7

The subkingdom Embryophyta (cont.):

division Tracheophyta, Part 2
Polypodiopsida (ferns) largely herbaceous, a number of ferns of the
The class Polypodiopsida encompasses both tropics and subtropics (mostly belonging to the
wholly fossil and also living representatives, many family Cyatheaceae) achieve the form and stature
of which have a long fossil history. The general fea- of simple trees. Cyathea in the Kermadec Islands,
tures of the class can be summarized as follows: for example, has a palm-like habit and reaches a
height of 20 m (65.5 ft). At the other extreme are
Sporophyte herbaceous or arborescent, in many
minute epiphytes hardly bigger than leafy liver-
forms rhizomatous. Leaves often compound (meg-
aphylls). Vascular system of tracheids and phloem,
worts (with which they commonly grow). Some
usually lacking clearly defined secondary tissue. families of ferns have a rich fossil record, their dis-
Stele often divided into meristeles. Leaf traces tinctive characteristics being recognizable as far
often complex, leaving a parenchymatous gap in back as the Carboniferous (see pp. 179, 211). These
the stele at their origin. Sporangia borne on ferns are amongst the most ancient of living
leaves, but never on the adaxial surface of a micro- plants.
phyll. Mostly homosporous; a few (living and A significant feature of many extinct and
fossil) heterosporous. Gametophytes (known only living Polypodiopsida is the close resemblance, in
in living forms) simple, usually autotrophic, appearance, development and behavior, between
lacking vascular tissue. Archegoniate.
leaves and branch systems. In species of the
Spermatozoids multiflagellate. Embryogeny typi-
Carboniferous Botryopteris (p. 176), for example,
cally endoscopic.
the decumbent fronds gave rise here and there to
The living Polypodiopsida fall into six orders, root and shoot buds. These evidently played a
namely the Marattiales, Ophioglossales, Psilotales, major rôle in vegetative propagation. Similar
Osmundales, Polypodiales and Hydropteridales, behavior is seen today in some living ferns (p. 194).
referred to collectively as ferns. Of these, the first In Stromatopteris, a rare fern of New Caledonia, it
three orders are eusporangiate (p. 151), while the is difficult to distinguish between frond and axis.
Polypodiales, and the Salviniales and Marsileales Similarly, aerial shoots (“fronds”) and branches
(p. 212) of the now validated Hydropteridales arise from the creeping rhizome of the Psilotales
(p. 216), are leptosporangiate (p. 190). The in an almost identical manner. Further, the
Osmundales have in general leptosporangiate fronds of the fern Stromatopteris and the aerial
characteristics, but the sporangia develop in a shoots of Tmesipteris (p. 185) are morphologically
manner recalling that of eusporangiate sporangia. closely similar.
The ferns are an important element of the world’s These stem-like properties of the megaphyll
flora, numbering about 10 000 species and being have given rise to the view that it is fundamen-
particularly conspicuous in warm humid regions. tally different from the microphyll of the
They show the greatest range of growth forms Lycopodiopsida. Its origin clearly lies within the
amongst the vascular archegoniates. Although Trimerophytopsida (p. 161) of the Lower Devonian.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 173

The lateral appendages of these early axes appear vascular system of the stem of the zygopterids was
to have yielded both the reduced leaves of the commonly a protostele, often with a parenchyma-
Equisetopsida (p. 162) and the branching leaf tous medulla. The fronds, which were usually in a
systems of the Cladoxylopsida (p. 171), progymno- recognizable phyllotactic spiral, received a single
sperms (p. 218) and ferns. The pinnules of these vascular trace which assumed in the petiole a
larger structures presumably arose by the flatten- definite and characteristic symmetry.
ing and fusion of the ultimate branchlets. The Consequently the genera and species of these
ferns distinguished themselves from the gymno- ferns are largely based upon the profile of the leaf
sperms by remaining largely homosporous, and trace in transverse section. In Metaclepsydropsis, for
failing to develop extensive secondary tissues. example, the section was hour-glass-shaped (clep-
Although the absence of secondary thickening sydroid). The protoxylem lay toward each pole,
limited the stature attained by the ferns, they each group associated with an island of paren-
were, nevertheless, an important component of chyma. Pinna traces arose from each pole in alter-
Paleozoic floras. nate pairs, in register with the quadriseriate
branching. In Stauropteris (sometimes separated in
Extinct orders of ferns the Stauropteridales), where the frond was simi-
Although it is generally agreed that no true ferns larly constructed, the rachis contained four
have yet been detected in the Devonian, it seems groups of tracheids ascending in parallel. Well-
likely that they share a common origin with other defined phloem with elliptical sieve areas has
megaphyllous groups within the early been seen in several of these petrified leaf traces.
Trimerophytopsida (see Chapters 6 and 8). In several zygopterid fronds there were small
Questions remain regarding the relationship of branched emergences, each with an exiguous vas-
the eusporangiate and leptosporangiate ferns. cular supply, at the base of the rachis and at the
Some analyses indicate a derivation of the leptos- sites of branching of the fronds. These are referred
porangiate from the eusporangiate, while others to as aphlebiae (Fig. 7.2), and occur in some living
favor a parallel development of both forms from ferns (e.g., Hemitelia and other tree ferns).
the Zygopteridales. Although metaxylem tracheids in radial rows
are occasionally seen in zygopterid stems, it is
The Zygopteridales doubtful whether these were produced by
The Zygopteridales, an order mostly confined to cambial activity. As in living ferns secondary activ-
the Carboniferous and regarded as truly fern-like, ity seems to have been absent.
may have been represented in the Devonian by the The sporangia of many zygopterids were
remarkable Rhacophyton (Fig. 7.1). This was prob- massive (often reaching or exceeding 2.5 mm
ably a large bushy plant reaching a height of (0.1 in.) in length) and presumably eusporangiate
about 2 m (6.5 ft). The main stem, about 2 cm (p. 151) in origin. In many forms (but not in
(0.75 in.) in diameter, bore lateral branch systems Rhacophyton) a distinct annulus of thickened cells
of two kinds. The sterile were complanately interrupted by a thin-walled stomium is visible.
branched leading to a spray of branchlets, appro- Homospory appears to have been general, but an
priately referred to as a frond. The fertile branches example of heterospory was possibly provided by
had a much more complicated morphology. At the Carboniferous Stauropteris burntislandica. The
each node of the axis of the frond (rachis) there sporangia (Fig. 7.3) of this species (known as
were two sterile branches subtended by two Bensonites), which were parenchymatous at the
densely branched tassels of sporangia. The base, produced only one tetrad, consisting of two
branching was clearly not in one plane, but quad- large and presumably functional spores about
riseriate. Rhacophyton (sometimes given its own 200 ␮m in diameter, with two small, possibly abor-
order, Rhacophytales) was probably homosporous. tive, spores lying between them. Interpretations of
The quadriseriate branching of the frond is Bensonites as indicative of heterospory depend,
characteristic of the Carboniferous zygopterids, of however, upon the assumption that reproduction
which Metaclepsydropsis is an example (Fig. 7.2). The of the parent was normal. A triploid form of living
174 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.1. Reconstruction of Rhacophyton ceratangium. (A) imate to assume that triploidy, and subsequent
Spiral arrangement of fronds. Oval areas (as at the arrow, f) meiotic irregularities resembling those in I. coro-
represent the position of fertile structures. Scale bar 20cm.
mandelina, were not already represented in the
(B) Detail of primary pinna. (From Stewart and Rothwell.
Paleozoic pteridophytes. Although the existence of
1993. Paleobotany and the Evolution of Plants, 2nd edn.
Cambridge University Press, New York.) regular heterosporous reproduction in Stauropteris
burntislandica may therefore be doubtful, it is strik-
ing that a similar form of apparent megaspory
Isoetes (p. 159), I. coromandelina, has been found to (although the two accompanying smaller spores
produce spore tetrads similar to those of Bensonites. were not detected) was found in an earlier zygop-
Two of the spores, however, lack nuclei. terid, Gillespiea, from the Upper Devonian of
Apparently, after the first division of meiosis the Virginia. This may, of course, have been an early
nucleus fails to divide again, but the mother cell example of dyad formation, accompanied by the
continues to form a tetrad, resulting in two of the omission of the second division of meiosis, an ireg-
products being anucleate. A similar mechanism ularity not uncommon in living free-sporing
may have produced Bensonites. It would not be legit- archegoniates, and possibly of ancient origin.
TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 175

Figure 7.2. Metaclepsydropsis.

Reconstruction of portion of frond
showing quadriseriate arrangement
of pinnae. The stem was
rhizomatous.

Figure 7.3. Stauropteris

burntislandica. (a) Megasporangium
(from a specimen in the Oliver
Collection, Natural History
Museum, London). (b) An isolated
tetrad (Bensonites). (After Chaloner.
1958. Annals of Botany (New Series)
22.)
176 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

curvature being adaxial. Where known, the vascu-

lar system of the axis appears to have been a proto-
stele lacking secondary thickening. Some species
of Botryopteris probably formed sprawling clumps,
Figure 7.4. Botryopteris forensis. (a) Reconstruction of a with decumbent branches rooting at intervals.
plant growing as an epiphyte on Psaronius (Fig. 7.11). Scale bar Others (Fig. 7.4a) were epiphytes, as were species of
10cm. (b) Sporangia. Scale bar 1mm. (Both from Stewart and Tubicaulis.
Rothwell. 1993. Paleobotany and the Evolution of Plants, 2nd The sporangia of the coenopterids (Fig. 7.4b)
edn. Cambridge University Press, New York; (b) after Galtier. were less massive than those of the zygopterids,
1971. Naturalia Monspeliensia Botanique 22.) and may have been leptosporangiate (p. 190) in
origin. The wall was a single cell thick and fur-
In a species of the Carboniferous Stauropteris, nished with a simple terminal opening mecha-
believed to be homosporous, spores germinating nism similar to that of Osmunda (p. 190). They were
in a manner typical of living ferns have been often attached to pinnules, either near the
found petrified within sporangia. Apart from a margin or superficially. The spores were trilete,
few isolated instances of this kind, nothing often with finely decorated exines, 40–70 ␮m in
further is known of the gametophytic phase of the diameter. There have been no indications of
zygopterids. heterospory.
The zygopterids and coenopterids persisted
The Coenopteridales until the close of the Paleozoic era, but so far as
With the exception of those forms clearly refer- known are absent from the Mesozoic.
able to families still existing, the remainder of
the Carboniferous ferns are placed in the Existing orders of ferns
Coenopteridales. As in the zygopterids, the fronds
of the coenopterids were often highly branched The Marattiales
and spreading, but the symmetry remained com- This small order of ferns is wholly tropical.
planate as in the frond of a living fern. Genera are Although not conspicuous in contemporary vege-
again defined by the shape of the leaf trace. In tation, they have a remarkably rich fossil record,
Botryopteris, for example, the trace was ␻-shaped and marattialean ferns have been recognized with
in transverse section, the convexity of the curva- certainty as far back as the Carboniferous.
ture being abaxial and the protoxylem lying at the Of the living genera, the most common are
tips of the adaxial extensions. In Tubicaulis, by con- Angiopteris and Marattia. Both have short upright
trast, the trace was C-shaped, the convexity of the trunks bearing large, pinnately branched and
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 177

show differentiation into palisade and mesophyll,

with the stomata confined to the lower surface.
The stems of the upright forms usually grow
not from a single apical cell (as in most ferns) but
from a more massive meristem. The leaves form
an apical crown, and since each receives an exten-
sive trace, consisting of several strands of vascular
tissue, the form of the stele is highly complex. A
transverse section of the stem shows a number of
concentric cycles of partial steles (meristeles), and
dissection reveals that the meristeles of each cycle
anastomose freely, occasional anastomoses also
occurring between adjacent cycles. Leaf traces
originate from the outer cycle of meristeles. Root
traces, which may arise at any depth, pass out
obliquely into the cortex. An endodermis,
although present in young plants, is usually
absent from the stelar regions of the older.
Tapering tracheary elements with long scalar-
iform perforation plates have been observed in
the xylem of stems and roots of a number of
Marattiales. These can justifiably be regarded as
vessels. The stems of the Marattiales as a whole
contain little if any sclerenchyma, but there is an
abundance of mucilage canals and tannin sacs, as
elsewhere in the plant (Fig. 7.6). These indicate a
particular kind of carbon metabolism that seems
Figure 7.5. Angiopteris evecta. Specimen in Las Cruces to have been widespread amongst the ancient
Botanic Garden, Puerto Rico. (Photograph provided by ferns.
C. Jermy, Natural History Museum, London.)
r e p ro d u c t i o n
rather fleshy fronds (Fig. 7.5), sometimes reaching The fertile fronds resemble the sterile in most
a length of 5 m (16.5 ft), and showing circinate ver- genera, and the sporangia, always eusporangiate
nation (i.e., the fronds expand from a closely in origin, are confined to the lower surface. In
coiled immature state). At the base of the petiole Angiopteris they arise in two ranks beneath veins
are two prominent stipules which persist after the toward the margins of the pinnules (Figs. 7.7a and
leaf has fallen. Christensenia, a monotypic genus of 7.9a). The group of sporangia is referred to collec-
the Indo-Malayan region, has a creeping rhizome tively as a sorus. Dehiscence of the sporangia,
with palmately divided fronds, which have the along a longitudinal stomium, is directed toward
distinction of containing the largest stomata the mid-line of the sorus (Fig. 7.9a). In Marattia the
known in the plant kingdom. Danaea, a small fertile regions are similar, but the sporangia are
genus confined to tropical America, has one congenitally fused into a synangium (Figs. 7.7b, 7.8
species with a simple, ovate frond, and another and 7.9b). As the synangium matures and dries, it
with a small pinnate frond in which the lamina is splits longitudinally into two valves (Fig. 7.9b), and
pellucid and filmy. These forms, although reveal- each compartment dehisces by a pore in the inner
ing the diversity in the fronds of the Marattiales, face. The number of spores in each sporangium
are nevertheless unusual, and a massive angular (or synangial compartment) in the Marattiales
construction is characteristic of the fronds of the reaches 1000 or more.
Marattiales as a whole. The laminae normally Given warmth, moisture and light, the spores
178 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.6. Angiopteris evecta.

Transverse section of secondary
rachis.

Figure 7.8. Marattia. Vertical section of synangium.

germinate rapidly, and after passing through a

brief filamentous phase generate a green thalloid
gametophyte with apical growth, resembling a
thallose liverwort such as Pellia. Although auto-
trophic, the lower cells contain an endophytic,
and presumably mycorrhizal, fungus. The gamet-
ophyte can be long-lived and old specimens reach
a length of 3 cm (1.4 in.) or more. The antheridia
are sunken, and occur on both surfaces, but the
Figure 7.7. Fertile pinnules of the Marattiales. (a)
archegonia, also sunken, are confined to the
Angiopteris. (b) Marattia.
median region of the ventral surface. The protrud-
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 179

Figure 7.9. (a) Angiopteris evecta. The abaxial surface of a

fertile pinnule showing the grouping of the sporangia into
sori, and the arrangement of the sori. The sporangia have
dehisced. (b) Marattia fraxinea. The abaxial surface of a fertile
pinnule showing the arrangement of the synangia. The
synangia have dehisced. Scale bars 2.5 mm.

Figure 7.10. Angiopteris evecta.

Vertical section of archegonium. (a)
Immature. (b) Prior to fertilization.
(After Haupt, from Foster and
Gifford. 1959. Comparative
Morphology of Vascular Plants.
Freeman, San Francisco. ©1959.)

ing neck cells form little more than a cap over the fossil history
ventral canal (Fig. 7.10). The Marattiales are represented in the
The first division of the zygote is by a wall Carboniferous period by both vegetative and
transverse to the longitudinal axis of the archego- fertile material. Psaronius, for example, is the
nium. The subsequent embryogeny is endoscopic, remains of a trunk surrounded by a mantle of
and the embryo often emerges from the upper descending roots (Figs. 7.11 and 7.12). The vascular
side of the gametophyte. A suspensor has been tissue, which was wholly primary, formed a poly-
reported in Danaea, but is elsewhere lacking. cyclic array of anastomosing, band-like meristeles.
Vegetative propagation of Angiopteris in glass- Morphologically and anatomically Psaronius is so
houses is achieved by culturing the massive sti- suggestive of an arborescent Angiopteris that there
pules in peaty soil. In these conditions they will seems little doubt of its affinity. Fronds of
give rise to one or more shoot buds. Asexual repro- Psaronius are encompassed by the genus Pecopteris,
duction of this kind may occur sporadically in while fertile material is represented by
nature. Scolecopteris (Fig. 7.13) and Eoangiopteris, the
180 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

sporangia of which were very similar to those of

Angiopteris, although there were minor differ-
ences in the sorus. Fertile fronds of marattialean
ferns, resembling those of various modern
genera, are also found throughout the Mesozoic.

The Ophioglossales
The Ophioglossales form a small, and morpholog-
ically peculiar, order of living ferns which, since
they have no well-established fossil record, are of
obscure origin. In all members the fertile region
of the frond takes the form of a spike or pinnately
branched structure, clearly set off from the vege-
tative portion. A feature that separates the
Ophioglossales from other living ferns is that the
fronds, instead of showing circinate vernation
(see p. 177), grow marginally from a more or less
flat primordium. That of Botrychium lunaria when
young shows a distinct kind of folding, the upper
margins of the pinnules being covered by the
lower margins of the pinnules above.
Of the three genera of the class, Botrychium
(moonwort) and Ophioglossum (adder’s tongue)
(Fig. 7.14b) are fairly widespread, the former
mainly in the north temperate zone and the latter
Figure 7.11. Psaronius, reconstruction. Scale bar 25cm. chiefly in the tropics. Both genera include species
(From Morgan. 1959. Illinois Biological Monographs 27.) native to the British Isles. The third genus,
Helminthostachys (Fig. 7.15), is restricted to the
Polynesian Islands in the South Pacific and a few
regions in the Asian tropics, but is often locally
abundant along roadsides. In parts of rural India
the young frond is used as a vegetable.

Figure 7.12. Psaronius conjugatus.

Transverse section of stem. From a
specimen in the Oliver Collection
(Natural History Museum, London).
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 181

Figure 7.13. Scolecopteris incisifolia.

Reconstruction of portion of fertile
pinnule. (After Mamay, from
Andrews. 1961. Studies in
Paleobotany. Wiley, New York.)

In Botrychium (Fig. 7.14a),

where the frond is annual, the
vegetative and fertile parts are
pinnately branched. Helmin-
thostachys is basically similar,
but the branches of the fertile
part of the frond are very con-
tracted (Fig. 7.15). In Ophio-
glossum (Fig. 7.14b) the sterile part of the frond,
which is reticulately veined, is elliptical and
entire or, in a few epiphytic forms, dichotomously
lobed. The fertile part is usually a simple
unbranched spike.

t h e va s c u l a r s y s t e m o f t h e r h i z o m e
The Ophioglossales are rhizomatous, growth
taking place from a single apical cell. In
Botrychium the rhizome of the young plant con-
tains a medullated protostele (Fig. 7.16), but in the
stele of older plants a parenchymatous area perfo-
rates the xylem anterior to the departing leaf
trace. The endodermis remains wholly exterior.
We thus arrive at a stele intermediate between a
protostele and a solenostele, often referred to as a
siphonostele (see Fig. 7.28). A rudimentary sole-
nostele does in fact arise in some species of
Botrychium as a result of an endodermis appearing
on the inside of the xylem cylinder. The stele
shows a number of points of anatomical interest.
The metaxylem tracheids, for example, bear
bordered circular pits, found outside the
Ophioglossales only in the gymnosperms and
angiosperms. There is also limited cambial activ-
ity leading to some secondary xylem, otherwise
unknown in living ferns. Apart from this feature,
the anatomy of Ophioglossum and Helminthostachys
resembles that of Botrychium.
The roots of all Ophioglossales tend to be
Figure 7.14. (a) Botrychium lunaria, habit. (b) Ophioglossum
vulgatum, habit. Scale bar 2cm. (After Lowe. 1874–78. Our
fleshy. The central vascular strand is either diarch
Native Ferns. Groombridge, London.) or, in the larger roots, polyarch. Many species of
Ophioglossum form vegetative buds on the roots.
182 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.15. Helminthostachys.

Upper part of plant showing fertile
spike. Scale bar 5 cm.
(Photographed in Sri Lanka by R. D.
E. Jayasekera.)

r e p ro d u c t i o n The gametophyte of Botrychium is a flattened

The spherical sporangia of Botrychium, eusporan- tuberous prothallus, subterranean and invested
giate in origin, arise in two ranks on the ultimate with an endophytic fungus, presumably in mycor-
branches of the fertile part of the frond. The spore rhizal relationship (Fig. 7.17). Gametophytes have
mother cells are enclosed in a tapetum, several also been raised in pure culture, but germination
cells in thickness, in whose disintegration prod- is poor unless the spore walls are first abraded by
ucts the spores mature. Even at maturity the wall shaking with sand. A period of darkness is also
of the sporangium is massive, and stomata inter- essential for satisfactory germination, although
rupt its outer layer. The spores, a few thousand in following germination the gametophytes will
number, are released by transverse dehiscence. grow in the light. Chlorophyll remains absent and
Botrychium, like the Ophioglossales as a whole, is sugar is essential for successful growth. The
homosporous. antheridia are sunken, and each yields over 1000
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 183

sometimes approaching 5 cm (2 in.) in length.

Both antheridia and archegonia are sunken. The
embryogeny is exoscopic.
Asexual reproduction by means of root buds is
well known in Ophioglossum, sometimes leading to
stands of a species more rapidly than sexual repro-
duction. Cleared lands in New Guinea, for
example, were observed to become rapidly colo-
nized by large populations of Ophioglossum derived
almost entirely from root buds. Some species of
Botrychium produce spherical multicellular
gemmae, up to 1 mm (0.04 in.) in diameter, from
meristematic regions of the cortex of the rhizome.
On abscission they develop in a manner similar to
that of embryos.
Figure 7.16. Botrychium lunaria. Transverse section of
rhizome. phylogeny
The Ophioglossales have no close relatives, and
multiflagellate spermatozoids. The archegonia, of the evidence of distribution and comparative
quite normal construction, are partially anatomy, particularly in relation to the massive
immersed. The embryogeny of Botrychium is some- eusporangiate sporangia and the stele, points to
what variable: in some species there is a suspen- their being the relicts of an ancient lineage. The
sor and development is endoscopic, in others the bordered pits of the tracheids, the epiphyllous
suspensor is lacking and the development exos- origin of the fertile regions, and the production of
copic. The first organ to emerge is the root, secondary xylem in the rhizome of Botrychium
infected from the first with the same endophytic have suggested to some that the Ophioglossales
fungus as the gametophyte. The young plant may are derived from some ancient progymnosperm
remain subterranean in an immature condition stock (p. 218), and that there is no close relation-
for several years. Some individuals may even ship with the polypodialean ferns. The negligible
become green and complete their life cycle while fossil record of the Ophioglossales as a whole sug-
remaining covered by litter. Permanently albino gests that they were never very numerous.
forms are also known, but the inheritance of this The chromosome numbers of Ophioglossum are
condition has not been studied. It seems that remarkably high, exceeding 1000 in one species.
photosynthesis plays a minor rôle in the metabo- The living forms may therefore be ancient poly-
lism of Botrychium, nutrition being, in some forms ploids.
at least, provided entirely by the mycorrhizal
fungus. Despite the gametophyte being subterra- The Psilotales
nean, interspecific hybrids of Botrychium are This order is represented by two small genera,
known and sometimes locally frequent. Psilotum (Fig. 7.19a) and Tmesipteris (Fig. 7.19b). The
The reproduction of Helminthostachys is similar former is pan-tropical and not uncommon, but
to that of Botrychium, but the dehiscence of the the latter, although locally abundant, is confined
sporangia is longitudinal, and the embryogeny is to Australasia and Polynesia.
regularly endoscopic. In Ophioglossum the sporan- The sporophyte of Psilotum, which may be
gia, which occur as two rows partially embedded either terrestrial or epiphytic, consists of upright
in the spike (Fig. 7.18), open by transverse clefts. (or, in one epiphytic species, pendulous), dichoto-
Those in the central region of the spike mature mously branching axes arising from a horizontal
first. Each contains numerous spores, in some system of similarly branching rhizomes. The
species of the order of 15 000. The gametophyte of rhizomes bear rhizoids, and contain an endo-
Ophioglossum is subterranean and cylindrical, phytic fungus, probably a symbiotic mycorrhizal
184 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.17. Botrychium

virginianum. Vertical section of
gametophyte. (After Campbell.
1905. The Structure and Development
of Mosses and Ferns. Macmillan, New
York.)

Figure 7.18. Ophioglossum

vulgatum. Longitudinal section of
young fertile spike.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 185

Figure 7.19. (a) Psilotum nudum,

fertile region. The trilocular
sporangia are subtended by small
forked bracts. (b) Tmesipteris
tannensis, fertile shoot. The bilocular
sporangia are attached at the forks
of conspicuous bifid bracts. Scale
bars 0.5cm.

a b

association. Small scales, which are at first green in the aerial stems, but tends to be mesarch in the
but soon become scarious, occur at irregular rhizome. Phloem surrounds the xylem, but, apart
intervals on the aerial stem. They lack a vascular from the lateral sieve areas, the sieve cells are
strand, but in one species a strand does approach little different from elongated parenchyma cells.
the base of the scale, but stops below the inser- An endodermis, separated from the phloem by a
tion. Stomata are present, but are confined to the narrow zone of pericyclic parenchyma, marks the
epidermis of the aerial stem. boundary of the stele. It forms a usually single-
The aerial stem of Psilotum contains a simple layered sheath around the stele, its cells character-
stele (protostele), frequently enclosing in the ized by the Casparian strip, a band of fatty
upper regions a central parenchymatous medulla. material embedded in the radial walls. The cells of
The xylem, consisting solely of tracheids, is often the inner cortex, adjacent to the endodermis,
stellate in transverse section, the arms narrowing often contain accumulations of phlobaphene, a
and standing opposite poorly defined ribs at the condensation product of tannin.
exterior of the stem (Fig. 7.20). The xylem is exarch The branches of both the aerial and terrestrial
186 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.20. Psilotum nudum.

