The diagnostic value of reproductive organs in some genera of articulated Coralline red algae

Clearcut differences exist between the reproductive organs of Corallina and Jania. Fully formed spermatangial conceptacles in Corallina have low ceillings and pronounced beaks whereas in Jania they have high ceilings and lack beaks. Fusion cells in carposporophytic conceptacles are thin and broad in the former genus and thick and narrow in the latter. Tetrasporangial conceptacles have less capacity in Jania than in Corallina and the fertile areas in young conceptacles cover a smaller area.

Haliptylon is changed from group to generic status and Corallina subulata is transferred to this genus. Haliptylon is characterised by conceptacles similar in all known respects to those of Jania, but the branching is pinnate, as in Corallina.

From the available evidence it appears possible that organisms having Corallina-type conceptacles diverged phylogenetically long ago from those having Jania-type conceptacles.     

REPRODUCTION AND LIFE HISTORY OF THE RED ALGA GALAXAURA OBLONGATA (NEMALIALES,GALAXAURACEAE)1

Culture and morphological studies showed that Galaxaura oblongata (Ellis et Solander) Lamouroux has a triphasic life history with conspicuous gametophytes and small filamentous tetrasporophytes. Development of male and female reproductive structures is very similar and both begin with the enlargement of a terminal cell of a filament branch occupying a normal vegetative position within the apical pit of a thallus branch. In male thalli this modified branch forms a conceptacle in which spermatangia are produced. In female thalli, this modified branch forms a three-celled carpogonial branch consisting of a carpogonium, hypogynous cell and basal cell. Filament branches from the basal cell form a pericarp and the gonimoblast develops directly from the carpogonium. Carposporangia are produced in conceptacles which resemble the male conceptacles. About the time the first carposporangia are produced, the carpogonium, hypogynous cell and basal cell form a large fusion cell. Released carpospores germinate in a unipolar or bipolar manner and form small filamentous thalli. Under short day conditions, cruciate tetrasporangia are produced in small clusters. Tetraspores germinate similarly to carpospores and also form small filamentous thalli. Under low nutrient conditions, small cylindrical thalli develop on the filaments and these appear similar to gametophytes collected in nature.     

Photoperiodic regulation of receptacle induction in Sargassum horneri (Phaeophyceae) using clonal thalli

We developed a clonal culture of Sargassum horneri to investigate the effect of photoperiod on reproduction in this species. Regenerated vegetative thalli were obtained using lateral branches excised from a thallus grown from a single embryo under short‐day conditions (SD = 10:14 h light : dark cycle). Lateral branches excised from the SD‐regenerated thallus became vegetative thalli that remained in that phase as long as they were cultured under SD. When an excised lateral branch was cultured under long‐day conditions (LD = 14:10 h light : dark cycle), it began to enter the reproductive phase while still less than 50 mm long. Induction of the reproductive phase was accompanied by a distinctive morphological change – suppression of blade formation at the apical region of the branch; elongation of branches without blades was then followed by differentiation of receptacles bearing conceptacles on their surface. Apices of receptacles were able to interconvert between reproductive and vegetative phases, as blades resprouted upon transfer from LD to SD. The critical day length for induction of receptacle formation was between 13 and 14 h; receptacle formation was also induced under SD conditions with night breaks (NBs). These results strongly suggest that reproductive regulation of S. horneri is a photoperiodic long‐day response. NBs with blue and green light were effective for reproductive induction but not with red light. This suggests that blue‐ and/or green‐light photoreceptors are involved in the photoperiodic reproductive response of S. horneri.     

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.     

Aragonite infill in overgrown conceptacles of coralline Lithothamnion spp. (Hapalidiaceae,Hapalidiales, Rhodophyta): new insights in biomineralization and phylomineralogy

New empirical and quantitative data in the study of calcium carbonate biomineralization and an expanded coralline psbA framework for phylomineralogy are provided for crustose coralline red algae. Scanning electron microscopy (SEM) and energy dispersive spectrometry (SEM‐EDS) pinpointed the exact location of calcium carbonate crystals within overgrown reproductive conceptacles in rhodolith‐forming Lithothamnion species from the Gulf of Mexico and Pacific Panama. SEM‐EDS and X‐ray diffraction (XRD) analysis confirmed the elemental composition of these calcium carbonate crystals to be aragonite. After spore release, reproductive conceptacles apparently became overgrown by new vegetative growth, a strategy that may aid in sealing the empty conceptacle chamber, hence influencing the chemistry of the microenvironment and in turn promoting aragonite crystal growth. The possible relevance of various types of calcium carbonate polymorphs present in the complex internal structure and skeleton of crustose corallines is discussed. This is the first study to link SEM, SEM‐EDS, XRD, Microtomography and X‐ray microscopy data of aragonite infill in coralline algae with phylomineralogy. The study contributes to the growing body of literature characterizing and speculating about how the relative abundances of carbonate biominerals in corallines may vary in response to changes in atmospheric pCO₂, ocean acidification, and global warming.     

Leptophytum flavescens comb. nov. (Corallinales,Rhodophyta), an Arctic endemic from the sublittoral of NW Spitsbergen,North Norway,and western Novaya Zemlya,with epitypification of L. laeve

Type material of Lithothamnion flavescens Kjellman, originally described from Karlsøy (Troms) and Karmakul Bay (Novaya Zemlya), is re-examined and a lectotype is selected. Type specimens and other collections from NW Spitsbergen and North Norway possess distinctive characters of the genus Leptophytum, including the development of flattened epithallial cells, short subepithallial cells, and simple spermatangial structures. Leptophytum flavescens (Kjellman) comb. nov. resembles the generitype Leptophytum laeve, differing in having: (1) a thicker perithallium, to 900?µm (vs. 350?µm in L. laeve), that embeds older conceptacles, and (2) non-differentiated (in size or shape) pore cells of multiporate roofs. An epitype for L. laeve is also selected, which consolidates the status of this species and the genus, in agreement with the current literature and all publications prior to 1996.     

