Chapter XXXVI: Cycadophyta (1)

The term Cycadophyta, suggested by Nathorst[1069], is used in a comprehensive sense to include both recent Cycads and the much larger number of extinct types which it is customary to speak of as Cycadean plants or fossil Cycads. The designation ‘Cycads’ in the case of the majority of the fossil forms is, however, open to criticism on the ground that they differ too widely from existing genera to be associated with them in one class. It would be pedantic and inconvenient to give up the almost universal practice of extending the term Cycad beyond the limits defined by the characters of recent species. The important point is to adopt some classification which gives expression to our views as to the degree of affinity between recent and extinct types. In a considerable number of cases, especially impressions of presumably Cycadean fronds and stems that occur without any fertile shoots, it is impossible to determine the degree of relationship to modern types. It was with a view to a rational group-designation for such fossils that Nathorst proposed the term Cycadophyta, including in it the two classes Cycadales and Bennettitales. The Cycadales comprise the recent genera and such extinct types as may legitimately be included in the same class, but as we shall see later there are hardly any fossil species that can be assigned to this section on thoroughly satisfactory grounds. The term Bennettitales is used by Engler, Nathorst, and several other authors as a class-designation for a large number of Mesozoic Cycads agreeing in their more important morphological characters with the Lower Cretaceous stems on which Carruthers[1070] founded the genus _Bennettites_, placing it in a new tribe, the Bennettiteae. Some authors have followed Carruthers in the use of the family-name Bennettiteae for a subdivision of the Cycadales equal in rank to the Cycadaceae, while others, wishing to give greater emphasis to the difference between the extinct and recent plants, prefer to adopt the class-name Bennettitales. Carruthers regarded _Bennettites_ as occupying the same position in relation to other Cycads as _Taxus_ holds with regard to the cone-bearing members of the Coniferae. The adoption of Bennettitales is intended to convey the impression that the class is more distantly related to the recent Cycads than is implied by the analogy of _Taxus_. Nathorst[1071], as the result of his discovery of certain reproductive organs associated with some Rhaetic fronds described as _Dioonites spectabilis_, proposed a third subdivision, the Dioonitales, but he subsequently[1072] restored the fronds to their original designation _Nilssonia pterophylloides_, and on further examination found that the supposed microspore-bearing organs were seeds. _Nilssonia pterophylloides_ would therefore find a more natural place in the class Nilssoniales instituted by Thomas[1073].

BENNETTITALES.

=Cycadeoidea.= Buckland.

In 1827 Buckland[1074] proposed the generic name _Cycadeoidea_ for some petrified stems from the Purbeck beds in the Isle of Portland and published a description of two species, _Cycadeoidea megalophylla_ and _C. microphylla_. Brongniart[1075] considered Buckland’s term _Cycadeoidea_ inappropriate and proposed in its place _Mantellia_, the type-species being _Mantellia nidiformis_ Brongn., the Portland stem which Buckland a month or two later called independently _Cycadeoidea megalophylla_. Subsequently Brongniart[1076] withdrew _Mantellia_ as it had been previously used by Parkinson for a sponge and substituted _Cycadites_. Some years later Carruthers[1077] revived _Mantellia_ for a type of Cycadean stem from Portland though one species, apparently indistinguishable from those referred to _Mantellia_, he named _Bennettites portlandicus_. There is no adequate reason for the retention of the generic name _Mantellia_. The close resemblance of the short and thick stems (12–30 cm. in height) described by Buckland to those of some recent Cycads was recognised by Robert Brown and Loddiges and the former suggested to Buckland the inclusion of the fossils in a new family Cycadeoideae. It was this suggestion that led Buckland to adopt _Cycadeoidea_ as a generic name. In a later account of the Portland stems Buckland[1078], in deference to Brongniart’s opinion, substituted Brongniart’s name _Cycadites_ for _Cycadeoidea_. It is noteworthy that no reference is made in the original description to the occurrence of lateral shoots among the persistent petiole-bases that encase the Portland stems, but in a later account such shoots are represented in one of the figured stems and are compared with the buds occasionally produced on stems of _Cycas_[1079]. The subsequent researches of Carruthers[1080] demonstrated the reproductive nature of precisely similar lateral shoots in the stem on which he founded the genus _Bennettites_. The generic name _Echinostipes_ given by Pomel[1081], who had a passion for instituting new nomenclature, to Buckland’s Portland stems has not been adopted: his genus _Crossozamia_ proposed for certain stems and fronds was revived by Carruthers[1082] but has not been generally used. A further complication in the nomenclature of Cycadean stems was introduced by Saporta’s institution[1083] of _Bulbopodium_ and _Cylindropodium_: in the former genus he included the small ovoid stem figured by Lindley and Hutton as _Cycadeoidea pygmaea_[1084] and two French Jurassic species which might reasonably be assigned to _Cycadeoidea_. To _Cylindropodium_ were referred some large French stems from Jurassic strata: an examination of the type-specimens in Paris convinced me that they are typical forms of _Cycadeoidea_. As Ward[1085] has pointed out, both Saporta’s genera may be merged in _Cycadeoidea_. Fliche and Zeiller[1086] also include the small globular stems named by Saporta _Bulbopodium_ in the older genus _Cycadeoidea_: one such type from the Portlandian of Boulogne is described by these authors as _Cycadeoidea pumila_. Saporta also proposed the name _Platylepis_[1087], the type-species being _Cycadeoidea micromyela_ Mor., from the Lias of Calvados, which has recently been investigated by Lignier[1088] who wisely adopts Morière’s designation. Another unnecessary generic name is _Schizopodium_ given by Morière to a stem, _S. Renaulti_[1089], regarded by Lignier as indistinguishable specifically from _C. micromyela_.

