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J. Hattori Bot. Lab. No. 73: 263 - 271 (Feb. 1993)

ANTHERIDIA AND IN CERATOPHYLLA (MITT.) GROLLE: EVIDENCE FOR RECLASSIFICATION AMONG THE

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 . Similarities of the schistocarpous capsules shared by Takakia and support a revised classification of the Andreaeopsida. Subclass Takakiidae is proposed to include the 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 Hattori & Inoue ( 1958) was proposed, after considerable contem­ plation and fermented opinions were expressed by various experts of 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 "." Tatuno ( 1958) disclosed its chromosome number n = 4, the lowest known for any . 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 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 , 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 of Takakia" (Hattori 1980) implored botanists to chemically or physically induce antheridia on female , 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. 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 Many mosses abundantly produce ranks of even-aged sporophytes. Takakia sporophytes exhibit a Jess synchronous developmental pattern and are far fewer in number. Fertilization would appear to be effected beginning in the mid-summer, coinciding with the first-ripening of antheridia and archegonia, and continuing through the growing season. It is uncertain if early embryogenesis proceeds immediately through the remainder of the growing season, or if young embryos forestall develop­ ment until the following spring. Specimens transplanted from the field to growth chambers completed sporophyte development to ripening for those sporophytes present at the time of field collection. Such development was marked by full enlargement of the capsule, dextrorse rotation of seta and capsule, formation of a single rift line of dehiscence, meiosporic (tetrad) development, and coloration changing from green to brown. Other younger sporo­ phytes appeared in the transplanted specimens during maintenance in the growth chambers, and followed the same sequence of development to maturity over a 60-90 day period. Conditions in the growth chamber were set to simulate field conditions of the growing season- day/night period set to a 18- 6 hour diurnal cycle of 10-l5°C and 0-50C. Periodic harvest of antheridial, archegoniate, and sporophytic shoot tips was conducted to monitor the production cycle of each. Clearly, the antheridia were least resilient to the transplant conditions. Antheridia appeared to arrest in further develop­ ment and a rapid degeneration of the spermatogenous mass followed. Chromoplast­ enriched, undehisced antheridia, centripetal to spent antheridia were squashed to release their spermatocyte contents, but sperm failed to escape from the vascicular membrane. Young green antheridia, most internal of the series, ceased further development. Two considerations from these observations may be invoked that bear on the few and serial development of sporophytes. Production of functional sperm may be exceedingly low despite the apparent over abundance of antheridial production, and/or sporophytes that emerged in the transplanted specimens may have developed from embryos already established in situ prior to field gathering. Archegoniate shoots that were dissected showed no evidence of fertilization but appeared as though limited serial development of archegonia continued to occur in the growth chambers. No embryos or early epigonial stages were detected suggesting that no fertilizations were achieved after the specimens were moved from the field to the growth chambers. Attempts to induce new gametangia and thus repeat sporophyte production have been unsuccessful. The original, fertile transplants maintained under simulated field climatic conditions 268 J. Hattori Bot. Lab. No. 73 9 9 3 over the past two years have responded only with continued vegetative growth. Archegonia are produced from merophytes displaced several cell generations lateral to the apical cell. Each female shoot apex is capable of producing several archegonia comingled with complete and incomplete phyllidia. Fertilization may occur in more than one , but subsequent development of sporophytes is generally one per shoot. Evidence for serial development of archegonia is provided by the persistence of arrested archegonia preserved at the base of the vaginula and rarely perched on the elevated calyptra of the sporophyte. Sporophyte development effects determinate conditioning of the shoot apex by disrupting and replacing the apical cell as the foot penetrates into elaborated shoot apical tissue (Renzaglia et al. 1991). In the event that fertilization of archegonia fails, the apical cell resumes propagating vegeta­ tive growth (the apical cell "not consumed," Hattori & Mizutani 1958) and barren archegonia become displaced outward and downward along the shoot axis. Fated archegonia become stranded laterally along the shoot among phyllid derivatives and may exhibit further elongation below the stalk in forming pedestals (Mizutani 1967). The ability to develop pedestals (noted previously by Mizutani 1967 and Hattori et al. 1968) appears to reflect an ontogeny directly linked to early merophyte potentialities. Merophytes of female shoots produce both archegonia and phyllidia. A similar ontogeny in male shoots results in antheridia and phyllidia. Sporeling development was not observed in populations either in situ or among transplants. germinations were attempted in several trials by surface sterilization of ripened capsules and sowing of spores into solidified and liquid agar-based, mineral­ nutrient media (Knop's and Parker-Thompson's). Trial germination cultures were subjected to treatments of light and dark exposures at ambient laboratory room temperatures (20-25°C) and light-dark exposure ( 16- 8 hrs.) at 0-5°C. No germina­ tion occurred after 120 days.

