THE STRUCTURE OF THE CONE IN

THE CONIFERAE
R. B. T H O M S O N
University of Toronto
There is at present much difference of opinion on the structure
and organisation of male and female cones in the Coniferae. The
writer has come to the conclusion that the differences have arisen
because the various bases upon which a solution has been sought
have not been broad enough, and that one is available if due con-
sideration is given to certain deductions from Hofmeister's (1849-
S1) classic comparative researches. In these, Hofmeister proved
the relationship of the seed habit of higher plants to the free-
sporing habit of vascular cryptogams by his interpretation of the
embryo sac of the Coniferae "als eine Spore welche yon ihrem
Sporangium umschlossen bleibt" (1851, 151), thus demonstrating
that both male and female cones were ancestrally free-sporing, and
premising homology between them at least in the fundamental
features of their organisation. There is certainly no evidence in
either homosporous or heterosporous vascular cryptogams, fossil
or living, that would lead one to suspect any fundamental differ-
ence in their male and female sporophylls; and, as a matter of fact,
homology between male and female sporophylls has long been
recognised in the most primitive of living seed plants, the
Cycadaceae.
Granting such homology in the ancestral conifer:s, this feature
should be given basic consideration in the interpretation of male
and female cones of their descendants, the living conifers of today.
This is not a new idea but, though subsequently overlooked, was
suggested over a hundred years ago by the distinguished exponent
of gymnospermy, Robert Brown. Acceptance of this idea makes
two other points clear: first, that the evidence of homology should
be most apparent in the most primitive conifers; second, that the
male cone having retained the free-sporing habit and being there-
fore more primitive than the female should show the fundamental
structural features of cone organisation more simply and more
clearly than the female.
In the light of these deductions from Hofmeister's work, the
73
74 THE BOTANICAL REVIEW

necessity of a thorough knowledge of the male cone as a basis for

interpretation of the female becomes evident, as also the necessity
of an acceptable explanation of the greater specialisation of the
female cone. On the latter point the evolution of sexual differen-
tiation in the gametophyte sheds significant light. Here the course
of evolutionary sequence indicates that there has been progressive
sexual differentiation beginning with the gametes and their differ-
entiation, and extending outward from them to the gametangia
and prothallia, as indicated by the successive acquirement of hetero-
gametangy and heterothally, whether the spores are exosporal or
endosporal in their prothallial development. On acquiring the seed
habit the female spore was retained within its sporangium and de-
rived all its nutrition from the surrounding tissue for the whole of
its endosporal prothallial development from the uninucleate stage
onward, including fertilisation and embryo development. We have
thus in the female cone an accentuated influence spreading from
the female spore and prothallium to the sporangium and then to
the structure on which it is borne, the sporophyll. With regard to
the second point, the relative primitiveness of the male cone com-
pared with the female, there are many difficulties. These are asso-
ciated with the fact that three different types of stamen, the Ta~us,
Pinus and .4raucaria types, are regarded as primitive by different
botanists.
Under the circumstances it was necessary to investigate the cone
and stamen of the whole conifer series anew, and since the Taxineae
presented the most difficult problems these were studied in most
detail. The results may be summarised as follows: (1) that the
stamen of Taxus is not primitively peltate and radially symmetrical
but that this appearance is due to the fusion of dorsiventral sporo-
phylls, usually of two but sometimes of three; (2) that similar
fusion occurs at the apex of the cone in every family of the conifers
but rarely at other parts except in the Taxineae; and (3) that in
,4ustrotaxus there is an additional fusion, that of the cone to the
subtending bract.
In general it may be said that wherever fusion of sporophylls
occurs it is either lateral or back-to-back depending on whether the
sporophylls are spirally arranged or in opposite series. Since
fusion usually occurs at the apex of small cones where the axis
contracts and there is aggregation of the sporophylls, it is consid-
 CONE STRUCTURE I N THE CONIFERAE 75

