Chapter XXIX: Pteridospermeae (1)

I. LYGINOPTERIDEAE.

LYGINOPTERIS.

The genus _Lyginopteris_ is selected for the first place in this chapter simply on the ground that we have a fuller knowledge of its morphology than in the case of other types. It is not regarded as the most primitive member of its class. _Lyginopteris_ may be described in a few words as a plant having the habit and to a large extent the anatomical features of a Fern, but differing from existing ferns in the possession of integumented megasporangia or seeds and in the power of secondary growth in thickness by means of a cambium in both stem and root. The seed (_Lagenostoma_) agrees with those of recent Cycads and Gnetales more closely than with the corresponding organs in Conifers or any other group, while the structure of the secondary wood is practically identical with that of Cycads. The microsporangia occur as groups of small bilocular sporangia, or synangia, at the tips of fertile pinnae of highly compound fronds.

_Nomenclature and Historical Summary._ In 1866 E. W. Binney[93] of Manchester published a short description of a small petrified stem from the Lower Coal Measures of Lancashire and named it _Dadoxylon oldhamium_, employing Endlicher’s term _Dadoxylon_ which that author substituted for _Pinites_ as previously used by Witham[94]. Three years later Williamson[95] drew attention to certain features in which Binney’s type differs from the genus _Dadoxylon_ and substituted a new name _Dictyoxylon_, suggested by the reticulate pitting on the walls of the tracheids. In a subsequent paper Williamson[96] gave a fuller description of Binney’s species and spoke of it as ‘one of the most common plants in the calcareous nodules of the Lower Coal Measures’ of Lancashire and Yorkshire. He connected certain casts of arborescent dimensions with Binney’s type on the ground that the surface-features of the casts are such as would be produced by partially decorticated stems having a hypodermal reticulum of mechanical tissue like that preserved in the small petrified specimen described by Binney (fig. 402). Mr Carruthers called Williamson’s attention to a paper by Mr Gourlie[97] in which the generic name _Lyginodendron_ is instituted for stem-casts identical in surface-features with the fossils figured by Williamson. In spite of the much larger dimensions of the reticulum on the casts described by Gourlie as compared with that in the outer cortex of Binney’s stem, Williamson concluded that _Lyginodendron_ is ‘undoubtedly an inorganic cast of the prosenchymatous layer of the bark of _Dictyoxylon_.’ It is but fair to add that Williamson was influenced in coming to this conclusion by a discovery by Mr Nield of a piece of a large petrified stem believed to be generically identical with Binney’s type, but subsequently referred to a distinct genus[98], which was comparable in size with the stems responsible for Gourlie’s _Lyginodendron_ casts. The type-specimen of Gourlie’s _Lyginodendron Landsburgii_[99], from Carboniferous rocks at Stevenston in Ayrshire, Scotland, is represented in fig. 401. The convex areas represent casts of depressions in a reticulum of cortical tissue, originally occupied by comparatively delicate cells, which decayed or shrunk more quickly than the enclosing framework of stronger fibrous elements that remained as a prominent reticulum and produced the depressions bounding the raised portions of the cast. Such a cast would undoubtedly be formed by the stem on which Binney founded his species: the radially disposed bands of thick-walled cells seen in the outer part of the section (fig. 402) are portions of an irregular anastomosing mechanical system, the reticulate arrangement of which is seen in the impression of a rachis of a _Lyginopteris_ frond shown in fig. 405, E, and indicated in the more slender axis reproduced in fig. 404, A, _b_. This reticulate form of cortical stereome on which Brongniart founded the genus _Dictyoxylon_[100], a term since applied by Solms-Laubach and other authors to a certain type of cortex not confined to a single genus of plants, occurs also in some Palaeozoic lycopodiaceous stems[101] and in itself cannot be regarded as a safe criterion of botanical affinity. The largest example of Gourlie’s _Lyginodendron_ that has come under my notice is an incomplete sandstone cast from Upper Carboniferous strata near Harrogate reaching a length of 100 cm. and with convex areas 13 cm. long. A similar cast, 36 cm. broad, has recently been figured by Nathorst[102] from the Culm of Spitzbergen, and from the Upper Devonian of Ellesmere Land the same author has described impressions of a cortical reticulum under the name _Lyginodendron Sverdrupi_[103]. These specimens are interesting as pointing to the former occurrence in the Arctic regions of stems—probably Lepidodendroid—reaching the dimensions of a fairly large tree. As Potonié[104] pointed out, Gourlie’s generic name serves a useful purpose for casts of stems of the type shown in fig. 401 that cannot be assigned to a definite systematic position. The genus was first used for a specimen which has nothing to do with the plant usually spoken of as _Lyginodendron oldhamium_ (Binney). Though loath to give up a name by which Binney’s type has long been known, in spite of its retention in the second volume of this work I feel compelled so far to conform to the recognised principles governing nomenclature as to adopt Potonié’s generic term _Lyginopteris_.

_Lyginopteris oldhamia_ (Binney).

i. _Stem_.

1866. _Dadoxylon oldhamium_, Binney, Proc. Lit. Phil. Manchester, vol.
+v.+ p. 113.

1869. _Dictyoxylon oldhamium_, Williamson, Monthly Micros. Journ. vol.
+ii.+ p. 66.

1873. _Lyginodendron oldhamium_, Williamson, Phil. Trans. Roy. Soc. vol.
+clxiii.+ p. 404.

1899. _Lyginopteris oldhamia_, Potonié, Lehrbuch der
Pflanzenpalaeontologie, p. 171.

ii. _Leaf_.

1828. _Sphenopteris Hoeninghausi_, Brongniart, Prodrome, p. 51.

1872. _Edraxylon_, Williamson, Proc. R. Soc. vol. +xx.+ p. 438.

1874. _Rachiopteris aspera_, Williamson, Phil. Trans. R. Soc. vol.
+clxiv.+ p. 684.

1877. _Calymmatotheca Hoeninghausi_, Stur, Culm Flora, +ii.+ p. 266.

1905. _Crossotheca Hoeninghausi_, Kidston, Proc. R. Soc. vol. +lxxvi.+
p. 358.

iii. _Seed_.

1877. _Lagenostoma_, Williamson, Phil. Trans. R. Soc. vol. +clxvii.+ p.
234.

1903. _Lagenostoma Lomaxi_, Oliver and Scott, Proc. R. Soc. vol. +lxxi.+
p. 477.

iv. _Root_.

