Characterization of Myhogramme Lnida, Myriogrammeae Trib

J. I’hyrol. 33, 106-121 (1997)

CHARACTERIZATION OF MYHOGRAMME LNIDA, MYRIOGRAMMEAE TRIB. NOV (DELESSEIUACEAE, FWODOPHYTA)

Max H. Hommersand‘ and Suzanne Fredericf Department of Biology, University of North Carolina, Chapel Hill, North Carolina 27599-3280

ABSTRACT ideae, and 40 genera, many of them new. Most ge- The Myriogramme group of Kylin was found to contain neric names proposed by Kylin had been used pre- two distinct clusters of genera that m’trecognition at the viously by J. Agardh (1876, 1898) for subgenera or tribal level. In this paper, we establish the tribe Myriogram- “tribes” (sections) in Nitophyllum or Delesseria. My- meae based on a study of the type species of Myriogram- riogramme Kylin (1924:55),type of the Myriogramme me, M. livida, from the Southern Hemisphere. The My- group Kylin (1924:53), for example, was based on riogrammae is charact~zedby 1) marginal and dijfuse Tribus 111 Myriogramma of subgenus I1 Aglaophyllum intercalaly meristems; 2) nuclei arranged in a ring bor- in Nitophyllum u. Agardh 1898:42). Kylin designated dm‘ng the side walls of vegetative cells; 3) microscopic veins Nitophyllum lividumJ. D. Hooker et Harvey 1845 as absent; 4) procarps scattered, fmed opposite one another the type species of Myriogramme because, in his opin- on both sides of the blade postm.or to one or more vegetative ion, it included Nit~hyll~mgrayanum J. Agardh pm’central cells {covcr cells) and consisting of a carpogo- (1876:449), the first species listed by J. Agardh nial branch, a one-/to two-celled lateral stmde group and (1898) under Mynogramma. An element of confu- a one-celled basal sterile group; 5) auxiliav cell diploidized sion was introduced from the beginning in that, al- by a connecting cell cut o~postm.olaterallyfrom the fiil- though Kylin selected M. livida as the type species, ized caqogonium; 6) gonimoblast initial cut off distally he based his concept of Myriogramme primarily on a from the auxilialy cell, generating one distal and one to study of M. minuta Kylin (1924:56), a new species two lateral gonimoblast $laments that branch in the plane from Naples, Italy. Subsequent investigations of re- of the expanding qstocarp cavity and later fuse to fm lated taxa placed in Nitophjllum Greville 1830 (nom an extensive, branched fusion cell; 7) spermatanpal and cons.), Myriogramme Kylin 1924, Haraldiophyllum Zi- tatrasporanpal sm’fmed inside the margzn on both sides nova 1981, or Hideophyllum Zinova 1981 have not of the blade by re.sumption of meristematic activity; and 8) resolved the many ambiguities arising from Kylin’s tetrasporangza produced primarily from the central cells. original characterization of Myriogramme based on The Myriogrammae currently includes Myriogramme nontype material (Kylin 1925, 1929, 1934, 1956, Kylin, Gonimocolax Kylin, Haraldiophyllum A. Zi- Hollenberg and Abbott 1965, Abbott 1969, Norris nova, Hideophyllum A. Zinova, and a possible unde- and Wynne 1969, Mikami 19’72, Zinova 1981, Wynne scribed genus from Pacajic North and South Amka. Gen- 1983, 1986, 1996, Millar 1990, 1994, Millar and era are separated based primarily on features of gonimo- Huisman 1996). blast and caqosporangial development. We began our study of Myriogramme by surveying procarp and cystocarp development in type and Kty index words: Ceramiales;Delesseriaceae; morphology; field-collected material of potentially interesting spe- Myriogramme; Myriogrammeae tib. now.; Rhodophy- cies placed in the Nitophyllum group, the Crypto- ta; subantarctic; systematics; taxonomy pleura group, and the Myriogramme group in the North Atlantic Ocean, Pacific North and South In 1923, Kylin investigated the vegetative and re- America, Australia, and New Zealand. Our prelimi- productive development of the type species of each nary observations indicated that the Myriogramme of five prominent European genera of Delesseri- group requires systematic revision. In this paper, we aceae using material stained with hematoxylin. He describe the developmental morphology of type and divided the Delesseriaceae into two subfamilies field-collected material of M. livida, the type species based on the position of procarps and cystocarps of ~yriogramm~,and propose a new tribe Myriogram- (pre-/and postfertilization stages of the female re- meae trib. nov., to contain Myriogramme, Gonimoce productive apparatus): along the midrib of a fertile lax, Haraldiophyllum, Hideophyllum, and a few species blade in Delesserioideae versus scattered randomly currently placed in Nitophyllum. over the blade surface in Nitophylloideae. The fol- lowing year, Kylin (1924) published a comprehen- MATERIALS AND METHODS sive taxonomic revision of the Delesseriaceae in Type collections of Myriagrainme lavida and M. crozicri used in which he divided the family into 11 “Gruppen” this study were kindly loaned by The Natural History Museum (groups), 5 in Delesserioideae and 6 in Nitophyllo- (Loridoil). Morphological observations were largcly niade on material fixed in 8-10% fornialiti-s~awater and preserved in 5% for- malin-seawater. Whole-mount and sectioned rnatcrial either was Received 25 June 1996. Accepted 16 October 1996. stained with aniline blue and mounted in browsyrup or glycer- Authot- for reprint requests. ine or was treated with Wittmann’s aceto-iron-hcniatoxylin-chlo- ’< Present address: Department of Biology, P.O. Box 42451, Uni- ral hydrate (Wittmann 1965) and mounted in 50% Hoyer’s versity of Southwestern I.ouisiana, Lafayette, Lousiaria 70504. mounting medium, as described in Hommersand et al. (1992). 106 MYRIOGRAMMEAE TRIB. NOV. 107

