Phycologia (1992) Volume 31 (2), 127-137
Disposal of auxiliary cell haploid nuclei during
post-fertilization development in Guiryella repens
gen. et sp. nov. (Ceramiaceae, Rhodophyta)
I.M. HUISMAN' AND G.T.
FT2
KRA
'School of Biological and Environmental Sciences. Murdoch University.
Murdoch. Western Australia 6150. Australia
2School of Botany. University of Melbourne. Parkville.
Victoria 3052. Australia
. 1992. Disposal of auxiliary cell haploid nuclei during post-fertil­
KRAFT
G.T.
1.M. HUIS MAN AND
ization development in Guiryella repens gen. et sp. nov. (Ceramiaceae, Rhodophyta). Phycologia
31: 127-137.
The marine red alga (Rhodophyta) Guiryella repens gen. et sp. nov. (Ceramiaceae, Ceramiales) is
described from the subtidal of Western Australia. Plants are filamentous, with prostrate and upright
axes. Branching of the upright axes is typically spiral, with a rotation of approximately 60° between
successive branches. Mature axes appear alternate-distichous. Female fertile axes terminate inde­
terminate branches and are composed of three modified cells, with the subterminal cell bearing two
pericentral cells as well as the supporting cell of the four-celled carpogonial branch. The supporting
cell also bears a sterile cell. Following fertilization, two auxiliary cells are cut of,f one from the
supporting cell and one from a pericentral cell. Each of these auxiliary cells receives a diploid nucleus
from the carpogonium via small connecting cells. After acceptance of the diploid nucleus, each of
the auxiliary cells cuts off a 'disposal cell' containing one or two apparently haploid nuclei. These
cells rapidly degenerate, but their hyaline remains are obvious in all but the most mature carpos­
porophytes. The remainder of the auxiliary cell divides to form carposporangia, with only a small
sterile cell subtending the single gonimolobe. The sterile cells of the procarp (the sterile cell on the
supporting cell, the sterile pericentral cell and the apical cell) each divide once to produce two-celled
branches. Their development is usually arrested at this stage, but additional cells may be cut of.f
Spermatangia are produced in compact heads on lateral branch cells. Tetrasporangia, with tetra­
hedrally-arranged spores, are produced in similar positions to the spermatangia. Two-celled pro­
pagules, which presumably repeat the parent phase, are also produced on the tetrasporophyte. Guir­
yella is clearly related to the propagule-producing genera of the Ceramiaceae, but differs with regard
to details of its post-fertilization development. Most notable is the production of a 'disposal' cell
(although this feature may prove to be more widespread), but the genus is also unique in the arrested
development of the inner involucral branches and the production of two lobes of synchronously
maturing carpospores without an extensive fusion cell. The method of deleting haploid nuclei from
the auxiliary cell via a terminal 'disposal' cell, which then degenerates, has not been described
previously, but it is suspected to occur in several other genera. The process is analogous to the
division (as occurs in several tribes of the Ceramiaceae) of the auxiliary cell into an intercalary 'foot'
cell (containing haploid nuclei) and the gonimoblast initial. The 'foot' cell, however, is typically
intercalary, and does not subsequently degenerate.
INTRODUCTION
Post-fertilization development in many red algae
involves specialized processes that have long been
of interest to phycologists. One of the most sig­
nificant of these involves the diploidization of
the initially haploid auxiliary cell, as a result of
which the latter receives a diploid zygotic nucleus
by means of a connecting cell or filament that
arises directly or indirectly from the fertilized
carpogonium.This zygotic nucleus divides with-
in or immediately adjacent to the auxiliary cell
following its fusion with the connecting struc­
ture, giving rise to the diploid carposporophyte.
