a simi lar manner and position to the ob erved
46 STEVEN . MU RR AY AN D P ETE R S. DI XO

unusua l structures, bu t the la tter d iffer in certai n cellul a r a nd mo rph o logica l

detai ls. In cul t ure, the a berra nt structures a re eventua lly released th ro ugh
the brea kd own of the bea rin g cell s which , as indica ted a bove, a re co lo url ess
a nd ephemera l. Su bseq uentl y, tricho blas t-like reprod uc tive structures have
been fo und in other species of Poly siphonia (Byun & Ka ng, 1986; Kud o &
M as uda , 1986; Dixon , un publ. obs.) a nd L ophocladia (Co rmaci & M o tta;
1985) a nd a ppear to have been observed in culture by ma ny inves tiga to rs
based o n persona l co mm u!1ica ti o ns. U npubli shed o bse rvatio ns by Di xo n,
not o nl y de tected these tricho blas t-associa ted structures in a fi eld
pop ula tion of Polysiphonia nigrescens in M assachusetts, bu t a lso e ta blished
thei r asex ua l re pro d uctive functio n.
T he highest level of mo rph o logica l specia lisatio n in co nnecti o n with
vegetative p ro pagatio n occurs in those t ructure term ed "gemmae " by
F ritsch ( 1945) a nd D ixo n ( 1973) a nd " pro pag ules" by so me, mo re recent ,
a uth o rs. O ne particul a rl y in te rest ing exa mple of co mplex, multi cellula r
struc tures su pposedl y fu nc tioni ng in vegeta ti ve pro paga ti o n was fig ured but
not described m ore tha n a century ago by So lm s- La ubach ( 188 1). These
structures we re subseq uently described by Coppeja ns ( 1978 , 1983), W oel-
kerli ng ( 1988), a nd Afo nso-Carri ll o ( 1989) in the sa me a nd o ther species
of Fosliella while Co ppeja ns ( 1978, 1983) has demo nstra ted their fun cti o n
in vegetative propagatio n. Jn add iti o n, H o llenberg ( 1970) described a di coid
rather than fan-s haped struct ure in F. paschalis which he believed func tio ned
as a vege tative mea ns of propagatio n a ltho ugh he was un a ble to suppo rt hi
co nte ntio n with d irect evidence. A tr ira di a te multice llul a r struc ture in vo lved
in vegetative propaga tion wa fig ured in a no ther mem ber of the Cora!lina le ,
Jania capillacea, by Dawso n ( 1953) a nd a lso by J o ha nsen ( 198 1).
Vegetative rep roductio n by pecia li sed two-celled truc tures, as in
Anisoschizus propaguli (H ui ma n & K ra ft, 1982) , three-celled structures as
in Deucalion levringii (Hui sma n & K raft, 1982) o r fo ur-celled truc tures as
in Acrosy mphy ton purpuriferum (Co rtel- Breema n & v.d . H oek , 1970) ha ve been
reported o n occasio n, but in a ll cases these struct ure bear some resembla nce
to o ther for ms of pora ngia fo und in red a lgae.
The vas t a rray of vegeta tive reprod uctive bodies fo und in the Rh o do phyta
has led to pro blem in the use of desc riptive te rms. The highl y pecia li sed
a nd rea d ily d istinguis hable mul ticellul ar o rga ns of vegeta ti ve pro paga ti o n
were te rmed "gem mae" initia ll y (Fritsch, 1945; Di xo n, 1973) but recentl y
the te rm " p ro pag ules" has received widesp read u age fo r no t o nl y the e
multicellul a r structures but a lso fo r simpler fewe r-celled vege ta tive
rep roductive bodie (Hui sma n & K raft, 1982) o r even fo r o ne-celled
mo nospo rangia (G uiry , I 990a) . [n rece nt eco logica l studies, the term
pro pag ule has bee n used even more widely to incl ude virtu a lly a ll
reproductive units, includ ing no t o nly vegeta ti ve th a ll us parts but a lso spo res
of a ll ki nds (e.g., H offma nn , 1987; Sa n telices & Paya , 1989) . Fo r thi s rea o n,
it might be mo re precise to use the te rm "gemm ae" fo r pecia li sed
mul ticell ula r o rga ns of vege ta tive re pro ducti o n to aid in di stin guishing
the e from other reprod ucti ve bod ies, in tead of a ppl ying the term "' pro-
pag ule" . In additi o n, it is imperative that when a reprod ucti ve func ti o n is
cla imed , thi claim sho ul d not be ba ed solely o n inte rpreta ti o n but
substa ntiated wit h ex peri me nta l evidence de rived from stud ies in cultu re or
in the fie ld .
----------------------------------·~
RHODOPHYTA. 111 47

LIFE HISTORIES

Red a lgal life histories have been of interest to phycologists since the classical
studies of Yamanouchi ( 1906a,b) who described the cytological events
associated with the reproduction of Polysiphonia. Prior to the 1960s,
re earchers were, however, unable to maintain red algae in laboratory culture
for periods sufficient to follow the development of spores and other reproduc-
tive cells to their maturity . Consequently, laboratory studies focused on
developmental stage achieved in only a few days and life histories were
mostly deduced from observations of reproductive structures identified from
preserved field-collected material and augmented, on occasion, by cytologica l
investigations. A umptions concerning the role and fate of reproductive
structures and spores were often made in the co ntext o f the existing dogma
and the diversity of red algal life histories was not a ppreci ated . The advent
of techniques to remove micro sco pic contaminants and the development of
enriched sea-water media , however, extended the periods that red a lgae could
be cultivated in the laboratory. These improvements in culture technique
led to a great expa nsion in resea rch on red algal life hi stories (see Knagg ,
1969; Kamma nn , 1970; West & Hommersa nd , 198 1).
Drew ( I 955b) has defined the life hi stor y of an alga as the recurrin g
sequence of m o rphological and cytological phase . Therefore, to establish
the life history of a n a lga, the inve tigator must obtain evidence substantiat-
ing both morphological and cytological events. Unfortunately, this is rarely
accomplished and, where de cribed, the life hi stories of mo t species have
been pieced together from incomplete data . A m orphological pha se ha s bee n
defined by Dixon ( 1973) as the entity beginnin g with a single cell, the spore
or zygo te from which it arose, a nd ending with a sin gle cell, the reproductive
body which it produces . In order to establish the complete sequence of
morphological phases, the germination of each reproductive body must be
acco mplished and its developme nt to reproduc tive maturity obtained (Dixon,
1973, 1982b; Dixon & Irvine, 1977). Thi s is impossible to acco mpli sh by
observing an alga and its germinating reproductive cells directly in the field.
Hence, where known , th e morphologica l seq uences comprising the life
hi tories of virtually all algae are based o n ob ervations performed on one
o r a few isolates cultured in the artificial confi ne of the laborato ry . It is
well kn ow n that , unde r labora tory co nditi o n , it i no t a lways possible to
grow the prod uct of spores to reprod uctive maturity, to obtai n all vegetative
pha es or pore types known to occur in natural field populations, or to
ob erve or acq uire mo rph ological evidence for gamete fusion . Therefore, life
hi to ry st udies based o n laboratory cul ture may not comp letely describe the
full seq ue nce of morphological phases, particularly when cu ltured spore
germli ng fa il to develop to reproductive maturity and may not fully de cribe
the diversity of reproductive activity representative of a population in the
field . In addition, there may be differences between what occurs in the
laboratory and in field population due to the a rtificiality or the laboratory
environment, a point that Di xon (1973, 1982b) ha emphasi ed repeatedl y
in hi concern that to be ecologically meaningful. conclusion drawn from
laboratory finding must be confirmed in the field.
Dre\\ ( l 955b) ha defined a cytological pha e as that tale characterised
by mitotic cell di' isions a ll ho,.,.ing the same chromosome number. Thi
48 STEVE N. MURRAY AND PETER . DIXO

requires that to determine the sequence of cytological phases, the ploidy

level of each of t he morphologica l entities must be obtained and the
positions of syngamy and meiosis determined (Dixon, 1973, l 982b; Dixon &
Irvine, 1977). Unfortunately, red algal chromosomes are extremely difficult
to observe due to their small size, often large number, tendency to clump
together, and the periodicity and ra pidity of cell division (Dixon, l 963a,b;
l 966a ; Cole, 1990). The most direct evidence of the ploidy level of a cell is
obtained by counting chromosomes and determining the number pre ent.
As discussed previously, Co"Ie ( 1990) has summari ed the state of know ledge
concerning red algal chromosomes a nd compiled a table of published reports
of red algal chromosome number . Interestingly, a n inspection of this table
reveals a disproportion a tely high number of published values are for
bangiophycid red algae (i.e., Bangia les, Compsopogonales, Porphyridiales,
Rhodochaetales) and four orders of the florideophycid red algae
(Acrochaetiales, Batrachospermales, Nemaliales, Gelidiales) , groups that are
characterised by relatively low numbers of chromosomes (n;:::; 2- 10). For
the remaining florideophycid red algae, where greater numbers of
chromosomes genera lly occur (n ;;::: 10), the majority of published counts were
made prior to 1965, underscoring the lack of attention devoted to
karyological studies of Rhod o phyta during the pas t 25 years. Consequently,
for most life-history investigations of red algae where the sequence of
morpho logical ph a es has been obtained, cytological data are incomplete or
lacking (see Table VJ , p. 53).
More recently, indirect a pproaches to obtaining information on the
cytological state and ploid y level of red algal thalli have appeared. These
include microspectrophotometry of DNA-specific Feulgen-stained nuclei
(e.g., Hurdelbrink & Schwa ntes , 1972; Breeman, 1979) and DNA-binding
fluorochromes such as OAP! ( = 4',6-di a midino-2-phenylindole), mithra-
mycin, and hydroethidine (Goff & Coleman, 1984, 1985, 1986, 1990; Kapraun
& Bai ley, 1989; Ka praun & Dutcher, 1991 ). l n addition , in the Giga rtinaceae
a nd Petrocelidaceae of the Gigartinales, it a ppea rs possible to determine the
life-history phase based on whether the wall of tha llus cells a re composed
of kappa-family carrageena ns, which are produced by gametophytes, or
lambda-fam il y carrageenans, which are produced by tetrasporophytes
(McCandless, Craigie & Walter, 1973; Chen et al., 1973 ; Waaland , 1975;
Craigie, 1990).
Microspectrophotometry of DAPl-treated cell ha s proved to be pa rti-
cularly info rm a tive in studies of red algae because DAPI binds quantitatively
to D A (i .e., the amount of DAPI associated with D A is directly propor-
tional to the amo unt of D A present) a nd suffers lea t from interference
resulting from non-specific binding to non-DNA component of the cell
(Goff & Coleman, 1990). Thus, indirect determination of ploid y level are
pos ible by measuring fluorescence from ingle nuclei in relative fluorescent
units (rfus), and establishing the "C-va lue" or the qu a ntity of DNA in the
non -replicated hapl oid chromosome complement. Although thi technique
hold much promise for determining the ploidy leve l of even the most
complex red a lgal developmental stages, it i not without its pitfall s. amely,
to protect agai nst misinterpretations due to polyteny or G 2-phase replica ted
D A, the basic -value needs to be carefully determined by examining a
large variety of cells a nd preferably calibrated agai nst actual counts of
 RHODOPHYTA . Ill 49

chrom osome number. Unlike most other eukaryotes, red a lga l cell s a ppear
to spend the vast majority of time in G z, where at lea st two copies of the
nuclea r genome are present (Goff & Colema n, 1984, 1990).
Di xo n ( l 963c) has discu ssed the various problems associated wit h
developing a n acce ptable terminology for describing a nd catego ri sing red
a lga l life histo ries a nd presented so und a rguments fo r the simplicity a nd
efficacy of a 'type' sys tem. Thi s scheme overcomes burden so me nomen-
clatural deficiencies associated wit h other suggested met hod s, fo r example
that of Chapman & C hapman ( 1961 ). The type method has received
widespread adoption by the ph yco logical community as evidenced by its
common use . The type method ha s, however, proved to be useful on ly for
categorising life hi stories in the ftorideo ph ycid red algae beca use of
limita tion s in o ur knowledge of sex ual reproducti o n and variations in the
sex ua l na ture of life hi stories in the bangio phycids.

Life histories of florideophycid red algae

A di cussed in a previo us review (Dixon , 1970a) , Drew ( 1955b) delineated
four types of life history for ft o rideoph ycid red a lgae in a n attempt to
ynth esise the data ava ilable some 35 yea rs ago . Th ese were life hi sto rie
in volvin g: ( I) a ha ploid gametophyte bea ring a ha pl oid ca rpos poro ph yte,
with meiosis occurrin g in the zygo te; (2) a ga metoph yte bea rin g a ca rpo-
sporoph yte, but with quadripa rtite carpospo ra ngi a (carpotetrasporangia)
a nd no inform ation o n the positi o n of meiosis; (3) a hapl oid ga metophyte
with a diploid carposporophyte producing carpospores that give rise to a
diploid tetrasporophyte, mo rph ologica ll y identical to the ga metophyte, with
meio is occurrin g in the tetras porangi um ; a nd (4) an a ppare ntl y trimorphic
life hi sto ry simil a r to the third type with mo rph o logica lly di stinct ga me-
tophyte and tetrasporophyte pha ses, or wth a ga meto ph yte developing
as a 'bud' o n th e latte r.
The first two life-hi story type were referred to as biphasic because of the
existence of o nl y two mo rpho logica l phases, whereas the last two types we re
con idered tripha ic because of the existence of three morphological en ti tie ,
the ga metoph yte, carposporophyte, a nd tetrasporophyte. As poi nted o ut
by Di xon ( l 970a, 1973), Drew's ( l 955b) first life- hi sto ry ca tego ry was
subsequentl y rejected on the basis of the cytological work of M ag ne ( I 960c,
196 la ,b, 1964a), despite the later claim by Faridi ( 197 1) that the site of
meiosis in Batrachospermum moniliforme i the zygote. The seco nd type of
life history is appli cable to o nl y a few species, includin g Liagora tetrasporifera
and Gymnogongrus griffithsiae. In these specie , the site of meiosis is now
as urned, perhap erro neously ( ee Guiry, 1990b), to be the quadripartite
carpotetrasporangium based on limited cytological data ( Boda rd, 1971;
Coute, 1971: ewroth, 1972). The last two tripha ic life histories are now
known to be widespread among ftorideophycid red algae. Since Stosch'
(1965) paper de cribing the life hi tory of Liagorafarinosa, the major focus
of much life-hi tory research ha been the documentation of species with
the fourth type of life history involving morphologically dissimilar but
independent tetra porangial and gametangial phases.
information concerning red algal life histories ha expanded ince the
previous re iew in thi eries (Dixon, 1970a), o ha the number oflife-history
50 ST E VE N N . M U RRAY AND PET E R S. DIXO

type . Four majo r types o f ftorid eophycid life hi sto ries were outlined by
Di xo n ( 1973), who substituted the Lemanea-t ype li fe hi story, in vol ving
soma ti c meiosis a nd o nl y ga meta ngia l a nd ca rpospora ngia l ph a es, for
Drew's ( I95 5b) no n-ex istent first life-hi sto ry type. La ter, Dixo n ( I 982b)
added a fifth type, the Pa/m aria-type life hi sto ry, to the four types described
previo usly. Othe r wo rke rs have ho wever, develo ped schemes with 6
(D esikacha ry, Krish na m urth y & Ba la kri shna n, 1990), 7 (Chiha ra , 1975), 8
(G a bri elso n & G a rba ry, 1986), 9 (U meza ki , 1977), a nd 11 (Umeza ki , 19 9)
life- histo ry ty pes fo r ft o rideophycid red a lgae, reflecting bo th ex pa nsio n in
knowledge a nd t he di ffic ul ties inherent in empl oying co nsistent criteri a in
the ca tego risatio n of species ex hibiting subtle but impo rta nt differences in
complex li fe- hi sto ry pa tte rn s. H erein , a scheme depicting 10 types o f life
hi story fo r ft o rideo phycid red algae i presented (T a ble V, p. 42). The first
eight of these are sex ua l life histo ries invo lvi ng ga me te fu sio n a nd meiosis.
T he last two (T ypes 9 and 10) represent modi fica tio ns o f sex ual life hi sto ries
whereby the develo pmen t of pres umably a po meio tic tetras pores recycles the
spora ngial phase o r the develo pment o f ca rpospo re occurs a poga mo usly o r
a po m ictica ll y a nd recycles the ga meta ngia l phase. These las t two no n-sex ual
life his tories have been added to the list o f ty pes foll o wing the lea d o f
Umezaki ( 1977, 1989) beca use of their broad occurrence in ft o rid eoph ycid
red a lgae a nd because they invo lve spo ra ngia l struct ure o rdina ril y associa ted
wit h sex ual reproductio n. Li fe hi sto ries whereby re p roductio n is ca rri ed o ut
solely by vegetat ive fr ag ments or specia l propag ules. o r by asex ua l spo res
such as mo nospo res have no t been assigned to a specific life-hi sto ry type.
The ten life-h istory ty pes (T a ble V) a re described below .

Ty pe 1. Audouinell a si m plex/ virga tula-1.1pe Thi s has a sequence of

gameta ngial, ca rpospora ngia l (except in A. simplex) a nd tet ras pora ngia l
phases, the first a nd last bei ng independent a nd mo rpho logica ll y di ssimil a r
or at least sli ghtl y so . T he gameta ngia l phase is sma ller a nd often with a
basa l system differe nt from that of the te traspora ngia l phase. As interpreted
here, development of the ca rpospora ngial p ha e ra nges fro m th a t in A .
simplex where the zygo te direc tl y becomes a carpo pora ngium a nd no
true carposporophyte is prese nt to a situa tio n where a multicellula r
carpospora ngial phase develo ps o n the ga meta ngia l ph ase. Meiosis occurs
pres umably in the tetraspo ra ngi um.

Type 2, Po lysip honia-type Thi s has a sequence of gameta ngia l, ca rpo-

sporangia l a nd tetraspo ra ngia l (or in some cases po lyspora ngia l) phases, the
first a nd last bei ng ind epende nt and morpho logica lly si m ila r, wi th a
m ul ticell ula r carposporangia l phase producin g ca rpo po ra ngia deve lo ping
on the gametangia l phase . Meiosis occurs presum ably in the tet raspora ngium
(polysporangium) .

Type 3, Bonnema isonia hamifera-type This has a seq uence of ga meta ngia l,
carpospora ngia l a nd tetraspora ngia l phases, the firs t a nd last being
independent a nd morp ho logica ll y di simi lar, wit h the tc tras pora ngia l phase
smaller, either cru stose or fi lamentous and often sim ila r to the you ng basa l
systems of the gameta ngia l pha e. A mu lticell ula r carpos pora ngia l p hase
 RHODOPl-IYTA . Ill 51

producing carpospora ngia develops on the garnetangia l pha e. Meiosis

occurs pre urnabl y in the tetrasporangi urn .

Type 4, Lia go ra tetraspo rifera-type Thi s has a sequence of garnetangial a nd

carpo pora ngial pha ses, with on ly the garneta ngial pha se being independ ent.
The multicellul ar carposporangia l pha e develo ps on the garnetangia l ph ase
and produces quadripartite carposporangia ( = carpotetrasporangia). A
tetra porangial pha se is interpreted as being absent. Mei osis occurs
pre urn a bl y in the ca rpotetrasporangiurn . Included in this category is the life-
hi tory type involving the ' tetrasporoblast' type o f carpotetrasporangiurn,
as in Gymnogongrus griffithsiae and ot her Ph yll o ph oraceae.

Type 5, Pa lm aria-type This has a sequence of ga rneta ngia l a nd tetra-

sporangial ph ases, with the la tte r developing directl y from the zygote without
the formation ofa ca rposporophyte or carposporangia . Both the ga rneta ngia l
a nd tetraspora ngia l phases a re ultim ately independent (the tetras po ra ngia l
pha se initi a ll y growi ng o ut of the femal e tha llu s from the zygo te). The ma le
garneta ngia l a nd tetrasporangia l thalli a re morph o logicall y si mila r, but these
pha se differ from female garnetangial th a lli which are very much smaller.
Meio i occurs in the tetrasporangiurn .

Type 6, Rh odophyse rna elegans-type Thi ha a sequence of garneta ngia l

a nd tetras porangia l ph ases . with only the ga rn eta ngia l phase independent.
The tetrasporangial pha se is reduced to two cells (sta lk cell a nd tetra-
sporangiurn) and develop directl y within the zygote. A carposporangial
ph ase a nd carpo porangia are a bse nt fr o m the life hi story. Meio is occurs
in the tetra porangiurn .

Type 7, Audouinella purpurea/ floridul a- type This has a sequence of

ga rneta ngia l, carposporangial a nd tetrasporangial phase , the fir t and last
being independent and morphologica lly di s irnilar, with the garneta ngia l phase
being mailer than the tetra pora ngia l pha e. The tetra porangial pha e
develop directly from the carpo porangial phase (or imply the zygote in
which ca e a carposporangial pha c i technically ab ent), ultimately
becoming independent of the gameta ngial pha e. fn all cases, carpo porangia
are ab ent a nd the tetrasporophyte grow directly from the carpo porangial
pha e (or zygote). Meiosi occu r pre um ably in the tetra porangium .

Type , Lemanea-type This ha a seque nce of garnetangial and carpo-

porangial pha e , \ ith o nl y the garnetangia l pha e being independent. The
multicellular carpo porangial phase develop on the garnetangial pha e and
produce carpo porangia . tetra poroph) te pha e and tetra porangia are
lacking with meio i occurring omatically during the de elopment of the
gametangial pha e.