Whole-mount preparations were sometimes cleared for critical cell, afterward radiating upwardly and bearing pri- observations. Slides were placed in an alcohol chamber for 12- mary carposporangia either terminally or in chains; 24 h after destaining in 45% glacial acetic acid, transferred by stages (% absolute ethanol, 34 xylerie; y3 absolute ethanol, *h xy- secondary carposporangia, where present, develop- lene) into xylene, and mounted in Piccolytem (Ward’s Natural ing sympodially from inner gonimoblast cells and Science Establishment, Inc., Rochester, New York). Drawings were either terminal and solitary, or forming clusters or made with a camera lucida, and photographs were taken with a branched chains. Fusion cell formed progressively, Zeiss Photomicroscope 111. Herbarium abbreviations follow Holm- gren et al. (1990). incorporating the supporting cell, central cell, residual auxiliary cell, and primary gonimoblast cell and OBSERVATIONS extending to include inner gonimoblast cells and cells in floor of cystocarp. Sterile groups either ex- Mynogramme Kylin (1924:55) cluded from, or included within, fusion cell. Cysto- Description: Plant body foliose, erect and basally carp cavity formed schizogenously, covered by a attached, or repent and attached secondarily by rhi- multilayered pericarp with a single ostiole overlying zoids; entire, sinuous, lobed, lacerate, or deeply di- sterile group 1. Tetrasporangia bome in small cir- vided; membranous above, thickening toward the cular, elliptical, or rectangular sori scattered ran- base, sometimes with a basal nerve, or the nerves domly bordered by a sterile margin in upper parts subdichotomously branched in lower parts; estipi- of blade. Sori formed by renewal of meristematic tate or with a compressed to cylindrical stipe. Blade activity, mostly five cell layers thick at maturity. Pri- monostromatic or tristromatic at margin, polystro- mary tetrasporangia arising two (to four) per cell matic toward base and in basal thickenings, nerves from central cells. Secondary tetrasporangia also cut and stipes. Microscopic veins absent. Cells polygonal off from central cells and possibly from inner cor- in surface view and rectangular in sectional view, ar- tical cells. Division of tetrasporangia tetrahedral. ranged in horizontal tiers and vertical rows in polystromatic parts. Growth diffuse, by marginal and Mynogramme Ziuida u. D. Hooker et Harvey) intercalary meristems, the divisions often perpendic- Kylin (1924:58) ular to one another, producing clusters of rectan- (Figs. 1-55) gular cells that later become polygonal in shape. Description: Thalli erect from a compact basal Chloroplasts parietal, simple or dissected in margin- rhizoidal system to 40 cm high, bluish red to rose al cells, later breaking into small units of defined red or reddish brown, foliose with acute to rounded size and shape linked initially by fine strands. Nuclei tips and smooth or ruffled margins, undivided, la- one to many in meristematic cells, at first arranged ciniate, lobed or deeply dissected; blade mostly in a median plate or ring alongside lateral walls, lat- monostromatic, polystromatic toward base, estipitate er forming two rings bordering side walls on either or with a compressed to cylindrical stipe and basal side of plane passing through middle of blade, ul- nerve, or the nerves subdichotomously branched be- timately lying in a broad band bordering side walls low. Central cell layer of stipes and polystromatic between chloroplasts. Primary and secondary pit parts typically broader than the cells on either side, connections initially median, usually one between or with several cell layers in the center distended each adjoining cell, sometimes with finer secondary forming a central core of larger diameter cells. Sper- pit connections formed later near cell surfaces. matangia borne in elliptical to irregularly shaped, Spermatangia produced in small circular to elliptical separate or confluent sori on both sides of blade. sori formed at random in upper parts of blade by Procarps initiated inside margins. Cystocarps low, renewed meristematic activity within thallus margin. circular with a central ostiole, scattered on both Sori initially solitary, sometimes becoming partly sides in monostromatic portions of blade. Gonimob- confluent. Procarps scattered, formed simultaneous- lasts initially bearing carposporangia in open, mon- ly on both sides of thallus from meristematic tissues opodially branched chains, subsequently producing near margin, the fertile central cell first cutting off secondary carposporangia sympodially in small clus- a vegetative pericentral cell (cover cell) on each side ters of tightly branched chains. Fusion cell initially from the anterior end, followed by a posterior fertile small, basal, later candelabra-like through progres- pericentral cell (= supporting cell). Functional pro- sive fusions of inner gonimoblast cells concomitant carps consisting of a one-/to two-celled lateral sterile with the formation of secondary carposporangia. Te- group, a four-celled carpogonial branch, and a one- trasporangia in small circular, elliptical or oblong celled basal sterile group. Carpogonium cutting off sori distributed uniformly over monostromatic por- two connecting cells after fertilization, the auxiliary tions of blade. cell diploidized by the second, posteriolateral con- Lectotype: BM; cystocarpic specimen correspond- necting cell. After diploidization, the auxiliary cell ing to the reverse image of a habit drawing in J. D. dividing into an anterior gonimoblast initial con- Hooker 1847:plate CLXXIX, upper right-hand fig- taining a diploid nucleus, and a posterior residual ure; Port William, East Falkland I., July 1842, Capt auxiliary cell containing a diploid and one or two Cr[ozier] (Fig. 1). (Selected from among the syn- haploid nuclei. Gonimoblast filaments developing types in BM by J. Price; see Kcker 1987.) monopodially in an arc encircling the supporting Nomenclatural synonyms: NitophyZZum ZividumJ. D. 108 MAX H. HOMMERSAND AND SUZANNE FREDERICQ

FIGS. 1-7. ~Vfjrk~prr~~elivida. FK:. 1. Habit of Iectotype (Port William, Falkland Islands). FIG. 2. Habit of specimen collected by,]. D. Hooker (Falkland Islands). FK;. 1. Meristeniatic margin. Specimen from type sheet of M. crozipr' (Hermite Island, Cape Horn). FIG.4. Meristematic margin of rapidly growing blade. FIG.5. Meristeniatic mai-gin showing patiems of intercalary cell divisions. FIG. 6. Mei-isle- trratic rriargiii sliowiiig enlarged marginal cells and dividing intercalary cells linked by primary pit connections. FIG. 7. Margin in slowly growing region of thallus. Figures 4, 5, 7, hcmatoxylin; Figures 3, 6, aniline blue.

Hooker et Harvey 184.5253. CTptqt&?zm lzvida u. D. u. D. Hooker et Harvey) Kylin 1924359. N~~@~~~~um Hooker et Harvey) Kutzing 1866:12, plate 31. grayanum J. Agardh 1876:449, 1898:42. Taxonomic synonyms: Nitophyllum crozim' J. D. Ricker (1987) questioned whether or not Myrio- Hooker et Harvey 1845:254, 1847:472, plate gramm crozieri is distinct from M. livida. Here we CLXXVII. C:ryibt@Zmra crozim' u.D. Hooker et Har- place it in synonymy under M. Zivida for the first vey) Kutzing 1866:11, plate 27. Myriogramm crozim. time. Another species, Myriogrammc smithii u. D. MYRIOGRAMMEAE TRIB. NOV. 109

