Notes on the Dicnemonaceae (Musci): 11. the Status of Dicnemon Rugosum and Werneriobryum Geluense

Journ. Hallori BOI. Lab. No. 61. 273- 280 (1986)

NOTES ON THE DICNEMONACEAE (MUSCI): 11. THE STATUS OF DICNEMON RUGOSUM AND WERNERIOBRYUM GELUENSE

BRUCE H. ALLEN

ABSTRACT. The dicranaceous pcristomes. unicellular spores, and lack of both leaf nematogens and leaf rhizoids in Dicnemon rugosum and Werneriobryurn geluense make the placement of these species in the Dicnemonaceae untenable. Conversely, the presence of leaves with a hyaline border, well differentiated alar cells, smooth, elongated and porose leaf cells, dense tomentum, and polyseteous condition all indicate that these species are properly placed in the genus Dicranoloma. D. rugosum and D. gelURnse belong to an atypical element of Dicranoloma. Species belonging to this element are also present in New Zealand, Australia, and ew Guinea. Erroneously attributed to Australia, Dicranoloma rugosum is endemic to Tahiti; D. geluense is endemic to the high mountains of eastern New Guinea.

A Systematic Account of Dicranoloma rugosum Dicranoloma rugosum was originally described by Hooker (1818) as a species of Leucodon . At the time Leucodon represented a group of mosses ..... having the peristome of a Trichostomum or Didymodon (i.e. single), and lateral fruit (i .e. pleurocarpous) .. . ,. (Hooker 1818). Hooker considered the species closely allied to Leucodon calycinus (=Dicnemon calycinum) and due to the mitriform calyptra of L. calycinus provisionally established the genus Lyellia for the two species. It was not until 1824, however, that Schwaegrichen transferred the two species from Leucodon. By then the name Lye/fia had been validly published by Brown (1819) for another genus of mosses and Schwaegrichen placed both species into the genus Dicnemon. Most subsequent authors have maintained this species in Dicnemon (Muller 1849; Jaeger, 1872; Paris 1896, 1904; Brotherus 1901 , 1924; Whittier 1976; Miller, Whittier& Whittier 1978). Muller (190 I), after examining the type of Eucamplodon, transferred a Tahitian species he earlier had described as Dicnemon banksii into Eucamptodon. M uller gave no other reason for his transfer, and shortly thereafter Salmon (1902) placed Dicnemon banksii into the synonomy of D. rugosum. Alien (1985) in a revision of the Dicnemonaceae considered the family highly derived and characterized by (among other features) the presence of a complex and strongly modified peristome; massive, endosporically germinating protonemata (so called " multicellular spores"); and numerous leaf nematogens from which leaf rhizoids arise. Hooker's L. rugosum, however, has a typical dicranaceous peristome, unicellular, exosporically germinated spores, and lacks both leaf nematogens and leaf rhizoids. These features make the placement of L. rugosum in the Dicnemonaceae untenable.