Transverse section of lower part of
aerial branch.

systems of the sporophyte

grow indefinitely from single
or small groups of apical cells.
There is no evidence that the
dichotomy of the axes follows
median longitudinal division
of a single apical cell, as in
certain algae (e.g., the brown
alga Dictyota dichotoma (p. 92)).
Tmesipteris is frequently an
epiphyte with trailing stems
(Fig. 7.19b). The general
morphology is similar to that
of Psilotum, but branching is
much less frequent. The
appendages are larger and
more leaf-like, remaining
green and possessing stomata,
and also frequently a vascular
strand. The insertion of the
appendages is, however, peculiar, being longitudi-
nal instead of transverse, so that they appear more
as flange-like outgrowths of the axis than as
normal foliage leaves.

r e p ro d u c t i o n
Spores are produced in the upper region of the
sporophyte of Psilotum (Fig. 7.19a). The spore-
bearing organs, which are distant from each
other, are three-lobed, and each is subtended by a
bifid appendage. The lobes correspond to three
internal chambers (Fig. 7.21), separated by septa,
and each filled with spores. It is still not clear
whether this spore-bearing organ is to be inter-
preted as a trilocular sporangium or as a synan-
gium formed by the fusion of three sporangia.
Three primordia are, however, visible early in the
ontogeny of the organ, perhaps indicating its syn-
angial nature. Since a distinct vascular strand
extends into the base of the synangium, it is
usually regarded as terminating a lateral axis,
rather than arising in association with a sporo-
phyll. This view is strengthened by the existence
Figure 7.21. Psilotum nudum. Transverse section of
of a cultivated form, “Bunryu-zan”, in which the trilocular sporangium (synangium).
synangia terminate vertical axes.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 187

Figure 7.22. Psilotum nudum. (a)

Gametophyte. (b) Mature
archegonium. (c) Antheridium. (d)
Young sporophyte. (After Bierhorst.
1953. American Journal of Botany 40
and Bierhorst. 1954. American
Journal of Botany 51.)

zoids. The archegonium has

four tiers of neck cells, but at
maturity all but the lower one
or two tiers degenerate.
Fertilization, which depends
upon the presence of a film of
water, is brought about by spi-
rally coiled, multiflagellate
spermatozoids.
The first division of the
zygote is in a plane transverse
to the longitudinal axis of the
archegonium, as in the bryo-
phytes. The outer (or epibasal)
cell yields the apex of the
Each of the three groups of archesporial cells embryo, and the inner (or hypobasal) the foot. The
in the synangium arises from several cells, and is embryogeny is thus exoscopic.
thus eusporangiate in origin. Part of the periph- In Tmesipteris, spore-bearing organs occur in
eral archesporium, although not regularly the upper parts of some of the shoots, each sub-
layered, functions as a tapetum. The remainder tended by a bifid appendage (Figs. 7.19b and 7.23).
yields sporogenous cells. Meiosis leads to tetrads These organs are regarded as synangia terminat-
of monolete spores. The exine is lightly reticulate ing very short lateral branches, but in Tmesipteris
with no very distinct ornamentation. The massive each consists of only two fused sporangia.
wall of the sporangium, some five cells thick at The reproduction of Tmesipteris is very similar
maturity, dehisces at three sites symmetrically to that of Psilotum. The foot of the young embryo
placed with respect to the loculi. of Tmesipteris is lobed, and the whole bears a strik-
The gametophyte of Psilotum is a subterranean ing resemblance to the young sporophyte of
axial structure (Fig. 7.22), dichotomously branch- Anthoceros. It is doubtful, however, whether this
ing, and resembling short lengths of the sporo- bears the phylogenetic significance that some
phytic rhizome. The similarity extends to the have claimed.
anatomy, the finer axes being wholly parenchyma-
tous, and the broader containing a central vascu- origin
lar strand. The peripheral cells, like those of the The anatomical and reproductive features of the
rhizome, house an endophytic fungus. Both the Psilotales recall the Rhyniopsida and
gametophyte and the sporophytic rhizome Trimerophytopsida of the Paleozoic. There is,
produce globular multicellular gemmae, a means however, no continuity in the fossil record, and
of vegetative propagation. the origin of the Psilotales remains conjectural.
Antheridia and archegonia arise from superfi- Their generally high chromosome numbers
cial cells in the region of the growing points of the (52–210 in the gametophytic phase) may indicate
gametophyte (Fig. 7.22). The antheridia, depend- a complex polyploid series developed with little
ing upon their size, liberate up to 250 spermato- evolutionary change over geological time, but
188 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

a crown of bipinnate leaves. The pinnules are com-

monly leathery, but in Leptopteris, a fern of New
Zealand and New Guinea allied to Todea, the
lamina is filmy (as in the Hymenophyllaceae, p.
194), a single cell thick and lacking stomata. The
leaves of all Osmundales show circinate verna-
tion. The robust leaf bases give considerable
support to the stem and in consequence older
specimens are able to develop a dendroid form.
Remains of osmundalean ferns, retaining suf-
ficient features to permit firm identification of
their affinity, are known from the Upper Permian
(late Paleozoic), and the record, supported by pre-
served axes, fronds and sporangia, continues
through the Mesozoic to the present. The stems of
early representatives of the Osmundales were
protostelic, but in later forms the central part of
the stele became replaced by pith, leading to a
siphonostele (p. 192). In living Osmunda (Fig. 7.24)
the stele is basically a siphonostele, and the
phloem and endodermis remain wholly external.
The continuity of the xylem, however, is broken at
the departure of the leaf traces, leaving a so-called
“leaf gap” which closes again anteriorly. Since,
Figure 7.23. Tmesipteris tannensis, habit. when dissected, the xylem (but not the stele as a
whole) has the appearance of a cylinder of
evidence of this kind is inconclusive. Similarity, netting, Osmunda is said to have a dictyoxylic siph-
both in sporophyte and gametophyte, between the onostele. A transverse section of the stem of the
Psilotales and certain New Caledonian ferns (e.g., late Permian Thamnopteris appears almost identi-
Stromatopteris, p. 172), together with the results of cal, even in the extent and arrangement of the
current cladistic analyses, support a placement of sclerenchyma and the packing of the leaf bases,
the Psilotales within the Polypodiopsida. with a comparable section of the rootstock of
Osmunda.
The Osmundales Some remains of osmundalean ferns can be
The Osmundales are an order of considerable identified even to species level. Well-preserved
antiquity. Their derivation may have been separ- specimens from the Upper Cretaceous of Canada
ate from that of other eusporangiate and leptos- have been found to resemble in all respects the
porangiate ferns. There are three existing genera, living Osmunda cinnamomea, still with an extensive
of which Osmunda is the largest and most widely range in North America. This is in line with the
distributed. Most living Osmundales have erect general impression that species longevity in
rootstocks, and some (e.g., Todea spp.) approach a homosporous pteridophytes commonly exceeds
small tree-like form. They currently have few eco- by far that provided by flowering plants.
nomic uses, but partially decomposed petioles
and leaves (“Osmunda fiber”) was popular in r e p ro d u c t i o n
Victorian times as a medium for growing orna- In Osmunda the early leaves are sterile, while later
mental orchids. leaves become fertile in the more distal regions
The stem of Osmunda grows from a broad apex, (Fig. 7.25). The fertile regions are devoid of chloro-
and in all but larger and older specimens a single phyll. The sporangia arise from single initial cells
apical cell is recognizable. The stem terminates in which may be cubic or tetrahedral. More than one
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 189

Figure 7.24. Osmunda regalis. Transverse section of the midrib. Following fertilization, the first divi-
rootstock.
sion of the zygote is in a plane parallel to the lon-
gitudinal axis of the archegonium. The second
cell may participate in the development of the division may also be parallel to the longitudinal
sporangium, so they are neither strictly leptospor- axis, but at right angles to the plane of the first,
angiate nor eusporangiate. At maturity the spo- leading to quadrants with a common edge par-
rangia are generally robust and each is borne on a allel to the axis. This contrasts with the common
short stalk. The sporangia do not cluster in sori, situation in the leptosporangiate ferns (p. 207).
nor is there any form of protective membrane Subsequent divisions tend to be irregular and
(indusium, p. 198). The wall of the sporangium is the embryo assumes a globular form. In Todea, the
two cells thick, although the inner layer, together young embryo can be expressed from the archego-
with the tapetum, is derived from the sporoge- nium by gentle pressure. Attempts to grow it to
nous tissue. In Osmunda the indurated cells, maturity in artificial media have not, however,
forming an annulus-like cluster, are grouped lat- been successful; any growth obtained has tended
erally (Fig. 7.26). A linear stomium extends from to revert to gametophytic form.
the cluster over the apex of the sporangium,
causing the dehiscent sporangium to open as two The Polypodiales
valves. Some 29 trilete spores are produced in each The Polypodiales form the largest order of
sporangium. They are green when released, and ferns, including (with the exception of some
soon lose their viability in unfavorable condi- Ophioglossales and Osmundales) all the homo-
tions. sporous ferns of temperate regions. The
The gametophytes of the Osmundales are Polypodiales reach their greatest representation
Marchantia-like, with a distinct midrib, and may in the humid tropics and subtropics. A square
reach a length of a few centimeters. The anthe- hectare of forest in Amazonian Ecuador, for
ridia are on the lower surface, often toward the example, was estimated to contain at least 50
margin. The archegonia, also on the lower species of polypodialean ferns of widely varying
surface, are found principally along the sides of growth forms. Despite the diversity of the
190 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Polypodiales, there are two features which distin-

guish them consistently from the remainder of
the living ferns. These are, first, the origin of the
sporangium, and, second, the plane of the first
dividing wall of the zygote. In the Polypodiales the
sporangium develops from a single initial cell, a
condition termed leptosporangiate, contrasting
with the eusporangiate condition of the
Marattiales, Ophioglossales and Psilotales. Also in
the Polypodiales, at least in those species which
possess the typical heart-shaped gametophyte, the
first dividing wall of the zygote is vertical or
slightly oblique, parallel to the longitudinal axis
of the archegonium, whereas in the eusporan-
giate ferns the first wall is perpendicular to the
archegonial axis. The subsequent embryogeny of
the Polypodiales is regularly endoscopic.

g row t h f o r m s a n d e c o no m i c u s e s
In the constantly humid and warm temperate con-
ditions of tropical mountains and rain forest the
Polypodiales adopt a wide range of growth forms.
Besides terrestrial species, both upright and rhi-
Figure 7.25. Osmunda javanica. Portion of frond with fertile zomatous, are found arborescent and scandent
pinnules. Scale bar 4cm. (From Backer and Posthumus. 1939. species, and numerous epiphytes. A remarkable
Varenflora voor Java. Buitenzorgs Lands Plantentuin.) creeping tree fern (Cyathea planadae), recently dis-
covered in mid-elevation cloud forests in
Colombia, has a decumbent stem giving rise to
upright shoots. Amongst the epiphytes, a curious
myrmecophilous form is Lecanopteris from
Southeast Asia. The inflated and chambered
rhizome houses colonies of ants. The sporangia,
the walls of which contain fat, are sought by the
ants and the spores thereby distributed.
Myrmecophilous adaptations of this kind are oth-
erwise found only in flowering plants. In many
tree ferns the dead fronds remain attached and
hang as a loose “skirt” around the trunk, making
it difficult for climbing plants to ascend and
smother the crown, a feature also of many palms.
The metabolism of the Polypodiales resembles
that of the land plants generally. A number,
mostly epiphytes, have been found to display CAM
(crassulacean acid metabolism), in which respira-
tory carbon dioxide produced in the dark is incor-
porated into oxaloacetic acid, yielding malic acid.
The carbon dioxide is released subsequently in the
Figure 7.26. Osmunda regalis, sporangium. light and assimilated in the normal way, a meta-
bolic pathway resembling that of C4 photosynthe-
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 191

Figure 7.27. Dryopteris aristata.

Longitudinal section of stem apex.
(After Wardlaw. 1944. Annals of
Botany (New Series) 8.)

g row t h o f t h e s t e m
The stems of the Polypodiales
grow from a single, conspicu-
ous, apical cell (Fig. 7.27), tetra-
hedral in shape. Studies of cell
lineages indicate that daugh-
ter cells are cut off in
sequence from its three poste-
rior faces. Nevertheless, fol-
sis (p. 6). Some terrestrial species are resistant to lowing autoradiographic studies, it has been
toxic metals. Athyrium yokoscense, a Japanese disputed whether the apical cell itself divides. It
species, for example, is copper-tolerant. This seems that the nucleus of the apical cell may
depends upon the plant’s ability to take the become polyploid. The cell then ceases to divide,
copper entering the plant into a thiolate complex, but meristematic activity is retained by the cells
and thus remove it from the general metabolism. adjacent to the posterior faces. Examination in
Few Polypodiales figure in today’s economy polarized light has shown that the cellulose
although some, for example Pteridium, have been microfibrils in the tangential walls of these cells
valued in the past as a source of fuel, thatch and lie in arrays transverse to the axis of the stem.
food. Young croziers of Pteridium are still cooked Consequently tangential growth is constrained,
and eaten in parts of Southeast Asia, despite the and expansion is predominantly radial and longi-
presence of a carcinogen. In North America tudinal.
Matteuccia is similarly used as a delicacy (“fiddle The apex of the polypodialean ferns is evi-
heads”). Secondary plant products are a notable dently much less specialized than that of a flower-
feature of some fern fronds and rhizomes (such as ing plant. A slice taken from the tip of the apex,
those of Central American species of Phlebodium), no more than 0.25 mm (0.01 in.) in depth, will gen-
and yield extracts with minor medicinal uses. In erate a normal stem in culture. The same result
some ferns these products are toxic. In Pteridium, with flowering plants can be obtained only with a
for example, they include the insect-moulting substantially greater explant.
hormone ecdysone, possibly providing protection The meristematic activity in the apical cone
from predators. diminishes toward its base. Below the apical cone,
In the less stable regions of the Andes local cell divisions are more generalized and variously
Indians use the trunks of tree ferns for the frame- directed. Leaf primordia arise in this region in a
work of buildings. The resistance of the scleren- definite phyllotactic sequence. A leaf primor-
chyma to shattering by earthquakes is superior to dium, first visible as a slight protuberance, soon
that of timber. Several species of herbaceous ferns develops its own apical cell. As the leaf primordia
are popular horticultural plants, particularly age and become separated by the expansion of the
those mutants with striking modification of the apex, bud primordia may be formed between
form of the frond. In Britain, avid collecting of them, but in some species buds do not appear at
ferns for horticultural use has led to the rarity of all so long as the apex is actively meristematic.
many native species. In Central America Rumohra Development of buds beyond the stage of primor-
adiantiformis (“leatherleaf”) is extensively culti- dia is rarely seen in the region of developing
vated and exported for use by florists. leaves. In a few ferns (e.g., Nephrolepis, common
in cultivation) some of the buds grow out as
runners (stolons) and provide a means of asexual
192 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

reproduction. Runners are also a feature of down in the apex the cells of the ring are contin-
Matteuccia struthiopteris (ostrich fern). uous with the procambium, and this in turn with
A curious situation is found in Pteridium the vascular tissue of the mature shoot. The posi-
(bracken). The rhizomes of the mature plant are tion of the protoxylem is variable, but commonly
arranged in layers, the lowermost (up to 30 cm mesarch. The large tracheids of the metaxylem
(12 in.) or more beneath the surface) consisting have scalariform pitting, and in some instances
solely of “long” shoots with extended internodes. (e.g., in the rhizome of Pteridium) the oblique end
Most of the fronds are borne on short stubby rhi- walls have scalariform perforations. These vessel-
zomes which ascend to near the soil surface. In like channels, found also in the Marattiales (p.
the event of a “front” of bracken invading a new 177), may occur more frequently in the xylem of
area, the lowermost rhizomes head the advance. ferns than commonly supposed, and recall the sit-
Since the apices of many ferns are compara- uation in some species of Selaginella (see p. 155).
tively broad and accessible, they provide excellent The phloem consists of sieve cells with sieve areas
material for experimental work on phyllotaxy. confined to the oblique end walls. The vascular
The results indicate that the young leaf primor- tissue is usually surrounded by a narrow zone of
dia, each a center of meristematic activity, sup- parenchyma, and then by an endodermis with a
press growth in their immediate vicinity. Thus, if clear Casparian strip (see p. 185). The walls of the
the position in which a leaf primordium is cortical cells adjacent to the endodermis are often
expected to arise is isolated by radial incisions thickened and made conspicuous by impregna-
from the neighboring recently initiated primor- tion with phlobaphene. The endodermis and
dia, then the new primordium develops with these thickened tangential walls probably
unusual vigor and outgrows the others. Similar together limit apoplastic transport between stele
experiments also confirm the fundamental simi- and cortex.
larity of stems and leaves in the Polypodiales. For The form of the stele in the Polypodiales shows
example, tangential incisions on the anterior side considerable variation (Fig. 7.28). In some species
of very young primordia that would normally of Gleichenia, for example, the procambial tissue
yield leaves result in the production of stem buds yields a solid core of tracheids from which the leaf
instead. Incisions on the posterior side are traces depart without any break in the continuity
without any effect. Consequently the determina- of the xylem (protostele, Fig. 7.28a). Some other
tion of the subapical primordia appears to depend species of Gleichenia show a similar stele, but with
upon their being initially traversed by gradients the medullation of the tracheidal core leading to
of metabolites originating in the apical meristem. the production of a siphonostele (Fig. 7.28b).
If a primordium is isolated from these gradients In some ferns, in which the stele is cylindrical,
by an anterior incision it yields the radially sym- phloem and endodermis are present both inside
metrical structure of a stem instead of the dorsi- and outside the xylem (Fig. 7.28c). This form of
ventral symmetry of a leaf. Naturally in stele, found principally in rhizomatous ferns, is
interpreting the results of microsurgery, the termed a solenostele (or amphiphloic siphonostele).
growth-stimulating effects of wounding must also Leaf gaps are regularly present and sometimes
be taken into account. additional perforations unrelated to the depar-
ture of leaf traces. The internal and external
formation and morphology of the phloem and endodermis are in continuity around
stele the margins of the gaps in the xylem. If the leaf
The cells which yield the vascular tissue first gap and other perforations are close together, as
become recognizable as a distinctively staining in Dryopteris, the stele in section appears as a ring
ring shortly below the apical cell. The diameter of of anastomosing vascular bundles (Fig. 7.28d),
the ring increases in register with that of the apex each with internal xylem and concentric phloem.
as a whole, and beneath the leaf primordia its This type of stele, which is of widespread occur-
cells become confluent with crescentic strands of rence, is termed a dictyostele. A complication,
similar cells descending from them. Further shown for example by the rhizome of Pteridium
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 193

Figure 7.28. Principal forms of fern steles. (a) Protostele.

girth of the apex. This relationship between size
(b) Siphonostele. (c) Solenostele. (d) Dictyostele.
and form is clearly the consequence of physiolog-
ical equilibria, but they are undoubtedly complex
(Fig. 7.29) and the trunks of the tree fern Cyathea, and have yet to be resolved.
is the presence of two or more concentric vascular
systems, interconnected at intervals and usually o t h e r a na t o m i c a l f e a t u r e s o f t h e
all contributing to the leaf traces. These steles are stem
said to be polycyclic. Steles are not always radially In addition to the xylem, which is wholly primary,
symmetrical. Dictyosteles in the ferns with creep- there are frequently bands or rods of scleren-
ing rhizomes, for example, are often markedly chyma in the stem contributing to its rigidity. In
dorsiventral, the departure of the leaf traces being the tree ferns, for example, many of which reach
confined to the upper surface and flanks (Fig. or exceed heights of 10 m (33 ft), mechanical stabil-
7.30). ity is dependent almost entirely upon the
extremely tough girdle of sclerenchyma in the
experimental investigation of outer cortex, often in association with the leaf
stel ar morphology bases. In those Polypodiales which are believed,
The form of the stele in the Polypodiales has also on the basis of fossil evidence, to be relicts of very
been the subject of experimental investigation. In ancient groups (e.g., Gleichenia), the parenchyma-
Dryopteris, for example, if the apical region is iso- tous tissue of the stem often contains resin sacs
lated by vertical cuts, but left in contact below, it and mucilage canals. Amongst the Polypodiales
continues to grow and a solenostele differentiates more recent in origin these features are less
behind it. As the apex expands and builds up a evident.
new crown, the stele gradually opens out to re-
form a dictyostele. In any one species, therefore, ro o t s
the size of the apex determines the form of the After the primary root all subsequent roots are
stele. This is also well shown in sporelings where adventitious, in arborescent forms often being
a protostele is always present at the beginning. In produced even in the aerial regions and providing
protostelic species this merely increases in diame- a mantle of stubby outgrowths between the leaf
ter as the plant develops, but in solenostelic and bases. Roots show a distinct apical cell, but in
dictyostelic species the protostele of the sporeling some instances this may be quiescent, divisions
becomes medullated, and phloem and endoder- being confined to the cells at its flanks. As in other
mis appear within in step with the increasing ferns a root cap is present, and in many species
194 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.29. Pteridium aquilinum.

Transverse section of rhizome.

root hairs. The xylem is com-

monly diarch, and in many
epiphytic forms all but the
protoxylem often remains
unlignified. The roots of some
ferns produce shoot buds.
These facilitate the rapid colo-
nization of a new area.

morphology and
a na t o m y o f t h e
v e g e t a t i v e l e av e s
The leaves of the Polypodiales
retain an apical cell during
their development from the
primordium. Some form of pinnate branching is upon the diffusion, and varying relative concen-
usually present in the mature leaves. True dichot- trations, of auxins (growth-regulating substances)
omous branching occurs very rarely (the frond of in the expanding leaf, but these auxins are not
Rhipidopteris peltata provides one of the few exam- necessarily identical with those in seed plants.
ples), but cymose branching, superficially resem- The expanding leaves of some ferns, for example
bling dichotomy, is shown by the leaves of several of the tropical Dryopteris decussata, are enveloped
species of Gleichenia. The filmy fern Cardiomanes in mucilage, possibly with some protective effect.
reniforme of New Zealand has a striking, entire, Extrafloral nectaries are found at the points of
kidney-shaped leaf, up to 5 cm (2 in.) in width. branching of the frond of Pteridium. There is no
Notable also is the filmy epiphyte Microgonium evidence that they have any function apart from
tahitense of the Asian tropics. The habit resembles the secretion of surplus metabolites.
that of the common angiosperm epiphyte The lamina of the leaf is commonly differen-
Dischidia. The filiform rhizome, growing on tiated into palisade and mesophyll, but the
smooth-barked trees, bears peltate leaves which texture is very variable and in some species a thick
are almost sessile and appressed to the substrate. cuticle on the upper surface gives the leaf a sur-
Roots are absent, but the rhizome and the prising harshness. “Filminess” is a consequence of
margins of the leaves bear rhizoids. the lamina being only one cell thick. This condi-
In a few Polypodiales meristematic areas are tion, already seen in Leptopteris (Osmundales,
retained in the differentiated leaf, and these sub- p. 188), is found throughout the family
sequently grow out to form either additional Hymenophyllaceae. Filmy ferns are necessarily
leaves (as in Trichomanes proliferum (Fig. 7.31)) or confined to situations of continuously high
new plantlets (as in Asplenium mannii and humidity. They are often able to thrive in irradi-
Camptosorus radicans). These forms illustrate how ances far below those tolerated by flowering
in the living ferns, as in the extinct (see p. 172), the plants, and more akin to those of the bryophyte
leaves sometimes display features suggestive of communities with which the epiphytic forms are
stems. All parts of the young leaves usually show frequently mixed. In Hymenophyllum malingii, a
circinate vernation. The extension of the rachis peculiar epiphyte of New Zealand, the leaf lacks
and the unrolling of the pinnae clearly involve a lamina. Instead the axes of the pinnately
considerable coordination of growth in space and branched frond bear green filaments interspersed
time. There is evidence that this is dependent with stellate trichomes. Some of the larger tropi-
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 195

Figure 7.30. Elaphoglossum latifolium. Reconstruction of material at the base of the funnel is freely pene-
stele showing the dorsiventral symmetry: v, ventral meristele; trated by absorptive rootlets.
d, dorsal meristele; b, bridge connecting the dorsal and The leaves of many temperate ferns die during
ventral meristeles; bt, bud trace; lts, strand of the leaf trace; r, the winter, but remain attached (and are said to
root trace; r´, root in association with bud trace. (From Bell.
be marcescent). In some species (e.g., Polystichum lon-
1950. Annals of Botany (New Series) 14.)
chitis) the leaves remain green, even in harsh con-
ditions. Experiments have shown that these leaves
provide a net contribution to assimilation, partic-
cal epiphytes are distinguished by producing ularly early in the following season’s growth.
sterile leaves of two forms. In addition to the erect
photosynthetic leaves are others which clasp the t h e f e r t i l e l e av e s a n d t h e na t u r e o f
support. The latter soon die, but persist in a rigid t h e s p o r a ng i a
scarious condition and serve as collectors of The fertile leaves of the Polypodiales are often
humus and moisture. Platycerium (Fig. 7.32) pro- quite similar to the sterile (as in Dryopteris), but
vides a striking example of this kind of habit. In dimorphy is not uncommon. In Blechnum spicant,
other epiphytes of similar situations the leaves, for example, both sterile and fertile fronds are
borne on a short upright rootstock, are stiff and simply pinnate, but in the fertile ones the sterile
tightly overlapping, so forming a funnel which part of the lamina is very reduced. The sporangia
traps rain and organic matter. Asplenium nidus pro- arise from single initial cells and are therefore lep-
vides a typical example of these “nest ferns”. The tosporangiate, either at the margin or on the lower
196 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.31. Trichomanes

proliferum. Frond, showing indefinite
growth. (From Bell. 1960. New
Phytologist 59.)

