J Hattori Bot. lab. No. 75: 15- 22 (Feb. 1994)

A RE-EVALUATION OF FISSJDENS SUBGENUS PACHYFISSJDENS, WITH A DETAILED DISCUSSION OF FISSIDENS GRANDIFRONS AND F GEIJSKESII

1 2 RONALD A. PURSELL AND BRUCE H. ALLEN

ABSTRACT . Subgenus Pachyfissidens, lectotypified by Fissidens grandifrons Brid., is based essen­ tially on plants with stiff leaves and pluristratose laminal cells. It is an unnatural and taxonomically superfluous taxon. Species assigned to this subgenus are placed in subgenus Fissidens section Aloma C. Miill. (Fissidens sedgwickii Broth. & Dix.), section Amblyothallia C. Miill. (Fissidens grandifrons Brid.), section Crispidium C. Miill. (Fissidens strictus Hook. f. & Wits.), and section Fissidens (Fissi­ dens rochensis Broth. and F. ventricosus Lesq.), subgenus Serridium (C. Miill.) lwats. (Fissidens boninensis lwats., F. jaiorum Whitt. & Mill., and F. perdecurrens Besch.), and subgenus Sarawakia (C. Miill.) lwats. (Fissidens geijskesii Florsch.).

Pachyfissidens, established as a section of Fissidens Hedw. by Muller (l 848), was rec­ ognized as a subgenus by Kindberg ( 1897) and later accepted at this level by Brotherus ( 1901, 1924) in his widely adopted system of classfication. The taxon is distinguished by its rigid leaves, pluristratose laminal cells, an absence of a central strand in the stem, and estomate capsules. Pachyfissidens is here lectotypified with Fissidens grandifrons Brid., Sp. Muse. I : 170. 1806. (Lectotype. In Nova Anglia habitat, without collector, B). Bruggeman-Nannenga (1974) demonstrated that the pluristratose lamina! cells and lack of a central strand are also found in species that unquestionably belong to subgenus Fissidens. Furthermore, estomate capsules are found in the subgenera Octodiceras (Brid.) Broth. and Sarawakia (C. Miill.) lwats., with both stomate and estomate capsules occuring in some members of the latter subgenus. In Sarawakia the estomate condition was consid­ ered a feature influenced by habitat (Pursell et al. 1988). Nevertheless, despite its lack of any uniquely defining characters, Bruggeman-Nannenga maintained Pachyfissidens as a section in subgenus Fissidens. Recent data derived from SEM studies on the p~ristome (Allen 1980, Bruggeman­ Nannenga & Berendsen 1990) and light-microscope studies on the costa (Bruggeman-Nan­ nenga 1990, Stone 1990) have been shown to be valuable in understanding the infra-gener­ ic relationships of Fissidens. These two features frequently appear coordinated throughout Fissidens and are here used in a re-examinations of Pachyfissidens. Pachyfissidens throughout its history has been a depository for species that share a similar type of habitat, i.e., submersion in rapidly running water. The principal features of this group appear to represent a cluster of convergent characters rather than a suite of coor­ dinated characters indicative of a natural relationship. Nine species of Fissidens are