1876. _Kaloxylon Hookeri_, Williamson, Phil. Trans. R. Soc. vol.
+clxvi.+ p. 23.

i. _Stem_.

The petrified stem on which Binney founded the species was first figured by Dr Arber[105] from a section in the Binney collection in the Sedgwick Museum, Cambridge: this section (13 mm. in diameter) is reproduced in fig. 402. The most striking features are: (i) the pith consisting of an unusually large and irregular group of dark thick-walled parenchyma, (ii) the broad cylinder of manoxylic secondary xylem characterised by multiseriate medullary rays, (iii) the outer cortex composed of dark radially disposed and oblique bands of mechanical tissue separated from one another by partially destroyed and tangentially elongated parenchymatous elements. It is this outer cortex that Williamson aptly compared with the Roman numerals on a clock-face. In the perimedullary region and in contact with the inner edge of the secondary-xylem cylinder are six strands of primary xylem representing the xylem halves of collateral bundles separated from the primary phloem strands by the intervening cylinder of secondary wood. Two of the primary xylem strands in lateral contact are seen in fig. 404, C; the other four occur as separate bundles. Each primary xylem strand contains a small group of spirally thickened protoxylem elements (_px_) associated with a few parenchymatous cells. The large primary tracheids internal to the protoxylem are characterised by multiseriate bordered pits on their walls, while those external to the protoxylem, which are in contact with the innermost secondary tracheids, have scalariform pitting. The dark patch _s_ (fig. 404, C) is a portion of the large group of sclerenchymatous cells, shown in figs. 402, 403. The perimedullary xylem strands of mesarch structure are the lower portions of leaf-traces and, as Scott points out, ‘each of the bundles surrounding the pith is, in fact, a sympodium, composed of the united lower ends of successive adjacent leaf-traces.’ The larger of the two bundles shown in fig. 404, C, is on the point of passing out to a leaf, while the smaller strand is on its way to a higher level before bending outwards through the secondary wood. Slightly beyond the middle of the secondary xylem there is an arc of narrower tracheids comparable with an incomplete annual ring. Although zones or arcs of narrow tracheids are not uncommon in the wood of _Lyginopteris_ there is no satisfactory evidence of regularly recurring seasonal changes. On the outer face of the secondary wood are a few leaf-trace strands pursuing a vertical course in the pericycle region; but the structure and behaviour of these bundles are more clearly illustrated in the stem reproduced in fig. 403. The tissue between the crushed phloem and pericycle and the outer cortex (fig. 402) consists of radially compressed parenchyma with scattered secretory cells separated from the more internal tissue by a narrow band of periderm formed by a phellogen in the outer part of the pericycle.

A larger and better preserved stem, 3·7 cm. in diameter, is seen in fig. 403. In this stem the pith of parenchyma and scattered sclerenchymatous nests is larger in proportion to the stele than in Binney’s type-specimen. From the inner edge of the secondary xylem several primary xylem-strands project as rounded wedges or tangentially elongated groups where two traces are laterally united in the perimedullary zone. The cylinder of secondary wood is partially interrupted at _r_ by the bending outwards of the stele of an adventitious root cut across transversely as it bends down after emerging from the outer cortical region. In more or less close association with the outer surface of the secondary xylem are four pairs of leaf-trace bundles and one larger trace at _d_ containing two widely separated protoxylem strands and faced externally with an arc of secondary xylem: this is a leaf-trace which shows by the slight constriction on the outer edge of its primary xylem that it is beginning to divide into a pair of equal strands. A precisely similar strand is shown on a larger scale in fig. 404, D. The twin bundles seen at _b_, fig. 403, represent a divided leaf-trace at a slightly higher level than the partially severed trace at _d_, and the arcs of secondary xylem are narrower. The appearance of the double leaf-trace at a still higher level is shown at _c_: the two strands are farther apart and the secondary xylem has almost disappeared, while those at _e_, nearer their entrance into the leaf-stalk, consist exclusively of primary xylem and phloem. At _a_ the two strands of a leaf-trace, still nearer to the petiole, are inclined towards one another preparatory to reunion after reaching the leaf-stalk. A slender root is seen in transverse section at _r′_ immediately outside the two leaf-bundles. As Williamson and Scott[106] have pointed out, there are always five leaf-traces beyond the xylem cylinder of a _Lyginopteris_ stem as seen in transverse section, and these traces in the pericycle, separated from one another by ⅔ of the circumference, alternate in position with the lower portions of leaf-traces in the perimedullary region of the same stem. The phyllotaxis is thus seen to be ⅖.

The secondary wood is succeeded by a cambium of normal structure passing gradually into a narrow band of secondary phloem which in well-preserved stems is seen to consist of sieve-tubes and parenchyma with medullary rays rather broader than those in the xylem. Beyond the phloem is the comparatively broad pericycle consisting of parenchyma with nests of sclerenchyma like those in the pith and scattered secretory cells. In the outer layers of the pericycle a phellogen was formed at an early stage in the growth of the plant, producing several layers of secondary tissue, which is regarded as periderm and forms a conspicuous feature in _Lyginopteris_ stems; it appears as a comparatively dark sinuous band where it bends outwards to wrap round the leaf-traces in their almost vertical course through the pericyclic region (fig. 403). The periderm is clearly seen at _p_ close to the crushed secondary phloem of the dividing leaf-trace in fig. 404, D. All the leaf-traces seen in fig. 403 beyond the secondary wood are still within the deep-seated periderm and, as Williamson and Scott showed, each leaf-trace after emerging from the secondary wood remains in the pericycle-zone for a length of five internodes as it very gradually inclines outwards. Once free from this region the twin bundles bend more sharply towards the petiole. Stated briefly, the history of each leaf-trace from the perimedullary region to the leaf-base is as follows: at the outer edge of the pith a single trace consists of a mesarch xylem bundle with one protoxylem strand; it passes vertically through five internodes and then bends out through a foliar gap in the xylem-cylinder, and the primary tracheids receive additions from the cambium of the stele on their outer face. As the trace leaves the secondary xylem it bends upwards and, as seen at _d_, fig. 403, begins to divide into twin bundles. As the trace passes higher the bisection of the protoxylem and metaxylem is completed and the secondary xylem-arcs are gradually lost until the separate strands of each pair are reduced to single mesarch bundles composed wholly of primary tracheids. As the trace bends outwards through the cortex the phloem gradually encircles each xylem-strand until a concentric structure is substituted for the collateral disposition of the conducting tissue. At the same time the protoxylem strands divide and occupy a position near the inner edge of the metaxylem. On reaching the petiole or after passing some distance up the axis of the frond, the twin bundles unite and usually form a V-shaped vascular strand (figs. 404, E; 405, A). The single meristele subsequently divides into two equal portions preparatory to the bifurcation of the petiole (fig. 406).

