THE MALE OlGANS OF THE FLORIDBiE
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177
.
M GRVBR.M.Sc.
Thc Male Organs of the FlorideE . By VIOLET
(Couimunicated Ly Dr E . M~1i1o-uDELF.P.L.S.)
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(With 36 Text-figures.)
[Read 4th Jleceniber. 1924.1
.
INI)I<S
X . Histnricnl Accoimt
.
......................................
It Terminology . . . . . . ...................................
I I I . Material +lid Metho!la ....................................
IV . Detailed Investigation of the Antharidial Structarecl in the
following Species :(1) C%onrlr.w crispus Slack11...........................
(2) Loi~zentrr~ict
o v n C Eldl .............................
(3) Clltriiapirc pnr~oukc(J Ag.) Ilnrv ......................
(4) Nituphylliw~€12lici! GET. . . . . . . . . . . .
Page
177
1r)0
183
184
187
.
191
( 5 ) Ilitophyllum h?~?rfltU??Z
Grev.......................
(6) Lnicrencirr pinnnt@Ea Lnni .........................
(7) Laumrcia obtzcsa (IIuds.) Lam .....................
( 8 ) ~.’o/ysip~~onicc
fast@ata Grev.......................
(‘3) I’uI~/siphoninviolnceii Grev ..........................
(10) Gt-rJWhsia corrcllinn (Lightf.) -4g...................
(11) Halurus equiset$&c, s Iciitz .........................
(1 2) CallitJcnntnion hi-acAialus~Bonnem...................
(13) Cernmiul,8 +Uh1*U?IL Ag.............................
(14) Dumosifiicfil~~til’ii~i.~
Grev ...........................
(15) Ao.ceZklr.infccYtillintra h i 1
198
201
YOti
%8
311
716
2%
2%
328
233
236
.........................
V . The Position of the .
I
ntheridial Orgnns . . . . . . . .,...........
VI . The Position and Structure of the Antheridid Nother-cells ....
VlI . The l)eveloprnent of the Autheridia and Spern~atia ..........
v11T. ‘L‘he Cytology of Spermwti:rl Development................... ,
IY. The Ilomologies of the Antheridia ..........................
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240
241
242
246
247
X Tile Clasviticlttion of the F1oride:e on the Busis of Spmitttial
,,
lypes ................................................
Suinninry ..............................................
liefbrences ..............................................
248
251
262
I. HiIistorical Account .
AX..CIIOIXH nearly 150 years have passed sincc the first record of
spermatin
the red
occurred in print. our knowledge of these niinute bo&es
wlrich play 90 iinportant a part in the reproductive processes of the lihodophycex is surprisiiigly inadcquato and limited Records of the observ:rtion
of a~itlicritliai i i niorc tlian 120 European species of the Floridm are to
jn
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VOL X L P n
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MISS VIOLET
M. GRUBB ON ‘PEE
be found scattered in algal literntiire, but of these the vast majority are
simply notes to the effect that male plants have been seen and recognized.
A certain number give a short description detailing the position of the
antheridia, and some inclcde a dight account of their structure, but owing
t o the n:rture oE the material, modern cytological methods of investigation have only been brought to bear on n. few forms. Where, however, such
methods have benn tried the results have well repaid the labour, nothing
being more striking than the remarkable uniformity shown by the antheridia in their development. At the same time their structure has thrown
interesting light on the question of systematic relationships, since these
have PO far been tnainly determined on the characters of the cystocarpic
and tetrasporic plants.
The first mention in literature of the antheridia of the red alate occurs in
a letter from John Ellis, Esq., F.R.S., to Dr. Linnzeus, F.R.S., of Upsala,
written in 1767. The main subject of the letter purports to show the
animal nature of the genus of zoophytes called Corallina, but it includes an
account of “ soinc remarkable discoveries in the year I754 on the coast of
Sussex ” ; these were the supposedly male and feniale fructiticatioiie of
Co?$eferw polytiiorplia Linn. and Conferva plumosa Ellis (now known
as Polysiphonia fustigiata Grev. and Heterosiplionia coccinea Falkcnb.
respectively), the male showing “ its amentaceous flowers or catkins, with its
riiinute male seed in spikes.” On the ground of the presence oE these
fructifications, Ellis recoinmended that Coqferca should bc included in
Linna.~ls’sclass of Dicecia. Ten years later Lightfoot (1777) repeated this
observation on Conferva polymorplu, sgiiin insisting from analogy with
Angiosperms that the “ small conic catkins ” were inale in character, though
knowing nothing of their true function. In the next thirty years these
observations were extended to other species of Yolysiphonia by Lloth (1797),
Lyiigbye (1819), and Bonneinaison (lt122,1828), who added nothing new as
regards the function of these bodies ; indeed, the first two authors rather
obscured the issues by suggesting that these “catkins” were really of
animal origin ; and although this was not accepted by Agardh (1828) in
his notes on the five species of Hutchirisia Ag. (Polysiphonia Grev.), in
which he had observed antlieridia, yet he acknowledges that their functiori
is unknown. Two years later Greville (1630) was much puzzled by the
discovery of yellow bodies on the upper branches of Rhodomela pinustroitles
Ag. ( 6 resembling what are o d e d anthers in the Jungernianni~,)’but caine
to tile conclusion that these were “certainly extraiieous and probably of
aniiiial nature.” A t the same tiine he saw capsules or cavities terminating
the branches in Laurencia pinnat$ila IJainour. filled with extraordinary
bodies ’’ ; these were also seen by Mrs. Griffiths in some Cornish speciniens,
but no explanation of them was found. Kiitzing (1843) noted the btructures
in IVvujigelia, species of Polysiphoniu, and in Odorithuliu dentata Lyngb.
‘‘
179
MALE ORGANS OF THE FLORIDEX.
under the name of’ ‘’ sperinatodia,” and added two ohservations of importance, oiie being t,h:tt, wherever these occrirrcfl, no other fruit-body was
foand on the siiine individual, and the other that the gonidia composing the
“sperniatodien ” were colourloss :tiid hoii~og~meons.Naegeli (1847) revived
the question :IS to what was the function o€ these bo(lies, coinparing them
with the :tntheritli:t of niosses :ind liverworts, but unfortunately suggesting by
this cornparison that the corpuscles liberated were motile, as i n the Hryophytn, a i d indeed sttitirig thxt a spiral ciliriiri coultf be see11 inside the
colourloss cell. This idea wits taken up enthusiiist i d l y by Derbes and
Solier, mlio worked it out in ni:iny of the 27 species in which they oliservetl
antlieridia !l850, ’ 5 6 ) ; in most cases more detailed descriptions than had
previously been undortalren were given, accoinpanietl by figures, but a t the
same time tliesc nccounts were coloured hy t,he idon that the Floridean
“ sperinatozoitls ” pos
:t fine motile teruiinal :ippcntiage.
Siaiultaneously
with tliese papers, others, wliich were models tiotli for their nccurticy and
the powers of acute observation to wliich they gave evidencc, were hi?ing
published by Gustnv T h r e t on thc autheridia of the ( Iryptogams and more
especially of tlie Floritlerc (1S5l. ’.Xi, ’78). Altogether this investigaior
listed 68 species in whicll Lc had observed t.he prcsrncc of anthcridia, and
these, added to the 1 7 others known pre!rioui4y, makes a total of 85
European species to date. In addition he gave descriptions of n good
many of these species, and, a s n result of his esteiisive observations, he came
to the coiiclnsion that tlie hyaliue corpusclt:..; wliicli are expelled in[o the
water show no signs of movement, nor can a.iip time of a filamentous
appendiige be distinguished ; this statcineiit, a s to Blie lack of iiiotility i i i the
spemxitia of tlie Floriclez his never since I~eonw G x d y tlispntetl. Tliiiret,
W:IS led early to speculate as to the function of tlictse organs, whicl~appearetl
te be so widespreiid, :ind on the grounds of their position (see p. 240) and
frequent occurreiice he suggested tlint they were “ orgaiies de fcrtilisntion.”
This kiold suggestion, wliich i r t tlie tinio did not seein to he justified, was
fully borne out by the retnarlrnble xiiiiounceiiieiit inRtle in cottipany with,
Bornet hef‘orr the hcnddniie des Sciences on Sept. l O t l i , 1866, o€ the fusion
of these “ corpnsclcs ” of bhr Floridea? with the t.ip of‘ tlie ’‘ :Ippareil trichophorique.” The good work done hy ‘Cliuret wiis carried on hy his disciple,
Guigiiard (1889), who pul)iieheci a niore detailed account, of soine of ttic
species already described and added several others. Sclirnitz, too, in his
account of the fertilization of the Floridtw ( 3 883), gives some description of
the antheridial bodies, inore cspecially trying to estahlisli the fact that the
cells from wliich the sperinntia ariso :I.IW always teriiiina1 in position (see
p. 241). During the past fifty years short, descrilkions of antheridia, too
many to enninerate, are found in the accounts of the algal flora of various
coasts, as ell as in monographs of different genera. But it is to Svedelius
and Kylin in tlie ni:tin that \ve owe the detailed cytological investigations
LINN. J0URN.-BOTANY,
VOL. XLVII.
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MISS VIOLET
M. GRUBB ON THE
which have been undertaken of several genera, and without which it is
impossible to arrive at any clear idea of the exact morphology, development,
and structure of the antheridia. With the idea of adding to tho number of
such fact,s and so perhaps throwing light on the many obscure problems
connected with the male organs, the following investigation and discussion
have been undertaken.
11. Terminology.
Before proceeding to the detailed description of the antheridia in the
following fifteen species, it is necessary to explain the nomenclature which
will be employed, for the terminology in use with reference to the male
organs of the Floridez is both ili-defined and confused. Tbis is partly due to
the fact that when names were first adopted for these organs, their function
and structure were not properly understood ; further knowledge has neceasitated the modification of the original terms and in some cases the addition
of new ones, and as a result there are several systems of terminology in
existence for the male organs and the cells subtending them.
The name “antheridium” was first applied by C . A. Agardh (1828,
p. 57) to the terminal pedicellate structures visible in Yolysiphonia Grev.
(then known as Hutcltinsia Ag.) at tho apex of the branches. Although it
had already been suggested by Ellis (1767) that these “ amentaceoua
flowers ” or ‘‘catkins ” might represent the male organs, the name was not
given by Agardh from any true conception as to the function of the bodies,
but merely from their close outward refiemblance to the anthers of stamens
in the Angiosperms. The word antheridium retained this original meaning
in the red algae throughout the works of Derbes and Solier, Thuret, and
Buffhnm, and by all these writers it was regarded as denoting “ productions
celluleuses incolores, de formes variees, qui se developpent
la mbme
place que des organes de la fructification. . . . elles ont toujours pour
caractere essentiel d’&tre coniposees de trBs petites cellules hyalines, qui
renferine chacune un coryuscule ovoi’de ou sphdriqne, 6galemen t incolore ”
(Thuret, Ann. Sc. Eat. 4“ s6r. Bot. iii. (1855), pp. 16-17).
Souie years later a change occurred in the terminology which had been
vaguely foreshadowed by Goebel (1887), for in one place he states that
‘ 6 These Q T 0 7 p of
mother-cells of the spermatia’ are called antheridia ”
(p. 73) ,and in another, speaking of all a l g s in general, “ The male elements,
the mother-cells of which are called antheridia ” (p. 6) ; in this second
quotation he definitely regards the single mother-cell from which the male
element or elements issue as the antheridium and not a group of such
cells. Guignard :I few years later adopted this new use of the term
antheridium, applying it in the Florides to denote “une petite cellule
incolore, dont le contenu est employ6 tout entier h former an seul pollinide ”
(1889, p. 175); in this sense the word has also been used by Rosenvinge
MALI ORGANS OF THE FLORIDEA!:.
181
and Oltmanns. If,however, this new terminology is adopted, some name has
to be found for the groups or masses of male organs which are developed in
many species and were originally known as antheridia ; for these the words
Antheridienst‘anden,” “ Sperinatangienstatrden,” or “ Gruppen ” have been
suggested by continental authors, while the term “ sorus ” has universally
been used (Delf and Grubb, 1924, p. 380, note).
Naturally, however, this new application of the term antheridiuin has not
been at once universally adopted, and i n the last century Schmitz strongly
upheld the use of the word in Agardh’s sense to denote a (‘grBsseren oder
kleineren Gruppe von Sperinatangien und Tragzellen der Spermatangien,
soweit sich diese Grnppen selbstiindig am Thallus der Mutterpflanze abheben ” (1893, p. 231, ftnote 2). This meaning of the term is also in use a t the
present day in the writings of Svedelius (1908, p. 77) and Kylin (1922,
p. 141) ; the latter, howover, inserts in most cases the term (‘Spermatangienfitiinde ” as a substitute for “ antheridium.”
The argument, in favour of changing the original meaning of the term
antheridiurn in the red alga? lies in the resemblances which can be drawn
between the male organs in this group and similar organs in the brown and
green algs, and the desire to avoid confusion by adopting a single tern1 to
denote the same structure in all the alga. As Oltmanns points out, the
word is used in the Phaeophyceae and Chlorophycea to describe the single
cell from which the male element5 or spermatozoids are produced, whether
many spermatozoids issue from this mother-cell as in Dictyota or Fzieus,
two as in Cglindrocupsa and most species of Bdogonium, or only a single
one as in Coleoclmte pirlvinata. Since the term is already in use in this
sense, i n the other algal groups it seems iinnecessary to add to the already
confusing terminology in the Florides by applying to the whole group of
male organs a word which is well known to bear another meaning, and
which in any case was applied to the Florides a t a time when the function
of the male organs was not known, and when, indeed, it was not even
realized that these bodies played any part in sexual reproduction, The
argument put forward by Svedelius (1908) in favour of retaining the
original meaning of the word and calling the cell giving rise to the spermatium, the spermatangium (a wort1 first introduced by Schmitz), is based
solely upon the peculiar apical successive constriction of the spermatia in
Murtensia. He contends that this production of spermatia is so entirely
different from any known method of spermatomid developmrnt in the green
and brown a l g q that it is impossible to apply the term antheridium to the
cell giving rise to the male element in both cases. But it must be remembered that the type of construction in Marten& as described by Svedelius,
is found only, as far as is a t present lmown, in two other cases in the
Floridez (see 1). 242), and cannot therefore be regnrded its sufficiently
typical to form an argutnent for the retention of’ the old terminology,
1’ 2
“
182
MISS VIOLET M. GRUBB OW TAF.
or to necodaitate t,he coining
cif
a new terin for the single cell such tw
sperinatangium.”
The single colonrless hodies which issue froin t,he antheridin are now by
geiieral consent known as spermatia. A t first no definite name was given
to t,hem, and they were simply called “ corpuscles ” (Derbes ancl Solier ;
Thnret and Bornet) or “ pollinides ” (Guigtrard and Schmitz). Derbes and
Solier, as well as Naegeli, had early suggested that these corpusc~esmight
possil)ly play some part, in sexual reproduct’ion, though not i n the least
Ittiderstanding what this part was, and, borrowing a term froin the animal
kingdom, they propotin led that these bodies, which they wrongly regarded
a s being iuotile, should he called spermitozoids ; it was also snggested thiit
to clistinguish thein as animal and trot plnnt striictures the term sltoiild be
cha!lgad to antherozoids. Thuret pointed out that the antherozoids were not
inotile, and. therefore this term was notr strictly applicable, but Goebel wa9
t,he first to introduce the name sperinatiuin for tlre body whioh escaped from
tlie antheridiuni, and this name was adopted by Schinitx in his later papers
(1897),as well as by Olttnanns ancl all recent writers on the snbject. If
further evidence i n favour of thc applicdion of the term antheridiuni in
Guignard’s or Oltmanns’s aenw were needed, it could be found in the pecaliiir
nuclear behaviottr of the spermatiuni. In section VITI. of this paper it is
shown that there is reason to suppoJe that, at: one time two sperniatia were
produced from R single antlieritliuai, but that in most caaes they have now
been reduced to a single one ; i1 similar stat.e of things is foiind in the genus
(&?O,q071i1lU%,
where, in the in:i<jorityof s p h , sucli :is 03. c i i y u n a (Hass.)
Wit.tr. and 03. Vauclwrii (de Clercj Ag., t w o anlherozoids :ire produced from
a single antberidid cell, Lot in others, such as U3. crtrtium Pringsh. and
03. c a l c w u m Cleve, only oiie escnpes froin each cell. None the less, this
cell is ciilled an :intlicridinm, and by analogy the niother-cell should equally
so be called tltrvngliout tlie Florides. When, as in :it:iny species of this
latt,rr group, a succession of mitheridia :we formed one witahin another, these
:ire thelr known ;IS secondiiry or tertiary antheridia.
There remains j e t another coll conoerned i n the forniation of the spernratia
to which a variilble terminology hits h i i applied, and this is the cell wllich
subtends the antheridiuin i r u d froni which the latter arises. By.Schinity,
(l883j i t was given the name of “ ‘l‘rtigzde.’’ SveJelius (1908) objects to
the term on the ground that it has no particular meaning and substitutes in
its place “ SperitlatRngientriutterzelle,” and this is also adopted t)y Kylin.
But since the word spermatangiuni has beet1 rejected for that of antheridiuttt,
on the ground o€ the luck of necessity for the introtluction of an entirely new
word, it is obvious that tlre cell froin wl~ic~h
the nnthetidiunl arises must
either be known by the name giveit by Sclrtnitz or else as the :intheridial
niother-cell. This latter term, though wrtainlp cutnhrous, will be adopted
here, as being more expressive mid less confusing than the introduction of
“
MALE OHGANS OF THE FLORIDEiE:.
183
an entirely nsw word such as “Tragzelle.” If, as in some cases, a special
vegetative cell is interposed between the antheridial mother-cell and the
nornial vegetative cells, this is lmown as the basal cell, though it has also
been called by Yainanouclii (1906) the stalk cell.
To sum up, the spermatia, which are colourless hyaline bodies, are, in the
higher Florideae, each borne singly in :I cell known as the antheridiuni, from
analogy with the cell containing the niale eleinent in otlier alga. These
antheridia are subtended by another cell known a s the antheridinl motliercell, and are frequently clustared together in sori or groups on tlie surface
of tlie thallus.
111. Materials and Methods.
‘Ihniaterial used in the present iiivestigation wfts gathered iiiainly on the
rocks at, Shanklin aiid Saannge during visits to these places a t ditt’ttrent
times of the year. In addition, :i certaiu number of deepsea foriils, which
would otherwise have beon inaccessible, were obtained frorir dredgings
carried out at the Plymouth Marine Biological Laborator! Ly the liiiidness
of the Director, Dr. E. J. Allen, in April 1.924. In each case the date when
the material was gathered is given with the detailed descriptioiis.
I n the nia,jority of instances it W:IS found that antheridial frolids or thiilli
could, after careful exi~mination,he recognized on the shore, The prevailiiig
cliariicteristic, revealing the presence of sprm:itia, is a paleotw or whiteness
of the t‘rond in tlie region of the developincant 01’ these bodies; in soiile cases,
ouce the iippearance is knou.n, t,his callnot be ovt-rlooked ci. e. pale sori of
hTitoplijZluniHillire) ; in other inst:inces, recognition is aided by the develop
tilent of spermatia in special structures (i. e . the pale yellow coriceptacles of
Lawencia pinnatijda, or the colourless (‘leaflets ” of Ilri’topliyllum lucerattwij.
But in a few species, although the position of the spermitiul sori was known,
it was found iiiipossible to pick out male froin sterile fronds :&part froni
microscopic exanhation (i. e. (’evaeuiunz rubrztwt, C,’allitha?nnionsp.).
WIren possible the spertiiatial rnaterial was fixed on the shore i n
Fleintiiing’~weaker solution for x l g ~ . This fixative was found to give tile
best ell-round results, both in preservation without shrinkage of the cytoplasm and chromatophores, and also in detailed structure of‘the nuclei. The
algs were allowed to reniain in thc liquid for varying times according to
their structure ; iu the ciwe of delicate filamentous types (Polysi@lLonia,
Ce~amiiim)1 to 3 liours was found to i ~ elong enough ; if left i n longer than
this the filaiiients were liable to frngnient. tiuring the prowss of wasbing.
For thal!oid t,ypes 24 liours was not too long. I n soine cases (IlhociomcZa,
Fururcellavia) the experiment was made of placing tlie f‘roiida in cl.ilorof‘ort~i
water for two minutes, directly on gathering, so as to prevent the nuclei
passing into a resting stage before the gradual penetration of the fixative ;
t.he resnlts, however, did not coniyeiisate f o r the extt a labour involved.