1 Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, Pennsylvania 16802- 530 I, U.S.A. 2 Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166-0299, U.S.A. 16 J. Hattori Bot. Lab. No. 75 I 9 9 4 presently placed in Pachyfissidens, i.e., F boninensis Iwats., F geijskesii Florsch., F gran­ difrons Brid., F jaiorum Whitt. & Mill., F rochensis Broth., F perdecurrens Besch., F sedgwickii Broth. & Dix., F strictus Hook. f. and Wils., and F ventricosus Lesq. The pur­ pose of this paper is to discuss these species and their taxonomic positions. Fissidens grandifrons is a widely dispersed aquatic species in the Northern Hemi­ sphere. Although gametophytically specialized for an aquatic habitat, e.g., the long-stalked archegonia (lwatsuki & Suzuki 1982) and thick imbricate leaves, the species has retained a terrestrial sporophyte, i.e., one having a long exserted seta. Such a sporophyte usually has stomata in the capsule. However, we have not been able to demonstrate the presence of stomata in the few sporophytes of F. grandifrons available for study. But, this combination of terrestrial and aquatic sporophytic features is not unique. The same combination of fea­ tures can be found in Dichelyma Myr., a genus in the Fontinalaceae with setae up to 20 mm in length and estomate capsules. The peristome of F. grandifrons has been described as belonging to the taxifolius-type (Bruggeman-Nannenga & Berendsen 1990). This type is commonly found in section Ser­ ridium C. Miill. [=subgenus Serridium (C. Miill.) Iwats.], but it also occurs in section Am­ blyothallia C. Miill. There is, however, no concensus on the peristome types in these two sections. Allen (1980) concluded that species of both sections had the same basic type, i.e. the taxifolius-type. Bruggeman-Nannenga and Berendsen (1990), on the other hand, recog­ nized two basic types of peristomes in these two sections, the taxifolius-type and the sim­ iliretis-type, with the former having three variations. They considered the taxifolius-type characteristic of Serridium while the similiretis-type was found mainly in Amblyothallia. However, these types of peristome were not restricted to one section or the other. To the contrary, some species of Serridium were found to possess a similiretis-type peristome and species of Amblyothallia were found with a taxifolius-type peristome. Recently, Stone (1990), upon examining some Australian species, thought that only one type of peristome was represented in Serridium and Amblyothallia. The lanceolate leaves of F. grandifrons (Fig.1) are usually tightly imbricate and stiff. A recent examinations of specimens from sites throughout the range of the species, however, has revealed that there is considerable variation in leaf thickness and costal structure. Mar­ ginal lamina! cells in the distal part of the leaf can be unistratose (Figs. 2, 3, 8, 12, 14), bis­ tratose (Figs. 6, 10), and even quadristratose (Fig. 5). The interior lamina! cells can be bis­ tratose (Fig. 14), pentastratose (Fig. I 0), hexastratose (Fig. 12) to pluristratose (Fig. 5). Moreover, the subsurface lamina! cells are generally larger than the surface cells. The basic structure of the costa includes three stereid bands in the proximal part of the leaf. A ventral and two lateral stereid bands are evident in Figs. 3, 4, and 13 (the ventral band in this last figure is interrupted) and also in the illustration in lwatsuki and Suzuki (1982, Plate LIII). The ventral band can be reduced to a single file of stereid cells (Figs. 7, 15) or it can be missing (Figs. 9, 11). There are basically two stereid bands in the distal part of the leaf (Figs. 6, 8, 12), although one can be lost (Figs. 10, 14), or both can be eliminated (Fig. 5), in which case the costa consists of more or less homogeneous cells. In both the proximal and distal parts of the leaf the lateral stereid bands may fuse (Figs. 2, 11 ; see also Fig. 45F R. A. PURSELL & B. H. AL LEN: A re-evaluation of Fissidens subg. Pachyjissidens 17

Figs. 1- 5. Fissidens grandifrons Brid. 1. Habit sketch of a leaf. 2, 5. Transverse sec­ tions of distal part of leaf. 3- 5. Transverse sections of proximal part of leaf. [1 - 3 from Pursell, Allen & Magill 10984, PAC; 4-5 from Frye: Moss Exsiccati 25, PAC] 18 J. Hattori Bot. Lab. No. 75 1 9 9 4

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s~. ?o~ § 9 gO•Oo' • o' · ·~ ~·• •• o :·o~ o ~~a ~0r- 6