The two names _Cycadeoidea_ and _Bennettites_ have been used by authors for stems which are unquestionably generically identical and as is often the case much confusion has been caused through the failure of palaeobotanists to arrive at an agreement. Lester Ward, a staunch advocate of the rule of priority, repeatedly pointed out that Buckland’s name _Cycadeoidea_ should take precedence of _Bennettites_ on the ground that stems for which these genera were instituted are clearly of the same type, and he added that the older genus, though abandoned by its author, cannot be given up without violating the inexorable rules of priority. On the other hand it has been urged that the genus _Bennettites_ as defined by Carruthers is characterised by the possession of (i) fertile shoots bearing strobili and (ii) vegetative organs exhibiting certain anatomical characters. Buckland’s species of _Cycadeoidea_, though bearing lateral shoots, are not well enough preserved to afford definite information as to the morphological features of the strobili, nor have we satisfactory data with regard to the degree of resemblance between the vegetative features of _Bennettites_ and the Portland stems. Carruthers laid stress on the elliptical section of the stele in _Bennettites_ in contrast to the cylindrical cylinder of Buckland’s _Cycadeoidea_ trunks. Subsequent research has shown that this difference is not in itself a valid criterion either of generic or specific rank but, as Wieland says, it is an open question to what extent the stem structure of _Cycadeoidea_ and _Bennettites_ agrees. The probability is that were our knowledge of the Portland stems less incomplete, they would be found to possess no anatomical features inconsistent with this generic union. Granting the correctness of this view, the adoption of the later generic term would be a reasonable course to follow on the ground that it stands for stems showing well preserved structure, while _Cycadeoidea_ was in the first instance applied to stems showing only partially preserved stumps of strobili, and the name was not retained by its author. Graf Solms-Laubach[1090] and some other authors have used _Bennettites_ for Cycadean stems possessing strobili of known structure such as those of _Bennettites Gibsonianus_, reserving _Cycadeoidea_ for similar stems but without strobili sufficiently well preserved to afford evidence of morphological characters. This practice I followed in 1895[1091], but my usage of the two generic names has not been consistent, the name _Cycadeoidea_ being afterwards employed[1092] in a more comprehensive sense. The investigation of the reproductive shoots of American Lower Cretaceous and Upper Jurassic Cycadean stems[1093] has demonstrated the practical identity of their ovulate strobili with those of the English _Bennettites_. It is clear that the American stems as well as numerous specimens from Italy and other European localities are generically inseparable from _Bennettites_. The adoption of _Cycadeoidea_ by Wieland, following Ward, has naturally strengthened the claim of Buckland’s genus at least so far as wide usage is concerned, and with some reluctance I propose to fall in with this terminology and for the sake of convenience to give up the use of _Bennettites_. Among Mesozoic Cycadean stems agreeing with those of recent genera in habit and in the presence of an armour of persistent leaf-bases are several which afford no evidence either of the occurrence of fertile shoots or of lateral shoots with terminal flowers. To such stems the name _Cycadeoidea_ has been applied, the designation _Bennettites_ being restricted to stems with lateral fertile shoots: this practice of treating the absence of reproductive shoots as a characteristic feature of _Cycadeoidea_ is regarded by Wieland as illogical and artificial; and if, as seems probable, he is correct in believing that the majority of the Mesozoic Cycadean plants culminated their vegetative period by prolific development of flowers, the absence of flowering branches would be contingent on a certain stage of development and not a generic character. Dr Stopes[1094] has recently published facts with regard to the anatomical features of Cycadean stems which have a bearing on the vexed question of nomenclature, but are more important from a morphological point of view as they indicate a closer agreement between certain types of Lower Cretaceous stems and those of _Cycas_ and other recent genera, in which successive rings of vascular tissue are developed, than has previously been recognised. In her diagnosis of _Cycadeoidea_ she includes the following statement: ‘In its internal anatomy the trunk shows two or more (up to eight are recorded) zones of secondary wood, the zones composed of distinct series of tracheids each more or less regularly arranged in radial sequence.’ It is claimed that the addition of this character constitutes for the first time a clear distinction between _Cycadeoidea_ and _Bennettites_. Dr Stopes states that the two stems on which Buckland founded the genus _Cycadeoidea_ are lost and adds that Buckland’s type has certain anatomical features which are not found in _Bennettites_. Buckland in his description of _C. microphylla_ states that there are ‘two laminated circles’ in the stem instead of the usual single cylinder, a character suggestive of _Cycas_. In the original figure of this species there are no indications of any lateral fertile shoots though, as Dr Stopes says, many of the Portland stems undoubtedly possessed such flowers. This author makes no reference to Buckland’s later description of _C. microphylla_: in this it is stated that the stem bears numerous buds rising from the axillae of petioles, and these are shown in the illustration[1095]. Without access to the actual specimen it is impossible to say whether or not the two ‘laminated circles’ described and figured by Buckland[1096] are two distinct cylinders or parts of one cylinder separated by the infiltration of some inorganic substance. In his description of _Cycadeoidea Yatesii_ Carruthers spoke of the occurrence of two cylinders of wood, and this was confirmed in a subsequent account of the type-specimen[1097]. Dr Stopes gives a fuller account of Carruthers’ type and re-confirm a the existence of two vascular cylinders; she also describes a new species, _C. buzzardensis_[1098] (fig. 578), in which there are 3–8 or more cylinders. Neither of these stems affords any evidence of the possession of fertile shoots; they agree closely with stems of the _Bucklandia_ type in their comparatively slender habit and differ in this respect from Buckland’s Portland species. The occurrence of more than one vascular cylinder in the stems _Cycadeoidea_ (= _Bucklandia_) _Yatesii_ and _C._ (= _Bucklandia_) _buzzardensis_ suggests the possibility that this feature was characteristic of other species included in _Bucklandia_.