The inner cortex, consisting of parenchymatous tissue and many secretory cells with an occasional group of sclerenchymatous elements in place of the abundant nests of this tissue in the pericycle, has been invaded in the stem shown in fig. 403 by numerous rootlets of _Stigmaria_ and _Lyginopteris_, some of which are seen interrupting the continuity of the outer cortex. The greater width of the cortical region at _f_, fig. 403, is due to the decurrent base of a petiole the meristele of which is not included in the section. The lighter and broader bands between the cross-sections of the stereome-network in the outer cortex are occupied by remains of tangentially stretched parenchymatous cells, and beyond this zone in a younger stem there are a few layers of parenchyma forming the superficial tissue, but there appears to be no well-defined epidermal layer.

A, B. Frond fragments; _a_, pinnule; _b_, reticulum of sclerenchyma.
C. Portion of stele of the stem reproduced in fig. 402.
D. _px_, protoxylem; _s_, sclerenchyma; leaf-trace close to the edge
of the secondary xylem; _p_, periderm.
E. Petiole; _m_, meristele.

(A, Kidston Coll. 664 B; B, Camb. Botany School 508; C, Binney Coll. 179; D, E, Camb. Botany School, 93, 159.)]

Young stems have been recognised in which there is very little secondary xylem and phloem: in these the stereome bands in the outer cortex are closer together than in the stretched hypodermal tissue of older shoots and the scattered sclerous nests are represented by unthickened cells. In addition to young stems Williamson and Scott described a distinct type of small stem in which the primary xylem forms an almost complete ring[107] comparable with the primary xylem of some adult Sigillarian stems (vol. +ii.+ p. 220) but distinguished by its mesarch structure and by the reticulate pitting of the centripetal xylem.

A characteristic feature of the stem is the occurrence of emergences from the outer cortex which have the structure either of spinous processes, broadly linear or flask-shaped, or of stalked glands[108]. A portion of a glandular emergence is shown in fig. 405, B: the group of small cells immediately below the blunt apex is in this instance still intact though showing signs of disorganisation in the centre; but in many cases the secretory tissue has not been preserved and the head of the emergence is occupied by a space. A single stoma is seen at _s_ in longitudinal section. Further reference to the emergences is made in the description of the leaf.

It occasionally happens that a meristematic layer is formed in the parenchymatous tissue immediately internal to some of the perimedullary xylem strands of a _Lyginopteris_ stem from which either secondary parenchyma is produced or a zone of secondary xylem and phloem, the phloem facing the centre of the pith. An example of such internal xylem was figured by Williamson[109] and similar occurrences are more fully dealt with by Williamson and Scott[110] who consider that the perimedullary cambium may represent an internal extension through a leaf-gap of the normal cambial cylinder. In the stem represented in fig. 403 there are two perimedullary xylem strands to the left of the bottom of the V-shaped gap in the secondary xylem-cylinder, _r_, and on the inner face of one of these, as shown in fig. 405, C, there is a narrow arc of internal secondary xylem, _c_, between the xylem-strand and the outer edge of one of the sclerous nests. The sporadic occurrence of arcs of inversely orientated secondary vascular tissue affords an interesting parallel with a similar morphological feature in some recent Dicotyledonous genera such as _Tecoma_ and _Iodes_. As Williamson and Scott point out, this similarity affords ‘a striking warning against the _indiscriminate_ use of even conspicuous anatomical characters[111].’ While admitting the necessity of guarding against the danger of attaching importance to occasional and abnormal characters they may have some significance as collateral evidence in comparisons of different types of stems. It is conceivable that these anomalous arcs of secondary tissue on the inner side of the primary xylem strands may, as Worsdell[112] maintains, be reversions to an ancestral character and in this sense comparable with the strands of inverted vascular tissue in some recent Cycadean stems. The question of relationship of _Lyginopteris_ and allied types to recent Cycads and the Palaeozoic Medulloseae is considered in a later chapter.

In 1902 Lomax[113] described two branching specimens of _Lyginopteris_, and more recently two others have been discovered at a locality near Bacup in Lancashire which have been thoroughly investigated by Miss Brenchley[114] who constructed models from drawings of serial sections[115]. One specimen shows six leaf-bases in a length of 4¾ inches and branches spring from the axils of five of them: some of the branches show secondary ramifications. The phyllotaxis of the leaf-bases on a branch is always the reverse of that on the main stem, a divergence to which no parallel was found in a selection of trees and shrubs examined by Miss Brenchley. The secondary wood of the stem swells below the point of exit of a branch and frequently a fairly large amount of wood occurs in the pith when a branch is given off: this anomalous wood may help to close the branch-gap.

ii. _Leaf_.