Hooker et Harvey) Kylin 1924, with strongly devel- Santa Barbara Co., California, male, female, and tet- oped macroscopic nerves that extend almost to the rasporic, coll. M. H. Hommersand, 21:vii:1966, margins u. D. Hooker 1847:plate CLXXVIII, central NCU. Nitophyllum nmthii Hollenberg et Abbott 1965: figure; see Cotton 1915), has sometimes been re- holotype, on Prionitis at 100 ft, Carmel Submarine garded as being closely related to M. livida (Kylin Canyon, Monterey Co., California, male and female, 1924). Pending further studies, we concur with the coll. Wheeler J. North, 1962, US 077797. Nitophyllum opinion of Mendoza (1969) that M. smithii repre- hollenbngiii (Kylin) Abbott 1969: syntypes, on piling, sents a separate species. municipal wharf, Monterey, Monterey Co., Califor- Distribution: Southern South America, Antarctic nia, female and tetrasporic, coll. G. J. Hollenberg, Penninsula and Scotia Sea, Falkland Island, South 20:vii: 1939, US 077788. Myriogramm sp.: Dichato, Georgia, Isles Kerguelen, Macquarie Island. (For Bahia de Coliumo, 40 km north of Concepcibn, more complete distribution records and synonymy, Chile, female and tetrasporic, coll. M. H. Hommer- see Papenfuss [ 19641, Mendoza [ 19691, and Ricker sand, 31:xii:1978, NCU. [ 198'71.) Vegetative mor;bhology.Juvenile thalli were not seen Specimens examined: Myriogramm livida (J. D. in this study. Growth of the adult thallus involved Hooker et Harvey) Kylin: lectotype of Nitophyllum liv- the activity of both marginal and intercalary meri- idum Port William, East Falkland, female, coll. Capt. stems. Meristematic cells may be uninucleate, binu- Crozier, vii:1842, BM (Fig. 1); Falkland Island, fe- cleate, or multinucleate, with few to many nuclei. male, coll. J. D. Hooker, BM (Fig. 2); on the beach, Marginal meristematic cells were mostly rectangular Berkeley Sound, Falkland Island, tetrasporic, vi: in shape, with cell divisions taking place either at 1842, BM; additional tetrasporic or sterile speci- right angles or parallel to the thallus margin. Oc- mens, Berkeley Sound or undesignated localities, casionally, marginal growth was initiated by trian- BM; (no specimen was found that corresponded to gular cells that divided obliquely, forming files of the habit of the tetrasporic plant on the left in J. D. cells oriented parallel to the thallus margin. Inter- Hooker 1847: plate CLXXIX); lectotype of Nitophyl- calary cell divisions often occurred successively at lum crozieri in deep water, St. Martin's Cove, Hermite right angles, forming patches in which the cells were Island, Cape Horn, tetrasporic, BM, J. D. Hooker grouped in twos, fours, or eights, similar to patterns 1847:472-3, plate CLXVII (right-hand side of com- seen in Porphyra. posite figure), Levring 1960:68-9, figure 18; other Rapid marginal growth is particularly well illus- tetrasporic and sterile specimens from the same lo- trated in type material of Myriogramme crozieri; in cality, BM; 8 km northeast of Punta Arenas, Strait of which the pattern of periclinal and anticlinal divi- Magellan, Chile, male, female, and tetrasporic, coll. sions near the margin gives the appearance of di- M. H. Hommersand, 9:i:1979, NCU. chotomously branched cell rows emanating from Specimens of other taxa examined: Myn~gramme clusters of cells in the interior (Fig. 3). This feature denticulata (Harvey) Kylin 1924: 1 km south of The had already been noted by J. Agardh (1898) and Kaik, Akaroa Harbor, South Island, New Zealand, Cotton (1915) in the type of M. crozieri (as Platyclinia male, female, and tetrasporic; coll. M. H. 8c F. C. crozieri) and is seen in rapidly growing margins in Hommersand, 13:x:1974, NCU. Mynogramme crispata our material of M. livida (Fig. 4). Often, cells in the u. D. Hooker et Harvey) Kylin 1929: drift, Ringa outermost one to three layers at the margin appear Ringa, Stewart Island, New Zealand, female and tet- to be growing slowly, while those in the interior di- rasporic, coll. M. H. Hommersand, 3:xii:1974, NCU. vide more rapidly, forming distinct meristematic Haraldiophyllum bonnemaisonii (Kylin) A. Zinova patches (Figs. 5, 6). Occasionally, marginal files 1981: on kelp stipe, Skomer, North Wales, female, overgrow one another to the left and right, forming coll. S. Hiscock, 5:xi:1984, NCU; Carrickadda spit, distinct marginal layers (Fig. 6). In slower growing Finavarra, Co. Clare, Ireland, male, female, and tet- tissues, cell enlargement keeps pace with cell divi- rasporic; coll. M. H. Hommersand, l:vii:1985, NCU. sions, both along the margin and in the thallus in- Hideophyllum yaoensis (Yamada et Tokida) Zinova terior, and cell shapes and sizes grade more or less 1981: Urakawa, Hidaka Province, Hokkaido, Japan, uniformly from inside to outside (Fig. 7). The range female and tetrasporic, coll. Mikami, 23:xii:1971, US of growth patterns described here were seen in dif- 070559. Haraldiophyllum mirabile (Kylin) A. Zinova ferent parts of the same thallus and in different thal- 1981: isosyntypes, Canoe Island, near Friday Harbor, li. Washington, female and tetrasporic, coll. H. Kylin, Cytokinesis takes place perpendicular to the plane 24:vi:1924, UC 279580. Haraldiophyllum nottii (R. E. of the blade. Primary pit connections are median Norris et Wynne) Wynne 1983: holotype, Hood Ca- when viewed optically in periclinal section (Figs. 5, nal, 10-m depth, 1 mi south of Eldon, Mason Co., 6). Rapidly dividing cells tend to be small and con- Washington, female and tetrsporic, coll. D. Russell, tain few (one to six) nuclei (Figs. 4, 5, 9). The num- 18:xi:1967,WTU 238051. Myriogramme spectabilis (Ea- ber of nuclei is closely correlated with cell volume: ton) Kylin 1924: syntypes, Santa Cruz, California, fe- the larger the cell the more nuclei, with up to 40- male and tetrsporic, coll. C. L. Anderson, 1874, FH; 60 nuclei in the largest cells. Nuclei aggregate in a reef, 1 km south of Jalama Beach State Beach Park, ring of cytoplasm along the side walls, such that mer- 110 MAX H. HOMMERSAND AND SUZANNE FREDEIUCQ