One aspect of this process that has continued to
attract the attention of phycologists concerns the
fate of the haploid nucleus (or nuclei) contained
within the auxiliary cell once the diploid zygotic
nucleus has been received: 'One of the most in­
triguing questions of carposporophyte develop­
ment is how the nuclei are sorted so that only
the diploid nuclei give rise to carposporophyte
127
128
Phyc% gia, Vol. 31 (2), 1992
cells' (Pueschel 1990, p. 31). Most work to date
indicates that the haploid nuclei degenerate or
remain dormant, although it has recently been
suggested that an 'electron dense cytoplasmic'
barrier can be formed within the cell that essen­
tially prevents the haploid element from partic­
ipating in any carposporophyte formation (Ku­
grens & Arif 1981). Previous studies, however,
have mostly dealt with genera in which a fusion
cell containing large numbers of haploid nuclei
subtends the carposporophyte.In such cases, the
haploid nuclei may remain more or less in place
without disrupting the ontogeny of the diploid
carposporophyte. Although the occurrence of a
fusion cell that incorporates the auxiliary cell is
common in red algae, it is by no means universal,
and no such cells occur in many genera. The
obvious questions concerning the fate of the hap­
loid nuclei within diploidized auxiliary cells in
such genera cannot be answered a priori.
It is known that in some Ceramiales the hap­
loid nuclei are physically compartmentalized and
excluded from the carposporophyte as a conse­
quence of the cutting off of the gonimoblast ini­
tial.In a number of genera, however, this process
does not occur, and the fate of the haploid nuclei
is unknown. During the course of our investi­
gations of deep-water marine algae of central
Western Australia, an undescribed epiphyte al­
lied to the propagule-forming genera of the fam­
ily Ceramiaceae proved particularly amenable to
observation with regard to the fate of its auxiliary
cell haploid nuclei following diploidization. It
was noted that, after receipt of the diploid nu­
cleus, the first division of the auxiliary cell gave
rise to a cell that contained haploid nuclei and
which thereafter rapidly degenerated. The re­
mainder of the auxiliary cell subsequently acted
as a gonimolobe initial, dividing entirely to pro­
duce groups of carposporangia, with only a small
subtending sterile cell remaining attached to the
supporting cell and eventually fusing with it.
Similar degenerating cells appear to have been
observed previously (Gordon 1972; Stegenga
1986), but their cytological details were not in­
vestigated and consequently their possible func­
tion was either misinterpreted or not described.
Thus this exact process has not been described
and explicitly interpreted as a means of excluding
haploid nuclei in red algae before, and it is con­
sidered to be an important cytological feature,
with possible phylogenetic implications, in the
following description of Guiryella repens gen. et
sp. nov.
MATERIALS AND METHODS
All specimens examined were preserved in ap­
proximately 5% Formalin/seawater.Whole plants
were mounted on glass slides in a solution of 1%
aniline blue, 3% IN HCl, 50% Karo® corn syrup
and 46% water. Material for nuclear studies was
stained using Wittmann's aceto-iron-haemotox­
ylin-chloral hydrate technique (Wittmann 1965,
according to procedures of Hommersand &
Fredericq 1988). Herbarium designations are
MELU (School of Botany, University of Mel­
bourne, Victoria) and Murdoch (School of Bio­
logical and Environmental Sciences, Murdoch
University, Western Australia). Cell dimensions
are expressed as diameter by length.
OBSERVATIONS
Guiryella gen. et sp. nov.
Figs. 1-20
DIAGNOSIS: Guiryel/a repens Huisman et Kraft, ge­
nus speciesque novum inter Ceramiaceas: axibus
erectis atque prostratis, ecorticatis; his rhizoideis
unicellularibus; illis spiratim ramosis, ramis succes­
sivis tertia parte fere rotatis; axibus fertilibus femi­
neis ramos indeterminatos terminantibus, cellula
subterminali tres cellulas pericentrales ferente una
earum pro cellulam sustinentem agente et cellulam
sterilem ferente; post fecundationem duabus cellulis
auxiliaribis ab cellula sustinenti atque alia pericen­
trali invicem scissis, utraque illarum nucleum diplo­
ideum ex carpogonio per cellulas conectentes parvas
carpente, deinde cellulam propriam in quam nucleos
illarum haploideos deponuntur et quae ipsa denique
degenerat abscindente, deinde reliquiis auxiliario­
rum gonimoblastos omnino carposporangialem for­
matum dividentibus; cellula cellulae sustinentis ste­
rili et pericentralio sterili et cellula axis fertilis apicali
quaque semel dividente: capitulis spermatangialibus
compactis in cellulis lateraliorum: tetrasporangiis
tetraedricis itidem dispositis: propagulis bicellular­
ibus ramos tetrasporophyti indeterminatos termi­
nantibus.