In his account of _Lyginopteris_ stems published in 1873 Williamson[116] suggested that the vascular bundles met with outside the xylem-cylinder might be the leaf-traces of large fronds and expressed the opinion that the ‘stems or petioles’ previously described by him under the generic name _Edraxylon_ might belong to _Lyginopteris_. A year later he substituted the name _Rachiopteris aspera_ for the petioles previously referred to _Edraxylon_ and inclined to the view that this type of _Rachiopteris_ may be the petiole of the Carboniferous fronds known as _Sphenopteris Hoeninghausi_ Brongn., an inference based to a large extent on the occurrence of emergences on _Rachiopteris aspera_ (fig. 404, E) preserved as petrifactions like those on impressions of _Sphenopteris Hoeninghausi_ as figured by Brongniart (figs. 404, A; 405, D, D’). In 1890 Williamson was able to demonstrate the truth of the surmise that _Rachiopteris aspera_ and _Lyginopteris oldhamia_ are respectively the petiole and stem of the same plant, which he believed to be an arborescent fern[117]. The petioles of _Lyginopteris_ fronds, which may reach a diameter of 1 cm., are attached by a broad base to the stem, and as already suggested by the number of internodes traversed by each leaf-trace, the leaves are comparatively far apart. A transverse section of a petiole is shown diagrammatically in fig. 405 A. The hypodermal stereome is a prominent feature, but the narrow radial plates of the stem-cortex tend to be replaced in the rachis by broader and confluent masses of strengthening elements: the upper surface of the petiole is slightly grooved. Glandular and spinous emergences are often very abundant, as in the section reproduced in fig. 404, E. A glandular emergence is seen at _a_ in fig. 405, A. The spinous emergences may be compared with those of _Davallia_ (_Odontosoria_) _aculeata_[118], a West Indian fern of climbing habit and with the prickles on _Hemitelia_ and other recent Cyatheaceous fronds[119], while capitate glands, though simpler than those of _Lyginopteris_, occur on the leaf-stalks of some recent Polypodiaceous species[120]. The concentric meristele may consist in the lower part of the petiole of two separate and slightly curved strands like those seen in fig. 404, E, _m_: sooner or later the two strands unite to form a wide-open V or a W-shaped bundle with several slightly internal protoxylem groups close to the lower edge. The two sections represented in fig. 406, A and B show the gradual divergence of the two meristeles of a petiole as they approach the level where it divides into two equal branches, a characteristic feature of _Sphenopteris Hoeninghausi_ and allied fronds. At a lower level than that represented in fig. 406 the vascular strand of the petiole would have the form of a W as figured by Williamson in one of his earlier memoirs[121]. The phloem with scattered secretory sacs and the adjacent tissue of the leaf-stalk are occasionally preserved in wonderful perfection[122]. No endodermis has been recognised. Sclerous nests are scattered in the ground-tissue as are also secretory sacs (figs. 404, E; 405, A). A small root _r_ has penetrated the parenchyma of the rachis shown in fig. 405, A.

_Sphenopteris Hoeninghausi_ Brongn.[123], founded on material from English Coal Measures, was regarded by Williamson as the foliage of _Lyginopteris_ chiefly on the ground of the occurrence of emergences on the axes (figs. 404, A, B) and laminae of the impressions like those on the petrified stems, and this comparison received support from the resemblance of the fragments of pinnules associated with _Lyginopteris_ and its petioles in the calcareous nodules to the leaflets of Brongniart’s type. This identification is supported by subsequent work. The quadripinnate fronds, which attain a considerable size, resemble those of recent species of _Davallia_ and other ferns, but the forking of the rachis and branches of the frond is a striking feature: the pinnae may reach a length of 15 cm.[124] The portion of carbonised rachis shown in fig. 405, E, reveals the existence of a hypodermal reticulum like that in the outer cortex of a _Lyginopteris_ stem and the same feature is seen in the more slender axis represented in fig. 404, A, at _b_.[125] The pinnules are usually deeply lobed and the segments may be comparatively broad and blunt or narrow[126] (fig. 290, C, vol. +ii.+ p. 399; fig. 404, A, _a_, B; fig. 405, D’). The lamina has a well marked dorsiventral structure: the palisade-tissue next the upper surface is separated from the epidermis by small hypodermal cells, possibly functioning as a water-storage layer, and the central part of the mesophyll consists of loose aerenchyma: the veins are collateral as in recent ferns and stomata occur in the lower epidermis. Emergences are seen both on impressions (fig. 405, D’) and on petrified specimens. A striking feature of the pinnules is the rounded surface caused by the revolute edge of the lamina as seen in the section reproduced in fig. 404, B. This character coupled with the occasional occurrence of groups of short tracheal elements at the termination of the veins denotes a tendency to a xerophilous habit.

On the strength of a very close resemblance between _Sphenopteris Hoeninghausi_ and _Calymmatotheca Stangeri_ (fig. 408, E, F)—characterised by fertile pinnules bearing stellate groups of small linear valves, regarded by Stur as the open lobes of an indusium—Zeiller included Brongniart’s type in the genus _Calymmatotheca_. The resemblance in general habit between the two species extends to the presence in their rachises of the _Dictyoxylon_ form of cortex[127]. The view formerly held by some authors that the valve-like appendages to the fertile segments of _Calymmatotheca_ are sporangia is incorrect: a re-examination of Stur’s specimen (fig. 408, E, F) has confirmed the original description[128]. The stellate lobes are now regarded as portions of a cupular investment of a seed similar to _Lagenostoma Lomaxi_, the female reproductive apparatus of _Lyginopteris oldhamia_. The axes of the fertile pinnae bear small thorn-like emergences probably identical with those on the cupule of _Lagenostoma_ and on the petioles of _Lyginopteris oldhamia_. It was stated in vol. +ii+ that the fronds known as _Sphenopteris Linkii_ (Goepp.) represent, with other closely allied forms, leaves belonging to _Heterangium_ stems. This statement was based on a misconception: the rachis of _Sphenopteris Linkii_, as I have satisfied myself by an examination of impressions shown to me by Dr Kidston, exhibits the reticulate pattern characteristic of _Lyginopteris_ and not the transverse ribs characteristic of _Heterangium_.

It is not an easy task even for those most familiar with Carboniferous fronds to distinguish clearly between species agreeing generally with _Sphenopteris Hoeninghausi_, a species regarded by some authors as the type of a group of very similar and closely allied forms all of which were probably borne on stems referable to the genus _Lyginopteris_. The species _Lyginopteris oldhamia_ as generally understood probably includes more than one specific type, and it is safe to assert that in the Carboniferous period _Lyginopteris_ was represented by several forms characterised by highly compound fronds with forked rachises like _Sphenopteris Linkii_, _S. Hoeninghausi_, and others. The features characteristic of fronds included in the _Sphenopteris Hoeninghausi_ group have recently been described by Gothan[129]. Stur’s generic name _Calymmatotheca_ originally applied to the species _C. Stangeri_ was applied to _Sphenopteris Hoeninghausi_ by Zeiller, and although the fronds of the latter type have not been found with fertile appendages of the _Calymmatotheca_ type there can be no doubt as to the generic identity of these, barely distinguishable, species both of which belong to stems of _Lyginopteris_. Prof. Johnson[130] has recently described some impressions from the Coal Measures of Ireland, which he refers to _S. Hoeninghausi_, bearing stellate groups of lobes like those of _Calymmatotheca_, and in one case he describes a seed in the middle of the carbonised remains of a stellate group of cupular segments. An examination of the specimen in Dublin convinced me that there is no satisfactory evidence of the seed-nature of the appearance on the rock believed by Johnson to be an elliptical _Lagenostoma_-like seed. The actual attachment of the stellate lobes to the pinnae of the frond is not clearly demonstrated.