Rc;s. 8-1 X. M~n'oi~~~mtlividn. FIGS. 8-14. Distribution of nuclei. FIGS. 8, 9. Meristematic margin seen in surface and nirdian focal planes. Frc :. 10. Cross-section of meristematic margin showing nuclei in single, medial band. FIGS. 11, 12. Cross-sections of nieristenratic and mature tissues showirtg nuclei iri two bands. FIG. 13. Meristematic tissue in median optical section showing medial pit ronnections and nuclei in two bands. FIG. 14. Cross-section of older monostromatic tissue showing nuclei dispersed in a broad peripheral band. Frcs. 15, 16. Surface and median optical section of mature tissue. FIG. 17. Cross-section of a nerve. FIG. 18. Cross-section of stipe. Figures 8- 14, 17, hematoxylin; Figures 15, 16, 18, aniline blue. MMUOGRAMMEAE TRIB. NOV. 111 istematic and mature cells present a window in sur- Femab reproduction. Procarps are formed on both face view (Fig. 8), framed by a border of nuclei surfaces of the thallus in growing regions near the when seen in median optical section (Figs. 4, 7, 9). margin. A fertile central cell is either binucleate or Nuclei are aligned in a single plane in dividing cells multinucleate. It first elongates in the prevailing di- near the margin of the thallus (Fig. 10). Further in rection of growth, usually toward the thallus apex or the interior, the nuclei divide and separate into two margin, and cuts off four pericentral cells, two an- distinct rings disposed along side walls on either side terior and two posterior on either side. Cytoplasm of the plane passing through the middle of the and nuclei first migrate toward the anterior end of blade in both meristematic and mature cells (Figs. the fertile central cell, the nuclei divide, and the 11, 12). These are resolved as two rings of nuclei cytoplasm divides twice obliquely, cutting off ante- lying in different planes around the periphery inside rior pericentral cells on both sides that remain ster- the cell wall when viewed in a median optical section ile and do not contribute further to the develop- under conditions of low resolution and high con- ment of the procarps (Fig. 19).An anterior pericen- trast (Fig. 13). Still older cells may have many nuclei tral cell was either uninucleate or multinucleate at distributed in a broad circular band around the cen- inception but became multinucleate and vacuolate tral vacuole and between the chloroplasts that face and elongated transversely and divided once or outward on either side (Fig. 14). Nuclei were vari- twice as the procarp enlarged and matured. Kylin able in size in dividing cells, ranging from 3 to 6 p,m (1934, 1956) called such vegetative pericentral cells in diameter, but were relatively constant at a 5-6 pm and their derivatives “cover cells.” They resemble diameter in mature, nonmeristematic cells. Larger ordinary vegetative cells but can usually be distin- meristematic and young mature vegetative cells guished by the presence of a single primary pit con- tended to have 12-16 nuclei per cell, or six to eight nection linking the innermost cover cell to the cen- in each circular ring, with greater numbers in larger tral cell (Fig. 20), even at late stages. Only rarely did cells. a fertile central cell divide transversely and then the Young marginal cells may contain parietal lami- cover cells were absent. nate chloroplasts; however, the chloroplasts are Once the cover cells have been cut off, the cyto- soon dissected into minute discoid elements ap- plasm is reorganized toward the posterior end of the proximately 3-4 pm wide and 4-8 p,m long, as seen fertile central cell, and a single, uninucleate peri- in older meristematic and mature cells (Fig. 15). central cell is cut off on both sides that form pro- Secondary pit connections appeared to be formed carps (Fig. 20). A fertile pericentral cell divides at a steady rate over time, with the result that there obliquely, cutting off the first sterile group initial were fewer secondary pit connections per unit area outwardly and to one side (Fig. 21). It then divides in rapidly dividing patches of meristematic tissue, longitudinally by a concavo-convex wall to form the and recently formed secondary pit connections were initial of the carpogonial branch, which divides more abundant near the margin in slower growing transversely to form first a two-celled and then a regions. Initially, they were median to submedian in three-celled carpogonial filament (Fig. 22). At this position and only rarely, if ever, were they produced stage, the supporting cell cuts off a second sterile adjacent to external cell walls. At maturity, each ad- group initial. Finally, the third cell of the carpogo- joining cell was connected by either a primary or a nial filament divides obliquely, cutting off the car- secondary pit connection, or a pit connection was pogonium, which lies partly beneath the third cell absent. Seldom was there more than one pit con- of the carpogonial branch. The tip of the carpogo- nection between adjacent cells. The arrangement of nium elongates into a trichogyne that emerges from cell walls, protoplasts, and pit connections is readily the thallus surface directly behind the cover cells seen in material stained with aniline blue and (Fig. 23). Sterile groups normally remained one- mounted in Karom syrup, a medium that tends to celled and uninucleate in functional procarps be- expand cell walls and the intercellular matrix and fore fertilization. Unfertilized procarps in which the shrink protoplasts (Fig. 16). sterile groups were divided had usually started to The vegetative thallus of Myriogramme lividu was degenerate and were nonfunctional. The second monostromatic except for the stipe, central midrib, and sometimes the third cell of the carpogonial and subdichotomously branched nerves that were branch becomes binucleate before fertilization, usually restricted to the base or lower portion of a whereas the first cell usually remains uninucleate blade. Reproductive structures were also polystro- (Fig. 23). The carpogonium is uninucleate. matic. Midribs and nerves were formed by a peri- The carpogonium divides twice after presumed clinal division of primary cells or surface cortical fertilization, cutting off two connecting cells, the cells on both sides of the thallus, such that the cells first distal and the second proximal on the side fac- are arranged in tiers and rows. The residual primary ing the supporting cell (Fig. 24). Each connecting cells form a central row that is distinctly broader in cell contains a highly condensed nucleus surround- young nerves (Fig. 17) but that may be variously ed by a hyaline region and an outer membrane or modified in older, thicker ribs and stipes, often as a thin cell wall (Fig. 29). At the same time, the sup- result of differential cell expansion (Fig. 18). porting cell cuts off a large auxiliary cell distally, and 112 MAX H. HOMMERSAND AND SUZANNE FREDERICQ

\\ 20 ) " 19 22 /f - .\

Fic;s. 19-27. Procarp and cystocarp development in Myriogrnmme lzvidn. Bars = 10 pm. Abbreviations: ac = auxiliary cell, cb,, cb,, cb,, chi = cells of the carpogonial branch, cc = central cell, con,, con2 = connecting cells, cp = carpogoniurn, dn = diploid nucleus, fpc = fertile pericentral cell, gon = gonimoblasts, hn = haploid nucleus, pb = protein body, pg = primary gonimohlast cell, sc = supporting cell, st,, st? = strrile groups, tr = trichogyne, vpc = vegetative pericentral cell (= cover cell). FIG. 19. Central cell with two nuclei and two opposite anterior vegetative pel-icentr-al cells with one nucleus each. FIG. 20. Anterior vegetative pericentral cell and posterior t'ertile pericentral cell. FIG. 21. Sterile group 1 cut off from the fertile pericentral cell. FIG. 22. Stage with a three-celled carpogonial branch and sterile group 2. FIG. 23. Stage with a four-celled carpogonial branch and trichogyne. FIG. 24. Postfertilization stage. Carpogoniuni with two cunnccting cells, auxiliaiy cell with a haploid nucleus and protein body. FIG. 25. Auxiliary cell containing a diploid arid a haploid MYRIOGRAMMEAE TRIB. NOV. 113 the first and second sterile groups sometimes also and old cystocarps. At first, the gonimoblasts grow divide (Figs. 24, 28). The auxiliary cell becomes and branch monopodially, and carposporangia ma- densely filled with cytoplasm, one or more protein ture basipetally, forming branched chains. The cen- bodies form, and the haploid nucleus is situated in tral fusion cell is initially small, nuclei are variable the lower corner on the side away from the carpo- in size, and most of the central cells in the floor of gonial branch (Fig. 24). The distal connecting cell the cystocarp remain intact. Later, a few central cells is nonfunctional whereas the proximal connecting are sometimes incorporated into the fusion cell, and cell fuses onto the lower side of the auxiliary cell, the gonimoblast filaments become highly branched and the diploid nucleus migrates toward the center (Fig. 36) and bear carposporangia in branched of the auxiliary cell (Fig. 25). The diploidized aux- chains (Figs. 37, 38). iliary cell enlarges and divides, forming a small distal As the first crop of carpospores mature and are gonimoblast initial and a larger proximal remnant released, intercalary gonimoblast cells elongate, auxiliary cell. Figure 30 illustrates the position of the their nuclei divide, and secondary gonimoblast fila- gonimoblast initial in relation to the remnant aux- ments are generated that bear carposporangia in iliary cell, supporting cell, central cell, and the two clusters at their tips (Figs. 39-43). Terminal goni- sterile cell groups in an unstained preparation. moblast cells distend and divided obliquely near The gonimoblast initial divides apically (Fig. 31) their apices, cutting off two to three initials (Figs. and laterally, usually producing three initials that 39, 40), each of which produces a branched chain branch radially, arching forward and backward of cells that mature into a club-shaped cluster of around the auxiliary cell (Figs. 26, 27). Fusions take carposporangia (Figs. 41, 42). Repeated nuclear di- place early during gonimoblast formation, starting visions and branching of intercalary gonimoblast with the supporting cell, which fuses with the rem- cells produce additional carposporangia as long as nant of the auxiliary cell (Fig. 31) and later includes the cystocarp remains productive. Inner gonimo- the central cell and its pericentral cell on the op- blast cells are added progressively to the fusion cell, posite side, the primary gonimoblast cell, and basal which becomes highly branched and filled with cells of the gonimoblast filaments (Figs. 32-35). The many small nuclei (Fig. 43). The basal portion of two sterile groups remain separate and distinct from the fusion cell continues to fuse with the central the fusion cell (Figs. 26, 27, 30-32) and are later cells in the floor of the cystocarp. The fusion cell of usually seen detached (Fig. 33). The haploid nuclei a fully mature cystocarp is massive, supported by ba- of the two sterile groups enlarge and stain heavily sal extensions looking like the legs of a stool and with hematoxylin (Figs. 26, 27, 31-33), whereas the gonimoblast filaments that resemble a candalabra multinucleate central cells in the floor of the cys- bearing clusters of carposporangia terminally (Fig. tocarp distend and their nuclei also enlarge (Figs. 42). 32,33). Gonimoblast filaments first grow unilaterally It should be noted that, whereas the primary gon- in a fan-shaped fashion, arching forward and back- imoblasts grow and branch monopodially, second- ward around the central fusion cell (Figs. 27, 34, ary gonimoblasts develop sympodially. Cystocarps of 35), ultimately surrounding it completely. An ostiole intermediate age contain both monopodially and develops above the first sterile group (Figs. 30-33) sympodially developed gonimoblasts and carpospo- and slightly off-center (Fig. 33). rangia borne both in branched chains and terminal, Vegetative cells in the vicinity of the young goni- club-shaped branched clusters. Older cystocarps moblasts divide periclinally to produce a pericarp usually contain clusters of gonimoblasts of different five to seven cell layers thick, in which the cells are ages and stages of development (Fig. 42). Function- rectangular in cross-section and organized roughly ally, these are like the gonimolobes found in genera into horizontal tiers and longitudinal rows (Figs. 36, of Ceramiaceae and Rhodymeniaceae. Mature cys- 38). Mucilaginous material is secreted into the cystocarps measure 1 mm in diameter and are about tocarp cavity beginning in the vicinity of the sterile 500-600 pm thick. groups (Fig. 30) and extending above the plane of Mate reproduction. Spermatangia are produced in the central cells (Fig. 33). Cells of the upper peri- small sori (Fig. 44) on both sides of the blade (Fig. carp detach from the central cells, leaving no rem- 50), except along the margin. Sori are initiated in nant of the original pit connections. Mucilage secre- monostromatic parts of the blade as a result of re- tion and lateral extension of the cystocarp cavity sumption of cell division in otherwise mature cells proceed well in advance of radial growth and exten- (Fig. 45). Development follows the general pattern sion of the gonimoblast filaments (Fig. 33). described by Kylin (1923) for Phjcodrys rmbens (Lin- The gonimoblasts and carposporangia develop naeus) Batters (as P. sinuosa) and by Papenfuss differently and have a different appearance in young (1939) for Acrosmkm acrospermum u.Agardh) Kylin. t nucleus. FIG. 26. Residual auxiliary cell and primary gonimoblast cell bearing one distal and one lateral gonimoblast filament. FIG. 27. Residual auxiliary cell and primary gonimoblast cell bearing a distal and two lateral gonimoblast filaments. Hematoxylin. 114 MAX H. HOMMERSAND AND SUZANNE FREDERICQ