It is clear that some at least of the stems referred to the genus _Bucklandia_ bore flowers of the _Williamsonia_ type[1099], and it is not improbable that the stems described by Dr Stopes as _Cycadeoidea Yatesii_ and _C. buzzardensis_ (fig. 578) possessed fertile shoots comparable with those of the Middle Jurassic species _W. gigas_. Dr Stopes’s contribution, while establishing a close agreement in anatomical features between some Lower Cretaceous stems and those of _Cycas_, does not warrant the further conclusion that these stems were in other morphological characters closely allied to modern Cycads. The main features of _Cycadeoidea_ may be summarised as follows: The principal trunk is generally unbranched (fig. 507) and identical in habit with some species of _Macrozamia_, _Dioon_, and _Encephalartos_ (cf. figs. 379, 382); in some species, _e.g._ _Cycadeoidea Marshiana_, _C. superba_[1100], _C. nana_[1101], the plant is represented by several approximately equal, thick, tuberous stems, in some cases easily separated from one another: a similar clustered habit is exhibited by certain forms of _Encephalartos_. The size of a _Cycadeoidea_ trunk varies from a few centimetres in length with a diameter of similar dimensions, as in _C. pumila_, to over a metre long as in _C. gigantea_ (fig. 535), or as much as 3–4 metres in _C. Jenneyana_ with a diameter of about half a metre. The surface is covered with persistent leaf-bases, exactly as in many recent Cycads, embedded in a thick mass of ramental scales which often stand out as a prominent reticulum, the petioles having partially decayed before the penetration of the mineralising solution through their harder tissues (fig. 507). On the conical terminal bud preserved in some stems (fig. 536) the foliage-leaves are replaced by linear scales. The leaf-bases often show the vascular bundles which form a simpler system than in the majority of recent species, their arrangement being, as Wieland says, more Fern-like; they form a series of collateral strands following the outline of the petiole-base[1102] with a U-shaped invagination in the middle of the upper face (fig. 517, A). Beyond the structure of the bundles at the base of the fronds and in the cortex of the stem our knowledge of the anatomy of the vascular supply of the rachises is very meagre. At the petiole-base each bundle consists either entirely of radial rows of centrifugal scalariform tracheids and medullary rays usually one-cell broad (fig. 519, B) or of centrifugal and centripetal xylem in varying proportions. The ground-tissue is well supplied with large secretory canals and in the larger leaf-bases there is a considerable development of periderm at the surface (fig. 517, B) as in recent Cycads. The ramenta formed from the epidermal cells consist in most species of fairly broad scales one-cell thick at the edges and broader in the middle; in _Cycadeoidea nigra_[1103] they are generally one-cell thick throughout and similar ramenta are common in _C. Gibsoniana_ (fig. 517, B). In _C. micromyela_ unicellular hairs replace the scaly ramenta, but transitional forms occur between hairs and scales. In _Williamsonia scotica_ (fig. 562) and in an Indian species of that genus the ramenta are exclusively long hairs as in recent Cycads, the scale-form of the ramenta in _Cycadeoidea_ being a Fern-character. The degree of development of the ramental tissue varies in different species; in _C. Stilwelli_ and _C. excelsa_ it is feebly developed while in _Cycadeoidea micromyela_ the ramenta almost cover the exposed leaf-base armour. The exceptional abundance of the ramental scales is a striking characteristic of some American stems referred to a separate genus, _Cycadella_[1104]. In the abundance of the ramental tissue, in the compact structure of the well protected cones, and in the thickly cuticularised epidermis of the bracts and leaves _Cycadeoidea_ exhibits xerophilous characters in a very high degree.