Figure 7.32. Platycerium. (a) Habit,

showing the two forms of leaves. (b)
Lower surface of fertile portion of
frond.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 197

Figure 7.33. (a–c) Anemia phylliditis: (a) fertile frond; (b) tains a group of indurated cells and a well-defined
portion of fertile region; (c) sporangium showing transverse stomium. The indurated cells are arranged in a
annulus. (d) Gleichenia, sporangium. single band (annulus) which encircles the sporan-
gium, transversely near the apex of the sporan-
surface of the leaf. The mature sporangium has a gium (as in Anemia (Fig. 7.33c) and other
distinct stalk, the structure of which ranges from Schizaeaceae), or obliquely (as in Gleichenia (Fig.
a broad multicellular stump to a delicate and rel- 7.33d) and the Hymenophyllaceae), or vertically
atively long column of cells. The wall of the (as in Dryopteris (Fig. 7.34) and most common tem-
capsule is only one cell thick, and it always con- perate ferns). The annulus is interrupted by the
198 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.34. Dryopteris. Stages in dehiscence of sporangium.

sporangia are produced in a continuous line,
(After Ingold. 1939. Spore Discharge in Land Plants. Oxford
referred to as a coenosorus, well shown, for example,
University Press, Oxford.)
by Pteridium. The sorus is often partly or wholly
covered by an outgrowth of the lamina, called an
stomium. Where the annulus is vertical, it is also indusium, which adopts a characteristic form. In
interrupted by the stalk of the sporangium, the Dryopteris, for example, the indusium is reniform
stomium then lying just in front of the stalk. The (Figs. 7.35 and 7.36), and in Polystichum peltate. In
sporangium dehisces at the stomium as a conse- Onoclea the sori are protected by a rolling up of the
quence of tensions set up in drying. The mecha- fertile pinnules. In some species of Polypodium,
nism has been studied in detail in those ferns where an indusium is typically absent, the sori are
where the annulus is vertical. Here, as the cell sap immersed in the lower surface of the lamina. A
in the annular cells diminishes by evaporation, few ferns show the so-called “acrostichoid” condi-
asymmetrical thickening of the cell walls (Fig. tion in which the sporangia arise as a continuous
7.34) causes an increasing tangential tension felt on the lower surface of the fertile frond (e.g.,
which tends to reverse the curvature of the Platycerium, Fig. 7.32). In some ferns (e.g., Gleichenia)
annulus. The stomium eventually breaks, and the the sporangia in a sorus are all of the same age
upper part of the sporangium gradually turns (Fig. 7.37a,b), in others they are produced in
back as if on a hinge (Fig. 7.34). Tension in the cells spatial and temporal sequence on an elongated
of the annulus soon reaches a critical level; at this receptacle (as in the Hymenophyllaceae) (Fig.
point the water remaining in the annular cells 7.37c,d), yielding a so-called “gradate” sorus, and
spontaneously becomes vapor. The tension is in yet others the sporangia are produced over a
immediately released, and the upper part of the period but intermingled, leading to a so-called
sporangium flies back to more or less its original “mixed” sorus (Fig. 7.37e,f) (as in Dryopteris and
position (Fig. 7.34). These two movements effec- most common temperate Polypodiales).
tively disperse the spores. It has sometimes been
observed that the movements are repeated, a d e v e l o p m e n t o f t h e s p o r a ng i a a n d
feature not so readily explained. spores
In the development of the sporangium a cluster
a r r a ng e m e n t o f t h e s p o r a ng i a of spore mother cells becomes surrounded by a
In most Polypodiales the sporangia arise in dis- two-layered tapetum. In origin this is part of the
tinct sori, usually beneath veins or near their wall tissue and not of the archesporium, as in
extremities, these two positions being called super- eusporangiate sporangia. The cytological changes
ficial and marginal respectively. Sometimes the accompanying meiosis provide a model for spor-
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 199

Figure 7.35. Dryopteris filix-mas.

Vertical section of sorus.

(a) (b)

Figure 7.36. The abaxial surface of fertile pinnules of

ogenesis in the land plants generally. As their
Dryopteris filix-mas. (a) The sori in a young condition, before
dehiscence of the sporangia. (b) Three weeks later, most of
nuclei enter prophase the spore mother cells
the sporangia having dehisced. Scale bars 2 mm. become surrounded by a thickened wall, and
cytoplasmic connections between them are extin-
guished. The presence of callose in this special
wall has not yet been convincingly demonstrated.
During prophase the density of the cytoplasm
diminishes and there is a loss in affinity for basic
stains, largely accounted for by a fall in the fre-
quency of ribosomes and hence in the concentra-
tion of RNA. Spores are produced in tetrads. The
first exine is secreted by the spore itself. At this
stage the thickened wall of the mother cell,
weakened by autolytic degradation, breaks open.
The spores then separate and complete their
development in the breakdown products of the
tapetum.
Some 26 to 28 spores are produced in each spo-
rangium, the higher numbers being characteris-
tic of the families believed to be more primitive.
The spores are usually of the order of 40 ␮m in
Figure 7.37. Principal forms of sorus. (a,b) Simple, the diameter, but measurements of a representative
sporangia all of the same age: (a) superficial; (b) marginal.
sample will usually show a normal distribution
(c,d) Gradate: (c) superficial; (d) marginal. (e,f) Mixed: (e)
with a range of about ⫾10 ␮m about the mean.
superficial; (f) marginal.
A few ferns, normally included with the
200 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.38. Platyzoma microphyllum. View of the fronds,

showing the two rows of subopposite cup-like pinnules. lower. The size of the spores is related to sex
Fertile regions occur at intervals along the frond, the expression (p. 204).
sporangia obscured by the recurved margins of the pinnules.
The outer part of the spore wall (exine), the
The juvenile fronds consist solely of a slender green rachis,
material of which is derived from the tapetum, is
lacking pinnules. Scale bar 1 cm. (Photograph provided by
Pamela Warren Wilson.)
sometimes deposited in a characteristic pattern of
bars and ridges. This is especially true of the
Schizaeaceae, and it provides a feature that has
homosporous, do in fact produce spores of differ- been very useful in identifying fossil forms. In
ent sizes. The most extreme example is seen in some ferns, principally the more recent, the
Platyzoma, a fern of very unusual appearance spores are monolete instead of trilete. Monolete
(Fig. 7.38) growing on deep sands in northeast spores (p. 160) often have an additional translu-
Australia. Although the mature sporangia are all cent investment, called a perispore, formed from
about the same size, some produce 16 large spores the remains of the tapetum. In a few ferns mono-
and others 32 smaller ones (although the diame- lete and trilete spores are found in the same spo-
ter of these is greater than that of fern spores in rangium.
general). A histogram shows a clearly bimodal Production of viable spores usually fails in
distribution. Nevertheless, a random sample of hybrid ferns. Meiosis is irregular, the pairing of
spores reveals a preponderance of small spores the chromosomes being only partial or even
and a wide range of spore sizes within each size wholly absent. Division spindles are largely dis-
class (Fig. 7.39). The difference in spore size seems torted, and, although there is an attempt at spor-
to result from the greater availability of nutrients ogenesis, most of the spores are usually inviable.
and space for spore growth when the number is They are also often irregularly fused together by
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 201

Figure 7.39. The size distribution of 177 spores of

Platyzoma microphyllum collected in Queensland, Australia. the gametophytic phase
The sample was taken from the fertile regions of three In some families, as in the Osmundales, the spores
fronds from different plants. The spores were mounted in are green when shed, but normally chlorophyll is
25 percent alcohol. Ten non-overlapping fields, selected at
absent. Non-green spores are often rich in lipid,
random, were photographed and the negatives printed at a
amounting in some instances to 60 percent of the
total ⫻80 final magnification. The maximum diameters of the
spores were measured with a magnifying micrometer, the
dry weight. Green spores are short-lived, but non-
scale graduated in 0.5 mm intervals (1 mm representing green spores may remain viable for many years,
12.5 ␮m). (S. Laird, unpublished.) particularly if buried in soil. In this way “banks”
of viable spores may be formed beneath stands of
ferns, germination occurring only if the spores
are brought to the surface. Such reservoirs of
exine into dyads or triads. Similar spore forma- spores provide for the re-colonization of areas
tions are well known in ancient deposits. This has cleared by cultivation or other disturbance.
given rise to the suggestion that hybridization Although moisture is essential for germina-
was also a feature of early land plants. However, tion, the requirement for light is variable. Some
the genetic control of meiosis is complex and spores (e.g., Pteridium) germinate in the dark, but
must itself have been subject to evolutionary others require the stimulus of red light. The phy-
refinement. Irregular spore formations in the tochrome system is evidently involved, but the sit-
Paleozoic era may have been a consequence of uation is not simple since in some instances the
meiosis itself at that time not having achieved effect of red is reversed by both far-red and blue.
the regular perfection that is commonly seen After the first division the protruding daughter
today. cell often yields a colorless rhizoid, the elongation
202 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.40. (a) Pteris ensiformis. Lower surface of

gametophyte, bearing young sporophyte. (b,c) Pteridium light) the gametophytes persist indefinitely as fil-
aquilinum: (b) median longitudinal section of young aments with elongated cells. In blue light, which
archegonium; (c) almost mature antheridium. changes the balance of the metabolism in favor of
protein, the cells divide more frequently and
of which may be promoted by metal ions present become progressively shorter, their width remain-
in the perispore. Continued divisions give rise to ing little changed. Ultimately the apical cell
an algal-like filament, the growth of which is pre- becomes broader than long. In these conditions
dominantly apical, furnished with a few rhizoids. 1D growth gives way almost immediately to 2D.
Germination and production of the first rhizoid The change in the direction of division at the apex
appear to be resistant to inhibitors of transcrip- of the filament is in accordance with the concept
tion, so it is probable that these initial steps are that the plane of the new wall in a dividing cell is
dependent upon long-lived messenger RNA transverse to the principal stress in the plasma-
already present in the spore. lemma (which in turn may influence the align-
In some Polypodiales (the Hymenophyllaceae, ment of microtubules). In cells which are longer
for example, and some Schizaeaceae), the gameto- than broad this stress, caused by the turgor of the
phyte remains filamentous and the sex organs are cells, is longitudinal, and hence the new wall
borne on lateral cushions of cells. Yet other game- transverse. In cells broader than long the princi-
tophytes are ribbon-like, and the ribbon may pal stress is transverse to the filament, and the
branch freely. In many ferns (of which Dryopteris new wall correspondingly longitudinal or almost
and Pteridium provide familiar examples) the cell so. Substances which affect the rate of growth,
at the apex of the initial filament soon begins to and the rapidity with which growth changes from
divide in a number of directions, leading to the 1D to 2D, can be isolated from media in which
formation of a cordate (heart-shaped) gameto- spores have been cultured. The proportions of
phyte (Fig. 7.40). There is no general agreement these substances vary in relation to the wave-
about the cause of this change from one-dimen- length of the light to which the cultures have
sional (1D) to two-dimensional (2D) growth, but it been exposed. Nevertheless, there is no evidence
seems likely that it is a consequence of a changing as yet that the transition from 1D to 2D growth is
balance between carbohydrate and protein metab- dependent upon the activation of specific genes.
olism. When the protein metabolism is depressed Since the transition can also occur in high irradi-
in relation to the carbohydrate (as can be caused ances of continuous red light, it seems much
experimentally by growing the cultures in red more likely that it is a consequence of correlations
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 203

between the carbon/nitrogen balance of the begin to be produced acropetally in more or less
metabolism of the gametophyte and the propor- orderly files behind the apical meristem. The gam-
tions and stresses in the walls of the dividing cells. etophytes of some ferns go through several cycles
Once established, the apical cell evidently of male/female sex expression in normal develop-
retains close symplastic connections with the ment, but in Pteridium aging female gametophytes
growing area of the gametophyte. Investigations lose an organized apical meristem, the production
of the developing cordate gametophytes of the of archegonia gradually ceases, and growth in turn
fern Onoclea sensibilis have shown that the basipe- becomes disordered and irregular. Lateral prolife-
tal walls of the apical cell are well furnished with rations of the gametophyte may then begin to
plasmodesmata. Frequencies of some 14 plasmo- produce antheridia. For a short time intragameto-
desmata ␮m⫺2 were regularly found, values com- phytic selfing is thus possible, but in Pteridium such
parable with those occurring in the walls of selfing often results in defective sporelings. This
glandular cells with high rates of plasmodesmatal may be a consequence either of the homozygosity
transport. of deleterious genes or of the egg cells produced at
Mycorrhizal associations are probably the time of the re-establishment of a male phase
common in fern gametophytes. The gametophytes being themselves defective. Nevertheless, in
of some tropical Schizaeaceae, for example, are Lygodium antheridia and archegonia appear to be
subterranean (resembling those of Psilotum (p. regularly produced intermixed, a condition recall-
187)) and are thus presumably wholly dependent ing that in synoicous mosses (p. 123).
upon endophytic fungi for their nutrition. In A sample of fern spores sown on an agar plate
Schizaea pusilla, a species with a phototrophic fila- will frequently yield, after a period of culture, a
mentous gametophyte, the presence of a truly scattering of small cordate gametophytes in
mycorrhizal fungus in wild populations was con- which a clear apical meristem is becoming
clusively demonstrated by isolation of the fungus, evident, and just behind it the production of
and the finding that continued development of archegonia. Other spores will have yielded clus-
aseptically germinated spores was dependent ters of cells lacking apical organization, and
upon inoculation. commonly covered with antheridia. These game-
Despite their delicate structure, the game- tophytes remain ameristic and male indefinitely.
tophytes of some ferns have proved surprisingly Some ameristic gametophytes are always present,
resistant to desiccation and freezing, their toler- but the proportion tends to rise with increasing
ances often far exceeding those of the sporo- density of sowing.
phytes. A few gametophytes have modifications Experiments have shown that the control of
which clearly promote survival. That of the sexuality in a culture of fern spores is remarkably
Mediterranean Anogramma leptophylla, for complex. When gametophytes are grown in pure
example, has a tuberous portion resistant to culture substances accumulate in the medium
drought, resulting in the curious situation of the which stimulate the production of antheridia in
sporophyte being annual and the gametophyte other young gametophytes. The chemical nature
perennial. The subterranean gametophytes of a of these substances, called antheridiogens, varies
few tropical species of the Schizaeaceae may also with species, but some are closely similar to gibbe-
have survival value. rellins. Currently 12 compounds have been iso-
lated and found to have antheridiogen activity. As
sex expression in the gametophyte a gametophyte passes from the antheridial to the
In those filamentous gametophytes which bear archegoniate phase it becomes insensitive to its
their sex organs in clusters on lateral cushions, the antheridiogen, but it is still secreted into the
male and female cushions are commonly separ- medium. A genetic control of the effects produced
ated. Cordate gametophytes, at least when young, by antheridiogens has been demonstrated in the
bear their sex organs in the apical region, sexual fern Ceratopteris. Here, the only stage which
expression almost always beginning with a male responds to the fern’s antheridiogen begins
phase. Following the male phase, archegonia just after germination and lasts only until the
204 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

gametophyte has reached 4–5 cells in size. In the escape from its initial constraints. It has not,
presence of the antheridiogen such a gameto- however, been demonstrated that this escape is
phyte will remain amerisitic and male. Several possible with gametophytes from the smallest
mutations, however, have been found to affect spores, and a full understanding of the factors
this response. One mutation (her) suppresses the determining sex expression in the gametophytes
response and the gametophyte behaves as a her- of Platyzoma awaits further research.
maphrodite. Another mutant (fem) interferes with It is conceivable that the ameristic gametoph-
the production of antheridia and gametophytes ytes arising in cultures of ferns whose spores are
grow into meristic females in the presence or more uniform in size are also the product of
absence of the pheromone. Interestingly the spores which have received by chance a reduced
effect of the antheridiogen on young gametophy- amount of cytoplasm during the final divisions of
tes can be suppressed by adding abscisic acid (a sporogenesis. Their relatively retarded develop-
known antagonist of gibberellin in flowering ment would leave them open to the full effects of
plants) to the medium. The gametophytes in these the antheridiogen coming from their more
conditions grow directly into hermaphrodites. advanced neighbors.
The mixed phenotype of a culture on an agar
medium evidently depends upon spore-to-spore differentiation of the gametes
differences in the times of germination and the Antheridia usually contain 25 or 26 spermatocytes,
rates of early development, combined with the often with callosed walls. Each differentiates a
interaction of at least three genes controlling spermatozoid. There is active protein synthesis
competence and response. Some alleles of the her during the initial stages of spermatogenesis, but
mutation, when homozygous in the sporophyte, the later stages (including the formation of the
interfere with the development of the fertile flagella) appear to be largely a matter of protein
frond. Adventitious buds may then be present assembly. When the antheridia are mature,
amongst the sporangia. flooding causes the mucilage within to swell. The
Although studied mostly in axenic conditions, cap cells are then forced off and the spermatocytes
there is now evidence that antheridiogens regu- extruded. The flagella of the spermatozoids
late sexuality in natural populations of gametoph- become active and each breaks free from its muci-
ytes. The results of some field experiments have laginous shell. The motile spermatozoid is about 5
indicated that the influence of antheridiogens on ␮m long and takes the form of a helix with a left-
the formation of apical meristems in developing handed (anticlockwise) screw (cf. Fig. 7.49). The
gametophytes and the induction of maleness are anterior gyre is taken up with the multilayered
separate effects. This would imply that antheridi- structure and the associated mitochondrion, and
ogens have the properties of both a hormone and the remaining gyres with the nucleus and micro-
a pheromone. tubular ribbon. Plastids are absent from the differ-
A particularly interesting situation is found in entiated gamete (Fig. 7.49). The flagella, confined to
Platyzoma (p. 200). Here the small spores give rise the anterior gyres, emerge tangentially and are
to gametophytes which remain depauperate and directed posteriorly. They beat with a helical wave
male, while the larger spores yield complex gam- which drives the spermatozoid forward and at the
etophytes which are female, but may subse- same time causes it to rotate in the sense of the
quently also bear antheridia. Spore size will screw. Current observations on a range of species
inevitably be related to the amount of cytoplasm reveal that spermatozoids may remain active for
forming the initial endowment of the spore, and up to two hours following release, but whether
it may be this feature which governs subsequent they similarly retain the ability to effect fertiliza-
growth and sex expression. Explants of the dimin- tion has not been established.
utive male gametophytes, if transferred to The necks of the archegonia, consisting of 4–6
mineral–agar medium, have been observed to tiers of cells, usually project conspicuously and
regenerate and give rise to hermaphroditic are often recurved. As in the liverworts Marchantia
growths, indicating that development is able to (p. 107) and Sphaerocarpos (p. 114), the maturation
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 205

Figure 7.41. Part of a median section of a maturing egg of present in all ferns. It is not, for example, a feature
Pteridium, showing the margin of the nucleolus (nu), and
of oogenesis in Osmunda. Nuclear-cytoplasmic
nuclear bodies (arrows) in the nucleoplasm and in vesicles
behavior similar to that seen in the maturing egg
budded off from the nucleus. The chromatin is highly
dispersed. m, mitochondrion; p, plastid. Scale bar 0.5␮m. cells of Pteridium and Dryopteris is seen in somatic
cells of Nicotiana infected with tobacco mosaic
virus. It is conceivable that some ferns, as do many
of the egg, completed within about 24 hours, wild herbaceous flowering plants, carry symptom-
involves in many species extensive interpenetra- less viruses, re-infection of the succeeding gener-
tion of nucleus and cytoplasm. Simultaneously, ation taking place during oogenesis.
small aggregates of dense material (“nuclear The mature egg lies in a chamber with a thick-
bodies”), 300–500 nm in diameter, and apparently ened and often callosed wall. The egg protoplast
formed at the periphery of the nucleolus, spread is surrounded by a conspicuous membrane.
throughout the nucleoplasm. These aggregates Although acetolysis-resistant, it does not appear
enter vesicles, bounded by both membranes of the to contain sporopollenin, but to consist of poly-
nuclear envelope, which bud off from the surface merized lipids or fatty acids (and thus to resemble
of the nucleus and are soon present throughout the acetolysis-resistant components of certain
the cytoplasm (Fig. 7.41). It has not been possible algal walls (pp. 45, 65)). The material for the mem-
to detect nucleic acids, either in the nuclear brane is secreted on to the surface of the egg by a
bodies or in the material in the vesicles; it appears process of exocytosis, being derived from a break-
to be principally, if not entirely, acidic protein. down of a proportion of the cytoplasmic orga-
These bodies are not therefore correctly called nelles during oogenesis. The egg cells of more
“micronucleoli”. The significance of this remark- recent ferns, such as Pteridium and Dryopteris, lack
able cytology is not yet known. Although it was the conspicuous amyloplasts which are a feature
first thought to be concerned with the establish- of the egg cells of Todea and Osmunda
ment of sporophytic growth, it is clearly not essen- (Osmundales), and Angiopteris (Marattiales),
tial for the generational change, since it is not undoubtedly relicts of ancient lineages.
206 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.42. Trichomanes speciosum. (a) A sporophyte

photographed at Flores in the Azores. (b) A stand of
gametophytes (arrows) growing on and under a sandstone
boulder at Bingley, Yorkshire. Although the species was
originally described from this locality, the sporophyte now
appears to be extinct here. (Photographs provided by
Johannes Vogel, Natural History Museum, London.)

Flooding causes mucilage within the canal of

the ripe archegonium to swell. The cap is forced
off and the contents of the canal ejected. A clear
passage, containing watery mucilage, now runs
down to the surface of the egg cell.
Some fern gametophytes appear reluctant to
produce sex organs in the wild, although they
may do so more freely in laboratory conditions.
Pale green ribbon-like thalli, resembling small
liverworts and locally abundant in shaded rocky
areas of parts of temperate North America, are
believed to be gametophytes of Vittaria, but sporo-
phytes are rare, and if present are commonly no
more than stunted juveniles. The evolution of
these forms may have followed from the game-
tophytes being more tolerant of cool conditions
than the corresponding sporophytes. The filamen-
tous gametophytes of some species of Trichomanes
are also found with defective sexual reproduction
(a)

(b)
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 207

well beyond the present distribution of the sporo- chemotactic properties), attracts the spermato-
phyte in both North America and Europe. Some zoids and effectively confines them to the region
wholly gametophytic stands of the European T. of the archegonia. Several spermatozoids com-
speciosum (Fig. 7.42), for example, occur more than monly enter an open archegonium, and occasion-
1000 km (c. 600 miles) from the nearest sporo- ally some can be seen to swim out again. Where
phytes, and may be 1000 or more years old. crosses are attempted between certain genera
Antheridia are found in about half these colonies, (e.g., Athyrium 씸 ⫻ Dryopteris filix-mas 씹) the muci-
but archegonia are very few. Reproduction of lage immobilizes the foreign spermatozoids and
these imperfect forms must be largely by fragmen- no hybrids are produced. Barriers to gametic
tation and gemmae (Fig. 7.43). The distribution of fusion in ferns are so far little studied. It is pos-
the filmy fern Mecodium wrightii of British sible that in some species self-fertilization is pre-
Columbia and Alaska has similar features, appar- vented, or its chances lessened, by incompatibility
ently sterile gametophytes being more wide- mechanisms in the archegonial mucilage or at
spread than sporophytes. Callistopteris baueriana, a the surface of the egg, but the evidence so far is
filmy fern occurring throughout the Hawaiian inconclusive. It appears, however, to be a general
archipelago, shows a less extreme situation. The rule that only one spermatozoid enters the egg,
gametophyte is a narrow branching thallus, although others may be seen pressed against its
which, at some sites, may form dense pure stands surface.
lacking sporophytes, although elsewhere sporo- Division of the zygote follows about 48 hours
phytes are conspicuous. after fertilization. Experiments in which game-
The gametophytes of some ferns with normal tophytes of Pteridium containing maturing eggs
cycles also multiply asexually. With ferns in have been fed with radioactive (tritiated) thymi-
which the gametophyte has a prolonged filamen- dine (which is incorporated into replicating DNA)
tous phase before becoming thalloid (as in the have shown that the nucleus of the zygote enters
family Grammitidaceae), fragmentation of the fil- mitosis without further DNA synthesis. This indi-
aments often leads to a number of independent cates that the nucleus of the egg, and presumably
gametophytes, each capable of sexual reproduc- that of the spermatozoid, each contain the repli-
tion. Specialized gemmae, borne at the tips of fil- cated (2C) amount of DNA. The zygotic nucleus is
aments (termed sterigmata) (Fig. 7.43), are a regular therefore ab initio in the G2 phase of the mitotic
feature of many of the filamentous gametophytes cycle, with the 4C amount of DNA of the diploid
of filmy ferns. Older gametophytes of the cordate nucleus. It is consequently able to divide mitoti-
kind of many ferns will proliferate at the margins cally as soon as the cell is re-organized following
and yield a crop of younger gametophytes which the disturbance of gametic fusion.
resume a sexual function. Others, such as those of The first vertical wall is succeeded by a hori-
the tropical Asian epiphyte Lecanopteris, produce zontal so that in lateral aspect the zygote appears
marginal multicellular gemmae on short stalks. divided into quadrants. These quadrants indicate
The tropical Asian Phanerosorus major has a ribbon- in a general way the course of the subsequent
like gametophyte which, as well as reproducing embryogeny. The upper anterior region, for
sexually, proliferates freely from the marginal example, goes to form the apex of the new sporo-
cells of the thallus, leading to a colonial gameto- phyte, the lower anterior the first leaf, while the
phytic mat. In consequence, many young sporo- posterior regions give rise to the first root and the
phytes may arise from initially only a few spores. foot (Fig. 7.44). There is no suspensor. Following
fertilization, possibly a consequence of growth-
f e r t i l i z a t i o n a n d e m b ryo g e n y regulating substances coming from the zygote,
Fertilization in the Polypodiales depends, as with the growth of the gametophyte diminishes and
most other archegoniate plants, upon the pres- the initiation of archegonia ceases. At the same
ence of water. The mucilage around the mouth of time the cells of the archegonium immediately
the archegonial canal, possibly because it con- above the fertilized egg proliferate, forming a con-
tains traces of malic acid (known to possess spicuous cap (calyptra).
208 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.43. Portion of a filamentous gametophyte of is clearly similar to that obtaining in the bryophy-
Trichomanes speciosum growing in culture, showing the tes (p. 103).
production of gemmae (terminating sterigmata) and sex
Experiments have shown that the calyptra
organs. Partly diagrammatic. Scale bar 100 ␮m. (After
Rumsey. 1994. PhD dissertation, University of Manchester.)
formed above the zygote, probably by exerting
mechanical pressure on the developing embryo,
plays an important part in modulating normal
The foot of the embryo remains surrounded by embryogenesis, again recalling the situation in
a thickened boundary in which parts of the ace- the mosses (p. 125). If the calyptra is removed from
tolysis-resistant membrane originally surround- above a very young zygote, the zygote gives rise to
ing the egg can be clearly seen in section. The a mass of parenchymatous tissue before produc-
apposed walls of the cells at the interface of ing differentiated growing points. With cordate
gametophyte and sporophyte develop a labyrin- gametophytes, an intact apical meristem, prob-
thine structure. Although these cells have been ably in consequence of the auxin it produces, is
termed “transfer cells”, the term is misleading also essential for normal embryogenesis. If this
and should be abandoned. Experiments with meristem is destroyed, differentiation of the
radioactively labelled, potentially informational, embryo is markedly slower and the emergence of
molecules, such as nucleosides, have shown that the first root very much delayed.
these molecules do not traverse the gameto- Information, probably in the form of messen-
phyte/sporophyte boundary. The wall labyrinth ger RNA, leading to the initiation of normal
appears therefore to be acting in respect of some embryogenesis appears to be already present in
metabolites as a molecular filter. “Transfer cells” the cytoplasm of the mature egg cell. If this RNA
at sites such as the gametophyte/sporophyte inter- is corrupted by allowing the egg to mature in the
face are better regarded as a developmental presence of a sublethal concentration of the
feature brought about by an active flux (no doubt uracil analog thiouracil, the zygote, formed fol-
containing “innocuous” metabolites, such as lowing fertilization with a normal spermatozoid
sugars) into the growing embryo through amor- and the immediate transfer of the gametophyte
phous mucopolysaccharides accumulating (as to a thiouracil-free medium, gives rise to an
part of a quasi “defense reaction”) at the apposed embryo which quickly reverts to gametophytic
faces of the dissimilar generations. The situation growth. This provides a very satisfactory demon-
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 209

Figure 7.44. Pteridium aquilinum.

