Morphology of Chondrophycus undulata and C. parvipapillata and its implications for the taxonomy of the Laurencia (Ceramiales,Rhodophyta) complex

Laurencia Lamouroux subgenus Chondrophycus Tokida et Saito was recently raised to generic status as Chondrophycus (Tokida et Saito) Garbary et Harper (Ceramiales, Rhodophyta). The previously unknown morphology and anatomy of two Chondrophycus species, C. undulata (Yamada) Garbary et Harper and C. parvipapillata (C.K. Tseng) Garbary et Harper, were studied in specimens from Korea, Japan and Hawaii. These species share some features, such as a strongly compressed thallus, vegetative axes with two pericentral cells, tetrasporangial production from pericentral cells and spermatangial development of the trichoblast type. However, they differ from each other in the position of the first pericentral cell relative to the trichoblast in axial segments and in the position of the tetrasporangial pericentral cell. In C. undulata, the first pericentral cell is always produced at one side of the basal cell of a trichoblast, whereas in C. parvipapillata it is formed underneath this cell. While tetrasporangia in C. undulata are produced only from three (occasionally four) additional pericentral cells, in C. parvipapillata they are formed by the existing second pericentral cell and two (occasionally three) additional pericentral cells, so the resulting tetrasporangial axial segment has only one sterile pericentral cell rather than two as in C. undulata. C. undulata produces spermatangial branches from two laterals on the suprabasal cell of trichoblasts but one of the two remains partly sterile, whereas in C. parvipapillata a spermatangial branch develops from only one of the two laterals. These two species also differ distinctly from each other in some vegetative features, such as presence or absence of (1) secondary pit connections between epidermal cells, (2) a palisade structure of epidermal cells with conical projections and (3) corps en cerise. The taxonomic implications of these vegetative and reproductive features of Chondrophycus and those of other genera of the Laurencia complex necessitate changes to the generic delineations of Osmundea Stackhouse, Laurencia and Chondrophycus. The required new combinations in Chondrophycus are made, mainly for species from the western Pacific. An infrageneric classification scheme is also proposed for Chondrophycus including Kangjaewonia subgen. nov., Palisada (Yamada) subgen. stat. nov., Yuzurua subgen. nov. and Parvipapillatae sect. nov.     

Morphology of Laurencia clavata and L. elata (Ceramiales,Rhodophyta) in relation to generic circumscription in the Laurencia complex

Laurencia Lamouroux (Rhodophyta) was recently separated into three genera–Laurencia, Chondrophycus (Tokida et Saito) Garbary et Harper and Osmundea Stackhouse – each of which was newly defined based on vegetative and reproductive structures. In this study, the previously unknown vegetative and reproductive morphology of two Australian endemic species of Laurencia, L. clavata Sonder and L. elata (C. Agardh) Harvey, was studied, particularly in the context of the revised generic delineation. These species exhibit vegetative axes with four pericentral cells and trichoblast-type spermatangial development. Tetrasporangia are abaxially produced from the existing third and fourth pericentral cells. L. clavata has terete thalli with distinctive verticillate branching and is similar to Chondria C. Agardh, rather than to Laurencia, in having an unusually marked constriction at the base of the branches and starch accumulation in subcortical and medullary cells. Compared to Laurencia, apical cells of this species exhibit a less oblique division ; the resulting recognizable axial cell rows extend somewhat below the branches, and particularly at a young stage they are also clear throughout branchlets. However, other vegetative and spermatangial structures show that L. clavata is more closely allied to Laurencia than to Chondria, and it is placed in Laurencia. By contrast, L. elata exhibits morphology typical of Laurencia and is characterized by large, robust, compressed thalli with fastigiately distichous branching and an extensive secondary cortex. Furthermore, it appears to be distinct from similar species in sometimes having a parasitic species of Janczewskia Solms-Laubach (Rhodophyta). Taxonomy of Laurencia is discussed on the basis of these and previous studies.     