184
MISS VIOLET M. ORUBB ON THE
After fixing, the a l p were passed gradually into fresh water and then
washed for 24 hours in running water. I n cases where it was necessary to
preserve the material for future examination, the best medinin proved to
be equal proportions of 50 per cent. alcohol and 50 per cent. glycerine, a8
ill this the ~nininiiini of shrinkage took place, while it was possible at the
same time to obtain a very clear and distinct nuclear differentiation with
haematoxylin. I n niost cases an endeavour was made to embed direct in
parafin wax, dehydration being carried out on the glycerine embedding
system (Dowson, 1922). Microtomed sections were cut from 3-5p in
thickness and stained for 24 hours in Haidenhain’s Iron-alum Hzmatoxylin,
Such sections, it was found, offered the only means of examining niinnte
nuclear details with accuracy, but all delicate structures, such as gelatinoas
walls and empty antheridial sheaths, were so contracted by the embedding
process that it was impossible to distinguish them with any certainty. As a
conseqiience of this effect, the drawings of spermatia made from microtomed
sections and published in descriptive articles have given a false impression
of the structure of the antheridial group, since the cells are depicted without
the delicate surrounding walls (cp. Kylin, 1922, fig. 77 C). Experience
shows that these walls are best seen in very thin, stained, hand sections, or,
in some filainen tous forms (i. e. Polysiplioiiia, Callithan~nion),in portions of
the filament mounted whole. I n this case, if the material has been carefully
handled, no shrinkage should have occurred. It would seem, therefore, that
no complete, or even adequate, idea of the structure of antheridia can be
obtained without observations made on both hand and microtomed sections.
IV. Inveetigation of the Antheridia and Spermatia in particular Species.
The species described here are arranged on the classificatory system for
the Rhodophycee, given by Sclimita and HauptAeisch in Engler and Prantl’s
‘ Pflarixenfamilien ’ (1897). It will be seen that this does not in any way
iniply that a similarity in antlieridial structure will necessarily be found
between two species placed close to one another; the scheme is merely
adopted for convenience. I n the descriptions an attempt has been made in
each case to refer to all previous records of antheridial occurrence, though
these accounts are mainly confined to notes concerning tho positioii of the
atructurea on the thallus. As far as possible thc species chosen have been
those of whish there exists 110 previous d e t d e d description.
(1) CHONDRUB
CRISPUS * 8tackh.
Material was gathered at Freshwater and Whitecliff Bay, Isle of Wight,
in April 1923, and Wembury Bay (Plymouth) in April 1924.
* Antheridis haw previonsly been recorded in a short note by Buffham (1896,p. 18S,
figa. 2 a d 3) and by Darbiehire (1902); this condensed account is referred to in the text.
MALE ORGANS OF THE FLORIDEE.
185
The antheridia develop in this species on the upper parts of the thallus of
an otherwise normal vegetative plant. They are recognizable as whitishpink patches or sori, the youngest regions of which are to be found just
below the apex, extending dois nwards for 3 to 4 inin. Occasionally the sori
do not completely cover this area, but are represented by spots or irregular
patches ; in any case, as Buffham noted, they can best be seen in half-dried
material, or even in fronds which have been completely pressed. All the
inaterial examined by me has been fully fertile in the spring, but, on tho
other hand, the plants described by Buffhain (from Hastings) and Darhishire
were mature in September or October. It seems hardly likely that thalli
which were already discharging their sperinatia in large numbers in April
should continue to do so throughout the summer until the autumn: the
more reasonable probability is that there are two seasms of spermatial
production on this species, male plants being developed in spring and
autumn.
FIG. 1.r
Chondrue 06pus.
Section of a vegetative thallus, showing “cortical ” structure. x 800.
b. Section showing the development of antheridial mother-cells. x 1800.
c. Section through similar region, with antheridia wising from mother-cells. x 1tMX).
a?. Escaping spermrttium, with nucleus in prophase. x 1800.
a.
I n a section of a vegetative region of a thallus it can be seen that the
central area is occupied by multi-nucleate cells full of contents; these are
circular in cross-section, but are elongated in the direction of the length of
the thallus. The latter i s bounded by small cells in close-set rows extending
perpendicularly to the periphery ; these chains of rounded cells arise in pairs
from the outer cells of the central thallus tissue, and each row is terminated
by a single rather elongated cell (fig.1 a). In the upper and youngest parts
of the thallus the ‘‘ cortex ” is coinposed of only a few rows OF cells ; lower
down eight or even iuore rows may be formed by division, each cell being
uninucleate and pigmented and the whole enclosed by a gelatinous ‘‘ cuticle.”
* The drawinga throughout were made with the aid of a camera lucida or by projection.
186
NISS VIOI,ET If. QltUBB OX TEE
I t in the e1ong:itetl cells foriiiing the outer layer which give rise to the
antheridial uiot,iier-cells, ~ i i dthis by means apparently of w longitudinill
division, for in the soral :wea of ;L inale frond the lust globose cell of each
corticsl row is alw:iys t.crmin:itcd by two narrow eloagatetl cells (fig. 1 I).
Th:it these are tlict tunthrr-cr.lls is c l a r l y seen in a slightly older region, for
:i,ntheridi:i epring from them (fig. 1c).
At t.he time of the fortiiation of antheridia the ‘’ cut,icle ” appears to
thicken in tho sor:il :ires ; t,lie tirst :iiitheridia arise laterally from tho surftte
of each of the pairs of inotlwr-cells :is thin narrow bodics coiiiposetl of an
iipwtird protop1:istiC: rxtrn4oti aurroriilded by the mothw-cell wall (fig. 2 aj.
llir cytoplasiiiic conf(wts, whi(41 e i i c h x :L single tiualeus hut, no plsist’ids,itre
ahstricted a t a point level witit the siirfrtce ot‘ the mother-cc?ll hy the ringlike ingro\yth ot tlw surrnunding wvoll ; when coii\plt?tc?d,this cnrves upward
in the centre and is ci)lnt)ilr:il)le i n . G I i : i p e to an inwrt.cd watch-glass. The
I \
k’l(i.
2.
Sntheridiiil sortis in Chonilrws crispus.
x 1800.
r h w i tig iuotber-cellu ctrisi~g from ‘ I cortictil ” cells and each
Rubtending two ~ 1tliaridiit.
1
h. Surface view uf the (‘ciiti~lr,”sho\viiig the ol)eiiings tlir,~iighwhich the syermtttia escape.
n. ‘l’rrtnnrerso section
antheridiuiu ripeils, 1)ecoiiiing titor(! rouiided in form, the wall swelling
consiJer;iblp. Wlieti iir!:irly i~;itiire{lie cytopl:wniic botly within can be
seen to be eut,irely siiriwiitide 1 by a clear narrow arc:t which is inore
refractivr than the antlicridial w d l : i d iii:iy represent the wall of the
sperniatiuin (fig, ,?a) ; when thc latter escapes I have no doubt tlut this
wall is present, :is :it1 osceudiiigly delicate iiieiii1)raiie. Tlie antheridium
lengthens upwards, t h o \wll piercing the “ cuticle,” though iiev(!r appretitly
protruding hct)-ontl it ; t,liis “ eloitptctl grl;it,iitous hotly ” Buff1i:ini ineaenred
:itid found to be (‘SO p high i L i i ( 1 7 p thick.”
A longitutlinal split then
occiirs i n tlte s.sollen anthnridinl w d l , and the wliole contents escape into the
surrountling wntcxt as a roundctl cytopliisn~ic body containing a single
nucleus : i d clothed in a thin wall. A surface view of tlic “ cntiole ” a t this
time phows i t t.o he pierced by numerous round holes, soiiie of which, as seen
f i w ) above, appcw to be einpby, while ottiers show :Lspermatium nearly
MALE ORGANS OF THE FLORIUEB.
187
extruded (fig. 2 6) ; if a frond is suspected of bearing antlieridial sori, their
presence caii easily be corifirined by exairlining the “ cuticle” in surface
view under thc microscopc, perforations being visihle if the sorus is present,.
Darbisliire states that only one sperinatiuiii aristas from c?ach wother-cell,
but a second lateral aiitliuridiuiii is clearly developed by the aide of the tirst
at the apex of the mother-cell (fig. 2 a) ; this grows up, ripens and liberates
its contents in exactly the same way as the first one. A third primary
aiitlieridiuiii does not see111 to be f’oririetl, though i n such closrly-packed
tissue where t8he mother-cells overlie one another it i s diiiifiotilt to inalte out
the nunibor of antheiidia connected with eacli motl~er-cell. Secondary
nnthcridia are cert’tiinly found growing u p within the empty walls of the
priuiary oiies, b u t 1 have iiot a.s i n soiiie oases (fig. 30 6 c ) .been able to
identify a third set within tlie walls of the secondary ones. Each set of
spertmtia takes a considerable tinie to trawl to the surface of the thick
“cutiole,” rind as it result thc second sperinatiuiii i b often forcing its way up
before the first is liberated. A low-power viow of :t cross-section at this
time shows what appear to be loose sperinatia scattered a t many levels in
the “ cuticlo,” the anthoridial walls being exccedingly difficult to see. After
the foriliatioil of antheridia hiis ceased the thallus probably returils to the
norinal vegetative structure.
It has already been noted that the aiitheridiai uiother-cc-11s are uninucleate
and pignierited, the plastids lyiiig tnaiiily at [lie Lase aiid sides of the cell.
On the formation of an antlieridiuiii tlie ikiother-cell nuoleus p.sses u p w a d s
and divides initotically a t the base of the protoplasmic projection, one
daughter nucleus passing into tlie latter. “he Lehaviour of this nucleus
seeins to follow in every detail the stjagus described for Pwrcellur*ia (p, 239),
and in the ripe sperrnatiuiii it caii be seen to be in early prophuse, a number
of chromatin granules or Kijrnchen ” being preseiit (fig. 1 ti). Apparently
uo plastids pass froin the mother-cell in to [lie speriiiatiuiii j t,he structure
figured by Darbishiro (pl. ti. fig. 32) as “:I fi.agment of plastid” is witLout
doubt the nucleus which he overlooked. \Vhen the syennatiurn is ripe aiid
about to be liberated it, iiieiisures from 7 - 5 to 10 p i n length, being 4 to 5 p
in dianieter * ; it is tlion ;I cytoplasmic bod) clothed in a delicate wall and
containing a central or apical nuclcus about 4 p in diaiiieter suspended above
a large vacuole.
‘L
(2) LOMENTAIUOVALIB E d . = Chyloclutliu oiralis Hook.
While cyatocarpic and tetrasporic plants of this species are well known,
the autheridial ones have rarely been EOUIICI, tlieir presence being noted only
by BuiYhaiii (1896). I n spite of continuous searuh in various localities, the
writer has found only a single plant at Swanage, in Augud 1934.
*
The nieaanreruentu of the speriiintis aiid nuclei were made throughout on uiishruiiken
material, except when otherwise stated.
168
MISS VIOLET M. GRUBB ON THE
Antheridia are developed in sori upon the obtuse, hollow, bladder-like.
lateral ramuli in the upper regions (fig. 3). These short branches are borne
in dense clusters at the tips of the branching " stem " ; the sori arise at
their base, spreading up towards the centre, so that the youngest antheridia
are to be found about half-way up the hollow sacs, the apex being sterile.
The sori are very irregular in shape, sometimes occurring as small isolated
patches or elongated lines, or often as one homogeneous mass formed by the
fusion of smaller sori. The presence of the groups of antheridia gives a
colourless appearance to the portions of the thallus where they occur, and it
FIQ.3.
Portion of a male plant of Lonmaturia oaalis. The position of the sori is shown by stippling.
The dotted lines around the lateral brmches represent the surrounding fringe of
unicellular hairs. x 2.
is by means of these whitish patches, not more than 1inm. in length, that
the antheridial plant can be recognized in the field (fig. 3).
The sterile swollen ramuli are composed of an outer single layer of cells
varying in size, while the whole central region is hollow and not traversed
by diaphragms ; in the youngest branches this central part is filled with a
thin watery fluid. I t has been shown by many workers that the origin of
this structure is from branching filaments of cells which gradually separate
from one another, forming a lining layer of cells and leaving a cavity within
189
MALE ORGANS OF THE FLORIDEE.
(i. e. Giard, Killian, Schmitx). The whole is clothed with a very thick
gelatinous “cuticle.” The cells forming the outer layer are irregular in
size, and from without the surface appears to be studded with large round
cells, each of which is surrounded by a ring of smaller ones filling the
interstices ; these are all pigmented, multinucleate, and filled with dense
contents resembling “ Floridean starch.” From these cells, both large and
small, arise very long rinicellular hairs (fig. 4a), which, when mature, are
cut off from the thallus by a cross-wall at the base, and themselves possess a
thick wall with little cavity except a t the apex, where there is a swollen
thin-walled knob containing the nucleus and rich protoplasmic contents.
These hairs are just visible with the naked eFe, and cover the thallus even in
the antheridial region (fig. 5 u ) .
FIG.
4.
..
C
a
Lometitaria ovalis.
a. Portion of young antheridial sorus. The bnsd cella are seen before the development of
the antheridial mother-cells. Vegetative thallus cells indicated by dotted lines.
x 800.
b. Microtomed section showing single antheridial mother-cell borne on a basal cell and
giving rise to two antheridia. The nucleus of the antheridium on the left shows the
chromatin separated into two granular masses. x 1800.
c. Antheridial mother-cell giving rise to first young antheridium. x 1800.
Unfortunately in the available material the sori were all mature, and it
was not possible actually to observe the stages in the formation of the
mother-cells. But a9 far as could be made out., a curious development
precedes the production of antheridia, in that a system of branching threads
arises from the thallus cells, spreading in overy direction over the surface
(fig. 4 a ) . When first observed in any isolated region, the threads resemble
some well-developed epiphytic growth, but on comparing them over a large
190
MISS VIOLET M. GRUBB ON THE
area, i t is seen that the system is made up of numbers ot' small groups of
cell-threads. Each group has arisen from a central cell which has been cut
off from one of the peripheral thallus cells (fig. 5 a). The order of development is therefore somewhat similar to that found in Callithamnion brachiaturn
(fig. 30a) or Grifithsia corallina (tig. 22) ; a central cell cut off from a
thallus cell gives rise by division to a system of branching threads which
spread over the surface of the thallus and are composed of s i n ~ luninucleate
l
pigniented cells linked to one another by protoplasniic connections (fig. 4 a).
Frorri each cell of these filanit.nts two or three antheridial mother-cells grow
out as small projections, generally densely pigmented and containing one
nucleus ; the cells of the filaments therefore function as basal cells. The
inotlier-cells increase greatly in length, stretching upwards until long aid
narrow and measuring about 1 5 - 2 0 ~i n length (fig. 5 a & b). Thrir :ipex
FIG. 5
b
Lonasnturirc ovrclis.
Outline drawing of a section through an antheridid I O ~ L I R , showing central cell git ing
rise to lateral ones. From each of these, two or t h e e antheridid mother-cells arise,
each bearing ultimately two or thiee antheridia. A nnicellular heir is seen (left).
x 1800.
b. Section of an aiitheridittl sorns, showing the production of secondary antheridin. Lefttirst qwrniatia have not yet escaped. Right-empty sheath of primarj antlieridiuni,
with a secondary one growing up within. Plastids omitted. x 1800.
11.
is somewhat equare aud blunt, and laterally from this primary antheridia
are formed ; these arise as small protoplasmic protuberances, clothed in the
mothey-cell wall, and containing a single nucleus derived from the divisioii
of the inother-cell nucleus. Two primary antheridia are always developed
and sometimes three (fig. 5 b ) ; there does not appear to be any general
regularity in the number as in other species, and though not developing
quite simultaneously, there is not such a marked interval between their
production as is often the case. They swell and increase in size and are
MALE ORGANS OF TEE FLORIDEE.
191
abstricte(1 froin the mother-cell hy the ingrowth of the gelatinous wall of the
latter, always, however, remaining connected by a very fine protoplasmic
strand (fig. a h ) and when ripe measuriuy 4-5,~.At this stage there is
a most striking resemblmce in form between the Inother-cell bearing tlie
antheridia and a basidiuni with two sterigmata bearing hasidiospores. The
walls OE the antlieritlia which appear as sarrountling gelatinous sheaths are
very difficult to see, hut it, is clear that they are much stretched upwar'Js,
piercing the " cuticle " and becoilling split and frayed at the apex (fig. 5 a).
Finally a decided split. occiirs, cleaving the whole wall, and through this
the spermatium escapes, being by now clothed in a delicate membrane ; t,he
antheridial wall, released from the pressnre of the spermatinin, at once
contraCfsr only leaving :L narrow cavity (fig. 5 b ) . Meanwhile a secondary
sntheridium develop within th(A sheath of the primary one (fig. 6 b, riglit.).
This sonietiines occurs hefore tjhe release of the first, hut i n any c:iJe the
development and liberation are exactly similar in the case of both primary
and secondary spermatia. No tertiary antheridia appear to be formed. A
inotlier-cell may therefore producc six ant.heridia altogether, three primary
and three secondary.
The iuother-cell of the antheridia is both uninacleatu and st,rongly pigmented, containing granular contents. I n the resting condition, the niiclcus,
which consists of a deeply-3taining central region and a colourless outer
area is central in position (tig. 4h). On the formation of antheridia it
moves to the apex oi the cell, where a sinall projection is arising, and there
divides mitotically, the spindle being arranged parallel to the long axis of
the n~other-cell, t.he whole figure measuring not inore than 2 p . Tlle
chromatin is visible at inetaphase as a darklystaining band across the sqiiat,or
of the spindle anti u t anaphase as two minute da.rk dots, one at either pole
(fig. 4 0 ) . One of these daughter nuclei passes into the young antheridinm
resting condit.ion. There it enters short,ly into early prophaw, the
in
ctlroinat,in being distributed as irregnlar dark thickenings aloug the t hrends.
Z;"ilially, at the time of liberation the chromatin is concentrated in regular
(1 ,& grnnules connected by delicate threads and often gathered into two
within the nucleus, which is n o w apioal in position (fig. dh) ; the
antheridial nuclei are, li kt! the spermatia, very small a i d meiisure only
aho11t 2 p i n tliameter. The spermatium is unpigmented but coiitainR a
considerable amount of granular cytoplasm arranged around a large vacuole
ileneath the nucleus.
*
(3) CHAMPIAPARVULA (J. Ag.) Harv. = Cliyloc:latl%a
parmila Hook.
Material consisted of one plant gathered at Perros, Britt,any, July 1924.
The antheridid plank of G'la?npiayarvula are exactly siniilar in outward
iy The presence of antheridia in
this irpeciea has previously been noted by I)&&
(1896,p. 111) and Nett (1896).
192
MISS VIOLET 1.GRUBB ON THE
appearance to the vegetative ones, but they may be distinguished on close
examination by pale patches scattered over the ramuli. These coloiirless
areas are the sori which, according to Davis, may appear as “ caps at the end
of the stem, but niore often as bands around the older parts of the frond.”
In the one plant collected it is the exception to find sori a t the tips of
branches, but they usually occur on t w o or more segments of the thallus
(fig. 6 ) . These segments are more swollen and rounded than the vegetative
ones, and the colourless cells may either cover them completely or may be
scattered in small patches on their surface.
FIG.ti.
Part of an antheridial plant of Chnmpia paruula. Sori represented by stippling.
x 8.
The development of the antheridial mother-cells in Clrampia parvula is f roiii
a system of branching threads. Nott pointed out that the basal cells of these
threads arose and were cut off from the angles of the peripheral cells of the
thallus, and by branching they formed “rows of cells which radiate out in every
direction from the stalk cells.” This, it will be seen, is an entirely similar
development to that found in Lonaentaria owulis, the cells being in the same
way uninacleate, pigmented, and filled with dense contents. From these basal
MALE ORGANS OF THE FLORIDEB.
193
cells, antheridial mother-cells are cut off singly or in pairs, and these, when
fully developed, attain to as much as 10 or 11p in length (fig. 7) ; they are
slightly pigmented, and the nuclsus is often difficult to make out owing to the
presence of granular contents. Froin these cells the antheridia develop, first
as slight blunt projections (fig. 7 a) and later, when containing a single nucleus,
becoming stretched and abstricted a t the base (fig. 7 d ) ; they remain, however,
in protoplasmic cotinection until fully ripe, when the connection is broken
and the spsrinatium escapes. The antheridial wall when mature pierces the
FIG.7.
r
C
d
e.
Development of antheridia in Champiapavvula. x 1800.
a. First signs of development of antheridium from mother-cell.
b. Microtomed section showing the nuclei in different stages of
prophase in the ripening antheridia.
c. Reconstruction of a mother-cell bearing three antheridia.
d. Antheridial mother-cell seen at a high focus.
c. Same at H. low focus, showing the third antheridium.