Fic:s. 28-33. Cystocarp development in Myn'ogramnze Zzvida. FIGS.28, 29. Surface and median focal planes of early postfertilization stage showing divided sterile group 1 (stl), sterile group 2 (stz), supporting cell (sc), auxiliary cell (ac), first, second, and third cells of the carpogonial branch (cb,, cbp,cb,) and the carpogonium (cp) that has cut off two connecting cells (con, and con,). FIG. 30. Cross-section of early postfertilization stage showing central cell (cc), supporting cell (sc), two sterile groups (st, and st2) surrounded hy a mucilaginous envelope (mu), gonimohlast initial (gi), residual auxiliary cell (ac), and a second pericentral cell (pc) below. FIG. 31. Cross-section of young cystocarp showing the first sterile group (stl) beneath the ostiole and recently divided gonimoblasts (g). FIG. 32. Cross-section of young cystocarp with gonimoblasts (g). (Note enlarged nuclei in cells of sterile group [st,] and in cells in floor of cystocarp.) FIG.33. Cross-section of cystocarp with an ostiole, steIile groups (st), gonimoblasts (g), and fusion cell (fu). (Note that the cystocarp cavity has formed in advance of the r-arnieing gonirnoblasts.) Figures 28, 29, 31-33, hematoxylin; Figure 30, unstained. MYRIOGRAMMEAE TRIB. NOV. 115

FIGS.34-43. Cystocarp development in Mp'opuamm livida. FIGS.34, 35. Median optical section showing branching pattern of gonimoblasts around central fusion cell (fu) and incorporation of inner gonimoblast cells onto fusion cell (arrows). FIG.36. Crosssection of cystocarp showing central fusion cell and monopodially branched immature primary gonimoblasts. FIG. 37. Primary carposporangia in branched chains. FIG.38. Cross-section of cystocarp showing multinucleate central fusion cell bearing primaIy and immature secondary carposporangia. FIG.39. Intercalary gonimoblast cell showing metaphase plate (arrow). FIG. 40. Fused gonimoblast filaments terminated by immature clusters of secondary carpo- sporanga (arrow).FIG. 41. Branched chain of secondary carposporangia terminating fused gonimoblast filament. FIG.42. Crosssection of old cystocarp with large central fusion cell that has incorporated most central cells in floor of cystocarp. (Note fused gonimoblast filaments bearing older [left side] and younger [right side] crops of secondary carposporangia.) Frc. 43. Chains of mature secondary carposporangia terminating fused gonimoblast filaments. Figures 34-41, 43, hematoxylin; Figure 42, aniline blue. 116 MAX H. HOMMERSAND AND SUZANNE FKEDERICQ

FIGS.44-55. Spermatangial and tetrasporangial development in Myriogrumme Zivida. FIG. 44. Spermatangial sori near margin. Fic;. 45. Surface view of young spermatangial sorus showing cortical cells, spermatangial parent cells and spermatangia. FIG. 46. Patterns of anticlinal division of cortical cells and spermatangia with primary pit connections as seen in surface view. FIG. 47. Crosssection of sorus showing young cortical cells. FIG. 48. Cortical cells undergoing anticlinal divisions. FIG.49. Spermatangia and a few spermatia. (Note pit connection to central cell [arrow]). FIG. 50. Cross-section of mature sorus showing basal nuclei in spermatangia and nuclei in released spermatia. FIG. 51. Tetrasporangial sorus in monostromatic blade near margin. FIG. 52. Developing tetrasporangia (t) in median focal plane cut off from primary cells (= central cells). FIG. 53. Cross-section of sorus at three-layered stage showing tetrasporangia (t) coruiected to primary cells (= central cells). FIG. 54. Surface view showing dividing tetrasporangia surrounded by cortical filarrie~its.FIG. 55. Cross-section nf sorus with mature tetrasporangia. Figures 44-54, Iiematoxylin; Figure 55, aniline blue. MYRIOGRAMMEAE TRIB. NOV. 117

