Heterangium Grievii has a radially symmetrical stem bearing compound leaves with decurrent petioles which give to the otherwise cylindrical axis an angular outline as seen in transverse section (fig. 411, A). The phyllotaxis appears to be ⅜. The stem rarely exceeds 1·5 cm. in diameter: in the centre is a comparatively large stele consisting in young stems of primary xylem and phloem, but in older stems these are separated by a cylinder of secondary vascular tissue which in this species is always narrower than in Lyginopteris oldhamia and, as Williamson pointed out, often of unequal thickness on different radii. The medullated stele of Lyginopteris is replaced by a solid xylem-cylinder consisting mainly of groups of large tracheids, reaching ·3 mm. in diameter, with multiseriate bordered pits (fig. 411, D) embedded in an anastomosing parenchymatous tissue-system. In the stele reproduced in fig. 411, B, which with the exception of a very narrow zone of secondary xylem, x2, consists entirely of primary xylem, x1, the parenchyma is represented by a darker reticulum (cf. fig. 415, B) dividing the metaxylem into islands as in Gleichenia. In the peripheral portion of the xylem the tracheids are rather narrower and arranged in more definite groups in many of which is a single strand of narrow spiral elements (fig. 411, A′, px) close to the outer margin. These peripheral primary bundles in which protoxylem is recognisable may be described as leaf-traces of mesarch structure consisting of centripetal xylem and, to a much less extent, of smaller centrifugal elements for the most part with dense spiral bands in place of the multiseriate pits of the rest of the metaxylem. The structure of these leaf-traces is practically identical with that of the primary bundles of Lyginopteris. There is, however, a difference to which attention is drawn by Williamson and Scott. While in Lyginopteris in any transverse section the primary bundles in the stele are equal in number to the leaf-traces in the pericycle and cortex, in Heterangium the peripheral groups in the stele may be as many as twenty, a number considerably in excess of the leaf-traces beyond the limits of the primary xylem of the stele. It may be that the leaf-trace of each leaf, which joins the stele at a distance of 6–10 internodes below its entrance into the cortex from the leaf-stalk, may branch in its descent in the axial region, or some of the primary groups of xylem may be confined to the axial region and independent of the leaf-traces. Portions of the peripheral region of the stele may be occupied by metaxylem groups without protoxylem and identical with those which make up the bulk of the metaxylem.
Scott[216] has recently published a note in which he states that most of the British Coal Measures Heterangiums were polydesmic. Two bundles, and not a single strand as in the Scotch H. Grievii, leave the stele for each leaf, and these divide into four, in some cases at least, before entering the petiole.
The secondary xylem is continuous at its inner edge with the outermost primary tracheids (fig. 411, A′) and consists of rows of tracheids, 1–3 elements broad, alternating with numerous broad medullary rays of radially elongated parenchyma. Beyond a typical cambium-zone the secondary phloem consists of parenchyma and sieve-tubes bounded by crushed arcs of primary phloem. Abutting on the phloem is a pericycle composed of several layers of small parenchymatous cells (fig. 411, A, p) and in the outer layers of this tissue a phellogen (fig. 411, C, p) and some periderm are usually present though, as Williamson and Scott point out, the periderm is less regular and narrower than in Lyginopteris. The inner cortex, composed of short parenchymatous cells, is traversed by numerous narrow bands of dark, thick-walled cells similar in the structure of the elements, though peculiar in the horizontal elongation of the groups, to the sclerous nests in the pericycle and pith of Lyginopteris. These characteristic bands are chiefly seen in the oblique longitudinal section of a stem represented in fig. 412. In this section, 25 mm. in length, the lighter band, p, is the pericycle and in it a few obliquely cut leaf-traces are shown as dark patches. The horizontal bands are similar in structure and shape to the diaphragms of thick cells in the pith of Abies magnifica[217], and in both plants they probably serve as supports to the softer parenchyma. There may be as many as 46 bands in a vertical length of cortex of 1 inch (about 19 per centimetre). It was the occurrence of precisely similar transverse lines on the carbonised impressions of the rachis of Sphenopteris elegans that led Kidston[218] to suggest a connexion between that species and the stem of Heterangium Grievii.
