CHAPTER XXVIII.

CYCADALES (+recent+).

Among the fossil genera described in the last chapter of the second volume some were spoken of as true Ferns though most of them, it was added, ‘may safely be regarded as plants which will ultimately be shown to belong to some other group, in most cases that of the Pteridosperms.’ Since this was written additional evidence has been obtained in favour of the inclusion of certain genera in the Pteridosperms. In the case of _Taeniopteris_, one of the genera already described, there is reason to believe that at least one species is a member of the Cycadales and not a true Fern as formerly supposed.

The Pteridosperms so far described are represented for the most part by sterile leaves preserved as impressions, the genera founded on more satisfactory material having been reserved for treatment in this volume. As these genera are founded to a large extent on anatomical characters oscillating in their essential features between recent Ferns and Cycads, it is important that the student should be in possession of the anatomical characteristics of both of these classes; and for this reason a general account of recent Cycads is intercalated between the Pteridosperms already described and those reserved for treatment in this volume.

* * * * *

The section of the Gymnosperms known as the Cycadales, represented by nine recent genera and less than 100 species, is of exceptional importance phylogenetically and demands special attention from palaeobotanical students. Familiarity with the morphology of recent forms is essential not only in relation to extinct cycadean plants but also to types which, though not sufficiently close to surviving species to be included with them in one class, exhibit features regarded by many botanists as indications of an affinity either to true Cycads or to some generalised stock of which they are an offshoot. The Cycads of to-day may fairly be spoken of as anachronisms, plants appropriate to a former age but out of harmony with the present. They are confined to tropical and sub-tropical regions in both the old and new world. In habit many of them resemble tree-ferns, but the columnar stem, which may live to a great age and attain a height of 20 metres, differs from that of ferns in its gradually tapered form consequent on the presence of one or more cambial cylinders. Though often unbranched (fig. 377) branching of the main trunk is by no means unusual (fig. 378; fig. 381, B). Many Cycads are geophilous and have short tuberous stems (figs. 383, 395, 1_a_; 396, E): the genus _Zamia_ includes a few epiphytic forms[1]. The typical cycadean stem is covered with persistent petiole-bases with or without an admixture of smaller scale-leaf bases (figs. 379, 380), while in several species a transversely wrinkled or irregularly fissured periderm forms the superficial tissue (figs. 381, B; 383). The foliage-leaves are relatively large and, with the exception of the bipinnate fronds of _Bowenia_ (fig. 391), they are always pinnate. The fronds usually form a terminal crown (figs. 377, 379) and as many as 100 may be produced from one bud. In _Zamia pygmaea_[2] the fronds are only 10–12 cm. long, but in some cycads they reach a length of several metres. On both young foliage-leaves and scale-leaves long and very rarely branched[3] unicellular hairs (fig. 396, N) form a characteristic feature and take the place of the ramental scales of the majority of ferns. The apex of the stem shown in fig. 386, A is covered with a mass of woolly hairs and several scale-leaves are seen on the lower part of the bud.

[Illustration: Fig. 377. _Cycas circinalis._ From a photograph taken by Mr A. Malins Smith at Teldeniya (Ceylon).]

[Illustration: Fig. 378. _Cycas revoluta_, as grown by Japanese horticulturalists. (After Wieland.)]

[Illustration: Fig. 379. _Encephalartos horridus._]

[Illustration: Fig. 380. _Cycas circinalis._ Stem showing alternate zones of leaf-bases (F) and scale-leaf bases (S). (From the _Encyclopaedia Britannica_.)]

[Illustration: Fig. 381. A. _Cycas revoluta_, megasporophylls. B. _Zamia Loddigesii_, branched stem.]

All recent Cycads are dioecious. The reproductive shoots, except the megasporophylls of _Cycas_—which have departed to a less extent than those of other genera from the foliage-leaf plan (fig. 381, A; fig. 392, A–C) and are borne in a terminal cluster through which the stem subsequently pushes its way—consist of a varying number of micro- or mega-sporophylls in dense spirals on the axis of an elongated or oval strobilus (figs. 386, B, 393, 394). The microsporophylls are occasionally verticillate[4]. The strobili are sometimes though rarely branched[5] and generally but by no means invariably[6] terminal on the main stem which branches sympodially[7]. A striking example of lateral strobili has recently been described by Chamberlain[8] who figures a stem of _Macrozamia Moorei_ with fertile shoots wedged among the persistent petiole-bases, a condition very similar to that in the Mesozoic Bennettitales. Pearson has also described clear cases of laterally-borne cones in _Encephalartos._ _Cycas_ exhibits two kinds of branching, the female plants being monopodial while in the male the branching is sympodial. The microspores are produced in sporangia grouped in more or less well defined sori (figs. 389, A; 392, E–G). There is no definite annulus, but in the occurrence of groups of thick-walled cells some microsporangia recall those of certain ferns[9]. The ovules vary considerably in size, sometimes exceeding 5 cm. in diameter: there are usually two on each megasporophyll (figs. 393, C; 394; 395, 1_d_) but in most species of _Cycas_ (fig. 392, B) and occasionally in other genera the number is larger[10]. A thick integument encloses the nucellus with which it is fused except in the apical region (fig. 396, A, B). Below the comparatively long micropylar tube is a well-developed pollen-chamber (fig. 396, B′, _p_), a striking feature of Cycadean ovules, immediately above the megaspore; the latter is filled with prothallus-tissue and bears a small apical group of archegonia on the floor of a depression (fig. 396, A–B′). In _Microcycas_[11] as many as 200 archegonia are recorded—a very exceptional case—and these are not confined to the apical region, though only the apical archegonia are functional. Each archegonium is characterised by a very large oval egg-cell and a much reduced neck[12]. The microspores usually produce a single prothallus-cell, a stalk-cell, and body-cell, and from the body-cell are developed two spirally ciliated spermatozoids (fig. 396, M). In this respect also the monotypic genus _Microcycas_ is peculiar: it may have as many as 8 body-cells and 16 male gametes in a single pollen-tube (fig. 396, G), while in _Ceratozamia_[13] 4 gametes have been seen in one tube. The pollen-tube grows like a fungal mycelium into the nucellar tissue and the male gametes are formed in the distended proximal end which on bursting liberates the motile sperms with the watery cell-sap. Fertilisation is succeeded by the development of a homogeneous proembryo partially or completely filling the zygote (fertilised egg): by the formation of long suspensors the embryo is brought into contact with the food-store of the prothallus. In some Cycads, _e.g._ _Encephalartos_, the embryogeny exhibits a close resemblance to that of _Ginkgo_[14]. The embryo is dicotyledonous[15].