iii. _Microsporangia._

In 1905 Kidston[131] announced the discovery of microsporangia on fronds of _Lyginopteris_: he described specimens from the Coal Measures of Dudley identified by him with _Sphenopteris Hoeninghausi_ showing sterile and fertile pinnae in organic connexion. The fertile pinnules (fig. 407, B) are slightly expanded distally into an oval limb about 2 mm. long bearing 6 to 7 bilocular fusiform microsporangia 3 mm. long and 1·5 mm. broad: in the immature condition the sorus is hemispherical, the summit being formed of the incurved apices of the sporangia. At maturity the sporangia spread out, the sorus assuming the form of an epaulet. Fig. 408, H, shows a sorus in transverse section and in fig. 408, G, the limb and two pendulous sporangia are shown. The microspores, 50–70 µ in diameter, are studded with numerous blunt spines and each spore shows a triradiate ridge. The section reproduced in fig. 407, A, from the Coal Measures of Oldham is probably a bilocular sporangium of the same type as those described by Kidston from Dudley. Dr Kidston[132] describes a second type of microsporangial sorus as _Crossotheca Hughesiana_ which agrees closely with _C. Hoeninghausi_, but the fertile segments are not associated with any sterile pinnae. The generic name _Crossotheca_, founded by Zeiller[133] in 1883, was substituted for _Sphenopteris_ on the ground that Brongniart’s species _S. Hoeninghausi_ is shown to possess sporangia of the _Crossotheca_ type. If Kidston’s specific determination is correct, his discovery demonstrates that _Lyginopteris_ fronds bore microsporangia having the characters of _Crossotheca_, a type characteristic of several Carboniferous species belonging both to the form-genera _Sphenopteris_ and _Pecopteris_. Reference has already been made to the difficulty of distinguishing between impressions of fronds of the _Sphenopteris_ _Hoeninghausi_ group, a difficulty that is illustrated by Dr Gothan’s statement[134] that the Dudley specimens of _Crossotheca_ are not identical in the character of the sterile pinnules with _Sphenopteris Hoeninghausi_. An examination of Dr Kidston’s specimens led me to agree with his determination; but, it may be asked, have we any evidence of the association with _Lyginopteris_ fronds of sporangia other than those of the _Crossotheca_ type? Prof. Chodat[135] believes that certain petrified fragments of pinnules occasionally met with in the calcareous nodules bearing sessile and apparently annulate sporangia belong to _Lyginopteris_ fronds. These sporangia appear to be identical with those named by Scott _Pteridotheca Butterworthi_[136] and regarded by him as filicean sporangia that cannot be referred to any known Carboniferous genus. The piece of lamina bearing an empty sporangium, which may or may not have possessed an annulus, reproduced in fig. 407, C, occurs in association with the larger specimen shown in fig. 404, B, and it would seem not unreasonable to regard both as parts of the same frond, namely a frond of _Lyginopteris_. As Prof. Weiss[137] points out, the accurate determination of small pieces of petrified pinnules is exceedingly difficult and without more decisive evidence we are hardly justified in asserting that the sporangia figured by Chodat and Scott and that shown in fig. 407 belong to the genus _Lyginopteris_. Although the available data appear to favour the view generally held that Kidston’s conclusion is correct additional evidence would be welcome.

_Telangium._ Reference was made in vol. +ii.+[138] to the genus _Telangium_ instituted by Dr Benson for some petrified sporangia from the Coal Measures regarded by her as the microsporangia of a Pteridosperm, probably _Lyginopteris_. The sporangia of _Telangium_ are similar to those of _Crossotheca_. Scott points out that they are borne on a flat disc or lamina ‘quite comparable to a fertile pinna of _Crossotheca_[139],’ and he concludes that these sporangia are not generically distinct from the impressions on which the genus _Crossotheca_ was founded. Kidston[140] regards _Telangium Scotti_, Benson, as the microsporangium of a Pteridosperm though not of _Lyginopteris_, on the ground that the microsporangia described by Miss Benson are not attached to a limb and that they have a single loculus in place of the double loculus (fig. 407, A) of _Crossotheca_. The presence of a limb in _Telangium_ recognised by Scott removes one of these distinguishing features. There are, however, no adequate reasons for regarding _Telangium Scotti_ as specifically identical with _Crossotheca Hoeninghausi_. The synangium of _Telangium Scotti_, 5 mm. in length, consists of 6–12 sporangia united basally and opening when ripe by longitudinal dehiscence. Fig. 493, E, shows eight sporangia of a synangium in transverse section: the two sporangia at the lower end of the section are less distinct than the others, some are full of spores and others have shed their contents by the splitting of the thin inner walls of the loculi. The sporangial walls are composed of an outer layer of large cells with dark contents succeeded by 2–3 layers of smaller and crushed cells. The spores, 5–6 µ × 3·5–4 µ in diameter, have a reticulately sculptured exine: Dr Benson[141] states that they agree closely with pollen-grains found in the pollen-chamber of _Lagenostoma ovoides_ except in their slightly smaller size; she notes the association of _Telangium_ with fragments of the vegetative organs of _Lyginopteris_ and draws attention to resemblances in the structure of the tissues; but the most interesting comparison, at least in an academic sense, is with the seed _Lagenostoma_, the integumented megasporangium of _Lyginopteris_. Dr Benson points out that a transverse section of a _Lagenostoma_ in the plane of the canopy, showing the nucellar apex surrounded by radially disposed chambers (fig. 409), presents a certain resemblance to a synangium of _Telangium Scotti_; and it is suggested that the chambers encircling the nucellus may represent sterilised sister-sporangia[142]. ‘The seed in fact is assumed to be a synangium in which all but one of the sporangia are sterile, and form an integument to the one fertile sporangium which has become a megasporangium with one large megaspore.’ This view, though clearly incapable of confirmation in the present state of our knowledge, is not merely an ingenious hypothesis but a stimulating suggestion as to possible homologies: as an argument in favour of associating _Lagenostoma_ and _Telangium_ as the spore-bearing organs of the same plant it has but little weight.

iv. _The Seed._ =Lagenostoma= Williamson.