‘(cuticle ” to a sufficient extent to permit the escape of the spermatium through
an apical split direct into the surrounding medium (fig. 7 6). As a general
rule three antheridia appear to be developed from each mother-cell, standing
around the slightly flattened apex at three different growth-stages (fig. 7 c).
These three can never be seen at the same focus, but a t a high focus it is
generally possible to see one or two, and a third becomes visible a t a low focus
(fig. 7 d &, e). Secondary antheridia are also developed in this species on the
liberation of the primary ones, but there is no sign of tertiary ones. Each
mother-cell has, therefore, the po~sil~ilit~y
of developing six nntheridia.
The cytological changes in the production of this structure are entirely
similar to those in Lovienturia ovalis. The mother-cell nucleus tnoves to t,he
apex of each mother-cell after a young projection has arisen ant1 there divides,
one nucleus passing into each antheridium in a resting state. While this
nucleus is moving to the apex of the latter it, passes into an early prophase
(fig. 7 b, left) until, when the- spermatiutn is mature, a nuinher of deeplystaining granules are present, united l y delicate threads (fig. 7 h, right,).
‘I’he nucleus is in this condition when the s~ierniat~iu~n
is liberated.
The resemblance between the method of development of the antheridia in
Champia parvula and Lomentaria oralis is so g e n t that,, given a transverse
section of a sorus, it would be almost impossihle to state from wltich species it
had been cut. I n both, the development proceeds in the following st.ages :-
1. Central cells are cut off from the peripheral cells of the tttallns.
2. Thcse central cells by division gave rise to branclting rows of basal cells
extending over the surface of the thallus.
3. From each of these arise two or t,hree elong:ited mothel*-cells.
4. These give rise sub-terniinally to two or t.hree antlieridin.
5. These on attaining maturity liberate their spermatia 1-hrough an apical
split in the antheridial wall.
6. Secondary antheridia are developed within the enrpt! slteaths of the
primary.
Such striking similarity in the details of ant~lieritlii~l
procluctiori ca,,not, fail
to emphasize the close systematic relationship hetweun the two geuera.
(4) NITOPHYLLUM
HILLIIF,
* Grev.
Material consisted of i n m y fertile thalli dredged in Plynioutlt I3ay ill
Ai)ril 1924. The alga was found at the same time attachetl to the roclis i n
the tidal region, but in this position was always sterile.
The antheridia occur on separate plants and apparently never i n coinbination
with the tetraspores or cyatocarps. The male plants are nornial in size :111d
ge1leral ilppearance, hut are easily distinguished when fresh by the preseiice
of numerous little pale spots or patches, exactly similar i n position to tile
darker areas formed on the tetrasporic plants. These are the tlisconnecated
soi.j, and are most marked near the base of the tliallus, beginning roughly
about 5 rnm. front the point of attachment ant1 decrc.asinp ill .size tom:rrds tlle
irregular margin, where the youngest sori are to IJe fonnd u s mirtute pale
spots. The sori occur on both surfaces, the larged ones n e a r the base
The presence of antheritlia in this species has previously been iiotrd by Thuret (1855).
MALE ORGANS OF THE FLORIDEX.
195
becoming more or less confluent with one another, forming irregular streaks
running in vaguelg parallel lines between the veins, but never crossing the
latter.
The normal antheridial thallus before developing the reproductive bodies
consists of a single !ayer of cells, except in the region of the veins, where it
becomes three cells in thickness ; antheridia are, however, always borne in the
single-cclled region, the cells composing the tissue of the frond hore being
three to four times as long as broad and containing numerous small plastids
FIQ.8.
Development of antheridia in Ntophyllum Hillie x 600.
Surface view of ed;e of young sorus, ehowing gradualdivieion of cells to give
antheridid mother-cells.
b. Transverse sectim through a siiiiilar position.
a.
clustered a t either end, as well as a single nucleus generally central i n position ;
the whole is enclosed in a gelatinous " cuticle " (fig. 8 b). On the forniation
of antheridia the single cells cut off one small cell a t each end, by walls
para!lel to the surface of the frond. Each small cell appears re.2tanguler in
CINN. J0UBK.- BOTANY, YOL, XLT'II,
Q
196
MISS VIOLET M. URUBB ON TBE
surface view, is uninucleate and pigmented (fig. 8 b) ; the thallus is now threelayered in the soral regions between the veins. Each of these small cells
divides hy a vertical wall and then by a second wall, also vertical, a t right
angles to the first, thus giving.rise to a little group of four uninucleate cells
in a single layer (fig. 8 a ) . Each of these is then divided by two additional
intersecting vertical walls giving finally sixteen cells in a single layer grouped
together as if i n a little packet (fig. 8 a ) . I n the soral areas, therefore, the
original thallus cells are clothed on either surface with groups of sixteen
small pigmented uninucleatc. cells, the whole covered with the gelatinous
“ciiticle” (fig. 8 a) ; these cells, which are now somewhat three-cornered in
surface view, are the antheritlial mother-cells and from them the antheridia
arise. It will be seen that this development is in .many respects similar to
that drscribed for Martensia (BveJelius, 1908) and also for certain species of
Delesseria (Kylin, 1922) ; in the former case the thallus also becomes threelayered on the formation of antheridia, the middle layer playing no further
part in the development and the outer layers dividing up to give numerous
small cells, 30 to 50 being formed from each original surface cell. These
antheridial mother-cells are uninucleate in Martensia as well :IS in Nitopliyllzcm,
but in the former the original vegetative cell contains many nuclei, and these
gradually diminish in number as continual divisions take place. I n both
Delesseria sanyuinea, D. alafa, and U . sinuosa a somewhat similar type of
development occurs (Kylin, 1922). Here the male t,halli, before the formation
of antheridia, are one-layered, except in the region of the midrib or of stiialler
veins where there may be as many as seven rows of cells ; in each case an
outer layer of cells or “ Rindenschiclit ” is formed by the cutting-off of small
cells on each surface. The cells then divide by perpendicular walls, giving a
larger number in a siugle layer, no intercalary divisions taking place ; liow
many cells are formed from each surface cell is not stated. In these three
species of Delesseria n o pnrticulars of the number and arrangement of the
nuclei in these divisions are given, though the large vegetative cells are known
to bg multinucleate ; in each case, however, .the antheridial mother-cell
contains only a single nucleus.
I n Nitophyllum Hillire the antheridia first arise from the mother-cells as very
narrow beak-like processes enclosed in :I comparatively thin wall which is
merely an extension of the mother-cell wall forced up. through the thick
‘ 6 cuticle ” (fig. 9 a).
This single sub-terminal antheridiuin is very sinall and
thin conipared with those formed in other genera as Grifithsia, where there is
no compression such as arises here froin the close packing of the mother-cells
side by side. Soon, however, the dense protoplasmic contents are abstricted
fromi the mother-cell by the gradual ingrowth of the surrounding gelatinous
w;Jl (fig. 10 a ) , though remaining for some time in connection (fig. 9 a). The
sperlnatium grows and swells, becoming much enlarged and almost spherical;
the single nucleus occupies a curved apieal position, beneath which is a large
MALE ORGANS OF THE FLORIDEE.
191
vacuole crossed here and there by strands of cytoplasm (fig. 9a). The
antheridial wall is now stretched to such an extent that it is actually forced
beyond the “cuticle,” and shows at this stage a distinct narrow outer layer, a
swollen middle one, and a delicate inner refractive region around the spermatium
(fig. 9 u). The latter finally escapes directly into the water around, through
an apical split in the antheridium wall (fig. 10a). But before this occurs a
second antheridium arises at another corner of the triangular mother-cell and
begins to develop, and even a third antheridium is commonly formed before
the first spermatium has passed out. On looking down, therefore, on an
Nitophyllum Willie. x 1800.
a. Transverse section of a young antheridial sorus, showing the thin “cuticle” pierced
by the antheridia in different stages of development.
b. Surface view of a siiiiilar sorus, with group of three antheridia developing
successively from mother-cells.
antheridial sorus from above, one sees little groups of antheridia in threes,
each member of the trio being at a slightly different stage of development,
while far below (as it seems) can be seen the surface of the pigmented mothercell (fig. 9 b ) . Each of these rounded spermatia is liberated in turn through
the apical split in the antheridial wall. The pressure exerted lipon this wall
by the spermatium during its difficult outward passage must be considerable,
Q2
1.98
MISS VIOLKf M. URFBB ON THE
for iininediatel~aftei its liberatiori the surrounding wall contracts. Though
tlie wall is supported by the “cuticle” and cannot shrink back upon the
illother-cell, yet the contraction is sucli that only a narrow slit-like opening
remains, a i d even that is often difficult to find (fig. lo/)). I n sori near the
base of the frond, where the ‘‘ cuticle ” is thicker and where the spermatiuin
must traverse i t greater distance before liberation, :Intheridit1 have several
times been found with shrivelled spermatia caught in their openings (fig. 10 d ) ;
evidently here the force which causes tlie expulsion of the sperinat,ium was
not qnite sufficient to overcome the resistance of tlie wall. I t is noticeable
that iii these lower sori the spermatia are longer, thinner, and smaller than in
the upper ones where the “cuticle ’ is not so thick.
As a general rule, secondary antlieridia appear to be formed within the
walls of the primary ones, developing in the sanie way (fig. 10 c ) . I n the
lower region: of the thallus, however, they could iiot always be found, and
apparentlj do not occur here regularly.
FIG.10.
Xttophylluna Hillin. x 1800.
Rntheridia from old BOPUS at base of a frond (optical section).
a. Young antheridium in process of gradual abstriction.
b, Empty antheridium after escape of first spermatiun.
c. Secondary antheridium forming within the empty wall of the primary one.
d. Sirirelled spermatium, apparently unable to escape from an antheridium.
(5)
NXTOPHYLLUM LACERATUM
* Grev.
Material Has obtained froin dredgings in Plymouth Bay, April 1924.
The antheridia in ATitopl~yllumlaceratuna are borne on leaflets which iiiay
be anything from 1 to 20 mni. in length. These are found in spring a t the
apex of the old and ragged growth of the past year, as many a s ten or
twelve growing on the divided tip of one old thallus. They show
branching veins, and the antheridia develop as lateral pale pink patches,
tlie sori gradually extending round the apex, leaving a non-fertile margin
and central region. The inale plants are apparently not common, for out
of a large number of specimens brought i n bg dredging a t Plymouth, the
* There are no previous references to antheridia in this species.
199
YALE ORGANS O F THE FLORlDEB.
inajority of which were either tetrasporic or cystocarpic, atitheridia were
found on less than a dozen.
The development of the antheridia resembles closely that) described for
iVitoplbylluna Hillice. The leaflets are composed of a single layer of elongated
cells coiit.aining generally several nuclei and plastidu clustered a t the two
outer surfaces.
When about to beconte Fertile, surface cells are cut off above and below,
making the thallus three-layered. Each of these divides, as in N. Hilliru,
to give, in many instances, sixteen stidler cells. I n some cases the full
number of divisions does not seein to be attained, and only twelve or
thirteen cells are fornied from an original surface cell ; this, however, does
not seein in any W:LJ'to prevent such cells from fulfilling their functions
as norm:ll mother-cells. The antheridia are formed in exactly the same
way as in iV. Hillice, and there is therefore no need to repeat the description
(see p. 196). They arise from each mother-cell in succession (fig. 1 2 b ) ,
FIG.11.
a
b
NitophylZu?n larerutuni bearing laterally rosettes of leaflets
known as Gonimophyllim Bufi.anti. These are covered with antheridial sori, and
also bear tetraspore-lilre structures. x 10.
6. Section through an ant,heridial sorus of
Iucemtunz. The central cells are rlothed on
the outer surfaces with mother-cells bearing anthoridin. x 690.
u. Portion of a thallus of
being a t first exceedingly thin and narrow as in the previous species, and
later rounding off and becotniitg 6 to 8 p, in length. Secondary antlieridia
appear regularly to be formed and to pass out through the empty sheaths.
The wall surrounding the young spermatiuni while still enclosed in the
antheridium is very clearly seen it1 this species (fig. 12 a).
The mother-cell nucleus lies at the base of the pigmented cell and only
passes upwards to divide. Tliis divisioii takes place when the ;intheridium is
represented by a very short-pointed process, and it is noticeable that the
antheridial nucleus on formation passes a t once into a resting stage wit,h a
central darkly-staining region and a clear area around (fig. l 2 f ) . As the
antheiidiuui lengthens, the nucleus inover3 along it as a narrow body surrounded hy dense protoplasm (fig. 1 2 d ) , until finally, when the spernint,iuni
has beeii cut off, the nucleus is at the apex, suspended by strands of cytoplasm
800
MISS VIOLET M. GRUBB ON T H E
with a vacuole below (fig. I d a & c ) . Before the spermatium has reached
maturity this nucleus is seen to be entirely made up of a tangled mass of
irregularly thickened threads (fig. 12 e ) . When the spermatium is ripe the
chromatin masses on these threads have formed a number of separate granules
strung together by means of delicate linin threads (fig. 12 c). The nucleus,
measuring about 2 . 5 , ~in diameter, is in this state when the spermatium
escapes.
FIG.14.
C
d
e
.Fa
Development of antheridia in Nitophylluin laceraturn. x 1800.
Antheridial mother-cell at high ( a ) and low ( b ) focus, showing the
three primary antheridia.
c to$ Successive stages in the development of spermatia.
The similarily between N . Hillice and N. laceratum in the method of
formation a i d structure of their antheridia is so close that it would be
iuipossiille to tell the species from a transverse section of a sorus. On the
other hand, the two species are easily separated by the position of the male
organ, these being situated on the thallns in the first case and on special
fronds in the second. I n a.Gmelini, where the antheridial sori are said to
MALE ORGANS OF THE FLORIDEB.
20 1
be borne either near the margin of the thallus or on special processes on the
tiiargin, one would conclude from Buffham’s tigure (1893, fig. 21) that the
development is in all probability similar. In NitopIiylZunz therefore as in
Delesseria, so far as is known the development of the antheridia is constant
throughout the genus, but the position of the sori may be either on the
normal thullus or on special antheridial fronds.
Note on GONIMOPHYLLUM
BUFFHAMI
Batt.
Batters (1892) described n. specimen of Nitopltyllutn laceratum bearing
groups of iriiniite leaflets on the surface or a t the margin of tlie thallus.
These leaflets, arising from a “basal cushion,” were said to be covered
indiscriminately with antheridia, ‘ procarps, and tetraspores. The whole
structure was regarded as a parasitic alga and described uiider the name of
Gonimopliyllum Bujhami Batt. Specimens of N. laceratum were dredged
from Plymouth Bay in April 1924, bearing similar small rosettes of
crinkled leaflets, and these have been examined for reproductive organs.
I n each rosette some part or the whole of the surface was covered with
colourless sori of antheridia, while in three specimens antheridial and tetraspore-like structures occurred in close proximity, even being found in the
same rosette (fig. 11a ) . From a slight exatiiination it seems probable that
the tetraspores do not develop normally in these cases and never come to
maturity. The structure of the leaflets and the development of the antlieridia
appears to be exactly similar in every detail to that described above for
N . Zaceratum. This resemblsnce is so striking, that, combined with the
fact that the procarps and cystocarps are also said to resemble those on
AT. Zaceratutn “ in all essential particulars,” the question arises a s to whether
the structure is i n reality a parasitic alga. The evidence seems to point
towards the probability that these curious rosettes of leaflets may be an
abnormal outgrowth of the thallus tissue of N. laceratuni. The cause of’
this abnormality is a t present a matter of speculation, but i t does not seem
unlikely that the outgrowth may be induced by the presence of some
intercellular or intracellular endophyte.
(6) LAURENCIA
PINNATIFIDA * Lam.
Material was obtained from Shanklin, Swanage, and Plymouth, January
and May, 1923 and 1924.
Observations show that plants bearing antheridia ripen in the spring on
the south coast of England, thus coinciding with the production of the feniale
organs. The male plant? are numerous, and tli.ere is 110 difficulty in obtaining
* Short notes recording the presence of antheridia have been niade by Greville (1830,
p. 110), Derbes and Solier (1850, p. 261), and Tliuret (1855, p. 17). Such facts as are
known about the details of development are found in Fttlkeuberg’s and Kylin’s descriptions
(1901 and 1923 respectively).
208
MISS VIOLE?
M. GRUBB ON THE
specimens, due possibly to the fact that they are as conspicuous as the female
and inore so than the tetrasporic thalli, and do not therefore give the
impression of being in the minority as in many species. The antheridial
plants can easily be distinguished by means of their fat swollen pinna tips,
due to the presence of embedded conccptacles with dense yellow contents ;
if in any doubt, a slight examination with a hand-lens will a t once reveal the
circular openings of these depressions, often with the tips of the antheridial
filaments showing within.
The antheridia are borne on axes lining the conceptacles. From the published figures it appears that the latter vary greatly in shape, some having
a wide opening and cup-like form, while others are contracted a t the apex,
leaving only a narrow entrance to the cavity. Both types of receptacle are
figured and described by Harvey (1849, pl. 55. figs. 4, 5 ) as being either
“ cup-shaped ” or “ urn-shaped,” the former apparently occurring on dwarf
plants witli broad, flat ramuli, which are distinguished as var. littoralis.
Kylin (1922, fig. S l a ) , however, fignres only the cnp-shaped type, evidently
regarding this as typical, since he mentions no other. On the other hand,
every male frond of the species examined by the writer has had conceptacles
of the urn-shaped form, with a contracted entrance leading to tlie swollen
cavity witliin (cp fig. 13).
The conceptacles have been shown by Hylin to be formed by rapid
growth of groups of cells around the apical cell of a pinna, the latter ceasing
to function and becoming carried down into a concave depression. A t the
same time, there is carried down a group of‘ hairs which devrlop from the
outer layer of cells at the apex of each fertile pinna, and these line densely
the whole internal wall and even the ostiole of‘ the conceptacle (fig. 13),
though fig. 81a in Kylin’s paper gives the impression that they only occur
along the floor of the latter. Those in the uppermost region remain sterile,
guarding the entriince, wliile the remainder form the axes around which the
antlieridial mother-cells and tlie antheridia are borne. These axes originally
consist of a single row of cells, but later they often become by division two
or more rows thick a t the base, and are terminated by two or three “ giant”
cells ; it is possible that these latter may be concerned in the extrusion of
the spertnatia from the receptacle. Lowia (1909, p. 656) suggosted that
in Grifithsia Bornetiana the spermatia are only liberated from the antheridia
when pressure is exerted on the cells of the thallus; his idea might be
extended to Lawencia, for when slight pressure is applied to the receptacles,
masses of spermatia contained in a drop of niucilage are exuded through the
ostiole. Probably this muci!atginous drop is obtained from the giant cells at
the tip of each antheridial filament, for in older receptacles, where the
majority of sperniatia havo escaped, these cells are found collapstsd and empty
of their ~nucilaginousyellow contents.
When fertile, according to Kylin, each cell of the upstanding axes cuts off
MALE ORGANS OF THE FLOHIDEE.
203
four pericentral cells, and these divide again several times so that the whole
axis is densely clothed with a number of pericentral cells (1922, fig. 816, c).
Each of these becomes an antheridial mother-cell and gives rise to a number
of antheridia. The mother-cells are pigmented and flattened in shape, with
broad bases which lie along the axes ; each one is said to abstrict three to
four antheridia. Observations show, however, that the usual number of
primary antheridia produced from a mother-cell is four, formed in regular
succession, no two being ever found in the same stage of development on one
FIG.13.
Photomicrograph of a longitudinal section through an aiitheridial conceptacle
of L a w e n c i a pinnatij?da. x 90.
mother-cell (fig. 14 a & b). When ripe each is a large, clumsy-looking
colourless body with a single apical nucleus, a central vacuole, aiid a little
peripheral protoplasni (fig. 14 d ) ; the surrounding wall swells considerably,
especially at the apex, and the contents are liberated as a single sperniatiuni
through a wide split at the top (fig. 14 6). While still within the antheridium,
the sperniatiuni has the appearance of being surrounded by a cloar transparent area which iiiight either be a u all or an empty space (fig. 14 a ) ; when
extruded the body is distinctly seen to be enclosed in a delicate gelatinous
204
MISS VIOLET M. GRUBB ON
THE
wall (fig. 1 . 1 ~) . The antheridial sheath which remains behind is often split
down to the base by the difficult exit of the fat spermatium (fig. l a d ) ,
which, when liberated, measures 7 to l o p in diameter; these sheaths are
apparently of a thicker consistency than in most other species, for on staining
they can be seen clustered over the axes and are very conspicuous. Kylin
makes no mention of the method of escape of the spermatium or of the
presence of antheridial walls; this rnay possibly be accounted for by the
fact that, judging from his figures, his work was solely done with the aid of
microtomed sections. But so resistant :ire the walls in this species that
it would appear impossible to overlook them even in microtomed sections.