Vertical section of embryo.

fectly formed and functional,

and are capable of fertilizing
eggs of related sexual species.
Subsequently, however, in
place of archegonia, a sporo-
phyte develops directly from
the subapical region of the
gametophyte. The cellular
mechanisms underlying this
kind of life cycle are not yet
understood. The condition is
however known to be geneti-
cally dominant since hybrids
stration of the rôle of RNA in the control of with sexual species have the same kind of apoga-
morphogenesis. mous cycle. Ferns such as D. affinis subsp. affinis are
It seems highly likely that intragametophytic said to be agamosporic; it is estimated that 10
selfing occurs not infrequently in fern popula- percent of homosporous ferns have a cycle of this
tions. Some experiments have failed to demon- kind.
strate deleterious effects of such selfing, but a Another, much rarer, form of apogamous cycle
long-term experiment with Athyrium filix-femina is found in a few ferns. Here it is the first meiotic
has clearly brought out the greater fitness of the division which fails, but the end result is the
progeny of intergametophytic mating. In natural same, 32 spores being produced in place of 64 (Fig.
populations, the progeny of intragametophytic 7.45B). The spermatozoids produced by the game-
mating are probably eliminated at an earlier stage tophytes of these ferns are sluggish and probably
than their heterozygous neighbors. inactive. The heritability of this form of cycle has
Aberrations of the fern life cycle are not not been established.
uncommon. Apogamy, the production of a sporo- Experimentally, apogamy can sometimes be
phyte without sexual fusion, occurs regularly in induced by withholding water from gametophy-
some ferns and can be induced experimentally in tes and preventing sexual reproduction.
others. Dryopteris affinis subsp. affinis (D. borreri) Sporophytes have been raised in this way from
provides an example of a regular apogamous cycle gametophytes of Dryopteris filix-mas and Dryopteris
(Fig. 7.45A). In this and similar species the final dilatata. In Pteridium in pure culture apogamous
mitosis of the sporogenous cells is incomplete. outgrowths are promoted by a high level of
Following division of the chromosomes the sucrose. Such experimentally produced sporo-
nucleus re-forms. The cell remains undivided, phytes are often depauperate, and if they reach
although it has grown considerably as if a normal meiosis fail to produce viable spores. They natu-
division were about to occur. Instead it becomes a rally lack the pre-meiotic doubling of the chromo-
spore mother cell. The restitution nucleus, which somes characteristic of the D. affinis kind of cycle.
has twice the sporophytic number of chromo- The direct production of gametophytes from
somes, enters meiosis. The four spores produced, sporophytes (apospory) can be very readily
reflecting the large size of the spore mother cell, induced in culture by placing fragments of juve-
have diameters of about 80 ␮m, and contain nile leaves in sterile conditions on an agar
nuclei with the same number of chromosomes as medium. The gametophytes are usually sexually
the parent sporophyte. The spores germinate in perfect and yield tetraploid sporophytes. This phe-
the normal way and the gametophytes pass nomenon may occur sporadically in the wild and
through a male phase. The spermatozoids are per- lead to the production of natural autopolyploids.
210 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.45. Apogamous life cycles in ferns. (A) As in

Dryopteris affinis subsp. affinis. (B) As in Asplenium aethiopicum.
(From Klekowski. 1973. American Journal of Botany 60,
modified.)
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 211

Autopolyploids may also arise (probably more relationships of a range of hybrids of A. septentrio-
usually) by chance failure of reduction in meiosis. nale and A. trichomanes (known collectively as A.
alternifolium). The molecular evidence, coupled
e vo l u t i o n with the knowledge from ultrastructural studies
The evolutionary relationships of the living that the fully developed spermatozoids of ferns
Polypodiales can be studied at two levels. First, by lack plastids, point conclusively to A. septentrionale
carrying out crosses between living species and having acted predominantly as the female parent.
examining the pairing behavior of the chromo- This unidirectional hybridization can be related
somes at meiosis we can obtain evidence of the satisfactorily to the ecology and phenology of the
extent of the genetic identity between them. gametophytes of the parent species.
Second, by comparing the morphology and By contrast, the study of the fossil Polypodiales
anatomy of living species with the fossil we can has given valuable information about the evolu-
obtain a general impression of the evolution of tionary status of the present-day families. The
the contemporary fern flora. Schizaeaceae, for example, have a well-established
Studies of chromosome homologies at fossil history, possibly extending back to the
meiosis, facilitated by the ease with which squash Paleozoic, although the oldest undisputed repre-
preparations can be made of developing sporan- sentative of the family is Klukia from the Jurassic.
gia, have shown that many familiar species are of Tempskya (Fig. 7.46), one of the strangest fern
hybrid origin. Dryopteris filix-mas, for example, is fossils, has been assigned to the Schizaeaceae.
an allotetraploid probably derived from a hybrid Known only from stem fragments of Cretaceous
between two diploid ancestors, one similar to D. age, it is believed to have been a small tree fern
oreades (D. abbreviata) and the other to D. caucasica. with a composite trunk consisting of numerous
Particularly interesting is that widespread forms ramifying axes bound together by adventitious
of some species are autotetraploids. A familiar roots. The branching crowns of some Osmundales
example is the subspecies quadrivalens of Asplenium approach a similar structure. Some authors prefer
trichomanes. Other species are possibly tetraploid to place Tempskya in a separate family
in origin, but isozyme analysis shows that they (Tempskyaceae). The Gleicheniaceae have a
behave as diploids. Representative of this situa- history similar to that of the Schizaeaceae, again
tion is the common Pteridium (n⫽52). Selfing becoming relatively abundant in the Mesozoic.
experiments with Pteridium have nevertheless Other families, such as the Matoniaceae, first
revealed considerable genetic variation in the appear in the Mesozoic. Nevertheless, despite
progeny. This may arise from recombination these evidences of antiquity, most of the living
between duplicated unlinked loci in homoeolo- Polypodiales either have no fossil record, or no
gous chromosomes (homoeologous heterozygosity), record extending back further than the Tertiary.
and would be in line with the view that, despite This is particularly true of the large family
the enzyme results, the species is ancestrally tetra- Polypodiaceae, and we must suppose that these
ploid. Hybridization and duplication of chromo- ferns are comparatively recent, probably having
some number undoubtedly account for much of evolved toward the end of the Cretaceous period
the diversity in living ferns, but provide for little and subsequently.
profound anatomical or morphological change. Comparison of the living Polypodiales with
The development of techniques involving the the fossil, quite apart from tracing particular lin-
polymerase chain reaction (PCR), allowing the eages, also reveals those features which can be
amplification of minute quantities of DNA, has regarded in a general way as primitive. Protostelic
enabled the investigation in depth of the chloro- and solenostelic vascular systems, the simultane-
plast genome, providing yet another approach to ous production of the sporangia in the sori, short
problems of recent phylogeny. In Asplenium, for thick sporangial stalks, the indurated cells of the
example, comparison of the lengths of a non- sporangial wall aggregated laterally or arranged
coding intron in the chloroplast DNA has facili- in a transverse annulus, and a large number of
tated a clear understanding of the parental spores in each sporangium are all features of the
212 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

retained here, and the position of some of the

more important families and genera in this
double classification is shown in Table 7.1. This
classification does not of course imply that living
families and genera have evolved from each other;
it merely illustrates relative primitiveness. The
arrangement is substantiated by the fossil record
which is of greater duration in respect of the
Polypodiales at the bottom of the table than of
those at the top.

The Hydropteridales (Salviniales and

Marsileales)
The Hydropteridales (water ferns) are outstanding
in being genuinely heterosporous. Although
mainly plants of fresh waters and swamps, some
Figure 7.46. (A) Reconstruction of Tempskya. Scale bar 1m. species are characteristic of sites subject to sea-
(B) Transverse section of composite trunk. Scale bar 20cm. sonal drying. Hydropterids of the family
(From Stewart and Rothwell. 1993. Paleobotany and the Marsileaceae have a creeping rhizome bearing
Evolution of Plants, 2nd edn. Cambridge University Press, New subulate (Fig. 7.47), bifoliate or quadrifoliate
York.) leaves. Those of the family Salviniaceae are
floating plants with short branching rhizomes.
early Polypodiales. Conversely, dictyosteles, the The leaves are shortly petioled or sessile. In
production of mixed sori, long and delicate spo- Salvinia the surface of the upper leaves is made
rangial stalks, vertical annuli, and low spore unwettable by a covering of waxy hairs; the lower
numbers are all features of Polypodiales with leaves are submerged and much divided, taking
little or no fossil record. the place of roots. In Azolla (Fig. 7.48) the leaves are
On the basis of these criteria it is possible to minute and unequally two-lobed, the larger upper
assign the families of living ferns to three grades lobe floating and containing a mucilaginous
according to their evolutionary advancement. It is chamber inhabited by the blue-green alga
also possible to arrange them in two series, Anabaena azollae. The delicate roots of Azolla, being
according to whether the sporangia are marginal devoid of soil, are very suitable objects for the
or superficial in origin, but recent research has study of root growth. Serial sectioning reveals how
thrown considerable doubt upon the significance the cell lineages derived from the three posterior
of this feature. Nevertheless, it is tentatively faces of the apical cell generate the mature root.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 213

Table 7.1 Classification of representative genera and families of living Polypodiales based on evolutionary
development and origin of sporangia.

Position of origin of sporangia

Features of evolutionary significance Marginal Superficial
27–8→25–6

Steles, commonly dictyosteles. Sori mixed. Pteridium Dryopteris

Numbers of spores per sporangium

forming sporangial stalk →

Sporangia with vertical annuli interrupted Davallia Polystichum

Reduction in number of cells

at stalk Asplenium
Athyrium
Polypodium

Steles, dictyosteles or solenosteles. Sori Hymenophyllaceae Cyatheaceae

gradate. Sporangia with oblique annuli

Steles, protosteles or solenosteles. Sori Schizaeaceae Gleicheniaceae

simultaneous. Indurated cells of sporangial
wall aggregated, or in transverse on


oblique annuli

Figure 7.47. Pilularia globulifera. (a) Habit. (b) Transverse

section of sporocarp showing the four sori. (c) Longitudinal
section of inseminated archegonium. ((a) after Hyde and
Wade. 1940. Welsh Ferns. National Museum, Cardiff.)
214 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.48. Azolla filiculoides. (a) Habit. (b) Lower surface

of shoot showing a pair of microsporangial sori: m, sufficiently to permit the entry of water. This may
microsporangial sorus; r, root. Accompanying sporulation (in take years, but the viability of the spores declines
temperate regions occurring toward the end of the growing only very slowly during this period of dormancy.
season) the leaves often develop a reddish pigmentation. When water eventually enters, the sori are carried
Scale bars 1mm. (After Campbell. 1905. The Structure and out of the ruptured sporocarp by a worm-like
Development of Mosses and Ferns. Macmillan, New York.)
expansion of the gelatinous remains of the fertile
pinnules. The liberated spores germinate at once;
Some hydropterids have economic value. In the megaspore rapidly gives rise to a single arche-
rice-growing areas Azolla, on account of its nitro- gonium surrounded by a few somatic cells (which
gen-fixing symbiont Anabaena, is used extensively may develop chlorophyll), while the microspores
as a green manure. The vegetative parts of Marsilea each produce a single antheridium containing 16
yield a sedative used in Indian medicine, and the spermatocytes. Investigation of the spermato-
sporocarps are a source of starch. zoids of Marsilea has revealed that they have the
same basic structure (Fig. 7.49) as those of the
r e p ro d u c t i o n Polypodiales, although about twice the length.
In Pilularia (Fig. 7.47), representative of the The mitochondrion entering into the structure of
Marsileaceae, fertile pinnules are produced at the the helix is spectacularly large.
base of the petiole. They curve over the developing The sporocarps of the Salviniaceae open more
sporangia and become concrescent and eventu- readily than those of the Marsileaceae. In Azolla the
ally hardened, so producing the sporocarp. The megaspore is surrounded by four frothy massulae
ridge-like placentae bear megasporangia below (Fig. 7.50) formed from the tapetum, and these give
and microsporangia above (although in Marsilea the liberated megaspore buoyancy, but it is doubt-
the positions are reversed). In Azolla (Salviniaceae) ful whether they keep it afloat indefinitely. A vari-
the sporangia develop on the submerged lower able number of massulae are formed in the
lobe of the leaf (Fig. 7.48b), microsporangia and microsporangium (Fig. 7.51). Each includes a
megasporangia being produced in separate sori. number of microspores at its periphery, and is fur-
The sporocarp is formed by an elaborate indusium nished externally with peculiar anchor-like glo-
which totally encloses the sorus. Sporogenesis in chidia. These male massulae hook themselves to
the hydropterids is similar to that in homospor- the female, and the complex then sinks.
ous ferns, but in the megasporangia all but one of Germination of the spores, in the main similar to
the potential megaspores are resorbed. that of the spores of the Marsileaceae, then
Contrasting with the single megaspore in the follows. Embryogenesis is much more rapid in the
mature megasporangium, the microsporangia heterosporous ferns than in the homosporous.
typically contain 64 microspores. Fertilization occurs within about 12 hours of the
The sporocarps of the Marsileaceae open only germination of the spores, and an embryo emerges
after the wall has weathered and been abraded from the archegonium on the following day.
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 215

Figure 7.49. Marsilea vestita, spermatozoid. Drawing based

on observation of living gametes and electron micrographs.
The prominent mitochondrion, if straightened, would reach a
length of approximately 75␮m. The plasmalemma at the
posterior of the cell is shown in its expanded, bladder-like,
form following shedding of the terminal vesicle containing
plastids and small mitochondria. Scale bar 1 ␮m. (From Myles
and Bell. 1975. Journal of Cell Science 17.)
216 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 2

Figure 7.50. Azolla filiculoides. (a)

Longitudinal section of
megasporangium. (b) Liberated
megaspore with male massulae
attached. (After Strasburger. 1873.
Über Azolla. Abel, Leipzig.)

Figure 7.51. Azolla filiculoides. (a)

Longitudinal section of young
microsporangial sorus. (b)
Transverse section of mature
microsporangium. ((a) after
Campbell. 1905. The Structure and
Development of Mosses and Ferns.
Macmillan, New York; (b) after
Smith. 1955. Cryptogamic Botany, vol.
II. McGraw-Hill, New York.)
 TRACHEOPHYTES WITH TERMINAL SPORANGIA (EUPHYLLOPHYTINA) (cont.): FERNS 217

origin
The origins of the hydropterid ferns are altogether
obscure. Although the fossil record of the
Marsileaceae is meager, remains of reproductive
parts resembling those of Azolla are identifiable as
far back as the Lower Cretaceous. Compressed
branching systems of Azolla, often with reproduc-
tive structures, are known from the Upper
Cretaceous. Recent fossil evidence has yielded a
possible common ancestor for the two families.
Hydropteris (Fig. 7.52), from the late Cretaceous,
had a marsileaceaean morphology but salvinia-
ceaean reproductive features, seemingly closely
linking these two families. The introduction of
Hydropteris as a generic name validates the use of
Hydropteridales as the name of the order contain-
ing the water ferns.

Figure 7.52. Hydropteris pinnata, reconstruction. Scale bar

5 mm. (From Rothwell and Stockey. 1994. American Journal of
Botany 81.)
8

The subkingdom Embryophyta (cont.):

division Tracheophyta, Part 3
Primitive ovulate plants and their spores 150–500 ␮m in diameter, the two classes of
precursors (Progymnospermopsida) spores being borne in separate sporangia.
The class Progymnospermopsida contains only Amongst other plants assigned to the progym-
fossil plants. The concept of progymnospermy, a nosperms are Aneurophyton (Aneurophytales),
stage at which plants with conifer-like anatomy known from the Middle and Upper Devonian of
and morphology were still reproducing by spores, Europe and North America, and Protopitys
followed the surprising discovery that certain (Protopityales) from the Lower Carboniferous of
well-preserved trees of the Upper Devonian bore Scotland. The axes of Aneurophyton contained a
frond-like sprays of branches, some of which bore core of primary xylem, triangular in section, sur-
clusters of sporangia. Callixylon, the first progym- rounded by secondary wood. The spirally
nosperm to be recognized, provides a splendid arranged branches dichotomized two or three
example of this stage of evolution (Fig. 8.1a). The times, some terminating in tassels of sporangia.
trunks reached a diameter of 1.5 m (5 ft) and a Aneurophyton appears to have been homosporous.
length of 8 m (26 ft) or more. Permineralized The abundant pycnoxylic wood of Protopitys indi-
remains reveal fine details of the anatomy. A cates that it is the remains of a tree. The branches
central pith was surrounded by mesarch primary were distichously arranged and sporangia were
xylem. Outside this lay a considerable thickness borne in small terminal clusters. The diameter of
of well-developed secondary xylem traversed by the spores lay between 80 and 160 ␮m. Protopitys
narrow rays. The pits in the radial walls of the was probably heterosporous.
tracheids were frequently grouped, the groups The progymnosperms, which first become rec-
aligned horizontally and in register with trach- ognizable in the Middle Devonian and extend to
eids in the rays. Dense wood of this kind, also the Lower Carboniferous (and possibly later), rep-
characteristic of modern conifers, is termed pyc- resent a significant intermediate stage in the evo-
noxylic. lution of the land flora. The notion that the frond
Although Callixylon was known for many years originated from a lateral branch system (p. 172) is
as the trunk of a late Devonian tree, only much clearly supported by Callixylon and Archaeopteris
later were discovered specimens in organic con- (Archaeopteridales). Anatomically the pycnoxylic
nection with frond-like branches. These branches wood of the progymnosperms is strikingly
were already known as Archaeopteris and had been modern in appearance, and some forms show
assumed to be the fronds of ferns. Archaeopteris is clear examples of a bifacial cambium producing
known both sterile and fertile (Fig. 8.1b). The spo- files of secondary phloem at its outer face. Further,
rangia were spindle-shaped, up to 3.5 mm (0.14 in.) gymnospermous reproduction presumably arose
in length, and occasionally with stomata in the from heterosporous of the kind seen in many pro-
epidermis. Heterospory occurred in some species, gymnosperms, although seeds are known almost
the microspores being 30–70 ␮m and the mega- as old as the progymnosperms (see p. 219).
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 219

Figure 8.1. (a) Callixylon

(Archaeopteris), reconstruction. (b)
Archaeopteris halliana.
Reconstruction of branch with
sterile leaves and fertile appendages.
(After Phillips, Andrews and Gensel,
from Stewart. 1983. Paleobotany and
the Evolution of Plants. Cambridge
University Press, Cambridge, New
York.)

present, consisting of tracheids

(in a few forms also of vessels)
and sieve cells. Sporangia
borne on specialized struc-
tures, probably of axial origin.
Heterospory general.
Megasporogenesis occurring
within a specialized tissue
(nucellus), this in turn sur-
rounded by a distinctive sheath
(integument), the whole
termed the ovule. Neither male nor female game-
SPERMATOPHYTINA (seed tophytes autotrophic. Fertilization by multiflagel-
late spermatozoids, or by male cells with no
plants): GYMNOSPERMS specialized means of locomotion, occurring
within the ovule, either before or after its being
The seed habit, the formation and retention of the shed. Embryogeny endoscopic, the embryo
embryo within an integumented megasporan- remaining contained within the seed developed
gium, is evidently of great antiquity. In paleobot- from the ovule.
any the term “seed” is also used for fossilized One of the most fully investigated of the early
ovules, the later stages of seed formation being gymnospermous seeds is Archaeosperma (Fig. 8.2a
inferred. In general the early seeds of the and b) from the Upper Devonian of Pennsylvania.
Paleozoic terminated axes, and were either bilat- Here the nucellus (megasporangium) was sur-
erally symmetrical (platyspermic) or radial (radio- rounded by an integument. This was deeply lobed
spermic). Examples of each are known from the late above, revealing radial symmetry. The single func-
Devonian. Very similar seeds are borne by some tional megaspore was surmounted by three
living plants. Together, the living and fossil forms abortive spores. Their triradiate markings show
constitute the gymnosperms, a name which that the tetrad had tetrahedral symmetry.
implies that the seeds are naked, unenclosed in Megasporogenesis in Archaeosperma thus resem-
any carpellary structure. The fossil record indi- bled that in heterosporous ferns such as Pilularia
cates clearly that gymnospermy is the most prim- and Marsilea (p. 214). In Xenotheca (Fig. 8.2c),
itive form of the seed habit. another early Devonian seed, the integument was
Although a diverse division with possibly even more deeply lobed above than in
more than one origin from the early land plants, Archaeosperma.
the general characteristics of the gymnosperms Little is yet known of the plants which bore the
(not all being represented in the fossil forms) can Devonian seeds. Knowledge of the early
be summarized as follows: Carboniferous gymnosperms, although fuller
Sporophyte usually arborescent; branching and than that of the late Devonian representatives,
leaves various. Secondary vascular tissue always also remains limited. It seems likely, however, that
220 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.2. Archaeosperma arnoldii. (a) The two-seeded

cupules were borne in pairs, the two pairs of seeds facing
radiospermy. By contrast, relatives such as the
each other. (b) Reconstruction of an individual seed showing Gnetopsida, Bennettitales and Caytoniales reveal
the three abortive megaspores at the top of the one which is features which suggest an affinity with the angio-
functional. The integument is deeply lobed above. (c) The sperms (Fig. 8.3). These groups may therefore be
primitive Xenotheca devonica, showing even deeper lobing of seen as representing a natural sequence from the
the integument, exposing the upper part of the nucellus. ((a), most primitive to the most specialized seed
(b) after Pettitt and Beck. 1968. Contributions from the plants. The Pinopsida (Coniferales, conifers) have
Museum of Paleontology, University of Michigan 22; (c) after
an obscure origin, but quickly became distinct in
Hilton and Edwards, in Kurmann and Hemsley (eds.) 1988.
their generally pycnoxylic wood, platyspermy, and
The Evolution of Plant Architecture. Royal Botanic Gardens,
Kew.) simple, often needle-like leaves. Their relation-
ship to the Ginkgoopsida is unclear, and judg-
ment depends upon the relative emphasis placed
some were impressive trees. Pitus (Pitys), for upon vegetative as opposed to reproductive char-
example, almost certainly a gymnosperm, had acters.
enormous trunks, reaching in some instances a
diameter of 2 m (6.5 ft). Later in the Carboniferous Early radiospermic gymnosperms
remains become sufficiently numerous for the
recognition of distinct classes, of which two Lyginopteridopsida
(Cycadopsida and Pinopsida) have descendants (Pteridospermopsida)
living today.
The Cycadopsida, of which few still exist, have The Lyginopteridales
a fossil record that can be linked to the Investigators of the fern-like fronds found in
Carboniferous Lyginopteridales and Medullosales Carboniferous rocks soon became aware that not
(the extinct “seed ferns”) with which they share all these were in fact referable to ferns. Some were
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 221

Figure 8.3. (a) and (b) Spermatophyte cladograms

branched. There was a central pith, which con-
illustrating two of many equally likely trees. (c) A consensus
tree (one in which an “average” of alternative cladograms of tained nodules of thick-walled cells (similar to the
the seed plants is presented). The consensus tree indicates groups of stone cells in the flesh of a pear), sur-
how poorly resolved the spermatophyte groups remain. ((a), rounded by a ring of primary xylem strands (Fig.
(b) after Doyle and Donoghue. 1992. Brittonia 44; (c) after 8.4). Exterior to these was a relatively large
Crane, in Beck (ed.) 1988. Origin and Evolution of amount of secondary xylem. The tracheids of the
Gymnosperms. Columbia University Press, New York.) secondary xylem, like those of the metaxylem,
were furnished with bordered pits, but in the
undoubtedly associated with seeds, and others somewhat smaller tracheids of the secondary
with stems in which there were secondary thick- xylem they were absent from the tangential walls.
ening and other anatomical features rarely found A girdle of phloem, rarely well preserved, lay
in the Polypodiopsida. Nevertheless, the habit of outside the xylem. A characteristic feature of
these plants was probably something like that of Lyginopteris was the anatomy of the outer cortex.
the Marattiales (p. 176). The leaves were megaphyl- This contained radially elongated bands of fibers
lous, compound and pinnately branched, and which anastomosed freely and clearly gave consid-
borne on stems of varying height. Together they erable mechanical support to the stem.
comprise the Lyginopteridales (Cycadofilicales), The leaves of Lyginopteris (originally described
and are representative of the earliest as Sphenopteris) were borne in a 2/5 phyllotaxy and
Lyginopteridopsida (pteridosperms). when young showed circinate vernation. In
The features of the pteridosperm stem are well mature leaves, which sometimes reached a length
shown by the Carboniferous Lyginopteris. These of 50 cm (19 in.), the rachis dichotomized at about
well-preserved axes ranged in diameter from half its length, but the remainder of the branch-
about 0.5 to 4 cm (0.2–1.6 in.), and occasionally ing was pinnate and the ultimate segments were
222 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.4. Lyginopteris oldhamia.