15

a8Q'.j 0 JJfm 14 ~D.o~··@ Q ~o o ~ 'J/013 12 Figs. 6-15. Fissidens grandifrons Brid. 6, 8, 10, 12, 14. Transverse sections of distal part of leaf. 7, 9, 11, 13, 15. Transverse sections of proximal part of leaf. [6-7 from Wilson 1909, PAC; 8- 9 from Sharp, Clebsch & Thornburgh 2230, PAC; 10- 11 from Bruggeman­ Nannenga 406, PAC; 12- 13 from Lin 12831 , HIRO; 14- 15 from Higuchi 20162, HIRO] R. A . PURSELL & B. H. A t.,LEN : A re-evaluation of Fissidens subg. Pachyfissidens 19 in Crum & Anderson 1981 ). The type of costa that is found in F grandifrons has been shown (Bruggeman-Nannen­ ga 1990, Stone 1990) to be a unique feature of section Amblyotha/lia. Most species of Fis­ sidens have a costa that has two stereid bands throughout its length, but in Amblyotha/lia there are three stereid bands in the proximal half of the leaf, two lateral and one ventral, separated usually by more than three enlarged cells (we include in this term 'guide cells,' 'deuters,' 'conjunctivae,' and 'conductivae' of authors). Therefore, in view of its costal structure, F grandifrons is hereby transferred to section Amblyotha/lia. Specimens examined. Taiwan. Pingtung Co. : Lai 9850 (NY); Taichung Co.: Lai 8699, c.fr. (NY); Taitung Co.: Lai 9651 (NY), Lin 12831, c.fr. (HIRO). Pakistan. Northwest Frontier Prov.: Haghan Valley, Higuchi 20162, c.fr. (HIRO). France. Hautes-Pyrenees: Bruggeman-Nannenga 406 (PAC). U.S.A. California. Mendocino Co. : Wilson 1909 (PAC). Idaho. Fremont Co. (?):Frye: Moss Exsiccati 25 (PAC). Missouri. St. Frarn;ois Co.: Pursell, Allen & Magi/110984 (PAC). Mexico.: Oax­ aca: Sharp, Clebsch & Thornburgh 2230 (PAC). Fissidens geijskesii is known from only the type collections made in Suriname, north­ ern South America. Its leaves (Fig. 16) are similar in shape, arrangement, and texture to those of F. grandifrons. The costa of F. geijskesii in transverse section, however, reveals two stereid bands throughout its length (Figs. 17, 18), separated distally by two enlarged cells and proximally by three or more enlarged cells. The costa is similar to the bryoides-type (Bruggeman-Nannenga 1990) which is found in all groups of Fissidens except sections Amblyothallia and Crispidium C. Miill., and subgenus Serridium. The sporophyte of F. geijskesii has an immersed estomate capsule and a very short seta (0.4 mm long), a feature found only in the aquatic subgenera Octodiceras and Sarawakia. The peristome of F geijskesii is fragile and missing from the holotype, paratypes, and most isotypes. There is, however, an isotype in LAF in which the peristomes are intact. The teeth are reduced, i.e., undivided or irregularly divided, and are papillose throughout their length. Reduced peristomes are found scattered throughout Fissidens, but they are characteristically found in members of Octodiceras and Sarawakia. The peristome of F. geijskesii is most similar to that of F. stissotheca Broth. var. im­ mersus (Mitt.) Pursell, Brugg.-Nann. & Allen, a member of Sarawakia found in southeast­ ern Brazil and Paraguay (Pursell et al. 1988). Indeed, the two peristomes differ only in their ornamentation. In F. stissotheca var. immersus delicate spirals on the teeth may or may not be obscured by papillae, while in F. geijskesii such spirals are not evident. Fissidens subgenus Sarawakia (Pursell et al. 1988) presently has only three species, all of which have unistratose lamina! cells, unlike the pluristratose lamina! cells of F. gei­ jskesii. However, the layers of lamina! cells of F geijskesii are here interpreted as represent­ ing a habitat-induced character, i. e., a selection for submersion in swiftly flowing water, rather than a character of great phylogenetic importance. On the basis of the internal struc­ ture of its costa, immersed capsules, and peristome we hereby transfer F geijskesii to sub­ genus Sarawakia. Specimens examined. Suriname. Paloemeu River, on rocks in shade, between high and low water mark in Trombaka Fall s, Geijskes s.n. (U holotype; H, LAF, MO isotypes), Gei­ jskes s.n. (LAF, MO paratypes). 20 J. Hattori Bot. Lab. No. 75 I 9 9 4