With very few exceptions the stems of _Cycadeoidea_ so far described afford no satisfactory evidence of the presence of more than one vascular cylinder in the main stem: in this respect _Cycadeoidea_ agrees with such recent Cycads as _Dioon_, _Ceratozamia_, and _Stangeria_. In the stem of C. _Jenneyana_ the secondary vascular tissue reaches a considerable thickness and shows signs of ‘rings’ in the xylem, but these are probably the result of some periodic interference with the uniform growth and not an indication of more than one xylem-cylinder. The secondary xylem (figs. 508, 509) consists only of centrifugal tracheids with some spiral elements on the inner edge; though manoxylic, _Cycadeoidea_ has more compact wood than that of recent Cycads; the medullary rays are 1–2 cells broad except near the perimedullary region where they are broader and the individual cells are tangentially stretched (fig. 508, B). The tracheids are scalariform, but in _C. micromyela_, an exceptional type, some of the xylem-elements have 1–2 rows of separate bordered pits (fig. 538). The phloem (fig. 518, B) is characterised by an alternation of thick-walled elements and thinner cells[1105]. From the main stele branches are given off to supply the flowering shoots in the form of a cylindrical stele like that of the primary axis, and each leaf-trace arises as a single bundle which, in the form of a U-shaped strand (fig. 519, A), pursues a straight course to the leaf-base (fig. 510) where it breaks up into several branches (fig. 538, B). Both leaf-trace and peduncle stele are given off from the lower edge of a medullary ray. In the parenchymatous cortex large secretory canals (fig. 518, B) are a conspicuous feature, and accessory cortical steles similar to those in _Cycas_ occasionally occur (fig. 511). The large pith consists of parenchyma and secretory canals, and internal periderm[1106] may be present; no medullary bundles have been discovered.