TAXONOMY AND PHYLOGENY OF OSMUNDEA (RHODOMELACEAE, RHODOPHYTA) IN ATLANTIC EUROPE

Two species of Osmundea Stackhouse (Rhodomelaceae, Rhodophyta) that occur in Atlantic Europe have been confused under the names Osmundea ramosissima (Oeder) Athanasiadis and Osmundea truncata (Kützing) Nam et Maggs, regarded until now as a synonym of O. ramosissima. An epitype from its type locality (Stavanger, Norway) is selected for Osmundea ramosissima Athanasiadis, recognized here as a valid name for Fucus ramosissimus Oeder, nom. illeg. Details of vegetative and reproductive morphology of O. ramosissima are reported, based on material from France, the British Isles, and Helgoland. Osmundea ramosissima resembles other species of Osmundea in its vegetative axial segments with two pericentral cells and one trichoblast, spermatangial development from apical and epidermal cells (filament type), the formation of five pericentral cells in the procarp‐bearing segment of the female trichoblast, and tetrasporangial production from random epidermal cells. Among the species of Osmundea, O. ramosissima is most similar to O. truncata. Both species have discoid holdfasts, secondary pit connections between epidermal cells, and cup‐shaped spermatangial pits. They differ in that: (a) O. ramosissima lacks lenticular wall thickenings and refractive needle‐like inclusions in medullary cells, both of which are present in O. truncata; (b) O. ramosissima has branched spermatangial filaments that terminate in a cluster of several cells, whereas in O. truncata the unbranched spermatangial filaments have a single large terminal sterile cell; and (c) cystocarps of O. ramosissima lack protuberant ostioles but ostioles are remarkably protuberant in O. truncata. Phylogenetic analyses of rbcL sequences of Laurencia obtusa (Hudson) Lamouroux and all five Atlantic European species of Osmundea, including the type species, strongly support the generic status of Osmundea. Osmundea ramosissima and O. truncata are closely related (5.2% sequence divergence) and form a well‐supported clade sister to a clade consisting of O. pinnatifida (Hudson) Stackhouse, O. osmunda Stackhouse and O. hybrida (A. P. de Candolle) Nam. The formation of secondary pit connections between epidermal cells is a synapomorphy for the O. ramosissima+O. truncata clade. The close relationship between species with cup‐shaped spermatangial pits (Osmundea hybrida) and urn‐shaped pits (Osmundea pinnatifida and Osmundea osmunda) shows that spermatangial pit shape is not an important phylogenetic character. Parsimony analysis of a morphological data set also supports the genus Osmundea but conflicts with the molecular trees in infrageneric relationships, placing O. hybrida basal within the Osmundea clade and grouping O. osmunda and O. pinnatifida but not O. truncata and O. ramosissima. A key to Osmundea species is presented.     

LAURENCIA MARILZAE SP. NOV. (CERAMIALES,RHODOPHYTA) FROM THE CANARY ISLANDS,SPAIN, BASED ON MORPHOLOGICAL AND MOLECULAR EVIDENCE1

Laurencia marilzae Gil‐Rodríguez, Sentíes et M.T. Fujii sp. nov. is described based on specimens that have been collected from the Canary Islands. This new species is characterized by distinctive yellow–orange as its natural habitat color, a terete thallus, four pericentral cells per vegetative axial segment, presence of secondary pit‐connections between adjacent cortical cells, markedly projecting cortical cells, and also by the presence of corps en cerise (one per cell) present in all cells of the thallus (cortical, medullary, including pericentral and axial cells, and trichoblasts). It also has a procarp‐bearing segment with five pericentral cells and tetrasporangia that are produced from the third and fourth pericentral cells, which are arranged in a parallel manner in relation to fertile branchlets. The phylogenetic position of this taxon was inferred based on chloroplast‐encoded rbcL gene sequence analyses. Within the Laurencia assemblage, L. marilzae formed a distinctive lineage sister to all other Laurencia species analyzed. Previously, a large number of unique diterpenes dactylomelane derivatives were isolated and identified from this taxon. L. marilzae is morphologically, genetically, and chemically distinct from all other related species of the Laurencia complex described.     

Two species of Dasya (Ceramiales, Rhodophyta) from Bonin Islands, southern Japan, with the description of Dasya boninensis sp. nov.