The outer cortex, consisting of alternate strands of parenchyma and stereome similar to that of Lyginopteris, is much narrower and a less conspicuous feature than in Heterangium; the stereome bands do not form so regular a hypodermal network and extend much further vertically without anastomosing. The epidermis has been described as a layer of fairly thick cells showing in one case an appearance of a depressed stoma[219]. There are no secretory canals like those of Cycads but, as in Lyginopteris, scattered cells with dark contents in the stem-tissues probably represent secretory sacs.
The leaf-traces on leaving the stele pursue a very gradually ascending course to the petiole; they retain their collateral structure in the pericycle and cortex and have no secondary xylem, but become concentric as they enter the base of a leaf.
Before passing to the description of the leaves, the more striking features in the stem may be summarised with reference to the diagrammatic sketches shown in fig. 411. Fig. 411, A, represents a section of Heterangium Grievii approximately 2 cm. in its maximum diameter; at the periphery of the primary xylem, x1, and close to its outer margin are several protoxylem groups, not shown in the drawing, each of which marks the position of a mesarch trace. The zone of secondary xylem, x2, is interrupted by the exit of leaf-traces and one of these is seen at a in fig. 415, A, separated from the central primary xylem by a foliar gap filled with parenchyma. The pericycle is shown at p in fig. 412 and its outer boundary at p in fig. 411, A. Beyond the pericycle is the broad parenchymatous cortex with leaf-traces, lt, and some sclerenchymatous patches, s. The vascular strand a is passing into the base of a leaf-stalk. In the stem shown in fig. 411, B, 1·4 cm. × 7 mm., a decurrent petiole is seen at the upper end with its single vascular strand, a, and two sclerous nests; a similar though detached leaf-base occurs at the opposite end of the long diameter. Other leaf-traces are seen at b and c. From the left-hand side of the stele a curved strand of tracheids is passing out to supply a root, r.
Adventitious roots of endogenous origin are occasionally met with in Heterangium stems, but we have less information as to their anatomy than in the case of Lyginopteris. In a specimen of Heterangium Lomaxi figured by Williamson and Scott[220] three roots are seen in a vertical series growing outwards through the cortex of a stem. The roots agree generally with those of Lyginopteris but the outermost cortical layers possess no special features.
The large compound fronds long known as Sphenopteris elegans were recognised by Kidston as the leaves of Heterangium by the closely arranged transverse striae or narrow ribs on the rachis and pinnae which are the expression on the carbonised impressions of the horizontal plates of sclerous tissue in the petrified stems and petioles of Heterangium. The dichotomously branched fronds are included by Stur in his genus Diplotmema and that author figures several typical examples in his ‘Culm Flora’[221]. Fig. 413, A, shows a forked axis with the bases of more slender branches and the characteristic transverse bands and in fig. 413, B, part of a pinna is reproduced. In general appearance, except in the bifurcating pinnae, the fronds resemble those of Davallia tenuifolia with which Brongniart compared the Palaeozoic species. There is little doubt that Sphenopteris dissecta and some other species were also borne on Heterangium stems. The rachis and petioles differ from those of Lyginopteris fronds in the absence of emergences (cf. fig. 404, E). The petioles (fig. 411, B, a) have a single concentric vascular bundle with internal protoxylem.
As yet no satisfactory evidence has been published with regard to the nature of the microsporangia but in all probability these were constructed on the same plan as those of Lyginopteris. There is a strong prima facie case for assigning the seed Sphaerostoma to Heterangium: absolute proof of organic connexion is still lacking though Dr Benson’s recent account of the seeds associated with Heterangium Grievii almost amounts to demonstration of continuity between vegetative organs and seeds.