Primary cells of the monostromatic thallus divide (Kylin 1924:figs. 43,47c). The carpogonium was said periclinally to form a layer of cortical cells on both always to develop inwardly from the third cell of the surfaces (Fig. 47). Alternatively, primary cells occa- carpogonial branch. No mention was made of "COV- sionally divide anticlinally into two or more cells be- er cells," which appeared to be absent. Our survey fore cutting off cortical cells on either side, with the showed that this type of procarp occurs in Myrh result that both central cells and patches of cortical gramme minuta Kylin (= Drachiella minuta [Kylin] cells are variable in size (Figs. 45, 46, 48). Division Maggs et Hommersand 1993) and in Schizoseris and of cortical cells is initially anticlinal with successive Neuroglossum but not in the type species of My& divisions usually taking place at right angles to gen- gramme, M. livida, or in most species assigned to My- erate a rectangular, filamentous cluster of surface n'ogramm. Instead, Myriagramme livida possesses pro- cells united by primary pit connections (Fig. 46). As carps in which the central cell cuts off two pairs of anticlinal divisions continue, every cell is converted pericentral cells opposite one another on each side into a spermatangium, with a nucleus located at its of the thallus, with the first of each pair developing base. Spermatangia are cut off by concavo-convex into a sterile vegetative cell, the cover cell, and the walls and are initially ovoid to ellipsoid in shape second forming the procarp. Each procarp contains (Figs. 45, 49). Released spermatia round up and ac- two one-/to two-celled sterile groups, but the car- cumulate beneath the outer cuticular layer (Fig. 50). pogonium is usually not inwardly curved to the ex- Evidently, the spermatia are released upon dissolu- tent seen in Drachiella minuta. Schizoseris, Neuroglos- tion of the outer layer. Spermatangial sori expand sum, and Drachiella all have similar procarps and are in area, and they sometimes link up to form irreg- distinguished from Myriogramme by a suite of char- ular patches in upper parts of the thallus. acters that call for the establishment of a new tribe. Tetrasporangiat development. Like the spermatangia, This will be the subject of a separate paper. tetrasporangia are produced in small circular to el- The type of procarp that characterizes Myriogram- liptical sori formed simultaneously on both sides of me livida was first observed in Nitophyllum bonnemai- the blade by resumption of cell divisions in other- sonii sensu Greville from Roscoff, France (Kylin wise mature cells. Sori are formed anywhere except 1934:fig. 1). Kylin showed that, in contrast to the in the basal region and along the margin of the thal- type species of Nitophyllum, N. punctatum (Stack- lus (Fig. 51). New sori are often interpolated be- house) Greville, the cover cell occupies an anterior tween preexisting soral patches, and sori sometimes rather than a lateral position, procarps on each side merge but are never confluent over an extended of the thallus stand directly opposite one another area. Central cells first divide periclinally on both rather than diagonally opposite, and the procarp sides to produce a cortical layer (Fig. 52). The first contains both a lateral and a basal sterile group rath- tetrasporangia are cut off laterally to obliquely, in er than just a lateral sterile group. Reinterpreting the plane of the blade from primary cells in the cen- his figures of the procarps of Nitophyllum miraln'le Ky- ter at the three-layered stage (Figs. 52,53). The cor- lin from Friday Harbor, Washington (Kylin 1925:fig. tical cells divide again to produce a five-layered 41), Kylin (1934) concluded that the procarp of that structure, and additional tetrasporangia are cut off species developed in the same manner as in N. bon- from the central cells. As the tetrasporangia enlarge, nmaisonii. In 1934, Kylin suggested that Nitophyllum cells in the outer cortical layer divide anticlinally, bonnemuisonii and N. mirabile should probably be forming a filamentous structure encircling each tet- placed in a new genus; however, he ultimately re- rasporangium (Fig. 54). Each central cell typically tained both species in Nitophyllum (Kylin 1956). produces two (to four) tetrasporangia, which divide In 1981, Zinova investigated the systematic posi- simultaneously into four tetrahedrally shaped tetra- tion of Nitophyllum bonnemaisonii and Mynogramme ye- spores. Tetrasporangia are spherical to ellipsoidal in zoense Yamada et Tokida, which Mikami (1972) had shape and measure 40-90 pm in length by 40-60 transferred to Nitophyllum based on the presence of pm in width (Fig. 55). cover cells and two sterile groups similar to those found in ~i~ophyllumbonnemaisonii. Zinova redefined DISCUSSION Nitophyllum to include species in which the fertile When Kylin (1924) established the Myriogramme central cell gives rise to a vegetative and a fertile group, he included four free-living and two parasitic pericentral cell at right angles to adjoining vegeta- genera: Myriogramme, Platyclinia7 Schizoseris, Neurog- tive cells, the fertile pericentral cell (= supporting lossum, and Gonimocolax and Polycmyne. The group cell) forms a single sterile group, and carposporan- was characterized as having bladelike thalli with gia are solitary and terminal. At the same time, she branching or proliferations from the margin, a mid- erected two new genera, Haraldiophyllum A. Zinova, rib or macroscopic veins present or absent; micro- based on Delessen'a bonnemaisonii sensu Greville, and scopic veins absent; transversely dividing apical cells Hideophyllum A. Zinova, based on Myriogramme ye- absent; and gonimoblasts with spores in chains. Pro- zoense, to contain species in which the fertile central carps were described as being of the Phycodrystype cell produces two pericentral cells situated vertically with two groups of sterile cells, but with the number with respect to the thallus axis with the top cell of cells in each sterile group reduced to one or two forming one to three cover cells and the bottom cell 118 MAX H.HOMMEKSAND AND SUZANNE FREDERICQ becoming the supporting cell bearing two one-/to scopic veins are absent. In Cryptopleura, the nuclei twocelled sterile groups and a four-celled carpogo- are scattered across the surface of the cell beneath nial branch. ~araldiophyllum was characterized as a layer of discoid chloroplasts, and microscopic having terminal carposporangia and Hideophyllum as veins are usually present; in Nitophyllum the nuclei having carposporangia in chains. In addition to H. are initially parietal along the lateral walls but are bonnemaisonii (Greville) A. Zinova, it was proposed later distributed uniformly across the cell surface that Haraldiophyllum contained H. mirabile (Kylin) A. just below the discoid chloroplasts, whereas in Dra- Zinova and H. versicolor (Harvey) A. Zinova. chieZZu the nuclei are situated beneath a single pari- Wynne (1983) reviewed and updated the classifi- etal platelike chloroplast or several convoluted, rib- cation of the Delesseriaceae. He accepted all the bonlike chloroplasts formed through the fusion of groups in Nitophylloideae recognized by Kylin many discoid plastids (Maggs and Hommersand (1924, 1956), except the Yendonia group. Most 1993). The cell type and nuclear and chloroplast groups and genera were defined in accordance with behavior characteristic of Myriogramme livida were characters recognized by Kylin. Wynne placed Hi- seen in all the species listed in this paper under deophyllum, with carposporangia in chains, in the My- “specimens of other taxa examined.” riogramme group and Haraldiophyllum, with termi- Blades form midribs and macroscopic