.Dot. J. Linn. SOC.,
62, pp. 233-239. With 3 plates
April 1969
Pteridophytic features in some Lower Carboniferous seed
megaspores
JOHN M. PETTITT, F.L.S.
Department of Palaeontology, British Museum (Natural History), London, S. W.7
Accepted f o r publication July 1968
Some Lower Carboniferous seed megaspores have triradiate sutures-unequivocal evidence
of their being arranged in a tetrahedral configuration. This type of tetrad arrangement is unknown in the ovules of modern gymnosperms. Some of the fossil tetrads consist of one large
functional megaspore and three smaller abortive spores attached at the apex of the large one.
All four spores have an exinous covering.
Spores arranged in tetrahedral tetrads, and hence with triradiate sutures, are characteristic of
many modern and fossil free-sporing pteridophytes. In possessing this feature the fossil seed
megaspores are more similar to the spores of these pteridophytes than to the megaspores of
modern gymnosperms.
CONTENTS
Introduction
.
Description of material
Discussion
Acknowledgements .
References
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PAGE
233
234
236
238
238
INTRODUCTION
Meiotic division in the megasporocytes of modern gymnospermous seed plants
generally results in a linear tetrad of megaspores. There are a few recorded occurrences
of L-shaped and cruciform tetrads (see Maheshwari & Singh, 1967) in which one or
two of the spores are disposed at right-angles to the longitudinal axis of the ovule,
but such configurations would seem to be unusual if not aberrant, and restricted to
particular genera.
In the majority of gymnosperms only one of the four megaspores of any one tetrad,
usually the innermost, develops to produce a viable gametophyte and becomes surrounded by a megaspore membrane. The other three spores of the tetrad degenerate
soon after the completion of meiosis and well before megaspore membrane deposition.
The abortive spores, therefore, do not receive a covering membrane and there are
no features on the functional spore at maturity to indicate their former presence.
A significant feature of many modern pteridophytes is the production of tetrahedral
tetrads of spores at meiosis. In the homosporous forms and in the microsporangia
of the heterosporous forms all the spores in the sporangium usually develop to
maturity. In the megasporangia of the heterosporous forms there is regular and controlled degeneration of the megasporocytes so that the megasporangium will contain
234
JOHN
M. PETTITT
one or a few tetrads after meiosis (in SeZuginelZu) and also controlled and regular
degeneration of the spores following meiosis so that the megasporangium contains
only one functional spore (in Mursilea). Characteristically, spores produced in tetrahedral tetrads have triradiate laesurae, and all pteridophyte megaspores are of this kind.
These different methods of spore formation serve to distinguish the meiotic cycle
in the living gymnospermous ovule from that in the pteridophyte sporangium. Linear
tetrads of spores are unknown in the pteridophytes and tetrahedral tetrads of megaspores have not been positively demonstrated in the ovules of modern gymnosperms.
I n only two instances, in the ovules of the conifers Thuja occidentalis L. (Martin, 1950)
and Thuja orientalis L. (Coker, 1904), have tetrahedral tetrad configurations been
suggested. Martin’s interpretation, however, was based only on observations of the
positions of the spindles, and tetrad formation was not followed to its conclusion,
and Lawson (1907), who reinvestigated megaspore formation in T . orientalis, was
unable to confirm Coker’s observations.
This paper describes some Lower Carboniferous seed megaspore tetrads which
show definite evidence of having been formed in tetrahedral tetrads and which indicate
that a linear configuration of megaspores has not always been the typical product of
megasporogenesis in the gymnosperms.
DESCRIPTION OF MATERIAL
Kidston (1893) describes two specimens of seed compressions from the Calciferous
Sandstone Series (Cementstone Group, Lower Carboniferous) of East Lothian,
Scotland as Cardiocarpus bicaudatus Kidston. Later, he transferred these fossils to
the genus Sumaropsis (Kidston, 1 9 0 2 ~ ) .I n an earlier publication Kidston (1901)
recorded seeds (as C. bicaudatus) from the River Whiteadder in Berwickshire, $ mile
below Allanton, and the following year (Kidston, 1902b) from the right bank of the
Whiteadder, scaur under Edrom church. The three specimens of seed compressions
from the Kidston Collection of Fossil Plants at the Institute of Geological Sciences,
London (Nos 2767, 2769, 2980) that were used in this study are labelled with the
earlier generic name, but are similar to the seeds included in Samaropsis bicaudata
by Kidston and also come from the Calciferous Sandstone Series of the River Whiteadder in Berwickshire.
