Fossil plants, Vol. 3

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, 1a; 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.

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, 1d) 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, Ia, 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].

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].

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.

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.

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.

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].

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, Ib).