16

Figs. 16-18. Fissidens geijskesii Florsch. 16. Habit sketch of leaf. 17. Transverse sec­ tion of distal part of leaf. 18. Transverse section of proximal part of leaf. [ 16 from Geijskes s.n., isotype LAF; 17- 18 from Geijskes s.n., paratype MO]

Fissidens rochensis Broth. is endemic to the West Indian islands of Jamaica, Puerto Rico, Hispaniola, Guadeloupe, and Dominica. The species was transferred to section Bry­ oidium C. Miill. (=section Fissidens) by Bruggeman-Nannenga (1974) on the basis of its bordered (Jim bate) leaves and central strand. Heretofore, the species has been known only gametophytically, but sporophytes have been found in a recent collection from the Domin- R. A . PuRSELL & B. H. A LLEN: A re-evaluation of Fissidens subg. Pachyfissidens 21 can Republic (Buck 5352 NY). The sporophyte is the terrestrial-type, i.e. seta long and exserted with stomate capsules. The peristome is of the bryoides-type (Allen 1980, Bruggeman-Nannenga & Berendseon 1990) which additionally supports its position in subgenus Fissidens section Fissidens. Fissidens ventricosus Lesq., endemic to the Pacific Northwest of North America, was for many years considered to be the same as the European F rufalus B.S.G. Ireland and Schofield (1967) demonstrated that these two species are distinct, and on the basis of its bistratose lamina) cells they placed F ventricosus in Pachyfissidens. Nevertheless, its well­ developed limbidium, bryoides-type peristome, and costal structure indicate that the species belongs in subgenus Fissidens section Fissidens where it was transferred by Bruggeman-Nannenga and Berendsen (1990). Fissidens sedgwickii Broth. & Dix. is a tropical Asian species with a scariosus-type of peristome (Bruggeman-Nannenga & Berendsen 1990). On the basis of its peristome type, smooth lamina) cells and semilimbate leaves they suggested that the species belonged in section Aloma C. Miill. They considered, however, the presence of pluristratose leaves, an estomate capsule, and the lack of a central strand in the stem to be anomalous features that made the species difficult to place. As noted above, we consider these features to be of minor phylogenetic importance and therefore consider the species properly placed in sub­ genus Fissidens section Aloma. Fissidens perdecurrens Besch. and F boninensis Iwats. (Inoue 18819, isotype NY) are two eastern Asian species for which sporophytes are unknown. Iwatsuki and Suzuki (1982) considered these species closely related, differing only in the presence of larger ( 10-17 µ.m vs. 7- 10 JLm), irregularly bistratose lamina) cells in F boninensis. These two species are considered together in the following discussion. Although lwatsuki and Suzuki ( 1982) considered F perdecurrens related to F gemini­ florus Dozy & Molk., they placed it closer to F grandifrons because both species had mul­ tistratose laminal cells and somewhat longer surface cells at the median part of the costa. However, F perdecurrens and F boninensis have only two stereid bands in the costa, and for this reason we consider these species distantly related to F grandifrons. Fissidens geminifiorus was placed in Serridium by Iwatsuki and Inoue (1984). We consider the relationship of F perdecurrens and F boninensis to be with that species and therefore transfer them to subgenus Serridium. Fissidens jaiorum Whitt. & Mill. (Whittier 2936, isotype PAC), for which sporophytes are unknown, is endemic to Tahiti. Inoue and Iwatsuki (l 969) compared this species with F boninensis and found it to consist of smaller plants with a shorter costa. These two species are similar in lamina) cells and costal structure. We consider the species to be close to F boninensis and therefore transfer it to subgenus Serridium. Fissidens strictus Hook. f. & Wils., known only from Victoria and Tasmania in Aus­ tralia, was not available for examination. However, based on recent notes and illustrations by Stone (1990), the costa has two stereid bands throughout its length that are separated distally by two enlarged cells and proximally by several enlarged cells. This corresponds with the taxifolius-type of costa described by Bruggeman-Nannenga (1990). Peristomes 22 J. Hattori Bot. Lab. No. 75 I 9 9 4 studied by Stone were variable but were most like the zippelianus-type (Bruggeman­ Nannenga & Berendsen 1990) that is characteristic of section Crispidium. On the basis of its costal structure and peristome the species is transferred to subgenus Fissidens section Crispidium.