Two species of Dasya in the Dasyaceae (Ceramiales, Rhodophyta) are reported from Bonin Islands, southern Japan. Dasya murrayana Abbott et Millar, new to Japan, is characterized by the following set of features: the tufted habit (up to 30 erect axes developing from a basal disc), small‐sized (6–10 mm high and 350–500 μm in diameter in the middle region), thinly but completely corticated axes, rigid and incurved pseudolaterals forming corymbose heads at the apices of axes and branches, the absence of adventitious monosiphonous filaments, a large number of tetrasporangial stichidia and spermatangial branches per fertile pseudolateral and slender spermatangial branches (35–45 μm in diameter). Dasya boninensis Masuda, Kurihara et Kogame, sp. nov. is characterized by short but thick (10–30 mm high and 600–1000 μm in diameter at the middle portion), heavily corticated axes, indistinct pericentral cells except for the upper portion in transverse sections, soft, straight pseudolaterals and adventitious monosiphonous filaments densely covering the axis and branches, a small number of tetrasporangial stichidia and spermatangial branches per fertile pseudolateral, thick spermatangial branches (65–90 μm in diameter), and short‐necked cystocarps. A dichotomous key to the taxa found in Japanese waters is given.     

Polysiphonia perforans sp. nova (Ceramiales,Rhodophyta) from the Mediterranean Sea

ABSTRACT

A new species of the genus Polysiphonia from the Mediterranean Sea is described. It is an ecorticate species, with 4 pericentral cells, showing prostrate axes from which erect axes arise. Rhizoids are formed by pericentral cells in a median position remaining in open connection with them. Erect axes are straight, simple throughout or pseudodichotomous at the base then simple or with one (rarely two-three) orders of branching; trichoblasts and scar cells not observed. Only tetrasporangial plants were found. They show ellipsoid tetrasporangia borne in short straight series, often interrupted by sterile segments. The new species is also characterized by a peculiar habit consisting of prostrate axes, adhering to lower faces of Peyssonnelia spp. by means of rhizoids growing upward, from which erect upright axes perforating thalli of the supporting species arise. A comparison with the related species of Polysiphonia was also carried out.     

A study of the red alga,Calonitophyllum medium (Hoyt) comb. Nov. [= Hymenena media (Hoyt) Taylor]

Ontogeny of the vegetative system and reproductive structures found in Hymenena media (Hoyt) Taylor (Delesseriaceae, Nitophylleae) indicates that the alga is similar to the Phycodrys group in its vegetative development, and to the Nitophyllum group in its female reproductive system. The vegetative system bears striking resemblance to the type species of a European genus, Radicilingua [R. thysanorhizans (Holm.) Papenf.]. Reproductive structures of two other species of this genus, R. adriatica (Kylin) Papenf. and R. reptans (Zanard.) Papenf. and the type species are inadequately known. On the basis of several vegetative characters and the location and superficial organisation of the tetrasporangial sori, a new genus, Calonitophyllum, is proposed to contain our Western Atlantic plants. The new combination, Calonitophyllum medium (Hoyt) Aregood, thus replaces Hymenena media (Hoyt) Taylor.     

New records of three marine red algae from Japan

Three species in the red algal order Ceramiales, Dasya longifila Masuda et Uwai (Dasyaceae), Endosiphonia horrida (C. Agardh) P. Silva (Rhodomelaceae) and Laurencia flexilis Setchell (Rhodomelaceae), are reported from Japan for the first time, and their morphological features are described along with taxonomic comments. Our findings point to the northernmost limit of geographic distribution of these species in the north‐western Pacific. Dasya longifila is characterized by small, sparsely corticated axes, long pseudolaterals in which intercalary cell divisions take place, and a small number of tetrasporangial stichidia and spermatangial branches per fertile pseudolateral. Endosiphonia horrida is characterized by frequently anastomosing branches that form a bush‐like tuft without a percurrent axis, inner cortical cells becoming the same length as the axial and periaxial cells, and luxuriously developed, unbranched trichoblasts. Laurencia flexilis is characterized by numerous cartilaginous rigid axes developing from a basal disc without creeping branches, the production of 4 periaxial cells per vegetative segment and the absence of longitudinally oriented secondary pit‐connections between contiguous superficial cortical cells.     