Nor does the above-mentioned author give any indication that the first crop
Fro.14.
Development of the antheridia in Lawencia pinnatifida. x 1800.
a S: 6. Optical sections of an antheridial mother-cell, seen at high and low focus
respectively. The antheridia are numbered in order of development.
c. Single escaped spermatium showing the nucleus in prophsse.
d. Microtomed section showing the development of sntheridia and the nuclear stages.
of spermatia is followed by a later one, yet this is undoubtedly the case.
I n an oider conceptacle, within each empty antheridial sheath a new
antheridium can be seen growing up (fig. 14a); this passes through the
same stages as a primary one and, finally, in tlle same way, discharges its
spermatium. No signs have been seen of more than two antheridial sheaths,
one within another, indicating the production of more than two sets of
antheridia ; there seems no obvious reason why antheridial production should
MALE ORGANS OF THE FLORIDEE.
205
not continue through many generations of spermatia as in the Nemalionales
(see pp. 242, 245), but in this Rpecies, a t any rate, this does not seem to be
the citse.
In addition to the development of antheridia upon the outgrowing axes,
antheridial mother-cells :ire formed in large numbers among the liiyers of
cells lining the cavity of the conceptacle in between the antheridial filaments.
These mother-cells with broad bases are cut off from the iriner layer of cells,
and in exactly the same way develop antheridia in succession. Appearances
suggest that every cell lining the cavity is capable of producing mother-cells,
and this productive area is naturally much increased by the axes extending
into the centre. Also, since the mother-cells are not closely packed in rows,
as in Chondrus (p. 185), freedoin is allowed for the outgrowth of antheridia
all around them, large numbers of these bodies being developed by this
means in a conceptacle. Since ii single average-sized antheridial plant may
bear well over 200 conceptaales, it is evident that this species produces
a very large number of spermatia. As far as I am aware, there are
no records of the presence of the spermatia upon the trichogynes, though
Kylin, in his account of the development of the procarps (1922, p. 127),
apparently takes it for granted that a fusion of the speriiiatial with the
carpogonial nucleus actually occurs.
The cells lining the conceptacles and those of the antheridial axes are all
uninucleate ; the mother-cells also contain a single small nucleus, and this
divides a t the base of each projection, one nucleus passing slowly up the
young antheridium, the other returning to the lower end of the mother-cell.
When the antheridial nucleus is first cut off, it appears as a small darklystaining body showing no signs of granulation (fig. 1 4 d ) ; at the time
of escape of the spermatiuni this nucleus has greatly increased in size, and
lies at the apex of the antheridiuni as a slightly oval body about 2 x 2 ' 5 ~
in diameter ; it is then composed of a number of deeply-staining chromatin
granules or " Kornchen " connected together by delicate threads (fig. 14 d).
Kylin states that there are abeut twenty of these granules present in each
nucleus, and with this estimate I should agree, though, owing to the thickness
of the nuclei, it is difficult in most cases to make out more than 15 or 16.
On escape of the speriiiatium the cytoplasmic contents become rounded
off around the nucleus, the vacuole disappears, the nucleus occupying
almost the whole of the spermatium with the exception of the small peripheral cytoplasmic layer within the delicate wall (fig. 14 e ) . The changes
in structure from the nionient when the nucleus is cut off to the liberation
of' the spermatium were not all so clearly observed as in Furcellaria (p. 237) ;
it can, however, be seen that the nucleus first appears as a small homogeneous
body, later showing the well-known granules. This affords support to the
view that, when first formed, the nucleus returns to the normal resting stage,
only to pass immediately into the earlier stages of a further division.
206
MISS VIOLET M. GRUBB ON THE
(7) LAURENCIAOBTUSA * (Huds.) Lam.
Material consisted of, one plant gathered a t Primel, Brittany, in July 1924.
The antheridkt i n Lawencia obtusa have, since the days of Kutzing, been
known to occur in shallow open cups, a t or near the tips of the pinns.
These cups are densely crowded together, giving to the plant a tufted busily
appearance ; on examination with a lens many of them seem to be sterile,
but in others colourless clusters of ripe antheridia can be seen a t the wide
entrance to the conceptacles, and following the slightest pressure on the
latter these clusters are at once extruded as gelatinous masses.
The conceptacles appear to be formed in a similar manner to those in
Laurencia yinnatijidu, though their ultimate form is somewhat different,
being shallower, with a wide mouth, a t the entrance to which hardly any
contraction lias taken place. The inner walls are lined with richly-branched
hairs, some of which remain sterile permanently, while others give rise to the
PIG.
15.
n
b
Branched axes dissected out from an antheridial conceptacle of Lauremia obtusa.
x 600.
n. Fertile axis bearing numerous antheridia.
b. Short sterile axis.
antheridial mother-cells and antheridia ; about eight to twelve axes showing
this latter development are present in the ripe conceptacle. The sterile
hairs, which are apparently absent in the lower part of the conceptacle of
L. pinnatifida, show :I very bushy appearance (fig. 15 b j ; they do not grow
to the same length as the fertile ones, but remain in contact it11 the wall of
the receptacle, forming a close “ undergrowth.” The fertile hairs are made
lip of brancliing rows of long narrow cells, poor both in pigment and in
protoplasniic contents (fig. 16a). On these cells the antheridial motlier-cells
* The presence of Hntheridia in this species has been recorded by Kutzing (1845, pl. 55.
fig. d), Derbes and Solier (1856, p. 75), Harvey (1849, pl. 148), Buffliam (1893, p. 2931,
and Falkenberg (1901, p. 247).
MALE ORGANS OF THE FLORIDEB.
207
arise, the earliest formed appearing near the base of the nxis ; a progressive
development therefore takes place both in the mother-cells and the antheridia,
the base of the axis often being fully fertile, while the apex shows no sigii of
atitheridin; the axis is sometimes terminated by a swollen “ g i a n t ” cell, but
this does not invariably occur (fig. 16u). The antheridid mother-cells are
cnt off as single small pericentral cells around the axial cells, sometimes
occurring opposite one another, bilt often being scattered, or even terminating
a branch (fig. 16 u ) ; in any case they are comparatively small, uninucleate,
and poorly pigmented. From each mother-cell two primary antheridia are
FIG.16.
a
Development of the antheridia in Laurencia obfuaa.
a. Apes of an antheridial filament terminated by R, “giant ” cell. A single antheridium
has developed on a mother-cell (right). x 1200.
b. Lower region of the same filament ; the mother-cells bearing ripe untheridia. x 1200.
c. Apex of an older filament, showing empty sheaths (above) through which the primary
spermatir have escaped. x 1800.
formed, following one another very closely and appearing almost a t the same
stage of development (fig. 16 f)). They arise in the usual way as protoplasmic
Outgrowths, clothed in the mother-cell wall, by thc ingrowth of which they
are alstricted. They then swell rapidly, the wall always remaining rather
thin, but the sperniatium becoming almost spherical and about 6 to 9 p in
208
MISS VIOLET M. GRUBB ON THE
diameter. A t this stage a branching filament covered with ripe antheridia
is almost visible to the naked eye, and strongly resembles a miniature cluster
of grapes (fig. 15 a). The gelatinous walls are soon split by the swelling of
the spermatium, and the latter escapes, clothed in a delicate membrane
and leaving behind it the tough antheridial wall (fig. 16 c ) . Secondary
antheridia arise within these sheaths, developing and forcing their way out
in a similar manner; it is noticeable that a t the time of exit of the first
spermatium there is no sign of the second, this appearing later. Anything
beyond two antheridial sheaths, one within the other, has not been seen.
As in Laumncia pinnatifida, the cells of all the branching axes and the
mother-cells are uninucleate. The behaviour of the antheridial nucleus is
exactly similar in the two species, there being apparently rather fewer
granules ultimatoly formed in L. ohtusa. Owing to the fact that the only
available material was not well fixed for cytological details, the exact number
could not be counted
It will be seen that the chief difference between the two species lies in
the structure of the antheridial axes and the rediiced number of antheridia
in L. ohtusa. I n the latter, antheridial mother-cells are not formed from
the cells which actually line the conceptacles, but only from the cells of the
filalnents ; even all these are not fertile, whereas in L pinnatijda there are
normally no sterile axes except around the ostiole. Again, four antheridia
develop from each mother-cell in L. pinnati@a and only two in L. obtusa ;
there is therefore a considerable reduction in the number of antheridia
formed in a conceptacle in this latter species, though in other respects the
structure is substantially the same. It is interesting to note that in
Ckondria tenuissinza Grev., a species formerly included in Laurencia, the
position of the antheridia is entirely different, since they arise all over both
surfaces of cellular structures h r n e on the side branches (Thuret, 1851) ;
there is here no sign of the characteristic conceptacular development of the
Laurencieze, and, working on the grounds of antheridial structure alone, one
could fully support the removal of this species to a separate genus.
.
(8) POLYSIPHONIA
FASTIGIATA * Grev.
Material was obtained from Shanklin, Isle of Wight, and Plymouth in
February and April 1924 respectively.
The male plants, which on the south coast are found in the winter and
the spring, can be identified in the field by means of their bushy yellow
apices, consisting of clusteis of antheridia (fig. li).
The antheridia are produced around specially developed multicellular
axes, four to eight of which occur at each apex. In the young plant, where
* The presence of mtheridia in this species ha&been noted by many, among them
Ellis (1767), Lightfoot (1777), T h u d (1855), and Buffhani(1884). No detailed description
exists.
MALE ORGANS OF THE FLORIDEI.
209
the branching exhibits apparent dichotomy, each branch is terminated by a
single apicirl cell. On the formation of the antheridial axes, these apical
cells divide- longitudinally several times, each cell thus formed constituting
the initial for the fertile axis. From each of these initials, six or eight cells
are cut off in a single row ; the cell-walls are all gelatinous in character
and form a resistant '' cuticle " around the axis.
811 these axes become fertile, none forming sterile hairs as in PoZysiphonia
nigrescens (Kylin, 1922). The two basal cells of the axis do not develop
further, but from the remainder a variable number of pericentral cells are
FIG.17.
Photomicrograph of the apex of PoZysiphonia fastigginta bearing clusters
of ripe antheridia. x 60.
cut off, approximately eight to each mother-celI. From these there are then
cut off laterally several ant,heridial mother-cells connected to one another by
In-otoplasmic threads (fig. 18 u). The cells are SO closely packed together
that their swollen walls are fused laterally, while the whole is still clothed
externally by the solid comnlon gelatinous investment, often infested with
minute epiphytic filament,^ and diatoms.
'rhe antheridia develop as protoplasmic protuberances from the mothercell. The first sntheridium arises laterally as a narrow outgrowth forcing
210
MISS VIOLET M. GRUBB ON T H E
up the layer around the mother-cell through the coinmon
cuticle.''
The
contents are abstricted by the ingrowth of the surrounding wall, and when
ripe lie as a nearly spherical body within the antheridial wall (fig. 186).
This latter shows two distinct layers, an outer denser one and a middle
swollen one, while around the sperniatium is a clear refractive area
(fig. 18 b & c). On the escape of the spermatiuin this area is seen without
"
FIG.18.
C
hntheridial development in Polys+homa .fustigiata. All x 1200.
Part of a longitudinal section of an antheridial cluster, showing the ceutral axis,
pericentral cells, and antheridid mother-cells giving rise to antheridia at the
periphery.
b & c. Stages in the development of antheridia.
d. Part of an antheridial cluster seen from above ; antheridia are in groups of three.
a.
doubt to be a delicate wall enclosing the contents. It is noticeable that these
areas are not present when the antheridiuin it still young, but only becorn@
MALE ORGANS 01’ THE FLORIDEa.
211
visible as the-body attains maturity. When in this position the antheridium
has increased in length to such an extent that it has now pierced the
“ cuticle” (fig. 18 b ) ; the wall then splits a t the apex and liberates through
the aperture the whole contents as a single rounded body.
Meanwhile both a second and third lateral antheridium have been
developing from the apex of the mother-cell, following the same stages
(fig. 18d ) . B y the time these are mature, the first spermatiuin has escaped,
and the mother-cell then exhibits one empty antheridial sheath and two
innture antheridia enclosing spermatia. These are then discharged successively.
The difficulties of technique in dealing with the antheridia of Polysiphonia
are so great that it is difficult to say whether secondary antheridia are
developed in the place of the primary ones. It is, as explained above,
impossible to employ microtomed sections, since in them no walls can be
clearly made out ; hand sections or an examination of the whole cluster is
necessary, and eveii then it is not easy lo determine whether an observed
spermatium is a primary or secondary one. However, in some clusters
where spermatia have not yet beeu all discharged, it is possible to find
single empty sheaths which are tlie walls of the primary antheridia, and
within them there is apparently no sign of :I new upgrowing antheridiuin
(fig. 1 8 b ) . This would point to there being no production of secondary
antheridia, a conclusion hardly to be expected, since the secondary tfevelopment is so common in the Plorideze ; on the other hand, it has never been
noted for any species of Polysiphonia.
The cytology of this species appears to follow the usual course exhibited
by members of the higher Floridet3+ such as that already described for
Laue*encia pinnat{@z (p. 205). The noth her-cell is only slightly pigmented
and is uninucleate, the nucleus moving to the base of each mtheridium and
there dividing. The daughter nucleus, which passes into the spermatium,
moves t o the apex, where it remains suspended by a small amount of
cytoplasm above the central vacuole. Details are difficult to make out, but
sufficient could be seen to show that the nucleus is in prophase a t this time,
though the granules could not be counted. The spermatium on liberation
is 1;trge and measures about 9 by 5 p , while the nucleus is 2 to 3 p in
diameter.
(9) POLYSIPHONIA
VIOLACEA * Grev.
Material was collected by Dr. E. M. Delf in August 1924 a t Sark.
The antheridia are developed in pale yellow clusters at the apices of the
filaments; to the whole cluster Yamanouchi gave the name of a n “antheriditun,” calling the escaping cells “ sperins.” Each cluster is i n reality a
* Antheridia are described by Yaiiianouchi (1906, p. 409) and mentioned by Rosenvinge
(1923).
LINN. J0URN.-BOTANY,
VOL. XLVJI,
R
212
MISS VIOLET Y. URUBB ON THE
ahorf branch, every cell of which, with the exception of the two lowermost,
is fertile. The two sterile cells form the stalk, the upper one giving rise to
a sterile hair, often branched (fig. 19).
I n the development of the antheridial cluster, Yamanouchi states that the
central axis “ becomes surrounded and covered by a number of small cells ” ;
these are the pericentral cells, and each one is said to subtend a single
antheridial mother-cell, though appearances suggest that more than one is
FIQ.19.
n
Part of the apex of an antheridial plant of Polyeiphonk uiolacea, showing antheridial
clusters with the accompanying sterile hairs. x 70.
borne by each pericentral cell, as in the case of P.fustigiatu. The mothercells when mature are not so closely packed as in the latter species, and it is
therefore easier in some ways to make o u t the structure.
The antheridia are produced as the result of a lateral elongation of the
mother-cell. This elongation is surrounded throughout by the gelatinous
wall of tho latter (fig. 2Ob), though this, of course, cannot be seen in a
microtomed section (cp. Yamanouchi’s figures, 1906, pl. 22. figs. 62-81).
while still short and narrow the young antheridium is abstricted at the base
MALE ORGANS O F THE FLORIDEB.
213
by the ingrowth of the surrounding wall. I t then increases greatly in size,
swelling and becoming spherical, the wall at this stage showing two layers,
the inner one being strongly marked and separated from the central
protoplast by a clear refractive area. The antheridia are borne around the
periphery of the outer surface of the flat-topped mother-cell (fig. 2 0 a ) ;
this can clearly be seen if viewed from above, when the antheridia appear
to be level with the apex of the mother-cell. Such a surface view of the
FIQ.20.
b
. .__._.
.
.
I
The developmeut of antheridia in Polyr@honin violaera.
Surface view of an antheridial cluster, with the autheridia in groups of four and five
around the mother-cells (dotted). x 1200.
b. Mother-cell bearing antheridia, seen at two different foci. x 1800.
c. Periphery of an antheridial cluster, showing the empty sheaths after the escape of the
spermatia. x 1800.
d. Surface view;of an old antheridial cluster, showing the mother-cells surrounded by
apertures through which the spermatia ha.re escaped. x 1800.
a.
structure was apparently not seen by Yamanouchi, or he could hardly have
stated that only two or three antheridia were produced from each mothercell, since four (or sometimes fire) primary antheridia can regularly be seen
(fig. 2 0 ~ ) . The arrangement of these four is perfect in detail, for one can
see that :the secondi:always arises a t the opposite corner to the first, the
third and the fourth developing between them (fig. 20a) ; in this way space
R2
214
MISS VIOLET nl. GRUBB ON THE
is allowed for the first two antheridia to swell and discharge their contents
before the alternating two have fully developed. The resemblance atj this
stage to a four-spored basidiuin cannot fail to st.rike the observer, particularly
since the sperinatia until quite ripe are attached to the mother-cell by a
protoplasmic extension, which after the release of the speriiiatium reniains
as a short projection similar to a sterigma. Liberation of { h e spermatium
takes place without doubt by nieans of a split in the apex of the antlieridial
wall, which by now bas stretched to the periphery of the surrounding
'(cuticle " (fig. 20 e) , a point entirely overlooked by Tamanonchi, who
concluded from his study of microtonied sections that the whole body was
cut off and liberated as one (pl. 22. figs. 72, 73), . In ail old antheridial
cluster it is possible with a high magnification and very carefully adjusted
illumination to see the " cuticle " traversed it! every direcation by wriiikled,
empty antheridial sheaths (fig. 20 c ) , still showing a swollen outer iayer and
a more deeply-staining inner region. Evidently t.he pressure exerted by the
spermatium in exit upon the resistant " cuticle " is great, for in surface
view each mother-cell crtn be seen to be surrounded by four, or sometimes
five, little pores or slits leading to the empty sheat'hs below, each pore h i n g
much smaller than the diameter of a spermatiuin and having apparently
contracted after the liberation of the latter (fig. 20 d). The sperniatia when
free measure about 7 to 9 p in diameter ; the contents, consistring of a single
nucleus suspended by strands of cytoplasm above a large vacuole, are
surrounded by a very delicate wall. NO evidence was obtained that
secondary antheridia are formed ; clusters can be found with the mothercells i n the upper regions entirely surrounded by empty primary antheridial
sheaths, while in the lower part t'he priniary sperniatia are still being
discharged. There is no sign in the npp,er region in t'hese cases that
further antheridial development will ever occur (fig. 20 d ) .
The cytology of the antheridia has not been re-invest,igated.
Altliougli the genus Polysiphonia is so widespread, detailed descriptions
of the antheridia exist only in three cases-those of P. violacea (Yamanouchi,
19OS), P.nigrescem (Iiylin, 1922), and P.fastigiata (this paper). I n each
case the general position and structure of the antheridia agree, though there
is some difference as to details. Antheridia in the whole genus appear t o be
developed in terminal, subterminal, or lateral clusters, these usually being
modified hairs. I n the three described species tlie fertile axis of the cluster
is subtended by two cells which remain sterile and may produce axil1:iry
branches. Around the axis, periaentr:il cells are formed in varying numbers,
giring rise by division to one or more mother-cells which in all cases
are small, uninucleate, and colourless, 01' only slightly pigmented.
In
p.izigrescens Kylin's account iniplies that another row of cells is iiiterposed
between the antheridial mother-cells and the pericentral cells, the latter
being comparatively few in number. It is, however, in the descriptions
M A L E ORGANS O F THE FLORIDEB.
215
given of the production of the spermatia that tile details fail to agree.
According to Yamanouclli, two or possibly three " sperms '' are constricted
off obliquely from the motlier-cell in P. wiolacea, and eTren in discharge they
'' retain the parent cell-wall.JJ The developinent in P.nipmeens is said by
Kylin to be similar to that which he had previously described lor Rhodomela cirgata (1914). It1 this he definitely st:ites that the sperniatiuin escapes
out of its surrounding sheath, this being left behind 011 the plant. The empty
antheridial wall is not, however, figured either for Rhodomela or P. nigrescens
(1922, fig. 77 L',dj, the tigures for the latter leaving on0 to presume that the
wliole antlieridiuin is cut off a s a single separate cell. It is true that in any
species of Yolysipkonia empty antheridial walls would be difficult to see
owing to the thick surrounding " cuticle," but in both P. fastiyiata and
Y.eiolacea they can be made out with certainty wheii the magnified
structure is exaniined in a suirable light. In liew of the fact that the
tlischarge of the spermatiuin froin the antheridiuin seems to be the usual
method of liberation in the Floridez and not the cut,ting off of the whole
body, it would be of special interest if any species of Polysiphonia differed
in this respect.