Transverse section of stem. The
glandular epidermis has been lost.
The leaf trace divides into two
strands in the cortex, but these
reunite to form a V-shaped trace at
the base of the petiole.

narrow pinnules. The outer

surface of many parts of
Lyginopteris was furnished
with peculiar multicellular
glands, a feature which has
enabled paleobotanists to
reconstruct the entire aerial
part of the plant from discon-
nected fragments.

r e p ro d u c t i v e
structures
The female reproductive
organs of Lyginopteris are also
known in detail. The ovules
(originally described as Lagenostoma) terminated space between the base of the sheath and the
axes which were probably branches of otherwise column (referred to as the “pollen chamber”).
normal leaves. Each ovule (or seed) was partially Germination may have occurred here, but few
enclosed in a cup formed by a number of glandu- details are yet known. A female gametophyte, sur-
lar and basally fused bracts (Fig. 8.5a). This struc- rounded by a distinct membrane and bearing
ture, called a cupule, in some forms contained archegonia at its upper surface, lay within the
more than one ovule. The ovule itself was an nucellus. This gametophyte probably developed
upright, radially symmetrical structure, about from a megaspore, formed as one of a tetrad
0.5 cm (0.2 in.) long and a little less broad. The within the nucellus, the remaining megaspores
central part (Fig. 8.5b), the nucellus, possibly a spe- degenerating.
cialized archesporial tissue, was surrounded by The male reproductive organ of Lyginopteris is
an integument of two layers, the outer of which not yet identified with certainty. It is, however,
contained a sclerenchymatous sheath. A single very probable that it consisted of a small ovate
vascular bundle entered the base of the ovule and plate, about 2 mm (0.08 in.) in length, terminating
divided symmetrically into nine parts which a branchlet and bearing about six or more bilocu-
ascended the inner fleshy part of the integument. lar sporangia (Fig. 8.6b). Each sporangium was
The upper part of the integument around the about 3 mm (0.13 in.) long and 1.5 mm (0.06 in.)
micropyle was shallowly lobed, the lobing corre- wide. The microsporangiophores were borne on a
sponding to the intervals between the ascending branch system (the whole being known as
veins. The nucellus was fused to the integument Crossotheca) which may have formed part of a
except at its summit. Here the apical portion Lyginopteris leaf (Fig. 8.6a).
ascended as a column, surrounded by a sheath of The pollen grains (Fig. 8.6c), which bore trira-
similar tissue (Fig. 8.5b). This specialized develop- diate scars, were presumably distributed by wind.
ment of the upper part of the nucellus, probably By analogy with the pollination of living gymnos-
serving as an effective pollen trap, is termed the permous ovules, it is thought the grains were
lagenostome. Pollen grains are often observed in the trapped by a drop of sugary fluid which protruded
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 223

Figure 8.5. Lagenostoma lomaxi. (a) Reconstruction of seed gumented megasporangium. Although no inter-
and cupule. The heads of the glandular hairs are shown in
mediate stages in such a transformation have yet
black. (b) Longitudinal section of seed. ((a) after a drawing by
come to light, it is significant that in one of the
F. W. Olive; (b) after Walton. 1940. An Introduction to the
Study of Fossil Plants. Black, London.) earliest pteridosperm seeds from the Lower
Carboniferous (Salpingostoma) the integument
consists of a ring of finger-like processes, each con-
from the micropyle, and that subsequent absorp- taining a vein, fused only in the basal region. In
tion of this drop drew the grains down into the such ovules, often termed “pre-ovules”, there was
pollen chamber. Germination of the grains is no clearly defined micropyle. Progressive fusion of
thought to have been proximal (i.e., at the site of components could nevertheless have led to the
the triradiate scar, as with the spores of ferns and entire integuments of the pteridosperm seeds of
bryophytes). This contrasts with the regular distal the Upper Carboniferous (Fig. 8.7D), the shallow
germination of living conifer and angiosperm lobing often seen in the micropylar region of
pollen. Pteridosperm pollen is accordingly often these integuments being the only remaining indi-
referred to as “pre-pollen”. The production of pre- cation of their compound origin. Experiments
pollen is thought likely to have been accompanied with models have shown that the finger-like
subsequently by zooidogamous fertilization. extensions of the integument seen in some of the
Embryos have only rarely been found in pteri- early seeds may, by setting up local turbulence,
dosperm seeds, and their absence is not readily have assisted in trapping wind-borne pollen above
explained. Megagametophytes with archegonia the nucellus. The development of the lagenos-
are not uncommon, and have been seen in the ear- tome, with its distinctive pollen chamber, at this
liest seeds of the late Devonian. site seems to have been a feature of the earliest
radiospermic seeds, and may even have been
origin present in remains of cupulate seeds found in the
The pteridosperms probably had their origin in Upper Devonian. The lagenostome of the pre-
axial plants resembling the progymnosperms, the ovule Hydrosperma, found in beds laid down at the
fronds again being derived from lateral sprays of Devonian–Carboniferous transition, has been
branchlets. The radial symmetry of many pterido- studied in some detail. It seems likely that, follow-
sperm seeds suggests that they may have evolved ing pollination, the floor of the pollen chamber
from tassels of megasporangia in which a central rose, pushing up the central column so that its
megasporangium became closely surrounded by a summit blocked the entrance to the chamber
ring of similar megasporangia (Fig. 8.7A and B). from above. In this way the chamber, in vivo prob-
Sterilization of the outer ring (Fig. 8.7C), but not ably containing a sugary secretion, became a
of the center, would then have resulted in an inte- sealed “culture sac” in which the pollen was able
224 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.6. Crossotheca. (a) Reconstruction of fertile shoot.

(b) Detail of the fertile pinnule of Crossotheca sagittata. (c)
Microspore (pollen grain). The deep cleavage at the site of
the triradiate scar indicates proximal germination. ((a) after
Andrews. 1961. Studies in Paleobotany. Wiley, New York; (b)
after Millay and Taylor. 1977. American Journal of Botany 64; (c)
from a preparation by R. Kidston, photographed by W. G.
Chaloner.)

Figure 8.7. Diagrammatic representation of the derivation

of an integumented lyginopterid ovule from a tassel of
megasporangia. Further explanation in text.
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 225

Figure 8.8. Reconstruction of

Medullosa, based on M. noei. The
plant reached a height of about 4m
(14ft). (After Stewart and
Delevoryas. 1956. Botanical Review
22.)

the end of the Paleozoic

other, more complex, forms
(of which Medullosa is repre-
sentative) became prominent.
They were more like tree ferns
in habit (Fig. 8.8), sometimes
possibly scrambling. The
leaves had large petioles
which bifurcated at some dis-
tance from the stem, result-
ing in a frond which consisted
of two symmetrical halves.
The subsequent branching
was pinnate. The pinnules (as
seen in Alethopteris, Neuropteris
and other dispersed leaf
genera) were conspicuously
larger than those of the
earlier pteridosperms. The
anatomy of the stem was par-
ticularly complex, the xylem
usually being split into
several segments. In addition,
axial bundles of primary
xylem (called “sympodia”)
were present at the outer
to germinate. This “hydrosperman reproduction” edges of these segments. Secondary wood, con-
is believed to have been widespread in the early sisting of large tracheids and extensive rays, sur-
radiospermic seeds. rounded the primary. Secondary wood of this
The development of ovules containing single kind, which is relatively soft and spongy, is
megaspores from progymnospermous megaspo- termed manoxylic. It is also found in some living
rangia is unlikely to have been a smooth progres- gymnosperms, notably the cycads (p. 247). The
sion. The regular failure of three of the spores in leaf traces were also complex, each consisting of
the tetrad to develop (seen also in Lepidocarpon, several strands. The strands comprising the trace
Fig. 6.14) indicates precisely controlled events for a single leaf originated from one or more of
within the tetrad. This may have been the conse- the sympodia.
quence of a relatively simple mutation, but clearly The seeds, placed in the genus Pachytesta, were
one of great significance in plant evolution. about six times the size of those of Lyginopteris,
and were more clearly borne in association with
The Medullosales foliar organs. They were distinctly trimerous and
Lyginopteris is typical of a wide range of lacked a cupule (Fig. 8.9a and b). The microspores
Carboniferous Lyginopteridopsida, but toward (pre-pollen), which were monolete, were produced
226 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.9. (a) Pachytesta attached

to Alethopteris foliage. The seed was
about 40mm (1.6in.) long and
12 mm (0.5in.) in width. (b)
Pachytesta illinoensis in section: m,
micropyle; pc, pollen chamber; n,
nucellus; i, integument. (From
Stewart and Rothwell. 1993.
Paleobotany and the Evolution of
Plants, 2nd edn. Cambridge
University Press, New York.)

in large tubular sporangia,

borne in fused clusters (synan-
gia).

The descendants of the

Lyginopteridopsida
The Lyginopteridales may well
have given rise to the Callis-
tophytales, a group of pterido-
sperms with a Lyginopteris-like
stele, platyspermic seeds and saccate pollen. A cal- puzzling plants, almost certainly derived from
listophytalean ovule from the mid-Pennsylvanian the pteridosperms and probably of very great
(Table 1.1) has provided the best evidence yet for importance in the evolution of the later seed
the existence, already in Paleozoic times, of a “pol- plants. Some of them had leaves with reticulate
lination drop” mechanism for the capture of venation and an appearance strikingly like that of
pollen (p. 237). The micropyle of the ovule was the leaves of some modern flowering plants.
filled with material, which in life may have been Others had seeds in partially closed cupules, a
a syrupy secretion, containing scattered pollen development possibly leading to the remarkable
grains. The grains of some forms may have germi- fruiting body of the Caytoniaceae (p. 254).
nated distally. Clear indications of nuclear divi- Elsewhere, from a pteridospermic ancestor, most
sions have been seen within some grains, and also likely within the Medullosales, the earliest cycads
indications of pollen tubes. Although many of appeared. The Glossopteridales (p. 255),
these features are suggestive of the Pinopsida, Bennettitales (p. 252) and other radiospermic
stratigraphic evidence precludes an origin of the orders are also most probably descended from
Pinopsida from the Callistophytales. Like the pteridospermic antecedents.
Lyginopteridales, the Callistophytales became
extinct at, or just after, the end of the Platyspermic gymnosperms and pine
Carboniferous. relatives
It seems beyond doubt that some pterido-
sperms persisted into the early Mesozoic, Pinopsida
although the remains become much less fre- The Pinopsida have been distinct since their
quent after the close of the Paleozoic era and of origin in the Upper Devonian/Lower
an unfamiliar form. There is also evidence that Carboniferous. Their origin in relation to the
the evolution of the pteridosperms in the north- Progymnospermopsida and Pteridospermopsida
ern and southern hemispheres diverged at this remains wholly uncertain. Pycnoxylic wood, pla-
time, but the two floras remained in contact in tyspermy and parallel-veined leaves have been fea-
certain regions of Africa. The early Mesozoic tures characteristic of the Pinopsida since the
rocks of these regions have yielded a number of Cordaitales of the Carboniferous.
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 227

Figure 8.10. (a) Reconstruction of

a cordaitalean shoot. (b)
Cordaianthus concinnus.
Reconstruction of two male shoots.
((a) after Grand’Eury, from
Andrews. 1961. Studies in
Paleobotany. Wiley, New York; (b)
after Delevoryas. 1953. American
Journal of Botany, 40.)

mineralized while they were

penetrating decaying remains
of other plants. They show a
triarch stelar structure, and a distinct root cap at
The Cordaitales the growing tip.
Although vegetatively resembling some modern
pinopsids, the Cordaitales were in other ways r e p ro d u c t i v e s t r u c t u r e s
quite distinct. They must have been amongst the The reproductive organs of the Cordaitales
most impressive of the seed-bearing plants of the (known as Cordaianthus) were borne on slender
later Paleozoic. So far as is known, they were branches. Although male and female were separ-
mostly arborescent with columnar trunks, many ate, they possibly occurred on the same tree. Each
probably reaching heights of 30 m (98 ft) and reproductive region was basically a axis, from 10
diameters of 1 m (39 in.). Some, however, were to 30 cm (4 –12 in.) in length (Fig. 8.10b), bearing
sprawling plants with adventitious roots, provid- two rows of bracts in a complanate distichous
ing a mangrove-like appearance. The leaves, arrangement. The male and female shoots
confined to the upper branches, were spirally occurred singly in the axils of the bracts.
arranged and strap-shaped (Fig. 8.10a). In some The individual male shoots (Fig. 8.10b) were
forms they were as much as 1 m (39 in.) in length about 1 cm (0.4 in.) long. Each consisted of a short,
and 15 cm (6 in.) in width. There was regular par- stout axis bearing a large number of linear-lance-
allel venation interspersed with longitudinal olate scales, each with a single vein, in a close
bands of hypodermal fibers, a structure not dis- spiral. The lower scales were sterile, and acute or
similar to that of the leaves of the modern conifer obtuse at their apices, but the upper were emargi-
Araucaria araucana (Fig. 8.13b). nate and terminated in several (usually six) cylin-
In general the vascular tissue of the cordaital- drical microsporangia. Since both sterile and
ean trunks consisted of a large amount of secon- fertile scales lay in one spiral, they appear to have
dary xylem, typically pycnoxylic, traversed by been of similar morphological nature. The pollen
narrow parenchymatous rays. The secondary grains were surrounded by air bladders (saccae)
tissues surrounded a medullated primary stele. formed by the separation of the layers of the wall.
The primary xylem tended to diminish in later The two layers remained in contact, however, in
forms, leaving a ring of mesarch bundles border- one region, possibly the site of liberation of the
ing an extensive pith, often broken up into lentic- gametes. This thin area was opposite the small tri-
ular diaphragms. The secondary tracheids showed radiate scar at the proximal pole of the grain. It
several series of circular bordered pits on their thus appears that the Cordaitales had true pollen
radial walls, and were closely similar to those of with distal germination.
living conifer Araucaria. The leaf traces, which The female shoots were of similar organiza-
passed outward from the primary xylem, were tion, but the fertile scales terminated in ovules
simple in origin and commonly consisted of two instead of microsporangia. In earlier forms the
parallel strands. The roots of the Cordaitales are fertile scales (megasporangiophores) projected
quite well known, since they often became per- conspicuously from the shoot, branched, and
228 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.11. Cordaitalean seeds. (A) Axis of Cardiocarpus

with ovules. (B and C) Mitrospermum in longitudinal (B) and
which was sclerenchymatous. The nucellus,
transverse section (C), demonstrating extreme platyspermy: except for the basal region, appears to have been
m, micropyle; pc, pollen chamber; sc, sclerenchymatous layer separate from the integument. A female gameto-
within the integument (sclerotesta); s, softer outer layer of phyte, surrounded by a distinct “megaspore mem-
the integument (sarcotesta), with a peripheral wing-like brane”, developed within the nucellus, and
extension (w); vb, vascular bundle entering the ovule, the archegonia were produced on its upper surface,
branches ascending in the sarcotesta. Both Cardiocarpus and the nucellus above this region becoming differen-
Mitrospermum were about 15mm (0.6in.) long and about the
tiated as a pollen chamber. Reticulate markings
same in maximum diameter. (From Stewart and Rothwell.
on the pollen grains lying in this chamber were
1993. Paleobotany and the Evolution of Plants, 2nd edn.
Cambridge University Press, New York.)
once regarded as indicating endosporic germina-
tion of the grain, but this interpretation is now
questioned. The pattern is more probably a relic of
carried more than one seed (Fig. 8.11A). In the later the sculpturing of the wall than of an internal cel-
forms, however, the megasporangiophores were lular structure. Firm evidence for the production
shorter and unbranched, terminating in only one of a pollen tube is lacking. Gametes were possibly
seed concealed amongst the sterile scales. liberated into fluid above the archegonia. As with
The seeds of the Cordaitales were not radially the pteridosperms, embryos are conspicuously
symmetrical, but bilateral, the margin of the seed absent from cordaitalean seeds. The integument
often being extended as a wing. Because of their of a cordaitalean seed (Fig. 8.11B and C) has the
characteristic flattened appearance, these seeds appearance of having been formed by two valves,
are termed platyspermic, and they are readily dis- each containing a vein, coming together and
tinguishable from the predominantly radio- enclosing a megasporangium. This view is sup-
spermic seeds of the pteridosperms. Platyspermic ported by the occasional occurrence in female
seeds, similar to those seen in cordaitalean inflo- shoots of what are interpreted as abortive mega-
rescences, are frequently found detached in sporangia subtended by two unfused lobes. Each
Carboniferous deposits and their structure is now seed would thus have three components, the two
well known (Fig. 8.11B and C). They are about 1 cm outer which form the integument possibly having
(0.4 in.) in height and only a little less in their been derived from sterilized sporangia. It is note-
major transverse diameter; the minor is of the worthy in this connection that the microsporan-
order of 0.5 cm (0.2 in.). The integument was differ- gia were commonly produced in multiples of
entiated into one or more layers, at least one of three.
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 229

Figure 8.12. (a) Erect female cones on a branch of The Voltziales

Utrechtia. Scale bar 2.5cm. (b) Reconstruction of a cone The Voltziales are regarded as early forms of coni-
segment of Emporia. The recurved ovule is sectioned to
fers, but they show a close relationship, both veg-
show integument, nucellus and megaspore membrane. Scale
bar 1mm. (c) Microsporangiophore of Emporia with pollen
etative and reproductive, with the Cordaitales.
sacs. Scale bar 1mm. ((a) from Florin. 1951. Acta Horti Representative of the Upper Carboniferous
Bergiana 15; (b), (c) from Stewart and Rothwell. 1993. Voltziales are Utrechtia and Emporia (Fig. 8.12). The
Paleobotany and the Evolution of Plants, 2nd edn. Cambridge Voltziales had eustelic stems with exarch primary
University Press, New York.) vasculature. The wood was like that of the living
Araucaria (p. 231). Resin ducts occurred in the pith
origin and fossil history and cortex, and in the mesophyll of the leaves. The
Little is known of the origin of the Cordaitales, but female cone consisted of an axis about 8 cm (3 in.)
it possibly lay well before the Carboniferous long, bearing spirally or asymmetrically arranged
period. Remains of substantial woody plants, the bifid bracts. In the axil of each was a radially sym-
xylem of which showed araucarian pitting (p. 231), metrical, but flattened, dwarf shoot bearing small
have been found as early as the Middle Devonian bracts and a fertile scale (Fig. 8.12b). This fertile
(p. 218). In the leaves of some of the Cordaitales of scale bore a single ovule. The ovule was inverted,
the Lower Carboniferous the nerves branched as platyspermic, and adjacent to the side of the
they approached the tip, possibly indicating an fertile scale away from the bifid bract. This fertile
origin in a fan-shaped structure. Axes bearing short shoot can reasonably be regarded as
leaves of the kind envisaged are in fact known morphologically intermediate between the fertile
from the Middle Devonian of Bohemia, but the female shoots of the Cordaitales and the ovulifer-
relationship of these fossils (placed in the genus ous scale of a modern conifer (Fig. 8.20). A series of
Barrandeina) to the Cordaitales is quite unproven. fossils of late Paleozoic and early Mesozoic age, in
Nevertheless, the impression is that the which the vegetative and fertile parts of the
Cordaitales were derived from axial heterospor- female short shoot become progressively less dis-
ous forms in much the same way as the pterido- tinct, leads ultimately to a structure extremely
sperms, but that in the Cordaitales the megaphyll similar to an ovuliferous scale.
condensed into the characteristic strap-shaped The male cones of the Voltziales (Fig. 8.12c)
leaf and the integument of the seed evolved in a closely resembled those of modern conifers, and
slightly different way. The earliest platyspermic thus differed sharply from those of the
seeds come from the later Devonian. Cordaitales. Although the pollen grains of the
The Cordaitales probably persisted into the early conifers and of the Cordaitales were quite
beginning of the Mesozoic, but then became similar, in some of the earliest they may still have
extinct. been at the stage of “pre-pollen” (p. 223) and
230 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

motile spermatozoids may have been produced. tions on lower hills, but a straggling shrub with
Nevertheless, it is also possible that the siphonog- no evident main axis (Krummholz) when on lime-
amous reproduction seen in modern conifers stone at higher altitudes. Some conifers, although
evolved quite early. Perhaps the advantages of resistant to cold, cannot withstand summer
siphonogamy saved the early conifers from the drought. Picea sitchensis, for example, is restricted
extinction that befell the Cordaitales. in its native Pacific Northwest of America to the
fog zone. Here its growth rate reaches an impres-
The Pinales and Taxales (Coniferales) sive 100 mm (4 in.) or more in a year. Most conifers
The Coniferales (conifers) are the most wide- tend to be surface-rooted, and many species
spread of all the groups of gymnosperms, and produce stubby rootlets in the humus layer which
they form the climax vegetation at high altitudes are associated with mycorrhizal fungi. Large
and in the colder regions of the temperate zones, stands of conifers may be linked from root to root
particularly the north. They are much less by the mycelia of these fungi, with inevitable
common in the tropics, and here they are usually implications for disease transmission. Taxodium
confined to mountains and are often mixed with distichum (swamp cypress), which grows in swamps
angiospermous trees. Of all the vascular plants in the warmer parts of eastern North America, is
discussed so far the conifers are the first of signifi- outstanding amongst conifers in producing nega-
cant economic importance. They are almost all tively gravitropic aerophores which rise above the
arborescent and the wood is used extensively as surface of the water. These specialized roots are,
timber and as a source of pulp for paper-making however, found only in mature specimens and are
and related industries. rarely produced outside the native habitat.
The growth form of a conifer is frequently One conifer, Podocarpus ustus, has been found
pyramidal, the conspicuous main axis being the as a parasite on a species of Dacrydium (also
principal source of the valuable timber. A few con- Podocarpaceae) in New Caledonia. It may regu-
ifers of this form attain remarkable sizes and ages. larly be a root parasite, and, if so, is unique in the
Specimens of Sequoia (redwood), for example, in gymnosperms.
California frequently exceed 100 m (333 ft) in
height, their trunks reaching diameters of several shoots and stems
meters and showing over 2000 growth rings. The stems of conifers grow from a group of meris-
Pseudotsuga (Douglas fir) in the forests of the tematic cells. In some genera, notably Araucaria,
Olympic Peninsula of the Pacific Northwest may the apex is organized into a distinct tunica, in
attain even greater heights (but not girth). Agathis which divisions are principally anticlinal, and a
australis, the kauri pine of New Zealand, reaches central corpus, where divisions are in several
up to 60 m (200 ft) in height, and the trunks a planes. The corpus gives rise to the pith and
diameter of 7 m (20 ft). The oldest living conifers primary vascular tissue. In some conifers, particu-
are probably specimens of Pinus aristata (bristle- larly of the Pinales, a succession of shoots, pro-
cone pine) at high altitudes on the arid White duced in the axils of scale leaves, regularly
Mountains of the California–Nevada border. undergo little extension growth. The apices of
Modern techniques of dating show that some of these short shoots produce a few scale leaves and
these are almost 5000 years old. Another con- then, before the apex becomes inactive, a limited
tender for longevity is a specimen of Lagarastrobus number of fully developed mature leaves. In Pinus
franklinii (Podocarpaceae), a Tasmanian endemic, the number of these varies from one (Fig. 8.13a) to
claimed to be 11 000 years old. five, depending upon species. Extreme defolia-
Some conifers (such as the junipers) are bushy, tion, following for example a massive attack by
and a few (confined to Australasia) are dwarf, caterpillars, may result in the normally dormant
heather-like shrubs of boggy alpine situations. apices of the short shoots resuming extension
Occasionally the growth form is markedly influ- growth, so deforming the architecture of the
enced by the habitat. Pinus montana, for example, entire shoot system. In other conifers which bear
is a pyramidal tree when growing in acid situa- their leaves on mature stems principally in short
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 231

Figure 8.13. Forms of conifer leaf.

(a) Pinus monophylla. (b) Araucaria
araucana. (c) Chamaecyparis obtusa.

rower than those at its begin-

ning (Fig. 8.15). In Pinus the
tracheids, which rarely exceed
4 mm (0.17 in.) in length, bear
bordered pits, usually in a
single row, on the radial walls.
The central part of the pit
membrane is thickened and
forms the torus (Fig. 8.15).
Thickenings often present
along the margins of the pits
are termed the “Rims of
Sanio”. In Araucaria the pits
are similar, but in 3–4 rows, the pits of adjacent
rows alternating (referred to as “araucarian
pitting”). The tracheids of Araucaria, but not of
Pinus, occasionally have small trabeculae (initially
of cellulose, but subsequently lignified) extending
across the lumen. These so-called “Bars of Sanio”
also occur in a number of other genera.
Considerable differentiation is sometimes
present in the parenchymatous rays of conifer
woods. In Pinus, for example, the cells of the upper
and lower margins in the xylem portion of the ray
may form radially oriented tracheids (Fig. 8.15),
and cells in a similar position in the phloem
closely apply themselves to the sieve cells and
Figure 8.14. Pinus sylvestris. Transverse section of young become conspicuously rich in cytoplasm. The rays
stem with only one season’s secondary vascular tissue.
provide a means of transporting materials later-
ally in the growing stem.
shoots (e.g., Larix, Cedrus, Fig. 8.19), the number of The resin canals of conifers, which are schizog-
fully formed leaves in the short shoot is less enous in origin and interconnected, run longitu-
definite and does not form a specific character. dinally in the leaves (Fig. 8.16) and xylem, and also
The mature stems of conifers are mostly secon- transversely in some of the larger rays. The resin
dary wood, the pith and primary xylem being rel- itself (a complex acidic substance containing oxi-
atively inconspicuous (Fig. 8.14). At the outside, dized phenols and terpenes) is synthesized in the
the phloem, cortex and periderm form a compar- epithelium of the canals, probably mostly in the
atively narrow band. The dense secondary xylem younger tissues, but the actual site of synthesis in
consists of radial files of tracheids, traversed by the cells is not yet exactly known. The resin system
narrow parenchymatous rays. Wood parenchyma can be tapped by driving a gutter-shaped steel
is not conspicuous. In Pinus it is confined to the wedge into the xylem near the base of the tree
epithelium of the resin canals, and it is entirely (Fig. 8.17), and from some species considerable
lacking in Taxus. The tracheids are usually differ- quantities of commercially valuable resin can be
entiated in distinct annual rings, those formed collected. Pine resin, for example, is the source of
toward the end of a season’s growth being nar- turpentine and colophony, both widely used in
232 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.15. Pinus sylvestris. (a)

Radial longitudinal section of
secondary xylem at junction of early
and late wood. (b) Tangential
longitudinal section of a ray similar
to that shown in (a).