The compressed seeds as seen on the rock are more or less circular to slightly oval
in outline and each consists of a central body surrounded by a wing-like carbonaceous
film representing the integument. At the micropylar end of the seed the wing is
extended to form two long, tapering processes or appendages (Plate 1A). T h e appendages in one specimen (2769) are more or less erect, but in the other two they curve
sharply away from the mid-line of the seed. T h e seeds are 8-9.5 mm in length,
excluding the appendages, and about 8 mm in greatest width. T h e two apical appendages extend some 6-9.5 mm beyond the apex of the seed and are about 2 mm wide
at their origin. The integumentary wing is 2.5 mm wide and at the chalaza1 ends of the
seeds is extended to form a short stalk or pedicel about 3 mm long.
The central body seen in each seed compression proves to be the megaspore. One
of these was removed (from specimen 2769), macerated in Schulze’s solution (nitric
SEEDMEGASPORE
FEATURES
23 5
acid and potassium chlorate), extracted in alkali and mounted for microscopical
examination.
The megaspore membrane of C. bicuudutus (Plate 1B) is more or less oval in outline,
some 7 mm long and 3.2 mm wide in the middle, Closely associated with the exine
is a tapetal membrane (Pettitt, 19663) clearly showing the outlines of a cellular
reticulum. The cells of the reticulum measure from 105-245 p in length (with respect
to the longitudinal axis of the megaspore) and 122 -192 p in width and have anticlinal
walls 10-25 p in thickness. The cellular pattern on the tapetal membrane is rather
indistinct at the apex of the megaspore.
The most interesting feature of the megaspore of C. bicuudutus is the clear indication
of a triradiate suture at the micropylar end, that is the end situated below the two
integumentary processes of the seed. The suture consists of simple, slightly curved
laesurae (Plate 1C).The two that can be measured are 105 p and 140 p long, but the
third laesura passes over the apex of the megaspore and its length cannot be determined.
Between the radii of the triradiate suture are distinctly circular areas in which the
exine is rather thicker than on the main body of the spore.
Large numbers of isolated seed megaspore tetrads were recovered from the grey,
fine-grained volcanic ash which outcrops on the foreshore at Oxroad Bay, East
Lothian. The ash is part of the Cementstone Group and the fossil megaspore tetrads
from Oxroad Bay are therefore the same age as the Berwickshire compressions
described above, Gordon (1941) and Barnard (1959) have described seed petrifactions
from Oxroad Bay.
Each megaspore tetrad consists of a large and presumably functional megaspore
and two, or usually three, much smaller and presumably abortive spores arranged at
one end of the large spore. The tetrads are, however, of two distinctly diflerent types.
In the first (type A), the large spore is considerably longer than wide, averaging 3 mm
in length and 1.2 mm in width (Plate 2A, B). The second type (type B) is somewhat
shorter (2.7 mm average length) and wider (1.9 mm average width), and has a prominent tent-pole-like projection at one end. The abortive spores of the tetrad are situated
at the apex of the tent pole (Plate 2C). The exine of the functional megaspore is
7-14 p thick in both types of tetrad.
The form and disposition of the abortive spores at the apices of the functional
spores is strongly reminiscent of the tetrad arrangement in the megasporangium of
some modern heterosporous pteridophytes, for example Marsilea (Plate 3 A ; and also
Pettitt, 1 9 6 6 ~P1.
: 9, figs 1, 2). In most of the fossil tetrads the abortive spores can
be resolved as three discrete bodies with a diameter range of 28-50 p, but they are
occasionally as large as 98 p. The exine is structurally amorphous and bears no external
ornamentation. Individual abortive spores cannot be recognized on some of the specimens, but instead a large mass of amorphous material occupies the same relative
position at the apex of the functional spore. The evidence suggests that these masses
probably originate by the coalescence of the exines of three individual abortive spores.
The seed megaspore tetrads are arranged in a tetrahedral configuration and this fact
is demonstrated by the clear indication of a triradiate suture on the functional spore
of some of the specimens (Plate 3B).