(10) GRIFPITHSIA CORALLINA * (Lightl't.) Ag.
Material consisted of two plants gathered on Slianklin Ledge, February
1924.
The antheridial fronds can be recognized in the field and easily distiuguished froni other .fertile inaterial of this species. Those gathered were
small-not niore than 2.5 cin. in height-though apparently fully developed ;
on them the antheridia are visible as colourless areas encircling the upper
constrictions of the articulations (fig. el),' these paler regions forming a
striking contrast to the otlierwise deep red colour of the plant. Tile antheridia
occur only a t the younger nodes, forming whorls arouiid the second, third,
and fourth constrictions (fig. 21). The thallus, which is sttached basally by
liieaiis of creeping rhizoids, is dichotomously branched a t irregular intervals,
rind is made up of single rows of elongated inflated cells from 1to 2 niin. in
length ; these are niultinucleate, with the liuclei and small round plastids
arranged around the periilhery. The wliole is enclosed in a very thicli twolayered gelatinuus " cuticle," which is risible to t,he naked eye and imparts
to the thallus its characteristic slimy feeling ; the inner layer is thin and
delicate, sheiirhing the cells j the outer one thick a n d resistant. This
6 ' cuticle" is contracted and thinner a t the nodes.
The antheridia are borne :it the apices of long richly-branched axes,
extending a t right angles to the surface of the thallus, und united by the
gelatinous matrix in which they are embedded. An antheridial axis first
* The presence of antheridia is mentioned by Thuret (18%) and Buff'ham (1884).
Guignard (1889) and Kylin (1916a) give short deccriptiuns of the structure.
216
MISS VIOLET M. GRUBB ON TEE
appears as a single cell which apparently arises as a protuberance froni a
thallus cell. In the earliest stages shown by the material the axis is
represented by a large round uninucleate cell connected with the thallus by
an elongated gelatinous wall (fig. 2 3 a ) . From this, six to eight cells one
above the‘other are cut off, more or less in a straight row, forming the
central axis of the antheridial branch (fig. 23 c). These increase greatly in
size, becoming multinucleate and when innture containing as many as ten
to twelve nuclei (fig. 22) ; the antheridial branch is approximately -1mm.
in length (fig. 22). Meanwhile around each of these central cells a number
FIG.21.
Portion of s n sntheridial plant of Graj’ithsin corallinn, showing the position of the
antheridial filaments. x 6.
of pericentral cells have been cut off in every direction, often as many as
ten to twelve being formed from each main cell, each containing two to
three nuclei (fig. 2 3 b ) . From the pericentral cells are cut off’ a further
series of cells, many of which grow out into short branches bearing at their
apices antheridial mother-cells, others however by their next divisiorl
giving rise to immediately mother-cells (fig. 22). At the same tirne it is
to be noted that occasionally antheridial mother-cells arise directly npon the
pericentral cells, or even, in the younger regions, upon the central cellJ,
though Kylin does not mention this in his short description ; both the mothercells and the antheridia are uninucleate (fig. 22). All these cells, with the
pvception of the antheridia are pigmented, but in nearly every case such
MALE ORGANS OF THE FLORIDEX.
217
dense granular contents are presont that the position of the plastids and, to
some extent of the nuclei is obscured. Typically, therefore, each of these
antheridial branches consists of a distinctive central axis surrounded in
every direction by pericentral cells, which agaiti in rriost cases give rise to
further cells, on which, sooner or later, the antheridial mother-cells and the
antheridia are botne (fig. 22). It is evident thitt i n this somewhat peculiar
structure there is no very regular rule of development, but the antheridial
FIG.22.
Single antheridial branch from a fertile node of Grilgthsiu corallina, showing the attachnient
to the thdlus and the development of lateral axes. X 1200.
mother-cells may be found growing out from central, pericentral or higher
orders of cells.
The antheridid mother-cells are uninucleate and contain a few poorlydeveloped plastids, the whole being surrounded by a gelatinous wall which
is thicker than that of the other cells of the aiitheridial branch ; like other
Florideaii cells, these remain in communication with the cell from which
they are cut off by ineans of a protoplasmic connection. Each mother-cell
218
1\II88 VIOLET M. GRUBB ON THE
gives rise to two (fig. 24 b ) and sometimes three (fig. 24 a) antheridia. These
are formed successively as small colourless sub-terminal projections from the
mother-cell, forcing upwards the gelatinous wall (fig. 24 u). The projections
are abstricted at a point level with the original apex of the mother-cell by
the irigrowth of the wall, leaving no apparent protoplasmic connection
between the two cells, and the contents then lie as slightly elongated bodies
within the young antheridium. When mature, the spermatium, which is
formed from the whole contents of the antheridiuni, consists of a large
colourless body, about 6 by 4 p in diameter, with an apical nucleus suspended
in a little granular cytoplasm, and a large vacuole below ; the wall surrounding the whole is very thick and shows signs of layers within it, while
FIG.23.
a
Three stages (a, b, and
c)
in the development of the antheridial axis of Gvifithsia corallinu.
Plastids omitted. x 1200.
iuimediately around the spermatiurn is a clear refractive area (fig. 2 4 b ) .
It is impossible to say with certainty at this stage whether this is an empty
sljace in which the spermatium is lJing, or whether it represents a very
delicate wall surrounding this body; but the latter suggestion is supported
by the fact that immediately after the apex of the \fall of the antheridium
splits and the spermatium is liherated, the latter can be seeu in the surrounding
medium as a spherical body enclosed in a very delicate but unmistakable
gelatinous wall. The question as to whether there is any secondary
antheridial development in this species is difficult to decide ; Kylin rnakes
no mention of any such development, implying that it does not take place.
21.9
MALE ORGANS OF THE FLORIDEB.
On the other hand, the only remark that Guignard has to make with regard
to this species is that a second antheridium grows up within the sheath of the
first, and he illustrates this with a very convincing figure. Unfortunately my
material was too young to be decisive, a s in only a few cases had the
primary spermatium been discharged ; there are signs, however, that a
secondary antheridium might develop (fig. 24 a, right), and in view of the
common occurrenc~of secondary antheridiit among the Floridc one would
expect it.
FIG.24.
a
d
Antheridia of Graj$thsiir cornllina.
x 1800.
a & b. Hand preparations, showing the development of the antheridia.
3Iicrotomed sections, Phowing the nuclear construction of the antheridia
and mother-cells.
d. Escaped sperniatium.
c.
Although the nuclei of the ripe syermatia are sniall-about 1.9 to 2 . 2 ~
in diameter-yet the details were fairly clear. On the formation of a young
antheridium the single small nucleus of the mother-cell n i o ~ e sto the babe
of the projection and there divides (fig. 2 4 ~ ) . The details of this division
can be observed, but owing to the small size there is difficulty in counting
the number of chromosomes. One daughter nucleus moves upward into the
antheridium, the other back into the mother-cell, where it remains until it
2 20
MISS VIOLET M. ORUBB ON THE
again passes to the base of another projection. The antheridial nucleus is
seen ae a large densely-staining body, which during the ripening of the
spermiitium inoves gradually to the apex and is there suspended by very
delicate protoplasmic threads. While still i n the bas0 sf the spermatium,
it is difficult to make out any structure, for it either stains a homogeneous
deep purple with hrematoxylin, or else loses the stain altogether. Half-way
up the spermatium the nucleua can be seen to consist of very delicate linin
threads, at the angles of which are small densely-staining bodies-the
granules or " Kornchen." When the nucleus is at the apex, the granules
are slightly larger and appear to be about 10 in number; appearances,
however, in certain cases suggest that the number is probably greater than
this, 13 or 14 being perhaps more correct ; the linin network is still present,
and though no nucleolus is visible the nuclear membrane can always be seen
(fig. 24 c ) . The nucleus is in this condition when the sperrnatium is liberated
(fig. 2 4 d ) .
(11) HALURUS
EQUISETIFOLIUS* Kutz.
Material was found both attached and among drift a t Shanklin, February
1924.
The antheridia appear to develop in the spring i n the south of England.
The inale plants are easily recognizable with the aid of a lens or even with
the naked eye, for the antheridia are borne clustered on the incurved ramuli
of small, pale pink involucres of whorled branches, which are developed
laterally on the lower part of the main stems or branches of the plant ; these
involucres are conspicuous, and, when examined closely, are seen to have
white patches in the centre, caused by the bunches of colourless ripe
spermatia (fig. 25).
The vegetative plant of H. equisetifolius consists of a main filamentous
stem, much branched, bolh stem and branches being composed of a single
row of multinucleate, pigmented cells enclosed, as in GriJithsia corallkna,
in a thick gelatinous " cuticle." The junctions of these cells, more especially
in the younger parts of the plant, are densely clothed with whorled filaments,
which are incurved and branched; towards the base of the plant the whorled
character is lost, and the whole stem appears to be covered indiscriminately
with short cellular filaments. On the formation of the antheridial involucre,
a thick, nearly colourless, lateral branch arises from a main or lateral stem
a t the point of departure of an involucre ; this branch develops at its apex
one or more whorled involucres on which the bunches of antheridia arise
(fig. 25).
~f any confirinatory evidence of the close relationship bet ween G. coralha
alld H. equisetifolius were required, it could be found in the unmistakable
Similarity of developnient and construction of the antheridial bunches in the
* Antheridia previously noted by Harvey (1849, pl. 67) and Chemiu (1923).
MALE ORGANS OF THE FLORIDEB.
221
two species, those in H. equisetqolius being somewhat smaller and simpler.
The antheridial filament arises as a lateral outgrowth from one of the cells
of the iavolucral branches ; this outgrowth, which is ~nultiniicleate and
pigmented, is cut off as a single cell always remaining enclosed in the
FIG.2.5.
Outline drawing of R €atera1involucre of Hulurw equisetifolius bearing antheridial branches.
The main axis with a whorl of branches is indicated. x 75.
FIG.26,
Outline drawing of a small portion of a lateral involucre of H. equisetifolius, showing a
young antheridial bmich in process of development. x 900.
gelatinous " cuticle " of the vegetative cell and in protoplasmic coniiection
with the latter. By division a short nntheridial filament is formed, generally
composed of not more than four cells (fig. 26) ; from these, about four to
222
MISS VIOLET M. GRUBB ON T H E
eight lateral cells, apparently always uninucleate, are cut off a t right angles
all round, and these give rise, by further divisions, to numerous small
interlacing branches, composed of short rows of slightly pigmented unincicleate cells, the whale of this structure forming a single bushy antheridial
group and measuring about *08of :I nnn. in diameter (fig. 26). Any cell of
the lateral Lranches of this 'antheridial group appears able to function as a
mother-cell and to give rise to antheridia, but only the three or four upper cells
generally do so (tig. 27 a & 6). This is i u contrast to G. corallina, €or here
only the terniinal or lateral cells borne on the filaments become mother-cells,
and never the intercalary cells of the filaments ; indeed, were the structure
not unmistakable in H. epuiseti/oZius, one would doubt the point, sitice in
Other Floridez described the antheridial mother-cells appear always to be
borne terminally. These mother-cells are very prolific, often giving rise in
the normal manner to four primary antheridia, while secondary ones are
developed successik ely within the empty sheaths (fig. 27). The antheridia
FIG.27.
The development of antheridia in Halzwus epuisetifolius.
x 1800.
a &, b. Drawings a t a low and high focus respectively of two terniinal cells of an antheridial
branch produciiig successively primary and secondary antheridia. These are numbered
c.
in order of development.
Development of secondary antheridia within the enipty sheaths of the primary ones.
I
when first formed are long and narrow, rapidly broadening out and assuming
the oval shape, with the large central nucleus suspended by cytoplasmic
threads. The antheridial wall is i n this case very thick, and when ripe it
distinctly shows a definite outer la) er (fig. 27 6), to whicll filainentous growths,
diatoms, etc. are often firmly attached. M'ithin, there is a clear area around
the sperinatium, and the latter when issuing from its sheath quite obviously
pOSSrSSeS a thin wall. When mature the body is before liberation about.
7 x 4 p, the nucleus :itt;tining a diameter of approxiinately 2 p.
The cytoldgicul details were difficult to make out, owing to the extremely
sinall size o t the nucleus and the difficulties inherent to such filaiiieutous
Illaterial. No stages i n the division of the mother-cell nucleus could be
found, though tliis apparently takes place in the usual manner, atid the
nucleus of tile sperinatium was only seen when the latter was about to
223
MALE ORGANS OF THE FLORIDEB.
escape ; a t that time the nucleus was composed of numerous staining
granules about, 10 in number, connected by delicate threads.
On comparing the structure of the antheridial filaments and the development of the antheridia i n the three species G. Bornetiajia Farlow (Lewis,
1909) (= G. globVera (Harv.) J . Ag)., G. corallzna (p. SlS), and H. eqirisetijolius, one finds that there is a considerable likeness. I n all three the
antheridia are borne on special antheridial branches, though in one case
these filainents are found covering the apices of the terminal cells of the
plant ( G . Bornetiana), in another confined to whorls at the nodes (G.
eorallinu), and in the third ssnttered a t random on special involucral
branches. The branches are iiiost strongly developed in 8.eorallina, where
they grow to be as long as -1 niin. and are very bushy and interlaced;
in H . egziiset$oZius they do not attain to inore tlian *08 min., while in
0. Bornetiann, though no measureinelits are given, they appear to reiliain
quite small, only being made up of the original primary cell, which buds off'
secondary cells, from which the motlier-cells are directly dei ived ; the
bushy ihterlacing habit is to a large extent loqt here. The different positions
of the antheridial mother-cells in the two species investigated have already
been noted, while in G. Bowzetiana these are always termiiial 011 the single
cell of the seconclary branch. The mother-cell in each case produces two or
threo antheridia, though four occur in E. equisethfolius. Secondary antheridia
are only definitely noted for the latter species, thougti probably occurring also
in G. corallinn. No mention of them is made in G . Bornetiana ; indeed, the
figures and descriptions lead one to believe that in thiq species the whole
primary antheridium breaks off and ewapes, n n assumption which would
probably require modification on further investigation. The spermatia, too,
are very small in G . Bornetiana, being orily 3 x 2 u
, ; their cytology is
unknown.
(12) UALLITHAMNION
BRACHIATUM * Bonnem.
Material was collected froin Freshwater, Isle of Wight, April 1923.
Mention has been made in algal literature of the discovery of inale plants
in no less than 13 species of Callithamnioiz, and in nearly all cases the
position of the autheridia as lateral bunches of cells horne on tlie upper
branches has been noted, though in
tetl-icum they are said to be <' almost
terminal " (Buffham, 1884), and in the closely related PtiZotAamnion yZunza
they are completely terniinal on the upper pinnae. So far as is known, the
structure of the collection of antheridia in each species is strikingly similar,
always appearing as a more or less spherical buiich of sm:ill cells &?thered
round a pedicel, while from the outerinost ones colourless bodies escape.
c.
# Thuet (1855) first saw antheridia
description of then].
ill
this species, and Buffham (2884)gave
t~
slight
224
MISS VIOLET M. QRUBB ON THE
The groups of antheridia of Callithamnion brachiatum do not, at first
sight at any rate, appear to show any serious deviation from what may be
regarded as the normal construction in the genus. The bunches of pale
cells are situated laterally on the upper crowded branches which terminate
each shootifig. 28). Often every cell can be seen giving rise to clusters,
the youngest of these being nearest to the pointed apex of the branch (fig.29).
At other times only a single bunch of antheridia will be found on a branch,
and possibly no others near it. A matuie cluster measures approximately
4Op in diameter, and in consequence of its small size and the absence of
other distinguishing features it is impossible to detect the antheridial plants
without the aid of a microscope. To the difficulty of ready recognition
FIG.28.
Outline drawing of a group of terminal pinnae of Cnllithnmnion brcrchiahm
bearing antheridial bunchea. x 225.
may possibly be due tho apparent scarcity of the plants, though this may
also be partially accounted for by the probability that after discharging
their function the useless antheridial bunches fall off and the plants appear to
be sterile. At the same time, there is some ground for thinking that fewer
male plants are actually developed than either female or tetrasporic. I n connection with this it is interesting to note that antheridia in this genus only
appear to be found, a t any rate on the south coast, from April to September.
Such statements as exist, record the presence of spermatia in April and
August, but it is not clear whether there are two distinct seasons of development-spring
and autumn-or
whether the antheridia are produced
throughout the whole summer,
MALE ORGANS OF THE FLORIDEB.
225
On close examination the bunches of antheridia in G. brachiatunt are seen
to exhibit a definite structure, for they are each borne on a pedicel composed
of three or four cells, the basal one of which is larger than the others,
and therefore more conspicuous. This pedicel arises, like the main axis in
HaZurus equisetifolius, as a single cell, cut off laterally from a cell of the
vegetative branch and enclosed in the common gelatinous wall of the latter
(fig. 29) ; in some cases a vegetative cell may give rise to two of these
pedicel cells, and two bunches of antheridia ?re then developed. The basal
pedicel cell then divides transversely, giving a row of three to four cell$
forming the main axis of the bunch, and each of these cuts off around it
about four cells (fig. 29) ; these are, of course, always in protoplasmic
FIQ.29.
Outline drawing of R branch at the apex of a shoot of CaUithamnion brachiatam, showing
stages in the development of bunches of antheridia. x 760.
connection with the central axis. The secondary cells divide at least once by
a transverse wall and sometimes twice, giving very short branches of two to
three cells, the terminal ones forming the antheridial mother-cells (fig. 3~ a).
The whole of this structure is enclosed i n R common gelutionous wall
derived from the original vegetative cell.
The antheridial mother-cells are, in appearance, very similar to the other
cells of these small branches, except for the somewhat thicker gelatinous
walls at the apex. Each mother-cell puts out a thin narrow protuberance,
forcing up its wall (tig. 30) ; this protuberance is abstricted by the ingrowth
226
MISS VIOLET M. URUBB
ON TKE
of the wall at the base, and the first antheridium thus formed is an elongated
body with protoplasmic contents, niuch swollen at one end and pulled out to
a tail at the other, the whole being enclosed by a very thick two-layered wall.
Gradually the antheridial contents hecome rounded off and swollen ; the
wall shows signs of strain ; a split appears a t the apex, and through the
hole the spermxtium escapes, passing through the surrounding thin gelatinous
Development of anthe4dia of Callithamnion hmchiatum.
x 1800.
a. Part of an antheridial bunch premed flat by the weight of the cover-alas$.
6. Two antheridial mother-cells, each with three sets of empty antheridial
she8ths. Secondary (left) and tertiary (right) antheridia developing.
c. Antheridid mother-cell giving rise to a tertiary antheridium.
d. Formation of a secondary antheridium.
matrix. No sign was seen of the little caps described and figured by
Guignnrd for C. roseurn (1889, pl. 6. fig. 2) and said to open at the apex of
the aiitheridium, allowing the spermatium to escape. The spermatium, which
itnmediately after liberation is about 3 X 5 p in size, is surrounded, a t any
rate when free, by an exceedingly delicate refractive wall (fig. 3 0 ~ ) . The
227
MALE ORGANS O F TEE FLORIDEB.
tough antheridial wall is either left standing as a sheath, or, when the strain
is released, it springs back and is seen as a wrinkled collar above the mothercell (tig. 30d). This production of primary antheridia is repeated three
times from different points arouiid the apex of most mother-cells (fig. 30 b) ;
in some cases only two primary antlieridia appear to be present, but it is
probable that this impression is due to the impossibility of cutting handsections and to the antheridia overlying one another. Immediately
following the production of primary antheridia, the development of the
secondary ones takes place in exactly the same sequence as was followed by
the first. Within the empty antheridial sheath grows up a small protuberance,
enclosed in a thick gelatinous wall (fig. 3 0 d ) ; this soon extends beyond
the shrunken sheath, which appears as :I collar around its base, and the
spermatium ripens rapidly and is discharged as before. Clear evidence was
:~lsoobtained in this species that a tliird crop of antheridia is developed within
the eiiipty sheath.: of the two previous (fig. 30 c) ; tertiary antheridia, thougl,
sometimes suspected, have not been noted iri any other species of the liiglier
FlorideE to the writer's knowledge. No sign o f more than three sheaths,
one within the other, could be found (fig. 30 c).