Type 9. direct derelop111e111 1ype-1e1raspora11gial phase Thi life-hi tor} l)pe

ha the tetra porangial pha e recycling producing a equence of independent
tetra p rangial pha e . Both a garnetang1al pha e (and gametangia) and a
carpo ' p rangial pha e (and carpo porangia) are ab ent. Tetra porangia
52 ST EV E N . MURRAY AND P ET E RS . DIXO

fun c ti o n as mitospo rangi a (apo mei o tic develo pment) a nd a sex ua l cycle does
no t occur in the li fe hi story.

Type JO, direct del'elopmenl ty pe-gam etang ial phase This life-history type
has ga meta ngia l tha lli recycling, producing a sequence o f ga meta ng1a l a nd
ca rp ospora ngia l phases, bu t o nl y the ga meta ngia l ph ase is independent. The
multicellula r ca rpospora ngia l ph a e develo ps o n the ga me tan gial phase
a po mictica ll y either direqly fr o m the ca rpogo ni a l a ppara tus o r fr o m
no n-ga meta ngia l cell ( = apogam o us development) a nd produces carpo-
spo res th at recycle th e ga meta ngia l phase. A tetras po ran gial phase a nd
tetra pora ngia a re lacking. A ex ual cycle is a bsent as neither gamete fusio n
no r meio is occur in the life hi to ry.
A compila tio n of info rma ti o n collected o n life hi sto ries of fl o rideo ph ycid
red a lgae is presented in T a ble VI. E mphasis has been placed o n those tudies
where the life hi sto ry was determ ined by fo ll o wing the sequence o f mo rpho-
logica l ph ases under la bora to ry c ulture co nditi o n . Al o included a re the
results of selected ka ryo logica l studies (i.e., ch ro m o o me enume rati o ns)
where t he principal a im was to cla rify life hi sto ry events. Li sted fo r ea ch
taxo n are: ( I) the locatio n(s) where the studied ma teri a l was co llected ; (2)
the life-hi sto ry type uppo rted by the publi hed in fo rm a ti o n; (3) the na ture
o f the o bservatio ns perfo rmed to esta bl ish the life hi sto ry, includin g whether
o r not ka ryo logica l da ta a re presented ; a nd (4) the publi shed so urces fr o m
which the li sted info rm a tio n was o bta ined .
Obvio usly, a co mplete listin g of a ll publi hed acco unts o f fl o rideo ph ycid
life hi sto ries is no t a tena ble goa l given the qua ntit y o f ex isting litera ture
a nd the la rge n umber o f o bscure publica ti o ns with limited circul a ti o n. The
vas t majo rity o f repo rts have, however, bee n included based o n in specti o ns
o f other compila ti o n a nd reviews o ffl o rid eoph ycid life histo ries (e.g., Dixo n,
1963a , 1970a, 1973; Kn aggs, 1969; U meza ki , 1977, 19 9; West & H o mmersa nd,
198 1); a t a minim um T a ble VI provides a representa tive accountin g of known
life hi stories of fl o rideo phycid red a lgae .
Life-hi sto ry in fo rma ti o n is li sted for a to ta l o f 345 fl o rideophycid taxa ,
a bo ut 60% o f which belo ng to the Cera mi a le a nd Gi ga rtina le , the most
speciose orders o f the Rh odo ph yta. The grea te t di ve rsity of life- hi sto ry
types occur in th e Ac rochaetia les where 7 o f the I 0 life-histo ry types ,
including 6 o f the 8 sex ua l life hi stories, have been repo rted . In co ntrast,
eight fl o rideo ph ycid o rders (Ahnfeltia les, Ba trachosperma les, Cerami a les,
Cora llina les, G elidia les, Gracila ri a les, Pa lma ri a les, Rh od ymeni a les) a ppea r
to exhibit o nl y a sin gle ex ua l life- hi sto ry type.
Of the 10 type o f life hi to ry, o nl y two (T ype I, A udou inel/a simplex/
l'irga tula-t ype a nd T ype 7, A udouinella purpurea/f loridu /a- ty pe) a re restricted
to a single o rde r, in bo th cases, the Acro chae ti a les (T a ble VI) . Two o ther
life- histo ry type (T ype 5, Pa/m aria- ty pe a nd T ype 6, Rliodopliysema
elegans- ty pe) , occur in re presenta ti ve o f two o rd e rs, Acrochae ti a les a nd
Pa lm a ri a les (includin g the Rh odo physemataceae). The sex ua l life-hi tory
type o f most wide prea d occurrence in the fl o rideo phycid s is the
Polysiphonia-ty pe (T ype 2) which has been repo rted to occur in even o rde rs.
In a dditi o n, the Polysiphonia-t y pe life hi sto ry is the o nl y ex ua l type reco rded
fo r fi ve fl o rideo ph ycid o rder , a n o bserva ti o n co nsistent with ea rlie r repo rt s
by Wes t ( 1986) a nd Ga brielso n & G a rba ry ( 1986) who indica ted th a t 100 %
 TABLE VI
L1st111g or selected studies describing life-h1~tory types of ftondeophyc1d red algae Locations of matenal studied are gl\·en !Ogether
w11h l1fc-h1story type :ind n:itun: of -upporting e\tdence. Life-h1stor) t)pes are described in the te\t T)pe I= A.11do11i11ella
/lllfl/i• ,\· \'itJ.:11111111; 2 = /'11/y.11pl11111w: J 81111m·111ut,Olllll humijaa (c = crustose and f = filamen!OUS sporang1al phase). 4 = LIU'.!,Ora
tetm1po11f1 •m, 5 = /'u/111ar1a , 6 = Rhod11p/11 ,u11u degum. 7 = 411do11111dlu purpureaJlondula. h = Lemanea. 9 =direct de,elopmenL.
tetrmporang1al ph.11>C, 10 = direct de,clopment. gametangial phase The t}pe of e\tdence ts coded as follows : aB = carpospore
producrng tctr:i~por.ingi:il pha~c bearing tctrasporang1a (b1sporang1a. polysporang1a). aO = carpospore producing enltl)
rccognisahlc as sporang1al ph:i~e . .iA carpo,porc recycling gametang1al phase. bA = tetraspore (b1spore. pol)spore) producing
;..1mclltngi;tl phase hearing gametang1a bO = tetraspore (b1s po re. pol] spore) producing entll) recognisable as gametangial phase:
h B ...., tetra~porc (hisporc, polyspore) recycling 'porang1al pha se. o B = tetras pora ng1al phase direct I) produced without carpospores:
·\ ~' c~upotctrasporc rroducing gametangial phase. K = ka r)Olog1cal data. no ne = ltfe hi story statement made but \\tlhout
11rp11rti11g e\ idcnc.:c. C) ucstion mark' arrear \\here sup po rting ende nce o r ltfe-h1stor) e'en ts a re not clear or locat1on of collected ~
:i:
material is not gl\ en 0
Cl
0
L1fc-hl\torv -0
Spc:c1es Locauon T) pc · E\ldence Reference :i:
-<
-l
>
J.1p.in a B bA Lee & K urog1. 1983

rrancc a B.bA M agne. 1977, Abdel Rahman & M agne, 1981.

I rancl· Abdel-Rahman , 198:!a. b. Abdel Rahman. 1982
Bnu'h l,Jc, 9'! bA Abdel- Rahman & M agne, 1984
bB Guir) et ul. 1987a
l· ranc.:•· :! bA B1dou\ & M agne. 1989

S"cdcn aB Stegenga & M ulder. 1979

t SA (( 1hf) 9 hB West. 1970c

f·ranc.:c
,- a B'' bA Abdel- Rahman et al. 1990 v.
"'
 ....
"'
TABLE VI -Continued
L1fe-h1story
Species Location Type Evidence Reference

dasyae (Collins) Woelk. (/)

-j
as Acrochaetium dasyae Netherlands I a B, bO Stegenga & Borsje, 1976 rn
densa (Drew) Garbary <
rn
as A crochaetium densum Netherlands I a B,bA Stegenga & Vroman, 1976
flondula (Dillw.) Woelk .
also as Rhodochorton floridulum and Bnush Isles, Netherlands, 7 o B, bA Knaggs & Conway, 1964: Stegenga, 1978,
Rhodothamniella floridula France Abdel -Rahman & Magne. 1990 s:
gynandra c
;>J
as Acrochae11um gynandrum (Rosenv.) Hamel France I, 5,6 a B, bA.o B Abdel-Rahman, 1985; ;>J
Abdel-Rahman & Magne. 1\190 >
hallandica -<
as Acrochae11um hallandicum (Kylin) Hamel Netherlands I a B, bA Stegenga & Bo rsJe, 1977 >
investiens (Lenorm.) Swale & Belcher
z
0
as Rhodochorton investiens British Isles I aB Swale & Belche r, 1963 "O
membranacea (Magnus) Papenf. rn
-j
as Rhodochorton membranaceum USA (Wash) 9 bB West, 1979 rn
moniliforme (Rosenv.) Garbary ;>J

as Chromastrum moniliforme Sweden I aB Stegenga & Mulder, 1979 !'.fl

nemalioms (De Notaris ex Du four) Di xon 0
as Acrochaetium nemafionis France I a B, bA Stegenga & van Erp, 1979 x
parvula (Kyhn) Dixon 0
as Acrochaetium parvulum France I a B, bA Abdel- Rahm a n, 1984
proskaueri (West) G arba ry in Garbary,
Hansen & Scagel
as Acrochaetium proskaueri USA (Wash) 9 bB West, 1972c
purpurea (L1ghtf.) Woelk.
as Rhodochorton purpureum USA (Alaska, Wash, 7 o B, bA West, 1969, I970a , I972a; Stegenga, 1978:
Calif), Chile, Ja pan , Ohta & Kurogi, 1979: Lee, 1985;
Netherlands Abd el-Rahman & Magne, 1990
 reduc/um
as Chromas1rum reduclum ( Rosenv.) Stegenga
& Wissen/ C. kylinoides (Feldmann)
Stegcnga & Wi sscn Sweden a B, bA Stegenga & va n Wi ssen, 1979
rosu/ow ( Rosenv.) Di xon
also as Ky linia rosu/a1a France, Sweden a B, bA Bo illot & M agne, 1973; Stegenga & W issen , 1979;
Abd el Rahman , 1985
secunda1a (Lyngb.) Di xon
as A croclwe tium secundatum France a B, bA Abdel - Rah ma n & Bido ux , 1989
simplex (Drew) Garbary, Hansen & Scagel
as Acrochaetium pectinutum USA (Wa sh , Ca lif) aB , bA West, 1968 ; Abdel-R a hma n & M agne, 1983
Canada ( B. Colmbi a)
subimmersa (Setch. & Gardn .) Garbary & Ru eness
as Rhodochorton subimmersum Japan 4 cA Lee & Ku rogi , 1978
subtiliss1111a ;o
as A crochae tium subtillissimum (Kuetz.) Ha mel France I
::c
a B, bA Abdel Rah man , 1980 0
tetraspora Garbary & Rueness No rway 9 bB Garbary & Rueness, 1980 0
unijila (Jao) Woelk . 0
-0
as A croc/1aeti11m unijilum France aO, bA Abdel Rahman, 198 I ::c
virga1ula (Ha rv) Dixon
as A crochae1ium 1•irga1ulum Netherlands, France
_,
-<
a B, bA Bo rsje, I 973a , b ?'"
NEMA LIAL ES
Cumaglaia
a11dersonii (Far!.) Setc h. & Gardn. USA (Oregon) IO? a? So uth , 1968
? 3f none D eCew, unpubl. , in Garbary el al., 1982
Dermonema
pu/vi11ata (Grunow) Umezaki
also as Nema/1011 pu/vi11atu111 Japan 3f? aO Umezaki , l 967a, l 972a
Ga/axaura
oblongcua (Ellis & Solander) Lamour. USA ( Hawa ii) 3f a B, bO M agruder, 1984b
Gloiophloea
scinaioides J. Ag. Australia 3f a B, bO Hu isman, 1987
He/111in1hocladia
aus1rafts Harv. Japan 3f! aO Umezaki , 1972a
..,,
..,,
 ..,,
TABLE VI-Cominued
"'
Life-history
Species Location Type Evidence Reference

calvadosii (Lamour.) Setch . France 3f aB,K Boillot, 197la , 1974

Germany 3f bO Kammann & Sahling, 1980
senegalensis Bodard Senegal 4 K Bodard, 1971 (/)

Helminthora -!
rt1
divaricata (C. Ag.) J. Ag. France, British Isles 3f aB , bA , K Boillot, 197lb, 1972a; Magne&Abdel-Rahman , <
rt1
1983; Guiry & Cunningham , 1989 z
Liagora z
californica Zeh USA (Calif) 3f aB, bO Hall , 1990
ceranoides Lamour. USA (Florida) 3f aB , bA Brodie, 1990 s:
farinosa Lamour. Italy 3f aB, bO S to sch , 1965 c:
;i::i
distenta (Mert.) C. Ag. France 3f aB , bO Coute, 1971 , 1976 ;i::i
har veyana Zeh Australia 3f aB , bO Guiry & Cunningham, 1989; Guiry, 1990b >
p111nata Harv . USA (Florida) 10, 3f? aO? Brodie, 1990 -<
te/rasporifera Baerg. France 4 cA Coute 1971 , 1976 >
Nemalion
z
0
helminthoides (Veil. in With .) Batt. Canada (N . Scotia) 3f aB , bA , K Chen el al., 1978; Cunningham & Guiry, 1989; ...,
British Isles Guiry & Cunningham, 1989 rt1
-!
British Isles IO? ? Martin, 1969 tT1
as N . multifidum ;i::i
Sweden, Germany 3f aB , K Fries, 1967, 1969; M iiller & Petronijevic, 1979
vermiculare Suringar Japan 3f aB , bO Umezaki, 1967b, 1972a ; Masuda & Umezaki, ~
1977; Masuda & H oriuchi, 1988 0
Nothogenia ><
erinacea (Turn .) Park . S. Africa 3c a B, bO Anderson & Stegenga, 1985 0
ova/is (Suhr) Park . S. Africa 3c aO , bO Anderson & Stegenga, 1985
z
fastigiata ( Bory) Park .
as Chaetangium fastigiatum Kerguelen Islands, C hile 3c aO, a B, K Delepi ne et al., 1979; Collan tes et al., 1981
Scinaia
complanata (Collins) Cotton France 3f a B, bO va n den H oek & Ca rtel -Breeman, l 970b
confusa (Setch .) Hu isman
as Pseudogloiophloea confusa USA (Calif) 3f a B, bA , K Ra mus, 1969c
furcata Zablackis USA (H awaii) 3f no ne Magruder, unpubl. , in Zablackis, 1987
 /orce/1010 Bivona-Bernardi
as S. furce/1010 British Isles IO none Jones & Smith, 1970; Smith , unpubl. ,
in Martin , 1969
France 3f a B, bO, K Boillot, 1968, 1969, 1972a
Germany 3f bO Kornmann & Sahling, 1980
joponico Setch . Japan 3f aB , bO Umezaki, 1971, I 972a
lurgido Chemin France 3f a B, K Boillot, 197lc, 1972a

BATRACHOSPERMALES
Boirochospermum
mohoboleshworensis Balakrishnan & Chaugule India 8 K Balakrishnan & Chaugulc. 1980
moniliforme Roth Germany 8 K,aA Hurdelbrink & Schwantes, 1972; Huth , 1979
vogum (Roth) Ag. ? 8 K Hurd elbrink & Schwantes, 1972
spp Austria, Germany 8 K? Stosch & Theil , 1979
Lemonea ?"
j/uvio1ilis C . Ag. Germany, British Isles 8 K
:c
Huth , 1979, 1981 ; Thirb & Benson-Evans, 1982 0
mamillosa (Sirodot) Silva France 8 K Magne, 1961 a , l 967a, b 0
cote1101a Kuetz. France? 8 K Magne, l 967b 0
-0
parvu/a Sirodot France? 8 K Magne, l 967b :c
sp France? 8 K Magne, l 967b -<
-l
BONNEMAISONIALES ?""
Asparagopsis
ormo1a Harv. France, Algeria 3f aO,bO Feldmann & Feldmann , 1939, 1942, 1952;
Stosch, 1964; Feldm a nn, 1965; Oza. 1977
1oxiformis (Defile) Trev. Japan 3f aO, bO Chihara, 1960, 1961
A troc1ophoro
hypnoides Crouan frat. France IO , (8?) aA Boillot, 1967
British Isles 3c, 9 a B, bA , K Maggs el al., 1983; Maggs & Guiry, 1987 ;
Maggs, 1988
Bonnemoisonia
asparagoides (Woodw.) C . Ag. Norway 8?, (IO?) aA,K Rueness & Asen, 1982
France 8 K Magne, l 960c, I964a
France 3f? aB?, none Feldmann & Feldmann, 1942, 1946;
Cortel-Breeman, 1975
France IO aA Kylin , 1945; Feldmann. 1966 V>
-.I
 TABLE Y I-Continued V>
00

Life-history
Species Location Type Evidence Reference

gemculata Gardn . USA (Calif) 3f aO, bA Shevlin & Polanshek , 1978

hamifera Hariot Canada (N . Scotia) 3f bA Chen et al., 1969, 1970
Germany, British Isles, 3f bA , aO, bO Harder, 1948; Harder & Koch , 1949; Koch , 1950;
Japan Segawa & Chihara , 1954; Chihara , 1961. Vl
-l
Kornmann & Sahling, 1962; Liining, 1980; m
Breeman et al .. 1988; Breema n & Guiry. 1989 <
m
nootkana (Esper) Silva USA (Calif) 3f aO Ch1hara , 1965 z
Delisea z
compressa Levring New Zealand 8 none Bonin & Hawkes, 1988a
e/egans Lamour. New Zealand 8? aA? Bonin & Hawkes, 1988a $::
;aponica Okamura c
;;o
as D. fimbriata (Lamour.) Mont. Japan 10. (8?) aA? Ch1hara, 1962 ;;o
2? )>
New Zealand none Bonin & Hawkes. 1988a
Naccana -<
)>
\\1ggii (Turn .) Endl. France IO, (8?) aA Bo11Iot. 1967
France, British Isles 3f aB , bO Boillot & L'Hardy- Halos, 1975;
z
0
Jones & Smith, 1970 '"C
Pttfonia m
-l
mooreana Levring New Zealand 8? aA? Bonin & Hawkes, 1988b m
okadae Yamada ;;o
as Delisea okadae (Yamada) Japan IO, (8?) aA? Chihara, 1962 ~
Chi hara & Y oshizaki 0
><
GELIDIALES 0
Gelidium z
coulteri Harv. Mexico 2 a B, bA Macler & West, 1987
crina/e (Turn .) Lamour. Australia 2? aO, bA Guiry & Cunningham , 1989
/atifo/ium (Grev.) Born . & Thur. Norway 2 bO R ueness & Fredriksen, 1989
pristoides (Turn .) Kuetz. S. Africa 2 K? Carter, 1985
pusil/um (Stack .) Le Joi. Norway, Bri tish Isles, 2? a B,bA R ueness & Fredriksen, 1989;
Australia G uiry & C unnin gha m, 1989
USA (N. Carolina) 2 K Kapra un & Bai ley, 1989
 Pterocladia
melanoidea (Schousboe ex Barnet) Isla Mallorca, (Spain) 2 bA Fredriksen & Rueness, 1990
Fredriksen & Rueness
lucida (R. Br. in Turn.) J. Ag. New Zealand 2 aB Luxton , 1977

HILDENBRANDIALES
Hildenbrandia
crouanii J, Ag. British Isles 9? b B? Fletcher, 1983
occidentalis Setch. USA (Calif, Wash) 9 bB DeCew & West , 1977a
prototypus Nardo Japan, USA (Alaska) 9 bB Chihara , 1956, 1975; Umezaki , 1969;
DeCcw & West , 1977a
rubra (Sommerf.) Menegh. British Isles 9 bB Fletcher, 1983

GIGARTINALES FAM . Calosiphoniaceae

;:tl
Calosiphonia
vermicu/aris Crouan frat. Syria 3c. 10 aB . bO Mayhoub, 1973, 1975, 1976;
:c
0
Mayhoub et al., 1976 0
S chmitzia 0
-0
evanescens Hawkes New Zealand 10, (8?) aA Hawkes, 1986 :c
hiscockiana Maggs & Gui~y British Isles 3c, 9 a B, bO, bB Maggs & Guiry, 1985; Maggs. 1988 -<
-l
neapolitana (Berthold) Silva France? 3c? aO Feldmann, 1954 )>

GIGARTINALES Fam . Choreocolacaceae

Dawsonioco/ax
bostrychiae (Joly & Yamaguishi-Tomita)
Joly & Yamaguishi-Tomita Australia 2 aB , bA West & Calumpong, 1988a
Har veyel/a
mirabilis (Rein sch) Schmitz & Reinsch Canada (B. Colmbia), 2 K Goff & Cole, 1973, 1976
USA (Wash)

GIGARTINALES Fam. Dumontiaceae

A crosymphy ton
firmum Hawkes New Zealand 3c? aO Hawkes, 1986
purpuriferum (J . Ag .) Sjiistedt France 3c aB , bA , K Cartel-Breeman & v.d . Hoek , 1970; Cartel-
Breeman, 1975; Cartel -Breeman & ten Hoopcn ,
1978; Breeman , 1979; Breeman & ten Hoopen , V>
1987 ""
 TABLE VI-Continued °'
0