The correlation of the numerous fronds[1107] preserved in Mesozoic strata with their parent-stems is seldom possible. It is known that leaves of the _Zamites_ type were borne on stems (_Bucklandia_) agreeing with _Cycadeoidea_ in certain features but differing in the habit of the fertile shoots (fig. 542), and there is evidence that similar stems bore _Ptilophyllum_ and _Dictyozamites_ fronds[1108]; but only unexpanded leaves have been found in actual connexion with _Cycadeoidea_ stems. Wieland[1109] discovered young pinnate fronds, agreeing in the form of the pinnae with _Zamites_ and with some forms of _Encephalartos_, embedded in a thick mass of ramental scales in the terminal bud of a stem: the rachises were erect and the two-ranked pinnae imbricate and folded inwards (fig. 512), the vernation being like that of _Dioon_ and not circinate as in _Cycas_ and Ferns. The mesophyll of the leathery pinnae is differentiated into palisade and lacunar parenchyma, and the bundles are said to be ‘mesarch’ though on this point more information is desirable. Each bundle is surrounded by a sheath of thick-walled cells and the same tissue forms =I=-shaped girders as in similar recent leaves. In one species, _Cycadella ramentosa_[1110], the rachis of a young frond found among the leaf-bases had a broad U-shaped vascular strand.

In most _Cycadeoidea_ stems a characteristic feature is the occurrence of reduced leaves, or bracts, arranged spirally about a cone which sometimes projects slightly beyond the general level of the persistent leaf-bases, or the cones may be fully developed yet still more or less hidden within the armour of petiole-bases (fig. 517, C). These cones, or flowers, are borne at the apex of lateral axillary shoots, and it is characteristic of the genus that they never project more than a very short distance beyond the truncate stumps of the old leaf-bases. The axis of a flowering branch bears numerous linear, hairy, bracts (figs. 513; 514, _b_) which with their thick felt of ramenta constitute an efficient protective investment. The summit of a fertile shoot forms a rounded hemispherical cushion (fig. 514), or the receptacle may be more elongate and conical (fig. 513) and in some species pyriform[1111]. The flowers are generally bisporangiate, but the fact that in flowers with mature microsporophylls the ovules are small and apparently immature (fig. 513) makes it difficult to determine whether the megasporophylls are merely immature or functionless as in the male flower of _Welwitschia_ (cf. fig. 818). It would seem, however, that in most cases the flowers were bisexual[1112] (fig. 513). A remarkable feature is the enormous number of flowers on a single stem; in _Cycadeoidea Dartoni_[1113], 54 cm. long and 35 cm. broad, 500–600 flowers were counted on one side. On the other hand the large stem of _C. gigantea_ (fig. 536) shows no flowers. All the flowers on a single trunk are approximately in the same stage of development: it would seem, as Wieland points out, that after a vegetative period of some considerable duration the plant produced a large crop of flowers, and it is conceivable that as in _Corypha_ and some other recent Flowering plants this supreme effort set a limit to the plant’s existence. In the development of flowers from the old stem _Cycadeoidea_ affords a striking example of cauliflory.

The structure of the flowers is one of the most obvious differences between _Cycadeoidea_ and recent Cycads (_cf._ figs. 393, 394). The bisexual flowers of the fossil stems are comparatively small, not exceeding a few centimetres in length, like a hen’s egg or a medium-sized pear and in marked contrast to the male and female cones of modern Cycads (_cf._ figs. 393, 394). A verticil of pinnate microsporophylls is attached by a circular collar formed of the concrescent bases of the sporophylls to the lower portion of the receptacle; each pinnule bears several shortly-stalked synangia divided into loculi containing microspores usually with smooth walls and similar, except in their larger size, to those of modern Cycads (fig. 532). Sections of some microspores figured by Wieland[1114] show what appear to be cells in the spore-cavity, but they are larger than ordinary prothallial cells and their true nature is doubtful. We lack information both as regards the nature of the male gametes and the tissue formed on the germination of the spores. The free portions of the microsporophyll-whorl may consist of as many as 20 pinnate sporophylls, but the number is generally smaller; these are much longer than the ovulate part of the flower and in an immature state the ends of the sporophylls are bent inwards and downwards (fig. 513) between the bracts and the receptacle. After expanding and shedding the spores the whole male disc is thrown off leaving a narrow rim below the hemispherical or conical receptacle (fig. 514, _d_). The sterile distal end of a microsporophyll is generally slightly expanded and spathulate; in _C. colossalis_[1115] it bears a pair of wing-like appendages (fig. 533).