CLASSIFICATION A relationship between Takakia and was initially inferred by Mizutani ( 1972) who established the class Takakiopsida and aligned it next to the Andreaeop­ sida. In a later refinement of his thoughts (Mizutani 1974) included subclasses Takakiidae and Andreaeidae within the . Steere and Murray ( 1976) ex­ panded the Andreaeidae (within Andreaeopsida) with their description of Andreaeob­ ryum macrosporum. Murray (1988) redefined the connection between the andreaeop­ sid mosses and Takakia. Murray's elegant paper expressed somewhat daringly, a novel comparison between Andreaeobryum and Takakia, drawing attention to shared struc­ tural homologies: ( l) secondary protonema (protonemal appendages) and the leaves on Takakia shoots, (2) beaked mucilage papillae, (3) and such papillae " .. . often massed and [ ] often seen at the bases of enations," ( 4) pedestaled archegonia, and others (see Murray 1988). The discovery and report of mosslike antheridia in Takakia ceratophylla (Davison et al. 1989) and a tetrahedral apical cell producing spiral ranks of leaves (McFarland et al. 1989), previously observed and convincingly figured by Inoue (1961) for T. D . K. SMITH & P. G. DAVISON : Antheridia and sporophytes in Takakia ceratophylla 269

/epidozioides, is compelling evidence that Takakia is a moss. In this regard we (Davison et al. 1989 and McFarland et al. 1989) proposed the realignment of Takakiopsida next to Andreaeopsida as originally suggested by Mizutani (1972). Our original presentation on sporophytes of Takakia (Smith et al. 1990) and the details presented here are final convincing evidence that Takakia is a moss. The pattern of sporophyte development, vis a vis, is consistent with other mosses; yet results in a structural design unique to Takakia. The capsule is simple, erect, and schistocarpous dehiscing along a single, spiral-vertical fissure without suture cells. All of these capsule characteristics occur also only in Andreaeobryum except its dehiscence involves multi­ ple vertical slits (2- 4- 8). The characteristics we have discussed of the sporophyte and antheridia seem sufficiently sound to consider Takakia an expression and member of the andreaeopsid­ line, both historically and even as most currently defined (Murray 1988). Our evidence, thus presented, is reflected in the following revised classification of Takakia as a moss: Class: Andreaeopsida Subclass: Andreaeidae Order: Andreaeales Genus: Andreaea Subclass: Takakiidae (Posito Novum) Order: Takakiales Family: Takakiaceae Genus: Takakia Order: Andreaeobryales Family: Andreaeobryaceae Genus: Andreaeobryum

ACKNOWLEDGEMENTS The authors wish to thank the following people and organizational units for support and advice in aid to this research: The U.S. Fish & Wildlife Service, Anchorage Office of Endangered Species (Michael Amaral and Brian Anderson) and Adak Office of The Aleutian Islands Wildlife Refuge (Michael Boylan, E. Van Klett, Vern Bird); The Department of the Navy, Adak; The Atxam Corporation; City of Atka (Ms. Julie Dirks, Lawrence Prokopeuff, Larry Dirks, Jr., Dennis Golodoff); The University of Tennessee, Hesler Faculty Awards Fund, Sharp Fund; Alan Heilman, Leslie G. Hickok, Kenneth D. McFarland; East Tennessee State University, Karen Renzaglia; University of Alaska, Barbara Murray. To the late Dr. Sinske Hattori we are grateful and offer this paper as a tribute to acknowledge his devotion to and seminal works on Takakia and who encouraged the publication of this manuscript.