veins or be- nal carposporangia, in the Nitophyllum group. Har- come polystromatic in two ways in the Nitophyllo- aldiophyllum versicolor (Harvey) A. Zinova became H. ideae: either by periclinal division with the cells ly- heterocurpum (Chauvin ex Duby) Wynne, and Nit& ing in horizontal tiers and vertical rows or by both phyllum nottii R. Norris et Wynne (1969) was trans- periclinal and anticlinal divisions producing ferred to Haraldiophyllum. Wynne (1996) kept the branched corticating filaments. Members of the My- same taxonomic arrangement with Hideophyllum in riogramme group become polystromatic primarily the Myriogramme group and Haraldiophyllum in the by periclinal divisions. Periclinal divisions predomi- Nitophyllum group. nate in the Cryptopleura group and the Nitophyl- Recently, Maggs and Hommersand (1993) trans- lum group intermixed with occasional anticlinal di- ferred Haraldiophyllum heterocarpum and Myriogramme visions (Kylin 1924, Wagner 1954),whereas periclin- minutum to Drachiella as Drachiellu heterocaqa (Chau- a1 and anticlinal divisions are both frequent in Schi- vin ex Duby) Maggs et Hommersand and Drachiella zoseris and Drachiella and give rise to regularly minutu (Kylin) Maggs et Hommersand and placed branched cortical filaments (Ricker 198’7, Maggs them in the Schizoseris group, a new group that and Hommersand 1993). they did not characterize. They retained Huraldi- Among the Nitophylloideae, vegetative pericen- ophyZlum bonn.emaisonii (Kylin) A. Zinova, established tral cells (cover cells) are present only in taxa allied on a new basionym, Myriogramme bonnemaisonii Kylin, with Nitophyllum or with those allied with Myriogram- and placed Haraldiophyllum in the Myriogramme me. Both groups have large prismatic vegetative cells group. with conspicuous central vacuoles. While the central All of the taxa listed in this paper under “speci- cells are not fully mature at the time they produce mens of other taxa examined” possess procarps of the procarps, they have usually ceased dividing and the Myriogramme livida type and on that basis alone are larger than in other members of the Nitophyl- are referable to the Myriogramme group. As impor- loideae. Cytoplasm is first concentrated to one side tant as procarp development has been historically in Nitophyllum and to the anterior end in Myriogram- for classification at the generic and suprageneric lev- me, where it is cut off with the cover cells, which els, it is not the only feature that unites a cluster of quickly become vacuolate. Most of the cytoplasm re- taxa with Mynogramme livida. Other vegetative and maining in the central cell is cut off with the fertile reproductive characters are equally important. Taxa pericentral cell (= supporting cell). This behavior related to Mynogramme lack transversely dividing api- appears to be related to the larger cell size and state cal cells, except occasionally in juvenile thalli. An of vacuolation of a potential fertile central cell in apical cell, if present, divides obliquely along two Nitophyllum and Myriogramme compared to that in cutting faces or, more often, growth is maintained other Nitophylloideae. If so, the striking differences by a marginal meristem, and intercalary cell divi- in the arrangement of the cover cells and sterile sions are abundant along the margin and in the in- groups in the two procarp types testifies to the interior of the thallus. The same is true of taxa that dependent origin of cover cells in each case and the cluster with CryptopZeura, Nitophyllum, and Schizoseris separate evolutionary histories of their procarp or Drachiella. The differences lie in the behavior of types. nuclei and plastids during cell division and the ap- Connecting cells have rarely been seen in mem- pearance of the mature vegetative cells. In Myno- bers of the Delesseriaceae. Papenfuss (1961) re- gramme, mature vegetative cells are large, polygonal, ported that the carpogonium cuts off a connecting highly vacuolate, and transparent when viewed from cell on the side facing the auxiliary cell in Caloglossa the surface, with the nuclei situated along the trans- that fuses with it and presumably delivers a diploid verse walls and the chloroplasts su erficial and nucleus; however, he notes “that this feature has not breaking up into small subunits (Figs. y-15). Micro- heretofore been observed in the many genera of De- MYRIOGRAMMEAE TRIB. NOV. 119 lesseriaceae that have been studied.” He further rangia are truly terminal in some species belonging comments that the presence of a connecting cell in to the Myriogramme group, whereas in others they Caloglossa, similar to those found in the Cerami- are formed in succession and only appear to be ter- aceae, lends support to the view that Caloglossa is minal. In still others, they are first produced termi- one of the most primitive members of the Delesser- nally and released in succession and only later re- iaceae. The reason, in our opinion, why connecting main attached, forming chains. Reports in the lit- cells may have been missed is because they are small erature concerning the arrangement of the carpo- hyaline structures that consist of a nucleus and a sporangia may not be reliable unless all bounding membrane without apparent associated developmental stages have been taken into account. cytoplasm. Thus, while they are easily seen with hematoxylin staining, they are not readily differenti- TAXONOMIC CONCLUSIONS ated with aniline blue. We have conducted a broad The morphological evidence presented here is for survey of most of the groups placed in the Delesser- a single species, Myriogramme livida, the type species iaceae and find that in each the carpogonium cuts of Myriogramme. We have shown that the concept of off two connecting cells, one anterior and the other the Myriogramme group of Kylin 1924, based as it lateral, with the lateral connecting cell usually being was on nontype material, has led to an incorrect the one that fuses with the auxiliary cell, as illus- characterization of that group. We now propose a trated here for Myriogramme livida (Figs. 24, 29). new tribe to replace the Myriogramme group of Ky- After diploidization, the auxiliary cell divides lin with a revised diagnosis and new circumscription transversely in Myriogramme livida, cutting off a small that includes part of the taxa recognized by Kylin gonimoblast initial containing a diploid nucleus and and excludes the rest. The diagnosis given below is a remnant auxiliary cell containing a diploid and a based on the type species and on species listed in haploid nucleus. The remnant cell corresponds to this paper under “specimens of other taxa exam- the foot cell seen in many Ceramiaceae; however, its ined.” size and the fact that it is filled with cytoplasm rather than being vacuolate mitigates against equating it Myriogrammeae Hommersand et Fredericq with the ceramiacean foot cell. Initials are cut off trib. nov. from the anterior and lateral surfaces of the primary Thallus foliosus monostromaticus aut tristromaticus gonimoblast cell that produce the gonimoblasts margzne, polystromaticus basaliter unico nmo basali aut (Figs. 26, 27). Of these, the anterior filament is nmisubdichotomi infme. Veni microscopici absentes. Cel- more strongly developed and has the appearance of lulae polygonales aspectu supe$ciali dispositae mdines a basal row of cells when seen in transverse section. hmkontales et sm’es verticab partibus polystromaticis. In- This arrangement, first reported by Kylin (1923) for crmtum diffuse meristematibus marginalibus interca- Phycodvs, has been seen in many Delesseriaceae. laribusque; nuclei lateriparietes in cellulas maturas, chb None of the features of early cystocarp develop roplasti parietales, initio