It is quite evident that, apart froin minute details, the nuclear structures
follow the usual course of behaviour. Apparently each cell of the
antheridial bunch contains a single nucleus. I n the antheridial mothercell this can be seen to move to the base of each protuberance, and there
presumably it divides, since a single nucleus is found in each young
antheridium, and the mother-cell nucleus has returned to the base of the
cell. I n the ripe spermatium the nucleus is about 2 to 3 p i n diameter,
and while still retained in the antheridium, it forms a band across the
centre, being suspended in this position by'strands of cytoplasm which
surround a large vacuole. When, on liberation, the spermatium becomes
spherical, the nuclens lias a completely central position. Of lhe internal
structure of the nucleus, no details can,be seen without microtomed sections,
and these, owing to shortage of material, were not available. The pigmeiit
present in the cells of the branches which subtend the antlieridia is iery
slight, though plastids can be observed : the whole structure has, when
fresh, a very pale pink appearance j in the antheridial mother-celis the
pigment is almost lacking, and in the antheridia there is none.
The resemblances between the bunches of antheridia in Callithamnion,
Grifithaia, and Haluvits could hardly be overlooked. I n all cases the
antheridial bunches arise as lateral outgrowths from vegetative cells and
take the form of a central axis surrounded by secondary branches. I n
G . Boirzetiana (Lewis, 19OY) this axis is said to be reduced to a single cell,
bearing the secondary branches at its apex ; in the species of Callithamnion
above described it consists of three to four cells, and in G. corallina,
G . setacea (Thuret, 1851), and H . eqziisetifo2ius of a large number. The
IJNN. J0URN.-BOTANY,
VOL. XLVIT.
S
228
MISS VIOLET M. GRUBB ON TEE
branches vary in length, in GriffithsiaBnrizetiana often consisting O ~ J of
- the
single antheridial mother-cell, in Cullithamnion byachiaturn having one or two
cells interposed between this and the main axis, and in the other two species
of Griflthsia and H. equisetifolilcs being composed of a considerable number.
The whole of this bushy structure appears to be, in each case, embedded in a
gelatinous matrix derived from the gelatinous walls of the vegetative cells.
Secondary antheridia probably occur in’ all the above-mentioned species,
though tliere is no record of tlieir development in G. Bornetiana. Such
striking similarities as showu in these two genera form a satisfactory
corroboration of a relationship which was originally recognized on the
grounds of’the structure of the vegetative organs and the similarity in
cystocarpic development.
(13) CERAMIUM
RUBRUM * Ag.
Material was collected a t Wenibnry Reef and Bovisand Bay, near Plymouth, April 1924.
The spermatia are borne on the surface of the radial thallus branches ;
they occur apparently in large numbers, but in spite of this they do not
appear to impart any distinctive charactrr to the plant by means of which it
can be recognized with the naked eye. When slightly magnified, branches
bearing spermatia are seen to be fringc,d with a colourless edge, owing to
the projection of the unpigmented antheridia (fig. 32 CE).
I n order to understand the relation of these antheridia to the tissues of
the thallus, i t is necessary to consider the vegetative structure of the mature
plant (fig. 31 a & h). This consists of a central axis of swollen cells, each
approximately 1 0 to 1.1 nim. long and much the same in diameter. These
cells are contracted a t their points of junction (;. e. the “ nodes ”), while
closely apl’lied to the wall are curiously elongated plastids (fig. 31 a ) .
Surrounding this axis is a layer of pericentral cells; these are much
elongated i n the internodes, extending the length of a single axial cell and
branching sparingly ; a t the nodes they are inore nearly isodiametric and
often two layers in thickness. Externally lie the cortical cells enclosed
i n a gelatinous “cuticle.” These cells are roughly isodiametric and very
irregular in form and position ; at the nodes of the articulations they are
regularly two cells deep in cross-section, but in the internodes they are
only occasionally so, an?, indeed, are somewhat widely separated froin Ontj
another, thus giving an indication of the connection uith those species where
the cortication clothes only the nodal area of the articulations (i. e. C. diaphanum Roth, C. acnnthotiotum Cam., etc.).
I n the younger regions of fertile portions of the thallus, practically every
peripheral cell appears to give rise to autheridial mother-cells, though in
+if
Thuret (1855) first recorded the antheridial plant#, while Petersen (1908) notes he has
found “a small number of antheridia.”
229
MALE ORQANS OF THE FLORIDEAC.
older p o r t i k these become limited t o definite areas (fig. 3 2 d ) as in
Ceramiurn t i i a p l m w n , where, according to Buff ham (1884),t h e antheridia
are entirely confined to the corticated nodal regions.
I n i i paragiaph on the devrlopment of the antheridia in the Ceramiaceae
as a whole, Petersen (1908) states that in t h e few cases (four) where he has
been able to observe t h e formation of the male cells i t is always preceded by
t h e continual division of the cortical cells. This certainly occurs in C. rzrbrum,
though t h e divisions ;(revery irregular in number. They apparently consist
first i t 1 the formation of periclinal ~ n l l sin- the peripheral cortical cells,
followed by anticlinal walls in the outer cells thus cut off, dividing these
into several smaller ones which form the mother-cells. No definite number
of itlother-cells a r e formed from a cortical cell, three, lour, or even five
heing found. E a c h motlier-cell contains a single nucleus and is pigmented.
FIQ.31.
vegetative thallus of
Cera?niunz rubwnz, showing the central, pericentrd, and cortical cells.
x 350.
b. Transverse section through an internode. x 750.
n. Longitudinal section throogh two internodes of a
Even a superficial view of t h e fertile male frond gives a clenr i n d i c d o n
oE the methoil of anthrridial development. I n fig. 32 d at tlie region A
(enlarged in fig. :32 a ) the xntheridinl mother-cells a r e seen as an irwgiilar
layer covering the surface of t h e frond. At n slightly lower level, I<, a
region (enlarged i n fig. 32 2)) is reachetl where these, viewed froiii :rLove, a r e
each seen to h a r e given rise to a small cell wliicli appears to be seated on
their upper surface ; sections show that this is the first antheridium 11hich
hes been formed as a n outgrowth on t.he srrrface of the cell. A t C (enlnrged
in rig. 32 e ) each original mot,her-cell is seen to have two or three clear
circtiliir areas on its surface, and these represent t h e two or three antlirriclia
which appear to be budded o P ~ at first from the mother-cell. Thus t h e
formation of antheridia takes place on t h e upper portions of t h e frorid in
regular acropetal succession. I n section (fig. 33 u & h) it is seen t,hat t h e
s 2
230
MISS VIOLET M. GRUBB ON THE
formation of the antheridia is preceded by a slight elongation of the mothercells towards the exterior of the frond. Prom each of these elongated cells
arises a small subterminal protuberance piercing the gelatinous " cuticle " ;
the latter does not peel off as in Rhod,ynzenia palmata, hut reniains clothing
the thallus, and is pierced in every direction by the rounded apices of rapidlygrowing projections (fig. 33 c). During its growth these are covered by
a gelatinous wall, which increases greatly in thickness a t the apex and later
becomes the anthsridial wall. When each projection has attained a length
FIQ.32.
Development of antheridia in C'eramium vnbrunt. rc-c, X 760 ; d, x 100.
Antheridial mother-cells.
b.
,, 1, B ,, Appearance of first antheridia on mother-cells.
C.
C
,,
Appearance of second and third antheridia.
d. Portion of young thallue, showing distribution of antheridia (stippled) both on
nodal (shaded) and internodal regions.
a. Surface view of A in fig. d.
,,
,,
approxiinating to that of the mother-cell, the cont,etits are abstricted by the
ring-like ingrowth of the gelatinous wall, which, when completed, is curved
upwards in the centre (cp. fig. 33 a ) . The constriction does not, however,
take place at the point of attachmentj of the projection to the mother-cell,
but a short) distance above, leaving about a third of the projection attached
as a blunt outgrowth to the mother-cell (fig. 33 aj. The upper portion,
which has been detached by abstriction, forms the antheridium, consisting
MALE ORGANS OF THE FLORlDEiE.
23 1
of an outer wall and cytoplasm surrounding a single nucleus. The contents
become rounded, and appear to be separated by a clear area Erom the outer
wall. The antheridium is now ripe, and the whole contents are ready to be
extruded as a single sperinatium. This has been observed to take place in
fresh material by means of a split in the apex of the antheridial wall, the
latter being left behind as an empty shrivelled sheath when the single thinwalled sperrnatium has slipped out (fig. 33 a). The size of this body at the
moment of extrusion is from 8 to 9 p in length and about 4 p in breadth.
FIG.
1
'J
-....=-
33.
..
.....,
..
...z-
L
'.".&
d
.....1
b
e
Cemmium rubrum.
All x 1800.
a, low focus, and 6, high focus of an optical section showing the production of
antheridia froni the mother-cell. Right-the antheridia are nnnibered in
order of development.
C. optical section showing the position of the antheridia with respect to the cuticle.
d. Imaginary solid view of the antheridial mother-cell. Antheridia numbered in
order of development.
e. Microtorned section through a mother-cell, showing the division of the nucleus.
Meanwhile another sub-terininal projection has been growing out from the
an theridial mother-cell, and this, following the ahove course of development,
'forms the second antheridium. Before the discharge of the second sperinatiuni a third projection arises, and similarly develops into a third
232
MISS VIOLET M. GRUBB ON THE
antheridiuin. T h e position of these three successively developed antheridia
is best seen in the diagram shown i n fig. 33 d, where the mother-cell is
depicted in stereoscopic view, the antheridia in three successive stages of
development standing around its dome-shaped apex. The same realization
of the position of the antlieridia is gained from fig. 33 a & b, where a
mother-cell with its aiitheridia is observed first a t a low focus and then at a
high one.
It seems, however, clear that the number of antheridia developed from
one mother-cell is not limited to three, for in regular order a new antberidiuui
is seen arising within the empty wall of each old one (fig. 33 a-c). ‘J’his
occurs by the developmeiit of the small projection left a t the base of each
antheridiuiii a t the moment when the first one is constricted off. This
projection grows upward, covered by its gelatiuous wall (fig. 33 b, left), and
is finally abstril.tetl, the conteuts then escaping and two empty iintlieridial
walls are left behind, one within the other. The reproductive capacity of
the mother-cell appears to be exhausted when six antheridia have been
produced in this way, for a tliird antheridium growing up in the same
position as the two previous ones has not been observed. One of the most
striking facts about the development ot’ these six antheridia from a single
mother-cell is the very reguliir manner in which it takes place (fig. 33 d),
no overlapping in the discharge of‘spermatia from one niotht.r-ce11 occurring.
Presumably this uiethod of successive discharge affords a far greater possibility of some a t least of the bodies fulfilling tl,eir function than if all were
cast into the sea a t the same moment and under t,he same conditions.
Considerable difficulty W:IS experienced i n observing the smaller cytological details, for although the inaterial was subjected to the same fixing
and embedding processes, yet the nuclear details after microtoming were far
from being as distinct ;is in Laumtciu or CIio?idms-a fact \ \ hich may partly
be due to the susceptible cliaracter of the material with regard to shriukage.
Apparently the pericentral cells are multinncleate, but the peripheral
cells and later the a n t h e d i a l mother-cells have each only one nuclells.
These latter cells contain uuinerous plastids, none of which, however, appears
to pass into the antheridiuni (fig. 33 P ) . On the forination of the latter the
nucleus of the niot,ller-cell, which in the resting position is central or basal,
passes up to the base of the projection and there divides (fig. 33 e). The
daughter nucleus passes into the young antheridium, and by the time the
latter is mature occupies the characteristic curved apical position ; this
behaviour occurs a t the fortnation of each antheridium. The spertiiatial
nucleus at the time of the extrusion of tlie spermatium is in prophase, and
shows a number of typical Kijrnchen ” or granules ; it was impossible to
count these with any certainty, but there appear to be from six to eight
present in each nucleus. When the spermatium is extruded it is ati oval
body, the blunt apex being occupied by the large nucleus (abont 3 p in
((
bfALE ORGAN8 OF THE FLORIDEB.
233
longest diameter), while around there is a sinall amount of vacuolate
cytoplasm enclosing a large central vacuole.
(14) DUMONTIA
FILIFORMIS ” Grev.
Material was gathered a t Weinbury Bay (Plynioutli) and Looe in
April 1924.
As a result of collecting between Febrnary aud July, D u n n ” came
to the conclusion that antheridial plants are, a t South Harpswell, Maine,
fertile only for two to three weeks in April. The antheridia are developed
in some cases over almost the whole of the thallus with the exception of the
base of the stipe and the hapteron. More often, however, sterile patches
are left, ;imong the sheets of antheridia, dividing these into irregu:ar
sori, especially a t the apex.
The thallus is composed of three regions : an inner one of long hyphal
cells kriown as tlie inoclullary hyphz, which on the exterior give rise to
larger and smaller sub-cortical cells. Dunn s’tates that the cells of this
outer layer (which are only slightly pigmented) become the antheridial
mother-cells ; i n other words, these latter are homologous with the outer
cortical cells of the tetrasporic or cystocsrpic plants. I t is difficult to make
this coniparison since sterile regions of mxle plants are not easy to tind, but
on examining the structure a t the base of the stipe where there are
as yet no signs of antheridia, and that of the sorus above, it is seen that
the production of anthcriditi is clearly preceded by a division of outer
cortical cells, the out’ermost layer thus becoming the antlieridial niothercells. In the upper regions of the tlia!lus a comparisoo” of a sterile
and a fertile area shows tliat in the former, if young, the outer layer
of cortical cells is missing, but is developed in the soral area, forming
the mother-cells. These, then, are not simply cells which would in any
case be present, but they are specially developed on the antheridial plants
to assist in the produdion of antheridia. These niother-cells are uninucleate
and are only poorly pigmented.
The antheridia develop as protuberances of the mother-cell and are
enclosed in the gelatinoiis wall of the latter, being cut off obliquely
by the iugrowth of this wall (fig. 34b). Dunn describes two spermatia
as being detached in this way, but a surface view of the thallus (fig. 3 4 a )
clearly shows that in several cases three are developed in succession
from the flattened surface of the noth her-cell. I t is easy to overlook this
if sections only are studied, since the antheridia are so croiided that
it is difiicult to ascertain liow many are attached to each mother-cell.
The antheridia stretch upwards to the surface of the “cuticle” which
* The presence of aihheridia was nientioued by Thuret (1856), and they have been
described by Dunn (1917, p. 437) and Rosenvinge (1917, p. 156).
234
NlSS VIOLET ill.GRUBB ON THE
covers the thallus ; the protoplasmic contents surrouiiding the nucleus
round off, becoining nearly spherical (fig. 34 b ) . A t this stage it is
possible to see quite clearly the colourless antheridial wall surrounding
the spermatiuin ; this wall shows a distinct outer layer, especially a t the
apex and a swollen middle layer, while there is a defiiiite inner refractive
region around the central body (fig. 34 b). The spermatium escapes, enclosed
i n what appears to be a delicate wall, leaving behind the empty antheridial
wall attached to the mother-cell (fig. 34 b). The observations of Dunn are,
however, directly oppoaed to tliese results ; she states and illustrates by
figures that “ n o empty cell walls were see11 attached to the spermatiuni
mother-cell,” and “the wall of the spermatiuni is ;I portion of the mother-cell
. , . no body is forined which would be homologous to the sperm:itangium
of Delesseria.” These statements, implying that the \\hole antheridium is
.
FIQ.34.
a
b.
Antheiidia in l)u~~~,LontiuJilifri~ia.
x 1800.
a. Surface view of part of a fertile area of an antheridial plant, ahowing the antheridia
borne upon the flattened apex of the mother-cell (dotted).
6. Transverse section through a siniilar sorua. Both primary and secondary antheiidia
call be seen in optical sections in course of development.
cnt off and liberated a t inaturity, can only be explained on the supposition
that Duiin worked w i t h n~icrotoined sections or with material4 which had
been much shruuken and i n which the gelatinous walls would be far from
easy to see.
S e c . d a r y antheridia are clearly developed within the empty walls of
the primary ones ; these new ones in many cases arise before the extrusion
of the primary sperinati:t (fig. :346j. I n no case have tertiary antheridia
been observed. The cytology of this form has not here been investigated,
since it was clearly shown by Dunn that the nuclei behave in a similar
NALE OKQANS O F T H E FLORIDEIE.
235
way to that which has been described in this paper for the antheridial
nuclei in many members of the higher Florideae.
The development of the antheridia in Dumoiitia @j‘ownis, togetlier with
the production and liberation of the sperniatia, does not therefore appear
to deviate in any outstunding particular from the course of events previously
described for other species.
( 1 5) FURCELLARIA
YASTIGIATA * Lam.
Material was obtained from Rwantige, Shanklin, and Plymouth in January,
February, and April respectively.
The antlieridial p1:tnts of I;icrcellaria jhstiyiuta have been known for
many years, and before their function was recognized were classified
as a peculiar variety of the normal plant characterized by the “little
ovate-lanceolate, transpnren t, very pale, soft termiliatioils of the branches ”
(Greville, 1830, p. 6 7 ) . Dawson Turner, however, though not understanding the method of reproduction of the alga, attaches the following
shrewd observatioii t q his description of this variety :-‘‘ That these ovate
transparent tips are in reality connected with the fructification I cannot
allow lmyself to doubt, as well as from their peculiar form and substance,
as from their appeariiig only a t the time of the cylindrical pods, and,
like them, withering and falling off, leaving the frond trunc ,ted. A t
the sanie tinie, when cut through, they exhibit no appearance of seed or
granules, but are full of a transparent miicus, interwoven witli reticulate
threads in cylindrical meshes.” Greville was under the impressiori that
they were to be regarded as “ imperfectly developed pods,” while Thuret
was the first to recognize their true significance. Sixty years later
Rosenvinge made a slight investigation of Danish material, leaving, however,
many points undetermined.
Antheridial plants are developed apparently i n the spring (December
to May in Denmark), and entirely resemble the vegetative plants except
in the upper regions, where all t,he branches are terminated by much
swollen, oval, nearly coloui.less “pods,” varying in length, but in a
healthy plant attaining to as much :IS 2 c n ~ s . These bodies are generally
pale yellow or pink and somewhat hyaline, their characteristic transpirent
look and slimy feeling being due to the thick gela.tinous “ cuticle ” enclosing
the antheridia which are found in large numbers over the whole surface.
The “pods” though all performing the same function appear to be
developed in two ways. I n those found on y o i ~ n gplants the nornially
dichotomously-formed apices of the thallua are replaced by pale-coloured
tips, generally borne on a short stalk. On the other hand, in more
*
Antheridial plants have been referred to by Dawson Tamer (1808, p. la), Greville
(1830, p. 67), Thuret (1855), and Rosenvinge (1917, p. 167).
236
MISS VIOLET
M. GRUBB ON THE
complicated cases the apex .dichotomises rapidly several times in succession,
and the branches, lying close to one another, are each terminated by a
((pod,”. giving a bushy appearance to the thallus. I n either case, when
ripe the “pods” shed their sperniatia and then break away a t the base,
or in some instances, owing possibly to their succulent nature, are probiibly
eaten away by animals which leave the truncated apices of the frond.
From the latter, vegetative growth may take place in the norinal way,
contiiiuing the growth of the thallus. Among drift rnaterial which has
probably been thrown u p from deeper water, plants have also been
found in which no vegetative growth had taken plttce a t the tips, but
froin the blunt end new “ p o d a ” were growing out in groups of three
or four, each one being borne on a short stalk.- This suggests that a
single antlieridial plant may bear at least two separate crops of antheridia ;
but whether this occurs successively in the sanie season or whether the
two crops are separated by :in intvrval of a year, could only be ascertained
by careful observatiori ocmale plants tlrroughout a year.
Before the formation of ant1;ericlia or the shedding of sperniatia, these
“ pods” show a iiormtil vegetative structure.
When mature this consists
of a central region of thin-walled hyphae, surrouiided by a zone of large
colourless cells filled with dense contents, while without is a “cortex”
of small pigmented uninucleiite ctAlls, enclosed in :I. co~uiiion ge1ati:ious
cuticle.:' The outer cells are seen to arise by one or more dichotomies
of the cells iiiimediately below theni, SO that the outer lajer is in reality
made up of pairs of cells, each pair arising froni the cell directly beneath
it (fig. % a ) ; it is from this outer layer that the antheridial mother-cells
develop. On t,lieir forination each outer cell elongates and becollies
niuch swollen i t t the apex, appearing club-shaped (fig 36 6 ) ; plastids
also which are pale in colour atid have a bright refractive appearance
accumulate in the enlarged tips. The cell is then divided by a cross wall,
giving a lower cell norinal in appearance and a short upper one, much
swollen, pigmented and with a single nucleus (fig. 36 c). This upper
one almost immed’iately divides by a longitudinal wall perpendicular to
the periphery, giving two cells which, iu an exact transverse section,
appear to lie one above another. The cell which was therefore the outer
one has now given three cells all joined by protoplasmic connections,
a lower one subtending two iipi’er ones which forin the mother-cells (fig.
