These two species serve to illustrate the type of stem for which Carruthers instituted the tribe Bennettiteae and the genus Bennettites. Bennettites Gibsonianus is the most important of the five species described by Carruthers[1133], as it was from its fertile shoots that information was first obtained as to the nature of the ovulate strobili of the Bennettitales. B. Saxbyanus[1134], originally described as Cycadites Saxbyanus from a specimen found by Mr Saxby at Bonchurch in the Isle of Wight and represented by Wealden examples from Brook Point, is chiefly interesting for the clear preservation of the anatomical features of the stem. Three other species were also described by Carruthers; they are: Bennettites maximus Carr., a large stem similar to B. Saxbyanus, in the Museum of the Geological Survey; B. portlandicus from the Lower Purbeck of the Isle of Portland, in the collection of the Geological Society; and B. Peachianus, a piece of a compressed stem, in the British Museum, from the Upper Jurassic of Helmsdale in N.E. Scotland.
This species was founded on a petrified portion of a large stem of Lower Greensand age discovered by Mr Gibson in Luccomb Chine in the Isle of Wight: the type-specimen is represented by pieces of the original block in the British Museum and in one of the Museums at the Royal Gardens, Kew. The following description is based partly on the published accounts and in part on an examination of sections in the British Museum, the Manchester University Museum, and in Dr Scott’s collection.
The elliptical form of the stem and vascular cylinder as seen in transverse section, regarded by Carruthers[1135] as a feature characteristic of the genus, has no morphological significance and is in part at least due to compression. In the large pith, the armour of persistent petiole-bases separated by dense ramental scales (fig. 517, A, B), and in habit, Cycadeoidea Gibsoniana agrees generally with the stems of many recent Cycads, but the resemblance of the vegetative organs is in marked contrast to the differences exhibited by the reproductive shoots. The pith consists of parenchyma with scattered secretory ducts but no medullary vascular bundles. In the pith of Cycadeoidea Peachiana there are patches of tissue superficially resembling vascular strands, but these are probably bands of internal phloem like those described by Solms-Laubach[1136] in some Italian stems. In none of the English stems are there any clear indications of the occurrence of more than one cambium in the stele. The secondary xylem is entirely centrifugal with some smaller crushed elements, presumably protoxylem, at the inner edge where the medullary rays are especially broad. The xylem is of the manoxylic type (fig. 518, A) as in recent Cycads; though the medullary rays, 1–2 cells broad, are rather smaller than in recent species. The tracheids are scalariform as in Stangeria (fig. 397). As in recent Cycads there is a broad cylinder of secondary phloem (fig. 518, B)[1137] composed of alternate layers of thick-walled and thinner elements—sieve-tubes and parenchyma: traces of lateral sieve-plates occur on some of the elongated elements. Each leaf-trace arises as a single strand from the lower edge of a mesh formed by the large inner end of a medullary ray: on emerging into the inner cortex the trace has the form of a U-shaped strand (fig. 519, A, lt) which passes direct to the petiole, following a steeply ascending course in Cycadeoidea Saxbyana and almost horizontal in C. Gibsoniana. Before entering the base of a leaf the trace breaks up into several collateral strands and these form a simple pattern as seen in a tangential section of the leaf-bases (fig. 517, A, C), the central bundles on the upper side forming a U-shaped involution. There is no indication of any girdling of the foliar bundles. The arrangement of the petiolar bundles is simpler and more Fern-like than in the majority of existing Cycads. Each vascular bundle consists in the petiole-base mainly of centrifugal secondary xylem and medullary-ray tissue (fig. 519, B); a group of centripetal tracheids is usually recognisable internal to the protoxylem: the structure is of the mesarch type with a variable amount of centripetal xylem, and agrees generally with that in recent Cycads.
The comparatively narrow cortex is composed of parenchyma with scattered secretory sacs (fig. 518, B, s), and occasionally an elliptical vascular strand (fig. 511) is present which is probably cauline as are the similar strands in Cycas. The persistent petiole-bases are covered with ramental scales which form a dense interfoliar packing: these frequently consist of a single layer of fairly thick-walled cells or, as seen in transverse section, of spindle-like scales one-cell thick at the edges and 2–3 cells broad in the middle (fig. 517, B).