The single stele of the stem is characterised by a large pith which in some genera (_e.g._ _Encephalartos_, _Macrozamia_) contains an anastomosing system of collateral bundles. The vascular tissue of a cycadean stem forms a cylinder of secondary xylem and phloem, the primary xylem being represented only by a few, usually crushed, protoxylem elements on the inner margin of the reticulately pitted or scalariform tracheids. Both xylem and phloem are traversed by numerous broad and deep medullary rays[16]. The looser texture and more parenchymatous structure of Cycadean wood afford a ready means of distinguishing it from the wood of Conifers: for the Cycadean type the term _manoxylic_ is proposed and _pycnoxylic_ for the more compact coniferous wood[17]. Rims (or ‘bars’) of Sanio, of which much has been said in discussions on the phylogeny of Conifers, have recently been described in the petiolar xylem of _Cycas revoluta_: the rims are short and ‘cling closely to the borders of the pits,’ features which also characterise the rims found in the cones of the Araucarineae and in the root- and cone-wood of certain Pines[18]. In some Cycads the secondary xylem and phloem form a single cylinder, but in others (_Cycas_, _Encephalartos_, _Macrozamia_, _Bowenia_) the cambium is succeeded by one or several concentric cylinders of meristem which have their origin in the pericycle. The spasmodic occurrence of separate arcs of inversely orientated secondary xylem and phloem between the normal cylinders is a feature of importance from the point of view of comparison with the Palaeozoic Medulloseae[19]. The occurrence of concentric cauline strands in the cortex of _Cycas_ is also a peculiarity worthy of notice. Successive bands of periderm, and occasionally a considerable amount of phelloderm[20], are formed in the peripheral region of the stem.

The leaf-traces in an adult stem exhibit a striking feature in their indirect or girdle-like course to the leaves (fig. 396, H, _g_) and in the gradual change from an endarch (fig. 396, O) to an apparently mesarch structure (fig. 400) as they pass from the perimedullary zone to the petiole: except at the base of the petiole the vascular bundles of the frond-axis consist of (i) centripetally developed xylem with a median protoxylem and a much smaller amount of centrifugal xylem (fig. 400) separated by a few parenchymatous elements from the centripetal xylem, (ii) an external arc of protophloem and within this metaphloem and parenchyma[21]. In the slender petiole of _Bowenia_ there are a few collateral bundles arranged in the form of a circle or ellipse[22]; in _Cycas_ and some other genera the more numerous bundles form a pattern like an inverted U, and in some species of _Encephalartos_ the number is greater and the strands more irregularly scattered[23]. In the vegetative stems there is no centripetal xylem in the stele, but scattered centripetal tracheids occasionally occur internal to the protoxylem in the steles of the peduncles[24].

* * * * *

=Cycadeae.= Megasporophylls each bearing 2–8 ovules, borne separately like foliage-leaves and not in strobili. Pinnae have a midrib but no lateral veins (figs. 384, 387, A). _Cycas_ (fig. 377).

=Zamieae.= Both kinds of sporophylls form strobili. Pinnae have several dichotomously branched, more or less parallel veins. _Zamia_ (figs. 388–390), _Macrozamia_, _Encephalartos_ (figs. 379, 386, C), _Ceratozamia_, _Dioon_ (fig. 386, B), _Microcycas_.