Figure 8.16. Pinus sylvestris. Photomicrograph of a several centimeters in length (Pinus, Fig. 8.13a) to
transverse section of a leaf, the flat adaxial side uppermost,
closely adpressed scales reaching only a few milli-
mid-way along its length. The epidermal cells are lignified and
meters (as in Cupressaceae, Fig. 8.13c). Araucaria
the stomata obscured, but the cells of the hypodermis are
visible and adjacent to them the resin canals. Two vascular
araucana is unusual in having broadly lanceolate
bundles, separated from the mesophyll by a common leaves 5 cm (1.4 in.) or more in length (Fig. 8.13b).
endodermis, lie at the center of the leaf. Thickened and In the Cupressaceae the plant frequently passes
lignified cells are found between these vascular bundles and through a juvenile phase in which it produces
below the phloem, but the cells elsewhere within the needle-like leaves. Cuttings or grafts of the juve-
endodermis are largely transfusion tissue. Scale bar 0.1mm. nile phase sometimes go on producing needle-like
leaves indefinitely, and these so-called Retinospora
the paint and varnish industry (although less so forms are common in gardens. The venation of
than formerly). The male bark beetle of Pinus pon- conifer leaves is never reticulate. There are either
derosa transforms a component of the resin into a number of parallel veins (as in some species of
the sex pheromone of the species. the Araucariaceae, Fig. 8.13b) or a single median
vein, often showing a double structure (as in Pinus,
l e av e s Fig. 8.16). In addition to Pinus, some other conifers
The leaves of conifers take a variety of forms (Fig. (e.g., Larix, Cedrus, Fig. 8.19) bear their leaves
8.13), but they are nearly always small and simple wholly or principally on short shoots (p. 231). The
in shape ranging from needle-like structures leaves of most conifers persist for several seasons;
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 233

Figure 8.18. Pinus sylvestris. Transverse section of young

root.

of ice crystals. The photosynthetic apparatus of

these conifers is also able to withstand long
periods of darkness without irreparable damage
and, when illuminated, to carry out photosynthe-
sis at unusually low temperatures. Additionally,
the pyramidal form and the diagravitropic
branches of many northern conifers are particu-
Figure 8.17. Pinus pinaster (maritime pine). The trunk of larly suitable for trapping the low-angle light
this tree (photographed in Portugal by G. E. Creber) has characteristic of high latitudes.
been tapped for resin. This species of pine is the principal
source of natural resin in Europe. Scale bar 5cm. ro o t s
The roots of conifers have a simple primary struc-
in only a few genera (e.g., Larix (larch)) are the ture, similar to that found in the ferns. The apical
leaves truly deciduous. In Taxodium and meristem is protected by a root cap, and root hairs
Metasequoia the leaves are confined to the ultimate are produced from a zone immediately behind it.
branchlets, and the branchlets (phyllomorphs) are Secondary vascular tissue begins to be formed at
shed as a whole at the end of the growing season. a very early stage, often before the primary tissues
Many features of anatomical and physiological are fully differentiated (Fig. 8.18). Resin canals are
interest are presented by conifer leaves. The cuti- abundant in the secondary xylem, rays and
cles, for example, are often furnished, especially cortex.
in the region of the stomata, with distinctive pat-
terns of tubercles and ridges. Palisade and spongy r e p ro d u c t i v e s t r u c t u r e s
mesophyll are commonly present, and in Pinus the As the vernacular name of the class implies, the
walls of the mesophyll cells have ridges projecting male and female reproductive organs of the coni-
into the cell (Fig. 8.16). A well-defined hypodermis, fers are commonly borne in cones (Figs. 8.19 and
the cells of which may be lignified, is present in 8.20). Most conifers are monoecious, but dicli-
many leaves. The vascular bundles are often sur- nous, the male and female cones being produced
rounded by transfusion tissue. Resin canals are in different regions. In Pinus, for example, the
frequent, and in some leaves (e.g., Thuja) a promi- female cones are produced near the apex of the
nent gland on the back of the leaf contains of fra- tree and occupy the positions of main lateral
grant oil. The leaves of conifers at high altitudes, buds, while the male cones are produced on the
and of arctic regions, are remarkably resistant to lower branches, usually in groups, each cone occu-
frost damage. Tissue water in twigs of species of pying the position of a short shoot. A few conifers
Pinus and Pseudotsuga, for example, can withstand (e.g., Taxus and Juniperus communis) are dioecious.
cooling to ⫺40 °C (⫺40 °F) without the formation The reproductive cones are usually compact, but
234 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.19. Larix decidua (larch).

Portion of a shoot showing the
short shoots and the female cone in
its second year. Note that the
female cone is negatively gravitropic
and that it terminates a lateral axis
having a position equivalent to that
of a short shoot. Scale bar 1cm.

Figure 8.20. Pinus sylvestris. (a)

Female cone in the early summer of
its first year. (b) Single scale from
cone in (a), viewed from above. (c)
Longitudinal section along line a–b.
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 235

Figure 8.21. Taxus baccata.

Longitudinal section of young ovule.
When fully mature, the nucellus
secretes a sugary fluid which
accumulates as a drop at the orifice
of the micropyle. This serves to trap
wind-borne pollen. Subsequent
resorption of the drop draws the
pollen down on to the surface of
the nucellus, where it germinates.

before being shed (Fig. 8.23). In

Pinus, the liberated pollen
grain contains two degenerat-
ing prothallial cells, a tube
cell and a generative cell (Fig.
8.26). The grains of the
Taxales, Taxodiaceae and
Cupressaceae, however, lack
in the Podocarpaceae the female cones are either prothallial cells and are uninucleate when shed,
lax or reduced, and in the Taxales the female whereas the mature grains of the Araucariaceae
reproductive region is not cone-like at all (Fig. contain up to 15 prothallial cells. The pollen
8.21). Nevertheless, the general affinities of the grains of all living conifers germinate distally,
Taxales are clearly with the conifers. that is, away from the center of the original
The male cones are fairly uniform in structure, tetrad.
although they range widely in size. Those of Taxus With regard to the morphology of the female
(Fig. 8.22b) and of the Podocarpaceae and reproductive regions, that of Taxus is considered
Cupressaceae are globose, hardly reaching 0.5 cm first as it facilitates an understanding of the more
(0.2 in.) in diameter, but those of other conifers are complex situation in Pinus and other conifers. In
commonly elongated (Fig. 8.22a), and in Araucaria Taxus the ovule terminates a short shoot bearing
they may exceed 20 cm (8 in.) in length and 3 cm three pairs of decussate bracts. The ovule itself is
(1.2 in.) in width. All, however, consist of a central upright and bilaterally symmetrical (Fig. 8.21).
axis bearing regularly arranged microsporangio- The single integument contains a sclerenchyma-
phores (Fig. 8.22a). These take the form of scales, tous layer, and two vascular bundles, diametri-
more or less peltate in shape, a variable number cally opposed, ascend in the fleshy portion
of pollen sacs being attached to the head and lying adjacent to the nucellus. A female gametophyte
parallel to the stalk. The pollen grains of many arises in the nucellus as in other gymnosperm
species are winged and readily identifiable. The ovules, and when mature it bears immersed
grains of Pinus (Fig. 8.23), for example, have two archegonia in its micropylar surface. The minute
asymmetrically placed air bladders (formed by short shoot terminating in the ovule is axillary to
local separation of the layers of the exine) another short shoot furnished with spirally
between which the pollen tube emerges. Other arranged scale leaves. This whole complex is itself
grains have characteristic ornamentation; those borne in the axil of a normal foliage leaf. Both
of Cryptomeria, for example, possess a peculiar cut- short shoots of the female reproductive system in
icular hook on one side. The pollen grains of some Taxus are highly condensed and can be seen only
members of the Cupressaceae are “dehiscent” or by a careful dissection.
“explosive”: following hydration the grains swell In the female cone of Pinus (Fig. 8.20) we
and the exine is shed. are again concerned with an axis bearing spirally
Pollen grains often begin to develop internally arranged scales in the axils of which are
236 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.22. (a) Pinus sylvestris. Longitudinal section of male

cone. Each microsporangiophore bears two pollen sacs. (b,c) Cupressaceae. In Araucaria (Fig. 8.24) the ovulifer-
Taxus baccata: (b) mature male cone, each ous scale produces and ultimately entirely sur-
microsporangiophore bearing 6–8 pollen sacs; (c) longitudinal
rounds a single inverted ovule. A specialized
section of microsporangiophore.
ovuliferous scale of this kind, also found in some
Podocarpaceae, is termed an epimatium. Despite
ovuliferous structures (Fig. 8.20b and c). In Pinus, these variations, ovules throughout the conifers
however, the ovuliferous structure is also scale- are regularly bilaterally symmetrical and the
like, and it is largely fused with and ultimately seeds are often winged.
projects beyond the bract scale in whose axil it The morphological and anatomical evidence,
arises (Fig. 8.20c). This, however, is not always the now supported by the paleobotanical (p. 229),
situation, even in the Pinaceae. In Abies (fir), for points to the ovuliferous scale being a highly
example, the bract and ovuliferous scales remain modified shoot. The vascular supply to the bract
separate, and in some species (e.g., A. venusta) the scale, for example, consists of vascular bundles of
bract scale projects far beyond the ovuliferous. In which the xylem is adaxial, the orientation
the Pinaceae the ovuliferous scale bears two normal for a leaf trace. The bundles passing to
inverted ovules near its base (Fig. 8.20b), but in the ovuliferous scale, however, are not only
other families evolution has clearly taken a differ- similar in position to those entering an axillary
ent course and the number of ovules and their shoot, but the xylem of each is also abaxial, an
orientation vary. In Cryptomeria, a forest tree of orientation often seen at the base of a shoot trace.
Japan, the ovules are upright and the ovuliferous The female region of Taxus can be readily related
scale develops after the ovules. In Libocedrus, a tree to the cone of Pinus if the primary axis with its
of western North America and the southern hemi- spirally arranged bracts is regarded as a cone,
sphere, the ovules arise from the axis, more or less only one scale of which is fertile. The secondary
in the axil of a bract, and again the development axis with its decussate bracts and terminal ovule
of the ovuliferous scale is subsequent. This situa- is then equivalent to an ovuliferous scale (Fig.
tion appears to be general in the family 8.25).
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 237

Figure 8.23. Pinus banksiana.

Median section of pollen grain
showing the first division of the
microspore nucleus and the nature
of the bladders.

Wind-tunnel experiments
have shown that air eddies
around the cone promote the
accumulation of wind-borne
grains between the scales.
Following pollination, rapid
growth of the scales causes
them to be tightly packed once again.
Pollination, which in temperate climates
occurs in the spring, involves in many species a
pollination drop mechanism of the kind found
in Taxus (Fig. 8.21). In Pinus sylvestris, however, the
drop is apparently formed after the pollen has
lodged in the micropylar region of the ovule.
Since the young female cone is more or less
upright, the ovule itself is inverted (Fig. 8.20b).
The entrapped grain, assisted by its air sacs,
Figure 8.24. Araucaria araucana. Longitudinal section of accordingly ascends through the drop and
young female scale. (After Hirmer. 1936. Bibliotheca Botanica reaches the surface of the nucellus. In Picea orien-
28.)
talis (oriental spruce) the female cones are
pendent and the ovules upright. Here grains
reaching the drop rapidly hydrate. The resultant
swelling of the grain forces the air out of the
sacs and the grain, when wholly waterlogged,
sinks to the nucellus. In some conifers (e.g., Larix)
the pollen is trapped by a stigmatic flap of the
integument covered with a sticky secretion
before reaching the micropylar canal. Some
members of the Podocarpaceae (a family largely
confined to the southern hemisphere) show
“pollen scavenging”: pollen alighting on wet-
table surfaces near the micropyle is “gathered
Figure 8.25. Diagrammatic representations of female up” by an emerging drop and drawn into the
reproductive regions of (a) Taxus and (b) Pinales, showing micropyle. In Abies, although the pollen is
how Taxus can be regarded as bearing a cone only one scale saccate, the ovule produces no pollination drop.
of which is fertile.
It is possible that pollination here is assisted by
rain drops carrying the floating pollen into the
p o l l i na t i o n a n d f e r t i l i z a t i o n interior of the cone. In families of conifers (e.g.,
The development of the female cone is so coordi- Cupressaceae) in which the ovules are regularly
nated with that of the male that at the time of upright and produce pollination drops the
release of the pollen the axis of the female cone pollen is non-saccate. In Araucaria the pollination
undergoes general elongation, thus opening the drop mechanism is entirely absent. The pollen
scales and allowing penetration of the pollen. germinates between the scales of the female
238 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.26. Pinus sp. Development of the pollen and ovule.

gonium, the spermatogenous cell, which has
Diagrammatic, not to scale.
moved into its tip, divides into two male (“sperm”)
cells of unequal size. The tube eventually pene-
cone forming a freely branching, multinucleate, trates the archegonium and the two sperm cells
mycelium-like weft, many of the branches reach- are liberated into the egg cytoplasm, taking with
ing, and some penetrating, the micropyle. them some male cytoplasm. The larger sperm
Pollination in Agathis (kauri pine) follows a nucleus passes into the egg nucleus, while the
similar course. smaller sperm cell, the sterile cell and the tube
In Pinus the germination and development of nucleus all degenerate. Several archegonia in one
the male gametophyte within the female cone are ovule may be penetrated by pollen tubes, and this
very slow and extend over a whole season (Fig. can result in the formation of several zygotes and
8.26), coinciding with meiosis in the nucellus and subsequent polyembryony.
the initiation of the female gametophyte. A Reproduction in Pinus is representative of that
pollen tube emerges from the grain in this first of the conifers generally. Amongst the principal
season’s growth (Fig. 8.26e and h), and the gener- variations is the “dehiscent” or “explosive” pollen
ative cell divides into a sterile (“stalk”) cell and a of the Cupressaceae (p. 235). In the Taxodiaceae
spermatogenous (“body”) cell. Little further the female gametophyte often produces many
occurs in the winter, but in the following spring archegonia, up to 60 being present in Sequoia.
development is resumed. After a period of free Pollen tubes may discharge gametes, which in this
nuclear division the female gametophyte family are similar in size, above adjacent archego-
becomes cellular (Fig. 8.26i) and 1–6 archegonia nia, each then being fertilized. In Taxus the male
are formed in its upper surface (Fig. 8.26j), each gametes are naked nuclei of equal size.
surrounded by conspicuous jacket cells. The In all conifers (including Taxus) the male
pollen tubes grow toward the archegonia, passage gametes lack any specialized means of locomo-
through the nucellus being facilitated by tion. The delivery of non-motile male gametes
enzymes secreted by the pollen tube which into the vicinity of the female gamete by means of
promote the separation of its cells and prevent a pollen tube is termed siphonogamy. It contrasts
actual penetration of intact tissue. When a tube sharply with zooidogamy (pp. 104, 244).
has come to within a short distance of an arche-
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 239

Figure 8.27. Pinus sp. Stages in the development of the

embryo. (After Bucholz, from Foster and Gifford. 1959.
suspensor, tetragonal in section, terminating
Comparative Morphology of Vascular Plants. Freeman, San below in four groups of embryonic initials, each
Francisco. © 1959.) capable of yielding an embryo. This so-called
“cleavage polyembryony” may be further compli-
cated by additional embryos budding off from the
e m b r yo g e n e s i s basal suspensor cells. Usually only one of these
The formation of the zygote is remarkable in that many potential embryos reaches maturity.
in Pinus, and in a number of other conifers in The development of the zygote in other coni-
which the male gamete retains its cytoplasm (e.g., fers differs only in detail from that seen in Pinus.
Larix), the original egg cytoplasm is largely In Sequoia, for example, there is no initial free
replaced by a new cytoplasm (“neocytoplasm”) nuclear division, and in the Podocarpaceae the
formed from that introduced by the male gamete. cells of the proembryo pass through a binucleate
During karyogamy the introduced cytoplasm sur- stage, a feature believed peculiar to this family. In
rounds the zygotic nucleus, and as the neocyto- other conifers polyembryony seems less common
plasm is formed it displaces much of the original than in Pinus. The embryos of many conifers have
egg cytoplasm. Correlated with this unusual cytol- several cotyledons; as many as 12 may be present
ogy is the discovery that in both Pinus and Larix, in Pinus.
although the inheritance of mitochondrial DNA is
maternal (despite the formation of the neocyto- formation and liberation of the
plasm), that of the chloroplast DNA is paternal. It seeds
has been observed in a number of conifers that The mature embryo lies in the remains of the
during maturation of the female gamete the pro- female gametophyte and nucellus, and is sur-
plastids of the egg cell become enveloped in mem- rounded by a hard seed coat formed from the
branous whorls (“inclusions”) which move to the integument. In some conifers (e.g., Sequoia, Pinus
periphery of the cell. The proplastids themselves sylvestris) this is expanded as a conspicuous wing
then appear to degenerate. It seems that their assisting the distribution of the seeds by wind (Fig.
DNA is also depolymerized. 8.28a). The female cone often becomes dry and
Germination of the zygote frequently involves woody during the formation of the seeds and
free nuclear division, but in Pinus this is not exten- sometimes does not open until a long period after
sive, only four nuclei being so formed (Fig. 8.27a). the seeds are mature. In P. sylvestris the cone opens
These move to the bottom of the archegonium and releases the seeds in the second year after pol-
and form a plate, walls then being laid down lination (the whole process of reproduction thus
between them. These cells divide transversely, the extends over three years), but in the “closed cone”
cells of each column behaving synchronously. pines of the Pacific coast of North America the
This leads (Fig. 8.27c and d) to the formation of a cones remain closed indefinitely and the seeds are
240 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.28. Sequoia gigantea

(Sequoiadendron giganteum). (a) Seed.
(b) Longitudinal section (at a–b) of
well-soaked seed. (c) Young
seedling.

Figure 8.29. Taxus baccata. Shoot

bearing seeds surrounded by mature
arils.

released by decay of the scales

or as a consequence of the sin-
geing of the cones by a forest
fire. The cones of some pines
are extraordinarily large;
those of the Californian P.
coulteri, for example, may
reach 40 cm (16 in.) in length
and 2 kg (4.4 lb) in weight. In
some Podocarpaceae and in
Juniperus the ovuliferous scales
become fleshy in fruit, the
“berries” of J. communis being used to flavor gin. In which the cotyledons are rapidly withdrawn (Fig.
some other podocarps and in Taxus the seed 8.28c). All conifer seedlings, so far as is known,
becomes surrounded by an aril which grows up become green in the dark, a remarkable property
from the base (Fig. 8.29). In Taxus this becomes that distinguishes them from the seedlings of
bright red and succulent. Although the seed is poi- most angiosperms.
sonous, the aril is wholesome and sought after by The seeds of Araucaria often germinate in the
birds, probably an aid to dispersal of the seeds. cone before it falls apart. In some species the hypo-
The non-winged seeds of some species of Pinus in cotyl swells to form a tuber, and the seedling is
both Europe and North America (“nut pines”) are capable of “resting” in this condition for several
edible and prized by both man and wildlife. months. It was this curious feature that facili-
tated the transmission of the first specimens of A.
g e r m i na t i o n araucana from Chile to Europe in the eighteenth
In most conifers, germination is initiated by the century.
root pole of the embryo elongating and breaking
through the seed coat. The vigorous primary root e vo l u t i o n w i t h i n t h e c o n i f e r s
soon anchors the seedling, and the elongating The fossil evidence points to the modern families
hypocotyl raises the remains of the seed, from of conifers having become recognizable by the
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 241

end of the Paleozoic or beginning of the Mesozoic Ginkgoopsida

(p. 5). The curious lax cone of many Podo- As with many Mesozoic gymnosperm groups, the
carpaceae, for example, is recognizable as far back Ginkgoopsida demonstrate what appears to be an
as the Lower Triassic, and the characteristic almost random assortment of characters viewed
female shoot of Taxus seems to have evolved by the as significant in taxonomy. In this case, a repro-
end of the same period. ductive syndrome comparable with that of the
The current geographical distribution of the cycads contrasts with a growth architecture and
conifers presents a number of features of evolu- anatomy resembling those of the Pinopsida.
tionary significance. Floristically, for example, the Situations such as this result from the relatively
conifers of the northern hemisphere are strik- common parallel development of particular char-
ingly different from those of the southern, and acters in different groups. The problem facing
some families (notably the Pinaceae in the north paleobotanists and systematists is then to identify
and the Araucariaceae in the south) hardly cross and distinguish those characters which have
the equator. Fossils of Quaternary and Tertiary multiple origins, and those which reveal phylog-
age give no indication that this is a recent segre- eny (Fig. 8.3). In many cases confusion is com-
gation, but they do reveal that the distribution of pounded by the scarcity of likely primitive
some families was formerly much more extensive. candidates which might indicate the antecedents
Sequoia, for example, now confined to the west of a group. The Ginkgoopsida, for example,
coast of North America, was once widespread in contain a single order Ginkgoales, of which there
the northern hemisphere. Climatic changes in are many fossil representatives but only one living
polar regions have also led to contractions in the species, Ginkgo biloba.
distribution of conifers. In the Tertiary period,
for example, Taxodium swamps occurred in The Ginkgoales
Spitzbergen, and in Eocene times Ellesmere The earliest plausible ginkgoalean fossil,
Island in the Canadian Arctic supported a forest Trichopitys, from the Lower Permian (Fig. 8.30) had
whose fossilized stumps consist of wood with a spirally arranged, highly dissected leaves. Some of
Metasequoia-like anatomy. Metasequoia, although the leaves bore shoots in their axes which in turn
found today only in Szechuan Province of China, supported a number of ovules, apparently with
had a wide distribution in North America in late bilateral symmetry. If Trichopitys was indeed gink-
Cretaceous and Miocene times. Another conifer goalean, then the emergence of the reproductive
whose distribution is currently contracting may shoot from a leaf axil suggests a relationship with
be the recently discovered Wollemia nobilis the Cordaitales within the Pinopsida, a relation-
(Araucariaceae), confined to a small population in ship supported by the pycnoxylic wood common
a remote part of the Central Tablelands of New to the two orders. However, a number of reproduc-
South Wales, Australia. It occurs mixed with tive features of living Ginkgo, such as a haustorial
angiospermous trees in warm temperate rain pollen tube and zooidogamy, are shared with the
forest. Surprisingly, all specimens of Wollemia so cycads (p. 244). It may be that the Ginkgoales, like
far examined appear to be genetically uniform. A the cycads, had an independent origin amongst
fossil pollen grain (Dilwynites), very similar both the pteridosperms of the Upper Carboniferous.
morphologically and ultrastructurally to that of The characteristic dichotomizing tendency in the
Wollemia, was abundant from the Upper ginkgoalean leaf may be foreshadowed in the
Cretaceous to the beginning of the Tertiary. The basal dichotomy which was a regular feature of
pollen data are consistent with a formerly wide- the medullosalean frond (p. 225).
spread distribution of “Wollemi pine” in the Leaf fossils of Mesozoic ginkgoaleans, abun-
southern hemisphere. Viewed globally, the fossil dant in some localities, have been assigned to the
evidence clearly points to the distribution of the modern genus on a basis of similarity. The genus
conifers having contracted substantially with the was widespread in the northern hemisphere in
rise of the angiospermous forests (p. 310). the Mesozoic and early Tertiary. Jurassic species,
such as Ginkgo huttoni and G. digitata (Fig. 8.31)
242 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.30. Trichopitys. (A) Part of

shoot with leaves and axillary shoots
with ovules. Scale bar 1cm. (B)
Detail of a fertile axillary shoot.
Scale bar 1mm. (C) Ovule. Scale bar
1cm. (From Stewart and Rothwell.
1993. Paleobotany and the Evolution of
Plants, 2nd edn. Cambridge
University Press, New York.)

resemble extreme forms of

leaf produced by G. biloba (par-
ticularly by juveniles). It is gen-
erally assumed that these
leaves were produced by trees
similar to the living species.
Reproductive organs are
uncommon and difficult to
associate with individual leaf
species.
Ginkgo biloba (maidenhair
tree), the sole living represen-
tative of the order Ginkgoales,
is a remarkable tree, with a striking pagoda-like tous rays. The tracheids have bordered pits,
arrangement of the main branches. It was usually in a single row, on their radial walls.
unknown to the Western world until the seven- The leaves of Ginkgo are fan-shaped, usually
teenth century. It was first discovered in Japan and with a distal notch (hence the specific name). Two
subsequently in China, but always in cultivation. vascular bundles ascend the petiole and dichoto-
Suggestions that wild stands of Ginkgo may occur mize in the lamina, with occasional anastomoses.
in remote parts of China, although not improb- Short resin ducts may lie between the veins. The
able, have never been confirmed. Ginkgo is now distal margin of the leaf is usually irregular, a
common in cultivation in all parts of the world. feature much more marked in juvenile leaves
Fully grown specimens of Ginkgo are tall, decid- where the distal part of the leaf may even be seg-
uous trees reaching a height of 30 m (98 ft) or mented.
more. The lateral branches bear both long and
short shoots (Fig. 8.32), and leaves occur on each. r e p ro d u c t i o n
Damage to a long shoot will cause one or more Ginkgo is dioecious, and sex determination
adjacent short shoots to behave as long shoots, appears to be chromosomal since the male karyo-
indicating that their manner of growth is not irre- type reveals a heteromorphic pair of chromo-
versible, and that the maintenance of the dwarf somes. The male reproductive structures (Fig.
condition probably depends upon the presence of 8.32) consist of small strobili, resembling catkins,
growth-regulating substances produced by the which arise in the axils of scale leaves of the short
meristem of the long shoot. Anatomically, the shoot. The axis of the strobilus bears a number of
apices of the long and short shoots are similar and microsporangiophores arranged in a loose and
show well-defined zonation, although no distinct irregular spiral. Each microsporangiophore is
tunica and corpus are present. Growth takes place slightly peltate and the sporangia, usually two,
from a superficial group of apical initial cells. A are attached beneath the head. The pollen grains,
large proportion of a mature stem consists of sec- which have a characteristic furrow in the wall,
ondary xylem, penetrated by narrow parenchyma- contain four nuclei when shed, two of the nuclei
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 243

Figure 8.31. Ginkgo huttoni (a) bore leaves with usually female gametophyte bounded by a conspicuous
three deep notches and many subsidiary shallow notches. G. membrane. The gametophyte is unique amongst
digitata (b) had leaves with few deep notches leading to a seed plants in containing chlorophyll. Sufficient
more rounded outline. Both of Jurassic age. Scale bars 1cm. light reaches the gametophyte to permit some
photosynthesis, supplementing the supply of
being associated with rudimentary prothallial photosynthates reaching the gametophyte from
cells, and the others identified as the generative the sporophyte. At maturity two archegonia arise
and tube nuclei respectively. The first prothallial at the micropylar end of the gametophyte.
cell soon degenerates. Meanwhile the nucellus above develops a pollen
The ovules are usually borne in pairs, two chamber.
sessile ovules being symmetrically attached at the Pollination is assisted by a “pollination drop”
end of a stalk-like sporangiophore. Not infre- at the micropyle, and the pollen chamber, having
quently, however, the sporangiophore branches received the pollen, then becomes closed above.
irregularly and bears more than two ovules. The The cavity of the nucellus progressively deepens,
sporangiophore itself arises, as in the male, in the carrying the pollen with it, until it reaches the
axil of a scale or a leaf on a short shoot. The ovules female gametophyte, the center of which is
(Fig. 8.33) are about 0.5 cm (0.2 in.) long and about extended upward to form a so-called “tentpole” (a
as broad, and are surrounded at the base by a feature seen also in many fossil seeds). The germi-
cushion-like swelling of the broad end of the spo- nating pollen forms a tube, but, as in Cycas (p. 251),
rangiophore. They possess a single integument this has a haustorial function. The tube penetrates
into which two (sometimes three) vascular the nucellus and there branches freely, growing
bundles, evenly spaced, ascend. The commonly through the air spaces at the interstices of the
bilateral symmetry is reflected in the micropyle cells. The proximal part of the grain forms a sac
which is slightly two-lipped at its tip. A megaspore hanging in the chamber above the archegonia. As
is formed within the nucellus and this yields a the archegonia mature the generative cell in the
244 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.32. Ginkgo biloba. Branch

of male tree, showing a long shoot
and a short shoot. The short shoot
is bearing microsporangiate strobili.
Drawn early in the growing season
before the leaves have reached
mature size.