'The creeping Guiryella, ' a new genus and spe­
cies of the Ceramiaceae; with erect and also pros­
trate ecorticate axes, the latter with unicellular
rhizoids, the former spirally branched, with suc­
cessive branches rotated by approximately 60°;
female fertile axes terminate indeterminate
branches, the subterminal cell bearing three peri­
central cells with one of them acting as the sup­
porting cell and bearing a sterile cell; two aux­
iliary cells arise after fertilization from the
Huisman and Kraft: Guiryella repens gen. et sp. nov.
supporting cell and another pericentral cell, each
receiving a diploid nucleus from the carpogo­
nium by small connecting cells, then cutting off
a special cell into which their haploid nuclei are
deposited and which itself eventually degener­
ates, the remainder of the auxiliary cells then
dividing to form gonimoblasts composed entire­
ly of carposporangia; the sterile cell on the sup­
porting cell, the sterile pericentral cell and the
apical cell of the fertile axis each divide once;
compact spermatangial heads arise on lateral
branch cells; tetrahedral tetrasporangia in similar
positions; two-celled propagules arise terminally
on indeterminate branches of the tetrasporo­
phyte.
TYPE SPECIES: Guiryella repens sp. nov.
OLOGY: The new genus is named in hon­
E TYM
our of Dr Michael D. Guiry, who has made a
substantial contribution to our understanding of
the red algae.
HOLOTYPE: (Fig. I). 'Mostyn's Lump,' a sub­
merged reef lying approximately 3 nautical miles
north of 'The Nook,' Pelsaert Group, Houtman
Abrolhos, Western Australia, growing on Dic­
tyota naevosa (Suhr) J. Agardh at 20 m (Kraft &
Huisman, 14.x.1990; MELU, A38705). Several
isotype specimens were also collected (MELU,
A38706-38728), with MELU, A38728 epiphytic
on Stypopodium australasicum (Zanardini) Al­
lender et Kraft.
DISTRIBUTION: Known from the type locality
and from Roe Reef, Rottnest Island, Western
Australia, growing on a variety of brown algae
at 12 m (Huisman, 15.iv.1989; MurdochJH 670).
VEGETATIVE STRUCTURE: Plants are filamen­
tous, uncorticated, with prostrate and erect axes
(Fig. 1). Prostrate axes are anchored by unicel­
lular rhizoids (Fig. 2) that arise from the proxi­
mal ends of axial cells. These rhizoids are at­
tached to the substratum by means of digitate
pads. Cell dimensions of the prostrate axes are
50-180 x 180-600 �m. Upright axes grow to a
height of approximately 5 mm and are spirally
branched with a rotation of approximately 60°
between successive branches. Mature axes ap­
pear alternate-distichous. Near the apex the lat­
eral branches overtop the main axis (Fig. 8). In­
determinate lateral branches arise every 2-5
(usually 4) axial cells and their growth and
branching are identical to those of the main axes.
Cell dimensions of the indeterminate lateral
branches and main axes are 45-75 x 150-360
�m, becoming shorter towards the apices. De­
terminate lateral branches are subdichotomously
129
branched, up to 5 or 6 cells long, with cell di­
mensions of 10-30 x 135-200 �m. All mature
vegetative cells are multinucleate.
PROPAGULES: Ovoid, two-celled propagules
(100-140 x 180-225 �m) terminate indetermi­
nate branches (Figs 3, 4). In all, four modified
cells are present as the propagules are borne on
two-celled stalks.The lateral branch on the sub­
tending cell becomes an indeterminate branch
and can produce further propagules. Propagules
contain many starch grains, are multinucleate,
and have only been observed on tetrasporo­
phytes (Fig. 4) or otherwise sterile plants.