A thin tapetal membrane with strong outlines of a cellular pattern closely surrounds
236
JOHN
M. PETTITT
each megaspore tetrad and completely encloses the abortive spores (Plate 2B; Plate
3 C). In the specimen on Plate 3 E the exine of the functional spore is collapsed and
here the form of the tapetal membrane is particularly evident. The method of formation and the terminology applied to the tapetal membrane in gymnosperms is
described by Pettitt ( 1 9 6 6 ~6).~
I n some seed megaspore tetrads of type A the tapetal membrane is extended to
form a short stalk-like projection at the basal (chalazal)end of the functional megaspore.
The projection is formed entirely by the tapetal membrane enclosing a mass of optically
dense particulate material.
Evidence for the occurrence of tissues external to the tapetal membrane is suggested
by the presence of a thin, delicate and rather incomplete cuticle overlying the tapetal
membrane in some megaspore tetrads. The cuticle shows the outlines of cells that
are several times longer than wide, but exactly what tissue surface it represents is
unclear. Its close association with the tapetal membrane, however, suggests that it is
probably either the cuticle of the nucellus or the inner cuticle of an integument.
DISCUSSION
Long (1960) considers S. bicaudata as the compression form of his petrified
lagenostomalean seed Lyrasperma scotica (Calder) Long because S. bicaudata and L.
scotica look alike externally, are similar in size and are found in sediments of the same
age in the same district. The three Berwickshire compressions described here are
almost identical with one of Kidston’s specimens of S. bicaudata from East Lothian
(No. 1941). Kidston’s other specimen (No. 1940) is somewhat larger than the Berwickshire seeds, and also of rather different shape.
Long’s acceptance of S. bicaudata as compression specimens of L. scotica means
that the three specimens from Berwickshire, now labelled as Cardiocurpus and which
could justifiably be included in S . bicaudata, should be similarly considered to be
compressions of L. scotica.
Mention must be made of the work of Arber (1914) and of Crookall (1933) who
recommend that compressions of bicornute seeds possessing many of the features of
S. bicaudata be included in the genus Cornucarpus Arber. However, the genus as
originally defined by Arber (1914) could not include seeds with a conspicuous lateral
wing.
There can be little doubt of the identity of the fossils from Oxroad Bay as isolated
megaspore tetrads from gymnospermous seeds. The general shape of the functional
megaspore of both types and the presence of the tapetal membrane closely associated
with the functional megaspore exine as well as the occurrence of a tent pole on one
type of functional megaspore exactly correspond to similar features described in
well-authenticated seed petrifactions of the same age. The megaspores with a tent
pole (type B) are very similar in size and shape to those isolated from the petrified
seed Eosperma oxroadme Barnard by Barnard (1959) and it is probable that they were
originally enclosed within seeds of this species. The tetrads of type A cannot confidently be related to any known species of Lower Carboniferous seed petrifaction.
The presence of triradiate sutures on the megaspores of C . bicaudata from the
Whiteadder and on the seed megaspores believed to be those of Eosperma from Oxroad
SEEDMEGASPORE
FEATURES
237
Bay are features of some botanical interest. They indicate that meiosis in the megaspore mother cells of the seeds resulted in a tetrahedral configuration of spores.
Similarly, the presence of a single large and presumably functional megaspore and,
in the Oxroad 3ay fossils, of three smaller and presumably abortive ones, indicates that
while only one spore of the tetrad developed to maturity all four spores received a
covering exine.
While the presence of only one viable megaspore in a mature ovule, except in rather
special cases, is usual in modern gymnospermous seed plants, neither a tetrahedral
configuration of spores nor exine-covered abortive spores have been recorded even
though megasporogenesis has been studied and documented in considerable detail
(Maheshwari & Singh, 1967). In their type of arrangement, therefore, the fossil seed
megaspore tetrads are more similar to the spores of some pteridophytes than to the
megaspores of modern gymnosperms. The organization of the seed megaspore tetrads
from Oxroad Bay bears comparison, for example, to that of the megaspore tetrads of
the modern free-sporing pteridophyte MursiZea. I n the megasporangium of this plant
one large, axially elongated functional spore develops with three very much smaller
abortive ones attached at its apex. The spores are arranged in a tetrahedral configuration and both the functional and abortive spores receive an exine, although the exine
of the functional spore is considerably more complex than that of the abortive spores,
Hoskins & Cross (1946) have reported the occurrence of non-functional tetrads
of megaspores adjacent to the functional megaspore in the Pennsylvanian seed petrifaction Pachytestu Vera Hoskins & Cross. The authors suggest that several megasporocytes occurred in the ovule of Puchytesta, all of which completed meiosis, but that
only one spore from one tetrad developed to maturity and was functional, the remninder aborting, The non-functional megaspores in P. veru are arranged tetrahedrally,
and the reconstruction by Hoskins & Cross (1946: 238, fig. 34) shows a group of three
abortive spores whose position in relation to the functional spore might suggest that
they represent the abortive spores of a tetrad which would include the functional spore
as the fourth member.