simplices, postea dissecti in par- ment-the formation of the ostiole above sterile vas monades. Spermatangza in smos circulares ad ellipti- group 1, the schizogenous development of the cys- cos fmatosfduito in partibus supernis per renovationem tocarp cavity, the horizontal spread and vertical divisionem cellularum maturarum. Procarpia opposita utr- growth of the gonimoblast filaments or the fusions inque thalli, cellula centrali initio abscissa cellulam anter- of the supporting cell, the remnant auxiliary cell, iorem pericentralem vegetativam (cellulam obtectam} post and inner gonimoblast cells to form a fusion cell- cellulam pmkntralem f&ilem posticam (cellulam susti- are unique to Myriogramme. Fusion cells are small in nentem} constantia ex laterali turma sterili 1-2 cellular- Nitophyllum, larger in Cqptophra, and larger still in um, $10 carpogonali quadricellulari et tunna sterili basali Myriogramme and Schizoseris, where the fusions ex- unicellulari. Carpogonium abscissum 2 cellulas conjunc- tend to incorporate the inner gonimoblast cells (Ky- tivas, 1 conjunctam cellula auxiliaris. Cellula auxiliaris lin 1924), but the differences are differences of de- dividens transversale in anticum cellulam gonimoblasti gree and, while diagnostic at the group or tribal lev- continentem nuchum diploideum, et in posticam cellulam el, are less easily defined than some other charac- residualem (cellulam pedalem) continentem diploideum ters. nucleum 1-2 haploideosque nucleos. Filamenta gonimob The interpretation of late stages in cystocarp de- lasti genita in arcu cellula primarii gonimoblasti cingenta velopment is fraught with difficulties, not the least cellulam sustinentam postea extrinseca radiantia praeben- of which is that mature young cystocarps may have tia caqbospmangia vel terminalia vel catenata. Cellulafu- a different appearance from mature older cysto- sionalis formatur ad modum progressionis incmpmans cel- carps. Such is the case in Mynogramme livida, in lulam sustinentm, cellulam centralem, cellulam auxiliar- which the carposporangia are borne in open- is, primam cellulam gonimoblasti, internas cellulas goni- branched chains in young cystocaps, only to be re- moblasti et nonnulas cellulas in pavimentum cystocarpii. placed by carposporangia borne in tight clusters at CTptia cystocarpii schizogenea fmatur obtecta per peri- the ends of candalabra-like fusion cells in older cys- carpium ostiolo singulari tegenti steribm sturmam-l. Te- tocarps that have produced a second generation of trasporangia in smos parnos circulares vel ellipticos usque carposporangia. We have found that the carpospo- ad quinquestromaticosfmtuito in partibus supernis lami- 120 MAX H. HOMMERSAND AND SUZANNE FREDERICQ nae per renovationem divisionem cellularum maturamm. lum is distinct in that an obliquely dividing apical Tetrasporangza pnmaria genita 2(-4) per cellulam e cel- cell has been shown to produce a recognizable cen- lulis centralibus. Tetraspmangza secunda genita uterque tral axis (Mikami 1972). Species belonging to the cellulis centralibus cellulis cmticalibus interim’bus, tetrae- tribe Myriogrammeae that occur along the Pacific drica divisa. Coast of North and South America as far south as Genus typicum: Myriogramme Kylin 1924. Concepcibn, Chile, have an unusual fusion cell, first Plant body foliose monostromatic or tristromatic described by Kylin (1925) for Nitophyllum rnirabile [= at margin, polystromatic toward base with a single Haru~~ophyllummirabile], in which inner gonimo- basal nerve, or the nerves subdichotomously blast cells fuse secondarily by lateral fusion onto the branched below. Microscopic veins absent. Cells po- central cells in the floor of the cystocarp. Schizoseris lygonal in surface view, arranged in horizontal tiers and Ne-uroglossum are excluded from the Myriogram- and vertical rows in polystromatic parts. Growth dif- meae, and Polycoryne, which is parasitic on both Schi- fuse by marginal and intercalary meristems; nuclei zoseris and Myriogramme, appears to be more closely bordering the side walls in mature cells, chloroplasts related to Schizoseris. Platyclinia includes species that parietal, at first simple, later dissected into small belong in the Myriogrammeae, notably the ones in platelets. Spermatangia in circular to elliptical sori, South America, but the lectotype species, P. stipitata formed randomly in upper parts of blade by re- J. Agardh from Australia (Wynne 1983), requires newed division of mature cells. Procarps directly op reinvestigation. posite on both sides of thallus, the central cell first cutting off an anterior vegetative pericentral cell This material is based on work supported by the National Science (cover cell) from anterior end followed by a poste- Foundation under contract number DPP74-13988 to the Sniith- rior fertile pericentral cell (supporting cell) that sonian Institution. We thank Dr. Frank Ferrari arid Dr. Ernani bears a one-/to two-celled lateral sterile group, a Metiez from the Smithsonian Institution Oceanographic Sorting Center for encouraging this study and the reviewers, Michael four-celled carpogonial branch, and a one-celled ba- Wynne and Alan Millar, for their helpful suggestions and com- sal sterile group. Carpogonium cutting off two con- ments. necting cells, one of which fuses with auxiliary cell. Auxiliary cell dividing transversely into an anterior Abbott, 1. A. 1969. Some new species, new cornhinations, and gonimoblast cell and a posterior residual auxiliary new records of red algae from the Pacific coast. Madf07To20 cell containing a diploid nucleus and one to two 42-53. haploid nuclei. Gonimoblast filaments developing Agardh, J. G. 1876. Spe& Genera et Ordines Algarum, Vol. 3(1). from primary gonimoblast cell in an arc around the Epicrisis Systematis Floridearurn. T. 0.Weigel, Leipzig, vii t 7’24 PP. supporting cell, later radiating outwardly and bear- 1898. specie,^ Cmma et Ordines Algarum, Vol. 3(3).DieDis- ing carposporangia either terminally or in chains. positzone Delesseriarum curae posterioires. I.und, vi + 239 pp. Fusion cell formed progressively, incorporating the Cotton, A. D. 1Y15. Cryptogams from the Falkland Islands col- supporting cell, central cell, auxiliary cell, primary lected by Mrs. Valentin. Linn. Sac. J. Bot. 43:137-231, plates 4-10. gonimoblast cell, inner gonimoblast cells, and some Greville, R. IL 1830. Algae britannicae Edinburgh. lxxxviii + cells in floor of cystocarp. Cystocarp cavity formed 218 pp., 19 plates. schizogenously with a single ostiole overlying sterile Hollenberg, G. J.& Abbott, I. A. 1965. New species and new group 1. Tetrasporangia in small circular or ellipti- combinations of marine algae from the region of Monterey, California. Can. J. Bat. 43:1177-88. cal sori up to five layers thick, formed randomly in Holmgren, P. K., Holmgren, N. H. & Barnett, I.. C. 1990. Index upper parts of blade by renewed division of mature Herbariorum, Pt. I. The Herbaria (If the World, 8th ed. Interna- cells. Primary tetrasporangia arising two to four per tional Association for Plant Taxonomy, New York, and Rotan- cell from central cells. Secondary tetrasporangia iral Garden, Bronx, 693 pp. formed from both central cells and inner cortical Hommersand, M. H., Fredericq, S. & Cahioch, J. 1992. Devel- opmental morphology of Gzgaflina pislillata (Gigatinaceae, cells, tetrahedrally divided. Rhodophyta). Phycologia 31:300-25. Type genus: Mynogramme Kylin 1924. Hooker, J.D. 18461847. The Botany of the Antarctic Voyage (fH. Besides Myriogramm, the tribe Myriogrammeae M. Discnuoy Ships Erebus’ and ‘Terror’in the years 1839-1843 contains Gonimocolax, Hara~i~~yZl~m,and Hideo- . . . , Vol. 1. Flara antarctica . . . , Pt. 11. 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