The upper part of the receptacle is covered with two kinds of organs which together form a layer of uniform depth; these are believed to be homologous, foliar structures; the majority are sterile and have the form of slender long and narrow appendages (fig. 514) each normally with a single axial vascular strand. These so-called interseminal scales increase in breadth in the apical region and form polygonal summits less than a millimetre in breadth or exceeding 2 mm. The low pyramidal apices of the interseminal scales give a mosaic-like appearance to the surface of the ovulate receptacle (fig. 515). In the lower part of the receptacle these sterile sporophylls are the only appendages, but over the greater part of the receptacle they are intermixed with a smaller number of similar appendages which bear a single terminal orthotropous ovule (fig. 514, _s_). Each ovule-bearing organ or megasporophyll (seed-stalk) is surrounded by 5—6 interseminal scales, and the narrow cylindrical micropylar tubes are readily distinguished from the sterile sporophylls in surface-view (figs. 516, 564). The seeds appear to be exalbuminous and the embryo is dicotyledonous (figs. 516, 521, 523)[1116]. The seeds are very small in comparison with those of living Cycads. The structure of the megasporophylls, both sterile and fertile, is described in more detail in the account of _Cycadeoidea Morierei_ and other forms. Fig. 516 represents a longitudinal section of one of the smallest seeds of _Cycadeoidea_, between 3 and 4 mm. long; an embryo occupies the greater part of the seed-cavity: the micropylar tube is formed of three layers, a strong inner palisade-layer, a thin middle layer, and an outer palisade-tissue, the interior of the tube being filled with parenchyma; at the shoulder of the seed above the root-end of the embryo the surface of the testa is characterised by 5–6 wings formed by the radial extension of palisade-cells. After the shedding of the spores and the abscission of the microsporophylls the flowering shoot probably increased slightly in length, thus pushing the ripening seeds beyond the ends of the surrounding leaf-bases. The ripe flowers were eventually cut off by an absciss-layer immediately below the receptacle (figs. 521, C, _a_; 522, _a_), large cup-like depressions being left on the surface of the stem (fig. 534). The ovulate cone on which the species _Cycadeoidea Morierei_ is founded probably represents the condition of a naturally detached flower of a _Cycadeoidea_. It is possible that the detached flowers freed from their encircling bracts may have been edible, the small seeds being dispersed by animal agency.