ered that these are predisposing factors. In Taxus the aggregation

is extreme, the stamens being massed in a small head at the apex of
the cone axis, their pollen sacs fused into a synangium. Another
feature of the apical sporophylls in many forms is elimination of
the lamina. This condition is characteristic of Taxus and results
in projection of the pollen sacs beyond the stalk to which they are
laterally attached. In other small cones the projection is often
quite marked, particularly where bud scales replace the lamina in
protection of the cone. In many cases complete or partial reduc-
tion of the lamina (the latter being characteristic of the apical re-
gion of all conifers) is accompanied by decrease in the number of
pollen sacs borne by these terminal sporophylls when compared
with the number on the lower sporophylls of the same cone, e.g.,
from four to one in Tetraclinis and from three to one in ]uniperus
and Thu]a. In no case is this reduction of sporangia accompanied
by increase in the number of resin cysts, as required by the 'sterili-
sation' theory of Coulter and Land (1905), but more often by
their reduction or elimination. In fact, reduction of the one is
generally correlated with reduction of the other, this being particu-
larly evident when the variation is great, as in the Araucarineae.
Thus this theory upon which the suggested derivation of the dorsi-
ventral stamen from the Taxus type depends, lacks confirmation of
its basal postulate---increase of resin cysts where there is reduction
of sporangia.
Austrotaxus affords further evidence that fusion plays an impor-
tant r61e in the organisation of the male cone. Here the cone is
fused throughout its entire length with the subtending bract, and
bears normally five sporophylls on its free surface, two of which
are located laterally at the base of the cone, have a much reduced
lamina and bear two sporangia each, while the three distal sporo-
phylls have no lamina and bear one projecting sporangium each. The
only fused sporophylls are the two most distal. The related genus
Cephalotaxus shows partial fusion of the cone to the bract. That
this represents a more primitive condition is indicated by other
features of its cone organisation (more sporophylls to a cone, less
reduction of the lamina, more sporangia to a sporophyU, less fusion
of terminal sporophylls). Though it is recognised that fusion of
floral parts in angiosperms is indicative of specialisation it is con-
ceivable that this might not be so in conifers. Interpretation in the
76 THE BOTANICAL REVIEW

reverse way, however, would involve the origin of the dorsiventral

stamen from the Taxus type. That it has not originated by 'sterili-
sation' of sporangia has already been shown, and its derivation by
splitting would imply an interpretation of the concentric vascular
bundle of the Taxus stamen, which would be difficult to accept since
the occurrence of this most primitive type of bundle if not the re-
sult of fusion of dorsiventral bundles would imply that the stamen
of Taxus is more primitive than that of the cycads or Ginkgo where
the vascular bundles of the sporophyUs are normally collateral and
dorsiventral.
The preceding considerations have led to the conclusion that the
dorsiventral type of male sporophyll, which characterises the great
bulk of the conifers, is the primitive and basic conifer type, reduc-
tion and fusion indicating the lines along which specialisation has
taken place. Which of the two dorsiventral types, that of Pinus
or that of Araucaria, is the more primitive will be more advan-
tageously discussed after consideration of current theories of cone
structure in connection with which certain evidence arises which
has a bearing on the question. These theories are of three types:
one, based on homology between radially symmetrical male and
female sporophylls; another, the ligular, in which homology of
dorsiventral sporophylls is involved; and a third, the brachyblast,
which regards the male and female cones as differing in organi-
sation.
The theories based on radial symmetry have been strongly sup-
ported by various botanists (~elakovsk)7, 1897; Doyle and O'Leary,
1934; and Hirmer, 1936). One of the main objects of these theo-
ries has been to provide an acceptable explanation of the location
of male and female sporangia on opposite sides of homologous
sporophylls, a point, however, which is capable of an equally simple
explanation when the location of the male and female sporangia in
the cycads is taken into account. In support of their basic require-
ment, radial symmetry, these theories cite the Taxus type of stamen
as the most primitive in living conifers. In view of the conclusion
arrived at in the present study that the Taxus type of stamen re-
suits from fusion of primitive dorsiventral sporophylls, it is clear
that these theories must depend on other evidence for their substan-
tiation. Such other evidence as has been presented, however, is un-
convincing, dealing as it does with external morphological features
 CONE STRUCTURE I N THE CONIFERAE 77