GIA: Spherical to ovoid tetraspo­
TETRASPO RAN
rangia, with tetrahedrally arranged spores, arise
singly at the distal ends of lateral branch cells
(Figs 5, 9). They are often surrounded by up to
three layers of mucilage (Figs 5, 9), and their
dimensions (including the mucilage) are 60-75
x 75-80 �m.
SPERMATANGIA: Spermatangia are formed in
ovoid heads (45-50 x 60-75 �m) in positions
similar to those of the tetrasporangia (Fig. 6).
Oblique divisions of the spermatangial head ini­
tial give rise to 2-3 axial cells that bear tiers of
pericentral cells or spermatangial mother cells
directly (Fig. 10). Spermatangia are 3-4 �m in
diameter, and each contains a single, distally
placed nucleus.
CARPO
NIAL
GO
B
NCH
RA
AND CARPOSPOROPHYTE:
Procarps are borne on the subapical cell of in­
determinate axes (Fig. 11). Three modified axial
cells are present-the apical cell, the subapical
cell which bears three pericentral cells (one of
which acts as the supporting cell of the carpo­
gonial branch and also bears a sterile cell), and
the hypogenous cell, which elongates but does
not produce a lateral branch. The carpogonial
branch is borne laterally on the supporting cell
and is four-celled, with an elongate trichogyne.
After fertilization both the supporting cell and
the pericentral cell adjacent to the carpogonial
branch cut off triangular auxiliary cells (Fig. 12;
one auxiliary cell is obscured). The carpogonial
branch cells begin to fuse, and two connecting
cells (each containing a presumably diploid nu­
cleus) are cut off laterally from the carpogonium
and fuse with each of the auxiliary cells (Figs 12,
18). At this stage the cells of the carpogonial
branch begin to degenerate, but their nuclei re­
main clearly visible when stained (Fig. 18). It
appears that additional connecting cells may be
cut off from the carpogonium (Fig. 19), as con-
130
Phyc% gia, Vol. 31 (2), 1992
1
3
50 lJm
Figs 1-7. Guiryel/a repens gen. et sp. nov. (all type collection; MELU, A3870S-38728).
Fig. 1. Holotype (MELU, A3870S), epiphytic on a fragment of Dictyota naevosa from the Houtman Abrolhos,
Western Australia.
Huisman and Kraft: Guiryella repens gen. et sp. nov.
131
8
30 ... m
8,10
Figs 8-10. Guiryel/a repens
gen. et sp. nov. (all type collection; MELU, A38705-38728). sp. m = spermatangial
mother cell; sp
spermatangia.
Fig. 8. Apex of an indeterminate branch.
=
Fig. 9. Tetrasporangia with tetrahedrally arranged spores.
Fig. 10. Optical section through a spermatangial head.
necting cells containing nuclei are visible during
the subsequent development of the carpospo­
rophyte, eventually degenerating along with the
carpogonial branch (Fig. 20). Following receipt
of the diploid nucleus, the haploid nuclei (usually
two) in each of the auxiliary cells can be seen
near the end of the cell (Fig. 18), and are cut off
in a special disposal cell (Fig. 13, in which one
auxiliary cell is obscured; Figs 16, 19). During
the earlier formation of the auxiliary cell its hap­
loid nuclei do not stain darkly, but they can be
seen during diploidization, and are particularly
clear in the disposal cell. It is therefore unknown
whether the two nuclei are present during the
formation of the auxiliary cell, or whether one
nucleus divides at some later stage. The remain­
ing portion of the auxiliary cell acts as a goni­
molobe initial and divides completely, with only
a small subtending cell remaining sterile. The
latter eventually fuses with the supporting cell,
but an extensive fusion cell is not formed. Ap­
proximately 20 uninucleate carposporangia are
produced per gonimolobe (Figs 14, 17, 20), and
the disposal cells degenerate (Figs 17, 20).While
the carposporophyte is maturing, the sterile cells
associated with the procarp (the apical cell, the
sterile pericentral cell and the sterile cell on the
supporting cell) all divide once to produce two­
celled branches (Fig. 15). Occasionally they di­
vide further, but this is rare, and the majority of
mature carposporophytes display three two-celled
branches. All of the carposporangia mature si­
multaneously, resulting in two lobes of equal­
sized sporangia (Fig. 7). Carposporangia are ovoid
to irregular in shape and measure 35-50 x 5065 �m. Mature carposporophytes are 200-300
�m in diameter. No involucral branches are
formed.
f-
Fig. 2. Unicellular, digitate holdfasts.