_Lagenostoma Lomaxi_, Oliver and Scott ex Williamson, +MS.+

In 1877 Williamson[143] proposed the generic name _Lagenostoma_ for some petrified seeds from the Lower Coal Measures of Lancashire and described two species, _Lagenostoma ovoides_ and _L. physoides_: in his +MS.+ Catalogue a third type is referred to as _Lagenostoma Lomaxi_. It is this third type that Prof. Oliver was the first to recognise as the megaspore-bearing organ of _Lyginopteris oldhamia_. Its structure has been thoroughly described by Oliver and Scott[144] and these authors contribute a judicial summary of the evidence on which _Lagenostoma_ and _Lyginopteris_ are believed to stand for one and the same plant. The evidence is based chiefly on the following considerations: an agreement in the structure of the vascular bundles in the investments of the seed with those in the leaves of _Lyginopteris_; the presence in the outer envelope of the seed of stalked glands identical with those on the stems and petioles. The evidence does not as yet amount to absolute proof, as the seeds, which occur either with or without a stalk, have not been found attached to a _Lyginopteris_ frond. But ‘where vegetative and reproductive organs presenting identical structural features, not known to occur in other plants, are thus found in close and constant association, the inference that the one belonged to the other appears irresistible.’ While most botanists believe that a satisfactory case is established there are a few[145] who refuse to believe in a connexion between _Lagenostoma_ and _Lyginopteris_ until an actual union has been demonstrated. The discovery by Kidston[146] of seeds attached to pinnae bearing _Neuropteris_ pinnules and the demonstration of organic continuity between seeds and the pinnules of other Palaeozoic fern-like fronds supply abundant confirmatory evidence that leaves no doubt as to the occurrence of seeds on modified pinnae of _Sphenopteris Hoeninghausi_ and of other closely allied fronds which represent the foliage of different forms of _Lyginopteris_. In this connexion it is pertinent to add that Grand’Eury[147] has found seeds of the _Lagenostoma_ type in close association with impressions of _Sphenopteris Dubuissonis_ and other leaves of similar habit.

A seed of _Lagenostoma Lomaxi_ reaches a length of 5·5 mm. with a maximum diameter of 4·4 mm.; it is broadly oval or barrel-like (fig. 408, C) and when immature was invested by a loose irregularly lobed glandular envelope (fig. 408, B) from which the seed eventually freed itself by a natural process of abscission. The central body or nucellus, except in the apical region, is concrescent with a fairly stout integument or testa (fig. 408, C, _f_) the outer portion of which is characterised by regular longitudinal rows of palisade-like cells comparable with the broad palisade-layer in the sporocarp of _Pilularia_. On the exposed surface of this palisade-tissue are small dark structureless pegs[148], possibly the remains of a mucilaginous layer such as occurs on the seed-coats of some recent Flowering plants. At the base of the nucellus the chalazal region, fig. 408, C, _ch_, is provided with sclerous elements and forms a hard investment to the axial vascular strand from the pedicel. It is at the base of this chalazal region that the seed is eventually cut off by an absciss-layer. The integument is supplied throughout its length by nine vascular bundles of endarch, or approximately endarch, structure. The free portion of the integument seen from the outside (fig. 408, B) has the form of a fluted cone with a circular opening at its summit. The greater part of this domical apex, as seen in longitudinal section in fig. 408, C, appears to be hollow, but in the living state the dome, or canopy as Williamson called it, was filled with parenchyma in which the vascular bundles were embedded and, as shown in the transverse section in fig. 409, the canopy is divided into compartments by radial septa which in its basal region are replaced by regular and deep furrows on the inner face. Enclosed by the canopy, with its outer surface fluted as the result of the partial collapse of the outer wall of each compartment due to the decay of the filling tissue, is the flask-shaped apex of the nucellus; between the apical cone of nucellar parenchyma and the superficial layer is an annular cavity which Williamson[149] called the lagenostome. The parenchymatous core tapers to a narrow summit which slightly overtops the integument and is constricted at the broad base (fig. 493, A, B; page 311). The bottle-shaped apical tissue is separated by an annular space, _c_, fig. 493, B, from the limiting layer of the nucellus: this space is the pollen-chamber formed in the living seed by the disorganisation of the subepidermal cells of the nucellar apex. The pollen-chamber is a feature characteristic of recent cycadean ovules (see p. 6). In _Lagenostoma_ the annular form of the pollen-chamber is a peculiarity distinguishing this type of seed from those of recent Gymnosperms and most other Palaeozoic seeds. As Oliver says, it marks an ‘advance in precision’[150] over other forms as the microspores which fall into the chamber are brought direct to the surface of the underlying megaspore and presumably to the archegonia which, it is reasonable to believe, were disposed in a circle at the base of the annular crevice. Microspores frequently occur in the pollen-chamber and some have been discovered apparently in the act of liberating male gametes[151].

The outer wall of the nucellus is bounded externally by a similar circular space (_d_, figs. 408, C; 493, B) which separates it from the domical canopy. In the great majority of specimens the central tissue of the seed is not preserved and an empty sac supported from the base of the nucellus-apex occupies nearly the whole of the interior: the shrunken wall of the sac is all that remains of the large megaspore. It would seem, then, that the nucellus was almost completely destroyed as a consequence of the growth of the megaspore or embryo-sac, which eventually occupied nearly the whole of the seed-body.

In an exceptionally well preserved specimen recently described and admirably illustrated by Mr McLean[152] part of the parenchymatous tissue of the prothallus which originally filled the megaspore is clearly seen: its surface-layer consists of small cells succeeded by a broad band of radially elongated elements closely resembling the alveoli in the prothalli of some recent Gymnosperms, particularly certain Conifers. No archegonia have been discovered. The cupular envelope of immature seeds, compared by Oliver and Scott with the lobed and glandular husk of _Corylus colurna_ L.[153], receives several vascular bundles of collateral and mesarch structure from the axial strand, and these subdivide as they ascend. The glands which occur on all parts of the cupule are sessile or stalked and identical with those on the vegetative organs of _Lyginopteris_. Assuming that pollination occurred at a comparatively early stage in the development of the seed when the cupule was still intact, it is conceivable, as Sir Joseph Hooker suggested, that the glandular secretion may have attracted insects and so aided in the transport of pollen which were perhaps drawn down the narrow pollen-chamber by exuded mucilage as in recent Conifers. The evidence obtained in recent years in favour of insect-pollination in certain Cycads and in _Welwitschia_ lends support to this view: the dragon flies hovering over a fertile _Lyginopteris_ frond in a recent restoration[154] may be a legitimate addition.

