Polish Botanical Journal 58(2): 475–480, 2013 DOI: 10.2478/pbj-2013-0057

Fissidens grandifrons: a possible explanation for the rarity of sporophytes

Ro n a l d A. Pu r s e l l 1 & Ja m e s R. Sh e v o c k

Abstract. Perigonia are described for the first time in grandifrons Brid. A possible explanation for the rarity of sporo- phytes in this species, the result of perigonial and perichaetial separated in different mats, is presented. Sexual reproduction in F. grandifrons is compared with that of F. perdecurrens Besch. and F. ventricosus Lesq. The peristome of F. perdecurrens is described for the first time. Key words: aquatic , Asia, California, Europe, Fissidens grandifrons, F. perdecurrens, F. ventricosus, North America, perichaetia, perigonia, peristome, rarity of sporophytes, rheophytes Ronald A. Pursell, Department of Biology, 208 Mueller Laboratory, The Pennsylvania State University, University Park, PA 16802, U.S.A.; e-mail: [email protected] James R. Shevock, California Academy of Sciences, 55 Music Concourse Drive, Golden Gate Park, San Francisco, CA 94118, U.S.A.

In t r o d u c t i o n

Fissidens grandifrons Brid. [subg. Pachyfissidens Taiwan, Pakistan, the western Himalayas, southern (Müll. Hal.) Kindb. sect. Pachyfissidens (Pursell India, and Siberia. Throughout the range of the & Bruggeman-Nannenga 2004)] is a large and species, however, sporophytes are rare, and have conspicuous aquatic species found principally been described and illustrated only from collec- in streams and springs of limestone geology or tions from Asia, the probable center of distribution aquatic systems with concentrations of calcium for the species. It is remarkable that a species with ions. The species has a circumpolar distribution such limited sporophyte production and no known in North America, Europe, and Asia. In eastern gemmae has attained such a broad distribution. North America the species ranges from Ontario Hill (1902), however, maintained that the species in Canada into the adjacent states Michigan and spreads by radiculose branches that are easily Wisconsin of the United States, and, south into detached in rapidly running streams. When en- the states of Alabama, Kentucky, Tennessee, Mis- countered, populations can be extensive, forming souri, and Arkansas. In western North America the large, robust colonies. Recent collections by the species extends from British Columbia in Canada second author in which perigonia were found in south into the states of Washington, Oregon, a California collection, and perichaetia and sporo- California, Nevada, Idaho, Montana, Utah, Wyo- phytes were found in a China collection prompted ming, and Arizona and also Mexico. In Europe a survey of the holdings of this species in MO to F. grandifrons is found in the Pyrenees mountains determine if these structures were present in other of southwestern France and northeastern Spain, collections of the species. The purposes of this southeastern Germany, north central Switzerland, paper are to report the finding of sporophytes in and the Caucasus of southern Russia. In Asia, the a collection from China; the finding of perigonial species occurs in Japan, China, northern Vietnam, and perichaetial plants; to describe and illustrate the perigonia and to describe the perichaetia; to 1 Corresponding author propose a possible explanation for the rarity of 476 POLISH BOTANICAL JOURNAL 58(2). 2013 sporophytes; to compare the sexual reproduction of AMERICA. U.S.A. Ca l i f o r n i a . Plumas Co.: Koch F. grandifrons with that of other dioicous aquatic 1893. Mi c h i g a n . Mecosta Co.: Smith B734. Mi s s o u ri . to rheophytic species of Fissidens, and to describe Carter Co.: Haggerty 2; Shannon Co.: Redfearn et al. the peristome of F. perdecurrens Besch. 