ACKNOWLEDGMENTS We thank the curators of the herbaria listed in the text for making available the num­ ber of critical specimens examined. Special thanks go the H. 0. Whittier and H. A. Miller (University of Central Florida) for sharing with us an isotype of Fissidens jaiorum. Support for this research was from the National Science Foundation through Grant BSR- 8905431 .

LITERATURE CITED Allen, B. H. 1980. Peristome variations in the genus Fissidens: an SEM study. Bryologist 83: 314- 327. Brotherus, V. F. 1901 . Fissidentaceae. In: A. Engler & K. Prantl (eds.). Die Natiirlichen Pflanzenfami­ li en 1 (3): 351 - 363. Leipzig. Brotherus, V. F. 1924. Fissidentaceae. Jn: A. Engler & K. Prantl (eds.). Die Natiirlichen Pflanzenfami­ lien 2, 10: 143- 155. Leipzig. Bruggeman-Nannenga, M. A. 1974. On the characterization and the taxonomic status of the group of Fissidens species known as Pachy.fissidens. Proc. Kon. Ned. Akad. Wetensch. C, 77: 141 - 148. Bruggeman-Nannenga, M. A. 1990. On the anatomy of the costa of Fissidens. Trop. Bryol. 3: 37-44. Bruggeman-Nannenga, M. A. & W. Berendsen. 1990. On the peristome types found in the Fissiden­ taceae and their importance for the classification. J. Hattori Bot. Lab. 68: 193- 234. Crum, H. A. & L. E. Anderson. 1981 . Mosses of Eastern North America, vol. 1. New York. Inoue, H. & Z. Iwatsuki. 1969. Bryophytes of the Bonin Islands and the Volcano Islands (1). Bull. at!. Sci. Mus. Tokyo 12: 291 - 309. Ireland, R. R. & W. B. Schofield. 1967. Fissidens ventricosus in North America. Bryologist 70: 257- 261 . Iwatsuki, Z. & S. Inoue. 1984. Cytotaxonomic studies of the Japanese species of Fissidens Hedw. (Musci). J. Hattori Bot. Lab. 57: 343- 362. Iwatsuki, Z. & T. Suzuki. 1982. A taxonomic revision of the Japanese species of Fissidens (Musci). J. Hattori Bot. Lab. 51 : 329- 508. Kindberg, N. 1897. European and N. American Bryineae (Mosses), Part I. Linkoping. Muller, C. 1848- 1851 . Synopsis Muscorum Frondosorum. Pars Prima et Secunda. Berlin. Pursell, R. A., M. A. Bruggeman-Nannenga & B. H. Allen. 1988. A taxonomic revision of Fissidens subgenus Sarawakia (Bryopsida: Fissidentaceae). Bryologist 91: 202- 213. Stone, I. G. 1990. Fissidens, sections Crispidium, Amblyothallia and Serridium and subgenus Pachy­ .fissidens in Australia: some taxonomic changes and a key to species. J. Bryol. 16: 245- 260.