OBSERVATIONS ON THE GENERA PHEGOPTEPdS, PSEUDOPHEGOPTERIS AND MACROTHEL YPTERIS

BY PRAKASH CHANDRA (National Botanic Gardens, Lucknow)

Received June 2, 1972

(Communicated by Dr. T. N. Kho shoo, r.A.s¢. )

ABSTRACT

Morphology of seven species of exindusiate thelypteroid belong- ing to three genera, viz., , Pseudophegopteris and Macrothelyp- teris is described. The paleae are gland-tipped except in M. ornata, P. hexagonoptera and P. decursive-pinnata where it is non-glandular. The dictyostele consists of 2-4 vascular strands. The lamina bears reduced scales (sometimes branched) mixed with the hairs, both acievlar and glandular. The sori are usually exindusiate; in P. decursive-pinnata the indusium is modified into tufts of fascJculated hairs whereas in M. torre- siana a small fugaceous indusium is present. The trichomes are borne on the capsule wall only. Spores are of bilateral type aad usually peri- hate. The exine is smooth or verrucate; in P. aurita and P. pyrrhorhachis it bears narrow ridge-like irregular reticulations. In M. ornata, the exine as well as perine are spinulose. It is concluded that the exindusiate species are quite distinct from the other members of the family and constitutes a natural group.

INTRODUCTION THE exindusiate thelypteroid ferns have been variously circumscribed under the genera Phegopteris, Pseudophegopteris and (Ching, 1936, 1963; Iwatsuki, 1965; Holttum, 1969). Of the three known species of the Phegopteris, the two (P. hexagonoptera, P. connectilis) are distri- buted throughout the North temperate zone and one (P. decursive-pinnata) in S.E. Asia. Ching (1963) assigned 10 species each to the genera Pseudo- phegopteris and Macrothelypteris. However, Holttum (1969)ascribed 20 species under the genus Pseudophegopteris. From India, 8 exindusiate species were recorded by Beddome (1892). There is much confusion with regard to the phylogeny and relationship of the exindusiate species of thelypteroid ferns. But for the little informa- 68 Genera Phegopteris, Pseudophegopteris and Macrothelypteris 69 tion available (Chandra, 1963 ; Nayar and Chandra, 1965) not much is known about this group. The present study was undertaken for the better under- standing of this group of ferns and deals with 7 species, viz., (Michx.) Watt, P. decursive-pinnata (Van Mall) Fee, P. hexa- gonoptera (Michx.) Fee, Pseudophegopteris aurita (Hook.) Citing, P. pyrrhorha. chis (Kze.) C/ling, Macrothelypteris ornata (Wall ex Bedd.) Ching and M. torresiana (Gaud.) Ching. All the species are mesophytic terrestrial ferns growing mostly in exposed or partially shaded forest beds. M. ornata and M. torresiana are generally restricted to semi-marshy areas near the streams and waterways and occur usually as isolated . The plants of P. aurita and P. pyrrhorhachis, however, form shaggy Loose_colonies with the individual plants rather sparse and often mixed with dense vegetation.

MATERIAL AND METHODS The plants were collected mainly from Khashi and Jaintea Hills and N. Cachar Hills of Assam. In the case of M. torresiana, the fresh material was used from the plants growing in the fernery of N.B.G. The herbarium speci- mens of P. connectilis and P. decursive-pinnata were procured from Makino Herbarium, Japan and from the herbarium of Fred G. Floyds, England. The spore morphology was studied from acetolysed preparations as well as from fresh spores mounted in glycerine jelly.