Fig. 3. Two-celled propagules terminating indeterminate axes.
Fig. 4. Propagule and tetrasporangia borne on the same plant.
Fig. 5. Tetrasporangia, with tetrahedrally arranged spores, borne at the distal ends of lateral branch cells. Note
that there are several layers of mucilage surrounding each sporangium.
Fig. 6. Spermatangial heads borne on lateral branch cells.
Fig. 7.
Mature carposporophyte with two lobes of equally mature carposporangia.
132
Phyc% gia, Vol. 31 (2), 1992
30 IJrn
11-14
60tJrn
15
ca
st. p.gr
15
14
su.st.gr
Figs 11-15. Guiryel/a repens gen. et sp. nov. (all type collection; MELU, A38705-38728): a = apical cell; a. gr =
apical cell group; aux = auxiliary cell; ca = carposporangium; c.b = carpogonial branch; c.b.r = carpogonial branch
remnants; con = connecting cell; d.c = disposal cell; f.p = fertile pericentral cell; g = gonimoblast; hy = hypogenous
cell; sa = subapical cell; st. p = sterile pericentral cell; st. p. gr = sterile pericentral cell group; su = supporting
cell; suo st = sterile cell on the supporting cell; suo st. gr = sterile cell on the supporting cell group; tr = trichogyne.
Fig. 11. Mature procarp. The fertile pericentral cell is obscured.
Fig. 12. Production of one of the auxiliary cells from the supporting cell and its subsequent fusion with the
connecting cell. The second auxiliary cell on the fertile pericentral cell is obscured.
Fig. 13. The auxiliary cell produced by the fertile pericentral cell after receiving the diploid nucleus. The disposal
cell has been cut off. The auxiliary cell on the supporting cell is obscured.
Fig. 14. Side-view (relative to Figs 11-13) showing the two auxiliary cells acting as gonimolobe initials and
dividing entirely. Two disposal cells can be seen.
Fig. 15. Mature carposporophyte. The sterile cells of the procarp have all divided once and the disposal cells
have degenerated.
Huisman and Kraft: Guiryella repens gen. et sp. nov.
133
16
20 �m
20 �m
Figs 16, 17. Guiryella repens gen. et sp. nov. (all type collection; MELU, A3870S-38728). Material stained to
show nuclei.
Fig. 16. Production of the disposal cell by the auxiliary cell after receiving the zygote nucleus. The latter is
visible in the auxiliary cell (arrow), and the two haploid auxiliary cell nuclei (arrowheads) can be seen in the
disposal cell. See Fig. 19 for details.
Fig. 17. Young gonimoblast formed from the division of the auxiliary cell. The disposal cell (arrow) is degen­
erating. See Fig. 20 for details.
DISCUSSION
At present, six genera of the Ceramiaceae are
known to produce propagules as a means of veg­
etative propagation, these structures differing
from 'monospores' in that they are released with
their wall layers intact, as opposed to being ex­
truded from a sporangial wall that remains at­
tached to the parent plant (Huisman & Kraft
1982; Guiry 1990, p. 357). Monosporus (Solier
in Castagne 1845), Tanakaella (Hono 1977), Ma­
zoyerella (Gordon-Mills & Womersley 1974) and
Desikacharyella (Subramanian 1984) all vege­
tatively resemble Guiryella in that they are ra­
dially and alternately branched, but all produce
propagules that are single-celled, rather than be­
ing two-celled as in Guiryella. Sexual reproduc­
tion is only known for the last three genera, and
differs from that in Guiryella in that a single
auxiliary cell is produced and well-developed,
branched, post-fertilization involucral branches
issue from the sterile cells of the procarp. In Guir­
yella, two auxiliary cells are formed and the post­
fertilization involucral branches are each re­
duced to two cells.
