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.     

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.     

Dasya enomotoi sp. nov. (Dasyaceae,Ceramiales), a new large Dasya from Japan

A new red alga, Dasya enomotoi, is described from Japan. This species is characterized by having a large thallus consisting of an elongated axis and many, radially arranged, polysiphonous branches both of which are heavily corticated and densely covered with numerous, soft monosiphonous filaments. It is distinguished from several similar species by the combination of the following: (i) indistinct pericentral cells in transverse sections except near the apices, (ii) the presence of enlarged, inner cortical cells, (iii) radially arranged adventitious monosiphonous filaments, (iv) three‐celled carpogonial branches, (v) six (sometimes five) tetrasporangia in each fertile segment of the stichidia, and (vi) three tetrasporangial cover cells that are not elongated longitudinally and usually not divided transversely. This species may have been identified as D. villosa Harvey by previous investigators in Japan.     

Phylogenetic Re-Evaluation of the Laurencia Complex (Rhodophyta) with a Description of L. Succulenta Sp. Nov. from Korea

Laurencia succulenta sp. nov. (Rhodophyta) is described from Korea. This species exhibits vegetative and reproductive structures typical of the genus, but is distinct from similar species in its epiphytic habitat and the fleshy, robust, thick and subcompressed thalli with basically distichous branching. In addition, it is readily distinguished from the most similar species, such as L. nipponica Yamada and L. okamurae Yamada, by the cystocarps with a somewhat protuberant ostiole. In a phylogenetic analysis of 47 species of the Laurencia Lamouroux complex from various localities around the world based on 49 morphological characters, four major clades (Laurencia, Chondrophycus palisadus (Yamada) Nam group, C. cartilagineus (Yamada) Garbary et Harper group and Osmundea Stackhouse assemblage), each of which forms a monophyletic group, were recognized. Among these, the Laurencia clade is basal to the overall assemblage, and is defined by the vegetative axis with four rather than two pericentral cells. The Osmundea clade is supported by autapomorphic characters for the genus, features associated with spermatangial formation of the filament type and tetrasporangial production from epidermal cells. By contrast, Chondrophycus, a genus characterized by a combination of features (vegetative axis with two pericentral cells, trichoblast-type spermatangial development and tetrasporangial production from pericentral cells), is paraphyletic, and the species were separated into two well-supported clades, the C. palisadus group and C. cartilagineus group. These clades are distinguished from each other by the position of the first pericentral cell relative to the trichoblast, the presence or absence of fertility at the second pericentral cells and number of sterile pericentral cells in the tetrasporangial axis, the pattern of formation of spermatangial branches on trichoblasts, post-fertilization feature associated with the formation time of the auxiliary cell, and, probably, the number of pericentral cells in the procarp-bearing segment. Of these features, the side position of the first pericentral cell in the latter group (a synapomorphy for the C. cartilagineus group plus Osmundea) suggests that the C. cartilagineus group is more closely related to Osmundea than to the C. palisadus group. This cladistic analysis indicates that Chondrophycus is not monophyletic, suggesting that the C. palisadus group should be separated from Chondrophycus at the genus level. Based on this result, Palisada (Yamada) stat. nov. is proposed for the group, together with an emendation of the generic delineation of Chondrophycus, and relevant nomenclatural changes for several Chondrophycus species are also included. In addition, Corynecladia J. Agardh is reinstated for the type species L. clavata Sonder.     

Melanothamnus maniticola sp. nov. (Ceramiales,Rhodophyta): an epizoic species evolved for living on the West Indian Manatee

Over 35 macroalgae have been documented growing epizoically on sea turtles, and macroalgae are also known to grow on the West Indian Manatee, but the number and identity of these latter species have not been determined. Analysis of DNA sequences of 12 samples collected from different manatees captured in three areas of Florida indicated that they represented a single undescribed species within the Rhodomelaceae genus Melanothamnus. Morphological analysis revealed Melanothamnus characteristics but also a previously undescribed combination of character states. These include eight to nine, but as many as 11, pericentral cells; heavy cortication restricted to the base of thalli, and a sharp transition between the corticated and ecorticate sections of the thallus; cells surrounding the ostiole being similar in size to the outer pericarp cells immediately below, and robust rhizoids that have no terminal lobes and develop from central axial cell filaments instead of pericentral cells. The unique characteristics of the rhizoids may be evolutionary adaptations for anchoring the thalli to manatee epidermis. This species is described as M. maniticola sp. nov.     