1 Missouri Botanical Garden, P. O. Box 299, St. Louis, MO 63166. 274 Journ. Hattori Bot. Lab. No. 61 1 9 8 6

As indicated by its dicranaceous peristome, erect habit, well difTerentiated, inflated alar cells, and smooth, elongated and porose leaf cells this species belongs in the Dicranaceae. Within the Dicranaceae, its strongly sheathing perichaetial leaves are reminescent of Holomitrium. However, the presence of leaves with a hyaline border of elongated cells, its robust size, dense tomentum, smooth elongate, porose leaf cells, polyseteous condition and the lack of strongly sheathing vegetative leaf bases all indicate the genus Dicranoloma. Furthermore, while many species of Dicranoloma lack sheathing perichaetialleaves, some species of the genus in New Zealand have more or less sheathing perichaetial leaves (D. plurisetum, D. robustum, and D. menziesii). Within Dicranoloma, D. rugosum belongs to an atypical element that macroscopi cally is very similar to the Hawaiian Dicranum speirophyllum . This element of Dicranoloma is also present in New Zealand (D. obesifolium), Australia (D. eucamplo dontoides), and New guinea (D . undulatifolium and D. geluense). There is some controversy surrounding the type locality of Dicranoloma rugosum . The species was originally described by Hooker from a "New Holland" (i.e. Australia) collection sent to Turner by Dickson. Mitten (1875), however, questioned the correctness of Dickson's reported localities in general: "Dickson obtained specimens of mosses from the voyages of trading vessels, and localities were then not so precisely mentioned, so that any gathered during the voyage were liable to be reported as if gathered in the country the vessel had returned from; and there are some of the species which Dickson in this manner procured, of which the native country has yet to be discovered." Salmon (1902) noting that this "conspicuous" moss had never been recollected in Australia and citing Mitten's comments regarded Dickson's New Holland locality for this species with suspicion. Finally, on a note accompanying an isotype of Dicranoloma rugosum in BM there is a discussion of Dickson 's localities that ends: "J . D . got the specimen from an East India man, & did not know she (sic) had called at Madeira. Nor did he know that the Leucodon rugosus specimen came from Tahiti or Fiji & not from New Holland." Aside from the type collection, this species is still known only from Tahiti. Despite its restricted distribution, Dicranoloma rugosum is far from a stenotypic species. Collections are extremely variable in plant size, leaf length, the degree in which the leaves are rugose, the strength of the hyaline border and leaf serrations, capsule shape and length, and the number of setae per perichaetium. Plants that are extremely robust, have long narrow rugose leaves that are distinctly denticulate have been called Dicnemon giganteum. M tiller (1858) described Dicnemon banksii for a Tahitian moss that differed from D. rugosum in a number of vegetative characters, most prominent of which were its denticulate leaf and non-rugose leaves. Bescherelle (1895) was thefirst to question the distinctness of these two mosses, noting that in all Tahitian collections he had examined the leaves were more or less rugose (as in D. rugosum) and had denticulate margins (as in D. banksii). Salmon (1902) examined the types of both species, and found them to be identical. More specifically, Salmon noted that the type of Dicnemon banksii was" . . . decidedly rugose (if first moistened and then allowed to dry naturally B. H. ALLEN: Notes on the Dicnemonaceae (Musci): Il 275 without being subjected to pressure) .. . " and that the leaf margin of D. rugosum was, contrary to Hooker and Schwaegrichen's description, not entire but rather, H ••• ir regularly denticulate, in exactly the same manner as in M liller's D. banksii." All au thors since Salmon have placed Dicnemon banksii under the synonymy of Dicnemon rugosum. Unfortunately, the type of Dicnemon banksii, which was deposited at B, appears to have been destroyed.

Taxonomic Treatment Dicranoloma rugosum (Hook.) Alien, comb. novo Leucodon rugosum Hook., Musei Exotici 1, t. 20. 18 18 . (basionym). Dicnemon rugosum (Hook.) Schwaegr., Spec. Muse. Suppl. 2(1): 127. 1824. Eucnemis rugosa(Hook.) Brid., Bryol. Univ. 2: 217. 1827. comb. inval. Type. Australia (sic). In Nova Hollandia. Turn. Herb. a Dicksonia missus (holotype, BM; isotypes, 'BM, G, MANCH, NY). Dicranum densifolium Mohr, Ann. Bot. 2: 246. 1806. nom. nudo (vide e. Muller 1858). Dicnemon banksii e. Mull., Bot. Zeit. 16: 16 1. 1858. Dicnemos banksii e. Mull ex Beseh., Ann. Sci. at. Bot. ser. 7, 20: 18. 1894. or/hogr. var. Eucamptodon banksii (e. Mull.) e. Mull., Gen Muse. Fr.: 248 . 1901. Type. Tahiti. Ex insula Tahiti retulit Banks (type, B; apparently destroyed). Dicnemon giganteum Schimp. in Salm., J. Bot. 40: 7. 1902. nom. inval. in synom . Dicnemon procerrimum Schimp. in Salm., J. Bot. 40: 7. 1902. nom. inval. in synom. Plants medium to large, 4 - 9cm high, more or less shiny, yellow-brown to yellow-green, caespitose. Stems red, densely tomentose; in cross-section 2 - 3 rows of small, thick-walled, red brown epidermal cells, a cortex of larger, thinner-walled, reddish-yellow cells and a central strand of small thin-walled hyaline cells. Branches infrequent, identical to stems. Leaves 4 - 6 mm x 1.5 mm, very dense, rigid, imbricate-appressed to erect-spreading, more or less transversely rugose, ovate-lanceolate to lanceolate, concave or plane; margins entire and plane below, more or less denticulate and incurved above, variably bordered by 2 - 7 rows of long, narrow, hyaline cells; apex acute or shortly acuminate; costa single, E-type (see Kawai 1968), percurrent, strong throughout (80 - 100 J.lm wide at base). Cells narrowly elongate, longer and narrower toward the margins, shorter and wider toward the costa; upper cells long-rhomboidal to rhomic, distinctly porose; alar cells orange-yellow to yellow-brown, conspicuously enlarged. Dioicous. Male plants dwarfed on female plants. Sexually mature males 1.0 - 1.3 mm long; leaves lanceolate, ecostate, 0.4 - 1.0 mm long, cells elongate-rhomboidal, more or less thick-walled, not porose, alar cells weakly differentiated. Perichaetia terminal, becoming laterally displaced; outer leaves 3 - 4 mm long, sheathing, abruptly long setaceous-acuminate, costa present; inner leaves