We know that the megaspores of the earliest seed, Archaeosperma arnoldii Pettitt
& Beck, from the Upper Devonian, are arranged tetrahedrally with only one spore of
the tetrad large and presumably functional (Pettitt & Beck, 1968).The seed megaspores
described in the present paper show that this type of tetrad organization persisted in
some gymnosperms during the Mississippian, and the specimen of Puchytesta veru
(Hoskins & Cross, 1946) offers evidence of tetrahedra1 tetrads in at least one group
of Pennsylvanian pteridosperms.
The assumption that the seed habit arose from an ancestral free-sporing, though
not necessarily heterosporous, condition is perhaps one that is not now seriously
challenged, and the occurrence of tetrahedral tetrads of megaspores in some ovules
of Devonian and Lower Carboniferous age is consistent with this assumption in
indicating a direct pteridophytic relationship. During the course of ovule evolution
this type of tetrad configuration was evidently replaced by the linear form that is
continued in the extant gymnosperms and angiosperms. Precisely when this change
occurred is not known, although the absence of tetrahedral tetrads (as judged by the
absence of triradiate sutures and abortive spores) in all Pennsylvanian seeds other
238
JOHN
M. PETTITT
than P.Vera and in all geologically younger seeds suggests that it was probably during
the late Mississippian or early Pennsylvanian.
Equally obscure is the question of why the change in tetrad configuration should
have occurred at all. The answer possibly will come from a more complete understanding of the evolution of the functional efficiency or adaptive change of function
of the ovule. A change in tetrad configuration (and possibly megaspore membrane
structure) might be correlated with a change in the nutritional mechanism of the
developing female gametophyte along somewhat similar lines to those that Kremp
(1967) has recently suggested to explain differences in aperture form in the pteridophytes.
ACKNOWLEDGEMENTS
I am very grateful to Dr K. L. Alvin for giving me some material that he collected
from Oxroad Bay and to Sir C. J. Stubblefield F.R.S., until recently Director of the
Institute of Geological Sciences, London, for allowing me to examine specimens in
the Kidston Collection of Fossil Plants. I should also like to express sincere thanks to
Dr W. G. Chaloner for much helpful advice and discussion.
The content of this paper formed part of a Thesis submitted to the University of
London in 1966 for the degree of Doctor of Philosophy.
REFERENCES
ARBER,
E. A. N., 1914. A revision of the seed impressions of the British Coal Measures. Ann. Bat. 23:
81-108.
BARNARD,
P. D. W., 1959. On Eosperma oxroadense gen. et sp. nov., a new Lower Carboniferous seed
from East Lothian. Ann. Bat. 23: 285-296.
COKER,
W. C., 1904. On the spores of certain Coniferae. Bat. Gaz. 38: 206-213.
CROOKALL,
R., 1933. The fossil flora of the Kent Coalfield. Mem. geol. Surv. Summ. Prog. 1932 (11):
44-70.
GORDON,
W. T., 1941. On Salpingostoma dasu: a new Carboniferous seed from East Lothian. Trans.
R. Sac. Edinb. 59: 351-370.
J. H. & CROSS,A. T., 1946. Studies in the Trigonocarpales. Part 1. Pachytesta Vera, a new
HOSKINS,
species from the Des Moines Series of Iowa. Am. Midl. Nut. 36: 207-250.
KIDSTON,
R., 1893. On some new species of fossil plants from the Lower Carboniferous rocks of Scotland. Proc. R. Phys. Sac. Edinb. 12: 258-268.
KIDSTON,R., 1901. Notes on Carboniferous plants from Berwickshire. Mem. geol. Surv. Summ. Prog.