=Stangerieae.= Strobili as in Zamieae. Pinnae fern-like, numerous dichotomously branched lateral veins given off from a midrib. _Stangeria._

=Bowenieae.= Leaves bipinnate (fig. 391), strobili as in Zamieae. _Bowenia._

_Distribution._ The most widely spread genus, _Cycas_, occurs in Siam, India, the Nicobar Islands, Ceylon, Madagascar, and Australia, in many of the islands in the Indian and Pacific oceans, in New Guinea, Borneo, New Caledonia, New Britain, China and Japan[25]. _Zamia_, the most northerly genus, extends from North Mexico and Florida through Central America and some of the West Indian islands to Ecuador, Bolivia, Chile, and Peru. _Dioon_ and _Ceratozamia_ are confined to South Mexico, and _Microcycas_ flourishes on the Cuban mountains. The continent of Africa possesses two endemic genera _Encephalartos_ and _Stangeria._ _Encephalartos_ extends from Cape Colony through Natal and Zululand to Zanzibar and Mombasa[26]: a specimen in the Kew Herbarium (probably _E. Hildebrandti_) is said to have been collected as far north as the Soudan. Two species are recorded from the Congo[27] and _E. Barteri_, discovered by Barter in Central Africa, is recorded from the Gold Coast[28]. _Stangeria_ has a much more limited range in S.E. Africa[29]; Australia possesses _Macrozamia_, represented by several species in Western Australia, New South Wales and Queensland, _Cycas_ in Queensland and the Northern territory and the Queensland genus _Bowenia_. There are no Cycads in New Zealand. As a whole Cycads have a limited range and with the exception of _Cycas_ and _Zamia_ none of them extend beyond the limits of a single continent. They are as a rule not gregarious plants and play a subordinate part in the facies of the vegetation. _Macrozamia_ forms dense thickets[30] in some districts and occurs both in exposed situations and in association with Palms in damp Queensland forests. Chamberlain[31] speaks of 100 plants of _Dioon edule_ as visible in one view in South Mexico where the species forms a mountain forest. In Florida _Zamia pumila_[32] grows in dense moist woods, a habitat in contrast to that of many Cycads. The Mexican _Ceratozamia_ is associated with luxuriant vegetation, while its compatriot _Dioon_[33] lives in blazing sunshine. Sir Joseph Hooker[34] speaks of _Cycas_ living in the deepest and hottest valleys in Sikkim. _Encephalartos_ is essentially a xerophilous genus. _Stangeria paradoxa_ is said to be confined to forests in Cape Colony, and another species grows among the grass of the Park-lands in open country[35]. While it is true that many Cycads are characteristic of dry regions some species flourish in places where shade and moisture are abundant.

Though it is impossible in many cases to form an estimate of the age of individual plants, there are clear indications that some specimens afford notable instances of longevity. Chamberlain estimates the age of some plants of _Dioon spinulosum_ as exceeding 400 years and mentions an example of _D. edule_ that is probably 1000 years old. An unusually tall plant of _Encephalartos_ in the Botanic Garden of Amsterdam is believed by Prof. de Vries to have reached the venerable age of 2000 years[36]. The restricted range and in many cases the solitary existence of recent Cycads, with their tall stems clothed with the persistent cork-covered stumps of thousands of fronds, deepens the impression of antiquity derived from a study of the geological history of this dwindling race.

_Stems._ The tall columnar stems of some species of _Cycas_, often branched or bearing numerous ovoid buds like enlarged bulbils[37], are characterised by the regular alternation of large and small leaf-bases as seen in the stem of _C. circinalis_ reproduced in fig. 380. In older stems of this species the leaf-bases are exfoliated and the stem is covered with wrinkled and fissured cork; but in _Cycas revoluta_ the leaf-bases are even more persistent. The columnar but relatively stout stems of _Encephalartos_ (figs. 379, 382, 386, A) and _Ceratozamia_ are similarly encased in a covering of petiole-bases, but in these genera the differences between foliage-leaves and bud-scales is much less obvious and there is no zonal alternation. On the stems of _Macrozamia_ the rhomboidal leaf-bases are more uniform in size and there are no scale-leaves. The tall and often palm-like stems of _Microcycas_ sometimes show transverse rings on the bark marking the position of former terminal buds, and in older trunks these may disappear, leaving a fissured bark[38]. In _Cycas siamensis_ the tuberous stem is similarly covered with a rough bark (fig. 383) and the stems of _Zamia_ are also characterised by an absence of persistent leaf-bases (figs. 381, B; 395, I_a_, _a_). It is pertinent to remind the palaeobotanical student of the occurrence of flowering plants with stems closely simulating those of some Cycads. Prof. Bower[39] in describing _Rhynchopetalum montanum_, an Abyssinian Lobeliaceous plant, drew attention to the similarity in surface-features and to some extent in anatomical structure to cycadean stems. The resemblances are further emphasised in a more recently published account of the same species under a different name, _Lobelia Rhynchopetalum_[40].

[Illustration: Fig. 382. _Encephalartos Ghellinckii._ (¹⁄₁₁ nat. size.)]

[Illustration: Fig. 383. _Cycas siamensis._ (From the _Encyclopaedia Britannica_.)]

_Fronds._ A general acquaintance with the various types of fronds illustrated by recent Cycads is important to the student of fossils not only to enable him to compare existing and extinct forms but as affording safeguards against possible sources of error in the description and identification of impressions[41]. The vernation exhibits less uniformity than in Ferns: in _Cycas_ the rachis is straight and the pinnae circinately coiled (fig. 220, B, vol. +ii.+ p. 283); in _Zamia_ and _Stangeria_ the rachis is bent and the pinnae straight, while in _Ceratozamia_ and other genera both the axis and leaflets are straight. As Braun pointed out, there is as a rule no terminal leaflet, or it may be pushed to one side giving a forked appearance to the frond apex[42].

[Illustration: Fig. 384. _Cycas circinalis_, abnormal frond. (From a specimen in the British Museum.)]