In 1877 Williamson described some detached petrified seeds from the Lower Carboniferous rocks of Fifeshire, Scotland, as Conostoma ovale and C. intermedium. Dr Benson’s investigation[222] of these two forms leads her to confirm Williamson’s doubts as to the validity of a specific separation and she assigns the single type to the new genus Sphaerostoma. The seeds are always associated with the vegetative organs of Heterangium Grievii. In 1909 Oliver[223] expressed the opinion that the Burntisland species of Conostoma (= Sphaerostoma) is probably the seed of Heterangium. The seed consists of a central body representing the nucellus, an inner integument, and an enveloping cupule or outer integument: most specimens have lost the cupule and in this condition they are 3·5 mm. long with a maximum breadth of 2·2 mm. In the middle the seed is circular in transverse section and octagonal near the base and apex. The free apical part of the integument forms a frill (canopy) round the micropyle and extends beyond the nucellar apex which consists of a relatively flat plinth surmounted by a central dome or lagenostome (fig. 414). The lagenostome is surrounded by an annular pollen-chamber on to the lower surface of which abuts the large embryo-sac, and remains of archegonia were noticed below the pollen-chamber. The roof of the chamber in the young state consists of a layer of thin-walled cells extending across the flattened apex of the nucellus, n, but as the pollen-chamber becomes differentiated from the nucellar tissue by the disorganisation of the zone of cells its roof-cells thicken their vertical walls and assume the structure of a multiseriate annulus, which acts as a mechanism for opening the pollen-chamber by a circular dehiscence in such a way that the edge of the ruptured roof of the pollen-chamber slightly overlaps the periphery of the central column of nucellar tissue after it has returned to its original position subsequent to the entrance of the microspores. The micropylar region is surrounded by eight lobes of the integument and each is characterised by a crest of radially elongated cells, fig. 414, f, especially prominent on the outer side. External to this is the slightly longer cupular sheath (fig. 414, c) which may also have been lobed. The surface of the integument below the terminal crests consists of a layer of cells with small papillae which eventually ruptured and discharged mucilage. Both integuments have a vascular supply, that of the inner integument being represented by eight vascular bundles, some of which were found to have mesarch xylem, given off from the single strand in the pedicel. Fig. 414 shows the apical region of a seed of Sphaerostoma: the flat-topped nucellar cap, n, is surrounded by the annular pollen-chamber, pc, below which are indicated the archegonia: the wall of the megaspore (embryo-sac) is seen at m and external to this vascular bundles, v, run up the inner portion of the integument accompanied by some large cells (aqueous tissue). The elongated epidermal cells at the apices of the lobes of the integument form the frill, f, and at a lower level the cells of the same layer are much smaller and papillate (e): the outer integument, c, forms the so-called cupule. The transverse section shown in fig. 414, B, is taken at the level of the roof of the pollen-chamber and of the nucellar cap; it illustrates the contrast between the ‘multiseriate annulus’ and the central column of small parenchyma.
Sphaerostoma differs from Lagenostoma in the whorl of crests around the micropyle, in the nearly hemispherical form of the lagenostome and in the relatively wider pollen-chamber with its peculiar form of dehiscence. Miss Benson, while regarding Sphaerostoma as similar to Lagenostoma in general plan, believes the distinguishing features of the former to be such as are consistent with a more primitive form.
An important argument in support of connecting this seed with Heterangium is derived from the juxtaposition of some seeds and portions of Heterangium petioles, a juxtaposition that is believed to demonstrate original continuity.
Grand’Eury[224] has recorded the association of two species of leaves, Sphenopteris elegans and S. dissecta, with small seeds compared by him with Lagenostoma. In the absence of petrified specimens it would be practically impossible to distinguish between Lagenostoma and Conostoma or Sphaerostoma.
Carpentier[225] has described some impressions from French Westphalian beds as Conostoma and he records cupules without seeds on fronds of Sphenopteris obtusifolia which he speaks of as having transverse striations like those of Heterangium. Dr Kidston pointed out to me that the surface-features of the Sphenopteris rachis are probably due to ramental scales and not to the presence of horizontal sclerous bands. Carpentier’s seeds may be compared with Lagenospermum Sinclairi.