Taxonomic notes on Laurencia brongniartii (Rhodomelaceae, Rhodophyta)

The red alga Laurencia brongniartii J. Agardh (Rhodomelaceae, Ceramiales) is characterized by: (i) the production of four periaxial cells from each vegetative axial segment; (ii) the presence of two or three corps en cerise per superficial cortical cell and one per trichoblast cell; (iii) the production of a single tetrasporangium-bearing periaxial (fourth) cell per fertile segment; (iv) a tetrasporangial arrangement that is intermediate between perpendicular and parallel types; (v) procarps produced from the last-formed (fifth) periaxial cell of the terminal segment of a two-celled female trichoblast; and (vi) distally positioned spermatangial nuclei, in addition to known features. The production of a single tet-rasporangium-bearing periaxial cell per fertile segment allies this species to Laurencia similis Nam et Saito.     

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

The Myriogramme group of Kylin was found to contain two distinct clusters of genera that merit recognition at the tribal level. In this paper, we establish the tribe Myriogrammae based on a study of the type species of Myriogramme, M. livida, from the Southern Hemisphere. The Myriogrammae is characterized by 1) marginal and diffuse intercalary meristems; 2) nuclei arranged in a ring bordering the side walls of vegetative cells; 3) microscopic veins absent; 4) procarps scattered, formed opposite one another on both sides of the blade posterior to one or more vegetative pericentral cells (cover cells) and consisting of a carpogonial branch, a one-/to two-celled lateral sterile group and a one-celled basal sterile group; 5) auxiliary cell diploidized by a connecting cell cut off posteriolaterally from the fertilized carpogonium; 6) gonimoblast initial cut off distally from the auxiliary cell, generating one distal and one to two lateral gonimoblast filaments that branch in the plane of the expanding cystocarp cavity and later fuse to from an extensive, branched fusion cell; 7) spermatangial and tatrasporangial sori formed inside the margin on both sides of the blade by resumption of meristematic activity; and 8) tetrasporangia produced primarily from the central cells. The Myriogrammae currently includes Myriogramme Kylin , Gonimocolax Kylin , Haraldiophyllum A. Zinova , Hideophyllum A. Zinova, and a possible undescribed genus from Pacific North and South America. Genera are separated based primarily on features of gonimoblast and carposporangial development .     

Reproductive morphology and taxonomic reappraisal of Exophyllum wentii Weber-van Bosse (Rhodomelaceae, Rhodophyta) from Bali Island, Indonesia

The little‐known and rarely collected alga Exophyllum wentii Weber‐van Bosse is re‐described in detail from the type material, as well as from new collections from Indonesia, which for the first time reveal in detail the structure of cystocarpic and spermatangial plants and the development of tetrasporangial stichidia under culture conditions. New morphological reproductive information confirms placement of the genus Exophyllum within the Rhodomelaceae. Exophyllum is distinguished from other related genera within the Rhodomelaceae by its cartilaginous, non‐trichoblastic decumbent thallus with multiple holdfasts and its discoid spermatangial organs. Some Pacific material earlier attributed to E. wentii was found to be misidentified and re‐assigned to the Dasyaceae.     

PHYLOGENETIC RELATIONSHIPS WITHIN THE GENUS HYPNEA (GIGARTINALES,RHODOPHYTA), WITH A DESCRIPTION OF H. CAESPITOSA SP. NOV.1

Species discrimination within the gigartinalean red algal genus Hypnea has been controversial. To help resolve the controversy and explore phylogeny within the genus, we determined rbcL sequences from 30 specimens of 23 species within the genus, cox1 from 22 specimens of 10 species, and psaA from 16 species. We describe H. caespitosa as a new species characterized by a relatively slender main axis; a pulvinate growth habit with entangled, anastomosing, and subulate uppermost branches; and unilaterally borne tetrasporangial sori. The new species occurs in the warm waters of Malaysia, the Philippines, and Singapore. The phylogenetic trees of rbcL, psaA, and cox1 sequences showed a distant relationship of H. caespitosa to H. pannosa J. Agardh from Baja California and the marked differentiation from other similar species. The rbcL + psaA tree supported monophyly of the genus with high bootstrap values and posterior probabilities. The analysis revealed three clades within the genus, corresponding to three sections, namely, Virgatae, Spinuligerae, and Pulvinatae first recognized by J. G. Agardh. Exceptions were H. japonica T. Tanaka in Pulvinatae and H. spinella (C. Agardh) Kütz. in Spinuligerae.     