Figure 8.33. Ginkgo biloba.

Longitudinal section of female
peduncle with young ovules.

male gametophyte divides,

yielding a spermatogenous
and a sterile cell, the latter
wrapped around the surviving
prothallial cell. The sperma-
togenous cell develops further
and produces two multiflagel-
late spermatozoids whose
major diameters are of the
order of 100 ␮m. These sper-
matozoids are released into
the fluid above the archegonia
and bring about fertilization.
Fertilization is thus clearly
zooidogamous.
In some locations the zygote may not be and resinous, and the inner hard. The formation
formed until after the ovule has been shed, but in of the seed is completed in one season.
others well-developed embryos have been found
at this time. Development of the zygote begins by Diversification of radiospermic
free nuclear division, leading to a proembryo con- gymnosperms
taining about 256 nuclei. Walls then differentiate
and a flask-shaped proembryo is formed, the lower Cycadopsida
part of which becomes the embryo proper. A The Cycadopsida in the broadest sense include all
clearly defined suspensor is thus absent. The those gymnosperms with radiospermic ovules
mature embryo has two cotyledons. Usually only which have their origin on a foliar structure. The
one of the paired ovules on the sporangiophore angiosperms can be regarded as merely specializa-
develops into a seed. In the mature seed (Fig. 8.34), tions of this situation, but are given a higher
which reaches a diameter of about 2 cm (0.75 in.), status in view of their predominance in modern
the outer layer of the integument becomes fleshy vegetation. Unlike the Pinopsida, in which the
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 245

Perhaps rashly, Beania has been associated in a

reconstruction with a relatively slender stem ter-
minating in a crown of simple leaves of a type
known as Nilssonia (Fig. 8.36b), but the leaves
borne by at least some species of Beania appear to
have been pinnate, like those of living cycads.
There was no dichotomy in the lower part of the
rachis, as in Medullosa (p. 225), although this
feature is retained by some Caytoniales (p. 254).
The cycads have some morphological resemblance
to the extinct Mesozoic gymnosperms assigned to
the Bennettitales and Pentoxylales, but they are
now seen to be distinct and to have retained many
features recognized as primitive amongst seed
Figure 8.34. Ginkgo biloba. Tip of short shoot bearing ripe
plants.
seeds. Although in Mesozoic times the cycads were
distributed as far north as Siberia and Greenland,
early orders are extinct, the most primitive they are today confined to tropical and subtropi-
Cycadopsida, the Cycadales, are still in existence, cal regions in both the Old and New Worlds. There
although much diminished in numbers. are nine genera in all, the commonest being
Zamia, Macrozamia, Cycas, Encephalartos, Dioon and
The Cycadales Ceratozomia, but only Cycas, extending eastward
The first cycads occur in the late Carboniferous, from Madagascar into Polynesia, has anything
and appear to be descended directly from pterido- approaching a wide distribution. Encephalartos
sperms, possibly the Medullosales (Fig. 8.3). They woodii of Africa is represented only by male plants,
share manoxylic wood, radiospermy, and frond- and is probably a natural hybrid.
like leaves with this group. Living cycads are
essentially pachycaulous in habit; extinct forms, stems
however, appear in some instances to have been The stems of the cycads are either short, stocky
leptocaulous and may have attained faster growth trunks (Fig. 8.37), often with a large portion below
rates. Early representatives such as Bjuvia (Fig. ground, or are much taller, some reaching heights
8.35) from the Upper Triassic of Sweden had entire of up to 15 m (50 ft). Below ground is a massive tap
leaves, in contrast to the ubiquitous pinnate root which bears, together with normal roots,
fronds of living cycads. Like those of Cycas, ovules others which are negatively gravitropic and which
were borne on the proximal part of a fertile leaf break up at the soil surface into coralloid masses.
(megasporophyll), the distal sterile portion being These contain endophytic fungi and blue-green
little developed. The robust trunk presumably algae (Cyanophyta, p. 27).
consisted principally of manoxylic wood, and Apart from stature, all cycads have a similar
owed much support to the leaf bases. Later cycads, growth form. The thick stem, usually
such as Beania gracilis from the Jurassic, appear to unbranched, bears an apical rosette of large
have produced axillary female cones. These can be pinnate leaves. The rate of growth is very slow and,
interpreted as determinate stems bearing highly although there are no recognizable annual rings
reduced fertile leaves. Each was terminally in the stem, the age of any specimen can be calcu-
peltate, and bore beneath two ovules, symmetri- lated approximately from the rate of leaf produc-
cally placed (Fig. 8.36a). A more condensed version tion and the number of leaf bases. A specimen of
of the cone of Beania is found in most genera of Dioon only 2 m (6.5 ft) high was estimated in this
living cycads, that of Zamia being closely similar. way to be about 1000 years old. Bowenia, confined
As in living Zamia, stomata were detected in the to North Queensland, is anomalous in possessing
epidermis of the nucellus of the seed of Beania. a tuberous rootstock bearing only one or two
246 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.35. Bjuvia simplex.

Reconstruction of plant with female
cone. (After Florin, from Arnold.
1947. An Introduction to Paleobotany.
McGraw-Hill, New York.)

Figure 8.36. (a) Beania gracilis.

Ovulate cone about 10cm (4 in.) in
length. (b) Possible reconstruction
of a Jurassic plant with relatively
slender axes terminating in a crown
of simple leaves, bearing lateral
Beania-like cones. Scale bar 2.5cm.
(From Stewart and Rothwell. 1993.
Paleobotany and the Evolution of
Plants, 2nd edn. Cambridge
University Press, New York.)
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 247

bases. The cycads generally thus provide typical

examples of manoxylic stems. Mucilage canals,
tannin cells, and cells containing crystals of
calcium oxalate occur in the pith and cortex of
mature stems.
Apart from the conspicuous foliage leaves (or
fronds), the stem also bears scale leaves, sequences
of each kind of leaf following a common phyllo-
tactic arrangement. The scale leaves cover the
apex and the upper part of the stem (Fig. 8.38),
often disintegrating to form a fibrous sheath
below. The foliage leaves in some species reach 1 m
(39 in.) or more in length. In Cycas and in most
other genera the vernation of the young leaves is
circinate (as in polypodioid ferns), but in a few the
vernation is similar to that seen in the fern
Botrychium (p. 180). In all cycads the leaves are pin-
nately branched, but are twice pinnate only in
Figure 8.37. Encephalartos hildebrandtii. Habit of plant Bowenia. In Cycas micholitzii, a distinctive species
bearing female cone. (After Eichler, from Eichler in Engler and from southeast China and north Vietnam, the
Prantl. 1889. Die Natürlichen Pflanzenfamilien, vol. II, 1.
primary pinnae are pedately branched into a
Engelmann, Leipzig.)
small number of pinnules. The vascular supply to
the leaf is seen in sections of the rachis as a horse-
leaves at a time. The leaves of cycads contain a shoe-shaped trace of individual bundles. The trace
variety of metabolic products, some poisonous has a complex origin in the stem. Some strands
and others of possible therapeutic value. arise opposite the insertion of the leaf and girdle
The stem grows from a massive apex in which the stem obliquely upward into the leaf base. In an
there is generalized meristematic activity, and individual bundle of the trace much of the metax-
considerable centrifugal expansion, as well as ylem is adaxial to the protoxylem, but character-
growth in length. Behind the apical initials a core istically a few tracheids, often separated by
of central tissue, which soon becomes distin- parenchyma, lie on the abaxial side adjacent to
guishable from the peripheral, differentiates into the phloem (“centrifugal xylem”).
the vascular tissue and pith. The peripheral zone The venation of the pinnae is various, but any
becomes cortex. The primary vascular tissue con- branching is dichotomous and open. In section
sists of a ring of bundles with endarch protoxy- small patches of transfusion tissue (anatomically
lem, and these surround an extensive pith. The intermediate between parenchyma and tracheids)
secondary xylem is traversed by wide parenchy- are often present on each side of the xylem. In
matous rays and the radial walls of its tracheids Cycas, where each pinna has only a midrib, a sheet
are furnished with several series of circular bor- of similar cells extends from the midrib to the
dered pits (except in Zamia and Stangeria where margin (“accessory transfusion tissue”).
the pits are of the narrower kind characteristic of The pinnae have a leathery texture. A conspic-
ferns). The first cambium is of limited activity, uous cuticle is usually present, and an epidermis
and it is followed by others which arise succes- (often accompanied by a hypodermis), palisade
sively outside the vascular cylinder. These cambia and mesophyll are well differentiated. The cell
are of diminishing activity, the last producing walls of the lower epidermis are straight or
merely a few concentric bundles lying out in the slightly sinuose, and the stomata, although
cortex. The stele is thus highly parenchymatous, usually sunken, are surrounded by a simple ring
and the main mechanical support of the stem of subsidiary cells (haplocheilic stomata; Fig. 8.44b).
comes from its armor of sclerenchymatous leaf These epidermal features, which remain clearly
248 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.38. Zamia sp. Young plant with female cone. The female cones vary in compactness and in
Although produced terminally, the female cone becomes the number of ovules borne on each megasporan-
pushed to one side by the sympodial growth and appears to giophore. At one extreme stands Cycas, in which
be lateral. Scale bar 5cm. (Photograph by Frank White.) the female cone consists of a loose aggregate of
megasporangiophores, the distal, sterile portions
evident in fossil material, are of great value in dis- of which are more extensive than in any other
tinguishing extinct Mesozoic forms from superfi- cycad. Several pairs of ovules are attached in the
cially similar contemporary plants (see Fig. 8.44). proximal region (Fig. 8.39b), the micropyles of the
ovules being directed obliquely outward. At the
r e p ro d u c t i v e s t r u c t u r e s other extreme are Zamia and Encephalartos, in
The mega- and microsporangiophores of the which small, peltate sporangiophores (Figs. 8.38
cycads are aggregated into separate strobili borne and 8.39a) are tightly packed in a distinct ovoid
on different plants. The female cone either termi- cone. Each sporangiophore bears two ovules, the
nates the main axis (in which case subsequent micropyles of which are directed toward the
growth is sympodial, Fig. 8.38) or it is lateral, center of the cone. Both the cones and ovules in
according to the genus. The situation in Cycas is the cycads generally are of extraordinary size. In
exceptional for here the main axis, having given Encephalartos female cones have been recorded
rise to a sequence of megasporangiophores, con- weighing as much as 45kg (90 lb), and in
tinues to be active and reverts to the production Macrozamia the ovules reach a length of 6 cm (2.4
of normal vegetative leaves. in.). The whole of the female reproductive system
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 249

Figure 8.39. (a) Encephalartos

hildebrandtii, megasporangiophore.
(b) Cycas revoluta,
megasporangiophore.

Figure 8.40. Cycas sp. (a) Male

cone. (b) Microsporangia, the scale
viewed from below.

erable variation in size. In

some species of Encephalartos
the male cones reach a length
of 50 cm (19 in.), but in Zamia
only 5 cm (2 in.). The microspo-
rangiophores are in the form
of scales, closely adpressed
during growth and when
mature covered on their lower
surfaces with several hundred
microsporangia (Fig. 8.40b).
The sporangia, about 1 mm
(0.04 in.) in length and structu-
rally resembling those of the
is thus on a much larger scale than in any other fern Angiopteris, are grouped in sori, each consist-
living plants. ing of 3–4 sporangia. Their origin is eusporangiate
The male cones of the cycads (Fig. 8.40a) are and their formation almost simultaneous. Each
also either terminal or lateral. Where terminal, sporangium produces some hundreds of spores.
subsequent growth is always (including that of In Encephalartos, temperatures some 15 oC above
Cycas) sympodial. Where lateral, growth is mono- the ambient have been recorded in male cones at
podial and the cones may be present in consider- the time of meiosis, a consequence of the intense
able numbers. In Macrozamia, for example, 20–40 respiratory activity throughout the cone at this
cones may be produced in rapid sequence around stage of development. The microspores of the
the lower part of the apex. There is much more cycads as shed (and partially dehydrated) are char-
uniformity in the structure of the male cones acteristically boat-shaped as a consequence of a
than in that of the female, although again consid- broad germination furrow (colpus) in the distal
250 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.41. Female reproductive system of cycads. (a)

Longitudinal section of young ovule. (b) Completion of
cells are comparatively small. A distinct and thick-
development of female gametophyte. (c) Archegonium ened boundary, known as a “megaspore mem-
containing newly formed egg. (After McLuckie and McKee. brane”, persists between the haploid gametophyte
1958. Australian and New Zealand Botany. Horwitz, Sydney.) and the diploid nucellus.
Although at first sight unfamiliar, the arche-
face. Since there is a single germination site, the gonia of the cycads can be seen from their devel-
grains are termed monocolpate. The exine on the opment to be quite similar to those of the lower
proximal face shows only an indistinct tetrad scar. archegoniate plants. A single initial cell divides
Germination of the microspores begins in the spo- into an outer primary neck cell (which subse-
rangium, and each spore when shed already con- quently gives rise to one tier of neck cells) and an
tains three cells, namely a single prothallial cell, inner central cell. The latter rapidly expands, and
a generative cell and a tube nucleus (Fig. 8.42a). then divides to form the egg and a small superfi-
cial ventral canal cell (Fig. 8.41c), which degener-
development of the gametophytes ates as the egg becomes ready for fertilization.
and fertilization Maturation of the egg involves considerable cyto-
The ovules of the cycads are distinctly radio- logical activity. The nucleus enlarges and becomes
spermic (although platyspermic forms may have weakly staining, and in Zamia small bodies, which
occurred in the Paleozoic), and the integument is appear in the light microscope as refractive drop-
differentiated into sclerenchymatous and fleshy lets, are seen to stream away from its surface into
layers. In Zamia stomata occur in the nucellar epi- the cytoplasm. This phenomenon, not yet investi-
dermis, a peculiar feature which may be present gated in depth, possibly resembles the events in
in other cycads. In the immature ovule the mega- the maturing egg of the fern Pteridium (p. 205). The
spore mother cell, which is deeply embedded in cycads possess the largest egg cells known
the nucellus, undergoes meiosis and gives rise to amongst land plants. The diameter may reach or
four megaspores in a linear or T-shaped tetrad. exceed 3 mm (0.13 in.) or more, and even that of
The three outer megaspores degenerate, but the the nucleus may be as much as 0.5 mm (0.02 in.).
inner (chalazal) megaspore remains viable and Pollination, which occurs during the closing
develops a layered wall of surprising complexity. stages of the growth of the female gametophyte, is
It germinates in situ and begins to form the female brought about by the microspores, which are dis-
gametophyte, the initial development of which tributed by wind, or in some species possibly by
consists of a sequence of free nuclear divisions insects. The existence of Microcycas calocoma, a
(Fig. 8.41a). The gametophyte enlarges with the Cuban species, for example, appears to be endan-
expanding ovule and eventually a vacuole forms gered because of the increasing rarity of its polli-
at its center. Wall formation then begins at the nator. The pollen grains are trapped in a sugary
periphery of the gametophyte and continues cen- “pollination drop” at the orifice of the micropyle.
tripetally. The archegonia (Fig. 8.41b) appear at This fluid, probably secreted by the cells at the tip
the micropylar end of the gametophyte where the of the nucellus, is subsequently withdrawn, carry-
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 251

Figure 8.42. Cycas sp.

Development of the male
gametophyte. (a) Vertical section of
microspore at liberation. (b)
Longitudinal section of pollen tube.
(c) Spermatozoid. ((a), (b) after
Swamy. 1948. American Journal of
Botany 35; (c) modified after Swamy.
1948. American Journal of Botany 35.)

may reach 300 mm in diame-

ter. Normally only two sper-
matozoids are produced, but
in Microcycas the sterile cell
continues to divide giving rise
ing the microspores with it. These now become to 10 or more spermatogenous cells, each of which
lodged in a shallow pollen chamber formed by yields a spermatozoid. Only the first-formed
autolysis at the tip of the nucellus (Fig. 8.40b). appear to be fully functional. This may represent
Here each grain puts out a tube from the distal the persistence of a primitive situation.
part of the grain (i.e., on the side away from the The spermatozoids are finally released from
center of the original tetrad) laterally into the the proximal part of the tube, close to the rup-
nucellus. This tube, which is of limited growth tured exine, directly into the fluid above the
(unlike the freely branching pollen tube of Ginkgo, archegonia. One or more eggs become fertilized.
p. 243), has a purely haustorial function, and only The penetrating spermatozoid sheds its cyto-
the tube nucleus enters it. In Zamia small out- plasm (including the flagella) in the cytoplasm of
growths of pollen tubes may invade and ulti- the egg, and its nucleus enters and disperses in
mately kill individual nucellar cells. the large female nucleus. As in Ginkgo, fertiliza-
In the presence of the pollen, and possibly tion is zooidogamous.
accelerated by enzymes secreted by it, the upper This account of the development of the male
part of the nucellus continues to break down, gametophyte and fertilization is based principally
until all that remains above the mature archego- on events in Macrozamia, Dioon, Zamia and Cycas.
nia is a small pool of fluid. The development of the The distal germination of the microspores in
male gametophyte meanwhile continues. The these genera coupled with the proximal release of
generative cell, the only cell to show further activ- the gametes suggest a position intermediate
ity, divides, giving rise to a spermatogenous (body) between the pre-pollen of most of the pterido-
cell and a sterile (stalk) cell which surrounds the sperms and the pollen of the conifers and angio-
prothallial cell (Fig. 8.42b). The proximal part of sperms. Many features of sexual reproduction in
the male gametophyte now extends and bends the cycads, however, need confirmation and re-
over the archegonia. The male gametophyte of the investigation by modern techniques. In
cycads thus shows bidirectional growth; initially Encephalartos, it has been observed that, in arche-
distally into the nucellus, and later proximally gonia receiving a single spermatozoid, the egg
down toward the female gametophyte. nucleus often fragments on penetration. This may
At the final stage of development the nucleus indicate the existence of a mechanism of sperm
of the body cell divides. Each daughter nucleus, selection in this genus, certain gametic genomes
together with some cytoplasm, then differen- being incompatible.
tiates into a coiled, multiflagellate spermatozoid
(Fig. 8.42c). The spermatozoids are constructed on e m b r yo g e n e s i s
the same principles as those of the lower arche- Although the development of the male and
goniates, but are much larger and in some cycads female gametophytes and the interval between
252 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

fats, prominent in the cells of the female gameto-

phyte (“pseudo-endosperm”). The mature embryo
has two or several cotyledons (depending upon
the species), directed away from the micropyle
and enclosing the stem apex (plumule). Although
a short axis is present below the cotyledons (hypo-
cotyl), a root is still lacking at this stage. The
whole is surrounded by the exhausted remains of
the female gametophyte and nucellus, and exter-
nally by the integument. Germination occurs as
soon as conditions are favorable and the seed has
imbibed sufficient water. The hypocotyl pushes its
way through the micropylar end of the seed and
then begins to develop a strong tap root which
persists throughout the life of the plant. The coty-
ledons remain partially enclosed in the seed, but
the plumule emerges and gives rise to scale and
mature leaves, the first of which have only a few
pinnae.

possible origin of the cycads

As described earlier (p. 245), the first cycads are
found in the late Paleozoic. In their radiospermic
seeds and in the complexity of their stelar struc-
Figure 8.43. Cycas sp. Embryo and suspensor. (After ture the cycads so closely resemble the later pter-
Swamy. 1948. American Journal of Botany 35.) idosperms that it seems beyond doubt that they
had their origin in some common stock. If so, both
pollination and fertilization is prolonged and leaves and sporangiophores would have been
may extend over months, the formation of the derived from lateral branch systems. If we
proembryo follows immediately after fertiliza- compare the megasporangiophore of Cycas revo-
tion. After a period of free nuclear division, in luta, with its pinnate distal portion, with that of
which as many as 256 (28) or even more nuclei may Zamia, where the sterile distal portion is lacking,
be formed, the proembryo becomes partly or we may see the process by which an ovuliferous
wholly cellular. Further growth takes place at the megaphyll lost its sterile region and became
chalazal end, and the embryogeny is evidently wholly reproductive. This specialization seems to
endoscopic. At the extreme base of the proembryo have been accomplished earlier in the male inflo-
is a group of small meristematic cells which rescences, since in all cycads, even those of
develop into the embryo proper, in some species Paleozoic age, the microsporangiophores have
protected on the outside by a layer of cap cells little sterile tissue.
which later degenerate. Above the embryonic cells
are a number of elongating cells which form a The Bennettitales
conspicuous suspensor. The mature suspensor The Bennettitales are wholly fossil, their record
may reach several centimeters in length, but the extending from the Triassic to the Cretaceous
resistance it meets in driving the young embryo periods. The frequency of their remains is such
into the nutritive tissue of the female gameto- that they were probably a more conspicuous
phyte causes it to be highly twisted and coiled (Fig. element of the Mesozoic flora than were the
8.43). Cycadales. In habit there was a general resem-
The embryo grows and differentiates at the blance to the cycads. Some Bennettitales were
expense of the food reserves, including starch and upright, sparingly branched plants, while others
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 253

Figure 8.44. Fossil cuticles of (a)

the bennettitalean type, and (b) the
cycadalean type. (From a
preparation by W. G. Chaloner.)

female (Fig. 8.45a). In

Cycadeoidea the ovules are
often well preserved, and this
genus provides the oldest
known example of mega-
spores produced in a linear
tetrad. The seeds were similar
in structure and symmetry to
those of cycads and pterido-
sperms, although the exis-
tence of a second integument
were squat, bearing a crown of leaves near the soil has been suspected in some forms. Unlike the
surface. pteridosperms, embryos are sometimes well pre-
The leaves of the Bennettitales were entire or served. A massive hypocotyl was directed toward
pinnate, and very similar to those of the cycads. the micropyle, resembling the situation in the
They were not in fact easily distinguishable from cycads.
these until it was discovered that the epidermal The general anatomical and reproductive fea-
features were quite different (Fig. 8.44). In the tures of the Bennettitales indicate that they also
Bennettitales the walls of the epidermal cells had their origin in some pteridospermous stock,
were highly sinuose, and the guard cells and sub- and in some respects the resemblance is closer
sidiary cells appear to have had their origin from than with the cycads. The microsporangiophores
the same mother cell, giving rise to so-called syn- (Fig. 8.45b), for example, can be readily envisaged
detocheilic stomata of characteristic form. as derived from condensed microsporangiate pter-
The stem structure, so far as it is known, was idosperm fronds. The derivation of the bisexual
similar to that of the cycads, except that girdling cones can be envisaged as following from the con-
leaf traces appear to have been absent. Secretory densation of an originally bisexual frond, or from
canals were, however, occasionally present, a an axillary shoot with upper female and lower
feature shared with cycads and some pterido- male branches. However derived, the bisexual
sperms. cones, often with subtending bracts, were
strongly suggestive of flowers.
r e p ro d u c t i o n The fossil record indicates that the
The cones of the Bennettitales appear to have been Bennettitales evolved in parallel with the cycads.
bisexual in most cases, the male portion being There is no obvious explanation of why they
below the female. Each consisted of an axis should have become extinct whereas the
bearing upright (outward-facing) ovules inter- Cycadales survived. It is noteworthy, however, that
spersed with sterile scales. The ovules were sur- the microsporangiophores of the bennettitalean
rounded by an elongated integument similar to cone commonly ascended close to the ovules, and
that found in the Gnetopsida (p. 259). The sub- self-pollination may have been the rule. This
tending whorl of microsporangiophores pro- would have limited genetic recombination and
duced either microsporangia (Fig. 8.45) or consequent adaptability.
complex synangia. The pollen grains were mono-
colpate, similar to those of the cycads and later The Caytoniales
pteridosperms. In most forms the inflorescence The Caytoniales, Triassic and Jurassic in age (and
was bisexual, the male portion being below the possibly extending into the Lower Cretaceous), are
254 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.45. Williamsoniella coronata (Bennettitales).

with blister-like swellings on the rachides and pin-
(a) Longitudinal section of fertile shoot. (b) Micro-
nules. The female branchlet was pinnately
sporangiophore showing partially enclosed microsporangia.
(After Harris, from Stewart.1983. Paleobotany and the
branched, each pinna terminating in a “cupulate
Evolution of Plants. Cambridge University Press, New York.) disk”, attached centrally to the pedicel. Attached
to the lower surface of the disk, and partly covered
by its recurved margins, were up to 20 ovules, a
a heterogeneous assemblage of Mesozoic seed curved “micropylar beak” sometimes being
plants with no living representatives. The evident (Fig. 8.47B and C). Their form gives rise to
Corystospermaceae, from the Triassic of South the name Peltaspermum for these female units. The
Africa, were characterized by ovules with a curved male branchlets were again similar to Crossotheca.
micropylar “beak”. In Umkomasia, which was prob- Although known principally from South Africa,
ably a woodland deciduous tree, the leaves were of early peltasperms have also been reported from
the doubly pinnate kind known as Dicroidium (a the late Permian of Western Europe.
form genus). The female reproductive structure The female reproductive branchlet of Caytonia
was a pinnate branchlet bearing several recurved (Caytoniaceae) was similar to that of the corysto-
cupules in opposite pairs (Fig. 8.46A). Each cupule sperms, being a pinnately branched axis (Fig.
contained a single ovule, the curved micropylar 8.48a), about 5 cm (2 in.) or more in length and pos-
beak (Fig. 8.46B) projecting conspicuously from sibly dorsiventral in symmetry. The pinnae, more
the cupule. The male branchlet (known as or less in opposite pairs, terminated in hollow
Pteruchus, Fig. 8.46C) was very similar to Crossotheca spherical bodies about 0.5 cm (0.2 in.) in diameter
(p. 224), but the pollen grains were bisaccate, with (Fig. 8.48b). A pore, communicating with the inter-
a well-defined colpus. Cupulate structures and ior of the sphere but concealed by a small flap of
fronds similar to those of the corystosperms are tissue, lay adjacent to the pedicel. Within the
known from the Lower Cretaceous of Argentina, sphere was a series of up to 32 upright ovules,
suggesting that the later members of the group appearing platyspermic, each about 2.5 mm
were coexistent with the earliest angiosperms (p. (0.1 in.) in length, and the nucellus furnished with
303). a short micropylar beak. The ovules were arranged
Also known from the South African beds are in lines, more or less opposite the basal pore.
the Peltaspermaceae. The leaves (Lepidopteris) of The pollen organs of Caytonia (Caytonanthus)
these plants were bipinnate fronds about 30 cm were branching clusters of elongate, pendent syn-
(12 in.) in length (Fig. 8.47A), characteristically angia, each with four loculi (Fig. 8.48c). The pollen
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 255