PLATE I. Distribution of Dicranoloma rugosum in Tahiti. 276 Journ. Hattori Bot. Lab. No. 61 1 9 8 6

8 - 12 mm long, closely sheathing the seta, long setaceous above. Archegonia numerous, 120 mm long, paraphyses absent. Capsules exserted or shortly emergent. Setae 8 - 15 mm long, red or yellow, I - 3 per perichaetium; in cross-section 3 - 4 layers of small, thick-walled epidermal cells, cortex of larger thin-walled, hyaline cells and a central strand of small, thin-walled hyaline cells. Capsules red, up to 3 mm long, smooth, erect to subcylindrical, struma absent; exothecial cells irregularly rectangular, incrassate, walls straight or wavy, irregularly quadrate and thick wall at mouth. Annulus non-revoluble, consisting of several rows of thin-walled quadrate to shortly rectangular cells. Opercula conic-rostrate, 1. 5 - 2.0 mm long. Phaneropore stomata present at base of capsule. Peristome haplolepideous. Teeth 16, 0.3 - 0.5 mm long, red-orange below, hyaline at tips; dorsal trabeculae weakly thickened, dorsal lamellae lightly horizontally striate; ventral trabeculae strongly thickened, ventral lamellae vertically striate below, papillose above; each tooth split 1/2 to 3/4 its length. Spores exceedingly variable, spherical, oblong, 50 - 100 (250) ~m long, single celled, thin-walled, smooth or faintly roughened; usually mixed with numerous, small, more or less collapsed, thicker-walled spores. Calyptra cucullate, 4 mm long, slightly scabrous near the apex. Etymology. The specific epithet, from the Latin noun ruga: wrinkle or fold, refers to rugose leaves of this moss. lIIustrations. Hooker (1818), PI 20, figs. 1 - 6; Whittier (1976), 0 - Q. Ecology. Corticolous (trunks, branches, and twigs), occasionally of humus. Most collections have been made at or above 1000m (range - lOOm to 2045 m). Distribution. Endemic to Tahiti. PI. 1. Specimens examined. TAHITI. Without locality: Tahiti, Wilkes 27 (G, NY). Affahiti: Mt. Cereania, 1000 m, Temarii Nadeaud (CHR , FH); Taravao, Temarii Nadeaud (PH, us). Hitiaa: Plateau region, lOO m, Whit/ier 2172 (NY). Punaauia: Mt. Orohena, south ridge, 1570m, Fosberg & SI. John 17135 (!OH) . Pirae: Mt. Aorai, 1000 - 1960 m, Whitlier 262, 267, 2703, 2710, 2717, 2730, 2742, 2753, 2758, 2779, 2781 , 2785 (B, BM , MO , NICH, NY, us); Mt. Aorai, 1800 m - summit, Decker 1, 7, /4, 27, 46, 51 , 74,80, 114, 115. 124, 125, /33, 144) (B, BM, MO, NICH, NY); Mt. Aorai, Mackee 3064 (MEL); Mt. Aorai, 2050 m, Gagne 1592 (L, us); Mt. Aorai, 1150 - 2050 m, Ba/gooy 1795A , 1841 A, 1847, 1865A, 1920B (L); Mt. Aorai, 1386m, Quay/e 156d (BM).