A striking feature of _Lagenostoma_ as of other Palaeozoic seeds is the absence of an embryo: this and other considerations have led certain authors, notably Chodat[155], to question the justification for the use of the term seed. Various suggestions have been offered in explanation of this fact. In recent Cycads, as already pointed out, the development of the embryo does not always occur before seed-fall. It may be that these older seeds had no resting-period or there may have been a period of rest after fertilisation and not as now at a stage subsequent to the formation of the embryo[156]; it is also suggested by Scott that ‘the nursing of the embryo had not yet come to be one of the functions of the seed, and that the whole embryonic development was relegated to the germination stage[157].’ In this connexion reference may be made to a statement by Miss Gibbs[158] who speaks of seeds of a _Podocarpus_ picked up from the ground in apparently a mature state and with the associated bracts coloured and swollen as though ready to aid in dispersal but with no embryo: the seeds had matured before fertilisation and fell from the tree after pollination. Whatever may be the true explanation of the absence of embryos this negative character should not be allowed to outweigh the evidence furnished by morphological features as to the applicability of the term seed. As Prof. Oliver says, ‘there is a long chapter in evolution to be deciphered before we can connect ... the seed of _Lyginodendron_ with the sporangium of any fern at present known to us’[159].

The cupule of _Lagenostoma_ has been homologised with the outer part of the integument of a recent cycadean seed[160] which, it is suggested, consists of an inner and an outer envelope that have become concrescent, and this hypothesis is supported by another author by a comparison between _Lagenostoma_ and Gnetalean seeds[161]. A comparison has also been made between the collar of a _Ginkgo_ seed and the much more conspicuous cupule of _Lagenostoma_[162]. Dr Benson and Miss Welsford[163] institute a comparison between the vascular supply of the outer integument of the ovules of _Carpinus_ and _Morus_ and that of the cupule of _Lagenostoma_, a comparison suggested by Miss Kershaw’s remarks[164] on the similarity between the vascular system of the ovules of _Myrica Gale_ and _Trigonocarpus_. In 1908 Dr Benson[165] described some germinating microspores in the pollen-chamber of another species of _Lagenostoma_, _L. ovoides_, and recognised what she believed to be antherozoids. I am indebted to this author for allowing me to make a drawing from her section (fig. 408, D). Two microspores are seen with thick outer walls showing irregular holes probably of secondary origin and not part of a regular reticulum as Dr Benson suggests. Close to the upper microspore is a hemispherical body, _s_, described as a male gamete, and a similar body is seen still enclosed by the lower microspore. It is by no means improbable that these are antherozoids: they were presumably ciliate like those of _Ginkgo_ and recent Cycads (fig. 396, M). The microspores are approximately 70μ in length and the supposed antherozoids have a maximum diameter of 45μ, the latter being about ⅔ the size of the sperms of _Microcycas_ and ⅙ the diameter of those of _Zamia_. The smaller and more delicate cells near the lower microspore (fig. 408, D) are no doubt fungal cells as Miss Benson suggests. With reference to the difficulty of determining the nature of Miss Benson’s supposed gametes it is worth calling attention to some figures given by Zopf[166] of vesicular cells and sporangia of the Phycomycetous genera _Rhizophidium_ and _Lagenidium_ in the pollen of Flowering plants and Pines. It has been suggested by Burlingame[167] that the ‘gametes’ may be prothallial cells; but this is very improbable.

_Lagenostoma ovoides_ Williamson.

In the memoir in which the genus was founded Williamson described two species from the Lower Coal Measures of Lancashire, _Lagenostoma ovoides_ and _L. physoides_[168]. The seeds described under the latter name had previously been assigned by him to another new genus, _Physostoma_, and named _P. elegans_[169]. _Lagenostoma physoides_ was afterwards figured by Butterworth[170] who recognised some new features. For this species Prof. Oliver[171] has adopted Williamson’s earlier name, _Physostoma elegans_. The former species, which has recently received exhaustive treatment by Miss Prankerd[172], agrees generally in its morphological characters with _L. Lomaxi_, but differs in the structure of the surface-tissue of the integument and in some anatomical features. Moreover no cupules have been found and there is ‘very little trace of a layer of separation’ such as occurs in _L. Lomaxi_. Over the surface of the integument is a layer of prismatic cells, much shorter and less palisade-like than those in _L. Lomaxi_, and there are none of the pegs which are a constant feature in that species. There are, however, indications that mucilage was poured out by the rupture of the distended cells. Some microspores were found in the pollen-chamber with an average size of 72 × 53μ; they may be as much as 90μ long. None were observed with sperm-like contents like those described by Dr Benson. Miss Prankerd discusses the morphology of the integument in relation to that of cycadean seeds and makes an instructive comparison between the lagenostome (that is the modified nucellar apex) and such fern sporangia as those of _Angiopteris_, _Osmunda_, and _Schizaea_, but especially the sporangia of _Senftenbergia_[173] with their multiseriate annulus.

An interesting feature is shown in the longitudinal section reproduced in fig. 493, A (p. 311). The apex of the nucellar cone appears to be composed of thick-walled, dark cells and it is suggested that this may have served as a stopper blocking up the circular orifice of the pollen-chamber (seen below the apex between the nucellar cone and the thick surface-layer of the nucellus) and serving as a protection to the embryo. A comparable closing-up of the micropyle occurs in the seeds of _Gnetum Gnemon_[174] and in the beak of cycadean seeds. At the time of pollination, when the pollen-chamber must have extended to the apex of the lagenostome, the tip of the nucellar cone may have secreted some sticky substance to which the microspores would adhere.

Prof. Lignier[175] has recently described some large megasporangia from the Westphalian Coalfield of Ostrau in Austrian Silesia which he made the type of a new genus _Mittagia_, after Herr Mittag, Director of Mines. Two sporangia, between 2 and 3 mm. in diameter, were found in close association as though belonging to a single sorus; one was empty and the other contained four megaspores. The structure of the thick wall of the sporangia is very similar to that of the testa of _Lagenostoma Lomaxi_, but it apparently split into two valves. Lignier refers the new type, _Mittagia seminiformis_, to some unknown Palaeozoic group of heterosporous Filicineae, possibly the ancestral stock of the Pteridosperms, and he thinks it probable that the sporangia resembled seeds in their facilities for dispersal. In the structure of the sporangial wall _Mittagia_ also resembles the sporocarp of _Pilularia_.