_Cycas._ The presence of a strong midrib and the absence of lateral veins are distinguishing features: the lower margin of the lamina is frequently decurrent (fig. 387, A). In _C. circinalis_ the pinnae may reach 40 cm. in length with a fairly uniform breadth of 2 cm. A frond of this species in the British Museum, not quite complete, has a length of 112 cm.: on the lower part of the rachis strong spines replace the leaflets and near the apex of the leaf concrescent pinnae form a continuous lamina traversed by seven ribs and dissected at the margin into acuminate teeth (fig. 384): some of the pinnae are forked as in _Cycas Micholitzii_[43] (fig. 385). Several years ago I noticed a similar instance of concrescence in a small plant of _C. circinalis_ in the Royal Gardens, Kew (fig. 387, I). In _Cycas Micholitzii_ the pinnae, reaching a length of 20 cm., are repeatedly and deeply forked (fig. 385, A, B; fig. 400): the pinnae of _C. Rumphii_ var. _bifida_[44] are also deeply dissected. _Cycas Beddomei_ has very narrow pinnae (15 cm. × 2 mm.) similar to those of the Wealden species _Cycadites Saportae_, and it is noteworthy that narrow leaflets with a strongly revolute lamina would produce casts with two parallel ribs (the grooves between the midrib and the edge of the lamina) simulating the double midrib of the fossil genus _Pseudocycas_. In some fronds, _e.g._ _C. Cairnsiana_, the midrib is hardly visible on the upper face of a dried pinna which shows a longitudinal wrinkling simulating parallel venation.

[Illustration: Fig. 385. A, B, _Cycas Micholitzii._ (After Thiselton-Dyer.) C, _Zamia angustifolia._]

_Encephalartos._ The fronds of this genus, in _Encephalartos Laurentianus_[45] reaching the exceptional length of 7 metres, bear alternate pinnae exhibiting a considerable range in form and breadth. In _E. longifolius_, _E. Altensteinii_ (fig. 386, C), _E. Lehmanni_, etc., the pinnae are for the most part linear, reaching a length of 20 cm. and a breadth of 2 cm.: in _E. caffer_ (fig. 387, D), _E. latifolius_, and others the pinnae are broader and shorter and often spinous. A frond of _E. longifolius_ or _E. Altensteinii_ may bear both entire and lobed, spinous pinnae. In _E. Frederici-Guilielmi_ (fig. 387, G) and _E. Ghellinckii_[46] (fig. 382) the pinnae are very narrow and almost filiform, with revolute edges. The thick and leathery pinnae of some species are attached obliquely to the edge or to the upper sloping sides of the rachis which forms a prominent ridge between the rows of leaflets, and characteristic oval scars are left on the fall of the pinnae (fig. 387, D, G′). The lamina in most species contains several veins more or less parallel to the margins and often much more prominent on the lower than on the upper surface.

[Illustration: Fig. 386. A. _Encephalartos Altensteinii_, apex of stem. B. _Dioon edule_,megastrobilus. (From a photograph by Mr S. M. Wadham.) C. _Encephalartos Altensteinii_, frond.]

[Illustration: Fig. 387. Cycadean fronds. A, _Cycas circinalis_; B, _Macrozamia Fraseri_; C, _Macrozamia Denisoni_; D, _Encephalartos caffer_; E, F, _Dioon edule_ from below and above; G, _Encephalartos Frederici-Guilielmi_, G′, side-view; H, _Ceratozamia mexicana_; I, _Cycas circinalis_, lower part of young frond.]

_Zamia._ In _Zamia angustifolia_ (fig. 385, C) and _Z. linifolia_ the pinnae are long and very narrow: the other extreme is represented by _Z. Wallisii_[47] (fig. 388) with broad ovate segments reaching a length of nearly ·5 metre and attached to the rachis by a short stalk; the veins are prominent and dichotomously branched. Other forms of pinnae are represented by _Z. integrifolia_, _Z. floridana_, and _Z. Loddigesii_ (figs. 389, 390, 395). The broad and short pinnae of _Z. furfuracea_[48] bear a close resemblance, except in the absence of an auriculate base, to those of some species of the fossil genus _Otozamites_. The broadly linear pinnae of _Z. pseudoparasitica_ (45 cm. × 3 cm.) often show longitudinal wrinklings on drying which suggest comparison with the corrugated lamina of the fossil species _Nilssonia brevis_. A basal pad or callosity on the slender bases of the pinnae is characteristic of many _Zamia_ fronds.

[Illustration: Fig. 388. Pinna of _Zamia Wallisii_. From a drawing after A. Braun in the Kew Herbarium. (⅓ nat. size.)]

[Illustration: Fig. 389. _Zamia integrifolia_ bearing a megastrobilus and showing foliage-leaves and scale-leaves. A, microsporophyll; B, megasporophyll. (After Rendle, from Jacquin.)]

[Illustration: Fig. 390. Small frond of _Zamia Loddigesii_. (⅔ nat. size.)]

_Ceratozamia._ The fronds bear a fairly close resemblance to those of _Macrozamia_: in _Ceratozamia mexicana_ the linear pinnae reach a length of over 30 cm. and a breadth of 2–3 cm.; the lamina tapers to a narrow apex and is more abruptly contracted at the base (fig. 387, H). The veins in _Ceratozamia_ are sub-parallel and dichotomy occurs up to the middle of the lamina[49]. A striking feature is the occurrence of two opposite stipule-like projections a short distance above the base of the petiole.