The anatomy of Neotenophycus ichthyosteus gen. et sp. nov. (Rhodomelaceae,Ceramiales), a bizarre red algal parasite from the central Pacific

A minute parasite of Neosiphonia poko (Hollenberg) Abbott from a shallow lagoon on the central-Pacific Johnston Atoll is described as Neotenophycus ichthyosteus Kraft et Abbott, gen. et sp. nov. The infective parasite cell first connects to a central-axial cell of the host, then emerges from between host pericentral cells at a node before dividing into a three- or four-celled primary axis. Epibasal cells of the parasite divide to form three pericentral cells whose derivatives produce a globular head on the basal cell and on which reproductive structures differentiate almost immediately. Trichoblasts on any life-history stage are completely lacking. Spermatangia are borne on mother cells across the whole thallus surface. Procarps consist of four pericentral cells that encircle a subapical fertile-axial cell in an ampullar configuration, one of the pericentral cells serving as the supporting cell and bearing a four-celled carpogonial branch and a single sterile cell. Diploidization results in a longitudinal/concave division of the auxiliary cell and formation of an arching linear series of inner gonimoblast cells, each dividing toward the thallus surface into gonimoblast filaments of very narrow, horizontally aligned cells terminated by initially monopodial, later by sympodial, carposporangia, the whole of the mature female gametophyte consisting of an amalgam of several cystocarps within a lax jacket of sterile gametophytic tissue. Tetrasporophytes are composed of lobes of pericentral-cell-derived filaments, each axial cell of which is ringed by three pericentral cells producing tetrahedral tetrasporangia enclosed by two pre-sporangial cover cells. Affinities of the new genus are discussed and comparison is made particularly to the enigmatic parasite Episporium centroceratis Möbius. It is concluded that relationships with any previously described tribe are so remote or obscure that the new tribe Neotenophyceae should be proposed for it.     

A new species of Laurencia, L. omaezakiana (Ceramiales, Rhodophyta), from Japan

Laurencia omaezakiana Masuda, sp. nov. (Ceramiales, Rhodophyta) is described from Japan. It is characterized by the following set of features: (i) the production of four periaxial cells from each vegetative axial cell; (ii) a shift in branching from distichous to spiral; (iii) the presence of projecting superficial cortical cells near the apices of branches; (iv) the presence of longitudinally oriented secondary pit-connections between contiguous superficial cortical cells; (v) the presence of lenticular thickenings in the walls of medullary cells; (vi) the occurrence of 1–2 corps en cerise in each superficial cortical cell and a single corps en cerise in each trichoblast cell; and (vii) a parallel arrangement of tetrasporangia. Furthermore, it produces a characteristic triterpenoid (enshuol), which has not been detected in other species of Laurencia, as a major halogenated secondary metabolite. A synoptical key to the 23 species of Laurencia growing in Japan is given. Laurencia ceytanica J, Agardh and Laurencia heteroclada Harvey are excluded from the Japanese marine algalflora. The latter is a distinct species from Laurencia filiformis (C. Agardh) Montagne.     

Research note: First report of Sporolithon ptychoides (Sporolithales,Corallinophycidae, Rhodophyta) for the Atlantic Ocean

Samples corresponding to Sporolithon ptychoides Heydrich were collected in the mesophotic zone (50 m depth) south of Espírito Santo State, Brazil. The collected material presented features characteristic of the species, namely: tetrasporangia of 75–105 × 40–55 µm grouped into sori that are raised above the surrounding vegetative thallus surface; presence of a basal layer of elongate cells in areas where the tetrasporangia develop; presence of buried tetrasporangial compartments deep in the thallus; and 3–5 cells in the tetrasporangial paraphyses. These same features said to collectively characterize S. ptychoides, were all observed in a representative specimen and the type specimen of Sporolithon dimotum (Foslie & Howe) Yamaguishi‐Tomita ex M.J Wynne. This latter species is thus conspecific with S. ptychoides and is therefore considered a heterotypic synonym thereof, as S. ptychoides has nomenclatural priority. This study expands the known geographical distribution of the species and may give insight into the origin of the species into other geographical regions.     

THERMAL ECOPHYSIOLOGY OF LAURENCIA PACIFICA AND LAURENCIA NIDIFICA (CERAMIALES,RHODOPHYTA) FROM TROPICAL AND WARM‐TEMPERATE REGIONS1

Laurencia is a globally distributed genus with about 80 species (order Ceramiales) that inhabit tropical, subtropical, and warm‐temperate regions of both sides of the Atlantic and Indo‐Pacific oceans. This study investigated how two species of Laurencia distributed in different thermal environments (California and Hawaii) varied in their photosynthetic responses to temperature. The thermal ecophysiology of both species was investigated at different temporal scales (short‐term responses and seasonal acclimatization) using oxygen evolution and pulse‐amplitude‐modulated (PAM) fluorometry. Our results indicated that seasonal acclimatization of both species of Laurencia influenced the short‐term photosynthetic response at both locations. Greater seasonal differences in the photosynthetic performance were observed for L. pacifica Kylin, which reflects the ability of this species to acclimatize to local environmental conditions characterized by short‐term fluctuations and a broader annual temperature range. Photosynthetic performance of L. nidifica J. Agardh was consistent with the less variable local environment (no short‐term fluctuations and a narrower temperature range). These results suggest that acclimatization to temperature variability in the environment can influence the degree of flexibility of physiological responses of species in this genus.     