OBSERVATIONS The rhizome is generally wide creeping except in M. ornata and M. torre- siana where it is short, stout and ca. 2-3.5 cm across; it is usually suberect in P. decursive-pinnata. The paleae mixed with the unicellular acicular hairs cloth the leaf bases and the surface of the rhizome. They are basally attached, non-clatherate, ovate-lanceolate and usually gland-tipped as in P. aurita (:Figs. 1, 11), P. pyrrhorhachis (Fig. 3), P. connectilis (Fig. 2) and M. torresiana (Fig. 9). In M. ornata (Figs. 5, 15), P. hexagonoptera (Fig. 4) and P. decursive, pinnata (Fig. 6) the apex of palea is non-glandular and terminated by an elon- gated thick-walled, acicular hair. The paleae are profusely hairy; the elon- gated acicular hairs are borne all over the margin (sometimes on the surface as in P. connectilis) of the paleae. In addition, unicellular, capped papillate hairs with hyaline protoplasmic contents occur on the margin of the palea. In P. aurita a few large, subglobose, unicellular hairs mixed with the papil- late ones are borne on the margin of the young palea ; in some cases some of Acad. B2 70 PRAKASH CHANDRA these hairs may be stalked. These hairs are different from the papillate ones in being larger, swollen, with yellowish contents and devoid of any secretion.

The palea originates as a uniseriate hair-like appendage composed of short discoid cells (Fig. 7). Early in the development, the terminal cell becomes much inflated, balloon-like and acquire dense nearly hyaline cytoplasmic contents (Figs. 8-11). However, in M. ornata, the terminal cell instead of swolling into a glandular structure, elongates excessively becoming acicular hair with slightly swollen base (Figs. 12-15). The marginal papillate and glandular hairs are developed early when the body of the palea is 4-8 cells broad (Figs. 9-11, 15).

The ground tissue of the rhizome is parenchymatous with dense deposits of starch (Figs. 17, 19, c). The sclerenchyma strands are entirely absent in the ground tissue of the rhizome. The vascular cylinder is a dictyostele, dissected usually into 2 broad ribbon-shaped meristeles (Fig. 18) by spirally arranged leaf gaps ; in P. com~ectilis and P. sexagonoptera, the meristeles are sometimes 3-4 in a transverse section. Xylem tissue usually consists of 1-4 rows of large metaxylem tracheids (Figs. 17, 19, rex) and small scattered groups of protoxylem on its outer surface. The phloem is scanty compared to the massive xylem on all the sides (Figs. 17, 19, ph). Pericycle is usually 2-3 layered (Fig. 19, p). Endodermis is well differentiated and consists of a single layer of radially compressed cells with their radial walls slightly thickened (Figs. 17, 19, n). The leaf gaps are short in most of the species except in the case of long creeping rhizome (P. aurita) in which it is much elongated. Branch- ing of the rhizome is fairly common in the species having creeping rhizome and is of the sub-dichotomous type with the stelar cylinder splitting nearly equally into two (Fig. 22, bg).

The leaves are usually simply pinnate except in M. ornata and M. torresiana where it is characteristically decompound. The stipe is glabrous, usually devoid of scales ; in hi. ornata the stalks of the paleae persist as warts making the surface of the stipe sub-muricate. In some species like M. torresiana the surface of the mature stipe has a prominent waxy covering; the stipe when young, however, bears unicellular glandular hairs all over the surface. The ~ascular supply of the slipe consists of a pair of broad, ribbon-shaped, ltea- rally placed vascular strands (Fig. 21). The xylem cells are usually 1-3 ceils thick and in some species the cells are highly corrugated (M. ornata, Fig. 20). The phloem surrounds the xylem on all the sides and in M. ornata groups of large secretory cells occur in the phloem tissue on the inner surface of the Genera Phegopteris, Pseudophegoptefis and Maerothelypteris 71 Y