The presence of fertile shoots, presumably axillary, is one of the most striking features of Bennettitean stems. The branching is monopodial and not sympodial as in most recent Cycads. The nearest approach to the method of branching in Cycadeoidea is afforded by some stems of Macrozamia recently described by Chamberlain[1138]. It is not improbable that some of the flowering branches of Cycadeoidea were branched. Solms-Laubach[1139] states that he observed certain characters in the secondary axes of Cycadeoidea Gibsoniana which led him to suspect that there may have been fascicled systems of fertile shoots emerging in a body or in close proximity to one another between the leaf-bases of the stem. An example of a branched flowering shoot is described in Williamsonia scotica[1140]. A fertile shoot agrees in structure with the main axis and Scott[1141] states that the phloem is particularly well developed, a feature by no means unusual in fertile branches. These lateral shoots (fig. 514) bear numerous linear bracts each with three collateral vascular bundles, and ground-tissue composed of thick-walled cells characterised by scalariform pitting (fig. 520): secretory sacs are abundant. The hypodermal stereome is especially developed on the inner face of the bracts. The apex of a lateral shoot has the form of a rounded cushion (figs. 514; 521, A, C) similar to the receptacle of many Composites, and on this are borne the sporophylls. It is characteristic of Cycadeoidea that the flowers project very slightly beyond the surface of the stem and the peduncles are not exposed except in tangential sections through the leaf-base armour (fig. 517, C, 1, 2). On the fall of the flower or ripe ‘fruit,’ which is effected by an absciss-layer (figs. 521, C, a; 522, a), a cup-like scar is left on the stem (cf. fig. 534). This method of flower-production suggests comparison, mutatis mutandis, with the phenomenon of cauliflory in certain recent Flowering plants; it is one of the distinguishing features between Cycadeoidea and stems bearing longer fertile shoots with flowers of the Williamsonia type.
Fig. 517, C, shows a tangentially cut surface of a portion of the stem of Cycadeoidea Gibsoniana with two axillary fertile shoots; one, 1, is cut across below the receptacle and shows the axis surrounded by bracts while the other, 2, is seen at a higher level, above the receptacle, where the section has exposed the numerous sporophylls. The rounded surface of the receptacle is covered with a dense cluster of long slender appendages, seed-stalks and interseminal scales, the latter being much more numerous than the former (fig. 521, A, B). These organs are believed to be homologous foliar structures, the seed-stalks being megasporophylls and the interseminal scales abortive or potential sporophylls (see also figs. 562, 563). Fig. 514 shows the form of a single flower from an American stem closely allied to Cycadeoidea Gibsoniana.
The megasporophylls are more or less polygonal in transverse section: there is a central concentric vascular strand surrounded by a thick cortex (fig. 527): at its upper end the sporophyll bears a single orthotropous seed containing a dicotyledonous embryo (figs. 521, D, E; 523). The vascular strand pierces the base of the testa and expands to form a shallow cup of tracheal tissue in the chalaza; there are no bundles in the single integument. The testa (fig. 521, D, t) consists of three regions, a median layer of rather large rectangular or palisade-cells with an inner and outer tissue composed of much smaller cells. The testa is prolonged distally as a slender cylindrical column or micropylar tube at the base of which it becomes broader owing to the increase in breadth of the middle or palisade layer. A nucellar beak projects as a cone into the base of the micropylar tube. No pollen-chamber has been found. It is noteworthy that the micropyle is closed in the ripe seeds. Internal to the testa there is a crushed membrane separated from the embryo by a space (fig. 521, D, sp): this is the remains of the nucellus and, as Solms-Laubach points out, there is no proof that any endosperm was present in the ripe seeds[1142]. The embryo consists of a short axis, the conical radicle and the very short apex of the epicotyl, also two equal cotyledons each with a few vascular bundles (fig. 521, D). The long interseminal scales, as seen in transverse section in the lower part of a flower between the sporophylls, appear as compressed polygonal organs (fig. 521, B, i) with an axial vascular strand surrounded by parenchyma and limited by a strong epidermis; they pass up between the seed-stalks, m, and in the distal end become considerably enlarged (figs. 514, 515), gradually expanding to form a truncate or slightly pyramidal apex (figs. 553, 563). The swollen peltate apices of adjacent scales form a continuous covering to the flower interrupted, except in the lower sterile part of the flower, by symmetrically disposed cylindrical micropylar tubes (fig. 515). The peripheral interseminal scales form a homogeneous parenchymatous tissue which springs from below the edge of the receptacle (fig. 521, A, B, pr) and the individuality of the scales composing this ‘pericarp’ is indicated by occasional invaginations of the epidermal layer which marks the boundary of the polygonal areas. The structure of the megasporophylls and scales is more fully described in the case of Cycadeoidea (Bennettites) Morierei[1143].