The propagules of Deucalion (Huisman & Kraft
1982) are three-celled, its branching is alternate­
distichous, and the fronds lack a creeping basal
component.As originally described (Huisman &
Kraft 1982) and is still the case, gametophytes
are unknown in the wild but can be obtained
under highly specific culture conditions. At the
time of publication, cystocarps had not been ob­
served in Deucalion, but the presumably post­
fertilization procarp was surrounded by an in­
volucre of well-developed filaments derived from
the hypogenous and subhypogenous cells. Deu­
calion has since been cultured through its entire
life history (Huisman, unpublished data), and it
has been confirmed that the origin of the invo­
lucral filaments around the mature carposporo­
phyte is that indicated by Huisman & Kraft
(1982).
The genus closest to Guiryella with regard
to critical taxonomic features is Anisoschizus
(Huisman & Kraft 1982), which displays similar
branching and habit, as well as having two-celled
propagules. Gametophyte and carposporophyte
stages were unknown at the times of its original
description, but have now been studied in detail
134
Phyc% gia, Vol. 31 (2), 1992
30.,.m
18-20
Figs 18-20. Guiryella repens gen. et sp. nov. (all type collection; MELU, A38705-38728). Material stained to
show nuclei. d.n
diploid nucleus; h.n
haploid nucleus. Other abbreviations as in legend to Figs 11-15.
Fig. 18. The auxiliary cell receiving a diploid nucleus from the connecting cell. Two auxiliary cell nuclei can
be seen near the opposite end of the cell.
=
=
Fig. 19. The two auxiliary cells cutting off disposal cells containing haploid nuclei.
Fig. 20. The auxiliary cells dividing to form the young gonimoblast. The disposal cells with haploid nuclei have
started to degenerate, as has the carpogonial branch.
from recent southern and western Australian col­
lections.I Anisoschizus produces two auxiliary
cells, but unlike Guiryella it develops lengthy
inner involucral branches from the sterile cells
of the procarp, and produces several gonimo­
lobes in sequence, rather than two lobes that ma­
ture simultaneously.
Tribal placement of the propagule-producing
genera has been uncertain, and various authors
have distributed and redistributed individual taxa
among the Griffithsieae, Compsothamnieae,
Sphondylothamnieae or Spermothamnieae. For
example, Mazoyerella was originally placed in
the Compsothamnieae by Gordon-Mills &
Womersley (1974), but was subsequently trans­
ferred to the Spermothamnieae by Moe & Silva
(1979). Like Guiryella, the propagule-bearing
genera do not sit comfortably in any of these
tribes. Vegetatively most of them appear to be
closest to the Spermothamnieae, being hetero­
trichous and alternately, radially branched.
Reproductively, however, they recall the Sphon­
dylothamnieae, particularly in the post-fertiliza­
tion division of the sterile cells of the procarp
I Penguin Is., Western Australia. 5-6 m on Sporoch­
nus comosus C. Agardh (Kraft & Borowitzka,
l 3.xii.1984. MELU, A36578, 36593, 36594, 36612).
Warmambool, Victoria. Drift on Sporochnus radi­
ciformis (Turner) C. Agardh (G. T. Kraft, Il.ii.1984.
MELU, A38684-38703).
into involucres that envelop the growing car­
posporophyte. On the basis of their studies of
Deucalion, Huisman & Kraft (1982) suggested
that the production of propagules was a feature
likely to have arisen independently in several
ceramiaceous tribes. However, more recent in­
vestigations of cystocarpic Anisoschizus (Gor­
don-Mills & Huisman, unpublished observa­
tions) and our interpretation of the description
of Desikacharyella by Subramanian (1984),
strongly suggest that the propagule-producing
genera form a natural assemblage and should all
be placed in a single new tribe (Gordon-Mills &
Huisman, unpublished observations).