A Systematic Account of Dicranoloma geluense In 1909, Herzog described the genus Werneriobryum for a distinctive New Guinean moss, W. geluense. In discussing the genus Herzog compared Werneriobryum to the Dicnemonaceae, citing its dicranoid peristome, similar leaf cells, apparently creeping stems, unusually large spores, leaf border of long, hyaline cells, single costa, and long sheathing perichaetial leaves as features common to both taxa. However, Herzog considered the habit, polysetous condition, lack of a stem central strand and single-celled spores of Werneriobryum to negate any close relationship, and that a relationship to the Hedwigiaceae or Grimmiaceae seemed just as likely. On balance, Herzog proposed that the genus be placed in its own family (the Werneriobryaceae). In his closing paragraph Herzog clearly stated his position: in the case of the mosses there are an increasingly large number of smaller families, many subjected to parallel development which in general causes one to find mutual relationships that are seized upon as family relationships. Nevertheless, without discussing the relationships of the genus, Brotherus (1925) placed Werneriobryum in the Dicnemonaceae, a position it has maintained until now (Crosby & Magill 1981; Walther 1983; Vitt 1984). Herzog's evalution of the relationship of Werneriobryum to the Dicnemonaceae is B. H. ALLEN: Notes on the Dicnemonaceae (Musci): 11 277 flawed on several accounts perhaps stemming from his familiarity with the South American Eucamptodon perichaetialis, the most atypical member of the family. Thus, while he considered the lack of a central strand in the stem of Werneriobryum as evidence against a relationship with the Dicnemonaceae, in fact stems without a central strand are the typical condition in the family. On the other hand, he considered the presence of a similar peristome, a leaf border of long narrow hyaline cells, and a single costa as evidence of a relationship to the family, while actually the presence of a highly derived peristome, and the absence of a leaf border and costa are typical features of the Dicnemonaceae. The only characters present in Werneriobryum that support its placement in the Dicnemonaceae are its leaf cells, sheathing perichaetialleaves, lack of a central strand and its creeping stems. The first three characters are general ones, and all three can be used to support a placement in the Dicranaceae as well as in the Dicnemonaceae. The report of creeping stems in this genus was based on the presence of a single lateral perichaetium in the type collection. An examination of the type (which consists of only two stems), however, indicates that this perichaetium may-have originally been terminal and later was laterally displaced by a branch from below. Until more fertile material of this species is examined, the creeping nature of this plant must remain a matter of conjecture. There are a number of features present in Werneriobryurn geluense that make its placement in the Dicnemonaceae unacceptable. Principal among these are its typical dicranaceous peristome (although reduced in size) and the lack of both massive endosporically germinated protonemata ("multicellualar" spores) and leaf nema togens that give rise to leaf rhizoids. As concerns this last feature, Werneriobryum has remarkably dense, tomentose stems , these rhizoids are however associated only with the stem, never the leaves. The relationships of Werneriobryum are clear if one considers the genus Dicranoloma in Australasia. This large genus is greatly in need of revision, but, at present it represents simply the southern hemispheric counterpart of Dicranum, differing chiefly in the presence of a hyaline leaf border. Overall, species of Dicranoloma have an aspect very similar to species of Dicranum. However, the genus harbors an element that appears very different, and it is with this element of Dicranoloma that Werneriobryum belongs. This element of Dicranoloma is present in Tahiti (D. rugosum), New Zealand (D . obesijolium), Australia (D. eucamptodontoides), and New Guinea (D . undulatifolium). A similar habit, sheathing perichaetial leaves, dicranaceous peristome, polysety, lack of a stem central strand, robust size, densely tomentose stems, large spores and undulate leaves are all features of Werneriobryum that can be found within this element of Dicranoloma. If the pleurocarpous nature of W. geluense is considered an open question, there is not a single feature of Werneriobryum that can not be found in Dicranoloma. Although Herzog's Werneriobryum may eventually find application for this sub group of Dicranoloma, until the genus is critically revised, Werneriobryum geluense 278 Journ. Hattori Bot. Lab. No. 61 I 986

