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Antheridia and Sporophytes in Takakia Ceratophylla (Mitt.) Grolle: Evidence for Reclassification Among the Mosses

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Antheridia and Sporophytes in Takakia Ceratophylla (Mitt.) Grolle: Evidence for Reclassification Among the Mosses J. Hattori Bot. Lab. No. 73: 263 - 271 (Feb. 1993) ANTHERIDIA AND SPOROPHYTES IN TAKAKIA CERATOPHYLLA (MITT.) GROLLE: EVIDENCE FOR RECLASSIFICATION AMONG THE MOSSES DAVID K. SMITH1 and PAUL G. DAVISON 1 ABSTRACT. Description, illustration, and phenology of antheridia and sporophytes in Takakia ceratop­ hyl/a are presented as evidence for reclassifying Takakia as a moss. Similarities of the schistocarpous capsules shared by Takakia and Andreaeobryum support a revised classification of the Class Andreaeopsida. Subclass Takakiidae is proposed to include the Order Takakiales and Order Andreaeobryales, separate from Subclass Andreaeidae. INTRODUCTION Dr. N. Takaki is credited with the first Japanese discovery of Takakia from near Mt. Goryu (Japanese Alps) in 1951. Nearly eight years elapsed before the formal name Takakia lepidozioides Hattori & Inoue ( 1958) was proposed, after considerable contem­ plation and fermented opinions were expressed by various experts of plant systematics (see Hattori & Mizutani 1958). This early knowledge was necessarily incomplete and its classification somewhat arbitrary because sterile, non-gametangial, non-fertile mate­ rial only was known. Soon after its description, the discovery of archegonia (Hattori & Mizutani 1958) firmly established a connection among the "bryophytes." Tatuno ( 1958) disclosed its chromosome number n = 4, the lowest known for any bryophyte. Further studies of this unusual archegoniate intensified because of ambiguous interpre­ tations of its peculiar form: e.g. undefined phyllotaxy of 2-4-pronged phyllidia; distinc­ tive axillary slime hairs (styli); small and numerous simple 'oil bodies;' non-leafy rhizomatous and stoloniferous subaerial axes bearing patches of branched, beaked mucilage papillae; naked, stalked and sometimes pedestaled archegonia with six rows of neck cells; and low chromosome number. Probably no other bryophyte has attracted as much attention to solve this puzzle of intractably related characteristics. Since Dr. Takaki's discovery and the addition of a second species Takakia ceratophylla (Mitt.) Grolle (1963), the world range of the genus has been demonstrat­ ed to be Northern Hemisphere, confined to the following areas: Himalaya (Nepal, Sikkim, China), Japan, Borneo, Aleutian Islands, southeastern Alaska, and British Columbia. The literature over the past 40 years reflects no consensus of opinion concerning Takakia's placement in the Hepaticae (i.e. Hattori & Inoue 1958, Schuster 1966, Hattori et al. 1968), Musci (Mizutani 1967, 1972, 1974), or even its own division (Crandall-Stotler 1986) ! Attempts to cultivate Takakia and further clarify its system­ atic position have failed to induce archegonia, antheridia, or sporophytes. Thus it has 1 Department of Botany, University of Tennessee, Knoxville, TN 37996-1100, U.S.A. 264 J. Hattori Bot. Lab. No. 73 I 9 9 3 been presumed that Takakia has lost the ability to produce sporophytes. Growth studies of cultured vegetative shoots have produced little new information and mostly have confirmed findings derived from study of freshly collected material. Further review of Takakia literature is not repeated here due to recent treatments by Crandall­ Stotler (1986) and Murray (1988). A passionate essay entitled "Can we find the sporophyte of Takakia" (Hattori 1980) implored botanists to chemically or physically induce antheridia on female plants, and thus coax fertilization and sporophyte production. During the course of recent field studies in the Aleutian Islands both antheridia and sporophytes of Takakia were discovered that answered Hattori's call. The senior author became interested in Takakia in 1975, when sterile specimens of T. ceratophylla were discovered on Adak Island of the Aleutian Islands (Smith 1978). That report represented only the fourth known locality for the species and extended its range east from Amchitka Island where it first had been reported in the Aleutians by Sharp and Hattori (1967). During the summer of 1988 antheridial plants were discovered on Atka Island in the central Aleutian district (Davison et al. 1989). In 1990 the authors of this report again collected antheridial plants on Adak and Atka Islands and also achieved the first discovery of sporophytes on Atka (Smith 1990). ANTHERIDIA (Pl. l & Fig. 1) Antheridia naked, cylindric, elliptic-clavate, (214) x = 226- (316) µm long X (65)- x = 87- ( 112) µm wide, on short centrically or subcentrically attached multi-seriate stalks 2- 3 cells high and ea. 28 µm long X 19 µm wide; jacket unistratose, ( 14 )- x = 19- (23) cells high, cells irregularly polygonal in surface view with thin