703. CANADA. On ta ri o . Bruce Co.: Ireland 20598; Grey Co.: Mixley s.n., 7 July 1971. – ASIA. Ch i n a . Sichuan Province: Shevock 36240. Sp o r o p h y t e s o f Fissidens g r a n d i f r o n s Both perigonial and perichaetial plants are pro- in Ch i n a duced in Fissidens grandifrons, although never in Only three collections of Fissidens grandifrons great numbers and not in the same mat. Both types with sporophytes have been reported previously of plants are present in North America. However, in the literature: TAIWAN, Lin 8699 (Li 1985; perigonial plants were not found among those Pursell 2007), Lin 12831 (Iwatsuki & Suzuki, collections from Asia with sporophytes. Interest- 1982; Pursell 2007); PAKISTAN, Higuchi 20161 ingly, only perigonial plants were seen in Euro- (Pursell, 2007). These collections are in NICH. pean collections. The latter, however, may be due The second author found immature sporophytes to the small sample (three collections). In North from the following site in China: Si c h u a n Pr o v - American specimens, gametangia are present from i n c e . m u l i c o : Hengduan Mts., ca 10 km N of the the later part of June through mid-August. This is city of Muli, 28°00′32.3″N, 101°12′38.0″E, elev. also the case for the collection from France, but in 2550 m [ca 8366 ft], on vertical wall of a road bank the collections from Germany and Spain, perigonia with dripping water, Shevock 36240 (mo). are present on the plants in February. Sporophytes of Fissidens grandifrons are indeed rare. The MO holdings of the species d e s c rip t i o n o f t h e p e ri g o n i u m (including the one listed above) total 362 collec- Perigonial branches develop primarily on the out- tions. Iwatsuki and Suzuki (1982) examined 91 ermost stems of a mat. They are acropetalous in de- specimens from Japan, giving a grand total of 453 velopment and occur in rows in the axils of leaves collections of which approximately 0.009% had on both sides of the upper one-third of a stem, sporophytes. but they can also occur further down on the stem and in the axils of leaves of branches of the pri- Pe ri g o n i a a n d p e ri c h a e t i a in Fissidens mary stem. Mature perigonial branches protrude g r a n d i f r o n s from the leaves and are easily seen. At maturity, a perigonial branch is ca 2 mm long and consists Fissidens grandifrons is a species that once recog- of a short stem with lateral or basal rhizoids, and nized is probably not further examined in detail. the perigonium (Fig. 1). Two perigonial branches However, a close examination of the holdings are usually present in each axil; the second branch of the specimens in MO has resulted in finding originating from a small lower leaf on the stem of 11 collections (0.03%) with either perigonial or the primary perigonial branch (Fig. 1). The ma- perichaetial plants. Unfortunately, Iwatsuki and ture perigonial branches can easily detach from Suzuki (1982) did not record Japanese collections the parent stem or branch or be tightly attached. seen with perigonia or perichaetia. Usually four pairs of leaves make up a perigo- Sp e c i m e n s e x a m i n e d wi t h p e ri g o n i a : NORTH nium, the lowest pair is very small, ecostate or AMERICA. U.S.A. Ca l i f o r n i a . Siskyou Co.: Shevock nearly so, and either rounded or obtuse. Each of 40560. Ca n a d a . British Columbia: Queen Charlotte Is- the remaining leaves consists of two very broad lands, Schofield 45292. – EUROPE. Fr a n c e . Pyrénées- vaginant laminae, at least one of which is notched Orientales: Husnot, Musci Galliae 163. Ge r m a n y . at the place where it joins the proboscis i.e., costa Rheinland: Frahm 11361. Sp a i n . Huesca: Granzow de and very narrow dorsal and ventral laminae. The la Certa 2245. largest leaf is ca 1 mm long. All laminae are unis- Sp e c i m e n s e x a m i n e d wi t h p e ri c h a e t i a : NORTH tratose. Juxtacostally in the vaginant laminae there R. A. Pursell & J. R. Shevock: Fissidens grandifrons 477

Fig. 1. Fissidens grandifrons Brid. Two perigonial branches from a leaf axil on the parent stem. Lowermost leaf is small and ecostate (from Husnot, Musci Galliae 163). is a broad area of large, oblong, nearly hyaline six, the largest of which is ca 60 µm long. Para- cells (few chloroplasts) bordered by a broad area physes are absent. of small, mostly quadrate, chlorophyllose cells The presence of two perigonial branches (Fig. 2). Together, the two uppermost and largest present in the axil of a leaf is probably a rare perigonial leaves form a cup that envelopes the condition among aquatic Fissidens. Loosely at- very short stalked antheridia that number around tached perigonial branches were found in Shevock