Life-history
Species Location Type Evidence Reference

Dudresnaya
japonica Okamura Japan 3c aB,bA Umezaki, 1968; Notoya & Aruga, 1989
minima Okamura Japan 3c aB , bA Migita & Kawamura, 1980; Notoya, 1988 Vl
Dumontia -l
rn
con1or1a (Gmel.) Rupr. British Isles, Netherlands, 2 bA Rietema & Klem, 1981 ; Rietema & Breeman, 1982 <
France rn
Far/oll'ia
z
compressa J. Ag. USA (Calif) 3c bO,aO DeCew & West, 198la
z
confer/a (Setch.) Abbott USA (Calif) 3c a B, bO DeCew & West, 198la s::
mollis (Ha rv. & Bail.) Far!. & Setch. USA (Calif) 3c aB , bO DeCew & West, 198Ia c
;o
Hyalosiphonia ;o
caespitosa Okamura Japan 2 a B, bO Umezaki , l 972b )>
M asudaph ycus -<
)>
irregularis (Yamada) Lindstrom
as Farlowia irregularis Japan 2 bA Shimizu & Masuda, 1983
z
0
Neodilsea "O
crispata Masuda Japan 2? bO Masuda, l 973a rn
longissima (Masuda) Lindstrom -l
rn
as N. integra var. longissima ;o
Vl
Japan 2 a B,bA Masuda, 1973b
Pikea 0
californica Harv. USA (Calif) 3c a B, bO Scott & Di xon , 1971 ><
Japan IO aA? Chihara, 1972 0
Thuretellopsis z
peggiana K yiin USA (Wa sh) 3c aB, bO Dixon & Richardson, 1969; Richardso n & Dixon ,
1970

GlGARTINALES Fam. Furcellariaceae

Furcel/aria
lumbricalis (Huds.) Lamour.
as F. fastigiata British Isles, 2 K Austin , 1960a , b
Denma rk
 Halaraclm'on
ligularum (Woodw.) Kuetz. France, British 3c a B, bA Boillot, 1965, I 972b; Kammann & Sahling, 1977;
also as Cruoria spp Isles, Germany Maggs & Guiry, 1987. 1989
Neurocaulon
grandifolium Rodriguez France 3c a B, bO Codomier, 1969
reniforme (Post. & Rupr. ) Zanard. France 3c a B, bO Codomier, 1972

GIGART INALES Fam. Gigartinaceae

Gigartina
acicularis (Roth) Lamour. France, Brit. Isles 2 aB,bA Guiry , 1984a; Guiry & Cunningham, 1984
canalicula1a Harv . USA (Calif) 2 none West & Guiry, unpubl., in West & Hommersand ,
1981
corymbifera (Kuetz.) J . Ag. USA (Wash) 2 a B, bA Kim, 1976
intermedia Suringar Korea 2 none West & Lee, unpubl ., in West & Hommersand ,

johnstonii Dawson Mexico 2 a B, bA

1981
West & Guiry, 1982
""
:r:
0
lep1orhynchos J . Ag. USA (Calif) 2 none West & Guiry, unpubl., in West & Hommersand, 0
1981 .,,
0
spinosa (Kuetz.) Harv . USA (Calif) 2 none West &Guiry , unpubl ., in West & Hommersand, :r:
1981 ...,-<
teedii (Roth) Lamour. British Isles , 2 aB,bA Guiry, l 984b; Guiry el al., >
France, Italy, Brazil 1987b
Chondrus
crispus Stackhouse Canada (N . Scotia), 2 aB , bA Chen & McLachlan , 1972; Prince & Kingsbury,
USA (Mass) 1973
ocel/arus Holmes Japan, Korea, China 2 aB West & Lee, unpubl., in West & Hommersand,
1981 ; Brodie & Guiry , 1988a, 1989; Guiry &
Cunningham, 1989
ocella1us Holmes f. crispoides Mikami Japan 2 aB Brodie & Guiry , 1988a, 1989; Guiry &
Cunningham, 1989
giganteus Yendo f. jlabella1us Mikami Japan 2? none Brodie & Guiry, 1988a; Guiry & Cunningham,
1989
nipponicus Yendo Japan 2 a B,bA Brodie & Guiry, 1988a , 1989; Guiry &
Cunningham, 1989; Brodie et al., 1991
pinnula1us f. pinnulatus (Harv .) Okamura Japan 2? none Brodie & Guiry, 1988a; Guiry & Cunningham,
1989
°'
 °'"'
TABLE Vl - Conrinued
--- ---
L1fe-h1slory
Species Location Type Evidence Reference

f!/111111/at111 ( I larv .J 0!...amur<i f ar111a1111 (I larv.) Japan 2? none Brodie & Guiry. 1988a: Guiry & Cunningham.
Yamada & M1!...am1 1989 Cll

lr11li1<·11
-l
m
.1p/c11dcm (Sctch & Gardn ) Kyhn <
as Ci1gartma corclata var \f1/e11de11.\
m
USA (Wash) 2?. 9 a B. bB Kim . 1976 z
nm111Cr>f>i11c (Post & Rupr .) Bor) 7
a' (i1gartma corn11C"opi<u• USA (Wash) 9 bB Kim . 1976
Canada (B . Colmbia) 2? aB Kim . 1976 :s:
lwtcrorarpa Posl & Rupr c:
;::i
i.1' Cilgar111w hcrcrocarpa USA (Wash) 2? aB. bA? Kim. 1976 ;::i
R/111dogloss11111 )>

a/h111 · ( I I an ) K)hn SA (Cahf) 2 a B.bA Chen & Mclachlan, 1979 -<

)>
rnllto1111rn111 (J Ag.) A hboll USA (Cahf) 2 none West & Guiry , unpubl.. in West & H ommersand, z
1981 0
ro.1<·11111 (Kyhn) Smith -0
''" Gigar1111a roscc1 USA (Wash) 2 bA? Kim . 1976 m
-l
m
;::i
<3 IG.•\ R 11 NA LES I am Gk,10:,1phontt1ccac
(1/ot •ophrru.' ~
A.ort'clllw11 Lt...'l' & '\ oo Japan Jc a B.bA. Notoya. I983a. I 984a 0
c;/c1ict.\l{'ho11w x
rn111/lan1· ( 11 uds .) Berk anada (N . Scotia). Jc aB.bA Edelstein. 1970: Edelstein & Mclachlan. 1971 : 0
Me\lcO. Japan DeCew et al .. 1981 : Notoya. 1983b
USA (Cahf) IO DeCe" et al .. 1981
Japan 10.(8?) Morohoshi & Masuda. 1980
Brllish Isles. Jc. 9 a B. bA. bB Maggs. 1988
Canada (N. Scoua)
l'1'rllcilhms I arl USA (Cahl) Jc aB . bO DeCe" et al.. 1981
Sl·hu11111t•l111cmw
p/11111<'.'<l (Scld1 ) \ hhLlll Japan 10? aA' Ch1hara. 1972
GIGARTINALES Fam. Halymeniaceae
Dermocorynus
mo111ag11ei Crouan frat. British Isles 2 a B, bA Guiry & Maggs, 1982
Gra1e/oupia
111rU111r11 Yamada Japan 2 ? Ohgai & Matsui, 1976
Halymenia
floresia (Clem .) C. Ag. France, Yugoslavia 2?,(8?) aO van den Hoek & Cortel- Breeman , 1970a
/a1ifolia Crouan frat. in Lloyd ex Kuetz. France. British Isles 2 aB , bA Codomier, 1974a; Maggs & Guiry, 1982b

GIGARTINALES Fam. Kallymeniaceae

Ca//ophy//is
firma (K ylin) Norris USA (Calif) 2 a B,bA Murray & Dix on, 1972
/acinia1a (Hud s.) Kuetz. France 2? aB Yarish er al., 1984
Cirr11/icarp11s
caro/inensis Hansen USA (N . Carolina) 10 aA? Hansen, 1974, 1977 ;o
Kallymenia :r:
0
req11ie1111ii J. Ag. France 3c? aO Codomier, I 974b 0
feldmannii Codomicr France 3c? aO Codomier, I 974b 0
-0
Meredi1hia :r:
m1crophy/la (J . Ag.) J. Ag. British Isles 3c a B, bO Guiry & Maggs, 1984 -<
as Kallymenia microphylla France 3c? aO Codomier, 1973 -l
)>

GIGARTINALES Fa m. Nemastomataceae
Predaea
kraf1ia11a Millar & Guiry Australia 3f a B, bO Millar & Guiry, 1989
feldmannii Boerg. Venezuela 3f aB Lemus & Ganesan , 1977
ollivieri J. Feldm. Greece 3f aO, aB? A thanasiadis, 1988
we/dii Kraft & Abbott
as P. p11silla Venezuela 3f aB Lemus & Ganesan, 1977
Schizymenia
dubyi (Chauv. ex Duby) J. Ag. France, Portugal 3c aO,bO Ardre, 1977, 1980; Migita & Kawamura, 1980
France 10? aA? Codomier, 1981
pacifica ( Kylin) Kylin USA (Calif), Mexico 3c, 2? bO,aO DeCew & Moe, unpubl. ; Moe, unpubl. , in
West & Hommersand 1981
Tsengia
nakamurae (Yendo) Fan & Fan
as Nemas1oma nakamurae Japan 2 aO , bO Umezaki, 1974a °'w
 TABLE VI -Coniinued ...
°'
Life-history
Species Location Type Evidence Reference

GIGARTINALES Fam . Peyssonneliaceae

Haematocelis
fissurata Crouan frat . British Isles 3c bO Maggs & Guiry, 1982c ...,
(/)

Peyssonnelia ['Tl
conchicola Pece. & Grun . ? 2 ? Umezaki, 1974b <
['Tl
z
GIGARTINALES Fam . Petrocelidaceae z
Mastocarpus
1ardin11 J. Ag. 5:
as G1gar1111a agardhii USA (Calif, Oregon , 3c, 10 aO,aA West et al. , 1978, 1983 c
;>::J
Wash) ;>::J
pacificus ( KJellm.) Perest. >
also as Gigartina ochotensis and Petrocelis spp Japan , USA (Alaska) 3c, 10 a B, bA,aA Polanshek & West , 1975; Masuda & Uchida, -<
1976; Ohno et al. , 1982; Masuda & Kurogi , >
1981 , 1985; West et al., 1983; Masuda et al.,
z
0
1984 "'O
papillatus (C . Ag.) Kuetz. ...,
['Tl

also as Gigartina papillata and Petrocelis spp Mexico 3c aO, bA Polan shek & West , 1977; West et al., 1983; ['Tl
Zupan & West , 1988 ;>::J

USA (Calif, Oregon , 3c, 10 a B, bA,aA West , 1972b; Polanshek & West, 1975, 1977; ~
Wash, Alaska), West et al., 1983; Zupan & West , 1988 0
Canada (B. Colmbta) x
stellatu' (Stackh. in With .) Guiry 0
also as Gigartina stellata , G. mammillosa a nd British Isles, France, 3c, 10 aB,bA,aA West & Polanshek , 1975; West et al., 1977, 1983;
Petrocelis spp USA (Maine), Japan Dion & Delepine, 1979; Fletcher & Irvine,
1982; Guiry & West, 1983; Masuda et al.,
1987; Maggs, 1988
Spain, Portugal 3c aO Guiry & West , 1983; West er al.,, 1983
Denmark, Iceland , 10 aA Rueness, 1978b; Guiry & West , 1983; West
Norway er al., 1983
Canada (N . Scotia) 10 aA Chen et al., 1974; Edelstein et ol., 1974
Canada (N . Scotia) 10, 3c? aO, bO, aA , K Maggs , 1988
 Petrocelts
hennedy1 (Harv.) Ba tt. British Isles 2 a B. bO Fletcher & Irvine, 1982

GIGARTINALES Fam. Ph yllophoraccae

Besa
papillaeformis Setch. ? 2 none DeCew & Sil va, unpubl. , in Wes t & Hom mersa nd ,
198 1
Gym11ogongrus
chiton (Howe) Silva & DeCew in Silva
as G. pla1yphyl/11s USA (Calif), Canada 4 K Do ubt 1935; Newroth & Ma rkham , 1972;
( B. Colmbia) DeCew & West, unpubl. , in Masud a et al.,
1979; McCa ndless & Vollmer, 1984;
Maggs, 1988
complicatus ( Kuetz.) Papenruss South Africa 3c bA Anderso n & Bolto n, 1990
;>:l
crenulatus (Turn .) J . Ag. France 4 bA Ardre, 1977, 1978 :r:
devoniensis (Grev.) Schott. British Isles , Canada IO a A, K Ardre, 1978; Maggs, 1988 0
(N . Scotia) 0
dilatatus (Turn .) J. Ag. So uth Africa 4 bA Anderson & Bolt on, 1990 0
"O
1abelliformis Harv . Japan 3c a B, bA Kasahara , 1977; Masuda et al., 1979; Mas ud a , :r:
198 1 -<
-l
urcellatus (C. Ag.) J . Ag . Chi le 3c a B, bA , K Candia & Kim , 1977; Maggs, 1988; Lewis :>
( = Ahnfeltiopsis?) eta/., 199 1
glomeratus J . Ag. South Africa 3c aB Anderson & Bolt on, 1990
griffithsiae (Turn.) Mart. Brazil 4 bA Cordeiro-M arino & Candia Poza , 1981
leptophy llus J . Ag . USA (Calif) 3c, IO a B, bO,aA DeCew & West, 198 Ib
Mexico 3c a B. bO DeCew & West , 198 Ib
linearis (C. Ag.) J . Ag . USA (Calif) 3c aO, bO DeCew, & West, 1981b
martinensis Setch . & Gardn. ? 3c none Wes t & DeCew, unpubl. , in DeCew & Wes t,
1981 b & Ma suda et al., 1979
parado.\us Suringar
as Al111fe ltia paradoxa Japan 3c none Masuda , unpubl. , in West & Hommersa nd , 198 1
po/y cladus (Kuctz.) J . Ag. South Africa 3c aB Anderson & Bol ton, 1990
vern11cularis (C. Ag.) J . Ag. South Africa 3c? aO Anderson & Bol to n, 1990
Phy llophora
crispa (Huds.) Dixon Algeria . N . Atlantic 2? none Scho ll er, 1968; Newroth , 1972
heredia (Clem.) End!. Algeria , N . Atlantic 2? none Scho ller, 1968; Newroth , 1972
°'
V>
 TABLE VI-Continued °'
°'
--
Life-history
Species Location Type Evidence Reference

pseudoceranoides (Gmel.) Newroth & Taylor British Isles, Canada 2 a B, K Newroth, 1972; Newroth & Markham, 1972
(N. Brnswk)
as P. membranifolia Algeria 2? none Scholler, 1968 (/)

/rail/ii Holmes ex Batt. British Isles, N . Atlantic? 3c aO, bA, K Newroth & Markham , 1972; Maggs, 1989 -I
["Tl
1n111ca1a (Pallas) Newroth & Taylor British Isles, Canada 4 bO, K Newroth , 1971 <
["Tl
(N . Brnswk)
z
GIGARTINALES Fam . Polyideaceae
z
Polyides :;::
rowndus (Huds.) Grev . c
;:o
as P. caprinus British Isles 2 ? Rao, 1956 ;:o
>
GIGARTINALES Fam. Pseudoanemoniaceae -<
Hummbrella >
hydra Earle New Zealand 10?, (8?) aA Hawkes , 1983 z
0
"C
GIGARTINALES Fam. Solieriaceae ["Tl
-I
Agardhiel/a ["Tl
.rnbulaw (C. Ag.) Kraft & Wynne USA (Conn) 2 aB Yarish e1 al., 1984 ;:o
£11che11111a ~
11nc111all/m Setch. & Gardn . Mexico 2 a?, b? Polne el al., 1980 0
Gardneriella ><
/l/berijera Kyhn USA (Calif) 2 a B,bA Goff, 1981 0
Turnerella z
111er1e11siana (Post. & Rupr. ) Schmitz Japan 3c aB , bO Kasahara, 1980
pennyi (Harv .) Schmitz Canada (Newfndlnd) 3c a B, bO South el al., 1972

GRACILARIALES
Gracrlaria
b11rsa-pas1oris (Gmel.) Silva British Isles 2 none Mclachlan, unpubl., in Bird et al., 1982
cervicomis (Turn.) J. Ag. Brazil 2 aO,bA Oliveira & Plastino, 1984 '
 crassiss;ma Crouan frat. ex J . Ag. Brazil 2? b? Oliveira & Plastino, 1984
debilis (Forsk.) Boerg. Brazil 2 a B, bA Oliveira & Plastin o, 1984
foliifera (Forsk .) Boerg. British Isles 2 a B,bA Mclachlan & Edelstein , 1977
"/emaneiformis" Chile 2 aB,bA Plastino & Oliveira, I 988b
pacifica Abbott
as G. verrucosa Canada (B. Colmbia) 2 a B,bA, K Bird el al., 1982
1ikvahiae Mclachlan E. Canada 2 a B, bO Bird el al., 1977
" verrucosa " Japan 2 aB,bA Ogata era/., 1972; Yamamoto & Sasaki, 1987
verrucosa (Huds.) Papenf. Norway, British Isles 2 aB , bA , K Rueness er al., 1987; Bird er al., 1982
" verrucosa " Brazil 2 aB . bA Oliveira & Plastino, 1984

AHNFELTIALES
Ahnfe/1ia
(Ahnfelriopsis) concinna J . Ag. USA (Hawaii) , Japan 3c a B, bA Magruder, 1977; Masuda, 1983
fasrigiara (Post. & Rupr. ) Makienko
(Ahnfelriopsis) sp
Canada (B. Colmbia) 3c a B, K Maggs er al., 1989
""
:r:
0
as A. gigartinoides J. Ag. Mexico 3c a B, bO DeCew & West , 1977b 0
plicara (Huds .) Fries 0
-0
also as Porphy rodiscus spp Canada (N . Scotia), 3c aB , bO. K Farnham & Fletcher, 1973, 1976; Chen , 1977; :r:
France Maggs & Pueschel, 1989 -<
-l
CO RALLINALES
>
Amphiroa
ephedraea (Lamarck) Decaisne Japan 9 bB Chihara, 1975
Coral/ina
officinalis L. France, Italy 2 aO, bA , K Yamanouchi , 1921 ; Stosch, 1969
Dermarolirhon
corallinae (Crouan frat.) Foslie
also as Lirhophyllum coral/inae Sweden 2, 9 K Suneson, 1950, 1982
lirora/e (Suneson) Hamel & Lemoine
also as Lirhophy llum lirorale Sweden 9 K Suneson, 1950, 1982
Fosliella
crucia1a Bressan Australia 2 bO Jones & Woelkerling, 1983
farinosa (Lamour.) Howe British Isles 9 bB Chamberlam, 1977
Jania
rubens (L.) Lamour. France 2? bA , aB, K Stosch, 1969 _,
°'
 TABLE VI-Continued °'
00

Life-history
Species Location Type Evidence Reference

Pneophy//um
lobescens Chamberlain British Isles 2,9 aB, bA , bB Chamberlain, 1987
my riocarpum (Crouan frat.) Chamberlain British Isles 2 aB,bA Chamberlain , 1987 en
--l
pluri11alidum Chamberlain British Isles 9 bB Chamberlain, 1987 CTI
zonale (Crouan frat.) Chamberlain British Isles 9 bB Chamberlain, 1987 <
CTI
=ostericolum (Foslie) Fujita z
as Fosliella zostericola Japan 2 a B, bA Fujita , 1988 z
RHODYM ENI ALES 3::
Binghamiopsis c
;i:l
caespitosa Lee, West & Hommersand USA (Calif) 2 aB , bA Lee et al. , 1988 ;i:l
Botryocladia )>

ardreana Brodie & Guiry -<

)>
also as B. boergesenii Portugal 2 a B, bA Brodie & Guiry, 1986, 1988a
pseudodichotoma (Fart.) Kylin USA (Calif) 2 none Lee & West , unpubl. , in West & Hommersand,
z
0
1981 -0
wynnei Ball antine Puerto Rico 2 a B, bA Ball antine, 1989 CTI
--l
Champia CTI
par11ula (C. Ag.) Harv. Steele, pers . comm., in West & Hommersand, ;i:l
USA ( Rh ode Is), Korea 2 none
1981 ; Steele et al., 1986; Lee & West, unpubl. , en
in West & H ommersand. 1981 and Lee & 0
West, 1980a x
Cordylecladia
erecta (Grev .) J. Ag.
Fauchea
British Isles 2 bA , aB Brodie & Guiry, 1988b -
0

laciniata J . Ag. USA (Calif) 2 aB Sparling, 1961

as F. pygmaea USA (Wash) 9 bB West & Norris, 1966
Gastroclonium
subarticulatum (Turn.) Kuetz.
as G. coulteri 2 none Lee & West, unpubl. , in West {ii. Hommersa nd ,
1981
 lomentarw
hatleyana CC Ag.) I !arv USA (Conn) 2 bO Yarish et al., 1984
ltakodatensis Ycndo Korea 2 a B, bA Lee & Wes t. 1980a
orcaden.m (Harv .) Collins ex Taylor Bnt1sh Isles 9 bB Foran & Gu1 ry, 1983
as l. rosea Europe 9 K Svedelius, 1937
M1111um
pan-um Moc USA (Calif) 2 a B, bO Moe, 1979

PALMAR IALES Fam. Palmanaccae

De\'O/eraea
ramenwcea (L.) Gu1ry
as l/a/osacct011 rame111aceum anada (N . Scotia) 5 bA , o B, K Vander Mee r &Chen, 1979; Va nderM eer, 198 1b
Iceland 5 K Jonsson & C hesnoy, 1982
fl a/osaccion
;>:l
americanum Lee USA (O regon) 5 bA,o B M itman & Phinney, 1985 :r:
Pa/maria 0
callopltvl/01de.1 1lawkcs & Scagcl Canada (B. Colmbia) 5 none Hawkes, unpubl. , in Ha wkes & Scagel, 1986 0
ltecaten1i.1 1lawkcs Canada (B. Colmbia) 5 none Hawkes, unpubl., in Haw kes & Scagel, 1986 0
"'C
molli.1 (Setch & Gardn ) Van der Meer & Bird anada (B. Colmbia) 5 bA,o B, K Van der Meer & Bird. 1985 :r:
pa/mall/ (L .) Kunt1e Canada (N . Brnswk, 5 bA,o B, K Van der Meer & Chen, 1979; Van der Meer -<
-l
N . Scotia) & Todd, 1980 )>
Japan 5 bA Yabu & Yasui, 1984