1900: 174-175.
KIDSTON,
R., 1902a. The flora of the Carboniferous Period. 11. Proc. Yorks. geol. polytech. SOL.14:
344-399.
KIDSTON,
R., 1902b. Report on the fossil plants from the Calciferous Sandstones of the Berwickshire
border. Mem. geol. Surv. Summ. Prog. 1901: 179-180.
KREMP,G. 0. W., 1967. Tetrad markings of pteridophytic spores and their evolutionary significance.
Rev. Palaeobot. Palynol. 3: 311-323.
LAWSON,
A. A., 1907. The gametophytes and embryo of the Cupressineae with special reference to
Libocedrus decurrens. Ann. Bat. 21: 281-301,
LONG,A. G., 1960. On the structure of ‘Samaropsisscotica’ Calder (Emended) and ‘Eurystomaangulare’
gen. et sp. nov., petrified seeds from the Calciferous Sandstone Series of Berwickshire. Trans. A.
Sac. Edinb. 64: 261-280.
MAHESHWARI,
P. & SINGH,H. 1967. The female gametophyte of gymnosperms. Biol. Rev. 42: 88-130.
P. C., 1950. A morphological comparison of Biota and Thuja. Proc. Pa. Acad. Sci. 24: 65-112.
MARTIN,
PETTITT,J. M., 1966a. Exine structure in some fossil and recent spores and pollen as revealed by light
and electron microscopy. Bull. BY,Mus. nat. Hist. (Geol.), 13: 221-257.
PETTI~.T,
J. M., 1966b. A new interpretation of the structure of the megaspore membrane in some
gymnospermous ovules. J. Linn. Sac. (Bat.),59: 253-263.
PETTITT,
J. M. & BECK,C. B. 1968. Archaeosperma arnoldii-a cupulate seed from the Upper Devonian
of North America. Contr. Mus. Paleont. Univ. Mich. 10: 139-154.
Bot.9. Linn. SOC.,62 (1969)
JOHN M. PETTITT, F.L.S.
Plate 1
( F a c i q p . 238)
Bot. J . Linn. Sor., 42 (1Y69)
Plate 2
B0t.J. Linn. SOC.,62 (1969)
JOHN M. PETTTTT, F.L.S.
Plate 3
SEED
MEGASPORE
FEATURES
239
EXPLANATION O F PLATES
(The specimens figured in Plate 1 are in the Kidston Collection of Fossil Plants at the Institute of
Geological Sciences, London and those in Plates 2 and 3 in the palaeobotanical collections at the British
Museum (Natural History), London. T h e registered number of each specimen is given in parenthesis
in the explanation.)
PLATE
1
Cavdiocarpus bicapcdatus Kidst.
A. Complete seed. The dense central body is the megaspore. x 8 (2985).
B. Entire megaspore removed from a seed compression. The micropylar end of the megaspore is
towards the top of the figure. The tapetal membrane forms a conspicuous reticulum on the surface of
the megaspore exine. x 35 (2767).
C. Triradiate suture at the apex of the megaspore shown in B. The arrows indicate the three laesurae.
x 450.
PLATE
2
A-C. Seed megaspore tetrads from Oxroad Bay, East Lothian. A and B are megaspore tetrads of type
A; C is a megaspore tetrad of type B-notice the tent pole at the apical end of the functional spore.
The abortive spores are discernible at the apices of the large spores. The tapetal membrane and the
basal stalk-like projection are clearly seen on the tetrad in B. A, x 36 (V. 53622); B, x 20 (V. 53623);
C, x 42 (V. 53624).
PLATE
3
A. Abortvie spores at the apex of an acetolyzed functional megaspore of Marsilea drummondii A. Br.
x 530 (V. 53625).
B-D. Abortive spores of megaspore tetrads from Oxroad Bay, East Lothian. In B the arrows indicate
the laesurae of the triradiate suture. The arrow in C indicates the tapetal membrane which encloses the
abortive spores. B and D are tetrads of type A, C is a tetrad of type B. B, x 330 (V. 53626); C, X 210
(same specimen as Plate 2C); D, x 150 (same specimen as Plate 2B).
E. Tapetal membrane with cellular pattern surrounding a collapsed functional megaspore of tetrad from
Oxroad Bay. x 32 (V. 53627).