Fig. 2. Fissidens grandifrons Brid. Single perigonial leaf showing the enlarged area of translucent cells (from Frahm 11361). 478 POLISH BOTANICAL JOURNAL 58(2). 2013

40560 from California, while in all three of the upstream to perichaetial plants, and the water flow collections from Europe they tightly adhered to strong enough to dislodge the loosely attached per- the stem. This perhaps indicates that at maturity igonial branches and transport them to the exserted the entire perigonial branch is detached or only perichaetial branches firmly attached to the parent the mature sperms are released. stems. Or, in the case when the perigonial branches are not detached, the sperm must be carried to the d e s c rip t i o n o f t h e p e ri c h a e t i u m perichaetial plants. This probably does not occur Perichaetial branches, like perigonial branches, are in plants in rapidly running streams but rather in found on the outermost stems of a mat, but are less those found along banks, in dripping water sites, or numerous. Like perigonial branches, the pericha- in splash zones where those collections with sporo- etial branches occur in the axils of leaves in the phytes or either perichaetial or perigonial branches upper one-third or lower of the parent stem where have been documented. Perigonial branches, or they protrude at maturity. A mature perichaetial the naked sperm, having survived this journey, are branch is ca 7 mm long and consists of a short stem probably directed downward into the perichaetium with basal rhizoids that firmly attach the branch to by the long rigid proboscides of the perichaetial the parent stem and 2–3 pairs of leaves. Each of leaves where they become lodged by the perigo- these leaves consists of a pair of broad, more or nial leaves close to the archegonia. Only then can less equal vaginant laminae that are occasionally fertilization occur. notched at the juncture with the long proboscis. The Fissidens grandifrons is streamlined for exist- uppermost pair comprises the perichaetial leaves, ence in its usual habitat of fairly rapidly running the larger of which is ca 6 mm long, and forms streams. The leaves are tightly imbricate, multistra- a cup that envelopes the archegonia. The vaginant tose (except the margins), and narrowly lanceolate laminae of these leaves are unistratose and consist with costae ending below the rounded apices; en- juxtacostally of a broad area of more or less hyaline tire margins; and, smooth cells, (Iwatsuki & Suzuki (few chloroplasts) cells bordered by a broad band 1982; Pursell & Allen 1994). The plants are rigid of much smaller, quadrate chlorophyllose cells. The and firm to the touch, and therefore, portions of ventral and dorsal laminae of the proboscides are plants eroded by abrasion during peak flows are bistratose. Paraphyses are absent. uncommon. Unlike other aquatic to rheophytic species, however, F. grandifrons has a terrestrial Se x u a l r e pr o d u c t i o n sporophyte – one with a long exserted capsule, but which is estomatose. On several occasions the first Sporophytes for many aquatic and rheophytic dio- author and Bruce Allen visited an area in eastern icous mosses throughout the world remain un- Missouri that seemed to be the perfect habitat for known or are rarely encountered. Based on the few sporophyte development. The stream has a modest specimens studied, there follows a discussion of flow and mats of the cover the bed of the the difficulty of sexual reproduction in Fissidens stream for some distance and extend onto the low grandifrons and why there are so few sporophytes banks. Neither perigonia nor sporophytes were produced. The probability of sexual reproduction ever found. Conditions for sexual reproduction of occurring in F. grandifrons apparently is extremely aquatic mosses, especially dioicous species, must low and among aquatic and rheophytic mosses is be rare indeed. Currently, nothing is known about perhaps the most difficult to accomplish. From the the ecological factors – light, temperature of the hundreds of collections of this species examined water, and nutrients – affecting the development only four had sporophytes, including the one re- of gametangia. Is a photoperiod involved, and, if corded here. Since the species is dioicous, plants so, do the hyaline cells of the vaginant laminae of of both sexes must be in proximity to one another. the perichaetial and