PALMAR IAL ES Fam . Rhodophysemataccae

Cortoph1•//11m
£'.\pan.111111 Setch. & Gardn Pacific N . America 4?, 6? bA DeCew, unpubl., in West & Homme rsand, 198 1
P.1e11dorltodod1.1"C111
111ppo11irn.1 Masuda Japan 9? b B? Masuda, 1976
Rltodoph 1•.1ema
ele11wa (Crouan frat ex J Ag.) Dixon NE Canada, Ireland 6 bA, K Saunders eta/., 1989
Canada (Newfndlnd) 9 b B, K Sou th & Whittick, 1976
Bnush Isles 9 ? Fletcher, 1977
/il'or11i1 Ba ttcrs anada (N . Sco tia, 9 b B, K Fletcher. 1975; Masuda & Oh ta, 1975;
P. Edward !. ), Bri ush Saunders & Bi rd, 1989
Isles, Japan
m111111 ll ollcnb. & Abbott
°'
as R l'iegan.1 Japan 9 bB Mas uda & Oh ta, 198 1a "'
 TABL E VI - Continued ....,
0

Life-hi story
Species Location Type Evidence Reference

odon1haliae Masud a & Ohta

as R. elegans USA (Calif) 6 bA DeCew & West , 1982
USA (Calif) , Japan 9 bB Ganesan & West, 1975; Masuda & Ohta, 198lb Vl
-l
m
CE RAM IALES <
Anisoschizus m
propaguli Huisman & K raft Australia 2?
z
bO Hu isman & Kraft . 1982 z
Anotrichium
yagii (Okamura) Bald ock Korea 2 aB , bA Kim & Lee, 1986 3::
Antithammon c
;:o
boreale (Gobi) Kjellm. Spitzbergen, No rway, 9 bB Sundene. 1962 ;:o
Sweden )>
cruciarum (C. Ag.) Naeg. USA (N . Carolina). 2?, 9? none Kapraun , 1977b; Whi11 ick & Hooper, 1977 -<
)>
Canada (Newfndlnd)
defectum Kylin USA (Wash) 2 a B, bA West & Norris, 1966; Lee & West I 980b
z
0
hererocladum Funk Greece 2 a B, bA , K A thanasiadis, 1983 -0
ky linii Gardn . USA (Wash) 2 none West & Norris, 1966 m
nipponicum Yamada & Inagaki -l
Korea 2 a B, bA Lee & West, I 980b m
sparsum Tokida Korea 2, IO a B, bA , aA Boo & Lee, 1983 ;:o
tenuissimum ( Hauck) Schiffner France 2 a B. bA. K Sundene, 1964a; Rueness & Rueness, 1973 Vl

Antithamnionel/a 0
occidentale K ylin x
as An1i1hamnio11 occidentale USA (Wash) 2 a B, bA West & Norris, 1966 0
sarniensis Lyle
also as Antirhamnion sarniense France, British Isles 2, 9 a B, bA, bB, Sundene, 1964b; Stosch, 1969; L' Ha rd y- Halos,
K 1968, 1985, 1986; Magne, I 986a , b
spirographidis Schiffner
also as Antithamnion spirographidis British Isles, France 2 a B, bA Drew, 1955a ; L' Ha rd y- Hal os, 1968. 1985, 1986
Bostrychia
binderi Ha rv. 10, 2 none West & colleagues , unpubl. , in West &
Calumpong, 1988 b '
 •)
111rmtugne1 I !Jn 2 none West & colleagues. unpubl. . in West &
Calumpong. 1988b
c~
•)
111rmt:1C111u '>ondcr Kuct7 2 none West & colleagues. unpubl. , in West &

pmnata TanJkJ & Ch1hara

., 2 none
Calumpong. 1988b
West & colleagues. unpubl. , in West &
Calumpong. 1988b
rad1<w11 (~ont J ~ont USA (1' Jersey) 2 a B. bA Yarish & Edwards . 1982
?
10 none West & colleagues, unpubl. . in West &
Calumpong, I988b
tc111·/la (Lamour ) J Ag . Puerto Rico 10.2? aA.bA West & Calumpong, 1988b
Philippines 10 aA West & Calumpong, 1988b
( al/11/1C1m1111111
hmlni I larv USA (M ass.). Canada 2 a B,bA Wh1tt ick & West, 1979
( Newfndlnd)
;i::i
h1pm1111111111 ( rouan frat Norway 2 a B,bA Rueness & Rueness, 1980
luu·r111·.1£"1111 Aponte & Ballanunc Puerto Rico 2
::c
a B,bA Apon te & Ballantine, 1990 0
h1 ·~:wuln Arnott c~ 1lar• in I look Norway. USA (Texas. 2 a B.bA Edwards, I 969a, 197 1; Ka praun , I 978a; 0
"'"' a\ , Jg/aotlwmnum hyu111d1•.1 N Carolina). Sweden. Ru eness & Rueness. 1980: L' Hardy- Halos 0
-0
rrance & Rueness, 1990 :r:
'al/11p/111/ultwla Ya mad a Korea 2 a B,bA Boo et al.. 1989 -<
-l
rnrdat11m Bucrg USA (Texas) 2 a B,bA. K O ' Kelly & Baca. 1984 >
'11r .rmh11111111 (Sm ) Lyngb Germany 2. 9 a B,bA, K H assmger- H umnga, 1952
lw11A"'1 CD1ll11. ) S I Gray Canada (Newfndlnd). 2 a B,bA. K Edwards. 1977, 1979. Wh1lllck. 1981a,b:
British Isles, Norway. R ueness & Rueness, 1982
N France, Faroe
Islands
1.-1r11i:m111111 (With ) S I Gray Sweden 2 a B,bA Rueness & Rueness, 1985
'f' SA (Wash) 9 bB West & Norri s, 1966
Cal11i:lm1t1
'"'"'''""' (Mont l J Ag. USA (N Jersey) 2 a B, bA? Yarish & Edwards. 1982
( '11111prl<1<plwra
h1p11111·11uln J Al,! Japan 2 a B, bA Notoya, 1979
Cn1tron·rt1\
dt1111/111111n (( '\g ) Mont Bra11l 2 bO? Oli veira & Brinall, 1974
(\•rtJlllllllll
1111g11/1111m1 Weber 1an Bo"c Italy 9 bB Cormac1 & M o tta , 1989 _,
 TABLE VI-Continued -..J

"'
Life-history
Species Location Type Evidence Reference

jlabelligerum J. Ag. British Isles 2 bA Edwards, 1973

gardneri Kylin USA (Wash) 2 none West & Norris, 1966
japonicum Okamura Japan 2 aB,bA, K Notoya & Yabu , 1979a Vl
kondoi Yendo Japan aB,bA , K Notoya & Yabu. 1979a; Suh & Lee, 1984 -l
2 (Tl
pedicillatum DC British Isles 2 a B,bA Edwards, 1973 <
(Tl
rubriforme Kylin Canada (N. Scotia) 2 a B,bA Garbary et al., 1978 z
rubrum (Huds.) C. Ag. British Isles. 2 aB,bA Edwards, I 973; Garbary et al. , 1978, I980a;
Canada (N. Scotia), Garbary, 1988
z
USA (Wash) s:
shurrleworthianum (Kuetz.) Silva British Isles 2 a B, bA Edwards, 1973 c
;;::i
srricrum Harv. Norway 2 aB , bA Rueness, l 973a ;;::i
Choreocolax )>
polysiphoniae Reinsch USA (Calif) 2 a B, bA , K GofT & Coleman, 1984 -<
)>
Crouania
pleonospora Taylor USA (Florida) 2 aB , bA Prince, 1979
z
Dasya .,,
0
(Tl
c/avigera (Womersley) Parsons Australia 2 aB,bA Parsons , 1975 -l
Dasysiphonia (Tl

chejuensis Lee & West Lee & West , 1979; Choi & Lee, 1988 ;;::i
Korea 2 aB , bA
Deuca/ion ~
/evringii (Lindauer) Huisma n & Kraft Australia 2 bA Huisman & Kraft, 1982 0
Griffirhsia ><
jlosculosa (Ellis) Batt. France 2? bA ,a B Stosch, 1969 0
globulifera Harv . z
as G. borneriana Far!. USA (Mass, NY) 2 K Lewis, 1909
japonica Okamura Japan 2 bA ,a B lima & Migita , 1990
Grinnelia
americana (C. Ag.) Harv. USA (Conn) 2 bA Yarish er al., 1984
H erpochondria
elegans (Okamura) ltono
as M icroc/adia elegans Japan? 2 aB,bA Notoya & Saito, 1980
Hererosiphonia
1aponica Yendo
as H . densiuscula and H . asymmerria USA (Wash) 9 bB West , 1970b
pulchra (Okamura) Falkenb. Japan 2 a B, bA Notoya & Yabu , 1979b
Hypoglossum
rhizoplwrum Ballantine & Wynne Puerto Rico, 2 a B, bA Ba llantine & Wynne, 1988
Guadalupe Is
nipponicwn Yamada Japan 2 a B,bA Notoya , 1986
Laurencia
brachyc/ados Pilger USA (Hawaii) 2 a B, bA Mc Dermid, l 990
pinnara Yamada Japan 2 aB , bA N otoya er al., 1978
Leve ii/ea
1imgermannioides (Her. & Mart.) Harv . India , Japan 2 aB , bA , K Rao, 1967; N otoya, l 984b
Lophocladia
;>:l
/allemandii (Mont.) Schmitz Italy 2 bA Cormaci & Mo tta , 1985 ::r:
Ma zoyerella 0
arac/moidea Gord -Mill s & Womers. Australia 2 aB , bA Gordon-Mills & Womersley, 1974 0
M embranoprera ..,,0
mu/11ramosa Gardn . USA (Calif) 2 a B, bA Waal and & Kemp, 1972 ::r:
pla1yphylla (Setch. & Gardn .) Kylin USA (Wash) 2 none West & N orris, 1966 -<
...,
M icrocladia >
califomtca Far!. USA (Calif) 2 a B, bA , K Gonzalez & Goff, 1989
co11/1eri Harv . USA (Calif) 2 a B, bA , K Gonzalez & Goff, 1989
Murra ye/la
periclados (C Ag .) Schmitz Puerto Rico 2 a B, bA Aponte & Ballan tine, 1987
Neorhodomela
aculeara (Perest.) Masuda
also as N. larix (Turn .) Masuda Japan 2 aB , bA Masuda , 1982
mun/la (Percst.) Ma suda Japan 2 a B, bA Masuda , 1982
oregona (Do ty) Masuda Ja pan 2 a B, bA Masuda , 1982
Odo111halta
annae Perest. Japan 2 aO, bA Masuda, 1982
corymbifera (Gmel.) Grev . Japan 2 a B, bA Masuda , 1982
jloccosa (Esper) Falkenb. Canada (B. Colmbia), 2 K Goff & Cole , 1973
USA (Wash)
macrocarpa Masuda Japan 2 a B, bA Masuda , 1982 _,
w
 ,,._,
TABLE VI-Continued
---
Life-history
Species Location Type Evidence Reference

Platythamnion "'
-l
('Tl
ye=oense Inagaki Japan 2 a B,bA,K Notoya & Yabu, 1980; Notoya, 1983c
sp
<
USA (Wash) 2? K West & Norris, 1966 ('Tl

Pleonosporium z
caribaeum (Boerg.) Norris Korea 2 aB.bA Kim & Lee, 1988
pusillum Yamada Korea 2 aB, bA Kim & Lee, 1988 s:
Plumaria c
elegans ( Bonnem.) Schmil7 Norway, Brit ish Isles 2? K ;>:>
Drew, 1939; Rueness. 1968 ;>:>
Polysiphonia :>
decumbens Segi Korea 2 a B, bA By1!n & Kang, 1986 -<
denudata (Dillw.) Kuetz. USA (Texas, N . Carolina) 2 a B, bA Edwards , l 970b; Kapraun , l 978b :>
echinata Harv. Texas, USA 2 none Edwards, l 970c z
feru/acea Suhr 0
USA (N. Carolina), 2 a B, bA , K Kapraun 1977a, 1978b "'t>
Bermuda ('Tl
fibriata (Dillw.) Harv. in Hook . Germany 2? a B, bA Stosch, 1969 -l
('Tl
jlexicaulis (Harv.) Coll. ;>:>
as P. vio/acea USA (Mass) 2 a B?, bA?, K Yamanouchi, l 906a, b ~
gorgoniae Harv. USA (Texas) 2 none Edwards, l 970c 0
hem1sphaerica Aresch .
var. hemisphaerica Scandinavia 2 a B, bA
><
Rueness, 197la , 1973b 0
var. boldii (Wynne & Edwards) Rueness z
also as P. denuda1a USA (Texas) 2 a B, bA Edwards, 1968, l 969b, l 970a; Rueness,
197 la, l 973b
;aponica Harv.
also as P. akkheshiensis Japan 2 a B,bA Kudo & Ma suda , 1986
urceo/a1a (Lightf.) Grev . USA (N . Carolina, 2 aB?, bA? Kapraun , l 978b. 1979
N . Hampshi re, Ma ss),
Norway
P.11/otha/110
dentata (Okamura) Kyl Korea 2 a B,bA Fredriksen et al., 1990
Pterothammon
p/umula (Eiits) Naeg.
also as Antithammon plumu/a Germany 2 a B,bA Sundene, 1959, 1975; L' Hardy- Halos, 1968;
British Isles, Stosch , 1969; Rueness & Rueness, 1975;
Sweden, Norway, Athanasiadis, 1985
Greece
Pterosiplwnia
grac1/i.1 Kyhn USA (Wash) 2 none West & Norris, 1966
pennata (C Ag .) Falkenb. Japan 2 a B, bA Masuda , I 973c
Rhodome/a
confervoide.I' (Huds .) Silva France 2 a B, bA Masuda, 1982
lrcopodwides (L.) C Ag. ;;:;
f tenui.rnma ( Rupr) Kjcllm Japan 2 a B,bA Masuda , 1982 :r:
.1achalinensi.1 Ma suda Japan 2 aO.bA Masuda , 1982 0
tere.1 (Perest) Masuda Japan 2 a B, bA Masuda, 1982 0
0
Rhodopti/11m "'O
plumomm (I larv & Bail ) Kyhn USA (Cahf) 2 a B.bA Miller, 1980 :r:
Scugelia -<
--l
pyla1.1ae1 (Mont ) Wynne USA (Mass) 2 K? Goff & Goleman , 1990 >
Spermotham11111n
r<•pens (D1llw .) Roscnv Norway, USA (Mass) 2 a B, bA. K Drew, 1934. 1943; Rueness, 1971b
a'> S tumeri
Sp/111ndylothan111io11
111u/1ifid11m (I I uds.) Na cg France 2? a B.bA Stosch, 1969
S1•mphyocladia
la1111,,.ula (1larv.) Yamada Japan 2 bA Matsuyama & Masaki, 1975
pennata Okamura Korea 2 aB,bA Choi & Lee, 1987
Sprridia
/tla111en10.w (Wulf) 1larv . Philippines 2 a B, bA West & Calumpong, 1989
Tiffanie/la
111rderae (Farl) Abbotl
as Spermothamnion .111ydcrae USA (Cahf) 2 K Drew. 1937

_,
V>
76 STEVE N MURRAY A D PETERS. DIXO

of pecies in the Ceramiales, Corallinale , Gelidiales, and Rhodymeniales

display "i omorphic" or Polysiphonia-type life historie . The fifth order
within which the Polysiphonia-type appears to be the only sexual life hi tory
displayed is the Gracilariales, an order whose member have only recently
been widely regarded as distinct from the Gigartinales (see Fredericq &
Hommersand, 1989). ·
The direct development of gametangial thalli from carpospores, a sequence
that by-passes a sporangi&l life-history phase and result presumably from
apomictic development, appears to be mo t common in species assigned to
the Gigartinales and Bonnemaisoniale . A few species of emaliales and
Ceramiale also have this life-history type (Table VI) but to date the direct
development of gametangial thalli from a pre umably apomictically pro-
duced carposporangial pha e has not been reported for members of other
ftorideophycid orders (but ee Krishnamurthy et al., Curr. Sci., 38, 1969).
on-sexual apomeiotic recycling of the sporangial phase by tetraspores,
polyspores or bispores occur in eight (including the family Rhodophyse-
mataceae of the Palmariales) of the thirteen ftorideophycid orders, and is
apparently absent from only the Ahnfeltiale , Batracho permales, Gelidiales,
Gracilariale and emaliales. Interestingly, apomeiotic direct development
of the sporangial phase appears to be best represented in ftorideophycid
orders where monosporangia are not of widespread occurrence and can be
found in only one ftorideophycid order, the Acrochaetiales, where
monosporangia are common . In two of the five orders ( emaliale and
Batrachospermales) where apomeiotic recycling of the sporangial phase
appears to be ab ent, asexual reproduction by monospores is of widespread
occurrence, whereas in a third order, the Gelidiales, asexual reproduction
by vegetative propagation is very common and is perhaps the principal means
of reproduction in many populations. Hence, it i possible that apomeiotic
tetrasporangia may have evolved as an alternative spore-mediated
mechanism of a exual reproduction to monosporangia in certain red
algae.
Karyological determinations of ploidy level have been made in conjunc-
tion with the morphological sequences occurring in the life hi tories of only
a few ftorideophycid red algae. For example, an in pection of Table VI
reveals that karyological data are available for le than 20% of the taxa
studied . This lack of critical information underscores the need for
investigators to obtain karyological information, particularly of spores and
spore products, so that knowledge of the equences of both morphological
and cytological phases can progre . The failure toe tablish the ploidy le el
of a morphological phase compromises the ability to fix the position of
meiosis in the life history, or to determine if gamete fusion has occurred.
For example, confu ion can exist in determining whether an observed life
hi tory sequence involves somatic meiosis, as occur in Le111anea, or apomictic
development involving direct carpospore recycling of the gametangial phase
(Hawkes, 1990). More complete karyological information is needed to clarify
whether such a Lemanea-type (Type 8) or a non- exual direct development
type of life history (Type 10), or both type, occur in severa l ftorideophycids,
including Bonne111aisonia asparagoides, Delisea fimbriara, D. okadae,
Naccaria 111iggii, Schmir::.ia evanescens, G/oiosipho11ia capil/aris, and Halymenia
floresia. As discussed earlier, direct chromosome counts of most red a lgae
...................................................

RHODOPHYTA . Ill 77

are very difficult to obtain. The DNA-binding ftuorochromes such as DAPJ

and hydroethidine have, however, made it possible to obtain important
karyological information, including the establishment of ploidy level, and
should become increasingly useful tools for investigators pursuing questions
concerning life-history events in the red algae.