None of the propagule-producing or closely
related genera have yet been explicitly described
as forming cells the function of which is to rid
the diploidized auxiliary cell of extraneous hap­
loid nuclei. Several descriptions of other entities,
however, have alluded to similar structures with­
out speculating on their likely role. Gordon (1972)
described 'non-functional gonimoblast cells' that
were cut off from the auxiliary cell in Lejolisia
aegagropila (1. Agardh) 1. Agardh (Gordon 1972,
p. 141, fig. 46c). These cells arose laterally from
opposite marginal lobes on the narrow remnants
of the auxiliary cell subtending the gonimoblast
initial, and appeared to degenerate without par­
ticipating in gonimoblast formation (Gordon
1972, p. 141). Similar, although apparently per-
Huisman and Kraft: Guiryella repens gen. et sp. nov.
sistent, cells were also described for Shepleya
elixithamnia Gordon-Mills et R.E.Norris (Gor­
don-Mills & Norris 1986, figs 13, 14).
Much closer in position and origin to the dis­
posal cells of Guiryella are what Stegenga (1986)
designated 'rest cells' in Pleonosporiumfilicinum
(Harvey ex J. Agardh) De Toni (Stegenga 1986,
pI.33.4), P. paternoster Stegenga (1986, pI. 36.4),
Lomathamnion capense Stegenga (Stegenga 1986,
pI. 43.5, 43.7, 43.8) and TifJaniella cymodoceae
(B0rgesen) Gordon (Stegenga 1986, pI. 46.3). In
each of these instances, a single cell (included
nuclei are not indicated) is cut off basipetally
from a primarily longitudinally aligned auxiliary
cell, and it soon disintegrates. All of the entities
mentioned by Gordon (1972), Gordon-Mills &
Norris (1986), and Stegenga (1986) appear on
reproductive grounds to be closely related to
Guiryella, although none produce propagules of
any form. It will be necessary to determine the
ploidy state of the nuclei segregated by such cells
in the above species before their homologies with
Guiryella disposal cells can be persuasively es­
tablished.
One process that performs a similar function
to that of the disposal cell occurs in members of
the ceramiaceous tribes Crouanieae, Warrenieae,
Dohrnielleae, Antithamnieae, Delesseriopsi­
dieae, Heterothamnieae, Ceramieae, Spyridieae
and Callithamnieae, where the auxiliary cell 'di­
vides into two parts.... the proximal foot cell
and the distal gonimoblast initial' (Itono 1977,
p. 302). The gonimoblast initial then produces
several gonimolobe initials. The proximal foot
cell contains the haploid nucleus/nuclei [e.g. as
described for Seirospora orienta lis Kraft (Kraft
1988) and further observations on material from
Western Australia2], which subsequently remain
dormant or degenerate, and the foot cell may fuse
with the supporting cell [e.g.as occurs in species
of Balliella (see Huisman & Kraft 1984)]. Hom­
mersand (1963, p. 193) had earlier focused at­
tention on this nuclear-segregating device in
members of a number of 'primitive' tribes of the
Ceramiaceae, including Ptilocladia Sonder (as
Gulsoniopsis Hommersand), Spyridia Harvey and
Ceramium Roth. This mechanism does not ap­
pear to be strictly homologous to disposal cells.
2 'Mostyn's Lump,' a submerged reef lying approx­
imately 3 nautical miles north of ' The Nook,' Pelsaert
Group, Houtman Abrolhos Islands, Western Australia.
20-24 m on Erythroclonium muelleri Sonder (Kraft &
Huisman, l 4.x.1990. MELU, A38729-38734).
135
The foot cell is always intercalary, and is the
remnant of the auxiliary cell following the pro­
duction of the gonimoblast initial. It does not
degenerate, but fuses with the supporting cell and
often (as in Carpoblepharis and Reinboldiella)
with the gonimoblast initial as an element of the
fusion cell (Hommersand 1963, pp. 201, 212).
In contrast, the disposal cell is terminal and de­
generates, with the remnants of the auxiliary cell
(in Guiryella at least) acting as the gonimolobe
initial.