perigonial leaves that admit And, since the species is in aquatic systems with diffuse light to the interior of the perigonia and flowing water, perigonial plants must be positioned perichaetia play a role in the maturation of the R. A. Pursell & J. R. Shevock: Fissidens grandifrons 479 gametangia? Aquatic species form linear distri- igonial branches were not observed. Mature sporo- butional patterns within the water column. The phytes were found in two collections or 0.05% of founder affect may also come into play depending the total of 40 collections, one from Japan and one on which sexual arrives first at a suitable from Taiwan. Perichaetial branches of F. perdecur- riparian area for colonization. The amount of un- rens are very similar to those of F. grandifrons. It suitable habitat between riparian systems can also can probably be safely assumed from their similar be formidable for a plant where gemmae are un- habitats, close similarity in vegetative features, known and spore dispersal through the production and perichaetial branch structure that the repro- of sporophytes is so infrequent. Fissidens grandi- ductive system in this species is similar to that of frons is an aquatic species that requires sufficient F. grandifrons. In addition, F. boninensis Z. Iwats. time in a hydrated state and the velocity of water in Inoue & Z. Iwats., known only from the Bonin flow over the plants probably also contributes to Islands, and F. pachyphyllus Dixon and F. nigro- a narrow window when successful fertilization viridis E. S. Salmon, known from Sawawak and could occur. Gametangia of both sexes would Borneo, respectively, may eventually be seen to need to develop about the same time. The cost of have a similar sexual reproductive system. producing gametangia when reproductive success The peristome of Fissidens perdecurrens, not seems extremely low may be another factor why seen by either Iwatsuki and Suzuki (1982) or Li these structures are so rarely observed in nature. (1985), is herein described for the first time. Sporophytes one per perichaetium. Setae Co m pa ri s o n wi t h t h e s e x u a l s y s t e m s smooth, to ca 12 mm. long; thecae ± inclined, o f o t h e r d i o i c o u s a q u at i c a n d r h e o p h y t i c ± bilaterally symmetric, ca 1 mm long; exothe- Fissidens s p e c i e s cial cells ± quadrate, thin-walled, stomatose in base of thecae; peristome taxifolius type, i.e., Two species were selected for comparison of their trabeculae prominent throughout a tooth, the sexual systems with that of Fissidens grandifrons, lower undivided part finely papillose dorsally, a species belonging to the same subgenus and sec- gradually changing to erect ornamentations at tion and a second species belonging to a different the bifurcation, and filaments with spiral orna- subgenus and section. mentation operculum long-rostrate, ± oblique, to ca 0.9 mm long. Calyptra cucullate, smooth, Fissidens perdecurrens Besch. naked, ca 1.1 mm long. Subg. Pachyfissidens (Müll. Hal.) Kindb. sect. Pachyfis- The sporophytes of Fissidens perdecurrens sidens (Pursell & Bruggeman-Nannenga 2004). differ essentially from those of F. grandifrons in This species is restricted to Japan, China, and the presence of stomata. The taxifolius type of Taiwan, where it occurs on dripping wet rocks or peristome is fully described and illustrated in Allen seasonally submerged in small streams. The spe- (1980), and Bruggeman-Nannenga and Berendsen cies is close to Fissidens grandifrons, differing (1990). essentially in a slightly smaller size, acute leaves Sp e c i m e n s e x a m i n e d wi t h s p o r o p h y t e s : Japan. that usually end in a small, hyaline cell, and promi- [Ho n s h u ] ôyama-saki, Tosa, S. Okamura 3750. nent guide cells in the upper part of the costa as – Taiwan. Hs i n c h u Co.: Shevock 41446. seen in surface view. Iwatsuki and Suzuki (1982) examined 43 specimens from Japan, all lacked Fissidens ventricosus Lesq. sporophytes but one [Iwatsuki & Suzuki 11801 from Honshu, Aichi-ken (NICH)] had perichaetial Subg. Fissidens Hedw. sect. Fissidens (Pursell & Brug­ geman-Nannenga 2004). branches. A total of 17 specimens in MO from China, Japan, and Taiwan were examined. Of these, This species is restricted to the Pacific Coastal only 6 from Taiwan had perichaetial branches. Per- Region of North America (British Columbia in 480 POLISH BOTANICAL JOURNAL 58(2). 2013