Life histories of bangiophycid red algae

Knowledge of life-hi tory events in bangiophycids remains much more poorly
developed than for ftorideophycid red algae . This is due in part to the low
level of differentiation that occurs in bangiophycids between ordinary vege-
tative cells and cells that carry out a reproductive function. Also , the common
and often copious occurrence of several kinds of reproductive bodies
contribute to difficulties in convincingly establi hing life histories for
members of this group. As a result of these problems, the number of
bangioph ycid species for which there exists clear morphological and cytolo-
gical evidence for a sexual life history remains low, with cases completely
documented only for species of the economically important genus Porphyra.
Asexual events are common and wide pread in virtually all examined
bangiophycids , including those species where sexual populations are known .
To date, sex ual reproduction appears to be documented (see Gabrielson ,
Garbary & Scagel, 1985; Garbary & Gabrielson , 1990) for members of only
three of the four bangiophycid orders (i .e., Compsopogonales, Bangiales,
Rhodochaetales) accepted in this review . Based on the available information ,
sexual life histories appear to be lacking in all members assigned to the
Porphyridiales (Gabrielson et al., 1985; Garbary & Gabrielson , 1990).
For Com opogonales, asexual reproductive cycles involving two or more
morphological phases are well documented , as for example in Boldia
(Herndon, 1964; ichols, 1964) and Porphy ropsis (Murray, Dixon & Scott,
1972; Kornmann & Sahling, 1985), and all species appear to have some form
of asexual reproduction mediated by monospores. Historically, sex ual
reproduction was reported for Smithora naiadum (as Porphyra naiadum) by
fusion of two released bodies (Knox, 1926), and for Erythrotrichia cornea
(Heerebout, 1968) by the purported fu ion of adjacent thallus cells. Both of
these claim , together with rare report of the fusion of released 's permatia'
with cells exhibiting trichogyne-like protuberances (see Dixon , 1973), are,
however, not well substantiated or widely accepted .
During the last six years, studies by Kornmann ( 1984, 1987) Hawkes
(1988), a nd Magne (1990) have provided evidence that a sexual life history
exists in at least four pecies of Compsopogonale . A sexual life hi story was
de cribed for Porphyrosrromium ciliare (as Eryrhrorrichope/ris ciliaris)
(Kornmann, 1984) a nd Porphyrostromium obscurum (Kornmann, 1987) based
on ob ervation of the fusion of what appear to be spermatia released from
the trichoid pha se with carpogonia that resemble thallus vegetative cells.
Unfortunately, Kornmann (1984, 1987) was not able to determine the
po ition of meiosi in either pecies, but did document for both a sequence
of heteromorphic trichoid a nd peltoid morphological phases. Recentl y,
Magne ( 1990) obtained evidence for a exua l life hi tory in Erythrotrichia
cornea whereby the apical cell of a three-celled gametangial filament
fir t cut off a permatium a nd then became a carpogonium. Following
78 STFVEN . MURRAY AND PETER . D IXON

fertilisation, the diploid zygote i not released but continues to divide to

produce the linear life of cells characteri tic of the filamentous Erythrotrichia
thallu . Magne ( 1990) wa unable to document the ite of meio i but
hypothe ised that the haploid chromo ome complement is established during
the formation of the tricellular gametophyte. Hawke ( 1988) has collected
evidence of gamete production and fu ion in Smithora naiadum, upportiflg
earlier suggestions (Hu, 1902; Knox, 1926; Hollenberg, 1959) that a exual
life history exi t for this taxon. Hawke ' ( 1988) evidence is limited to
ob ervations of gamete fusion, the tructural detail of the gametogenesis
of permatia and carpogonia, and their unique development from a single
parent cell. Hawkes' ( 1988) findings are in many ways para llel to tho e of
Magne ( 1990) as only in Smithora and Erythrotrichia does the same cell first
produce a spermatium and then a ume the role of the carpogonium. Unlike
Magne' ( 1990) work on Erythrotrichia, however, Hawkes ( 1988) wa unable
to document the fate of the zygote in mithora. The ite of meio i wa not
determined for Smithora, and ha still not been verifed for any member of
the omp opogonale .
umerous report of a exual life history appear in the literature for
Porphyra and Bangia, members of the Bangiales ( ee Dixon, l 970a, 1973;
Hawke, 1978; Cole & Conway, 1980). It has been appreciated ince the
work of Drew ( 1949, 1958) that both Porphyra and Bangia have life hi tories
involving a filamentou conchocelis and, therefore, two distinct and
heteromorphic phases. Extrapolating from studies of florideophycid where
the pre ence of distinct heteromorphic pha es appear to be invariably linked
with exual reproduction and numerou equivocal claims for gamete fusion,
it wa often a sumed that such a bipha ic equence repre ented a sexual life
hi tory. A reviewed by Dixon (I 963a, I 970a, 1973), the existence of exual
life histories in Porphyra and Bangia has, however, frequently been
contradicted by cytological data supporting identical chromosome numbers
throughout the sequence of morphological phase . onsequently, exuality
in Porphyra and Bangia ha been a di puted i sue. In thi light, on way
(1964) recommended that the term a- pore and {3- pore be used in tead of
carpo pore and permatia, to avoid the implication of sexuality when the
occurrence of sexual reproduction wa in doubt. Since the last review (Dixon,
I 970a), a clearer picture of life hi Lorie in Porphyra and Bangia ha emerged .
Re olution of the que tion of sex in bangiophycid ha been provided by
Hawke ( 1978) who obtained in Porphyra gardneri both direct ob ervational
evidence of gamete fu ion and production and cytological verification of
reduction in ploidy level resulting from meio i . This tudy by Hawke
(197 ) i ignificant because it e tabli hed, without a doubt, the occurrence
of exual reproduction in bangiophycid red algae.
umerou que tionable reports of gamete fusion in Porphyra ( ee Dixon ,
1970a, 1973: Cole & Conway, 1980; Hawke, 1978) and Bangia ( ee Dixon,
1970a, 1973) appear in literature dating back almo t 150 year . During the
pa t half-century, numerou karyological studie have confirmed the
exi tence of difference in chromo ome number between filamentous
conchoceli (orcarpo pore that give ri e to a conchoceli ) and leafy Porphyra
(e.g .. Magne, 1952: Kito. 1966, 1967, 1968, 1974. 1978: Migita, 1967; Giraud
& Magne. 196 : Yabu. 1969a.b. 1970. 1971, 1972, 1978; Kito. Ogata &
Mclachlan. 1971: Mumford, 1975: Mumford & ole. 1977; Hawke. 1977.
----------------------------------~
RHODOPHYTA . III 79

1978; Cole & Conway, 1980; Krishnamurthy , 1984; Ma & Miura , 1984;
Burzycki & Waaland, 1987; Tseng & Sun , 1989) or multiseriate, filament-like
Bangia thalli (Yabu , 1967; Co le, 1972, 1990; Co le, Hymes & Sheath, 1983).
Based on chromosome counts, it appears that a biphasic sexual life history
involving the sequentia l development of heteromorphic parenchymatous
gametangial and filamentous sporangia l (i .e. , conchocelis) phases appears
to be establi shed for certain Porphyra and Bangia. Clear documentation of
gamete fusion has, however, a lways been a difficult problem , largely because
of the low level of differentiation between gametangial and vegetative cell s.
The sexual life history outlined for Porphy ra and Bangia is unique to the
Bangiales and has been designated the Bangia-type by Gabrielson & Garbary
(1986).
Two other life-history types, both of which are non-sexual , also exist
among Porphyra and Bangia populations. The first is a life history where
the seq uence of morphological phases is identical to that just described for
sexually reproducing populations, with the exception that gamete fusion and
meiosis do not occur. Therefore, in these populations, a non-sexual sequence
ofheteromorphic, parenchymatous gametangia l and filamentous conchoceli s
phases exists. This has often been demonstrated for members of both genera
based on cytological and morphological data (e .g., Krishnamurthy, 1959,
1984; Richard on & Dixon , 1968; Sommerfeld & Nichols, 1970; Conway &
Cole, 1973; Conway, Mumford & Scagel, 1975; Coll & Oliviera Filho , 1977;
Mumford & Cole, 1977; Kapraun & Luster, 1980; Freshwater & Kapraun ,
1986; Kapraun & Freshwater, 1987; Kapraun & Lemus, 1987). Thus , an
alternative non-sexual heteromorphic life history exists for many populations
of Porphyra and Bangia, where the equencing of morphological phase can
apparently proceed without change in ploidy level due to apomictic
production of carpo pores (=ex-spore of Conway, 1964), and the occurrence
of apomeiotic conchosporangia . In these asexual populations displaying
distinct heteromorphic phases, the spermatia ( = /3-spores of Conway, 1964)
appea r to be non-functional (Hawkes, 1978). Because the life hi tories of
both exua l and asexual populations exhibit heteromorphic phase , a sexual
population of Bangia or Porphy ra can only be demonstrated by careful
karyological study or acquisition of evidence for gamete fu sion . The
occurrence on Bangia and Porphy ra tha lli of carpospores or spermatia i
not ufficient evidence for the e tablishment of sexuality. The econd non-
sexual life-history type found in certain specie of Porphy ra a nd Bang ia
involve the recycling of the parenchymatous gametangial phase by asexual
monospores or aplanospores (Richardson & Dixon , 1968; Kri shna murthy ,
1969; Richardson , 1970; Mumford , 1973 ; Conway el al., 1975). fn thi s
type of life history, only one morphological pha e exists and a filam entou s
conchocelis phase i ab ent.
For the monotypic Rhodoch aeta le , it has been esta bli hed (Mag ne,
l 960a ,b; Boillot, 1975) th a t, simila r to the case in Porphy rostromium a nd
Ery throtrichia, relea ed sperrn a ti a in Rhodochaete pan •u/a fu se with la rgely
undifferentia ted vegeta ti ve cells tha t fun ctio n as ca rpogo nia. In R . parvu/a,
carpo pores indi tingui ha ble fro m mo no po res, however, a ppea r to be
formed extern a l to the fertili sed ca rpogo nium . U nfo rtun a tely, co ncrete
e idence e tabli bing the ite o f meiosi in R . parvu/a has not yet bee n
obta ined , a lthough meiosis is believed to occur durin g spo re producti on by
80 STEVEN . MURRAY AND PETERS . DIXO

diploid, sporangial plants based on observations that some of these spores

develop into gametangial thalli (Magne, l 960a,b; Boillot, 1975). This type
of life history, termed the Rhodochaete-type by Gabrielson & Garbary ( 1986),
is unique to R . parvu/a.

EVOLUTION OF RED ALGAL LltE HISTORIES

During the past decade, new insights into the evolutionary relationships of
the taxa compri ing the · Rhodophyta and of the Rhodophyta to other
eukaryotic organisms have been obtained largely through studie performed
at the cellular and subcellular level. In addition to the active interest in
elucidating red algal phylogeny , researcher have also attempted to develop
models of life-hi tory evolution in the Rhodophyta , particularly in the
Aorideophycids where our understanding of life-history events is much more
fully developed . In this regard, two competing proposals for life-history
evolution in Aorideophycid red algae exist. The first, outlined by Feldmann
( 1952), hypothesise that the life history of the ancestral Aorideophycid red
alga consisted of three independent, free-living phases- the gametophyte,
tetrasporophyte, and carpo porophyte . According to Feldmann ( 1952), the
Po/y siphonia-type life history wa derived from this primitive condition by
reduction and para itism of the carposporangial phase. The viewpoint that
evolution in the red algae has favoured reduction and parasitism of the
carposporangial phase has been upported by Magne ( l 967c, 1972, 1982,
1987), Umezaki ( 1977, 1989), and Garbary ( 1978) among others . In fact,
Magne ( 1972) ha made the argument that evolution in the Rhodophyta has
operated in uch a way that any generation can potentially grow parasitically
on the preceding one . Magne ( 1987) use as an example of thi viewpoint
his interpretation that the erect, foliose phase of Pa/maria pa/mata , instead
of being the tetrasporophyte as interpreted by Van der Meer & Chen ( 1979)
and Van der Meer & Todd ( 1980) and others, should be referred to as an
independent carposporophyte corresponding to Feldmann 's ( 1952) ance tral
free-living carposporophyte. Magne ( 1987) con iders the tetra porophyte
phase of P . pa/mata to be reduced to a parasitic stalk cell and its
accompanying tetrasporangium . The life history of Audouine//a simplex (a
A . pectinatum) ha been described by Abdel-Rahman & Magne (1983) with
the Feldmann model in mind . They report that the zygote can either be
released f~om the carpogonium immediately following fertilisation
( = sporozygote) or retained to develop into a parasitic carposporophyte.
Hommer and & Fredericq ( 1990) also support the Feldmann ( 1952) model
by hypothesising that the ancestral carposporophyte must have been
essentially autotrophic and may have been a somatic pha e "related
fundamentally to an asexual fruiting structure bearing monosporangia" . The
latter statement is based on their observation that in many Acrochaetiales,
branches bearing reproductive bodies (i .e., monosporangia, permatangia,
carposporangia, or tetrasporangia) are similar in appearance, suggesting that
they are under the same or related genetic control. Interestingly, current
understanding of the development and ultrastructure of mono pore most
clo ely resemble that for carpospores indicating that these structures may
indeed be homologous . Detailed inve tigations of monosporogenesi
and monospore structure, particularly in Aoricleophycids, are, however,
-------------------------------- ....
RHODOPHYTA . III 81

desperately needed to understa nd fully their evolutionary origin.

Hommersa nd & Fredericq ( 1990) a lso support th eir view th at the a ncestra l
carposporophyte must have been a uto trophic with evolution proceeding
towards increasing dependency o n the gameto ph yte by no ting that mat ure
chloroplasts can be found in certain go nimobla st cell s o f the carposporo-
ph ytes of more primitive florideoph ycid genera such as Nema lion, but
only proplas tids can be found in comparable structures of more advanced
genera such as Scinaia and Bonnemaisonia . Advocates of Feldmann's ( 1952)
hypothesis (e.g., Umezaki, 1977 , 1989) also generall y a rgue for the
primiti veness of isomorphic, free-livin g phases a nd the Polysiphonia-t ype life
hi sto ry, a nd use it as a basis for derivi ng all other kinds of life hi sto ries
displayed by livin g florideophycid s (see Umezaki, 1977, 1989; Gabrielson &
G arbary, 1986). Umezaki ( 1977, 1989) ha s even ca tego ri sed Feldmann's
( 1952) hypo thetical a ncestral life hi sto ry, with three independent or free-li vi ng
generatio n , as one of hi s life- history types despite the fact that thi s life
hi story has never been reported for a ny red a lga, ex ta nt or exti nct.
A second model o f life- history evolution in floride ophycid red a lgae ha s
been proposed by Guiry ( 1987). This model underscores the evoluti o na ry
importance of zygote a mplificatio n a nd supports Sea rles' ( 1980) hypothe is
that the carposporo phyte evolved in situ as a mea ns of disseminating the
products of presumably rare fertili satio n events. As o utlined by H ommersa nd
& Fredericq ( 1990), the retenti o n a nd nou ri shment of the ca rposporophyte
by the gameto phyte i an essentia l feature of red a lga l evolutio n that has
com pensated for inefficient fertili sa tion resulting from the ab ence of motile
ga metes. In Feldmann's ( 1952) model, ga mete fu ion wou ld result in the
minimal di emination of diploid reproducti ve cell , perhaps o nl y the
zygo te it elf, from each fertili sa ti o n event. H ence, Feldmann 's (1952)
hypo thesi tha t the a ncestra l red a lga l life hi story co ntai ned a free-living
carpo porophyte phase is not consistent with Searles' ( 1980) argument fo r
inefficiency in fertilisation becau e a bottleneck in production of diploid
carposporophyte individuals would necessa ril y re ult. If fertilisation in
the a ncest ra l red a lga was indeed a rare occurrence, then survival of the
re ultant diploid ge netic complement wou ld be en hanced by retention of the
zygote o n the gametangial thallus and it am plification into a multiple
pore-producing body in co nt rast to it release into the ea. Guiry (1987)
hypothe i e that zygote amplification ha evolved in two ways in the
Rhodophyta, creating: ( 1) a triphasic life history through the development
of a mi to porangial generation directly from the zygo te, the pores of which
produce a meiosporangia l generation; and (2) a bipha ic life history through
the development of a meio porangial generation directly from the zygote,
the pores of which produce a gametangial generation . Searle ( 1980) sugge t
that the former mean of zygote amplification, which characterises exual
reproduction in mo t red algae, would be more ucce sful in an evolutionary
en ·e. Guiry ( 19 7) a rgue that this mechanism of zygote amplification may
have ari en independently on e eral occa ions in the red algae, only in ome
ca ·e from an ance tor with a Polysiphonia-type life hi tory, thereby negating
<he need to develop elaborate evolutionary linkage among all life-
hi tory t pe such a tho e figured by Umezaki ( 1977, 19 9). Guiry' ( 19 7)
model account for an independent evolutionary track for rhodophyte
\\ ith bipha ic life hi torie . uch a tho e found in exually reproducing
82 STEVEN . MURRAY AND PETERS . DIXON

bangiophycids, a view in line with statements by Hommersand & Fredericq

( 1990) who rega rd the fruiting structures of biphasic bangiophycid as being
" neither equivalent nor prototype of the ftorideophycid carposporophyte" .

ENVIRONMENTAL ONTROL OF RED ALGAL LIFE HISTORIES

It ha been appreciated since the advent and availability of controlled

laboratory culture condit!ons that for many red algal species the development
of reproductive structures occurs only under certain regimes . The goal of
mo t studies during the 1960s and 1970s was to establish the sequence of
morphological phase , particularly for species where one reproductive phase
was unknown . Inve tigators routinely grew their cultures under more than
one set of conditions , generally concentrating on temperature, photoperiod
and light inten ity, conditions readily manipulated within controlled
environmental chambers. In some ca es, researcher also cultured algae under
variable nutrient regime , subjected cultures to desiccating conditions and
even to mechanical abrasion in hopes of inducing reproduction in otherwise
vegetative thalli . During this era , culture experiments carefully designed to
test pecific hypotheses concerned with the environmental control of
reproduction were uncommon . Recently a truly experimental approach to
life history research has, however, become more evident and in the case of
red seaweed , considerable progress has been made for a few species in
under randing the role played by environmental conditions in controlling
reproductive cycle and field distributions .
The control of reproduction and, hence, life-history sequences by
environmental conditions has now been firmly e tabli hed for a number of
red algae, but mostly for specie with heterombrphic life histories including
several non-ceramialean ftorideophycids and for bangiophycids belonging
to the order Bangiale (see reviews by Liining, 1980, 198 la,b; Dring &
Liining, 1983; Dring, 1984, 1988; Maggs & Guiry, 1987; Liining & tom
Dieck , 1989; Santelice , 1990) . Laboratory experiments under controlled
conditions have revealed that factor such as temperature, photoperiod ,
irradiance quantity, a nd nutrient levels can exert control over the
development of reproductive structures, particularly in red algal populations
occurring at mid- and higher latitudes where natural environments are
characterised by prominent, abiotic seasonal ignal . Also, phenological
patterns observed in the field or the environmental requirements for
completion of the life history in the laboratory have been correlated with
field conditions , particularly temperature and photoperiod, to determine
possible causes of geographic distributions . uch tudies have generated a
considerable body of information on various North Atlantic ea weed (v .d .
Hoek , 1982a ,b; Liining, 1984, 1990; Yari h, Breeman & v.d. Hoek, 1984;
Breeman, 1988) concerning the temperature requirements and , for elected
specie , the photoperiodic requirements for completing life history events and
su taining natural populations.
Historica lly , light a nd particularly photoperiod ( = the daily sequence of
light and dark period ) has received the greatest attention of those abiotic
fact o r known to control red algal reproductive processes within temperature
a nd irradia nce limits supporting g rowth and urvival. In an earlier re iew
of red algal growth and reproduction in relation to photoperiod, Dixon &
----------------------------------~
RHODOPHYTA . Ill 83

Richardson (1970) noted that despite the extensive body of knowledge that
had been generated for flowering plants, little attention had been given to
studying photoperiodic responses in algae and other cryptogams. As,
however, noted by Dring ( 1984), a great increase in the number of algal
species reported to exhibit photoperiodic responses occurred during the late
1970s and early 1980s, a trend that continue today.
We now recognise (Dring, 1984, l 988) that photoperiodic responses of
macroalgae are diverse and, therefore, cannot be limited to only those that
fit the " cl assic" and simplistic criteria outlined earlier by Dixon & Richardson
( 1970): (I) induction of the effect even after transference to non-inducing
condition ; and (2) sensitivity to short breaks in either the light or dark
period s. In his thorough review of algal photoperiodism, Dring ( l 984)
de cribed re ponses in the algae and called for a broader definition (see
Hillman , l 979) of photoperiodism : "the control of some aspect of a life cycle
by the timing of light and darkness". Dring (1984) suggested that "i f a
difference is observed in the development of an algal species in long and hort
days under identical temperature and nutrient conditions, and the re ponse
can be shown to be caused by light period and not by light quantity, it can
be described as a photoperiodic response" . Using these extended criteria for
photoperiodism creates a n inherent negative bias with regard to identifying
long-da y responses (Dring, 1984) because to do so generally require that
the effect of photoperiod be eparated from the concomitant increa e in
total daily irradiance resulting from longer daylight periods . Thi contra ts
with the ca e for short day respon e where the induced developmental event
is unlikel y to be controlled by a reduction in the total irradiance received.
ft i with this broader definition of photoperiodism in mind that a list of
red a lgae where the available evidence indicates photoperiodic control of
life-histo ry or developmental respo nses ha been compiled (Table Ylf). Any
such li sti ng is likely to be incomplete becau e of differences in interpretation
and the variety of experimental conditions and protocols, many of which
are non-definitive for detecting genuine photoperiodic or other environ-
mental effect .
The marine red algae are well represented in any summary of algal
photoperiodic re ponse and, together with the brown eaweeds, contain the
vast majority of records for macroalgal taxa (Dring, 1988). In Table VII, a
total of 46 photoperiodic responses are listed for 42 red algal species. Of
the e, 43 re ponses have been reported a short-day, 2 a long-day, and I
a a dual daylength (i.e., a respon e requiring a hort-day treatment followed
by a long-day regime) . Of the 43 hort-day re ponses listed , the cla ical
night-break treatment was attempted in 27 ca es and found to be inhibitory
in 19 and to have no effect in 7; in one pecies, Audouinel/a purpurea (a
Rhodochorton purpureum), effect oft he night-break treatment were variable.
Mo t of the Ii ted photoperiodic re pon e occur in red algae exhibiting
life hi torie other than the Polysiphonia-ty pe (Type 2). The development or
relea e of reproducti e tructure i the mo t common type of photope-
riodic re pon e recorded for red algae (3 of 46 respon es Ii ted in Table Vlf).
In mo · t pecie of ftorideophycid , the reproducti e tructure -who e
de\'elopment i under photoperiodic control i the tetra porangium wherea
in the bangioph cid , where photoperiodic control of development ha been
demon trated onl) for certain pecie of Bangia and Porphyra, control
 TABLE VII
...
00

Studies where evidence is provided indicating photoperiodic control of life history and developmental responses' in red algae