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~' Ph ~ ~mx bZ ' l g 22 Fzos. 1-22. F~s. 1-2. Palea of P. attrita (Fig. 1) and P. eonnectilis (Fig. 2). Figs. 3-5. Apical region of the mature palea of P. pyrrhorhachis (Fig. 3), P. hexagonoptera (Fig. 4) and M. ornata (Fig. 5). Fig. 6. Palea of P. decursive-pinnata. Figs. 7-10. Stages in the development of palea of P. pyrrhorhachis (Fig 7), M. torresiana (Figs. 8, 9), P. aurita (Fig. 10). Fig. 11. Young palea of P. aurita. Figs. 12-15. Stages in the development of palea in M. ornata. F!g. 16. Marginal hairs on the young palea of P. ato'ita. Fig. 17. T.S. Rhizome of P. connectilis. Fig. 18. T.S. Rhizome of P. attrita. Fig. 19. A portion of the same showing cellular structure. Fig. 20. T.S. of the rachis of M. ornata. Fig. 21. T.S. of the stipe of M. ornata. Fig. 22. Vascular cylinder cf a portion of rhizome of P. aurita. (b, branch traces ; c, cortical cells ; e, epidermis; n, cndodermis; p, pericycle; bg, branch gap; lg, leaf gap; It, leaf trace; ph, phloem; rex, metaxylem.) 72 PRAKASH CHANDRA vascular strand opposite the protoxylem. These cells in the mature stipe may disintegrate forming lysigenous cavities filled with mucilage. The rachis is similar to the stipe in structure; it is muricate in M. ornata. In P. hexagonoptera, P. decursiPpinnata and P. connectilis elongated uni- cellular acicular hairs are profusely borne on the surface of the rachis; in other species the rachis is glabrous. The vascular bundle of the rachis is solitary, gutter-shaped and often with the base more or less flattened and the sides divergent (Fig. 20). The vascular supply of the secondary rachises and of the pinnae originate as intramarginal branches from the vascular strand of the main rachis. The pinnae are sessile and subopposite to alternate usually connected by a wing along the rachis. There is a prominent brown coloured elongated gland at the base of pinnae near the point of attachment to the rachis in P. aurita. The leaf lamina is usually herbaceous and thin in texture. Both the upper and lower epidermis are chlorophyllous. The cells of upper epio dermis are large and irregularly disposed. The anticlinal walls are broadly sinuous (Fig. 24). The lower epidermal cells are irregular and disposed more or less parallel to the veins. The anticlinal walls are deeply sinuous (Figs. 23, 25). Stomata are restricted to the lower epidermis and are of polocytic type (Van Cotthem, 1970). The mesophyll consists of 3 (M. ornata) to 6 layers of densely chlorophyllous parenchyma cells and in some species (M. torresiana, M. ornata) there is little differentiation between the upper and lower layers of mesophyll cells (Fig. 26). In all the species hairs are borne all over the midrib and the lateral veins on both the surfaces. They are usually unicellular, elongated, thick-walled and acicular ; in P. hexagono~,tera the hairs on the upper surface of the veins are short and spine-like. Sometimes, as in P. connectilis the hairs are septate (Fig. 27-a). Characteristic multicellular, uniseriate hairs crowned by much elongated thick-walled acicular cell occur on both the surfaces of the main veins in M. ornata. The club-shaped glandular haris (with an extracellular cap-like secretion at the apex) are borne all over the lower surface in M. ornata, P. connectilis and P. hexagonoptera; in M. torresiana these hairs are very pro- fuse and with copious secretion. Similar but smaller non-secretory papillate hairs also occur sparsely on the veins in P. aurita and P. pyrrhorhachis. In addition, characteristic reduced scales are borne on the lower surface of the midrib and the veins in M. ornata (Fig. 30), P. connectilis (Fig. 27-b) and P. decursive-pinnata. Among all the species, P. decursive-pinnata is most distinct in possessing various forms of characteristic irregular reduced scales Genera Phogopteris, Pseudophegopteris and Macrothelypteris 73

(Figs. 29, a-h). These scales are usually multicellular with one or two aeicular hairs on each component cell.