of abnormalities in living conifers and with the questionable pres-

ence of radial symmetry in the postulated ancestral forms.
The ligular theory, on the other hand, though it implies homol-
ogy between the sporophylls of male and female cones, does not
attempt to explain the reversed location of male and female spo-
rangia. It also ignores certain other implications of homology. For
example, it fails to account for the absence of a lignle in the male
cone where homology would suggest its presence. Here, if the
primitiveness of the free-sporing habit is taken into account, the
ligule should be more evident than in the female. Again, on the
basis of the ligular theory the conifers are usually regarded as de-
rived from such ligulate lycopsid forms as Selaginella where there
are ligules, not only on the micro- and mega-sporophylls but on the
vegetative leaves as well, making comparison with the conifers still
more difficult. In the case of these ligulate Lycopsida there is an-
other feature, difference in spore size, which distinguishes them
from the conifers. All ligulate Lycopsida produce spores of two
sizes, very small and very large, whereas in the conifers and in fact
in all seed plants the spores are not significantly different in size
(Thomson, 1927). Homospory and not heterospory is thus basic in
the ancestry of the conifers. That such homosporous ancestry
should be sought in the Pteropsida instead of in the Lycopsida is
apparent from the work of Jeffrey in which he demonstrated that
the conifers belong to the Pteropsida because they invariably have
leaf gaps, no matter how small the leaves, while in the Lycopsida
no such gaps are present. It is on these facts that the comparison
which Seward (1919, 117) made between the organisation of the
female cone in the Coniferae and that of Lycopodium must not be
considered as indicative of their ancestry. His comparison with
Lycopodium, however, is important in that it indicates that the
ligule, not being present in Lycopodium, cannot be homologous
with the outgrowth associated with the ovule in the Coniferae.
The brachyblast theory, unlike the ligular and also unlike the one
here proposed, does not admit that the male and female cones are
homologous but regards the female cone as one grade higher in
organisation than the male--an 'inflorescence' instead of a 'flower.'
This interpretation of the female cone is based on the presence of
an upper series of inversely oriented bundles which is considered
to indicate that the ovule-bearing structure is a short-shoot or
78 T H E BOTANICAL REVIEW

brachyblast arising in the axil of a bract. Thus on the basis of the

brachyblast theory those conifers which show the greatest develop-
ment and independence of the ovuliferous scale are regarded as
most primitive. These are included in the Abietineae which in
anatomical structure have the greatest array of specialised features
of any family of the Coniferae---highly developed systems of lig-
neous resin canals, both vertical and horizontal, the latter extending
into the bast with bulbous expansions capable of continued growth;
ligneous rays with very abundant and sometimes elaborately sculp-
tured ray tracheids; tracheids with pitting provided with specialised
"rims of Sanio," etc. This statement is not intended to imply that
there is of necessity a phylogenetic correlation between anatomical
structure and cone organisation, but only that any theory which is
corroborated by such evidence should be given preference over an
equally acceptable one which lacks such corroboration. On this
basis the ligular theory takes precedence over the brachyblast, since
it accords primitive place in cone organisation to the Araucarineae,
forms which at the same time have very simple anatomical structure
of their wood--none of the specialised features characteristic of the
Abietineae. Viewed from this standpoint the ligular theory pro-
vides evidence that the dorsiventral araucarian type of stamen
(multi- and free-sporangiate) is more primitive than that of the
pines (bisporangiate, and the sporangia fused with the filament).
Strong support of this view was presented by Thibout (1896) in
his comprehensive study of the male cone of gymnosperms, from
which he concluded that the 'cycad-araucarian' type of stamen was
the most primitive in the Coniferae, a study which has not received
the attention it deserves. Additional evidence that the araucarian
type is primitive is provided by one of the deductions from Hof-
meister's work, that homology between the male and female cones
is most clearly expressed in the most primitive forms. Since the
extension of sex-differentiated features proceeds outwardly it fol-
lows that resemblance in external features becomes a valuable cri-
terion of primitiveness. Seward was the first to apply this prin-
ciple to the conifers where similarity in both size and external
morphology of the male and female cones and sporophylls of the
araucarians is in some cases almost as marked as in the cycads, a
condition which is not approached in any other conifer family.
In both cycads and araucarians there is also similarity in the
 CONE STRUCTURE IN THE CONIFERAE 79

structure of the male and female cones, in that both show a func-
tional correspondence between the upper and lower inversed vascu-
larisation of their respective dorsiventral male and female sporo-
phylls which is associated with the vascular supply of their spo-
rangia. In the araucarians the sporangial-supply nature of the
lower in the male is evident from the fact that the number of
bundles varies directly with the number of pollen sacs (from 23 to
2 as observed). On the other hand, in the female cone with its
uni-ovulate sporophylls the variations are correlated with size of
the seed, the differences in which are very marked. Where the seed
is small, as in Agathis, its inversed supply is small and detaches
itself from that of the sporophyll near the base of the seed; where
the seeds are progressively larger in different species of Araucaria
their supplies are correspondingly larger and detach themselves pro-
gressively nearer the axis of the cone; and in A. bidzeilli where the
seed is largest the supply is largest and there is direct attachment to
the vascular bundles of the cone axis. These facts coupled with the
finding of four ovules on a scale of Zamia, two of which were on
the upper surface (as in the conifers) and supplied entirely by in-
versed bundles, finally made it evident that the inversed upper supply
is not indicative of a brachyblast, but that both upper and lower
are of sporangial-supply nature and so more comparable to the
inversions characteristic of 'enations.'
Viewed from the standpoint of sporangial supply, it is evident
that if the conifers are monophyletic, as indicated by the organisa-
tion of the male cone, the female should show basic similarity of
organisation throughout the whole group. In this connection im-
portance attaches to the number and size of the ovules and also of
their associated protective structures, the ovuliferous scales (a
designation appropriately applied by Seward to the so-called ligule
of ,4raucaria). When so interpreted it becomes evident that the
living conifers represent two divergent lines of development, one
with a single ovule to the sporophyll and the other with several.
If these two lines are associated with the araucarians in ancestry
both ovular conditions must be present in their ancestral forms.
Far back in the fossil record there are sporophylls ascribed to the
araucarian conifers bearing one, three and five ovules, each ovule
with an ovuliferous scale more or less developed. That the uni-
ovulate condition of living araucarians is closely associated in an-
80 THE BOTANICAL REVIEW