Short or Night break

Type o f lo ng day Critical treatment
Species response (SD or LD) period At tern pted/ Resul ts Comments References
Vl
Acrosymphyton purpuriferum Tetraspore SD < 16hL Yes Increased Cortel-Breeman & ten -l
production no effect irradiance Hoopen, 1978: Breeman ['Tl

reduces & ten Hoopen , 1987 <

['Tl
response a t sho rter
photoperiod s
Asparagopsis armata Tetraspore SD < IOhL Yes High and low Oza , 1977, 1989;
productio n inhibito ry temperatures Liining, 1981 a
s:
c
and nutrient ;:r:i
;:r:i
concentration
inhibitory >
-<
A udouine/la asparagopsis Tetras pore SD < 12hL Yes Reduction at Abdel Rahman & Magne, 1981 ; >
as Acrochaetium asparagapsis production inhibitory higher temp- Abdel-Rahman, I 982a, b; z
erature; Abdel-Rahman, 1982 0
"O
involvement of ['Tl
circadian -l
['Tl
rhythm ;:r:i
Audouinella botryocarpa Tetraspore SD <: IOhL Yes High and low Guiry et al., I987a Vl
production ( <8.5 hL) inhibitory temperature
inhibitory 0
A udoui11ella caespitosa Tetra spore SD s; 10 hL Not Tetrasporogenesis Bidoux & Magne, 1989 ><
0
as Rhodotham11ie/la caespitosa production a ttempted not affected by z
temperature
under condtions
tested
Audouine/la codicola Tetras pore SD s; 10 hL Not Tetrasporogenesis Bidoux & Magne, 1989
as Rhodo1ham11iel/a codicola production a ttempted not affected
by temperature
under conditions
tested
Audouine/la purpurea Tetraspore SD :S;9.5 Yes Critical period West, 1969, 1972a;
as Rlwdochorton purpureum production to inhibitory and effects of Dring & West , 1983.
:S; 14.ShL or no effect night-break vary Breeman et al., 1984
with strain;
night-break
affected by
irradiance
quality; high
temperatures
inhibitory
Audouine/la simplex Tetraspore SD :S;IOhL Yes Reduction at West , 1968
as Acrochaetium pectinatum production no effect higher temp-
erature
Bangia fuscopurpurea Conchospore SD < 12.ShL Yes High temperature Richardson & Dixon, 1968;
;:o
formation inhibitory inhibitory; Richardson , 1970 ::r:
irradiance 0
quality affects 0
night break ..,
0
Batrachospermum moniliforme Development LO > 14hL Not Some erect ax is Huth, 1979 ::r:
of erect axes attempted development -<
-l
under higher ?>
irradiances at
< 14 hL but not
at IOhL ; higher
temperatures do
not cause erect
axes under 10 hL
Bonnemaisonia asparagoides Development SD :S;l2hL Yes Low temperature Rueness & Asen , 1982
of erect axes inhibitory inhibitory
Bonnemaisonia hamifera Tetraspore SD < 12hL Yes High and low Liining, 1980; Breeman
production inhibitory temperatures et al .. 1988;
and nutrient Breeman & Guiry, 1989
concentration
inhibitory; tides
afTect induction
..,,
00
 00
°'
TABL E VII -Continued

Short or Night break

T ype of long day Critical treatment
Species response (S D o r LD) period Attempted Results Commen ts References

Calosiphonia vermicularis
- _,
C/l
Tetraspo re SD <8hL Yes None Ma yho ub, 1973, 1975, 1976: rn
production inh1b1tory Mayho ub et al., 1976 <
rn
Chondrus nipponicus Gamete SD s;8hL Not Tetraspore Brod ie et al., 1991
formation attempted formation is
not under
photopenod1c ~
co ntrol ; only c
;o
two conditions ;o
)>
tested
Constantinea subulifera New blade SD < ll - 12hL Yes lrradia nce quality Powell , 1964, 1986 -<
)>
initiation inhibitory affects night break z
Constantinea simplex New blade SD no data ? No data Powell , 1986 0
initiation .,,
Constantinea rosa-marina New blade SD s;8 hL Not Only two light Lindstrom, 1980 _,
rn
initiation a ttempted treatments rn
;o
performed
Cordylecladia erecta Gamete SD s; 12 hL Yes T ota l daily Brodie & Guiry, 1988c
fo rmati on; no effect irradiance did 0
tetras pore SD s;8 hL Yes not affect ><
production no effect gametangial 0
response
z
Delesseria sanguinea G a mete SD <1 4hL Yes Temperature Kain (Jones), 1987
fo rma tion; inibitory ha s little o r
tetraspo re SD? <8 hL? Yes no effect o n
production inhibitory gametogenesis;
blade initiation
greater at lower
temperature
Dumo111ia conlorta Formation of SD s; 12- 13 Yes Critical period Rietema & Klein , 198 1;
erect axes to 16h L inhibitory varies by strain ; Rietem a , 1982; Rietema
nutrient & Breema n, 1982
concen tra ti on
and temperature
afTect ax is
formatio n
Farloivia conferta Tetraspore SD s;8 hL Not Only two DeCew & West, 198 l a
production a ttempted conditio ns tested
Far/owia mollis Tetraspo re SD s;8 hL No t Only two DeCew & West, 198 la
production a ttem pted conditions tested
Gigarlina acicu/aris Gametogenesis SD s; 12 hL Yes High and low Guiry l 984a; Guiry &
and inhibitory temperature C unningham, 1984 ;>:l
cystocarp inhibits gamete ::r:
forma ti on; formatio n; low 0
SD s;lOh L at Yes temperature 0
tetraspore 0
producti on 16°C inhibitory quantitatively -0
inhibits ::r:
tetrasporogenesi s -<
-l
)>
Gloiosiphoma ver1icillaris Tetraspore SD s;8h L Not Only two DeCew el al. , 1981
production a ttemp ted conditio ns tested
Halymenia /a1ifo!ta Tetraspore SD < 20h L Yes Tempera ture Maggs.& Guiry, 1982b
production inhibi tory a fTect s number of
tetrasporangia and
induction period
Mastocarpus ste//atus Tetraspo re SD s;8h L Yes High temperature Guiry & West, 1983
as Gigartina stellata production inhibitory inhibits tetra-
sporogenesis
Meredi1hia microphy lla Tetras pore SD s; 12 hL Yes Hi gh and low Guiry & Maggs, 1984
production inhibitory temperature
inhibitory;
high nutrient
concentra tion
inhibi tory
_,
00
 00
00

TABL E VII - Continued

Sho rt o r N ight brea k Cll

-l
T ype of long day Critical trea tment en
Species respo nse (SD o r LO) period Attempted Results Comments References <
en
Nemalwn helmm thoides Develo pmen t LO :2: 12 hL Yes High tempera ture C unningpa m & Guiry, 1989
of erect axes no effect inhibitory a nd
under sho rter 3::
inducti ve c
;>:l
photo peri ods, ;>:l
)>
both high a nd
low tem perature -<
)>
inhibito ry z
Plagiospora graci/is Tetraspore SD No data Yes No da ta Maggs, unpubl. , in 0
productio n inh ibit o ry Dring, 1984
Porphy ra abbo11ae Conchospo re SD $8 hL Not Limited informati on Waaland & Dick son , 1983 ""
en
-l
ma tura ti on a ttempted a nd experimenta l en
;>:l
a nd release co ndit ions
Cll
Porphyra carolinensis Co nchospo re SD $ 10hL N ot Hi gh tempera ture Freshwa ter & Kapraun , 1986
ma tura ti on a ttempted inhibito ry 0
a nd release x
Porphyra co fum bina Co nchospore SD $ l 2 hL Not High a nd low A vii a et al., 1986 0
fo rma tion a ttempted temperatures
inhibit ory under
longer but not
sho rter inductive
pho to peri ods;
lower temper-
ature required
for release
Porphy ra nueocystis Conchospore SLD s;l2hL& Not Two step induction Dickson & Waaland, 1985
maturation ;::: 16hL attempted treatment:
and release SD followed by
LO; high temper-
ature during
LO inhibitory
Porphy ra perforata Conchospore SD s;8hL Not Limited information Waaland & Dickson, 1983
maturation attempted and experimental
and release conditions
Porphy ra rosengurtii Conchosporc SD s; 12 hL Not No effects of Kapraun & Luster, 1980
formation attempted irradiance
and release or temperature
Porphy ra sptra!is Conchospore SD < 12hL Yes Temperature Kapraun & Lemus, 1987
var. amplifolia formation inhibitory can be inhibitory;
s; 11 hL no effect of i':l
and ::c
conchospore irradiance 0
release 0
Porphyra tenera Conchospore SD s; 10 hL Yes Temperature Dring, l 967a, b; 0
"O
formation inhibitory does not affect Rentschler, 1967 ::c
response but -<
-l
influences in- >
duction time
course; irradiance
quality affects
night break
Porphy ra torta Conchospore SD < 12hL Yes High temperature Waaland et al., 1987
maturation no effect reduces
and release magnitude and
can be inhibitory
Psilothal/ia dentata Tetraspore SD s; 8 hL Yes Irradiance level Fredriksen et al., 1990
production no effect does not affect
response

00

"'
 "'
0
TAB LE VII -Con tinued

Short or Night break

Type of long day Critical treatment
Species response (SD or LD) period Attempted/ Results Comments References

Rhododiscus pulcherrimus Tetraspore SD $8 hL Not Pretreatment affects Maggs et al., 1983 "'
-I
production attempted induction [Tl
Schmit=ia hiscock1a11a Tetraspore SD $8hL Not Results consistent Maggs & Guiry, 1985 <
[Tl
production; attempted at two temper-
formation of SD $8 hL Not atures and two z
erect axes a ttempted photoperiods
Thuretellopsis peggiana Tetraspo re SD $9 hL Not Only two Richardson & Dixon , 1970 s:
production attempted conditions tested
c
i"l
i"l
>
-<
>
z
0
-0
[Tl
-I
[Tl
i"l

"'0
><
0
z
-------------------------------- ....
RHODOPHYTA . III 91

appea rs to be exerted over conchospore maturation and relea se. The

remainder of photoperiodic re ponses reported for red algae involve either
the initiation of erect axes from prostrate filaments or pseudoparenchymatous
discs (5) or the seasona l initiation of new blades which has been reported
for three species of the perennial red alga Constantinea (3) .
fn compiling the information presented in Table VII, it became clear that
severe problems exist in discriminating 'genuine photoperiodic responses'.
It is now appreciated that red and other algae display a diversity of
photoperiodic mechanisms and, therefore, it is necessary to examine a
broader set of criteria for establishing a photoperiodically-controlled
re ponse. It i also clear that many culture studies focus only on describing
life-history events not on determining factors involved in controlling them
and, therefore, provide observations a nd data that implicate but do not
demonstrate experimentally photoperiodic or other environmental control
mechanisms. fn these studies, investigators generally fail to perform definitive
experiments providing adequate control of other confounding environmental
variables or to obtain appropriate quantitative measures of the induced
re ponses. For example, it is now widely known that temperature or nutrient
concentrations can modify or block the inductive effects of photoperiod ( ee
numerous examples listed in Table VII) , thus affecting interpretations of
culture experiments where each of these variables has not been atisfactorily
controlled. fn addition, photoperiodic responses are not always qualita tive
or 'a bsolute', (i.e., where th::: majority of individuals exhibit the response
following exposure to the appropriate inductive photoperiod but the response
is totally blocked under non-inductive photoperiods). Absolute responses
contrast with what Li.ining ( 1981 b) has referred to as " quantitative"
photoperiodic responses where such completely definitive results are not
realised because non-inductive photo-regimes do not totally block the
response . In many tudies where absolute photoperiodic responses have been
reported , only two or three photoperiod treatment have been employed.
Thi may ob cure the ability to detect quantitative responses that would
have been revealed with multiple photoperiod treatments and considerations
of other variables such a temperature or nutrient levels . Also, in cases where
quantitative rather than definitive or ab olute responses are encountered,
inve tigators are faced with interpreting whether or not a particular
photoperiod treatment produces a 'significant ' quantitative difference in a
developmental response such a tetrasporogenesis. In virtually all labo-
ratories where life history and developmental studies are undertake n,
inve tigators do not, however, have the equipment avai lable (i .e., large
numbers of environmental chambers or devices) to replicate independen tly
experimental treatments of temperature or photoperiod. Therefore, v.hen
multiple culture ves el are a igned to a photoperiod or temperature
treatment, pseudoreplication sensu Hurlbert ( 1984) occurs a nd inferential
tatistical tests of ignificance for treatment effect cannot legitim ately
be performed . Anot her interesting ob er ation i that the nature of the
data may al o have an effect on the interpretation of the re ults . For example,
different interpretations may be real ised if quantifica tion of a response en tai ls
determining the frequ ency of plants producing tetrasporangia compared with
count of the total number of tetra porangia formed.
92 STEVEN N. MURRAY AND PETERS. DIXON

Consequently, in laboratory culture studies, where algae are often

maintained in nutrient-enriched sea water under temperatures known from
field observations to support growth, the failure of reproductive structures
to develop may not be directly attributable to photoperiod but may be due
to other factors . Only a carefully designed experimental protocol can rule
out effects of nutrients, temperature or other variables on algal
photomorphogenesis. Also, in such cases where the developmental effi ct is
not 'absolute' (sensu Llining) with respect to photoperiod , proper
quantification , data reduction and analysis techniques are essential and
multiple (more than three or four) photoperiod treatments are probably
needed to provide proper evidence for a photoperiodic response .
Unfortunately, such crucial experiments are frequently not performed . A
review of the literature indicates that studies including multiple photoperiod
treatments and experimental examination of other environmental variables
(e.g ., temperature) , together with appropriate quantitative measurements of
the developmental response being studied, are indeed rare.

TAXONOMY AND SYSTEMATlCS

There have been many important findings reported during the past two
decades, but perh a ps the most significant change in the overall understanding
of red algae concerns the systematic treatment of the group as a whole.
Views on red algal systematics have changed during this period not only
because of new information and interpretations that have brought focus on
the efficacy and importance of the classical criteria hitherto given pre-
eminence, but also due to a willingness to increase the number of criteria
applied to systematic analysis. As a result, the field of red algal systematics
is in a dynamic period and it is highly probable that the changes which have
occurred during the past ten to fifteen years are likely to be minor compared
with those incipient. Contributing greatly to this current trend of accepting
instead of rejecting new systematic proposals is the fact that the field is no
longer dominated principally by one school of thought, that of Harald Kylin .
Kylin 's ideas monopolised red algal ystematics for the first half of the
twentieth century. Through the period of the previous two reviews in this
series (Dixon, I 963a, I 970a), most new ideas or criticisms of Kylinian
systematics were rejected or regarded as being insignificant. Attitudes have,
however, changed and a period now exists where new views on systematic
relationships are being accepted , and where much more phylogenetic diversity
among red algal taxa is a ppreciated . As a result, many changes in the higher
systematics of the Rhodophyta have occurred since the last review. Although
complete agreement as to the number or exact nature of red algal order
that should be recognised does not yet exist, a consensus has been reached
that the number should be greater than the I I (5 bangiophycid and 6
florideophycid) described by Kylin (1956) . For example, Woelkerling (1990)
has accepted I 7 (4 bangiophycid and I 3 florideophycid) orders ( ee Table T,
p. 2). In addition , to changes in ordinal level classification, most recent
worker no longer recognise the classical separation of the red algae into
two classes or subclasses, e.g., the classes Bangiophyceae and Florideophyceae.
This is not the pl ace to reproduce either the historical profile of the
--------------------------------....
RHODOPHY TA . Ill 93

development of red algal systematics which has in pa rt been summa rised by

Pa penfu (1955), K ylin ( 1956) a nd , more recentl y, by Garbary & Gabrielso n
( 1990), or the various previous criticisms of the Kylinian a pproach. This
review will concentrate o n the inform ation o btained during the pa t two
deca des that has contributed to the current trend of restructuring hi gher
level classifi ca tion of the Rhodoph yta a nd will point out a reas where future
re earch hold promi e for refi ning systematic ideas about this gro up of
organisms.

G ROSS VEGETATIVE MORPHOLOGY

Gross th a llus form ha s been the principal criterio n for taxonomic

di scrimination since the very first descriptions of red a lgae by the early Greek
philoso phers. Over the centuries, knowledge of red a lgal morphology has
improved, although for ma ny taxa there are till aspects of vegetative
structure in need of de cription . Tha lli of red a lgae, like those of a ll other
algal group , are subject to con iderable variatio n in appearance, often as
a consequence of expos ure to different environ menta l co nd itio ns. Previously,
each morphol ogica l va ri a nt within a population was assigned to a different
taxo n even after the Linnaean system of binomial nomenclat ure ca me into
use. Even a t the midpoint o f thi s century in the historically well-studied
British Isles, a lack of a ppreciation of morphological variatio n was
wide pread a nd resulted in the incon sistent application of taxonomic names,
particul a rl y between floras of different a reas where a lga l nomenclature a nd
pecies concepts were often delimited o n a loca l basis. Under tandably, many
morphologica l variants have sub eq uentl y been reduced to syno nym y wit h
greater availability of field collected ma te ri a l resulting in radical taxonomic
changes. One of the most extreme examples concern the va ri o us enti ties
now acce pted as belonging to the sin gle species Ceramium ciliatum which
150 yea rs ago were a ttributed to abo ut 25 different species and four genera
(Dixon , I 970b) .
Modes of spore germin a tion have historica ll y been acco rded so me
sy tematic significa nce. For exa mple, the mode of spore germination has
been deemed to be of system atic impo rtance withi n the Cora ll ina les where
generic di crimin a tion has been based o n differing patterns of spore
development (e.g., Chihara , 1973, 1974; Chamberlain, 1983). Th e efficacy of
thi s criterion must, however, be carefu ll y con idered. Although spore
germin a ti o n appears to be mo re fixed within the florideophycids than in the
ba ngio phycid , intra pecific va riatio n is known to occur (Guiry, I 990a), and
Wet (per . co mm . cited in Guiry, 1990a) has even observed that the age o f
spo res ca n affect their developmental patterns. Thu , until more exten ively
exa mined , the y tematic implications of pore germination pattern hould
be regarded as bein g of dubiou significance.
D es pite the previou ly di cu sed problem with describing erect axis
orga ni atio n in fl orideophycid a being uniaxial or multiaxial, the e concept
ha e been u ed exten i ely a featu re that characteri e orders, families and
e en genera of fl o rideophycid red algae ( Kylin, 1956; al o, ee Gabriel on &
Garbar , 19 6). Recent worker generally have continued thi tradition,
alth ough in everal ca e , the uppo ed uniaxial or multiaxial organi atio n
of the thallu ha been deemed le important than other character a nd
94 ST E VE N . M U RRAY AND P ET E RS . DIXON

ta xo no mic assign ments have been made tha t co ntradic t uni fo rmity in ax ial
co nstructi o n . For exa mple, bo th uniaxial a nd multiaxia l species a re currentl y
placed within the sa me o rder in both Ba trac hos perm ales a nd Gi ga rtina les .
A t th e fa mil y level, G a bri elso n & H o mmersa nd ( 1982a) reco mmended th e
tra nsfer o f the uni axia l genera Rhabdonia, A reschougia, a nd M elanema to
the Solieri aceae, genera lly tho ugh t to be a multiax ia l fa m ily, beca use of o th"er
feat ures held in comm o n by these genera . A simil a r decisio n was madi;: by
K raft & M in-Thein ( 1983) who pl aced a newl y described uniax ia l genu s
(Antrocen trum) in to the previo usly mul tiaxia l fa mil y Acro tylaceae based o n
sim ilarity in reproductive a nd o ther mo rph ologica l fea tures . T o emphasise
the co nfusio n that ex ists in determinin g the ro le ax ial constructio n sho uld
play in red a lga l systematics, G a bri elso n & G a rba ry ( 1986) have go ne so fa r
as to state th a t "we questio n the use o f ax ia lity as a fea ture delim itin g fa mil ies
in va rious o rd ers of red a lgae" .
C lea rl y, not o nl y is the genera ll y accepted conceptu al basis of referrin g
to ax ia lity suspect a nd in need o f cl arifica ti o n but, at thi s point, a ny system a tic
co ncl usio ns [or phylogenetic ana lyses such as those perfo rmed by G a brielso n
& H ommersa nd ( 1982a ,b) a nd Wilce & D avis ( 1984) ] based o n this feature
mu st be carefu ll y exa min ed before bei ng acce pted . Observatio ns of the events
involved in erect axis develo pment must be made fo r ma ny mo re species
unde r co ntrolled la boratory cond itio ns in o rde r to increase und ersta nding
of the genesis of axia lity a nd to assess the use of ax ia lity as a systematic
criterion for ftori deoph yci d red a lgae. If g ross tha llus mo rpho logy is to pl ay
a mea ningful ro le in systematic a nd taxo nomic studies of red algae, mo re
emphasis mu st be placed o n understa nding the mo rphogenetic events tha t
prod uce t ha llus fo rm . U nfort unately, the re has been o nl y a lim ited
commi tme nt to studyi ng red a lga l mo rphogenesis, a surpri sing situa ti o n as
mem bers o f t hi s gro up display ela bora te a nd intricate tha llus fo rms a nd
rep resent perhaps the a lga l gro up with the greatest potentia l fo r stud yi ng
developmen ta l events a nd t heir co nt ro l.