An experimental approach to study the biosynthesis of brominated metabolites by the red algal genus Laurencia

The production of labeled brominated metabolites with radioactive ⁸²Br in Laurencia species was investigated as part of a study of the biosynthesis of halogenated metabolites from species belonging to the red algal genus Laurencia (Rhodomelaceae, Ceramiales). Radiobromide [⁸²Br], thin-layer chromatography (TLC), and TLC–autoradioluminography (ARLG) were used. When cultured in artificial seawater medium (ASP₁₂NTA including Na⁸²Br) under 16:8 h light:dark (LD) illumination cycles for 24 h, each of the strains of Laurencia, Laurencia japonensis Abe et Masuda, Laurencia nipponica Yamada (laurencin-producing race and laureatin-producing race), and Laurencia okamurae Yamada, produced species- (or race-) specific ⁸²Br-containing metabolites. In the case of the laurencin-producing race of L. nipponica, laurencin and deacetyllaurencin were found to be produced in approximately 1:1 ratio, though laurencin is the major metabolite in the wild sample. Furthermore, when cultured in the dark, the production rates of brominated metabolites in Laurencia spp. were found to be diminished. The present study strongly indicates that the use of radiobromine [⁸²Br] in combination with the TLC–ARLG method is an effective approach for investigating the biosynthesis of brominated metabolites in Laurencia.     

MORPHOLOGY OF PLACENTOPHORA (SOLIERIACEAE,GIGARTINALES: RHODOPHYTA), A NEW GENUS BASED ON SARCODIOTHECA COLENSOI FROM NEW ZEALAND1

The only member of the red algal family Solieriaceae known from New Zealand is the endemic Sarcodiotheca colensoi (Hook. & Harv.) Kylin. This study shows that it differs in several respects from the type S. furcata (Setch. & Gard.) Kylin; thus a new genus Placentophora is created for the New Zealand alga. Although P. colensoi nov. comb. is retained in the Solieriaceae on the basis of vegetative, spermatangial, tetrasporangial, carpogonial-branch and early gonimoblast features, it differs from typical members of that family in its pattern of later carposporophyte development. After a single gonimoblast initial is cut off from the auxiliary cell towards the center of the thallus, further gonimoblasts develop from the initial as ramifying, radiating filaments. These filaments enter an extensive “nutritive-cell” region surrounding the auxiliary cell, form, numerous connections to the “nutritive” cells, and incorporate most of them into a central placenta of interconnected, and variously-fused vegetative and gonimoblast cells. Carpo-sporangia then form in short chains around the periphery of the placenta. The cystocarp lacks both a central fusion cell and a sterile-celled investment, or “Faserhülle.” The distinctive carposporophyte of Placentophora is compared to patterns of gonimoblast development, known in other members of the Solieriaceae.     

REVISION OF THE MASTOPHOROIDEAE (CORALLINALES,RHODOPHYTA) AND POLYPHYLY IN NONGENICULATE SPECIES WIDELY DISTRIBUTED ON PACIFIC CORAL REEFS1