134 131

PLATE 2. Distribution of Dicranoloma geluene in New Guinea. must be placed with its closest relations in Dicranoloma. Noteworthy features of Dicranoloma geluense include its squarrose, undulate leaves, large spores, densely tomentose rhizoids, inflated, hyali ne alar cells, and lack of branches. The species appears very close to Dicranoloma rugosum, and both species have long been associated with the Dicnemonacae. Large spores, reduced dicranaceous peristomes, erect capsules, polysety, a robust size, undulate leaves and leaves with a hyaline border are features common to both species. They differ by the absence of a stem central strand and the presence of hyaline rather than red-brown alar cells in Dicranoloma geluense. The generally unbranched habit of Dicranoloma geluenseis apparently due to the suppression of branch primordia rather than a lack of their differentiation. In the small portion of the stem I was able to examine there occurred three branch pr'imordia. A distictive feature of this moss is found in the pinkish color of its rhizoids when moist (when dry the rhizoids are hyaline). If detached from the stem the moist rhizoids are actually a dull gray, but when on the moist stem they appear pinkish due to the dark red color of the stems.

Taxonomic Treatment Dicranoloma geluense (Herz.) Alien, comb. novo Werneriobryum geluense Herz. , Hedwigia 49: 122. 1909. (basionym). Type. New Guinea. Auf dem Gipfel des Gelu (Finisterregebirge), Werner. (holotype, lE). Plants robust, to 14cm long, yellow to golden-yellow. Stems red-brown, creeping(?), infrequently branched; epidermal cells elongate-rhombodial, thick-walled, not storied; in cross section with 2 - 3 rows of small, thick-walled epidermal cells, an inner cortex of larger, thin walled cells, central strand absent. Rhizoids densely matted, of two types: predominantly slender, hyaline, much branched and a few larger, thicker-walled, red-brown; when dry rh izoids white, when moist appearing pinkish. Leaves 6 - 7 x 3 mm, yellow, more or less shiny, squarrose and undulate wet or dry; from a short sheathing base, broadly ovate-acuminate, concave; margins entire, inftexed nearly to the apex; apex acute. Costa single, d-type (see Kawai 1968), faint, percurrent or ending a few cells below the apex. Cell more or less incrassate, smooth and porose throughout; elongate-rhombodial at base, 130 - 200 f1m x 17 - 20 f1m , becoming B. H. ALLEN : Notes on the Dicnemonaceae (Musci): 1I 279 rhombodial above, 75 - 100 {lm x 17 - 25 {lm, then elongate-rhombodial in apical region 100 - 150 {lm x 17 - 20 {lm; 4 - 5 cells at the margins long, narrow, forming a more or less prominent leaf border; alar cells hyaline, enlarged, inflated, thin-walled; cells between the alar cells red-brown across the base. Perichaetial leaves long-convolute sheathing at base, piliform acuminate above, reaching to 1/2 the seta length. Polysetous, I - 4 setae per perichaetium. Seta to 8 mm long, red-brown' to yellow. Capsule (including the operculum) 3.5 mm long; suberect, ellipsoid-cylindrical, smooth; exothecial cells thick-walled, irregularly incrassate, 2 - 3 rows of cells beneath the mouth small more or less thin-walled; phaneropore stomata present at base; annulus none. Opercula conic at base, long and obliquely rostrate. Peristome haplolepideous. Teeth 16,0.3 mm long, red inserted below the mouth, irregularly divided 1/2 their length; dorsal lamellae horizontally striate at apex, striate-punctate below; ventral trabeculae prominently projecting. Spores large 80 - 120 {lm x 50 - 65 {lm, ovoid or irregularly pyramid-oblong, smooth, single celled. Etymology. The name Werneriobryum honors the collector of this moss, Dr. Eugene Werner. Dr. Werner, a German chemist working in German New Guinea and Malacca, achieved some reknown for his observations on the geography and ethnology of the area as well as his extensive entomological and botanical collections. On 16 January 1914, at the age of 34, he met an untimely dea!h at Penang (now George Town, Malaysia), the result of blood poisoning. The specific epithet refers to the mountain (Mt. Gelu) on which the type collection was made. Illustrations. Herzog (1909), Tab. 6, figs. a - h; Herzog (1926), fig. 133. Distribution. Endemic to eastern New Guinea. P!. 2. Specimens examined. NEW GUINEA. Papua. Milne Bay District: 9' 54' S; 149" 20' E, 1940m, Pul/en 8038 (COLO). Morobe District: summit of Mt. Kaindi. 8000 ft. Theirs 3400 (NY); Madang District: summit of Mt. Gelu, Finisterre Range, 1700 m, Werner (lE). Acknowledgements This work was supported in part by the Department of Biological Sciences, University of Cincinnati and in part by a Jesse Smith Noyes post-doctoral Fellowship (Missouri Botanical Garden) to B. Alien. I am grateful to the curators of B, BM, CHR, COLO, FH, G, 1£, L, MANCH, MEL, MO, NICH, NY, us fo r the loan of specimeI)s. I thank M. R. Crosby, R. Magill, H . Robinson, and J. Snider or their comments and suggestions on the manuscript.