CELLULAR AND C HEMI C AL FEATURES

T he expa nsion in the num ber of cellul ar a nd subcellul a r investigatio ns of

red a lgae during the past twe nty yea rs has been pheno mena l. M ost detai ls
of red alga l cellu lar structure a nd orga ni satio n we re un known to K ylin ( 1956)
and occupied a tota l of less t ha n 3% of the pagin atio n in Dixo n' ( 1973)
review of red a lga l biology . C learly, there now ex ists a co nsidera ble body
of info rm ation , some recognised as bei ng of systematic significa nce, a nd
some which suggests systematic potentia l when more observatio ns o n more
taxa have been made.
A feat ure of cell ular biology that ho ld s great prom ise for so rtin g o ut
evo lutio na ry relations hi ps a nd , hence, red a lga l systematics in the fu tu re i
the mode of nuclea r divisio n . Scott and colleagues (see Scott & Broadwate r,
1990) have presented stro ng evidence suppo rting the systematic uti lity of
nuclear divisio n character , but have a lso stressed that t he grea test problem
in maki ng broader use of t hese criteria is that data a re avai lable o nl y for a
very sma ll number of taxa . Chl oropla ts are proba bly the most distinctive
feat ures of photosynthetic red a lgal cell s. As indicated previously, they ex hibit
much uniformity, bu t a lso certain differences, suggesti ng potentia l systematic
----------------------------------..
RHODOPHYTA. Ill 95

significance as de cribed by Hara & C hihara (1974). Scott ( 1984) has

a l o drawn attenti on to the systematic implications of associations between
organelle in red algal cells. In certain members of the bangiophycids a nd
a ll orders of the ' higher' florideophycid there appears to be a mito-
cho ndrion-dictyosome association. Intere tingly, among genera cu rrently
assigned to the Porphyridiales, mitochondria and dictyosomes ca n be found
both in as ociation and also devoid of any uch association suggesting that
this order i indeed polyphyletic. More work needs to be completed before
the systematic implications of mitochondrion-dictyosome associations can
be fully appreciated.
Knowledge of the variable structure and organisation of pit plugs
represents perhaps the greatest advance in understanding of red algal
sy tematics since Schmitz ( 1883) first used the auxi liary cell as the basis of
delineating red a lga l orders. Ba ed on a study of 63 species from 34 different
fami lies, Pue chel & Cole (1982) were able to demonstrate the existence of
consistent tructural features and proposed that pit plug structure be given
systematic importance at the ordina l level. In a later, expanded survey of
an additional 90 species, Pueschel (I 989) was able to confirm systematic
predictions made from this earlier study. In addition, in te rms of pit plug
tructure, Pueschel ( 1989) determined that the Acrochaetia les were a
heterogeneous group and that different phases in the life history of a species,
indeed, had the same pit plug structure.
A number of unusual chemica ls and chemical features occur in various
members of the Rh odophyta that are of potential systematic importance.
The biochemical features deemed to be potentially valuable in determining
systematic relationships among the red algae have recently been summarised
and briefly reviewed (Gabriel on & Garbary, 1986; Garbary & Gabriel on,
1990). Thee features included the biochemical composition of: phycobilin
and carotenoid pigments; cell wall and extracellu lar polysaccharides and
storage products; halogenated compounds; and selected protein . In addition ,
the presence of certain trace metals in high concentration , Dragendorff-
po itive compou nd s, and hemagglutinic and antimicrobial activity may be
distributed among taxa in a manner indicating y tematic importance. At
this time the applicatio n of chemotaxonomy to red algal systematic i ,
however, of on ly limi ted value and the ultimate ystematic importance of
biochemica l variabi lity remain to be realised. As emphasi ed by Garbary
& Gabrielson ( 1990), the contributions of chemotaxonomy to red a lgal
y tema tics have been hampered by a lack of adequate chemical data for all
but a few selected pecie , limited under tanding of both intra- and
inter-populational variation in the presence and form of potentia l
biochemical markers, a nd uncertainty as to the degree to which red algae
are able to obtain and concentrate biochemical compound from urrounding
sea water. a re ult , chemotaxonomic characteristic have not generally
been u ed as primary criteria but instead have been mostly used to support
y tematic conclu ions ba ed on other features .

REPRODUCTI E TRUCTURE A 0 LIFE HI TORY

The red algae are characteri ed by a diver ity of reproductive mode and
mean and reproducti e feature have been accorded major y tematic
96 STEVE N . MURRAY AND PETERS . DIXO

importance. Knowledge of red algal reproduction first appeared through the

classic works of Bornet & Thuret a little more than a century ago and has
been accumulating ever since mostly through examination of dried herbarium
specimens which fortunately still allow for the extraction of considerable
descriptive information .

Sporangia
As discussed previously, sporangia in the red algae are of many different
kinds and are generally named on the basis of the number of spores that
they contain . As indicated by Guiry (1990a), "sporangia and spores provide
many potentially useful characters for the ordinal classification of the
Rhodophyta, but they are often rejected in favor of the more alluring
female sexual characteristics" . For example, the three specific types of
tetrasporangium are not distributed randomly among florideophycid red
algal orders (see Guiry, I 990a). Cruciately arranged tetrasporangia occur in
all florideophycid orders except for the Batrachospermales where tetra-
sporangia are unknown. In contrast, tetrahedrally-arranged tetraspo-
rangia are limited to two orders, the Ceramiales (where they occur in all
families) and the Rhodymeniales. Polysporangia, the contents of which also
cleave simultaneously into polyspores, are similarly restricted to the last two
orders . Zonately-arranged tetrasporangia are found in three orders
(Gigartinales, Corallinales, Hildenbrandiales), although the production of
tetrasporangia within these structures differs with simultaneous cleavage of
the four spores occurring in the Corallinales and a transverse division
followed on both sides by two other parallel divisions occurring in members
of the Gigartinales and Hildenbrandiales. The basis for distinguishing
between these two modes of producing zonate tetrasporangia, together with
the development of irregularly cruciate and irregularly zonate tetrasporangia ,
requires, however, additional study. Within the bangiophycids, endosporangia
and conchosporangia are found but tetra- and polysporangia are not.

Spermatangia
Most studies have generally upheld the previous notion that features of the
structures producing male gametes are of little systematic importance.
Recently, however, Gabrielson & Garbary (1986) suggested that the plane
of division by which a spermatangium is formed (which is oblique in all red
algae except for the Gelidiales where it is transverse) may be of systematic
importance. Another aspect of the spermatium that may be of future
systematic significance relates to the biochemical mechani m by which
spermatia recognise and adhere to the receptive part of the female thallus.
Magruder (I 984a), for example, has shown that spermatia of Callitha111nio11
( Ag!aothamnion ) neglect um would bind only to female thallus parts of other
species within the genus, but would fail to bind with species within the same
family, or with specimens belonging to different genera or orders. The
mechanism by which recognition occur between compatible gamete may
possibly be mediated by the production of a binding substance by the
trichogyne of the carpogonium as has been demonstrated by Broadwater &
Scott ( 1982) for Polysiphonia. Resolution of this compatibility mechanism
______________.......................... ~

RHODOPHYTA. Ill 97

and ubsequent research on the biochemistry of the substance involved

would certainly provide useful sy tematic information.

Carposporophyte development
The development of the carposporophyte generation was first accorded major
sy tematic importance and proposed as the basis for systematic egregation
of red algal orders more than a century ago . An important part of
carposporophyte development in most ftorideophycids involves an auxiliary
cell which , following fertilisation, provides nutritional support and may
give rise to the gonimoblast filaments that form the body of the carpo-
sporophyte generation. Features of the auxiliary cell have long been regarded
(i .e., Schmitz. 1883) as a primary criterion for taxonomic discrimination
among ftorideophycids but interpretation of whether or not such a cell is
present and , if pre ent, its origin and role, have not always been consistent.
A significant problem in determining the sequence of events occurring during
post-fertilisation development in ftorideophycids, including the nature of the
auxiliary cell , is that these are relatively short-lived and it is difficult to
obtain material demonstrating complete developmental progressions . As a
consequence, for many red algae published descriptions of carposporophyte
development have been interpreted from ob ervations of a very limited
number of stages obtained from only a few specimen and may not be entirely
accurate; for cores of species post-fertilisation development has never been
described at all. Yet, the events involved in carposporophyte development
continue to play a major role in red algal systematics despite the
acknowledged deficiencies . Careful documentation of carposporophyte
development in many more taxa is required before post-fertilisation events
can rightfully be accorded the systematic significance that historically they
have held .
One source of difficulty in understanding post-fertilisation development
in red algae concerns the role played by auxiliary cells during carpo-
sporophyte formation. fn some cases these cell presumably have solely
a nutritive function whereas in other cases the auxiliary cell not only provides
nutritive support but also serves as the site of initiation of the gonimoblast
filaments . It has been traditional to refer to tho e auxiliary cell that have
the former nutritive role as "nutritive auxiliary cells" whereas tho e initiating
gonimoblast filaments have been referred to a "generative auxiliary cells".
Much uncertainty exists, however, with regard to the nutritional significance
of auxiliary cells and essentially nothing is known about the means by which
such cells become involved in generating gonimobla t filaments . In the most
recent analyse of carposporophytc development in red algae, Hommer and
& Fredericq ( 1990) have restricted the term auxiliary cell only to those cell
initiating gonimoblast filaments ; tho e cells with solely a nutritive function
have been referred to a " nutritive cells", " nutritive filament "or "nutritive
tissues".
In view of the difficulties in observing the tructures and sequence of
vents involved in post-fertilisation development , it is not surprising that
differences in interpretation exist. A classic example where such differences
have led to major systematic di agreement has occurred in determining the
ordinal status offtorideophycid treated herein a belonging to the Gelidiales.
98 STEVE N . MURRAY AND PETERS . DIXO

The original de cription of carpo porophyte development proposed for this

group by Kylin ( J 928), where the carposporophyte was said to arise following
fertilisation directly from the unchanged carpogonium, wa inaccurate.
Subsequently, Dixon (1959) howed that the carpo porophyte did not
develop from the original carpogonium and that the structure interpreted
by Kylin ( 1928) as the initial stage of the gonimoblast was in fact an ag~d
and unfertilised carpogonium of distorted shape; in tead , a large
multinucleate cell was formed which gave rise to the gonimoblast tissues.
Smith (1938) provided even more confusion by producing a copy of Kylin's
(1928) figure that had been modified to reveal instead of a carpogonium
with a lobe, a carpogonium from which a cell (suppo edly a gonimoblast
cell) had been cut off but remained connected by means of a pit connection!
According to Dixon (1959), the large multinucleate cell i uing gonimoblast
tissue was formed as a result of fu ion with various adjacent cells but that
the e fusions did not alway take place. Fan ( 1961) in hi account of
po t-fertilisation development in Gelidiales described , however, the
obligatory fusion of the carpogonium with the upporting cell upon which
it was borne. Thus, on the basis of the auxiliary cell concept prevailing at
the times of their inve tigation, Kylin, Dixon and Fan developed different
and contradictory interpretations of the presence of an auxiliary cell in
Ge/idium during post-fertilisation development. Kylin ( 1928) and Dixon
( 1959) both argued for the absence of an auxiliary cell. In Kylin 's case, this
was erroneously ba ed on the a sumption that no fu ions between cells
occurred, whereas Dixon argued that an auxiliary cell did not exi t because the
fusions were not obligatory. In contrast, Fan ( J 961) claimed that an auxiliary
cell was present due to hi view that fusions were obligatory. Interestingly,
Hommersand & Fredericq's ( 1988) recent interpretation of po t-fertilisation
development in Gelidiale re embles that of Dixon . They regard post-
fertilisation fusion in the Gelidiales a being merely nutritive in nature so
that on the basis of their definitions they al o conclude that an auxiliary
cell does not exist.

Life history
The type of life hi tory wa used as a principal criterion for y tematic
segregation by early inve tigator who were unaware of the diversity of
life-history pattern now known to exist in red algae . Early work by
Yamanouchi (1906a ,b) demon trated that isomorphic gametangial and
tetrasporangial thalli occurred in Po/ysiphoniajlexicaulis (a P . 1•iolacea) . In
addition , cytological evidence obtained by Yamanouchi (1906a,b) indicated
that the site of meiosis occurred in the tetrasporangium of Polysiphonia
leading to the assumption that thi structure played a imilar role in all
florideophycids . For numerous genera, particularly many currently assigned
to either the Nemaliale , Bonnemaisoniales or Gigartinale , male and
female gametophytic thalli were, however, commonly encountered in the
field but neither tetra porangia l thalli nor tetrasporangia were known .
On the ba is of questionable cytological evidence pro ided for Sci11aia
( vedeliu s, 1915), N e111alion (Kylin, 1916), and Asparagopsis and
Bonnemaisonia (Svedeliu , 1933) it was claimed that meio i occurred in the
zygote in such genera and that the carposporophyte generation was,
..................... ... ._ ._ ................
RH O D O PH YTA . Ill 99

therefo re, ha pl oid . Th is co nclusio n, reached witho ut kn owledge o f the

sequence of mo rp hologica l p hases comp rising the life hi to ri es o f these
genera , re ulted in the co ncept tha t in certa in ft o rid eo phycid a eco nd ty pe
of life hi story could be fo und a nd used fo r taxo nomic di scrimina ti o n. Thi s
type of li fe hi story, cha rac teri sed by the a bsence o f a tetraspora ngia l
genera tio n a nd the occurrence of meio is in the zygote, was o ne of fo ur
designated fo r ft o rideo ph ycid s by Drew ( l 955b) a nd , a t that time, was a
principa l criteri o n for assigning genera (incl uding those pl aced herei n in the
Bo nnema iso ni a les) to the N ema lia les . As d iscussed previo usly in thi s review
a nd by Di xo n ( 1970a, 1973), cytologica l tudies performed d uring the 1960s
by M ag ne have Jed to the rejectio n of this life-history ty pe in ft o rideop hycid s
a nd , hence, its use as a prim a ry criterio n to as ign genera to the ema lia les
or other red a lga l o rders.
Since the 1960s, info rmatio n o n li fe hi to ries has increased co nsiderably.
As po inted out by Garbary & Gabrielson ( 1990) , cul ture stud ies ena blin g
the linkage within the sa me li fe histo ry of heteromorph ic te tras pora ngia l
a nd ga meta ngial forms that had been assigned to separa te genera have had
significa nt ystematic re percuss io ns, particula rl y wit hin the Nema lia les,
Bo nnema iso nia les and Gigartina les . In these orders, fi lamento us a nd cru tose
taxa known o nl y to bear tetras pora ngia have in ma ny case bee n shown to
be syno nymous with la rge r, erect gameta ngial entities leadin g to shi fts largely
in infra -o rdi na l taxono mic assignments .
We now recogni se a di ve rsity of li fe- histo ry types in the red a lgae a nd
a ppreciate tha t thi s di ve rsi ty ca n occur even within trad itio na ll y recog ni sed
taxo nomic ra nk s. Different li fe- histo ry types have been repo rted not o nl y
wi thin member o f the sa me order, b ut a lso withi n members of a ingle
fa mily o r genu s a nd , as poin ted o ut by Maggs ( 1988) , even amo ng
po pula ti o ns o f the sa me species (see T a ble VI , p. 53). As a result o f the
fa ilure o f life- histo ry type to co rrespo nd com p letely wi th accep ted patte rn s
of taxo no mic d iscrimin atio n, it is p refera ble at this time to treat this feat ure
a onl y o ne of a number of character meriti ng co nsideratio n in systematic
wo rk . Such has been th e a pproach u ed in rece nt systematic a na lyses of the
relatio nship o f red alga l o rd ers usi ng clad istic methodo logies (Gabriel on ,
G a rba ry & Scagel, 1985; G ab rielso n & Ga rbary, 1986, 1987) .
Life-histo ry type ca n be un ifo rm o r ca n va ry within mem bers of a n order.
Fo r exa mple, as di scussed p rev io usly in eigh t (A hnfeltia le , Ba trac hosper-
ma les , Cera mia les , Cora ll ina les , G elid ia les , G racilaria les, Pa lmaria les,
Rh odymeni a les) o f the thirteen ft o rideo phycid o rders recogni sed in this
review, o nl y a sin gle ty pe o f sex ua l li fe histo ry has been recorded . The
rela ti vely unusua l life-hi sto ry types in members of the Pa lma ri a les (i.e., the
Pa lm ariaceae a nd Rhod oph y ema taceae) amo ng the ftorideo phycids and in
the Rhodochae ta le and Ba ngia les amo ng the ba ngiophycids ap pea r to be
o f systematic signi fica nce. In other red a lga l orders, the sys tematic
implica ti o ns o f li fe hi to ry re ma in , howeve r, unclear as the number of types
ca n be ext remely di verse as in the Acrochaetia les where six of the eight sexua l
and o ne of the no n-sex ua l li fe- hi story types ( ee T a ble V I, p. 53) ha ve
been repo rted . In add itio n, in the emalia les, Bo n nemaiso nia les, a nd
Gi garti na le bo th i omorphic Polysiphonia-type a nd heteromorphic Bonne-
maisonia hamifera-type li fe hi tories are known to occur a mong genera
trad it iona ll y assigned to the same famil y, makin g life-hi tory type an
100 STEVEN N . MURRAY AND PETERS . DlXO

uncertain criterion for taxonomic assignments. A similar situation also exists

within the same genus, as in Audouine//a, Gymnogongrus, and Phy //ophora ,
where different species exhibit different sexual life-history types .

BIOSYSTEMATIC STUDIES

The acquisition of cytological and genetic information represents the

penultimate phase in tl:ie development of taxonomic and systematic
knowledge. We discuss herein three major areas of red algal biology where
such information is of biosystematic importance: studies of chromosome
numbers and morphology, hybridisation studies, and investigations to
determine for certain characters the patterns of nuclear or non-nuclear
inheritance. Little progress has been made to date in employing molecular
genetics to answer systematic questions, although research such as that
performed on Graci/aria and related taxa (e.g., Goff & Coleman, 1988; Bird
& Rice, 1990; Rice & Bird, 1990; Bird, et al., 1990) indicates the advent of
a new era in red algal systematics.

Chromosome numbers and morphology

The first chromosome counts in a red alga were made at the turn of the
century by Yamanouchi (1906a,b). Subsequently, counting has been limited
by technical difficulties and progress has been slow in expanding the list of
species for which chromosome numbers are known . Even with the limited
data available on chromosome numbers, certain general conclusions of
ystematic importance can be made. First, at least for certain orders, a
pattern in the number of chromosomes appears to exist, although in virtually
all cases one or two 'o utlier' values have been published . In the Bangiales,
for example, chromosome numbers are characteristically quite low (2 to 7)
(see Cole, 1990). In certain cases, such as in the morphologically similar
Porphy ra perforata (n = 2) and P. abbottae (n = 3), chromosome numbers
can even be used as the principal criterion upon which to di tinguish taxa .
From an inspection of Cole ( 1990), it appears that members of the emaliales
have chromosome numbers that generally are low (n ~ 8- 10) whereas, in
contrast, members of the Ceramiale (n = > 20- 30) and many Gigartinales
(n = > 20) have relatively high chromosome numbers . Due largely to the
previou ly discussed contributions of Goff & Coleman based on the
application of DNA-specific ftuorochromes , polyploidy, aneuploidy, and
endopolyploidy have been documented for various red algae and caution
must be taken in establishing haploid and diploid chromosome numbers .
Chromosome morphology is frequently of biosystematic importance in
higher plants although, in the e organisms, the nuclei and chromosomes are
very much larger than is the ca e for the red algae. Red algal chromosomes
were known for many years to be of differing size and shapes, but much
more information is required before chromosome morphologies can be used
to any extent in systematic inve ligations.

Hybridisation studies
The capacity to grow red algae in unialgal or axenic culture ha enabled
experimental studie of hybridi sa tion . Sexual compatibility or incompatibility
!1111-.......................................... .

RHODOPHYTA . III IOI

has long been employed as a criterion for taxonomic discrimination in higher

plants, but has been used in the red algae in only a few cases. Most successful
studies have been performed on members of the Ceramiales and particularly
on pecies that are relatively easy to maintain in laboratory culture.
Hybridisation research to delineate species boundaries has also been
employed successfully on selected species in the Gigartinales, Gracilariales,
and Palmariales and promises to be u eful in species which can be grown
in laboratory culture. A major problem which must, however, always be
con idered in interpreting the systematic implications of hybridisation studies
has been pointed out by Rueness (1978a) : incompatibility may be real or
may be due to nothing more than the experimental conditions employed .

Nuclear and non-nuclear inheritance

Obviously knowledge of the basis for the inheritance of persistent and
identifiable characters would be of great value in systematic studie of red
algae. Unfortunately, knowledge of red algal genetics, as discu sed
previously, is still in its infancy and is limited to only a few select pecies
(see Van der Meer, 1990a). Although both nuclear and non-nuclear
inheritance pattern are known to occur in red algae, the list of character
and example is till too short to evaluate systematic application. A possible
exception, however, may be sex and phase determination which appear to
have different inheritance mechanisms in Graci/aria compared with Pa/maria ,
Deva/eraea, Chondrus, and Champia . At this time it is , however, premature
to accord much systematic importance to red algal genetics and inheritance
patterns because of the limited available data .

SY OPSIS OF RED ALGAL CLASSES AND ORDERS

Despite their diversity in morphology, reproductive mechanisms and life

historie , the red algae have consistently been regarded a being a
monophyletic group since the era of Fritsch ( 1945) who referred all member
of thi algal group to a ingle class, the Rhodophyceae. More recently, the
monophyletic nature of the red algae has been reflected in their placement
in a single division, the Rhodophyta . The major debate for many year ha
been whether or not the red algae hould be regarded as consisting of one
or two major clas e or subclasses. The latter opinion prevailed until recently,
with the two subunit being initially of ubclass statu (as the Bangioideae
and Florideae, de ignations subsequently corrected to Bangiophycidae and
Florideophycidae to comply with the International Code of Botanical
omenclature). Tncrea ing support for a more distant relation hip became
prevalent more recently and the two ubunit were accorded cla rank and
referred to a the Bangiophyceae and Florideophyceae, respectively . Recent
cladi tic analy e of red algal order (Gabriel on et al., 1985; Gabriel on &
Garbary, 19 6, 19 7) do not, however, upport thi epa ration becau e
neither the bangiophycids nor the ftorideophycids can be con trued a having
a unique et of hared. deri ed character or what are referred to in cladistic
terminolog ( ee Theriot, 19 9) a ynapomorphie . An equi voca l
relation hip between bangiophycid and ftorideoph ycid orders wa a rticulated
earlier b Lee ( 19 0) who al o did not divide the Rhodoph yta into two
102 STEVEN N . MURRAY A D PETERS . DIXO

distinct classes or subclasses . The most recent systematic treatment (Garbary

& Gabrielson, 1990) places all red algal orders into the single Class
Rhodophyceae and referv to bangiophycids and florideophycids only for
convenience. Thi position has been adopted herein .
As di cussed previously , cla sification of the red algae at the ordinal level
is in a tate of flux and as noted by Garbary & Gabrielson ( 1990) "current
revisions are potentially as far-reaching as those that occurred in the
Chlorophyta in the 1970s and early 1980s" . This revolution has been led by
the application of cladistic methodology which by definition expands the
base of characters deemed to be of systematic importance and seeks to
determine relationships among taxa based upon evolutionary transitions (see
Theriot, 1989). Cladistic analyses have provided support for new and
previou ly rejected proposals for ordinal segregation and have led to an
increased understanding of interordinal relationships and red algal
phylogeny. In the following ection, a brief synopsis of the red algal orders
accepted in this review (see Table 1, p. 2) is provided together with selected
comments regarding their status. The interested reader is referred to
Papenfuss ( 1955), Dixon ( 1973 , I 982a), and Garbary & Gabrielson ( 1990)
for a historical per pective, and to Gabrielson & Garbary ( 1986, 1987) and
Garbary & Gabrielson (1990) for additional di cussion of current views of
criteria u ed in ordinal discrimination .