The flowers of Cycadeoidea Gibsoniana appear to be unisexual and ovulate: in view of the discovery by Wieland of numerous bisexual fertile shoots on American species of Cycadeoidea it would be reasonable to regard the apparently unisexual flowers of the English species as originally bisexual but preserved at a stage subsequent to the loss, by abscission, of the disc of microsporophylls. Fig. 514 shows a flower of an American Cycadeoidea practically identical with those of C. Gibsoniana, but the remains of the staminate disc are clearly seen at d below the swollen apex of the flowering axis. In the photograph of half of the same region in C. Gibsoniana reproduced in fig. 522 there is no indication of any similar trace of a whorl of microsporophylls. Admitting the fact that a shrivelled remnant of the persistent base of a whorl of microsporophylls might easily escape observation, it is difficult to believe that any fertile leaves ever existed in the flower represented in figs. 521, 522. It is equally difficult to regard the specimen represented in fig. 561 as other than a true unisexual (ovulate) flower.
The name Bennettites was adopted by Lignier for this species which was founded on a detached flower from the Gault[1144] of Vaches-Noires, Normandy. It was first described by Morière[1145], then by Saporta and Marion[1146], who named it Williamsonia Morierei, and it has since been thoroughly investigated by Lignier[1147]. There is no evidence as to the nature of the parent-stem though Morière suggested a possible connexion with Zamia Brongniarti Mor. (figured by Saporta[1148] as Fittonia Brongniarti) from the same locality. There can be no reasonable doubt that Bennettites Morierei was borne on a lateral branch of a stem of the Cycadeoidea type: it is constructed on essentially the same plan as the flowers of Cycadeoidea (Bennettites) Gibsoniana, and in both cases there is no indication of the presence of microsporophylls. The type-specimen is 5·5 cm. long and 3·5 cm. broad, ovoid, and characterised by a depressed cushion-like receptacle as in Cycadeoidea Gibsoniana. The enveloping bracts with their ramental scales agree generally in structure with those of the English species and, except as regards the ramenta, with Williamsonia scotica: numerous stomata occur on the lower surface; the ground-tissue consists of thick-walled parenchyma and the narrow pit-canals simulate the scalariform bands in Cycadeoidea Gibsoniana (cf. fig. 520). The pitted sclerous cells in the bracts of W. scotica are of the same type. There is an anastomosing system of secretory canals, also several vascular bundles like those in C. Gibsoniana but more numerous; the latter are composed of a group of phloem-elements abutting externally on fibres, a well-defined cambium, and radially disposed scalariform tracheids: internal to the protoxylem is a group of elements considered by Lignier to be centripetal xylem. From the branching and slightly divergent course of the bundles in the upper part of the bracts Lignier concluded that these organs represent the basal portions of leaves originally provided with a terminal limb. It may be that the small lateral appendages to some of the bracts of Williamsonia scotica (fig. 561, l) afford support to this view.
Megasporophylls (seed-stalks and seeds). These organs, 3–4·5 cm. long and approximately 1·5 mm. in diameter, are in most cases imperfectly preserved. In transverse section and at a level of 1 cm. above the receptacle a stalk bearing an atrophied seed shows the following features: an epidermis with very thick internal walls encloses a parenchymatous ground-tissue with an axial conducting strand. At a higher level the epidermal cells have walls of uniform thickness, and a hypodermal layer of cells with coloured contents is differentiated from the ground-tissue (fig. 524, D, ac). As the seed-base is approached the epidermal cells tend to separate from one another and divide longitudinally, the compact epidermal layer being replaced by an envelope of tubular, dissociated, cells (fig. 524, D, Et). Similar tubular elements occur in the seed-stalks of Cycadeoidea Gibsoniana. A fully developed seed-stalk bearing a complete seed cut across in the middle region shows the following features: a concentric vascular strand surrounded by thin-walled parenchyma and the coloured hypodermal layer (fig. 524, D, ac), the whole being enclosed in the tubular envelope of epidermal origin (Et) which is more strongly developed than in the stalks of imperfect seeds: there may be as many as 10–12 tubular cells on one radius. When traced downwards towards the receptacle the tubular envelope decreases in breadth, though the cells become more numerous and smaller, until in the immediate neighbourhood of the receptacle the tubular tissue is transformed into a compact parenchyma of large cells each of which corresponds to a group of tubes formed by the septation of the cells. Traced upwards this thin-walled parenchyma gradually passes into thick-walled tubes, and near the seed-base the tubular envelope is reduced to two layers, an inner consisting of relatively small cells with sinuous radial walls (the folded layer of Lignier) and an outer tubular layer. Lignier describes an interesting abnormality, a bifid seed-stalk enclosed in a common epidermis which he compares with the occasional branching of the seed-stalks of Ginkgo biloba.