This species, founded by Williamson on material from the Lower Coal Measures of Halifax, Yorkshire, while agreeing in the structure of the primary stele and in the general features of the cortex with the older Heterangium Grievii, is clearly distinguished by certain well-marked characters. Sclerous groups occur in the inner cortex as in H. Grievii but they are present also in the pericycle. The peripheral leaf-traces in the stele show the mesarch structure rather more distinctly than in H. Grievii, and the secondary xylem, which forms a much broader cylinder than in the Scotch type, is divided by broad medullary rays into characteristic cuneate masses each of which rests at its base on the centrifugal tracheids of a leaf-trace strand of xylem (fig. 415, B). The most striking distinctive feature is afforded by the secondary phloem, which is often preserved in wonderful perfection; this is unusually thick and owing to the tangential expansion of the principal medullary rays the secondary phloem is divided into separate masses which decrease in breadth towards the external arcs of primary phloem. The triangular form of the phloem rays, composed of tangentially stretched parenchyma, suggested the specific name tiliaeoides on account of their striking resemblance to the rays of Tilia. The leaf-traces are nearly always in pairs as they pass out through the cortex; they subsequently divide and appear as four vascular strands in the petiole. The portion of stem reproduced in fig. 415, B, 8 mm. broad, shows clearly the separation of the secondary xylem and phloem into wedge-shaped groups: in each group there are several narrow medullary rays. The extrastelar tissues are represented by a few fragments only. Several layers of crushed periderm occur in the pericyclic region but the more external tissues have been almost completely exfoliated[226].
Reference has already been made to Heterangium Lomaxi, the English type originally included by Williamson in Heterangium Grievii. The provisional species Heterangium cylindricum Williamson and Scott[227] differs, as Scott says, in no important respect from H. Lomaxi and should not be retained. A new species, H. minimum Scott[228], has been founded on a very small stem from the Coal Measures of Dulesgate in which the leaf-traces leave the stele as single bundles as in the Scotch H. Grievii.
The French species Heterangium Duchartrei[229] Ren. from Permian rocks was originally referred by Renault to the genus Poroxylon: it is represented by little more than the xylem of the stele and bears a close resemblance to H. tiliaeoides. Heterangium punctatum Ren. and H. Renaulti[230] (Brongn.) also from the Permian of France were originally placed in the genus Lycopodium and afterwards recognised as stems of Heterangium. A fourth French Permian species, H. bibractense[231], is peculiar in the possession of a very small primary stele encircled by deep wedges of secondary xylem, but without more information it is impossible to speak with confidence as to its systematic position. Kubart[232] has recently published brief descriptions of some stems from the Ostrauer coal-basin in Moravia all of which he regards as specifically distinct from the English types. In Heterangium Sturi the primary xylem is almost exarch and the peripheral xylem groups are not very clearly defined: in H. alatum, so called from the presence of lateral wings on the petioles, the leaf-trace strands are more sharply differentiated from the rest of the stele. H. polystichum is a similar type, and H. Andrei, with a relatively larger amount of parenchyma in the stele and thicker stems forms an additional link between Heterangium and Lyginopteris[233]. Prof. Johnson[234] has described a species of Heterangium, H. hibernicum, from Upper Devonian and Lower Carboniferous beds in Co. Cork, Ireland, based on some impressions of frond fragments without any pinnules. The occurrence of numerous transverse striae on the rachis and lateral branches suggests comparison with Heterangium fronds, but an examination of the specimens led me to suspect that some at least of the striae are cracks and not original features. The presence of spur-like appendages from the lower surface of the pinnae near their origin from the rachis is recorded as a peculiar character, and some obscure oval bodies, the nature of which is extremely doubtful, are considered to be seeds. The imperfection of the material hardly justifies the institution of a new species of Heterangium.
Heterangium ranges from the Lower Carboniferous to the Permian strata and is thus older than Lyginopteris which in the form of petrified stems is not recorded from the Lower beds of the Carboniferous system. Heterangium has been described as having a ‘great preponderance of fern-like characters,’ but having regard to the resemblance of the primary xylem of the latter to that of the Osmundaceae it would seem doubtful whether in their relation to the Ferns there is any important difference. Heterangium may safely be spoken of as the more primitive genus. The polydesmic character of the petioles of most species is particularly interesting as it brings the genus nearer to the Medulloseae and to Rhetinangium[235].