LITERATURE CiTED

Allen, B. H. 1985. A revision of the Dicnemonaceae (Musci). Ph. D . dissertation, University of Cincinnati. Bescherelle, E. 1895. Florule bryologique de Tahiti et des lies de Nukahiva et Mangareva. Ann. Sci .. Bot. Nat. ser. 7, 20: 1- 62. Brotherus, V. F. 1901. Dicnemoneae. In A. Engler & K. Prantl, Die natiirlichen Pflanzenfamilien 1(3): 337- 342. Leipzig. __. 1924. Dicnemonaceae. In A. Engler & K. Prantl, Die natiirlichen Pflanzenfamilien ed 2, 10: 214- 219. Leipzig. __. 1925. Nachtrage und Verbesserungen zu Band 10 und 11. In A. Engler & K. Prantl, Die natiirlichen Pflanzenfamilien ed. 2, 11: 524-535. Leipzig. Brown, R. 1819. Characters and description of Lye//ia, a new genus of mosses, with observations on the section of the order to which it belongs; and some remarks on Leptostomum and Buxbaumia. Trans. Linn. Soc. London 12(2): 560-583. Crosby, M. R. & R. E. Magil!. 1981. A dictionary of mosses. Monogr. System. Bot. Missouri Bot. Gard. 3 (3rd ed): 1- 43. 280 Journ. Hattori Bot. Lab. o. 6 1 I 986

Herzog, T. 1909. Laubmoose aus Deutsch-Neu-Guinea und Buru. Hedwigia 49: 119- 127. ---. 1926. Geographie der Moose. Jena. Hooker, W. J. 1818. Musci exotici I: 1- 96. London. Jaeger, A. 1872 . Genera et species Muscorum systematice disposita seu Adumbratio florae Muscorum totius orbis terrarum. Ber. Thatigk. SI. Gallischen Naturwiss. Ges. 1870-71 : 357- 451. Kawai, 1. 1968. Taxonomic studies on the midrib in Musci. (I) Significance of the midrib in systematic botany. Sci. Rep. Kanazawa Univ., BioI. n 127- 157. Miller, H. A., H. O. Whittier, & B. A. Whittier. 1978. Prodromus florae MlIscorum Polynesiae, with a key to genera. Bryophyt. Biblio. 16: 1- 334. Mitten, W. 1875. Muscineae. In J . C. Melliss, St. Helena: 357- 374. London. Muller, C. 1849. Synopsis MlIscorum Frondosorum I: 1- 812. Berlin. - -. 1858 . Additamenta nova ad Synopsin Muscorum. Bot Zeit. 16(23): 161 - 165 . - --. 1901. Genera Muscorum Frondosorum. Leipzig. Paris, E. G . 1896. Index bryologicus sive enumeratio Muscorum: 325- 644. Paris. - - - . 1904. Index bryologicus sive enumeratio Muscorum ed. 2, 2: 1- 375 . Paris. Salmon, E. S. 1902. Bryological notes. J. Bot. 40: 1- 9. Schwaegrichen, F. 1824. Species Muscorum Frondosorum. SlIpplementum 2(91): 87- 179. Paris. Vitt, D. H. 1984. Classification of the Bryopsida. 111 R. Schllster (ed.), New Manual of Bryology 2(13): 696--759. Nichinan. Walther, K. 1983. Syallabus der Pflanzenfamilien. Vol. 2, Bryophytina, Laubmoose: 1- 108. Whittier, H. O. 1976. Mosses of the Society Islands. Gainsville.