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37 ~,.- '~"40 ~41 FIGs. 23-41. Figs, 23-24. Lower (Fig. 23) and upper (Fig. 24) foliar epidermis of P. aurita. Fig. 25. Lower epidermis o f M. torresiana. Fig. 26. T.S. of lamina of M. ornata. Fig. 27. Acicular hairs (27, a) on the upper surface and reduced scales (Figs. 27-b) on the lower surface of midrib in P. connectilis. Fig. 28, a-f. Hairs on the margin of the pinna in P. connectilis. Fig. 29. Reduced scales (Fig. 29, a-h) on the lower surface of pinna in P. decurslre- pinnata. Fig. 30. Reduced scales on the midrib in M. ornata. Fig. 31. Indusit)m of P. deeursive- pinnata. Fig. 32. Sporangium of M. ornata. Figs. 33-35. The same of P. aurita. Fig. 36. The same of P. decurslve-pinnata. Figs, 37-41. Abaormal sporangia of M, torresiana, 74 PRAKASH CHANDRA

The margin of pinna consists of a row of large, sparsely chlorophyllous thin-walled cells. Unicellular acicular hairs similar to the superficial ones are borne on the margin of the pinna or lobe. In P. conneetilis a few multi- cellular, uniseriate (sometimes branched) hairs occur mixed with the uni- cellular, acicular ones, on the margin of the pinna. These hairs consist of 2-4 barrel-shaped cells crowned by a long thick-walled acicular cell,

Sporangia and Spores The fertile leaves are similar to the sterile ones. The sori are usually circular (shghtly elongated in P. aurita and P. pyrrhorhachis) and borne super- ficially over the secondary veins. Indusium is absent in all the species except in M. torresiana where a small fugaceous indusium occurs. The indusium in this species consists of thin-walled, slightly sinuous cells and are shed early during development. In P. decursive-pinnata no true indusium has been observed. In this case the indusium is modified into tufts of fasciculated hairs attached towards centre of the receptacle. These acicular hairs arc much elongated, slightly curved with a broad articulated base (Fig. 31),

The sporangia are of the common leptosporangiate type (Figs, 32-36). The stalk is two cells thick throughout except at the capsule base where there is a short third row of stalk cells in continuation with the stomium. In P. aurita, the third row is one cell long, in M. ornata and P. hexagonoptera it often extends up to the base of the stalk. The stomium is well developed and possesses prominent lip-cells. Annulus consists of 13-17 thick-walled indurated cells. In M. torresiana several abnormalities in the structure of annulus are met with; the annular ring is sometimes interrupted variously~ or occasionally bifurcated or forming irregular circles (Figs. 37-41). The sporangia bear trichomes on the capsule wall in all the species investigated. The trichomes are (i) elongated moderately thick-walled, acicular and (ii) thin- walled, glandular hairs with swollen apices crowned by an extracellular cap- like secretion. The intensity of these hairs varies with the species. In P. hexagonoptera, P. connectilis and P. decursive-pinnata (Fig. 39) usually 1-2 capped glandular hairs occasionally mixed with acicular ones are present on the capsule. Some species like M. ornata (Fig. 32) and M. torresiana possess only the papillate type of hairs; rarely in M. torresiana acicular hair may also be found. The sporangium of P. aurita is by far the most abundantly hairy ; the capsule wall often bearing up to 7 hairs, both the acicular and the papil- late types may be found together on the same sporangium (Figs. 33-35). Genera Phegopteris, Pseudophegopteris and Ma.crothelypteris 75 The spores are monolete, bilateral, piano to slightly concave-convex in the lateral view and elliptical in polar view. A distinct perine is present in most of the species except in P. connectilis (Fig. 47), P. decursive-pinnata and P. hexagonoptera. The perine is hyaline, smooth, rather loose and devoid of folds in P. aurita (Fig. 42) and P. pyrrhorhachis (Fig. 43), whereas in M. ornata (Fig. 45) the perine is minutely and sparsely spinulose and folded into lobate and flap-like folds; the folds are mostly parallel to the equatorial axis. In some species like M. torresiana (Fig. 44) the perine folds are short,