Ordinal classificarion of bangiophycid red algae

Since Skuja 's ( 1939) attempt to segregate bangiophycid taxa into orders,
numerou s alternative schemes have been proposed . Yet, the systematics of
this red algal group remain unclear and in need of additional study.
Generally, the bangiophycid red algae are now regarded to consist of four
orders (Bangiales , Compsopogonales, Porphyridiales, and Rhodochaetales),
following in essence, the scheme proposed by Garbary, Hansen & Scagel
( l 980b) . Of the four orders, the Bangiales appear to be best defined whereas
the Porphyridiale clearly represents the most problematical group .
Historically, the ordinal name Bangiales wa first used by Schmitz (1892)
to include all bangiophycid red algae. Later, Kylin (1937) re-defined the
Bangiale to include only the non-unicellular bangiophycids and proposed
that the unicellular forms be placed within the Porphyridiales. Skuja ( 1939)
restricted the use of Bangiale to include those bangiophycids where the
thalli are multicellular, filamentous , tubular or plate-like and where growth
is accomplished by intercalary cell division . Skuja ( 1939) placed those
remaining bangiophycids which are strictly unicellular in the Porphyridiales,
those which occur in irregular colonial masses in the Goniotrichales, and
those with thalli that are initially filamentous but then become tubular in
the Comp opogonales . Skuja ( 1939) also strongly uggested consideration
of a higher taxonomic rank for the monotypic Rhodochaetaceae, where the
thallu i filamentous and growth occurs by apical cell di vi ion . This proposal
was apparently supported by Kylin (1956) who later accorded Rhodo-
chaetales ordinal tatu . Subsequently, Garbary et al. (1980b) assigned to
the order Erythropeltidale those familie (Erythropeltidaccae, Boldiaceae)
of the Bangiales in which the mono porangium is formed from an undiffer-
entiated vegetative cell through the formation of a curved wall , leaving the
_________............................ ~

RH O D O PHYTA . 111 103

Ba ngia les as a we ll -defi ned m o notypic o rde r co ntai ning o nl y membe rs o f

the fa mil y Ba ngiaceae. T he Compso pogo naceae, a fa mil y wh ose mem ber
also ex hibi t m onosporangi um producti o n by a curved wa ll , was incl uded o n
thi basis by G arba ry et al. ( 1980 b) in the order Ery thro peltida les. Tn
addi tio n, G a rba ry et al. ( 1980b) a rg ued fo r the inclusio n of the pseud o fil a-
men to us go ni otrichalea n fo rm s wi thin th e Po rph yridi a les, a viewpoint
genera ll y accepted by subseque nt wo rke rs. La te r, W ynn e ( 1986) ho wed tha t
beca use the Compso pogo naceae had been given o rdina l sta tu s by Skuj a
( 1939), t he na me Compsopogo na le hou ld be rega rd ed as havi ng p ri o rit y
over E rythropeltida les .
La rgely due to new cellula r in form a ti o n a nd rep roducti ve tudi es, it is
now kn ow th a t the evo luti o na ry di versity within the ba ngio phycid s is much
grea ter tha n previo usly believed . As a resu lt, it is likely that there wi ll be
new pro posa l , pro bably fo r m o re o rdina l taxa , as new in fo rm atio n become
ava ila ble. Thi s i particula rl y a ppa rent fo r t he Po rph yrid ia les, a seemingly
a rtifici al and polyphyle tic gro up tha t curre ntl y incl ud es taxa tha t have been
combined together la rgel y based o n their simple unicellula r to palmel-
loid mo rpho logie . Ga rba ry & G a brielson ( 1990) have referred to the
Po rph yridia les as " t he most pro blema tica l o rde r of red algae in te rm s of
classifica ti o n a nd potentia l rela ti o n hips". C la rificatio n of the systematic
rela tion hips a m o ng Po rph yridia le awai ts add iti o na l resea rch, pa rtic ula rl y
a t the cellul a r a nd su bcellul a r level where fea tures o f o rga nelle structure a nd
mode o f nuclea r d ivisio n ho ld stro ng promi se fo r esta blishin g evo lutiona ry
rela ti o n hips a m o ng the entities co mpri sing thi s e nigm a tic gro up . As the
simple unicellul a r fo rm s have been ass umed (see Di xo n, 1973) to incl ude
some o f the m ost primiti ve ex ta nt rh od o ph ytes, such resea rch sho uld also
shed light o n the evoluti o na ry o rigin s o f the red a lgae as a whole a nd lea d
to the develo pment o f hypo th eses co ncern ing rela ti o nships between the
Rh od o phyta a nd o ther e uk a ryo tes.

Ordinal classification of jlorideophy cid red algae

Durin g the pas t deca de, the number of acce pted o rd ers within the
ft o rideophycid s has expa nded fr o m the six pro posed by K ylin ( 1956) to the
thirteen o utlined by W oelkerlin g ( 1990) . M ost of the o rd ers li sted by
Woelkerling ( 1990), in additio n to the o rigina l six of K ylin ( 1956) , were
pro posed pri o r to the pas t decade o n the basis of mo rpho logica l, reprod uc-
ti ve o r life-histo ry tudies. It was , however, not until the ul trast ructu ra l work
o n pit plugs by Pue chel & Co le ( 1982) a nd empl oyment of the cladistic
methodo logy fo r ph ylogenetic a na lysis by Ga brielso n et al. ( 1985) and
G a bri elso n & G a rba ry ( 1986, 1987) t hat accepta nce of ord ina l expa nsio n in
the ft o rideoph ycid red a lgae beca me widespread . O ne major res ul t of th is
revi ion has been t he fragmenta ti on of the emalia les into severa l orders,
a system a tic cheme tha t a ppea rs to descri be better the p reviously recognised
(see Di xo n, 1973) heterogeneity a nd po lyp hyletic character of the Nema lia les
sensu K ylin ( 1956) . A seco nd majo r repercussio n co ncerns the elevation to
o rdina l stat us of elected fami lies trad itiona ll y assig ned to the C ryptone-
mi a les a nd Gi ga rtinales (incl ud ing the A h nfeltia les, Cora ll ina les, Gracila-
riale , a nd Hildenbra nd ia les), a nd the grouping together of the remaining
fa mil ie into a single, en larged Giga rtina les . Although the established
104 STEVEN N . MURRAY AND PETERS . DIXON

Kylinian system for systematic treatment of cryptonemialean and

gigartinalean families has undergone considerable modification in recent
years, a number of additional changes are probable as more data on the
cellular, morphological , and reproductive features of critical genera become
available, and a more accurate picture of their phylogenetic relationships to
one another and to other red algal orders becomes available . A third change
in the ordinal classification of ftorideophycids since Kylin ( 1956) involves
the creation of a new 9rder, the Palmariales , to receive certain genera
previously assigned to the Rhodymeniales .
Initially established to contain those red algae where an auxiliary cell was
lacking, the Nemaliales was one of Schmitz's (1889 , in Schmitz &
Hauptfteisch, 1897; Schmitz, 1892) four original ftorideophycid orders .
Kylin 's ( 1956) concept of the Nemaliales has been subject to considerable
revision in recent years and has now been fragmented into five orders:
Acrochaetiales, Batrachospermales, Bonnemaisoniales, Gelidiales, and
Nemaliales . As pointed out by Garbary & Gabrielson (1990) , with the
removal of the other four groups, the Nemaliales with its remaining families
becomes a much more homogeneous and possibly monophyletic order. Now
that the Acrochaetiales, Batrachospermales, Bonnemaisoniales, and
Gelidiales are, however, recognised as orders distinct from the Nemaliales,
the relationships between these and other red algal orders are unclear and
need to be re-assessed . The ongoing debate as to whether the ordinal name
should be spelled as Nemaliales or Nemalionales appears to have been settled
in favour of the former (see Nicolson & Norris, 1983).
The Acrochaetiales contains a number of diverse genera initially regarded
as belonging to the family Acrochaetiaceae of the order Nemaliales . Although
the elevation of this family to ordinal rank has not been accepted by all
authors , most recent systematic treatments agree with Garbary (1978) who
has asserted that ordinal status for Acrochaetiales is warranted because this
group of genera represents the most primitive of the extant ftorideophycids .
Later cladistic analyses (e .g., Gabrielson et al., 1985; Gabrielson & Garbary,
1986, 1987) of rhodophytan orders have 'without exception' supported this
position , which is also strengthened by Garbary & Gabrielson 's ( 1987)
conclusion that there are no clear sister groups to the Acrochaetiales among
living ftorideophycids . Generic limits and the criteria for assigning species
to defined genera within the Acrochaetiales remain unclear and widely
divergent 0pinions exist as to how the classification of this problematic group
should be structured . Garbary (I 979c), from his numerical analysis of
Acrochaetiaceae, was unable to obtain species clusters either comparable
with generic circumscriptions suggested in the past or that represented a
potential new set of better defined genera . At this time, it is only possible
to conclude that much additional research is needed before the systematic
relationships within the Acrochaetiales and between its members and other
red algal orders can be clarified .
The order Batrachospermales represents a group of genera originally
placed in the Nemaliales but elevated to ordinal statu by Pueschel & Cole
( 1982) based on pit plug structural characters. Also , life history events of
Batrachospermales appear to involve somatic meiosis and the absence of a
tetrasporangial generation (see Lemanea-type, Table V, p. 42). As currently
recogni sed, the order contains three families , Batrachospermaceae,
__________.............................
RHODOPHYTA. Ill 105

Lernaneaceae, and Thoreaceae, each of which is well circumscribed although

information on thoreacean life hi tories is still incomplete.
The Bonnernaisoniales wa proposed by Feldmann & Feldmann ( 1942)
for the family Bonnernaisoniaceae which had been placed in the Nernaliales .
Justification for Bonnernaisoniales wa initially based on the life history,
which was observed to consi t of heterornorphic tetrasporangial and
garnetangial phases. Ordinal statu wa opposed by Dixon ( 1961) who
recognised the heterogeneity oftaxa evident within the ernaliales but refused
to accept proposals for its division ba ed on the available information .
Feldmann & Feldmann 's ( 1942) argument for ordinal status was subsequently
supported by the morphological and reproductive studies of Chihara &
Yoshizaki ( 1972), aithough general acceptance for the Bonnernaisoniales did
not occur until Pueschel & Cole (1982) determined that pit plug structural
features of members of this group differed from those of other Nernaliales.
A key is ue to be resolved concerns the relationship between the
Bonnernaisoniaceae and the accariaceae, the two families currently a igned
to the order. As constituted, the Bonnernaisoniales appear polyphyletic
(Gabrielson & Garbary, 1987) and members of the two families are very
different from one another vegetatively (Garbary & Gabriel on , 1990).
Gabrielson & Garbary (1987) have suggested that the accariaceae may
have closer affinities with the Gigartinales than with the Bonnemaisoniaceae.
In contrast , as uggested by Chi hara & Yoshizaki ( 1972) based on
morphological and reproductive evidence and reinforced by the absence of
plug-cap layers (Pueschel & Cole, 1982), the Bonnernaisoniaceae may be
more closely aligned with the Cerarniales.
The removal of the Gelidiaceae from the Nernaliales was initially made
by Kylin (1923, 1928) who believed (albeit erroneously) that Gelidiaceae
resembled other Nernaliales because an auxiliary cell did not occur during
carposporophyte development , but differed becaLise a Polysiphonia-type life
history wa evident. This position was disputed by Dixon ( 1959; see also
Dixon, 1973) who , as discussed previously in this review, provided evidence
that, contrary to Kylin's view concerning post-fertilisation development in
Gelidium, the carposporophyte did not always develop directly from the
carpogoni urn . As summarised by Dixon ( 1973), retention of the Gelidiaceae
in the Nernaliales was necessary becau e Kylin's ernaliales was not a
homogeneous group and that little justification for holding the other families
together could be made if the Gelidiaceae were elevated to ordinal rank .
Dixon 's viewpoint appeared to gain increasing acceptance during the 1970s
and 1980s as several taxonomic treatments of the Rhodophyta included the
Gelidiaceae within the order Nernaliales . Fragmentation of Kylin's
Nemaliales has, however, now occurred and ordinal status for the
Gelidiaceae, an apparently rnonophyletic group based on the pattern of spore
germination , vegetative and reproductive morphology and pit plug structure
(Garbary & Gabrielson , 1990), is widely accepted.
The heterogeneity previou ly evident in the ernaliales, has al o long been
recogni ed among familie ultimately a signed by Kylin (1956) to the orders
Cryptonemiales and Gigartinale , and as discussed by Silva & Johansen
(1986) led to everal publi hed attempt by Kylin to sharpen the boundarie
between the e two groups . Recent studie have led to the recommendation
that everal families be assigned ordinal rank and removed from their
106 STEVEN . MURRAY A D PETERS . DIXO

traditional assignments in the Gigartinales (Ahnfeltiales, Gracilariales) and

Cryptonemiales ( orallinales , Hildenbrandiales). In addition, the principal
criterion employed by Kylin to dis tinguish these two ftorideophycid orders
is no longer accepted by many red algal systematists following the arguments
of Kraft & Robins (1985) . As a consequence, the families comprising Kylin 's
( 1956) Cryptonemiales (with the exception of the Hildenbrandiaceae and
Corallinaceae) are now included within the Gigartinales . Acceptance of these
revisions by no means resolve all the y tematic problems inherent in this
set of families , but instead ieaves the boundaries of an enlarged Gigartinales
in a state of flux . Even before the inclusion of the cryptonemialean families ,
the Gigartinales was viewed as being heterogeneous and paraphyletic
(Garbary & Gabrielson , 1990), and this situation still exi ts . Garbary &
Gabrielson ( 1990) describe thi controversial enlargement of the Gigartinales
as " a necessary interim step in sorting out relationships among the included
families ".
The Gigartinales and the Cryptonemiales were two of the four orders
established by Schmitz (1989, in Schmitz & Hauptfteisch , 1897; Schmitz,
1892) in the first ordinal classification of the red algae . As with the other
orders, the Cryptonemiales and Gigartinales were circum cribed by Schmitz
on the basis of the pattern of carposporophyte development and the po ition
of the auxiliary cell. More information was subsequently obtained for everal
genera of these orders leading Kylin in a series of papers (see Silva &
Johansen , 1986) to attempt to delimit more preci ely what had become an
uncertain boundary between the Cryptonemiales and Gigartinale . In his
final treatment of red algal systematics, Kylin ( 1956) distinguished the
Gigartinales on the basis that the auxiliary cell is homologou with a normal
vegetative cell and concluded that the Cryptonemiales pos e sedan auxiliary
cell that is not homologous with a vegetative cell , but instead is located in
a special 'accessory' filament that can be distinguished from those filaments
constituting the normal vegetative thallus . The difficulty in distinguishing
between the auxiliary cells of the Gigartinales and Cryptonemiales sensu
Kylin ha been discussed by several authors (see Fritsch, 1945; Dixon, 1973),
and this difficully together with problems in interpreting other selected
reproductive structures and events have been outlined by Silva & Johansen
( 1986) . Recently, Kraft & Robin ( 1985) argued that distinction between
these two orders ba ed on whether or not an 'accessory' auxiliary-cell filament
i present could not be justified , and recommended that a merger of
cryptonemialean and gigartinalea n families occur, excepting the Corallin-
aceae and Hildenbrandiaceae which should be regarded as meriting eparate
ordinal status .
The Corallinaceae, which includes the articulated and non-articulated
coralline algae, ha long been recognised as one of the mo L distinctive red
algal families . Ever since it initial a ignment to the Cryptonemi a les by
Schmitz (1889, in Schmitz & Hauptfteisch, 1897; Schmitz, 1892), the
taxonomic disposition of the Corallinaccae has been in quc Lion (see ilva &
Johan en , 1986). Following the lead of Pueschel & Cole ( 19 2) who
determined a distinctive pit plug structure, and at least three other previous
authors, Silva & Johansen ( 1986) argued for formal elevation of the extant
family Corallinaccac Lo ordinal rank and provided a Latin diagno i . The
segregation of the Corallinale from the enlarged Gigartinale of Kraft &
 RHODOPHYTA . Ill 107

R obins ( 1985), has been consistently supported by cladi stic a nal yses (see
Gabrielso n e l al., 1985; G abrielso n & G ar bary, 1986, 1987) a nd is acce pted
here.
The taxonomic disposition o f the Hildenb ra ndi aceae has lo ng been
problem atica l due to the complete a bsence of gameta ngia l structures. Placed
by K ylin ( 1956) within the Cryptonemiales based upo n a co nsideratio n of
vegeta ti ve characteri tics, the elevatio n of this fami ly to o rd inal status was
proposed by Pueschel & Cole ( 1982) based upon pit plug structure. Thi s
proposal was subsequentl y acce pted by Silva & Johansen ( 1986) a nd a lso
a ppea rs to be suppo rted by the cladistic analyses performed by Gabrielson
el al. ( 1985) a nd Gabrielson & Garbary ( 1986, 1987).
Recent proposa ls, acce pted herei n, have a lso been made to elevate to
ordina l tat us two groups of taxa traditionally assig ned to the Gigartinales
sensu K ylin , A hnfe/1ia a nd its relatives and the Gracilariaceae. The order
Ahnfeltiales was recently proposed by Maggs & Pueschel ( 1989) to receive
Ahnfe/1ia plicala and certai n related taxa previously assigned to the
Ph yll ophoraceae of the Gigartinales. M aggs & Pueschel ( 1989) were able to
demo n trate that reprod uctive development of the female gametophyte and
post-fertilisation events leadin g to carposporophyte formation were different
from o ther Ph yll ophoraceae a nd Gigartinales, and that these features (in
co njuncti on with a distinctive pi t plug structure) warranted ordinal
segregation. Although Garbary & Gabrielson ( 1990) upport Maggs &
Pueschel's ( 1989) proposal , they argue that more evidence is required before
the relationships between the Ahnfeltiales and other red a lga l orders can be
resolved . Progress has been made in understanding the infrageneric taxonomy
of Ahnfe/1ia (M aggs, Mc l achl an & Saunders, 1989), but other studies are
needed before the relationships between taxa traditionally assigned to this
gen us a nd to the ge nera Phyl/ophora and Gymnogongrus can be clarified .
The Gracilariaceae co nta ins a number of economica ll y important a lgal
species a nd , therefore, its members have received con iderable attention .
Recently, a st ud y by Fredericq & Hommersand ( 1989) of the reproductive
development o f Graci/aria verrucosa, the type species of the family
Gracilariaceae, revealed the ab ence of an auxiliary cell and connecting cells
or connecti ng filaments during post-fertilisation development. These
reproductive characteristics differ from the criteria required for inclusion of
the Gracilariaceae in either the Gigartinales sensu Kylin or the enlarged
Gigartinale specified by K raft & R obin (1985) . Hence, Fredericq &
Hommer and ( 1989) have propo ed elevation of the Gracilariaceae to ordinal
rank, a proposition a long with the previously di cussed segregation of the
Ahnfeltiales that creates of the condensed Gigartinales a more homogeneous
but till problematical assemblage .
The Rh odymeniale was al o one of the four original florideophycid orders
e, tablished by chmitz (1889, in Schmitz & Hauptflei ch , 1897; chmitz,
1 92). ub equently. Oltmanns ( 1904) egregated the Ceramiales from the
Rh odymenia le for tho e taxa where the auxiliary cell wa not formed until
after fertili ation . originally circumscribed by Oltma nn ( 1904), the
Ceramiale remain perhap the mo t clearly defined florideophycid order,
and i regarded b Garbary & Gabriel on ( 1990) a monophyletic. Members
of it four familie exhibit a high degree of uniformity in the devel o pment
of the egetati e thallu and the carpo poroph) te (Dixon , 1973). nlike the
108 STEVEN N . MURRAY AND PETERS . DIXON

Ceramiales, however, the Rhodymeniales remains a somewhat enigmatic

order. Kraft & Robins ( 1985) suggested that, as defined , the Rhodymeniales
could also be merged with the Gigartinales, an idea raised earlier by Drew
( 1954) . Garbary & Gabrielson ( 1990), believe the Rhodymeniales to be
monophyletic and continue to recognise the Rhodymeniales as an order
distinct from the Gigartinales, a viewpoint consistent with that adopted
herein.
One of the most important discoveries during the past decade was the
establishment by Van der Meer & Todd (1980) of the unique life history
characteristic of the PalmCJriales. This life history, which consists of
macroscopic tetrasporangial and male gametangial thalli of similar
appearance and a microscopic female , is unique and definitive for this group,
together with the presence during tetrasporangial formation of a superficial
cortical cell that divides unequally to produce an inner stalk cell and an outer
tetrasporangial initial. Guiry (1974, 1978) initially detected this different
pattern of tetrasporangial development among selected genera formerly
attributed to the Rhodymeniales, and subsequently assigned these to the
Palmariaceae and , ultimately, to the order Palmariales. General acceptance
of Guiry's proposal for ordinal status for Palmariales is now widespread
and supported not only by the fact that a unique life history is also
characteristic of these genera but also by Pueschel & Cole's (1982) observ-
ations that pit plug structure in Palmariales differs from that of other
Rhodymeniales.

ACKNOWLEDGEMENTS

We are especially indebted to the following for their assistance with

discussions and in providing publications: Ors J. F . Brauner, S. Broadwater,
D . Cheney, K . M . Cole, J. S. Craigie, S. Fredericq , D . J. Garbary, L. J. Goff,
M . D . Guiry, M . W. Hawkes, D . F. Kapraun, J. LaClaire II, F. Magne,
1. P. Van der Meer, J. McLachlan , L. Pellegrini , J. L. Scott, and J. A . West .

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