As mentioned previously, the initial transverse
division of the auxiliary cell into an intercalary
foot cell and terminal gonimoblast initial occurs
in a number of ceramiaceous tribes. However,
in several of the remaining tribes (including the
Compsothamnieae, Sphondylothamnieae, Grif­
fithsieae and Spermothamnieae) the 'auxiliary cell
does not divide ... into two parts. Instead, the
auxiliary cell functions as the gonimoblast initial'
(Itono 1977, p. 302). Itono (1977) considered this
feature to be of great importance, and used it as
one of the defining characters in his description
of the subfamily Compsothamnioides. This group
of tribes is also united by the production of sub­
apical procarps, a feature considered by most
authors to indicate one of the major develop­
mental lines in the Ceramiaceae (Kylin 1930;
Itono 1977, p. 307; Moe & Silva 1979). Although
the presence of a true auxiliary cell in the Grif­
fithsieae is debatable [it appears in many cases
that the role of auxiliary cell is taken by the sup­
porting cell itself (Baldock 1976; Kim & Lee 1986,
pp.90, 93), a feature also clearly exhibited in the
Radiathamnieae (Gordon-Mills & Kraft 1981)],
and in several other entities an apparently true
gonimoblast initial is produced, it appears that
in the large majority of genera Itono's description
of the events is applicable. We therefore have a
group of clearly related tribes in which there is
apparently no division of the auxiliary cell into
a foot cell and gonimoblast initial, the latter role
being taken directly by the auxiliary cell. Guir­
yella and all of the taxa suspected of producing
disposal cells (including, as well as those men­
tioned previously, Spermothamnion repens
(Dillwyn) Rosenvinge and Medeiothamnion
lyallii (Harvey) Gordon; Hommersand, personal
communication) are included in this group of
tribes. It is possible that the disposal cell evolved
as an alternative to the foot cell for the isolation
of the haploid nuclei. In most evolutionary
schemes, gonimoblasts composed entirely of car­
posporangia are considered to be primitive, with
136
Phyc% gia, Vol. 31 (2), 1992
the presence of sterile tissue in the gonimoblast
regarded as advanced (e.g. Hommersand 1963,
p. 316; Itono 1977, p. 303). The development of
the gonimoblast in Guiryella would thus be prim­
itive, as the remains of each auxiliary cell act as
a gonimolobe initial and divide entirely, forming
a single lobe of carposporangia with only a small
subtending sterile cell that eventually fuses with
the supporting cell. It is likely that the disposal
cell has arisen in response to this condition. The
production of a cell that immediately degener­
ates is energetically inefficient, however, and may
have been secondarily lost in more advanced
genera where sterile tissue forms part of the gon­
imoblast and is available for the isolation of the
haploid nuclei. Nevertheless, it would appear that
the cell may also have persisted in some cases,
as it is likely that they occur in Spermothamnion,
a genus with extensive sterile tissue in the gon­
imoblast.
It appears that the Ceramiaceae have evolved
various methods for compartmentalizing and
isolating haploid nuclei during carposporophyte
development that is mediated and directed by
the diploid nuclei. One of these (the division of
the auxiliary cell into a foot cell and gonimoblast
initial) is easily observed and occurs uniformly
in the majority of tribes. In the remaining tribes
the immediate post-fertilization events are dif­
ficult to observe, and often do not persist beyond
the early stages of carposporangial development.
These tribes would appear to have evolved sev­
eral methods of dealing with the 'problem' of
haploid nuclei disposal but, at present, only the
production of a specialized 'disposal' cell as de­
scribed for Guiryella has been conclusively shown
to fulfil this function. Given that such cells are
relatively minute, transitory, and easily over­
looked or confused with gonimoblast initials, it
may well be that their occurrence is more wide­
spread than was previously thought. A closer ex­
amination of genera that are possibly related to
Guiryella may show this process to be wide­
spread, and provide some indication of its phy­
logenetic significance in the Ceramiaceae.
ACKNOWLEDGEMENTS
We would like to thank Peter Robins (University
of Melboume) for preparing the Latin translation
and Dr Michael Borowitzka (Murdoch Univer­
sity) for his continuing support and enthusiasm.
Dr Alan Millar (National Herbarium of New
South Wales) kindly allowed us to use 'Guir­
yella,' which he had previously employed as a
manuscript name. Financial support was pro­
vided by A.R.C. grant no. AO 8700739.
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Accepted 4 July 1991