Ochtodes searlesii sp. nov. (Gigartinales,Rhodophyta), from the Pacific tropical coast of Mexico,based on morphological and molecular evidence

Ochtodes searlesii Mendoza‐González, Mateo‐Cid et Sentíes sp. nov. is described from Michoacán, tropical Mexican Pacific, on the basis of comparative morphology and rbcL sequence analysis. It is distinguished from other Ochtodes species by its erect axes arising from an encrusting base, its small terete fronds, regularly dichotomously branched axes, and obliquely divided zonate tetrasporangia. Phylogenetic analyses showed that three Pacific Mexican samples, from Caletilla, Zapote and La Majahuita (Michoacán), were identical and formed a distinctive and well supported Clade segregated from other species of Ochtodes from Brazil, Cuba, Ecuador, Guadeloupe and Mexico. The Mexican entity is morphologically distinct from other Ochtodes species as well. On this basis we propose a new Ochtodes species.     

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.     

DICROGLOSSUM CRISPATULUM GEN. ET COMB. NOV. FROM WESTERN AUSTRALIA,REPRESENTING A NEW TRIBE WITHIN THE DELESSERIACEAE (RHODOPHYTA)1

Dicroglossum gen. nov. (Delesseriaceae, Ceramiales) is a monotypic genus based on Delesseria crispatula, a species originally described by Harvey for plants collected from southwestern Western Australia. Distinctive features of the new genus include exogenous indeterminate branches; growth by means of a single transversely dividing, apical cell; absence of intercalary divisions in the primary, secondary, and tertiary cell rows; lateral pericentral cells not transversely divided; not all cells of the secondary cell rows producing tertiary cells rows; all tertiary initials reaching the thallus margin; midrib present but lateral nerves absent; determinate lateral bladelets arising endogenously; blades monostromatic, except, at the midrib; carpogonial branches restricted to primary cell rows, on both surfaces of unmodified blades; procarps produced on both blade surfaces, each procarp consisting of a supporting cell that bears two four-celled carpogonial branches and one sterile-cell group of three to four cells; and tetrasporangia borne in two layers, separated by a central row of sterile cells. The combination of exogenous indeterminate branching and bicarpogonial procarps is considered to warrant the recognition of a new tribe, the Dicroglosseae, within the subfamily Delesserioideae.     

Species diversity of the genus Osmundea (Ceramiales,Rhodophyta) in the Macaronesian region

Species diversity within the genus Osmundea in the Macaronesian region was explored by conducting a comprehensive sampling in the Azores, the Canary, and the Madeira archipelagos. Toward identification, all specimens were first observed alive to verify the absence of corps en cerise, a diagnostic character for the genus and morphometric data were measured (thallus length and width, first‐order branches length and width, branchlets length and width, cortical cell length and width in surface view, cortical cell length and width in transverse section). Specimens were sequenced for COI‐5P (39 specimens) and three species delimitation methods (Generalized Mixed Yule Coalescent, Automatic Barcode Gap Discovery method, and Poisson Tree Processes) were used to assess the threshold between infra‐ and interspecific relationships. Subsequently, one or several sequences of plastid‐encoded large subunit of RuBisCO (21 specimens) per delimited species were generated to assess the phylogenetic relationships among Macaronesian Osmundea. Moreover, for each delineated species, vegetative and reproductive anatomy was thoroughly documented and, when possible, specimens were either assigned to existing taxa or described as novel species. This integrative approach has provided data for (i) the presence of O. oederi, O. pinnatifida, and O. truncata in Macaronesia; (ii) the proposal of two novel species, O. prudhommevanreinei sp. nov. and O. silvae sp. nov.; and (iii) evidence of an additional species referred as “Osmundea sp.1,” which is a sister taxon of O. hybrida.     

Discrimination and Characterization of Two Mediterranean Species from the Laurencia Complex (Rhodomelacea) Using an NMR‐Based Metabolomic Approach

Generic and specific determination among the Laurencia complex is a challenging task. DNA barcoding combined with phenotypic investigations are mandatory for species differentiation. In this study, two morphologically different members of the Laurencia complex were investigated using untargeted ¹H‐NMR‐based metabolomics. Twenty‐one population samples were collected in order to evaluate both temporal and geographical homogeneity. Data obtained from ¹H‐NMR analysis followed by statistical analysis allowed a clear separation of all the samples into two groups. DNA mitochondrial tests confirmed this pattern and identified the two species as Laurenciella sp. and Laurencia obtusa. In addition, metabolites responsible of this discrimination were investigated directly in crude extracts by ¹³C‐NMR using an in‐house computer‐assisted method. The combination of both untargeted (¹H) and targeted (¹³C) NMR‐based metabolomic approaches proves to be a powerful and complementary approach to discriminate species from the Laurencia complex.     

The reproductive structures of the Mediterranean alga Laurencia pelagosae (Ceramiales,Rhodophyta)

Reproductive structures of Laurencia pelagosae are described for the first time. Tetrasporangia, in parallel arrangement, are cut off from the mother cells adaxially; antheridial branches, which are unramified, are inserted in depressions lacking a row of axial cells on their bases; cystocarps are sessile and subspherical. The occurrence of secondary pit-connections between epidermal cells and of lenticular thickenings in the walls of medullary cells is documented. The species is included in the new section Pelagosae within the subgenus Laurencia.