walls, chlorophyllose in development aging to a bright yellow-orange and after-ripening to a burnt red-brown, chromoplasts 1- 4, evident; cap cells differentiated as an apical, opercular dome of enlarged jacket cells, dissociating and becoming rounded-inflated during spermatocyte release. Takakia occurs within a wide elevational band (75 - 700 + m). Plants of lowland habitats are invariably sterile. Antheridal plants appear confined to exposed, wind­ swept, fog-enshrouded upland tundra of interior-island montane sites. Male popula­ tions are often locally abundant and occur more frequently and throughout a wider range than do sporophytic plants. Antheridial shoots are produced sparingly to abundantly within patches of densely packed, caespitose aerial shoots. Each shoot may produce few to many (1- 3)- 12- 15- (20 + ) antheridia at the apex. Their development follows a centrifugal pattern whereby antheridia partially or fully replace phyllidia. The apical cell is not consumed and vegetative growth may resume apically following the cycle of antheridial production. Some shoots bear several discrete series of aged antheridia separated by phyllidia; evidence that production is seasonal. Antheridia begin maturing in mid-July while those initiated later continue to develop sequentially through the growing season. Previous to this report of antheridial plants, archegonia have been known for T. lepidozioides (Hattori & Mizutani 1958) and T. ceratophylla (Hattori et al. 1968) and it has been assumed that Takakia is dioecious. It may be stated, at least for T. D. K. SMITH & P. G. DAVISON: Antheridia and sporophytes in Takakia ceratophyl/a 265 Fig. I. Habit photograph of Takakia ceratophyl/a sporophytes and antheridial shoots, X 18 (photograph courtesy of Alan S. Heilman). ceratophylla, that the dioecious condition is confirmed. In appearance, there are no differences among sterile, male, or female plants indicated by vegetative morphology and size. SPOROPHYTES (Pl. 1, Fig. l & 2) Sporophytes terminal, solitary (rarely 2), without accessory protective perichaetial struc­ tures; erect 1.5- 2.Smm tall (including vaginula), seta 0.5- l.25mm long, capsule 0.6- 1.0mm long, vaginula to 0.2 mm long, calyptra 0.2--0.3 mm long; development as a moss from a cylindric, beaked epigonium, rupturing as seta elongates with apical calyptra, sporogonium expanding apically, chestnut brown at maturity. Seta erect, straight and stout, becoming slightly twisted with age. Capsule erect, elliptic, green in development, symmetrically tapered at base and apex, dextrorsely spiralled at maturity, nearly 360°, columella present, stomata and operculum absent; schizocarpous, dehiscence along a single linear slit following the spiral of exothecial cells, beginning near the middle of the capsule and extending to the base and apex, suture cells absent. Spores slightly roughened, with a triradiate ridge, 29- 32 µm diameter. Calyptra mitriform, erose 266 J. Hattori Bot. Lab. No. 73 1 9 9 3 Fig. 2. Habit photograph of Takakia ceratophylla sporophyte, dehiscent capsule, X 85 (photograph courtesy of Alan S. Heilman). and effaced at base covering the upper 1/4 or Jess of the capsule. Sporphyte-bearing plants of Takakia ceratophylla appear to be more narrowly confined (above 300m elevation) within upland tundra sites than antheridial plants. Sporophyte production is dramatically low compared to the abundance of antheridia produced; an estimated ratio (sporophyte: antheridial shoots) of l: IOO's in many occurrences and rarely 3- 12: lOO's in particularly bountiful expressions. Sporophytes occur only within crowded patches ( 1-5 cm diameter) exhibiting abundant antheridial production. A majority of patches in proximity to sporophytic clumps produce copious antheridia yet fail to show any production of sporophytes. Emergent sporophytes become evident by mid-July. They may occur singly and scattered or as several and closely nested. A sub-synchronous pattern of development is indicated by differences in the extent of seta elongation and degree of capsule swelling that varies among developing sporophytes. During development both setae and capsules are well-invested with chlorophyll. A few sporophytes of the previous year's production often persist, being a seasoned chestnut brown in color with fully dehisced capsules containing few or no spores. D . K. SMITH & P . G . DAVISON: Antheridia and sporophytes in Takakia ceratophyl/a 267 Spore liberation is accomplished passively through repeated cycles of drying that cause the capsule to gape open. The mechanics of dehiscence involve a reverse torsion as if to restore a vertical realignment of the capsule wall cells. Shrinking of the exothecial cells in response to dessication pressure spreads the dehiscence slit. The fixed position of the capsule at the seta juncture provides a fulcrum against which the forces of shrinkage widen the gap laterally. PHENOLOGICAL DISCUSSION
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