_Macrozamia._ A noteworthy feature in some species is the attachment of the linear pinnae along the middle line of the rachis (fig. 387, C); in others (fig. 387, B) the leaflets are attached laterally and may have a basal callosity. The parallel veins, which branch dichotomously near the base of the lamina, are often much more prominent on the lower than on the upper face. In _M. heteromera_[50] (fig. 396, F, F′) the narrow pinnae are deeply forked and strongly revolute. The spirally twisted rachis of _M. spiralis_, _M. heteromera_, etc., is a striking feature recalling the Rhaetic fern _Camptopteris spiralis_ Nath[51].

_Dioon._ The arrangement of the linear pinnae of _D. edule_ (fig. 386, B), _D. spinulosum_, and _D. Purpusii_[52] forms a ready means of distinguishing the fronds of this genus: the pinnae, often contiguous and at right-angles to the rachis, are attached in a lateral groove by an expanded and slightly decurrent base. The difference between the lower and upper face of a frond (fig. 387, E, F) affords a good illustration of a common source of error in the identification of fossil specimens. The leaflets of _D. spinulosum_, which except in their spinous margin are very similar to those of _D. edule_, may reach a length of 15 cm. and a breadth of 8 mm. The parallel veins are unbranched[53].

_Microcycas[54]._ The pinnae of this genus, very like those of the Wealden species _Zamites Buchianus_, reach a length of 20 cm. and a breadth of 8 mm.: on falling they leave oblong scars resembling those on the rachis of _Encephalartos_.

_Stangeria._ This genus is particularly interesting because of its fern-like habit and venation. The large fronds of _S. paradoxa_[55] bear broadly linear acuminate pinnae with entire, unevenly lobed, serrate, or pinnatifid margins. Some leaflets are so deeply dissected as almost to justify the appellation pinnate. Both entire and dissected leaflets may occur on one frond and the lower ones may be stalked while the upper pinnae are sessile. The venation agrees closely with that of the genus _Taeniopteris_[56].

_Bowenia._ The large fronds of this genus (fig. 391) are peculiar in being bipinnate; they may reach a length of 2 metres and have a long slender petiole: the asymmetrical lamina of the segments, entire or deeply serrate, is attached by a very short stalk; the veins branch dichotomously[57] and diverge slightly. Both entire and serrate pinnae may occur on the same plant, but Chamberlain has revived André’s specific term _serrulata_ in preference to the generally adopted designation for the serrate forms, _B. spectabilis_ var. _serrata_[58].

[Illustration: Fig. 391. _Bowenia spectabilis_, frond. (From the _Encyclopaedia Britannica_.)]

_Reproductive shoots_[59]. In _Cycas circinalis_, _C. Rumphii_, and other species the megasporophylls reach a considerable length and bear several lateral ovules each of which may be as large as a goose’s egg: the sterile distal end has the form of a spear-point with an irregularly serrate edge. In _C. revoluta_, _C. pectinata_, etc., the sterile part is deeply dissected and may break off (fig. 392, A) from the fertile portion of the sporophyll. The megasporophylls of _C. Riuminiana_ exhibit a striking variation in form (fig. 392, B, C); some are 15 cm. long with several ovules, while others, reduced to 8 cm., bear only two ovules and resemble the sporophylls of _Dioon_. In all other genera the megasporophylls are aggregated into cones, but in _Dioon_ the strobili are characterised by their more ovoid form and by the looser arrangement of the sporophylls (fig. 386, B), each of which consists of a horizontal stalk expanded distally into a broadly lanceolate upturned end covered with a thick felt of hairs and bearing at its base usually 2, rarely 5–6, ovules on cushion-like swellings. In _Dioon spinulosum_ the cones may be 50 cm. long. Between the cones of _Microcycas_, over 90 cm. long, and those of some Zamias, a few centimetres long, there are many intermediate forms. The large strobilus of an _Encephalartos_ reproduced in fig. 393, D, shows the convex ends of the sporophylls with a jagged edge, and in monstrous cones the marginal lobes may be abnormally developed and assume the appearance of pinnae[60]. Each megasporophyll bears two large ovules (fig. 393, B). In certain species of _Encephalartos_ the swollen ends of the sporophylls have a truncate centre like the flattened umbo of some Pines (fig. 392, D). The presence of two divergent spines is a peculiarity of the megasporophylls of _Ceratozamia_ (fig. 393, C): in _Macrozamia_ (fig. 394) the distal ends are prolonged as tapered processes. The surface of the strobilus of _Stangeria_ is formed by imbricate and rounded ends of sporophylls (fig. 392, H) not unlike the cone-scales of _Pinus excelsa_ or _P. cembra_. The megasporophylls of _Zamia_ are expanded into regular cushion-like hexagons with a flat central area (figs. 389, B; 395, I_b_).

[Illustration: Fig. 392.

A. _Cycas pectinata_, apex of megasporophyll. (¾ nat. size.) B, C. _Cycas Riuminiana_, megasporophyll. (¾ nat. size.) D. _Encephalartos Altensteinii._ Distal end of megasporophylls. (From the _Gardeners’ Chronicle_.) E, F. _Cycas angulata_, microsporophyll and sorus. G, I. _Ceratozamia mexicana_, I, microsporophyll with scars of sori (_s_); G, sorus. (After Thibout.) H. _Stangeria paradoxa_, megastrobilus.]