3 6 d ) . These latter have each a single nucleus and are pigmented, while
the wall around thaiii is somewhat swollen.
The antheridium arises as a sub-teritiinal conical projection froin the
mother-cell surrounded by the common gelatinous wall, pushing up through
the now niuch swollen “cuticle” (fig. 36 e). A t first this projection
is pigmented, and it is not until the division of the iuother-cell nucleus
has taken place a t the Oase of the j o m g antheridiuin that the piginent
237
MALE ORGANS OF THE FLORIDILE.
disappears ; no s i p 1 of definite plastids passing back into the mother-cell
has been seen, but t h e pigment appears to degenerate, and it is noticeable
t,h;rt the protoplasm of the antheridiuni is markedly granular ; possibly
some of these conspicuous and highly refractive granules may be t,he
Fro. 36.
b
d
Stages in the formation of the rntheridia of Furcellariafast&iuta.
x 1800.
a. Young secondary antheridium being constricted off; nucleus in resting stage.
b. Spermatium nearly ripe. Nucleus showing beaded deeply-staining reticulum.
c. Spermatium escnped. Chromatin granules clearly visible in the nucleus.
d. Right-formation of a secondary antheridium betore the liberation of the
first spermatium.
products of degeneration of the plastids. The young, somewhat wedgeshaped antheridium with its single nucleus is abstricted by the ingrowth of
t h e surrounding wall (fig. 3 6 e ) and grows rapidly in length, always,
238
NISS VIOLET M. GRUBB ON TEE
however, remaining long and narrow, possibly owing to the confined
space. The antheridial wall stretches greatly until it reaches the surface
of the “cuticle ” ; at this point‘it is ruptured (fig. 36 e ) , and the spermatium
escapes through a circular aperture. The “ cuticle ” of a ripe “ pod ”
seen in surface view from above is punctured all over with these ragged
circular openings, through soitie of which sperinatin can be seen escaping.
During the growth of‘ this first primary antheridium, a second primary
on0 has been forming in exactly the same way on the other side of the
FIG.36.
_-
b
C
d
a
Furcellariafastigiata.
a. Outliue drawing of a transverse section of the vegetative thallus, showing outer
6‘
b to
cortex ” of small cells developed from large storage cells below.
x 750.
a. Stages in the development of antheridial mother-cells. x 1200.
e. Drawing of a transverse section of a “ pod.” The antheridial mother-cells are givirip
rise to primary antheridia. I n one case the spermatium has escaped, leaving
behind an empty sheath. X 1200.
mother-celi. The expulsion of the spermatia from the antheridia is,
however, slow, owing to the thickness of “cuticle” which has to be
traversed ; and while the upward growth of the primary antheridia is taking
place, secondary ones are foriiiing below each spermatium and have often
been cut off before the latter has escaped (fig. 35 d). Generally, therefore,
MALE ORQANS OF THE FLORIDEIE.
239
two pairs of antheridia, one above the other, are developing at the same
time from each mother-cell ; the upper one of‘ each pair is, of course, more
mature. Everjthing points to the probability that even more antheridia
are produced in the place of tlie empty ones, but t,hey have not been seen.
The proof should lie in the presence of the empty antheridial sheaths
within one another, h u t owing to the close packing of the anthericlia and
the fact that the sheaths are only seen embedded in the “cuticle” and
never free, there is difficulty in distinguishing the first-formed sheaths,
and even inore so, later-formed ones, The spermatia are on the whole
large, within the antheridium nieasuring in some CilSeS as much as 11 x 5 p,
though generally about 9.5 x 3.5 p. On’escape t.hey become rounded off,
and a t that stage are clothed with n wiill. It is impossible to say whether
this wall has been developed beEore discharge ; from analogy with the
majority of other . xauiined species one would expect this to be the case.
The single nucleus of the antlieridial motlier cell always remains small, but
divides in a normal mitotic manner at the base of the antheridium, one of
the daughter nuclei passing back into the mother-cell, and the other gradually
increasing in size and moving into the young antheridiurn before the latter is
abstricted. It then passes slowly to the centre 6f‘ the sperniatium, where i t
remains suspended by cytoplasmic thread?, never appearitig to take up t.he
apical position so coinnion in spermatia of other species. The details of
nuclear structure show unusually iiiteresting stages. Immediately after the
antheridium is cut off, the nucleus can be seen lying near the point of
constriction obviously in a resting condition, a structure siniilar to a nucleolus
being distinctly Pisible and surrounded by a clear area in which indicaticbns
of a faint network can be made out (fig. 35 a). At a somewhat later stage,
when tlie sperniatium is nearly ripe but has not yet ruptured the antheridial
wall, tlie dark central body has entirely disappeared, and the nucleus consists
of a deeply-staining reticulum with marked thickenings at the corners, the
whole surrounded by a nuclear membrane (fig. 35 b ) . Finally, sper1aati:i
which have escaped show in their nuclei a number of well-defined, denwlystaining granules or “KSrnchen,” as many as 16 or possibly inore beiilg
present ; linin threads connecting these together can be seen in some cases
(fig. 35 c).
These st.ages, which can be repe..tedly observed, clearly indicate, as
suggested in the case of Laurencia pinnatijida (€1. 205) and Nitophyllum
laceratum (p. 199), that the nucleus of the antheridium when first fortned
passes definitely into a resting state ; this, on the ripening of the spermatium,
is followed by the early stages of a nuclear division which in the higher
Floridea? is believed never to be completed. No evidence on the latter point
is a t present available for Furcellaria, for Rosenvinge (1917), who has studied
the changes in the citrpogoniuni, stated that he has never seen sperinatia on
the trichogyne ; he considers that parthogenetic development takes place,
240
MISS VIOLET M. QRUBB ON THE
sporogenous threads being formed apart from any fertilization stimulus.
There are, however, no signs of degeneration in the spermatia, and i t is
difficult to believe that they should be prodirced in peifect condition and in
such large numbers a t the same season as the ripening of the trichogyneu, if
they are not called upon to take any part in the reproductive process.
V. The Position of the Antheridial Organs.
The sexual plants of the Florideae are usually dimcious, but the following
members of the Nemalionales are reported as frequently exhibiting the
moncecious habit : Nemalim nadtifidum, Batrachosperinum, Helnzinthora,
Helminthocladia, and Bonneviuisonia asparagoides. .in theridia and procarps
borne on the same plant are also noted for some spcciw oi Callithamnion
and for Utcdresrrayn purpurgera, Ghosiplionia capillaris, and Halarachnion
Zigulatunz. It will be seen that this developtneut is exceptional among the
higher Florideae.
The young antheridial plant is nearly always normal in appearance,
resembling in every respect the young procarpial or tetraaporic thallus.
Occasionally, however, as in itfartensia fragilis or Caloglossa Leprieurii, it is
smaller or has a more ephemeral existence tlian the female, and in numontia
jlijbrtttis it is thought to die after dischtirging its spertnatia (Duun, 1917).
Thuret (1855) first pointed out that the antheridia are developed on these
male plants in ,the same position as that in which the procarps and tetraspores
are borne. This statement holds for the majority of cases, but in some
species as Laurencia yinnat$da or IT,. obtusn, P d y i d r s rotundus, etc., the
antlteridia resemble the procarps in position, differing in this respect from
the asexual organs. I n others, such as Plocamium coccinei~rn, Ceramiziin
ruhrum, etc., the p r o c a r p occur in a difftxent position from the antheridia
and tetraspores, while in the species of Polysiphonia the position of the
antlleridia does not resemble that of either the tetraspores or the j~rocarps.
The actual arrangement or grouping of the antheridia on the thallus is very
varied. I n Netkialion and Batrachosperinunz tlie antheridia are sc:ittered
iudiscri~ninatelyupon tlie assiltdating fil,iuients, though in HeZinzntlLora and
He1,ninthocladza the reproductive bodies are confined to clusters a t the apes,
while in Liagora and some members of the Lemaiieaceae special lateral
antheridid braitches are developed. Such clusters of branctilets are also
borne laterally in Callithananion (fig. 28), Seirosyoru, and Halurus equisrtifolius, and terminally in Spemotliamnion and Ptilothaninion, while in
Grifithsia corallina they are arranged in definite whorls around the noties
(fig. 21). Fiiially, in such genera as Sterrocladia, Gafa,caura, or Lauren&,
these antheridial clusters are sunk in conceptacles on the surface of the
thallus.
'rile Illore general position of the antheridia is, however, in superficial sari.
These may be scattered without order as in Rhodophyllis bifida and Cystoclonium
MALE ORGANS O F TH E FLORIDEX.
241
purpurascens, or the antheridia ma! be developed in acropetal succession, as
in Rhodyinenia palmatti and Chondws c r i s p s . Among the Delesser iaces,
trans-itions from sori developetl on the ’thillltis to those on special leaflyts can
be found, while i n Furcellaria jastigiata the special structures take the form
of a swollen apical “pod.” I n the o or all in ace^, and probably also in the
species of Gracilaseia, the sori are sunk in conceptacles.
These various facts concerning the position of the antheridial groups can
be summed up in the following scheme :1. Autheridia scattered, showing no regular order of development :Nemalionales.
2. Antheridia combined in clusters 011 specially developed branchlets :( a ) Single clusters ................................
CuUtth~umzimspp.
Huhrrm rquisetifolius.
( b ) Clusters aggregated in a definite order . . . . . . . . . . . . Griflth.vn rot u l h z .
( c ) CluRters sunk in conceptacles ....................
Lnuwmrrr yip.
Gu1aaato.n spp.
3. Antheridia combiued in a sorus :( a ) Sorus on thallns showing no definite order of development.
Cbstoclonium ~ p p etc.
.
( b ) Sorus on thallus showing definite order of development. Rhodymenia pahnata etc.
(c) Sorus on a specially-developed organ . . . . . . . . . . . . . . Delesseriu spp.
Nitophyllzcrn spp.
Corallinacere.
(d) Sorus sunk in a 6onceptacle. .....................
VI. The Position and Structure of the Antheridial Mother-cells.
Antheridia in the Floridee are always developed froin a cell which is
variously known as the “ cellule anthhridifAre,” the “ Spermatangienmutterzrlle,” or the nntheridial mother-cell. Schinitz (1883) stated that in all tlie
Floridoa the>e iriother-cells are the terminal and not the intercalary cells of
branch systems. This is certainly the case in the vast majority of species,
the mother-cells either forming an outer layer produced by division 011
the surface of a thallus as in fiitopl8yllum (pp. 195, 199), C’eramiuin rubrunz
(p. 229), Fuwellaria fastigiata (p. 236), etc., or arising as the end cells of
specially-developed branches which are not incorporated in the thallus tissue
as in (&ifithsiu coyallina (1). 215), Callitluini~tionbrachiatum (p. 223), etc.
Exceptioiis to this rule are, however, known in which both tlie intercalary
ant] the terminal cells take part in antheridial production. Such cases
are Nenzalion nwlt@dimn (Cleland, 1919, p. 333), CullitltanaiLion T o S e U m
(Gnignard, 1889, p. 334), and Halurus equisetifolius (fig. 27). It seems
probable that Further investigation will bring to light more instances of this
1:Ltter type of development.
I n structure the aiitheridial mother-cell is unbranched, giving rise terminally, subterminally, or laterally to antheridia. Three species have been
listed b~ Svedelius (1908) as bearing branched mother-cells : these are
242
MISS VlOLET M. GRUBB ON THE
Choreocolax Reinsch (Harweyella Schmitz), in which the mother-cell has now
been shown by Sturch (1924) to be unbranched ; Champiu pavvula, where
the mother-cells certainly show no signs of branching on further investigation (see p. 193), and Gigartina mamillosa. The evidence for the latter
case lies in a single figure given by Buffham (1896, fig. 8), the interpretation
of which is somewhat doubtful.
Whatever the number of nuclei in the vegetative cells, the inother-cells
are always uninucleate, the nucleus when not dividing lying near the base
of the cell. The amount of pigment present varies considerably. I n
Ratrachospermum and flemalion, where the mother-cell is homologous with a
vegetative cell, the pigment is found in both in equal quantities. The most
common state of pigmentation is, liowever, the presence of reduced or rudimentary chrornatopliores, but i i i Qrifithsia Bornetiana, h>linia rosdata, and
Ilumontia fil+ormis the niother-cells are recorded as being usually completely
colourless. I n Martensia, where the chromatophores cannot be distinguished
in the mother-cells, the suggestion is made by Svedelius (1908) that the
dense protoplasm present is due to the solution of the piiistids i n the plasma
for use as food material.
V I I . The Development, of the Antheridia and Spermatis.
The antheridia (or spermatangia of German authors) are developed as
terminal, subterminal, or lateral outgrowths from the upper (outer) surface of
the antheridial mother-cells. There are, however, few records of terminill
antheridia wliich can be regarded with any confidence. Champia parvula and
Cystoclonium purpurascens have both been said to exhibit tJiis characteristic,
though this is now known not to be the case (see p. 192 and Kylin, 1922) ;
Hypnea muscjformis and Pteroclodia capillacea have also been placed in this
oategory (Guignard, 1889) together with Peyssonellia squamaria (Thuret, 1855),
but on such slight evidence that re-examination with the aid of niodern
technique would probably lead to other conclusions. The terminal metliod of
production is, however, both described and figured c1e:trly by Svedelius (1908)
for Martensia fragilis, by Guignard ( 1889) for Melobcsia msnibranncea, and by
Sturch (1924) for Harveyella pachyilerma, though it must be noted with
regard to the latter that in the closelp-related species H . nziyabilis “the
antheridia are produced obliquely :ind laterally.”
Antheridia are developed laterally in 110 particular order or number in
Batrachospermum and Nernaliort. Among the higher Floricieae, however, the
dcvelopment has become more regular, a definite number of primilry
antheridia being produced in a subtarminal rather than lateral position, and
ripening in orderly sequence around the upper surface of tlie mothcr-cell.
The number appears to vary from two to four, only two being sitid to occur
i:i Uelesseria sanguinea (Svedelius, 191%),Lernanea Jluviatilis (Kylin, 1922),
Chondrus crispus (p. 187), Furcellaria fasti,yiata (p. 238), and Rhodyhenia
243
MALE ORGANS O F TEE F L O R I D E X .
paltnata (Delf and Grubb, 1924). Kylin (1922) lists eight species i n which
two 01’ three antheridia are found, while thtee antheridia arising from a
mother-cell are definitely known in a n u d e r of cases some of which are
recorded in this paper (see p. 249). Four antheridia to a mother-cell is a
rare occurrence only known with certainty in five instances-Cliondtia
teiuuissinia and Cullithanmioii roseutn (Guignard, 1889), LauTeticia pinnuti@
(p. ZOl), Hulurus eqicisetifolius (p. 2221, and Polysiphonia uiolacea (p. 213).
It is noticeable, that in those cases where the mother-cells are closely packed
or confined by a thick “ cuticle ” the nuniber of antheridia appears to be
strictly limited by the available space.
The antheridia develop as protuberances of the wall and protoplast of the
mother-cell, and into these slight projections passes the nucleus formed by
tlie division of the mother-cell nuclcus. As a rule the other contents of tlic
antheridirim are solely cytoplasniic, though the presence of chromatophores or
portions of plastids has been recorded for ATei~iuZionniult$tlicm (Wolfe, 1904),
13atraclios/)ei,,)iicni(O.jterhout, 19OO), and possibly these bodies also occur in
.Ftircelliwiu jus/igiatu (1). 237).
The young antlieridium is either long and narrow (fig. 9 u) or round a.nd
swollen (fig. 20 b). When it is eqnal in length to the mother-cell, the contents
arc abstricted from those below by a ring-like ingrowth of the surrounding
elongated mother-cell wall, the cbnstriction generally taking place a t a level
with the upper surface of the mother-cell, though in Ceranrium rukruin i t is
sbQve this level (p. 231). The fact that the sperinatium is separated by
abstriction and not by a norinally-formed cross-wall does not appear to have
been generally recognized ; in the cases here described it seems impossible to
doubt that t,he prd,oplnsniic contents gradually become narrower a t the point
of selmration until only :I small connecting strand is left which presuniably
passes through a pit in the otherwise complete wall (fig. 12 b) ; finally, ever1
this connection is no longer visible.
A rapid ripening .of t,lie antlieridium now tnlies place ; it generally swcIIs,
tlie cytoplasm beconiirig vacuolate and the nucleus taking up either an apical
or central position. Thc wall thickens greatly, and in some cases can be see11
to show three layers-a tliiclier outer one generally denser a t the apes, a c:lear
swollen central liiyer, arid then around the contents which will form the
sperriiatiuni a very nwrow, Irighly refractive region (fig. 27 6). Ultiiiiately
a point is rcaclied, a t irny rate in the great nxijority of cases, when a split
occurs a t the apes of the elastic surrouiiding wall, and through the narrow
aperture thus foriiied the cytoplasm and nucleus slip out as a single sperniatinni.
I n those species where the antheridia are borne on filamentous branches
( e . g . GtvljidLiu) tlic exit of tlie sperniatium is quite simple, since i t is not
1i:tiiipered by the surrouiidiiig ‘’ cuticle ” of a thallus ; in other c:rees (e. g.
Bhoclynieniu pulniata) the “ cuticle ” peels off in the region of an antheridial
sorus. But in such species as Choiidrus c r i s p s or P’urcellaria fastiyiata,
where tlie ‘.cuticle ” is very thick, the antheridial wall continues to eloiipte
LINN. JOUItS.-BO’I’IS
Y. VOL. X L Y I I .
T
244
MISS VIOLET 31. GItUnB OK TIIE
until it rcaches tlie surface of the latter ; tlieii the wall sl’lits and tho
spcrmatium escapes direct into the surrotinding water (fig. 36 e). In
Cullithamnion rosezcrn (GiiignarJ, 1889) little c a 1 ~are said to be formed a t
tho apex of the antheridia, liberating the speimatin, and iii l a r r e y e l l u “ wually
the outer coat (i. e., ‘cnticle’) is so weakened by tlie mass of qminatia tlriit
i t flies off like a broken spring and all the speriniitia are set free a t o w e ”
(Sturch, 1924).
Species have been described in which the whole antheridium is apparently
cnt off and liberated a t this point, the two best-known records being those
for Polysiphmzia violacea (Yitmanonchi, 1906) and Dumontiu filgbrnis
( I h n n , 1917). Figures and observations given in this paper have, however,
clearly shown that in both these species tho antheridid walls remain behind
after the spermatia have passed from tlicm (figs. 20 c and 34 0). Though
denied by Lewis (1909) re-examination would probably show that this samo
bohaviour takes place in Grifltlisia Bornelianu in view of tho fact tliat in
two nearly-related species ( C;. eoralliira and Ilalurus equieetijiolilcs) walls
cm clearly be niade out (figs. 24 and 27).
In t.lic case of Burtensia,
:tlthougli SveJelius believes that tlre whole or part of tbe antheridial wall
is cut off with the spermatium, yot he clearly figures mother-cells with
empty gelatinous sheaths standing up above tliein (1908, pl. 4. fig. 6).
Tho sl’erinatium, immediately on discharge, is oval in form and may be as
long A S 11 p (Furcellariu); it rapidly, however, beconies rounded off,
measuring in diameter anything from 2 or 3 p (Callitiurn~iio~r,
Grifitlisiu) 10
6 or 7p. A t this stage it consists of delicate cytoplasmic contents SUTrounding a central nucleus, but opinions differ as to whether or not it is
enclosed in a wall. Svedelius (1912) reported that in Belesseriu satiguinea
tho spermatium is discharged as n naked ~wotoplast, while Kylin, after
exanlining this latter spccies together with Klrodoiiiela ~iryatu(1914) and
Bonneniaismtia asparayoitleu (19161, agrcwd with this, stating, however, that
soonor or later a wall is acquired. Guignnrd (1889), on the other lland,
observed walls around a11 the escaping sperinatilr he examined, and
Yainanouchi believes that in Coralliiia oficinalis the spermatiuni “ has a
thin wall derived entirely from the mother-cell” (1921, p. 9:3). I n all the
species described in this paper the spermtttiuin when liberated :tppears to be
clothed with a very delicate, liiglily relractivc wall. This, in some C:IS~S
a t least, s e e m to be preseilt when the body is still within the antheridiu~~l
(l’ol~pi‘lionia j h t i y i u t a , fig. 18 1) & c, Lauremia pinnatifida, fig. 14, otc.), for,
as the spern~atiumapproaches maturity, (I narrow layer appears around the
body, staining less deeply than the true surrounding antlieridial wall. This
internal wall can t)c been even more distinctly when tho spermatium has
contracted away froin the base of the antheridium, or when half in and h:llf
out of the latter (fig. 18 c), but wlic!tlier it is ail iiiuer layer of thc antheridial
.wdl or ;in ontirely new structure is not clcnr.