Canada, and the states of Washington, Oregon and zone or even those species seasonally submerged, California in the United States) with a disjunct may indeed have a few plants with sporophytes but population in the adjacent state of Idaho (Ireland their coloration can be similar or nearly identical & Schofield 1967), and is found on wet rocks be- to the gametophytes and grow parallel to the plants side streams and is often submerged in streams, so they can be easily overlooked. or exposed during low water levels. The species is characterized by smooth, unistratose to irregularly Ac k n o w l e d g e m e n t s . The use of microscopes and bistratose laminal cells, multistratose limbidia on imaging software at the Mishler Bryolab at UC that all laminae, and emergent capsules on thick, often generated the figures is greatly appreciated. We also geniculate setae. The perigonia and perichaetia are thank William Buck for reading an earlier version of terminal and at maturity neither is shed, unlike the the manuscript and offering valuable suggestions for its improvement. Comments provided by Ida Bruggeman- loosely attached perigonia of F. grandifrons. The Nannenga during the peer-review process enhanced the uppermost leaves of a perichaetial stem form the final version and is greatly appreciated. perichaetial leaves and differ from lower leaves only in being larger. A perigonium is nested be- tween the uppermost stem leaves and consists of Re f e r e n c e s one or two smaller perigonial leaves enclosing Al l e n B. H. 1980. Peristome variations in the genus Fissidens: the antheridia. Both perigonial and perichaetial An SEM study. Bryologist 83: 314–327. plants are usually intermingled, in contrast to their Br u g g e m a n -Na n n e n g a M. A. & Be r e n d s e n W. 1990. On counterparts in F. grandifrons so that fertilization the peristome types found in the and their is frequent. Sporophytes were present on 16 of the importance for the classification. J. Hattori Bot. Lab. 68: 46 (34.8%) specimens examined. 193–234. The genus Fissidens has a remarkable number Hi l l E. J. 1902. Fissidens grandifrons. Bryologist 5: 56–58. of species that are either aquatic or rheophytic and Ir e l a n d R. R. & Sc h o f i e l d W. B. 1967. Fissidens ventricosus occur on all continents except Antarctica. Several in North America. Bryologist 70: 257–261. of these rheophytic Fissidens are localized or re- Iwat s u k i Z. & Su z u k i T. 1982. A taxonomic revision of the gional endemics. Generally, populations of aquatic Japanese species of Fissidens (Musci). J. Hattori Bot. Lab. and rheophytic Fissidens can be locally common. 51: 329–508. In some cases, however, such as the exceedingly Li Z.-H. 1985. A revision of the Chinese species of Fissidens rare F. aphelotaxifolius Pursell, only a few collec- (Musci, Fissidentaceae). Acta Bot. Fenn. 129: 1–65. tions have been obtained and sporophytes remain Pu r s e l l R. A. 2007. Fissidentaceae. Fl. Neotrop. Monogr. unknown. In other Fissidens species only perigonia 101: 1–278. or perichaetia have been reported. There is a need Pu r s e l l R. A. & Al l e n B. 1994. A re-evaluation of Fissidens to examine aquatic and rheophytic Fissidens popu- subgenus Pachyfissidens, with a detailed discussion of Fissidens grandifrons and F. geijskesii. J. Hattori Bot. lations carefully in the field before making col- Lab. 75: 15–22. lections to determine if perigonia, perichaetia or Pu r s e l l R. A. & Br u g g e m a n -Na n n e n g a M. A. 2004. A re- sporophytes are present at that locality. Fissidens vision of the infrageneric taxa of Fissidens. Bryologist within aquatic systems, especially in the splash 107: 1–20.

Received 17 October 2013