[Illustration: Fig. 393.

A. _Stangeria paradoxa_, part of microstrobilus. B, D. _Encephalartos villosus_, megastrobilus in surface-view and in section. (¼ nat. size.) C. _Ceratozamia mexicana_, single megasporophyll.]

[Illustration: Fig. 394. _Macrozamia Preissii_, megastrobilus and (A) single megasporophyll; _a_, axis of cone; _p_, stalk of megasporophyll; _s_, unripe seeds. (After Rendle.)]

[Illustration: Fig. 395. _Zamia floridana._ I_a_, complete plant; _a_, main trunk; _b_, branch-scar; _c_, secondary root; _d_, primary tap-root. (⅛ nat. size.) I_b_, I_c_, megastrobilus. (¼ nat. size.) I_d_, megasporophyll. (½ nat. size.) I_e_, pinna. (¾ nat. size. After Wieland.)]

The microsporophylls (figs. 389, A; 392, E) are in all genera aggregated into strobili which often bear a close resemblance to seed-cones (fig. 393, A). On a single sporophyll of _Cycas circinalis_ there may be as many as 700 sporangia while in _Zamia floridana_ there are only two microsporangia. The spore-output is large and in extreme cases, _e.g._ in _Dioon spinulosum_, the average number of spores in a sporangium is said to be 30,000[61].

_Seeds._ In the great majority of recent species the seeds may be described as large and afford a striking contrast to the small seeds of the Mesozoic Bennettitales. A feature of interest from the point of view of comparison with Palaeozoic seeds is the absence of a resting stage, germination in some cases following seed-fall without an interval. As Warming pointed out, the embryo is often undeveloped when the seeds are shed. An interesting fact is recorded by Capt. Dorrien-Smith[62] with regard to seed-dispersal: he describes the heavy pebble-like seeds of a _Macrozamia_ as being hurled from the ripe cones a distance of 12 ft. The seeds of _Cycas_ are platyspermic; the woody shell exposed on removal of the outer flesh is slightly flattened and has two prominent angles, but three-angled seeds may occur as in _Ginkgo biloba_ (fig. 631, C). In other genera the seeds are radiospermic. The seed of _Encephalartos Altensteinii_[63] (fig. 396, D) has a square-cut distal end with a small papilla at the summit of the unusually long micropylar canal (17 mm.). The stone of this seed (fig. 396, C) shows parallel curved ridges which mark the position of vascular strands in the inner region of the outer flesh. The large ovules of _Cycas circinalis_[64] have an integument 1 cm. thick consisting of an outer and inner flesh and an intervening stony layer which reaches its greatest development at the base and apex. Three vascular strands enter the base of the seed, the concentric strand breaks up in the broad inner flesh into a group of bundles which embrace but do not penetrate the lower end of the nucellus. Each of the two lateral strands branches in the outer flesh near its entrance into the seed; the outer and larger collateral and mesarch bundle passes up close to the surface of the shell to the seed-apex, while the inner branch penetrates the shell and, occasionally branching, passes up the inner region of the inner flesh as far as the micropyle. In other seeds the tracheal supply of the outer flesh consists of several bundles and not two as in _Cycas_. The inner flesh abuts on the nucellus and is connected with it except at the apex (fig. 396, B). In ripe seeds the nucellus is reduced to a thin membrane enclosing the large megaspore at the upper end of which is a depression (fig. 396, B′) or sometimes two depressions (fig. 396, I) in the prothallus containing the archegonia. In the seed of _Dioon edule_[65] (fig. 396, A) the position of the absciss-layer (_s_) is indicated by a slight transverse constriction. In the seeds of _Bowenia_, constructed on the same plan, the inner series of vascular strands appears to be nucellar in position, thus differing from the strands in _Dioon_, _Cycas_, and other genera which are confined to the integument. Miss Kershaw[66] in describing _Bowenia_ speaks of an upper and a lower pollen-chamber; the former serves as a storage-place for the microspores prior to their further development in the lower chamber. Dr Stopes[67] regards the integument as double in origin, a view suggested by Griffith[68] in 1835, and as homologous with the single integument _plus_ the cupule of _Lagenostoma_. This view is supported by Mrs Thoday[69]: on the other hand Miss Kershaw’s investigation of _Bowenia_ seeds leads her to regard the integument as single. Although there would seem to be a _prima facie_ case in favour of the dual nature of the integument, the arguments on the other side have greater weight[70].

[Illustration: Fig. 396.]

[Illustration: Fig. 396.

A. Seed of _Dioon edule_ in longitudinal section; _a_, integument; _v_, vascular tissue; _m_, prothallus; _n_, nucellus; _p_, pollen-chamber; _s_, absciss-layer; _ar_, archegonia. (After Chamberlain.) B, B′. Seed of _Cycas circinalis_; _a_, _v_, integument (sarcotesta) and vascular tissue; _b_, sclerotesta; _c_, inner sarcotesta; _m_, _n_, prothallus and nucellus. (After Stopes.) B′. Apex of nucellus; _p_, pollen-chamber; _i_, integument; _n_, nucellus; _ch_, archegonial chamber; _ar_, archegonia. C, D. Seed of _Encephalartos Altensteinii_; C, surface of stone. (After Stopes.) E. Stem of _Bowenia serrulata_; _g_, level of ground. (After Chamberlain.) F, F′. Pinnae of _Macrozamia heteromera_. G. Pollen-tube of _Microcycas Calocoma_. (After Caldwell.) H. Transverse section of stem of _Encephalartos horridus_; _s_, stele; _g_, girdle-bundles. (After Mettenius.) I. Apical view of prothallus of _Cycas_ showing two archegonial chambers (_ch_). (After Treub.) K. _Encephalartos Barteri._ Transverse section of stem; _x_, xylem; _p_, phloem. (After Matte.) L. _Cycas siamensis._ Transverse section of vascular tissue of young stem. (After Matte.) M. _Cycas revoluta_; two motile sperms. (After Miyake.) N. Long hair with short basal cell from the petiole of _Macrozamia heteromera_. (After Robertson.) O. Vascular bundle of _Dioon edule_ from base of petiole; _p_, phloem; _c_, cambium. (After Mettenius.)]