cestry with the tri-ovulate is indicated by the work of Mitra (1927)

on .4raucaria in which there is both morphological and anatomical
evidence that two extra (lateral) ovules and ovuliferous scales had
aborted, while in .4#athis vestigial lateral inversed bundles suggest
abortion of two ovules in this genus (Thomson, 1906). That there
is a similar relationship between the five- and the three-ovulate con-
ditions may be inferred from Walton's (1928) description of
Voltzia Liebeana. Here there are three large and two small scales
attached proximally to the sporophyll at their united bases. The
large ones are each considered to have had an associated seed as
indicated by detachment scars, and since in the living forms one
ovuliferous scale to the ovule is the rule and this is smaller if the
ovule aborts it is probable that this fossil form bore two extra
ovules which aborted early. Thus in the living and fossil arau-
caftans there is evidence of the basis necessary for the related origin
of the two lines of development as seen in the living conifers, lines
which may be appropriately designated taxacean and pinacean since
they culminate respectively in Taxus and Pinus.
In the taxacean line, where the uni-ovulate condition is basic,
specialisation shows itself in reduction of the number of sporophylls
to a cone and the gradual loss of community protection, such as that
provided in the araucarian sporophyll type of cone. An early stage
is illustrated by Saxegothaea and Microcachrys, in the latter of
which one ovule may early take precedence over the others and be
the only one to mature (Thomson, 1909). Accompanying reduc-
tion in the number of sporophylls to a cone there is gradual attain-
ment of individual protection of the single ovule as it increases in
size by acquirement of a thick, sclerotic (sometimes fleshy) testa, and
by differentiation of the ovuliferous scale into a fleshy arillus, as
seen in the higher Podocarpineae and Taxineae. The stages of
differentiation of the ovuliferous scale are gradual, beginning with
its broadening and partial encirclement of the ovule in the lower
Podocarpineae where it is unvascularised, and ending with com-
plete encirclement and vascularisation in the higher forms, where
the structure of the arillus in Taxus indicates that several infertile
ovuliferous scales are concerned in its formation, a condition simi-
lar to that in the ovule as described by Miss Aase (1915). In the
taxacean line the inversed ovular supply, which in the lower forms
 CONE STRUCTURE IN THE CONIFERAE 81

is derived from the normal sporophyll bundle, soon becomes axial

in origin as the ovule becomes larger and more axially located.
In the pinacean line, the sporophyUs bear several ovules each and
there is community protection of the ovules, at first (as in the
araucarians) almost entirely by the sporophylls themselves. This
sporophyll type of cone is found in the most primitive Taxodineae.
Here the ovuliferous scales (one to each ovule) are small and un-
vascularised, their number varying with the number of ovules, each
of which is supplied by one inversed bundle (3 in Cunninghamia
and 3 to 6 in Athrotaxis selaginoides). Further advance involves
shifting of part of the protective function from the sporophylls to
the ovuliferous scales which become larger and vascularised, each
from the bundle supplying its ovule. These ovuliferous scales are
independent of one another and of their sporophyll in the young
stage but later fuse at their bases with each other and with their
sporophyll, growth in this region producing a combination type of
scale with its component parts (fused ovuliferous scales and sporo-
phyll) showing as free tips when the cone is mature. This combina-
tion type of structure is illustrated in Cryptomeria where the number
of ovules and ovuliferous scales per sporophyll was found to vary
from 3 to 6 with corresponding variation in their vascular supplies.
Sciadopitys shows a more extreme variation in the number of
ovules, ovuliferous scales and bundles (5 to 13). In the Cupres-
sineae, where the ovules also vary greatly in number but are
attached closer to the cone axis than in the Taxodineae, fusion takes
place so early that at maturity scarcely a trace of the individuality
of the different parts is evident. That the ovuliferous scale in the
higher Taxodineae and Cupressineae is of the fusion type, is indi-
cated in the lower forms, where the number of ovules is large, by
correspondence between the number of inversed bundles and ovules
at an early stage, the lack of such correspondence at a later stage in
the lower and in all stages of the higher forms being probably
associated with early abortion of ovules, chiefly of the lateral.
Whatever the origin of the increase in the upper series it is corre-
lated with decrease in the normally oriented lower, from the large
number in the Araucarineae to one in most of the higher Taxodi-
neae and Cupressineae, a change which is associated with the
gradual transfer of the protective function from the sporophyll
proper to its fused ovuliferous scale component, and with the more
82 THE BOTANICAL REVIEW