_Seeds presented as impressions, without internal structure,
superficially resembling Lagenostoma._

_Lagenospermum_ Nathorst.

This generic name is adopted for seeds represented by casts or impressions agreeing in external features with _Lagenostoma_ but which on the available evidence cannot be confidently assigned to that genus[176]. Two types of seed were described by Arber[177] from the Lower Coal Measures of Scotland as _Lagenostoma Kidstoni_ and _L. Sinclairi_: the former has been removed by Oliver[178] to _Physostoma_ and both are included by Arber[179] in a recent paper in the genus _Radiospermum_. This new generic term is proposed by Arber for a number of small sub-cylindrical seeds founded on impressions including ‘small seeds which, when the structure is preserved, are known as _Lagenostoma_, _Physostoma_, and _Conostoma_.’ The question of nomenclature is invariably raised by cases in which impressions resemble in their superficial characters genera founded on anatomical characters: the seeds originally referred to _Lagenostoma Sinclairi_ afford a good example of this difficulty. Nathorst has recently proposed the generic name _Lagenospermum_ as preferable to _Lagenostoma_ and _Radiospermum_ in the case of _Lagenostoma Sinclairi_ and similar seeds which afford no proof of the possession of such morphological characters as would justify their inclusion in the genus _Lagenostoma_ but which may be examples of that genus. As Nathorst points out, the adoption of _Radiospermum_ for _L. Sinclairi_ is inadvisable on the ground that it is also applied to seeds of a different type. The type-species of _Lagenospermum_ is _L. Sinclairi_ and Nathorst describes additional species from Lower Carboniferous rocks in Spitzbergen.

_Lagenospermum Sinclairi_ (Arber ex Kidston +MS.+).

Although it is not certain that these seeds are morphologically identical with the genus _Lagenostoma_, a brief description is intercalated here as the habit of the seed-bearing axes supplies a probable key to the habit of the fertile fronds of _Lyginopteris_. The type-specimens were collected by Mr Sinclair from the Lower Coal Measures of Ayrshire, Scotland, and recorded by Kidston as _Lagenostoma_ sp.: they were afterwards named by him in manuscript _L. Sinclairi_ and handed to Dr Arber for description. The seeds are elliptical-oblong, 4–5·5 × 1·5–3 mm., radially symmetrical and enclosed by a loose envelope which is longitudinally ribbed and divided distally into several linear-lanceolate lobes (fig. 408, A, A′). This covering, though much longer than the cupule of _Lagenostoma Lomaxi_, is probably a homologous structure. The most interesting point is the attachment of the seeds to slender branches of a compound axis (fig. 408, A). It is probable that the seeds were borne on a frond characterised by the reduction or complete abortion of the sterile lamina or perhaps, as in the recent Fern _Thyrsopteris elegans_[180], some of the pinnae of a large compound frond were fertile. It is worthy of note that Arber recognised pinnules of _Sphenopteris obtusiloba_[181] in association with _L. Sinclairi_, a fact, as he says, in itself of no value but which acquires significance in view of the discovery by Carpentier[182] of cupules in close proximity to the same species of frond. Specimens described by Dr Stopes from Westphalian rocks of New Brunswick as _Pterispermostrobus bifurcatus_[183] bear a close resemblance to _L. Sinclairi_.

_Lagenospermum oblongum_ (Kidston).

The species recently described by Dr Kidston[184] as _Lagenostoma oblonga_ from the South Staffordshire coal-field appears to be closely allied to Arber’s _L. Sinclairi_: it is represented by pairs of seeds borne at the ends of forked branchlets: the seed is 2·5 mm. long by 1·5 mm. broad and is surrounded by a longer oblong cupule divided distally into 6 free lobes.

A larger type of seed, 3 cm. long and 2·5 cm. broad, is described by Kidston[185] from the same coal-field as _Lagenostoma? urceolaris_. A characteristic feature is the truncate apex surrounded by a prominent canopy formed of the expanded apical free portion of the integument. The lack of anatomical data in both these seeds is a reason for the substitution of some less committal term than _Lagenostoma_.

Grand’Eury[186] and Carpentier[187] have published accounts of impressions of seeds from the Coal Measures of France compared by them with species of _Lagenostoma_ though not assigned to new species. These and similar seeds should be referred to Nathorst’s genus _Lagenospermum_.

The difficulty of recognising the true nature of seed-like impressions is illustrated by some specimens in the Goldenberg collection in Stockholm described by Arber[188] as _Carpolithus Nathorsti_: these consist of pieces of _Sphenopteris_ pinnae probably, as Zeiller suggested, _Sphenopteris Schaumburg-Lippeana_ (Stur) bearing at the ends of the segments of deeply divided pinnules what appeared to be seeds 1 mm. long, oval and longitudinally ribbed, and possibly enclosed in a cupule. Arber considered the ‘seeds’ to be related to _Lagenostoma_, probably belonging to some member of the Lyginopterideae. An examination of the specimens by Nathorst[189] showed that the supposed seeds are collections of spores; but whether the spores of a true Fern or the microspores of a Pteridosperm cannot be determined.

_Pterispermostrobus_ Stopes.

_Pterispermostrobus bifurcatus_ Stopes.

Dr Stopes[190] has recently called attention to a resemblance between specimens from the Westphalian of New Brunswick, described by her as _Pterispermostrobus bifurcatus_, and _Lagenospermum Sinclairi_. The New Brunswick fossil is made the type of a new genus _Pterispermostrobus_, which is employed for fructifications of Pteridosperms that cannot be associated with a known species of parent and may be either seeds or complex male organs borne on a definitely branched rachis. The type-species is represented by a slender axis bearing lateral branches divided into two widely divergent arms each of which bears a terminal body, 4 × 3 mm., characterised by 3–5 apical lobes extending 2 mm. beyond the distal end of the seed-like organ and resembling a cupule. In this as in many other cases it is impossible to determine the true nature of the reproductive bodies, whether they are small seeds or groups of microsporangia: the new generic name serves a useful purpose though it is not always possible definitely to refer doubtful fructifications of this kind to a Pteridosperm. The organs in question may also be compared with _Codonotheca_[191].

_Pterispermostrobus pusillus_ (Nathorst).