Recent observations point to the probability that insects play a part in the pollination of cycadean ovules. Kraus[71] drew attention to the strong smell emitted by the microstrobili of _Dioon edule_ and noticed that small bees were attracted to the ripe strobili of _Macrozamia_, while odourless cones of a neighbouring _Ceratozamia_ received no attention. Pearson[72] and Rattray[73] have obtained evidence that beetles and weevils act as pollinators to species of _Encephalartos_.

_Anatomical features._ Allusion has already been made to some of the more striking anatomical features; the large pith, the occasional occurrence of medullary vascular bundles, the presence of one or more cambiums, the large size of the medullary rays, etc. It is worthy of remark that the occurrence of an anastomosing system of medullary bundles is not a constant feature within a genus; in _Macrozamia Fraseri_ such a system is present, but absent in _M. Denisoni_[74]. In the pith of stems with no medullary bundles cylinders of collateral bundles may occur in connexion with a fertile shoot. These bundles arise from the inner face of the main cylinder and pass upwards as a domical system into the base of the terminal strobilus which is eventually pushed to one side by the growth of a lateral bud[75]. The secondary xylem tracheids are usually provided with several rows of bordered pits on the radial walls and resemble those of the Araucarieae[76], but in Cycads the pits are often not contiguous and less compact in their distribution. The wood of _Stangeria_ is peculiar in consisting of scalariform tracheids[77] (fig. 397). Chamberlain describes growth-rings in the wood of _Dioon_; but this is exceptional. In tangential sections of the stele leaf-trace bundles are constantly seen passing horizontally through the broad and deep medullary rays. The pith-cast of a cycadean stem reproduced in fig. 398 shows the wide meshes in the reticulum of tracheal tissue originally occupied by parenchyma, which on decay left lenticular depressions represented on the cast by tapered convex areas occasionally bearing the impress of an outgoing trace in the form of a narrow groove. The secondary phloem often rivals the xylem in breadth and is not always easily distinguishable from it; it consists of sieve-tubes, parenchyma, and fibres. The secondary cambial cylinders characteristic of _Cycas_, _Encephalartos_, _Macrozamia_, and _Bowenia_, to which reference was made in the summary of anatomical features, arise in the pericycle, and a few layers of pericyclic parenchyma occur between adjacent extrafascicular cylinders of xylem and phloem. In a stem of _Cycas media_ 35 cm. in diameter examined by Worsdell there were 12 concentric cylinders. Matte[78] and Miss Dorety[79] have described partially flattened arcs of extrafascicular xylem and phloem in the hypocotyl of _Ceratozamia mexicana_. Worsdell[80] first drew attention to the occasional occurrence of short tracheids on the inner edge of the secondary wood and to the spasmodic development of cambial arcs in the tissue between the extrafascicular cylinders forming strands of inversely orientated xylem and phloem. More recent work by Matte gives support to Worsdell’s comparison between Medullosan stems and those of recent Cycads with inversely orientated arcs or concentric vascular cylinders. The French author draws attention to the close resemblance between the seedling stems of such species as _Encephalartos Barteri_ (fig. 396, K) and _Cycas siamensis_ (fig. 396, L) with their polystelic type of structure and the adult stems of _Medullosa_[81]. In the stems of _Dioon_, _Microcycas_, _Stangeria_, and _Zamia_ no extrafascicular cylinders are recorded. Two main vascular bundles enter the cortex from each leaf-base and in most stems these diverge right and left and more or less completely encircle the stele before passing through the medullary rays and joining the inner portion of the xylem of the stele either as double or single bundles. These girdle-bundles (fig. 396, H) first described by Karsten and Mettenius form a very characteristic cycadean feature[82]. Adjacent girdles are joined by connecting cortical bundles and, in addition, there are cauline collateral bundles in the cortex which form an anastomosing system. In some cases, _e.g._ species of _Macrozamia_ and occasionally in _Stangeria_, the female peduncle of a _Ceratozamia_, and in seedlings of _Bowenia_ and _Cycas revoluta_[83], the leaf-traces pursue a direct course from petiole to stele as in stems of Bennettitales. It is noteworthy that in seedlings of _Microcycas_[84], a genus characterised by a large number of male gametes—presumably a primitive feature—the leaf-traces are of the girdle-type. The two bundles at the base of a petiole by repeated subdivision give rise to the numerous collateral strands of the rachis. A leaf-trace in its passage to the leaf is like that of a Conifer in having the protoxylem on its inner edge, whereas in the petiole and elsewhere in the frond it is characterised by an arrangement of the xylem that has usually been described as mesarch. A typical vascular bundle from a cycadean frond is seen in fig. 399, C; by far the greater part of the xylem is centripetal, the centrifugal xylem being confined to an arc of scattered tracheids or a small strand separated by a few parenchymatous cells from the protoxylem.