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FIGs. 42-47. Figs. 42-45, 47. Lateral view of the spores of P. aurita (FIB. 42), p.pyrrhorhaeMs (Fig. 43), M. torresiana (Fig. 44), M. ornata (Fig. 45) and P. connectilis (Fig. 47). Fig. 46. Spored©tin stratification in M, ornata. thick, ca. 4 tz tall, irregular and appearing conical in optical section. Exine is light brown and usuall) smooth except in P. ~,urita and P. pyrrhorhachis where the exine bears elongated, sparse, narrow ridge-like thickenings which often form an irregular faint reticulate pattern with large meshes. In P. conneetilis and P. hexagonoptera the exine consists of very small (ca. 1-3 t~ high, ca. 1-3 t~ across) irregularly arranged verrucae, whereas in M. ornata the exine bears straight or slightly curved spines with sharp apex (Fig. 46). On an average the size of spores in the different species is 24 x 40 # (P x E~) (exclusive of perine), 76 PI~KASH CHANDRA

Prothallus The present account is based on 5 species, viz., P. connectilis, P. aurita, P. pyrrhorhachis, M. ornata and M. torresiana. The spore germination is of the Vittaria-type and the prothallial development(Figs. 48-55) is Drynaria- type (Nayar and Kaur, 1968, 1969). The mature prothallus is cordate (Fig. 56) with deeply notched apex and overlapping wings (Figs. 57, 58), ca. 0.75 cm across. The thalli are profusely hairy bearing unicellular, papillate secre- tory hairs (Fig. 59) on the margin and the lower surface; the superficial hairs are larger than the marginal ones. Antheridia are produced from the fila- mentous stage onwards and are of the same type (Fig. 60) as reported by Verma and Khullar (1966). The structure and ontogeny of the archegonium are similar to those reported in advanced leptosporangiate ferns.

54 55

8

FIos. 48-60. Figs. 48-55. Stages in the development of prothallus in M. ornata (Fig. 48), P. pyrrhorhachis (Figs. 49, 50, 53), P. aurita (Fig. 51), P. conneetilis (Figs. 52, 55), M. torresiana (Fig. 54). Fig. 56. Mature prothallus of M. torresiana. Figs. 57, 58. Apical region of mature prethallus of M. ornata (Fig. 57) and P. conneetilis (Fig. 58). Fig. 59. Marginal hairs on mature prothallus of M. torresiana. Fig. 60. Antheridia of M. torresiana.

Discussion Only a few groups of ferns have perhaps suffered such taxonomical vicissitudes as the exindusiate thelypteroid ferns. Fee (1852) separated all the free-veined exindusiate species with Dryopteris-lJke habit into the genus Genera Phegopteris, Pseudophegopteris and Macrothelyptoris 77

Phegopteris. To the contemporary pteridologists (Ching, 1940; Copeland, t947; Holttum, 1954), who considered the loss of indusium in thelypteroid ferns to have taken place in numerous lines of evolution~ the genus Phegop- teris as such was untenable. Later, Ching (1963), while recognising the exindusiate species as a natural group divided them into three genera Phegop- teri~, Pseudophegopteris and Macrothelypteris. Holttum (1969, 1971) also recognised these as distinct genera showing no close relationship to any other member of the family. There is much confusion with regard to the circumscription and affinities of these geneca. According to Pichi-Sermolli (1970) there is no clear dis- tinction between Macrothelypteris and Pseudophegopteris and he, therefore, united the two under the generic name Macrothelypteris. Based on the pre- sent investigations, the Macrothelypteris species (M. torresiana, M. ornata) appear to be more primitive and quite distinct from the Pseudophegopteris species. Macrothelypteris are large ferns characterised by stout erect rhizome (rhizome devoid of sclerenchyma strands), large multicompound leaves, paleae profusely hairy and crowned by long acicular hair (M. ornata), papillate glandular hairs on the sporangia and interrupted annular ring in M. torresiana. The Pseudophegopteris species on the other hand are comparativel~ more advanced with their long creeping rhizome, acicular hairs mixed with the paleae, the paleae bearing large marginal glandular hairs, pinnae posses- sing cartilagenous margin, sPorangia profusely hairy; the hairs being acicular. Among the Phegopteris species presently investigated, P. decursive-pin- nata is most distinct in possessing conspicously reduced scales on the various parts of the . Also, there is much controversy with regard to the nature of the indusium in this species. According to Ching (1963) and Iwatsuki (1965), a true indusium is absent in this species but a cobwebby hairs are pre- sent in the centre of the sorus. However, according to Hotttum (1969), small caducous indusium is present in this species. During the present study; no true indusium was observed in this species. There are tufts of long acicular hairs attached to the centre of the receptacle. These hairs are much elongated, thick-walled with a broad base and tapered to a pointed apex.