Seeds. The seeds (figs. 525, 526), 6–7 × 2·5–3 mm., are tetragonal or pentagonal in the upper half (fig. 527, 1, 2), the angles being formed by thick but not very prominent wings of tissue (fig. 524, C, cf); they are orthotropous and have a single integument (figs. 525, 526). The tubular layer forming the outer portion of a seed-stalk near the seed-base is prolonged over the surface of the testa as a discontinuous covering in the form of isolated or small groups of tubes, giving a striated appearance to the seeds. This layer though apparently a part of the seed is derived from the neighbouring interseminal scales of which it is the epidermal layer; it consists of elongated cells and scattered stomata[1149]. The folded layer persists only in the lower part of the seed, being replaced by a layer of radially extended cells (radial layer; ar, figs. 524, C; 525, ar; 527, c) in the upper region of the seed. In the micropylar region both the tubular and folded layers undergo further change; the external, tubular, layer forms a kind of epidermis (at, figs. 524, 525), the subepidermal layer, consisting of the radially elongated cells (figs. 524, 525, ar; 527, c). The superficial layer assumes a different aspect in the micropylar region, its cells being thicker walled, as are also those of the subepidermal layer (fig. 524, A and B). The micropylar canal (figs. 524, 525, cm) is cylindrical in the lower part but at the apex is reduced to a long and narrow slit bounded by an internal epidermis of radially stretched cells which in the lower portion of the tube are thinner walled and isodiametric. The rest of the testa is differentiated into two regions; an outer fleshy region immediately internal to the folded (or radial) layer and an inner fibrous region next the nucellus, which is one-layer broad between the wings but opposite the wings it extends radially outwards across the fleshy tissue to the radial layer (figs. 524, C; 525; 527): in the winged portion of the seed this tissue forms the inner fibrous portion of the wings but in the lower part of the seed below the wings it forms a single layer of uniform breadth finally spreading out as a basal cup in the chalazal region where it is pierced by the vascular strand. The fleshy portion of the testa forms one layer in the proximal part of the seed and becomes several layers wide between the fibrous wings in the upper part. This fleshy tissue appears to be derived from the coloured, subepidermal, layer of the seed-stalk, while the internal parenchyma is regarded by Lignier as the equivalent of the fibrous layer of the testa. In the micropylar tube the fibrous layers are replaced by 2–3 layers of sclerous cells (fig. 524, A, B). The testa has no vascular supply: the concentric strand of the seed-stalk passes through the fibrous tissue at the base of the seed and reaches the base of the nucellus (fig. 525). The nucellar apex extends into the lower part of the micropyle (fig. 525, n), and in some cases Lignier noticed an axial canal formed by the breaking-down of the cells which abutted below on a cavity above the embryo, probably the remains of a pollen-chamber (figs. 525, 527). No microspores have been found. Two dark spots shown at co, fig. 525, may represent archegonia but this is doubtful, especially as the seed contains a well-developed embryo. The nucellus is free from the testa only in the apical region and a dicotyledonous embryo occupies the interior without any trace of endosperm. Lignier points out that in some seeds containing embryos the nucellar beak is not completely perforated: in this fact and in the absence of microspores in the micropylar canals he is inclined to see evidence of parthenogenesis[1150].
In several respects the seeds of Cycadeoidea agree with those of Gnetum: reference should be made to the account of the seed of Gnetum africanum in Chapter lii. and to the papers referred to in the footnote[1151].