* * * * *

The splendid petrified stem, _Cycadeoidea etrusca_ Cap.[1117], one of the treasures of the Bologna Museum, was found on a tomb 20 miles west of that city where it was doubtless placed by the Etruscans who obtained it from the Upper Jurassic scaly clays in the Apennine Hills. It was in an imperfectly preserved flower of this fossil that Graf Solms-Laubach discovered some microspores, but it was not until Wieland’s examination of the more complete American stems that information was obtained as to the spore-bearing organs. Another Italian stem, _Cycadeoidea montiana_ Cap., was described in 1753 as a ‘congeries of barnacles[1118].’ The specimen named by Goeppert _Raumeria Reichenbachiana_[1119] was described in the middle of the eighteenth century as a mass of _Hippurites_ or coral cups: this was found in a swamp in Galicia and is now one of the most striking objects in the Dresden Museum; a brief account of it is given on page 409. In 1859 Tyson discovered two large trunks in the Potomac beds of Maryland for which Fontaine subsequently proposed the name _Tysonia marylandica_[1120], but as Ward pointed out the species is clearly a _Cycadeoidea_ (fig. 507). In 1894 Lester Ward[1121] recorded several additional stems from Tyson’s locality. It is, however, from the Black Hills of Dakota, an isolated spur of the Rocky Mountains, formed of older rocks encircled by Lower Cretaceous strata[1122], that the greatest number of Cycadean trunks have been obtained: the magnificent collection now in the Yale Museum is largely due to the energy and munificence of the late Prof. Marsh. From the Upper Jurassic beds in Carbon Co., Wyoming[1123], several stems have been collected, and a preliminary study of their external features led Ward to institute 20 species of a new genus _Cycadella_. Stems have also been discovered in the Freezout Hills of Wyoming and additional specimens have been found in the Potomac formation of Maryland. The discovery of over 1000 specimens of Cycadean stems in the Lower Cretaceous and Upper Jurassic beds of a few localities in the United States bears striking testimony to the abundance of these extinct Gymnosperms during the latter part of the Mesozoic era. It is perhaps true that, as Lester Ward wrote, ‘Cycads are to the vegetable kingdom what Dinosaurs are to the animal, each representing the culmination in Mesozoic times of the ruling Dynasties in the life of their age[1124].’ Although the number of stems obtained from European countries is relatively small, the abundance of specimens in the Upper Jurassic strata of the Isle of Portland and Northern Italy and their occurrence in Belgium[1125], France, Germany, Austria, Poland, India and elsewhere, together with an abundance of Cycadean fronds in practically all Jurassic and Lower Cretaceous plant-bearing beds, demonstrate the dominant position of the Bennettitales. The occurrence of the genus _Williamsonia_ in many European localities as well as in India, Afghanistan, and other countries, and the not infrequent occurrence of stems assigned to _Bucklandia_, _Yatesia_, _Cylindropodium_, and other genera furnish evidence of the rich development of the Bennettitales in later Jurassic and Lower Cretaceous floras. Wieland’s recent discovery[1126] of numerous Cycadean fronds, _Williamsonia_ flowers, and stems in Liassic rocks in Mexico shows that the group had already assumed an important position in the early part of the Jurassic period.

The memoir by Carruthers[1127] on British Cycadean stems contains the first account of the morphological features of Bennettitalean flowers based on petrified material. In 1891 Solms-Laubach contributed an important paper on the Bennettitean flower and several years later Lignier[1128] contributed additional data derived from a careful study of a well preserved strobilus[1129] from the Gault of Normandy. Wieland’s researches[1130] added very greatly to our knowledge, particularly with regard to the morphology of the microsporophylls. Among the earlier descriptions of the reproductive organs of the Bennettitales is Buckland’s account[1131] of a specimen from the Inferior Oolite of Charmouth, Dorset (fig. 560), which he referred to the genus _Podocarya_ (= _Williamsonia Bucklandi_[1132]): a thorough examination of the type-specimen, which unfortunately cannot be found, would probably furnish many important facts.

{ _Cycadeoidea_ (_Bennettites_) _Gibsoniana_ (_Carruthers_). { _Cycadeoidea_ (_Bennettites_) _Saxbyana_ (_Brown_).

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.

_Cycadeoidea (Bennettites) Gibsoniana._

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.

_Cycadeoidea (Bennettites) Morierei_ (Saporta and Marion).

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_.

A. Transverse section of the micropylar tube containing the apex of
the nucellus; _Ei_, inner epidermis; _Tf_, ground-tissue; _e_,
outer epidermis with the thickening of the walls shown in a few of
the cells.
B. Transverse section of the upper part of the micropylar tube;
lettering as in fig. A.
C. Transverse section at the level of the wings formed by the fibrous
layer and corresponding to the angles of the seed, approximately at
the level _cp_ in fig. 525; _cn_, nucellar cavity; _Ei_, inner
epidermis of seed-coat; _cf_, fibrous layer of wings, _f_, which
extend across the fleshy layer, _tch_, to the radial layer _ar_
(_cf._ fig. 525); _at_, tubular layer; _Ee_, epidermis of adjacent
scale detached from the other tissues, _ase_, along the line of
fracture _d_; _EE_, epidermis of two adjacent scales.
D. Transverse section of peduncle; _tr_, tracheids; _ac_, coloured
subepidermal layer; _Et_, tubular epidermis, double in places;
_EE_, epidermis formed from neighbouring scales. (From Prof.
Lignier’s drawings; A, B, D, × 118; C, × 90.)]

_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.’

The letters _a_, _b_, _c_, in this figure correspond to _cp_, _cf_, and _ar_ in figs. 525, 526.]

_Cycadeoidea dacotensis_ (McBride).