With respect to the spores, the more primitive condition is apparently one in which the perine is absent as in P. decursive-pinnata, P. connectilis and P. hexagonoptera. From this primitive condition evolution appears to have been towards the development of perine~ increase in the folding and development of ornamentation on the perine. In P. aurita and P. pyrrhorha. 78 PRAKASH CHANDRA ehis, though the perine is well developed, it is smooth and devoid of folds. In these species the exine is well developed and bears ridge-like thickenings forming reticulations. Among all the species, M. ornata and M. torresiana are most advanced with respect to the nature of spores. The perine in these species is very well developed and variously folded; in M. ornata both perine and exine are spinulose.

It is concluded from the present studies that the exindusiate species are quite distinct from the other members of the family and constitutes a natural group.

ACKNOWLEDGEMENTS

Thanks are due to Dr. R. V. Sitholey, Director, National Botanic Gar- dens, for the encouragements and to Prof. B. K. Nayar under whose guidance part of this work was completed. I am indebted to Prof. R. E. Holttum for his valuable suggestions from time to time,

REFERENCES

Beddome, R. H. .. Handbook to the Ferns of British India, Calcutta, 1883 and 1892. Chandra, P. .. "Observations on the gametophyto and juvenile sporophyt¢ of Lastrea phegopteris and L. pyrrhorhachis," Sci. & Cult., 1963, 29, 259-60.

Ching, R. C. .. "Revision of Chinese and Sikkim-Himatayan Dryopteris with reference to some species from neighbouring regions, Part II," Bull. Fan. Mere. Inst. Biol., 1936, 81, 157-268. .. "On natural classification of the family Polypcdiacea¢," Sunyatsenia, 1940, 5, 201-68. .. "A reclassification of the family Tholypteridaceae from the main land of Asia," Acta Phytotax. Sinica, 1963,8,280-335. Co~land, E. B. .. GeneraFilicum, Waltham, Mass., U.S.A., 1947. Holttum, R. E. .. Flora of Malaya, Ferns, Singapore, 1954, p. 2. "Studies in the family ,". "fh© genera Phegopteris, Pseudophegopteris and Macrothelypteris," Blumea, 1969, 17, 5-32.

"" Studies in the family Thclypteridac~a¢. tIL A now systtm of g~neta i~ P-no Old World." Ibid., 1971, 19, 17-~2, Genera Phegopteris, Pseudophegopteris and Macrothelypteris 79

Iwatsuki, K. .. " of the thelypteroid ferns, with special reference to the species of Japan and adjacent regions. IV. Enume- ration of the species of Japan and adjacent regions," Mem. Coll. Sci. Univ. Kyoto, ]965, 31 ~3), 125-97.

Nayar, B. K, and '" The gametophyte of some species of La~trea Bory.," J. Indian Chandra, P. bot. Soc., 1956, 44, 84-94...... and Kaur, S. "Spore germination in homosperous ferns," J. Palynology, 1968, 4, 1-14. "Types ofprothalliat development it~ homosporous ~," Phytomor,phology, 1969, 19, 17°-88. Pichi-Sermolli, R. E. G. "Adumbratio Florae Aethiopicae. 5. Parkeriaceae, Adianta- ceae, Vittariaceae," d a Webbiu, 1957, 22, 645-703. Van Cotthem, W. R. J. "A classification of stomatal types," Bot. J. Linn. Soc., 1970, 63, 235-46.