The subfamily Mastophoroideae (Corallinaceae, Rhodophyta) is characterized by species possessing nongeniculate, uniporate tetrasporangial conceptacles without apical plugs, the presence of cell fusions, and the absence of secondary pit connections. However, molecular phylogenetic studies not including the type genus Mastophora indicated that the Mastophoroideae was polyphyletic. Our molecular phylogenetic analysis of the subfamily including the type genus using DNA sequences of SSU rDNA and plastid‐encoded gene of PSII reaction center protein D1 (psbA) revealed that Mastophora formed a robust clade only with Metamastophora. The other mastophoroid genera were divided into six lineages within the family Corallinaceae. Five supported lineages—(i) Pneophyllum; (ii) Hydrolithon gardineri (Foslie) Verheij et Prud’homme, Hydrolithon onkodes (Heydr.) Penrose et Woelk., and Hydrolithon pachydermum (Foslie) J. C. Bailey, J. E. Gabel et Freshwater; (iii) Hydrolithon reinboldii (Weber Bosse et Foslie) Foslie; (iv) Spongites; and (v) Neogoniolithon—were clearly distinguished by the combination of characters including the presence or absence of palisade cells and trichocytes in large, tightly packed horizontal fields and features of tetrasporangial and spermatangial conceptacles. Therefore, we amend the Mastophoroideae to be limited to Mastophora and Metamastophora with a thin thallus with basal filaments comprised of palisade cells, tetrasporangial conceptacles formed by filaments peripheral to fertile areas, and spermatangia derived only from the floor of male conceptacles. This emendation supports Setchell’s (1943) original definition of the Mastophoroideae as having thin thalli. We also propose the establishment of three new subfamilies, Hydrolithoideae subfam. nov. including Hydrolithon, Porolithoideae subfam. nov. including the resurrected genus Porolithon, and Neogoniolithoideae subfam. nov. including Neogoniolithon. Taxonomic revisions of Pneophyllum and Spongites were not made because we did not examine their type species.     

ULTRASTRUCTURE AND CYTOCHEMISTRY OF EARLY SPERMATANGIAL DEVELOPMENT IN ANTITHAMNION NIPPONICUM (CERAMIACEAE,RHODOPHYTA)1

Spermatial development and differentiation of wall components were investigated by electron microscopy and cytochemical methods in Antithamnion nipponicum Yamada et Inagaki. The spermatium is composed of two parts, a globular head and two appendages projecting from near the basal portion. The appendages originate form spermatangial vesicles (SVs) and follow a developmental sequence beginning as amorphous material and ending as fully formed fibrous structures compressed with in the SVs. SV formation is due to contributions initially from endoplasmic reticulum and later form dictyosome-derived vesicles. Chemical differentiation of the spermatial wall occurs early in its development. Calcofluor white ST does not label spermatial walls, indicating an absence of cellulose polysaccharides, which are abundant in vegetative cell walls. Labeled lectins show that α-d -methyl manose and / or α-d -glucose as well as N-acetyl-glucosamine, β-d -galactose, and α-l -fucose moieties are present on the spermatial wall but not in the vegetative cell wall. The glyconjugate with α-d -methyl mannose and / or glucose residues, previously reported as a gamete recognition molecule in this species, is distributed along the surface of spermatia as well as in the SV during spermatangial development.     

Chemical relationship between red algae genus Laurencia and sea hare (Aplysia dactylomela Rang) in the North Borneo Island

Red algae genus Laurencia is an interesting alga with the ability to produce halogenated secondary metabolites that exhibits ecological and pharmaceutical potential. In nature, Laurencia is selectively grazed by sea hares (Aplysia dactylomela). In this study, Laurencia populations in three islands (Mantanani, Sulug, and Dinawan Islands) in the coastal waters of North Borneo were investigated and their chemical relationship with sea hare determined. Four species of Laurencia were found to grow abundantly in these waters, Laurencia snackeyi, Laurencia majuscula, Laurencia nangii, and Laurencia similis. Sea hares, Aplysia dactylomela, found grazing on Laurencia were collected and their chemical composition determined. A total of 20 halogenated metabolites were isolated and identified via spectroscopic data. Isolated compounds could be grouped into syndrean (5), chamigrane (6), non-chamigrane sesquiterpene (3), cuparane (1), bromoindole (2), and C15 acetogenin (acetylene type) (3). Sea hares from Mantanani, Sulug, and Dinawan Islands contained a total of 9, 10, and 10 compounds, respectively. In addition, 12-acetoxypalisadin B (1), which was isolated from sea hares of Sulug Island is a first record of its existence in nature.