Interseminal scales. The young seed-stalks agree very closely with the interseminal scales: each seed-stalk is surrounded by 5–6 scales (fig. 527) as in other Bennettitean flowers (fig. 564). For the greater part of their length the interseminal scales are compressed, but above the seeds, where they are free from pressure (fig. 526), they become much thicker and form a covering (‘pericarp’) as in Cycadeoidea Gibsoniana. In its upper region an interseminal scale consists of an epidermis with strongly thickened inner walls, hypodermal thick-walled cells and parenchymatous ground-tissue with a single axial bundle. In the lower part the scale is more flattened and the thick-walled hypoderm is replaced by thin-walled parenchyma. Some of the scales at the periphery of the receptacle where there are no seed-stalks are broader and may have six vascular bundles; this, Lignier suggested, might be regarded as evidence of the reduction of the interseminal scales from leaves possessing a terminal limb; but a further examination of scales at the periphery of the flower led him to the conclusion that the distal swelling of the scales is solely due to the hypertrophy of conjunctive tissue and is not the result of the modification of a reduced limb[1152]. The morphological value of the interseminal scales and seed-stalks has not been definitely settled, though the probability is that they are homologous organs and foliar. Solms-Laubach[1153] suggested that both may be axial, the seed-stalks representing axes ending in a flower reduced to a single ovule; or, he adds, the seed-stalks may just as well be carpels, though in that case we should have the unusual phenomenon of terminal seeds. The interseminal scales may be aborted seed-stalks crushed between the latter; or if the seed-stalks are axes, the scales may be foliar. He is inclined to see in the scales the bracts and prophylls of seed-stalks to which must be added such bracteoles, preceding the seed or flower, as may happen to spring from the seed-stalks. Pearson[1154], on the assumption that the seed-stalks are axial structures, institutes a comparison between Welwitschia and Bennettites and regards each flower of Welwitschia as a much reduced Bennettitean strobilus. Lignier believes the interseminal scales to be leaves borne on the swollen apex (receptacle) of an axis of the second order, while the seed-stalks are fertile leaves of a unifoliar bud of the third order possibly axillary though not necessarily so to the interseminal scales. My own view, influenced by the examination of the immature flower of Williamsonia scotica, is that the seed-stalks (megasporophylls) and scales are homologous, the former being sporophylls and the latter sterile foliage leaves, the whole flower, as Wettstein[1155] says, consisting of a conical axis bearing numerous fertile and sterile carpels enclosed by a perianth of bracts. Worsdell[1156], who shares Čelakovsky’s opinion that sporophylls were originally radially symmetrical organs bearing a terminal sporangium, regards the flowers of Cycadeoidea Gibsoniana and other species as more primitive than those of recent Cycads: he does not see any justification for the view that the Bennettitalean flowers are in advance of those of existing Cycadean plants as regards a supposed tendency towards the Angiospermous type. He maintains that Bennettites ‘shows absolutely no indication of such an advanced structure in its essential organs, the sporophylls, which remain primitively radial in structure, bearing the ovules in a terminal position.’
McBride[1157] first described this Lower Cretaceous species from the Black Hills of South Dakota as Bennettites dacotensis, the generic name Cycadeoidea being adopted by Ward[1158] who distinguished some of McBride’s specimens as Cycadeoidea McBridei. The stem is elliptical in section, 32 cm. long and 45 cm. in girth: owing to the partial decay of the petiole-bases the ramental reticulum forms a prominent feature. Numerous flowers, all of which are approximately at the same stage of development, project like conical buttons above the general level of the stem-surface[1159]. The bisporangiate flowers consist of a conical receptacle bearing interseminal scales and megasporophylls, the whole being surrounded by spirally disposed bracts (fig. 529). A whorl of 18 or 19 nearly mature microsporophylls is attached to the base of the receptacle (figs. 528, 530); each microsporophyll has a strong rachis extending beyond the apex of the flower-axis and bent inwards and downwards with the distal end tucked between the ascending rachis and the receptacle. The slender pinnules, in two alternate series, are bent downwards and bear synangia in rows. A transverse section just below the ovulate portion of the cone shows a continuous ring of tissue encircling the receptacle with vascular bundles parallel to the surface (fig. 530, A, m); at a higher level the bundles fall into groups preparatory to the breaking up of the disc into separate microsporophylls. Immediately above the apex of the central cone the coherent basal portion of the verticil of sporophylls is replaced by the separate rachises which in section have the form of isosceles triangles (fig. 530, B). Each microsporophyll is approximately 10 cm. long; the longest pinnule being 1·5 cm. in length and bearing two lateral series of synangia, 10 in each row. At maturity the microsporophylls probably spread out and the whole whorl was thrown off leaving an annular rim (fig. 514, d) such as is often seen at the base of older ovulate strobili. The immaturity of the ovules in this (fig. 528) and other specimens led to the suggestion that the strobili of Cycadeoidea were protandrous. The synangia (fig. 531) are several times broader than long and similar in size to those of the Fern Marattia. In each synangium are two rows of elongated loculi (fig. 532) containing oval microspores usually with a smooth exine and rather larger than those of recent Cycads. The synangium-wall is composed of a palisade-layer of thick-walled cells and a layer of smaller and thinner cells: the palisade-layer is narrowest at the apex where dehiscence occurs and broadest at the base where the hypodermal tissue is more abundant and forms a short thick pedicel. The two rows of loculi are bounded by flattened cells and there are 10–20 loculi in each of the two rows: dehiscence of the individual loculi occurs in the middle of the inner wall.