245
MALE ORGANS OF THE FLORIDEIE.
Secondary antheridia are known to occur in several species, but their
presencre has often bec11 overlooked. Guignard figured them for Grifithsia
corallina and Chondria tenuissinta (1889, pl. 6. figs. 6, 7), and Zerlang
( 1 889) described them for Wran,qelia penicillata. Svedelius notes them for
Martensia fragilis (1908), though he fails to find any development comparable to this in Delesseria sanguinea (1912), except in very rare cases ;
it, however, occurs regularly in Scinaia fui*cellata (1915). Rosetivinge notes
the phenomenon in Dunzontia incrassata (1917, p. 157), but Uuan (1917),
working on microtonied sections of this species, failed to see it. Kylin
neither denies nor describes the occurrence of these secondary antheridia in
the many species which he has investigated, apparently not having observed
them. I n every species described here bearing mature sperinatia, with the
exception of Po1,ysiphonia spp., it has been possible to find secondary
antheridia developing and forcing their way up through the empty primary
ones (cp. fig. 27).
I n some instances a third series is formed (Callitl~amnionbracliiatum,
fig. 30), while in ivernalion lulricum, Kurssilnow (1909) figured as imny
as six antheridial slieiiths one within another arising- from the same point.
The apparently inultiple formation in Harveyella pacliyderma (Sturch, 1924)
arid Alelobesia (Guignard, 1889) seems to require further investigation.
The fate of the mother-cells following on the cessation of the production
of antheridia is various. I n some cases (Martensia, Delesseria) the ledlets
on which they were borne die away, or the part of the thallus disappears
(Furcellaria). In other species the mother-cells simply return to the
function of normal vegetative cells, and it is no longer possible to distinguish
that they have played any distinctive part in tho life-history (Clioiihus
crispus, 12ltoily~tieriiapal mata).
VIII. The Cytology of Spermatial Development.
Spermatial development, seems to include a characteristic and, on the
whole, uniform series of nuclear changes, both in the mother-cell and in the
antheridiuni. The single nucleus of the mother-cell, which is generally
at the base of the cell, appears, in the resting condition, to consist of two
regions-a central denser one and a colourless outer area. According to thc
figures given by Kylin and Yamanouchi, this appearance is explained in
Griflthsia corullina, Kliodonzela virgatu, and Polysiphonia violacea by the
central position of the spherical nucleolus, the surrounding area being
occupied by a delicate network bearing chromatin granules. On the first
signs of the formation of a spermutium this nucleus passes up to the h e of
the small projection, there entering into an early prophase (cp. Kylin, 1914,
fig. 14); here it undergoes the normal karyokinetic division similar to that
of vegetative nuclei ; the mitotic figures are exceedingly small, and it is
generally impossible at this stage to count the chromosomes, since they
T 2
246
MISS VIOLET Dl. GRUBB ON TBE
appear only as a dark line along the equator or’as a densely-staining mass at
either pole. Of the two daughter nuclei thus formed, one enters into the
young antheridiutn, while the other returns to the base of the mother-cell,
and remains there in a resting condition until the formation of a further
antheridium. This mother-cell nucleus may repeat the process as niany as
eight times in the case of those species in which four primary and four
secondary antheridia are formed from each mother-cell.
The antheridial nucleus passes up the length of the antheridium, nntil,
when this is mature, the nucleus is to be found as a large soinewlrat elonbody 2 to 3.5 p in diameter, occupying either a central or an apical
position (Ftircellaria and Laurencia respectively). Opinions differ as to the
behavioiir of the nucleus when first formed ; Yanianouchi states that in
Polysiphoniu ciolacea ‘‘ the chro~nosornesmaintain their individuality and
are united by linin threads” (1906, p. ll), while Svedelius thinks that the
same inay hold good for hfartensia fragilis (190s) and Beltmeria sanyuinea
(1912), thus implying that this uucleus never passes through a resting stage
before entering into the next division. On the other hand, Kylin has shown
in t w o cases that in the J O U I I ~spermatium the nucleus can be seen in the
resting condition, later passing into prophase (Bonneniaisonia asparagoides,
1916,.a11d Rhodomela virgata, 1914). This has also been observed in this
paper in cases where it has been possible to make out detailed structure,
and particularly in Furcellayia fastigiata ( f i g . 351, Laurencia pinnatipda
(fig. 14), and Aitopliyllu~iilaceyatum (fig. 12).
In these latter species the ant1:eridial nucleus after its formation is first
Seen as a dark central region surrounded by a paler a r e a ; in Delesseria
sanguinea Kylin (1922) attempted to show that there was a small central
nocleolus, though this was absent in the closely-related
sinuosa alld
D.mscifolia ; in Rliodosnela rirgata (1914) it was absent or could only be
nlade out with difficulty, while it has not been seen in any of the forms
exaillined here. But what appears to be the dark nucleolus is apparently
a dense mass of chromatin or possibly very minute chroniatin granules
stainillg deeply and connected by liuin threads with one another ; a silnilar
construction of the pseudo-r~ucleolushas been shown by van TVisseliilph to
be I’resent in Spirogyru. Sooner or later changes t:iBe place in the nucleus,
while thc sperinatium is still retained within the antheridium. The definite
lluclear membrane is lost, and there appears a well-defined and reguI:lr
lluniber of small deeply-staining bodies known as K i i r n c h e ~ ~
Karyosoniee,
,
or
grunules, united to one mother by delicate linin threads. It seeins probable
tllat these Kiirnchen represent and indeed may be true chromosonies. 111
every case where detailed examination of the sperinatiol nucleus has been
undertaken it is recordcd as being in this condition of prophase at tlie tiille
of discharge of the sl)eriiiatiutn, about t\$eiity buch inst;inces being k11owll in
addition to those rdcorded iii tliib pitper.
a.
MALE ORGANS OF THE FLORIDEIE.
247
The subsequent fate of the sperinatial nucleus appears to vary. I n
Batracliospermum (Schmidle, 1899 ; Kylin, 1917) and A-emalion (Wolfe,
1904; Iiylin, 1916 ; Cleland, 1919) it is said to divide and give two daughter
nuclei when the sperniatiutn becomes attached to the trichogyne. I n other
genera, however, this division is not known to take place, but the spermatial
nucleus while still in prophase passes down the trichogyne and fuses with
the carpogonial nucleus. There appears, therefore, to be a inarlced difference
in this respect between the lower and the higher Floridez, the evidence from
the former pointing to the probability that what is now a single spermatium
originally possessed the potentiality of becoming two. I n the higher
Floridex!, even this nuclear division within the spermatium has become
suppressed, the only remaining sign that it ever occurred being the condition
of prophase in which the nucleus is found a t the time of fertilization.
Although it is almost impossible to obtain a n accurate chromosome count
in the tnihotic figure in the antheridial mother-cell, this has been done in the
antheridium in twenty-one species besides those recorded in this paper 1)y
countring the number of granules a t the time of prophase. Owing to the
small size of the nuclei, the numbers are not to be regarded as equally
accurate with those counts made in the comparatively large veget. t’iv e or
tetrasporic nuclei, and indeed in such cases as Neinalion niultij$dum, where a
cqunt lias been taken by two different workers, there is often a divergence of
opinion (Kylin, 1916 ; Cleland, 1919). It is curious to note that Kylin
finds ten chromosomes to he the haploid number in both Batracliosper?num
and Netnalion representing the lower Ploridez, while in the eleven species
of the higher Florideze where he has counted the number he always obtains
twenty or about twenty. This uniformity is not borne out hy other
workers, Lewis (1919) recording seven for Grifitlisia Bornetiana, Dunn
(1917) seven for Durnontia jlifornzis, and Yamanouchi (1921) twenty-four
for Corallinn o f i c i m l i s . The same variability has been found in the
different species investigsted here, the numbers varying from about eight in
Aitophyllunz laceraturn :ind Ceraniium rubrum to sixteen or possibly more
in Furcellari~fastigiata.
IX. The Homologies of the Antheridia,.
The antheridia of the Floridea can be compared with similar structures
in three different groups. Among the a1-m the only close resemblance is to
be found in the ChlorophyceE, the similarity with Coleockwte in methods of
sexnal reproduction having long been recognized. The antheridia in this
geniis arise in a manner and position almost exactly comparable to that in
the Nemalionaies, the contents of an antheridium in C. scutata consisting
of a nucleus, cytoplasm, and plastids. At this point the comparison breaks
dawn, for the liberated speruiatozaid is said to be both ciliated and lldied.
248
MISS VIOLET ni. GROBB ON THE
Even if, howcver, 110 close phylogenetic link exists between Goleochn te ant1
the Floridez, there is here an interesting esainple of parallel evolution in the
ni:tle a s well ;is in the female reproductive organs.
The resemblance between the Floridem and certain groups of the Funpi
h a s been noted by several writers, notably Sachs (lS82), Schmitz (1SS393), and Dodge (1914). These parallels have mainly been drawn from
comim-isons between the ascogonium and the carpogonium of the Ascomjcetcas. Structures known as antheridia are, however, found in many species
of thc latter group, and particularly in some of the Pyrenomycetes, where
tlicse bodies are borne at the extreinitics of very fine uninucleatc h y p h
,a:r tlicred into spermogonia. I n Gnomoniu e y t h ~ o s t o m athe resemblance to
the Floridcae is very close, for the antheridia are said to be constricted off
terminnlly, each containing ‘‘a long thread-like nucleus and a relati\ely
siiinll amount of cytoplasm ” (Brooks, 1910). Birnilarly, in Gyniiiosi’o?,an!iiic?lz
clurariteforme (Blackman, 1904) figures show thaC the sperirlatia are cut off
from the hyphse by the ingrowth of the surrounding wall, tlic walled
sperrnatium containing a fine granular cytoplasm and a single nucleus.
Characters such as these in antheridial structure suggest that there may I,e
soniething more here than an accidental resemblance to the anthericlia of the
Floridez.
The siermatia of the Laboulbeniales offer possibly an even closer comparison. Within this group they are developed in two ways : exogenous
spermatia are cut off as uninucleate rod-shaped bodies from a specinlized
branch, and there is evidence that ‘‘ as soon as they drop off they are replaced
by others from the same hase” (Faull, 1911, p. 650); endogenous sperinatia
are Constricted off one after another from a mother-cell, and covered by a
thin protoplasmic membrane, are extruded through a more or less elongated
flask-shaped neck (Tliaxter, 1908). I n other words, they escape as thinm d l e d bodies through a split in the antheridial wall, in a manner entirely
coniparable to that described here for Floridez. The resemblances are so
close that one can imagine that the ancestors of the Laboulbeniales rnoy have
been niinute Floridez which first became parasitic upon aquatic insects and
thus reduced in size, only later niigrtiting t o an existence upon aeiial Iiobts.
Such comparisons as the above, however, throw little light upon the origin of
tho nntheridial cornplex, and only tend to emphasize tlie liighly-de\elopd
cliaracter of the male organs in the F1oride:P.
x’. Classification of the Florideie on the Basis of Spermatial Types.
Tht?only pnblishetl c1:tssificatiou of the Elorideze h e e d on the methods of
pprirratial production is tliat of Svedelius (1’308). The species were subdivided 011 two critc.rin dealing with tlie structure of the a n t h i d i a l
mother-cell : first, whetlier this resombld or tlifferrtl from n wgctative cc.11
and. second, wliethcr it w:ts sini1)le or branched. This second c1iar:icter h i s
h e n rejected in the following sclietne, and in its place the variations in the
position a i d niirnl)er of tlie nntheridia hive been substituted. Only thrw
spwics hare been included in tlie group with terminal :intheridi;i, and wlieii
fiirtlwr ltnowleclgo is available it seems prob:tble thitt this sub-gronp will not
persist.
CLASSIFICATION OF S P F X l A T I A L
TSPES.
A. Ant1ioridi:il mother-cell not differing from a vegetative cell eitlicr i n
form or contcnts.
ilEniaZioiz sppp. (Wolfe, 1904).
D~I[,.aehosl,er,,tzl,tzspp. (Rylin, 1916).
B. Antheridial mother-cell differentiated Eroin a vPgctati1 t! cell.
1. Antlieritiia doveloped termin:rlly on tlte motlaer-ccll.
dt(ccrtemia spp. (Svedelius, 1908).
ilfelobesiu spp. (Guignard, 1889).
Ilurcyellu pacliyder~ncccBntt. (Sturch, 1924).
2. ArithericIia developed sub-terminally on the mother-cell.
(a)
Mother-cell subtending two primary sub-terminal nnthcridia.
Tlelrsse&c scozyctitien Lainour. (Svedelius, 1913).
I</wdynzruiizpalmata Ag- (Dclf &, Grubl), 1924).
Cltortclrirs c r i s p s Stackh. (p. 184).
Furcellariaftrstiyitrtn Lain. (p. 238).
r,e,)iarienpiLz'i~tiliBAg. (Kylin, 1312).
Lazwenciu o b t z i . ~Lam. (p. 207).
( b ) Mother-cell subtending two
antheridia.
or
three primary sub-tertniiial
Scitmia furcellata Bivona (Svedelins, 1915 ) .
Cystocloaiuin yurpurasce,rs Kutss. (Kylin, 1922).
1)elesseria siizuosa Lam. (Kjliii, 1922).
I ) . cuscijolin Lam. (Kylin, 1922).
1).crluta Lain. (KyIiri, 1922).
Lowrrtttavin c4aoellosa Gnill. ( Kylin, 1922).
PZocmzium c o c c i w z m Lyngb. (Kylin, 19%2),
Polysip?tonia )iiyres(wu Grev. (Kylin, 192:').
Illudophgllis I$du Kiitz!. (Kyliii, 1923).
250
MISS VIOLET M. GRUEB ON THE
(c)
Mother-cell subtending three primary, sub-terminal antheridia.
Bonnernaisonia asparagoides Ag. (Kylin, 1916).
Polyides rotuiitlits Grev. (Kylin, 1922).
Ceramium rubrum Ag. (p. 231).
Grijithsia corallina Ag. (p. 21s).
G. Bornetiunu Farlow (Lewis, 1909).
1CTitop7iyllumElillice Grev. (p. 196).
N . laceraturn Grev. (p. 199).
Loinenturia ovalis Endl. (p. 189).
Champia parvula Harv. (p. 193).
numontia Jilqornzis Grev. ( p. 231).
Callithainnion brachiatunz Bonnem. (p. 223),
Rhodomela wirgata Kjellm. (Kylin, 1514).
Polysiphonia fastigiata Grev. (p. 210).
( d ) Mother-cell subtending four primary sub-terminal antlieridia.
Polysiphonia violacea Grev. (p. 213).
Chondria tenuissima Ag. (Guignard, 1889).
Lawencia pinnatifida Lam. (p. 204).
Callitliainnion roseurn Harv. (Guignard, 1889).
lialurus eqiiisetifolius Kiitz. (1). 2 2 ) .
It is clear that the position of the antheridia and also their number varies
greatly even among genera of the Floridez, which on anatomical and other
grounds are regarded as closely related. Yet any intenske study of the
niale organs in this group cannot fail to impress the inquirer with a sense
of the reinarliable uniforniity exhibited in the details of development
and liberation i n every case. Although the examples selected for examination in this paper are drawn from species which in ontward form and
cystocarpic development differ widely, yet in each case the formation,
ahs(riction, and liberation of the contents of the individual antheridium is
the same. Similarly, no deviation has been observed so far from what has
come to be regarded as the normal cytological behaviour in the antheridium.
Thus the course of events in the development ,of these male orgnns points
undoubtedly to the fundamental resemblance underlying the species of the
higher Florideae and their probable common origin.
I n conclusion, I should like to thank Dr. E. M. Drlf for her constant
interest and generous assistance throughout the course of this investigation.
My grateful thanks are also due to Mr. A. D. Cotton for many helpful
suggestions ; to Miss Halket, B.Sc., and one or two other friends for gifts
of antheridial material ; and to the Committee of the Dixon Research Fund
for two grants towards the expenses of collecting algal material.
MALE ORGANS O F THE PLORIDEAE.
251
SUMMARY.
1. A detailed investigation of the antheridia in fifteen species of the
Florideix! has been undertaken with a view to ascertaining the course of
events in the development and liberation of the spermatia. Of the species
examined, the antheridial plants were previously entirely unknown in one
ciise (iVito~il~ylluna
lacsrat urn) ; in ten instances ( Chontlrus crispus, Lomentaria
ovalis, Chiimnpia parcula, Xitopliylluni Hillirp, Lawencia obtzisa, Polysiphonia
fustiyiata, Hulurits eqitisetifolius, Callitliainnion brachiatum, C'eramium
Tubrum, and Furcellariu jlzstigiuta) little or nothing was known beyond the
existence of male plants, aud only in four species (Laurencza yinnatijda,
Polysiplionia zliolacea, Grifithsia corullina, and numontia Jilifor)&) had more
or less complete examinations of the structure been made.
2. I t has been shown that in each case a definite number of aatheridia are
produced sub-terminal!y from an antheridial mother-cell which is specially
developed for this function a t the apex of a branch or upon the surface of
the thallus. The number of primary antheridia from each mother-cell may
be two, and is commonly three, even four or rarely five being found. These
antheridia invariably arise as colourless protoplasmic uninucleate outgrowths
clothed in the elongated gelatinous wall of the mother-cell. B y the ringlike ingrowths of this mall a t the base, the contents are abstricted and form
the single spermatium.
3. Tile mature antheridium has been shown to consist of a swollen gelatinous wall surrounding a single apical nucleus, a central vacuole, and a
small amount of cytoplasm. The wall is three-layered ; the outermost
layer is narrow and deeply staining; within is a gelatinous region which
swells greatly a t the time of liberation of the spermatium, while around this
body is a narrow highly refractive region which may possibly represent the
spermatial wall. The spermatium when free measiires from 4 to 9 p in
diameter, and in some instances is undoubtedly surrounded by a very
delicate wall.
4. The method of liberation of the spermatium has been studied from
unshrunken material, and in Lnurencia and Ceramiuni has actually been
watched in living material. The exit always takes place by means of a split
in the anthcriclial wall beginning in the swollen apical region and sometimes extending to the base (i. e. Lawencia). Through this narrow aperture
the wliole contents escape, leaving behind them the empty antheridium as a
shrunken gelatinous sheath. I n some species, e. g . RILodsyntetiinyalmata, the
" cuticle " estrnding over the thallus is known to peel off' in the region of a
ripe antheridial sorus, leaving the antheridia freely exposed to the snrrounding medium. I t has also been deniocstrated here, that in other species,
e . g. Choiidrus, Fiwcellaria, Cewmium, and Polysiphonia, this does not occur,
but the developing antheridia grow up tliroziyli tlie cuticle until tliey reuch
252
MISS VIOLBT M. GRUBB OX THE
the silrface, where they discharge their spcrmatia. I n no case is the
complete antheridium cut off and libwited as described by Yamanouchi €or
PoZysii)hot& uioZucm or Dunn for J ) m ~ o i i t i j/(/brmi.e.
u
5. W i t h the exception o € the species of Yolysiplmnia, observalions made
on mature plnnts have shown that secondary antheridia develop within the
shrivelled sheath-like rerriains of the primary ones, discharging thcir contents
in a similar way. I n one species (Callithamnion bracliiat?rm) tertiary
anthericlia were found.
6. Cytological investigation shows that the antheridial mother-cell is
always uninucleate. This nuclcus divides at the base of each young antheridiuin, and the daughter nucleus passes into the upgrowing projection. At
this stage it is in thc resting condition, but as it moves to the apex of tlie
a n theridiuin it passes into early prophase, deeply-staining granules becoming
visible, connected with one another by linin threads. When the sperrnatiuin
escapes, the nucleus consists of R definite nunihcr of chromatin gmnules or
IGirnclien unitcd by linin threads. This nuinber never varies within a
species, and it is probable that these granules are the true chromosomes.
7. A clmsification oE the sperinatial types among the Floridecc has been
drawn up, based on the position of the antheridial mother-cells and the
number of primary antheridin. Prom this and the preceding investigation
it can be seen that while thc mcthods of spermatial procluction are of little
w e as a character of systematic importance, yet the funda~nentalsiniilarit>y
underlying the development in all species points to a common origin for all
types.
Westtield College, Univmity of London,
January 19%.
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