Figure 8.46. Triassic Corystospermaceae bore (A and B)

ovules (Umkomasia) in clusters on short branches. Pollen The Glossopteridales
organs (C) consisted of a disk-like lamina with numerous
The glossopterids were an enigmatic group of
pendent microsporangia. The leaves (D and E), referred to
the form genus Dicroidium, had a basal dichotomy. Scale bar
gymnosperms with complex and peculiar repro-
1 cm. (From Stewart and Rothwell. 1993. Paleobotany and the ductive structures. They were abundant in the
Evolution of Plants, 2nd edn. Cambridge University Press, New southern hemisphere in the Permian and
York.) Triassic. Glossopteris was a large, probably decidu-
ous, tree, the trunk reaching 40 cm (16 in.) in
diameter (Fig. 8.49a). The wood was pycnoxylic,
was bisaccate, and similar to that of the corysto- and the pitting araucarian. The roots (Vertebraria)
sperm Pteruchus, but lacked a well-defined colpus. had characteristic radiating wedges of secondary
The leaves of Caytonia (Sagenopteris), about 6 cm xylem, a feature thought possibly to indicate a
(2.5 in.) in length, were palmately compound, con- semi-aquatic habitat. The leaves were elongate-
sisting of usually four leaflets (Fig. 8.48d), each ovate with a distinct central midrib, probably
resembling in shape and reticulate venation the borne with a spiral phyllotaxy. The lateral veins
leaves of Glossopteris (p. 258). The stomata were commonly anastomosed, yielding a reticulate
haplocheilic. mesh (Fig. 8.49b).
Caytonia extends from the Upper Triassic to the The reproductive organs were peculiar and
Lower Cretaceous, and had a wide northern hemi- complex, and those of both sexes were associated
sphere distribution. Since pollen has been found with leaves. The ovules were borne on short stalks,
in the micropyles of the ovules of Caytonia, the believed to have been axial to the leaf in origin,
plant was evidently a gymnosperm. but becoming adnate to the midrib, either ontog-
The general features of the Caytoniales, partic- enetically or phylogenetically. In some forms the
ularly the tendency for the ovules to be borne stalk supported a small lamina, about 6 mm
within, or to be partially, or wholly, enclosed by a (0.2 in.) wide, bearing a cluster of ovules on the
cupule-like structure, indicate that their origin, adaxial side and partially enclosing them with its
like that of the Bennettitales, is likely to have inrolled margins (Fig. 8.50). In later forms the clus-
been in the late Paleozoic forms of the pterido- ters of ovules were open, each ovule almost
sperms. entirely surrounded by its own lamina. In general
256 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.47. Triassic Peltaspermaceae had large fern-like stalk arising from the midrib of a leaf, the posi-
leaves (A), referred to the form genus Lepidopteris. Ovules
tion corresponding to that bearing the ovules in
were pendent from the lower surface of disk-like cupules (B
and C). Scale bars: (A) 2cm; (B) 1cm; (C) 1mm. ((A) from
the female organ.
Hughes. 1994. The Enigma of Angiosperm Origins. Cambridge Glossopterids are known to have occurred at
University Press, Cambridge; (B), (C) from Stewart and high latitudes in the southern hemisphere
Rothwell. 1993. Paleobotany and the Evolution of Plants, 2nd (Gondwana). They may have formed a conspicuous
edn. Cambridge University Press, New York.) part of the polar ecosystem at the close of the
Paleozoic era, a system of which there are no
the ovules were platyspermic, barely reaching modern parallels. The particularly prominent and
2 mm (0.8 in.) in length. Bisaccate pollen grains wide growth rings of some glossopterid stems sug-
have been observed within the pollen chambers. gests that they may have grown continuously over
In the male organ (Eretmonia), solitary or the long days of the polar summer. They would
paired clusters of microsporangia were borne on a have escaped the diurnal cycle of lower latitudes,
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 257

Figure 8.48. Caytonia nathorsti. (a) Reconstruction of fertile

shoot. (b) Longitudinal section of cupule. (c) Caytonanthus cheilic stomata on the lower surface. Female
kochi, reconstruction. (d) Sagenopteris phillipsi. ((a), (b) after cones were borne on solitary or branched pedicels
Thomas, from Andrews. 1961. Studies in Paleobotany. Wiley, arising from the short shoots. They consisted of
New York; (c) after Harris, from Andrews. 1961. Studies in densely packed, spirally arranged ovules (Fig.
Paleobotany. Wiley, New York; (d) from Stewart and 8.51B), each with a bulky integument. The micro-
Rothwell. 1993. Paleobotany and the Evolution of Plants, 2nd pyle was placed centrally in each outer face. The
edn. Cambridge University Press, New York.)
male reproductive structure, borne terminally on
separate short shoots, consisted of a ring of
and the physiological limits which this imposes filiform axes, fused at the base and spirally
on the rate of wood production. branched above. The branches terminated in uni-
The reticulate venation in the leaves of the locular microsporangia. The pollen was monocol-
glossopterids, coupled with the carpel-like lamina pate and similar to that of cycads.
associated with the ovules in some forms, have led The Pentoxylales are very difficult to classify.
to their being considered as possible ancestors of Like the Ginkgoopsida, they seem to have been an
the flowering plants. There is, however, no clear entirely separate group of plants, presumably
evidence for such a relationship. The glossopter- originating from somewhere within the wide
ids were extinct by the end of the Triassic. range of Paleozoic pteridosperms. Cladistic analy-
ses, utilizing a multiplicity of characters, suggest
The Pentoxylales a relationship with the Bennettitales (Fig. 8.3).
The Pentoxylales, known only from the Jurassic, Another plant, well preserved but of at present
are poorly understood, but possibly of importance entirely obscure affinities, is Sanmiguelia from the
in relation to the origin of the angiosperms. The Upper Triassic of North America. Erect stems,
stems of Pentoxylon (Fig. 8.51A) commonly con- bearing apparently plicate leaves, rose from a
tained five distinct segments of vascular tissue, basal rhizome (Fig. 8.52A). The venation was retic-
consisting principally of pycnoxylic secondary ulate, and each leaf had a sheathing base which
xylem. The primary xylem was mesarch. The encircled the stem. Vessels occurred in the root.
plant, which was presumably a small tree or Male and female reproductive regions were separ-
shrub, produced long and short shoots in the ate, and appeared to terminate stems and lateral
manner of Ginkgo. Both bore entire ovate leaves branches. Male “cones” consisted of paired micro-
about 7 cm (3 in.) in length, and with syndeto- sporangia spirally arranged on a short axis.
258 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.49. Glossopteris.

Reconstruction of a specimen about
4m (14ft) in height. Scale bar in (b)
1cm. (Based on Gould and
Delevoryas, from Stewart and
Rothwell. 1993. Paleobotany and the
Evolution of Plants, 2nd edn.
Cambridge University Press, New
York.)

Figure 8.50. Glossopteris.

Diagrammatic representation of the
female reproductive region. The
leaf-like megasporangiophore was
borne in the axil of a foliage leaf.
(From information in Gould and
Delevoryas. 1977. Alcheringa 1, and
Taylor and Taylor. 1992. Proceedings
of the National Academy of Sciences
U.S.A. 89.)
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 259

Figure 8.51. Pentoxylon sahnii. (A) An axis about 1cm

(0.4in.) in diameter, bearing a short shoot, from the Indian However, although the Gnetopsida indicate how
Jurassic. (B) A short shoot with ovulate cones. (After Sahni, certain characteristics of angiosperms may have
from Stewart and Rothwell. 1993. Paleobotany and the arisen, they themselves appear to be as derived as
Evolution of Plants, 2nd edn. Cambridge University Press, New the angiosperms, and cannot be considered as
York.) having participated in angiosperm ancestry. The
Gnetopsida are united by the presence of vessels
Numerous such axes occurred in helical arrange- in their secondary xylem, and the tendency for
ment at the termination of a branch. The female the tip of the nucellus to be extended as a micro-
unit consisted of clusters of cupules subtended by pylar tube. In Gnetum and Welwitschia the female
bracts (Fig. 8.52B), arising either terminally or in gametophyte takes the form of an embryo sac.
the axils of leaves. Although the detail is not ade- Unfortunately the fossil record of the
quate to be certain, each cupule probably con- Gnetopsida is very fragmentary and does not
tained a pair of recurved ovules, each with two extend further back than the Cretaceous. Drewria
integuments. Despite its possessing a number of (Fig. 8.53) has features of leaf venation similar to
angiospermous features, Sanmiguelia is best those of the leaves of Welwitschia (p. 263), and
regarded as a specialized gymnosperm, some of similar dichasial reproductive structures. There is
the specializations (e.g., its carpel-like cupules) also a resemblance in this respect to the
being shared with angiosperms. Chloranthaceae, believed to be primitive dicotyle-
dons (Magnoliopsida, p. 303). Nevertheless,
Gnetopsida Welwitschia is such a bizarre plant that the signifi-
The class Gnetopsida consists of three extant cance of such resemblances is altogether doubt-
orders: Gnetales, Welwitschiales and Ephedrales. ful.
Each order is monogeneric and one
(Welwitschiales) monospecific. Not only are the The Gnetales
Gnetopsida very different from other gymno- The genus Gnetum is exclusively tropical, occur-
sperms, but the orders also differ markedly ring in Asia, Africa and South America. Many
amongst themselves. They have been extensively species are lianes, but others are small trees. The
studied by morphologists because of certain fea- leaves are well developed (Fig. 8.54), and possess
tures which make them appear intermediate broad, oval laminae with reticulate venation,
between gymnosperms and angiosperms. some of the veins ending blindly in areolae.
260 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.52. Sanmiguelia lewisii. (A) Male and (B) female sieve cells. The cortex adjacent to the phloem is
reproductive shoots. The larger leaves were 48–60cm
rich in fibers, occasionally used as cord. In some
(19–24in.) long and 28–31cm (11–12in.) broad. (From
species the stems contain laticifers, one of the
Cornet. 1986. Evolutionary Theory 7.)
very few instances of these tissue elements occur-
ring outside the flowering plants.
Vegetatively, therefore, Gnetum has very much the The placing of Gnetum in the gymnosperms is
appearance of an angiosperm. justified by the nature of its reproduction. Both
The stem of Gnetum usually has a small pith, male and female reproductive regions are strobili,
surrounded by a little primary xylem. Most of the usually terminating lateral axes, although some
xylem is secondary and is interspersed with broad species show cauliflory. In the male strobilus (Fig.
parenchymatous rays. In the climbing forms the 8.55a) the axis bears a succession of gallery-like
stem is eccentric, and successive cambia give rise sheaths, usually about eight in number, probably
to a polycyclic stelar structure, and asymmetry in formed from coalesced bracts. In the axil of each
any particular region depending upon its spatial sheath are whorls of male flowers, in some species
orientation. In general features, therefore, the surmounted by whorls of abortive ovules. The
stem is closer to that of the cycads and pterido- male flower (Fig. 8.55b) consists of a single micro-
sperms than to that of the conifers. A striking dif- sporangiophore, terminating in two microsporan-
ference, however, is the differentiation of gia, surrounded at its base by a delicate
authentic vessels in the secondary xylem. membranous sheath. The pollen grains are spher-
Another notable feature in Gnetum is the close ical, inaperturate or with widely dispersed pores.
association between parenchymatous cells, recall- They are trinucleate when shed, one nucleus prob-
ing the companion cells of angiosperms, and the ably being prothallial.
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 261

inverted flask (Fig. 8.56b), commonly called (by

analogy with the angiosperms) an embryo sac.
Much of the cytoplasm, in which the nuclei are
irregularly scattered, lies at the base of the sac, but
the remainder is distributed as a thick layer
around the periphery, a large vacuole occupying
the center. While the embryo sac is completing its
development, the pollen tubes, having penetrated
the nucellus, approach the sac. One of the nuclei
in the male gametophyte moves to the tip of the
tube and divides into two sperm nuclei.
Meanwhile one or more nuclei in the upper part
of the embryo sac in the region adjacent to the
closest pollen tube become conspicuously large.
The pollen tube, having by now made contact with
the sac, discharges the two sperm nuclei into it.
Microspectrofluorometry has shown that the
sperm nuclei at the time of discharge have already
replicated their DNA, so that they contain twice
the basic (2C) amount. The male nuclei immedi-
ately migrate to the nearby large nuclei of the sac,
Figure 8.53. Drewria potomacensis. Reconstruction of a which can thus be identified as egg nuclei. There
vegetative and (above) a terminally fertile shoot. Scale bar
is no clear segregation of egg cells or nuclei within
1 cm. (After Crane and Upchurch, from Stewart and
the sac, and both sperm nuclei from the pollen
Rothwell. 1993. Paleobotany and the Evolution of Plants, 2nd
edn. Cambridge University Press, New York.) tube may enter into fusions.
The entry of the male nuclei stimulates
general division of the somatic nuclei within the
In the female strobilus (Fig. 8.55c) each sheath embryo sac. The contents of the sac become cellu-
encloses a whorl of female flowers. Each flower lar, the cells often containing several nuclei,
consists of a single, radially symmetrical ovule which subsequently fuse. The male nucleus and
(Fig. 8.56a) surrounded by three integuments, the egg nucleus meanwhile coalesce and form a
outer of which is possibly homologous with the zygote lying within what can now be regarded as
basal sheath of the male flower. The inner integu- equivalent to a cellular endosperm. Development
ment is extended into a cutinized micropyle, and of the zygote proceeds at once, presumably
the nucellus beneath becomes transformed into a because the egg nucleus, like the sperm nucleus,
pollen chamber. One or more of the tetrad of meg- has already replicated its DNA. Karyogamy would
aspores formed in the nucellus enters into the for- then result in a zygotic nucleus with the pre-
mation of the acellular female gametophyte. mitotic 4C amount necessary for the maintenance
Pollination is by wind, and also by insects, of the diploid condition (cf. Pteridium, p. 207).
attracted to the male flowers by the sugary pollina- Early development does not involve any free
tion drops of the adjacent abortive ovules, and nuclear division. A complicated suspensor, pos-
subsequently transferring the pollen to functional sibly partly haustorial in function, is formed
female strobili. The entry of the pollen into the before the embryo proper. Although, since more
micropyles of functional ovules initiates renewed than one egg nucleus may be present in the
growth of the ovule. The germinating grains, embryo sac and several male nuclei may be dis-
trapped by the proliferation of the cells lining the charged into it, there is potential polyembryony,
micropyle, send pollen tubes into the nucellus. only one embryo usually comes to maturity. The
Meanwhile the female gametophyte completes its embryo has two cotyledons.
development. At maturity it is shaped like an Although the reproductive apparatus is quite
262 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.54. Gnetum gnemon.

Portion of a shoot bearing female
strobili. Scale bar 5cm. (After
Madhulata, from Maheshwari and
Vasil. 1961. Gnetum. CSIR, Delhi.)

Figure 8.55. Gnetum gnemon. (a) Young microsporangiate

strobilus with whorls of abortive ovules. (b) Dehiscent The Welwitschiales
microsporangia. (c) Megasporangiate strobilus. (From In respect of habit Welwitschia (Fig. 8.57) is one of
Maheshwari and Vasil. 1961. Gnetum. CSIR, Delhi.) the most peculiar plants in existence. The genus is
monotypic, and the single species is confined to
desert regions of southwest Africa. The stem is
different, the seed of Gnetum recalls that of some short and upright, and mostly below soil level. At
Bennettitales. When ripe, the outer integuments the upper end it bears two strap-shaped leaves
of the Gnetum seed become fleshy, and in some with indefinite basal growth. Developmentally
species are edible. Gnetum gnemon is functionally these are the first pair of leaves after the cotyle-
dioecious, male and female strobili being formed dons, and growth soon becomes confined to them.
on separate plants, but the situation in other A further pair of decussate leaf primordia is
species is not clear. formed in the young plant, but these differentiate
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 263

Figure 8.56. Gnetum ula. (a) Longitudinal section of very

young ovule. (b) Longitudinal section of mature female
gametophyte (embryo sac) showing entry of pollen tube.
(After Vasil, from Maheshwari and Vasil. 1961. Gnetum. CSIR,
Delhi.)

Figure 8.57. Welwitschia mirabilis. Habit of the male plant.

(After Hooker. 1863. Transactions of the Linnean Society, London
24.)
264 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.58. Welwitschia. (a) The

male flower, enclosed by two pairs
of decussate bracts. (b) The
stamens, the filaments fused below
into a membranous tube, surround
a sterile ovule. Scale bars 1mm.

into horn-like protuberances.

Below, the stem passes into a
long tap root which gives rise
to an extensive root system.
The stem contains much sec-
ondary tissue, and it shows
anatomical peculiarities simi-
lar to those found in Gnetum and Ephedra. upper part of the embryo sac give rise to tubular
Welwitschia is dioecious, the cone-like repro- processes. These grow up toward the descending
ductive structures terminating small dichasial pollen tubes and potential egg nuclei move to
branch systems arising in the axils of the leaves their tips. When a pollen tube and process make
(Fig. 8.57). The cones consist of a series of scales, contact the separating walls dissolve and the
arranged in decussate pairs, in the axils of which sperm and egg nuclei fuse. The zygote then
are the individual flowers. The male units consist becomes ensheathed in cytoplasm and a cell
of a short axis bearing, first, two decussate pairs of membrane forms. There is no free nuclear divi-
small scales, and then a ring of trilocular synan- sion in the development of the zygote. A suspen-
gia. The filaments supporting the synangia are sor is formed and below it the embryo proper.
fused together at the base into a membranous cyl- Only one zygote yields a mature embryo. There
inder (Fig. 8.58). In the center of the unit, and ter- are two cotyledons. In fruit the outer integument
minating its short axis, is an abortive ovule. The of the seed persists as a broad wing which assists
pollen grains are binucleate when shed, but aerial dispersal.
neither nucleus can be regarded as belonging to a
prothallial cell. The Ephedrales
The female unit consists solely of an ovule The genus Ephedra is widely but discontinuously
with two integuments, terminating an axis with distributed. Some 35 species occur in the
occasionally two minute lateral outgrowths. The Mediterranean region, Asia and the Americas.
outer integument, which is broadly winged tan- They are typical “switch plants”, consisting of
gentially to the cone and is traversed by several densely branched axes, the younger of which are
vascular bundles, may be homologous with the green and photosynthetic (Fig. 8.59). The leaves
upper pair of bracteoles of the male flower. The consist of whorls of small scales which soon
membranous inner integument is extended at its become scarious. Many species grow in extremely
apex into a cutinized micropylar tube. The basic arid situations, such as sand dunes and scree
symmetry of the ovule seems to be radial rather slopes, and these not unexpectedly have an exten-
than bilateral. sive root system. The young twigs of some species
Pollination and the initiation of the embryo have medicinal uses, and the genus is the source
sac take place much as in Gnetum, but in the later of the alkaloid ephedrine.
stages, especially at the time of pollination, there The stem of Ephedra grows from a group of
are features peculiar to Welwitschia. After the meristematic cells, and a distinct tunica and
initial free nuclear division in the sac, walls are corpus are recognizable in the apex. The primary
laid down, many of the cells so formed being vascular system consists of a number of bundles
multinucleate. As the pollen tubes penetrate the symmetrically placed around a central pith (Fig.
nucellus, some of the multinucleate cells in the 8.60), the bundles being linked at the nodes by a
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 265

transverse vascular ring, as in Equisetum. The

primary xylem becomes surrounded by secon-
dary, traversed by broad parenchymatous rays.
The tracheids have bordered pits on their radial
walls, well-developed tori also being present.
Many of the tracheids are arranged in columns,
and the end walls are so extensively perforated
that they can be legitimately regarded as vessel
segments with foraminate perforation plates. The
phloem consists of sieve cells and parenchyma,
the sieve cells, like those of the conifers, having
highly inclined end walls.
Ephedra is dioecious. The male reproductive
regions are cone-like terminations of short shoots
which arise in the axils of the scale leaves. The
short shoot bears a number of bracts in decussate
pairs, and in the axil of each bract is a male unit
(Fig. 8.61). This consists of a single microsporan-
giophore, enclosed in the basal region by two
medianly placed bracteoles, and bearing at its
summit 2–8 microsporangia. The pollen grains
Figure 8.59. Ephedra sp. Portion of shoot system showing are ellipsoidal and furnished with prominent lon-
the articulated stem, reduced leaves, and female reproductive gitudinal ridges. Nuclear divisions occur immedi-
structures. ately after the formation of the grains and when
mature they contain four or five nuclei. The first
two daughter nuclei, which do not again divide,
are regarded as prothallial.
The female reproductive organ is similar in
structure to the male, but only the uppermost

Figure 8.60. Ephedra sp.

Transverse section of young stem.
266 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Figure 8.61. Ephedra altissima.

Microsporangiate shoot.

pair of bracts is fertile. Each

subtends an upright ovule
which is surrounded by a
sheath, sometimes two-lipped
above and probably homolo-
gous with the two bracteoles
of the male flower.
Hermaphrodite flowers are
occasionally found. The radi-
ally symmetrical ovule (Fig.
8.62) is bounded by a papery
integument, the apex of
which is prolonged into a
micropylar tube, highly cutinized at maturity. a period of free nuclear division before becoming
Megasporogenesis is initiated in the nucellus and cellular. Two, rarely more, archegonia are differ-
in the usual way only one megaspore of the tetrad entiated at the micropylar end, and they are
persists. The female gametophyte passes through unusual in being quite deeply sunken into the
somatic tissue of the gametophyte. Although the
cytology within the archegonium is normal, fol-
lowing division of the central cell nucleus there is
no cytokinesis, and the ventral canal nucleus
remains in the upper part of the now binucleate
cell. As the archegonia mature, the upper part of
the nucellus breaks down to form a pollen
chamber, and complex cytological phenomena,
amongst them the amoeboid migration of nuclei
and endomitosis, occur in the upper cells of the
gametophyte. A prominent “pollination drop”
forms at the orifice of the micropyle (Fig. 8.63).
The pollen is distributed by wind and possibly
also by insects attracted by the sugary pollination
drop produced by non-fertile ovules associated
with the male flowers of some species.
Germination of the pollen occurs directly on the
surface of the female gametophyte and a pollen
tube pushes its way into an archegonium. Two
sperm nuclei, produced by division of the sperma-
togenous cell, enter the egg cell. One fuses with
the egg nucleus and the other, in some species at
least, regularly fuses with the ventral canal
nucleus (a form of double fertilization). Both
fusion products undergo mitoses and eight pro-
Figure 8.62. Ephedra sp. Longitudinal section of ovule with
embryos may result. There is thus potential poly-
archegonia. (From a photograph by W. R. Ivimey-Cook, in
embryony, but only one embryo normally reaches
McLean and Ivimey-Cook. 1951. Textbook of Theoretical Botany.
Longman, London.)
maturity. A suspensor, of complex and compound
origin, drives the surviving embryo into the
 SPERMATOPHYTINA (SEED PLANTS): GYMNOSPERMS 267

Figure 8.63. Ephedra. Pollination

drop secreted from the tip of the
slender micropylar tube of a mature
ovule. Scale bar 1mm. (Photograph
by W. E. Friedman, reproduced by
permission of the American
Botanical Society.)

central region of the female gametophyte, rich in In many species of Ephedra the bracts below the
food reserves. The mature embryo has two cotyle- ovules become hard and wing-like in fruit, but in
dons and lies surrounded by the membranous the alpine E. helvetica they become fleshy and
remains of the ovular tissues and the hardened brightly pigmented.
integument. Reproduction in Ephedra is more
rapid than in the conifers; the interval between Gymnospermy as an evolutionary grade
pollination and fertilization may amount to no The diversity of the gymnosperms taken as a
more than 24 hours in Ephedra (cf. Pinus, p. 238). whole, in both vegetative and reproductive fea-
The “double fertilization” in Ephedra has been tures, indicates that gymnospermy must be
held to be relevant to the origin of the formation regarded as a grade of evolutionary advance, prob-
of endosperm in flowering plants (p. 298). ably first attained in the second half of the
268 THE SUBKINGDOM EMBRYOPHYTA (CONT.): DIVISION TRACHEOPHYTA, PART 3

Devonian period. The seed habit may of course the vessels of the Gnetopsida also foreshadow
have arisen independently more than once in those of the angiosperms. Further, studies of the
groups of plants at the progymnospermous level nucleotide sequences of the nucleic acids show
of evolution. This would be in line with the over- that those of the Gnetopsida more closely resem-
lapping of the progymnosperms and gymno- ble those of the angiosperms than any other seed
sperms in geological time, and the diversity plants. This agrees well with those cladistic anal-
present in both. Within the gymnosperms, for yses of seed plants which, utilizing morphologi-
example, the affinities of the cycads appear to be cal characters, can include fossils. However, recent
pteridospermous, those of Ginkgo cordaitalean. and more penetrating comparative analyses of the
Here then are two groups of plants whose evolu- nuclear, mitochondrial and chloroplast genomes
tion has probably been independent for many mil- of a range of representative plants have indicated
lions of years, but which are at the same level of that the affinities of the Gnetopsida lie within
advancement in respect of the reproductive the conifers, the Pinopsida and the Gnetopsida
process. A number of features in these primitive forming sister groups. The angiosperm-like fea-
seed plants may have evolved in parallel. tures of the Gnetopsida may thus have arisen
Siphonogamy, for example, may have arisen inde- independently. The origin of the angiosperms
pendently in the Pinopsida and the Gnetopsida. may even have preceded the emergence of the
Similarly, the symmetry of the ovule, although it Gnetopsida, lying in a more ancient stock of
is useful to distinguish between radiospermy and seed plants, possibly identical with that which
platyspermy in the early seeds, may also have been gave rise to the Bennettitales and Pentoxylales
a feature which responded independently to (although such a remote origin would be difficult
reproductive specialization in the evolving line- to reconcile with comparatively late appearance
ages. The ovules of Caytonia (p. 254), for example, of fossil angiosperm pollen (see p. 303)). Further
appear to be platyspermic, although the affinities discussion of the implications of the recent unex-
of the plant seem undoubtedly to be with the later pected molecular discoveries will be found in
radiospermic pteridosperms. The Proceedings of the National Academy of Sciences
The highest grade of gymnospermy is clearly U. S. A., volume 97, pp. 4086-4097 (2000). Taking the
shown by the Gnetopsida. The peculiarities of the wider view, the relationship between the gymno-
female gametophyte in Gnetum and Welwitschia sperms and the angiosperms is analogous to that
indicate the kind of developments which, in between the progymnosperms and the gymno-
some early transitional forms, may have led to sperms, the latter in each case being a special-
the angiospermous embryo sac. Although there ized subset of the former.
are differences in the manner of their formation,