LITERATURE CITED Crandall-Stotler, B. 1986. Morphogenesis, developmental anatomy and bryophyte phylogenetics: contra­ indications of monophyly. J. Bryol. 14: 1- 23 . Davison, P. G ., D. K . Smith, & K . D . McFarland. 1989. The discovery of antheridia in Takakia. ASB 270 J. Hattori Bot. Lab. No. 73 I 9 9 3

Bulletin 36(2): 65. Grolle, R. 1963. Takakia im Himalaya. Osterr. Bot. Z. 110(4): 444- 447. Hattori, S. 1980. Can we find the sporophyte of Takakia? Bryol. Times 6: 2. Hattori, S. & H. Inoue. 1958. Preliminary report on Takakia lepidozioides. J. Hattori Bot. Lab. 19: 133- 137. Hattori, S. & M. Mizutani. 1958. What is Takakia lepidozioides? J. Hattori Bot. Lab. 20: 295- 303. Hattori, S., A. J. Sharp, M. Mizutani & Z. Iwatsuki. 1968. Takakia ceratophylla and T. /epidozioides of Pacific North America and a short history of the genus. Misc. Bryol. Lichen. 4(9): 137- 149. Inoue, H. 1961. Supplements to the knowledge on Takakia /epidozioides Hatt. & Inoue. Bot. Mag. (Tokyo) 74: 509--513 [in Japanese with English summary]. McFarland, K. D., D. K. Smith, & P. G. Davison. 1989. Observations on antheridial and apical organization in Takakia ceratophylla. Amer. J. Bot. 76(6): 11. Mizutani, M. 1967. A new knowledge of archegonia of Takakia /epidozioides. J. Jap. Bot. 42(12): 379- 381 [in Japanese with English summary] . Mizutani, M. 1972. Koke no Soseiki (Genesis of Mosses) . Shida to Koke ( and Mosses) 7(1 /2): 1- 9 [in Japanese] . Mizutani, M. 1974. Relationships with ferns and mosses. Shida to Koke (Ferns and Mosses) 8(1): 4- 6 [in Japanese]. Murray, B. M. 1988. Systematics of the Andreaeopsida (Bryophyta): Two orders with links to Takakia. Beih. Nova Hedwigia 90: 289--336. Renzaglia, K. S., D. K. Smith, K. D. McFarland & P. G. Davison. 1991. Ultrastructure of the /sporophyte junction in Takokia ceratophylla. Amer. J. Bot. Suppl. 78(6): 8- 9. Schuster, R. M. 1966. Studies on Hepaticae XV. Calobryales. Nova Hedwigia 13: 1- 63. Sharp, A. J. & S. Hattori. 1967. Takakia ceratophylla found in the Aleutians. Misc. Bryol. et Lichen. 4: 120. Smith, D. K. 1978. Takakia ceratophy/la (Mitt.) Grolle from Adak Island, Aleutian Islands, Alaska. J. Hattori Bot. Lab. 44: 17- 23. Smith, D. K. 1990. Sporophyte of Takakia discovered. Bryol. Times 57/58 : I, 4. Smith, D. K., K. D. McFarland & P. G. Davison. 1990. The sporophyte of Takakia. ABLS Meeting, Wakulla Springs, Florida. [Abstract published in Meeting Proceedings] . Steere, W. C. & B. M. Murray. 1976. Andreaeobryum macrosporum , a new genus and species of musci from northern Alaska and Canada. Phytologia 33(6): 407- 410. Tatuno, S. 1958. Chromosomen bei Takakia lepidozioides Hattori et Inoue. J. Hattori Bot. Lab. 20: 119- 123.

EXPLANATION OF PLATES

Pl. I: Habit photograph of Takakia ceratophylla antheridial and sporophyte shoot, X 25 (photograph courtesy of Alan S. Heilman). D. K. SMITH & P. G. DAVISON: Antheridia and sporophytes in Takakia ceratophylla 271

Pl. I