axial origin of its vascular supply. Finally, in the Abietineae,

where the two components of the sporophyll are almost separate,
the transfer of the protective function to the upper becomes prac-
tically complete, the lower sharing in this usually only when the
cone is very young, and acquiring a new functionwthat of aiding
(by uprolling of its margins) to separate the ovuliferous scales for
the access of pollen. In the resultant fused-ovuliferous-scale type
of cone, the individual scale has much more vascularisation than
required for the supply of its two ovules, a supply which in the
upper part of the cone may make as many as five separate attach-
ments to axial bundles. That the central part of the extra vascu-
larisation of the scale is associated with the abortion of an ovule is
suggested by Miss Aase's (1915, 289) work on Keteleeria in
which she found evidence of a third (abortive) ovule between the
other two, a feature that may also have a bearing on the origin of
the keel which, like the sporophyU in the young stage, aids the
access of pollen. In the Abietineae, however, there is no similar
evidence on the origin of the extra lateral bundles, but the condi-
tions referred to in the Taxodineae and Cupressineae are sugges-
tive. In the pinacean line, as in the taxacean, the inversed ovular
supply bundles in the lower forms arise by division of the normally
oriented bundles of the sporophyll, and in the higher independently
from bundles of the cone axis, but whereas in the uni-ovulate line
the transition is abrupt accompanying the more rapid change in
size of the seed and reduction of the cone, in the pluri-ovulate line
where the number instead of the size of the ovules is important and
the reduction of the cone of significance only in the higher Cupres-
sineae, there are more intermediate forms.
Such intermediate forms not only show the general trend of spe-
cialisation very clearly but the individual cone of certain of them
may also show a similar trend, repeating the group sequence more
or less completely from base to apex of the cone. It was, for ex-
ample, at the base of the cone that Miss Aase found indications of
tri-ovulate scales in Keteleeria, and Mitra a similar condition in
Araucaria. There is also clear evidence of this trend in the source
of the upper vascularisation which in basal scales may arise in the
primitive way by division of the normally oriented sporophyll
bundles and towards the apex from those of the axis as in the spe-
cialised forms. In assessing the significance of this change of
 CONE STRUCTURE IN THE CONIFERAE 83

origin, infertility might seem to be involved, but this cannot be the

determining factor since the origin is still axial in infertile scales
toward the apex of the cone. In the male cone where the requisite
intermediate degree of specialisation is more often found than in
the female, the trend is of more general occurrence and more
clearly expressed than in the female cone. This trend is exception-
ally clear in the common type of hi-sexual cone in which the more
primitive (male) sporophylls are borne at the base and the more
specialised (female) above, an explanation which is equally ap-
plicable to the angiosperm flower. In the basal region of the female
part of such cones the sporophylls may bear ovules on the lower
surface, a reversion to their original position as indicated by the
normal location of the pollen sacs of the more primitive male
sporophyll. In other cases the ovules in this region may be later-
ally located, as in cycads', and so show partial attainment of their
normal location in the upper part of the cone. A similar primitive
location of ovules may occur in the case of sporophylls from the
base of wholly female cones.
On the basis established by Hofmeister's work it is evident that
in the conifer series specialisation of the male and female cone
structure has followed two distinct lines, the specialisation in these
lines arising from sex-associated differentiation of homologous dor-
siventral sporopl~ylls of araucarian type and culminating in strik-
ingly different ways. In the final stage of the taxacean line both
male and female cones are much reduced and have fused sporo-
phylls, the female with a single apical ovule and elaborate individual
protective structure, while in the final stage of the pinacean line
both sporophylls have attained a stabilised two-sporangiate con-
dition with the sporangia in the male grown to the filament and in
the female partly embedded in the highly developed ovuliferous
scale, the aggregate of such scales forming the most specialised
community type of ovular protection in the conifers. In the course
of specialisation of the male and female cones in both lines reduc-
tion and fusion play such significant r61es that they assume an
importance somewhat commensurate with that accorded them in
connection with the flower of the angiosperms.
84 T H E BOTANICAL REVIEW

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