[Illustration: Fig. 397. Tracheids from the stem of _Stangeria paradoxa_. (After Marsh.)]

[Illustration: Fig. 398. Pith-cast of a _Macrozamia_ stem, (⅖ nat. size.)]

[Illustration: Fig. 399. Sketches illustrating the changes in the structure of Cycadean vascular bundles in their course from stem to leaf: _cp_, _cf_, centripetal and centrifugal xylem; _p_, phloem; _px_, protoxylem. (After Marsh.)]

As considerable stress has been laid on the anatomical features of the cycadean foliar bundles in discussions on the affinities and phylogeny of certain Palaeozoic genera, it is important to consider the facts more closely[85]. French anatomists described the cycadean bundle as diploxylic on the ground that the centripetal and centrifugal xylems are distinctly different things, the centripetal xylem being primary—a relic of a former organisation—and the centrifugal xylem secondary and homologous with the normal wood of the cauline bundle. The term mesarch has in recent years been applied to the cycadean type of bundle. A mesarch bundle is, however, one in which centripetal and centrifugal xylem are alike in origin, both being primary structures derived from a desmogen strand. Typical mesarch bundles occur in several recent ferns; in the stele of the Osmundaceae, _Gleichenia_, and other genera; but in these plants the xylem is all produced directly from one primary desmogen region and there is no question of ‘primary’ and ‘secondary’ as in the two portions of the xylem of a cycadean bundle. Recent researches into the development of cycadean foliar bundles show that they do not conform to the mesarch type as generally understood. A leaf-trace at the base of a petiole (fig. 399, A) comprises centrifugal xylem only, and this consists of regular rows of tracheids separated by medullary rays: in the lower part of the petiole the structure is gradually modified, the centrifugal xylem is reduced and the formation of centripetal xylem is initiated. At a higher level (fig. 399, B) the centripetal xylem is in excess of the centrifugal and the latter, for a time connected with the former, eventually becomes separated by a few parenchymatous cells from the protoxylem and persists as a small strand or arc of tracheids. Fig. 399 illustrates stages in the transformation of a typical collateral bundle, at the base of a _Stangeria_ petiole, into one in which the xylem is almost wholly centripetal at a higher level in the axis of the frond. A cambium is present in all: in B the centrifugal xylem is more or less clearly differentiated into two portions, loosely arranged tracheids near the phloem, and the more compact groups abutting on the centripetal xylem: figs. C–E show a further reduction in the centrifugal tracheids. The conclusion drawn from developmental study is that the two xylem portions of the bundle are independent in origin[86]. Marsh has, however, shown that in _Stangeria_ bundles near the base of the petiole the centrifugal xylem consists of rows of secondary tracheids and an inner portion not in rows which connects the centrifugal with the centripetal elements; this connecting portion, he adds, is ‘probably primary and connects up the Cycadean foliar bundle with the truly mesarch bundle of the Cycadofilices.’

[Illustration: Fig. 400. _Cycas Micholitzii_. Vascular bundles in a forked pinna; _px_, protoxylem; _s_, sheath of thick-walled cells; _cf_, _cp_, centrifugal and centripetal xylem.]

In the xylem portion of the bundle from the midrib of a forked pinna of _Cycas Micholitzii_ shown in fig. 400 the centrifugal xylem elements are unusually numerous: the space between the two xylems is occupied by parenchyma and the whole strand is enclosed by a sheath of crystal-containing cells, _s_, with thick inner walls. Fig. 400, 1–4, illustrates the gradual change in the form of the bundle in the region of dichotomy[87]. The ground-tissue of the petiole is abundantly supplied with secretory canals and in the hypodermal region is a cylinder of stereome. In some petioles, _e.g._ _Macrozamia heteromera_[88], the ground-tissue cells are lignified and reticulately pitted, a feature met with in some Mesozoic cycadean leaves[89]. In _Cycas media_ Worsdell noticed a tendency of the leaf-trace bundles towards a concentric arrangement and similar vascular strands are recorded in the peduncle of _Dioon edule_, in various sporophylls[90] and in other cases. It is possible, as Worsdell believes, that the fairly frequent occurrence of concentric bundles in plants characterised by collateral bundles may have a phylogenetic significance.

The pinnae are dorsiventral and the veins exarch or pseudomesarch: secretory canals occur between (_Encephalartos_), above, or below the veins. The mesophyll of _Cycas_ is characterised by the presence of isolated xylem-elements passing from the midrib to the edge of the lamina and, as Lignier[91] suggests, these may be regarded as a reduced system of lateral conducting strands.

The epidermal cells of the leaflets have straight or slightly curved walls except in _Stangeria_ where they are undulate and fern-like[92]. The stomata, with few exceptions confined to the lower epidermis, are larger than in other gymnosperms (on the average ·075 × ·034 mm.) and are more or less depressed below the surface; the guard-cells are usually surrounded by 4–6 subsidiary cells.

The roots exhibit no feature to which attention need be called: the pericycle is several cells broad and as in the stem there may be extrafascicular cylinders of xylem and phloem.