Pycnidial development ofPhyllosticta harai andSphaeropsis sp.

The development of conidiomatal structures is divided into three stages: primordia, cavity formation, and conidiogenesis. These ontogenetic features of conidiomata indicate diversity. This study clearly shows the difference in pycnidial development betweenPhyllosticta harai and a species ofSphaeropsis. InP. harai, a cavity is formed at the center of the pycnidium following the meristogenous or symphogenous primordium formation. This process is characterized by autolysis of cells at the pycnidium center. The pycnidial primordium ofSphaeropsis sp. is meristogenous. It can be assumed that the cavity is formed by dispersion and spacing of original hypha, with subsequent hypha filling the spaces between hyphal cells. The cavity enlarges gradually due to the mechanical force caused by successive conidium production and increasing conidial size.     

Lithophyllum cuneatum sp. nov. (Corallinaceae, Rhodophyta), a new species of non-geniculate coralline alga semi-endophytic in Hydrolithon onkodes and Neogoniolithon sp. from Fiji, South Pacific

A new species of semi-endophytic coralline alga, Lithophyllum cuneatum (Corallinaceae: Lithophylloideae), is described from Fiji. The species is characterized by a wedge-like thallus that is partially buried in the thallus of the host coralline, Hydrolithon onkodes (Heydrich) Penrose et Woelkerling or occasionally Neogoniolithon sp., and that appears at the surface of the host as a small pustule that is usually paler in color than the host. The thallus consists of erect filaments that are derived from a single cell. The basal cell, when visible, is non-palisade, and areas of bistratose margin are absent. Cells of contiguous erect filaments are joined by secondary pit connections. Epithallial cells are present in 2–3 layers, and individual trichocytes are common. Gametangial plants are dioecious. Male conceptacles have simple spermatangial systems that are confined to the floors of their elliptical chambers. Carposporangial conceptacles contain 5–8 celled gonimoblast filaments that are borne at the margin of a more-or-less discoid fusion cell, and so occupy the periphery of the elliptical conceptacle chambers. Tetrasporangial conceptacles are uniporate, with roofs formed from peripheral filaments, and chambers lack a central columella of sterile filaments. Despite its semi-endophytic nature, haustorial cells are absent, and plastids and pigmentation are present.     

Algal affinity and possible life cycle of the early Cambrian acritarch Yurtusia uniformis from South China

Abundant, well-preserved specimens of spheroidal organic-walled microfossil Yurtusia uniformis are reported from the basal Cambrian Yanjiahe Formation in the Changyang area of Hubei Province, South China. Thin and hollow processes extend between the double walls of the vesicle. The single to multiple internal bodies within the vesicle cavity are observed in the genus for the first time, representing reproductive structures (dividing daughter cells). A small circular perforation may occur on the vesicle wall to release the internal bodies. Morphological analyses of specimens preserved at various life stages reveal that processes gradually became longer as the vesicle grew in size. The internal bodies (daughter cells) underwent several successive divisions within the vesicle, which was accompanied by the simultaneous growth of both vesicle and processes. The regular growth of cells, formation and release of daughter cells, and the remarkable morphological similarity between extant algae and the studied microfossils suggest that Yurtusia uniformis is probably a green microalga that may be closely related to the Trebouxiophyceae or even Chlorellales (Chlorophyta). The growth and reproductive mode of individuals indicates that Y. uniformis is an actively growing vegetative cell of microalgae, rather than a metabolically inert cyst or resting spore. A life cycle involving vegetative growth and asexual reproduction is proposed for Y. uniformis on the basis of the life histories of modern chlorophytes. The multiple internal cells may represent autospores produced by a mature autosporangium during asexual reproduction, which subsequently developed into separate young vegetative cells after their release from the opened autosporangium.     

A taxonomic reassessment of Spongites (Corallinaceae,Rhodophyta) based on studies of Kützing's original collections

Results from critical studies of the original collections upon which Spongites Kützing, 1841 is based have led to the designation of S. fruticulosa as lectotype species and to the resurrection and recognition of Spongites as a distinct genus of Corallinaceae (Rhodophyta). Spongites is characterized by the absence of geniculae, uniporate tetrasporangial conceptacles, a multistratose non-palisade and non-coaxial medulla (“hypothallium”) and cortex (“perithallium”), fusions between cells of adjacent filaments, and trichocytes which are solitary or arranged in a vertical series. Since at least 1883, the Kützing epithet “fruticulosa” has been misapplied widely to a taxon with multiporate tetrasporangial conceptacles, whereas the type collection of S. fruticulosa possesses uniporate tetrasporangial conceptacles. Of the six original species, three (S. fruticulosa, S. racemosa, S. stalactitica) are retained in Spongites; S. dentata is referred to Lithophyllum and S. nodosa to Lithothamnion as distinct species; and S. confluens is regarded to be conspecific with Lithophyllum incrustans Philippi. Detailed morphogological-anatomical accounts of specimens in the type collections are presented along with relevant historical data on the genus and on the various species studied. The relationships of Spongites to Neogoniolithon and to other genera of Corallinaceae also are discussed.     

Late Hauterivian coralline algae (Rhodophyta,Corallinales) from the Iberian Chain (E Spain). Taxonomy and the evolution of multisporangial reproductive structures

Upper Hauterivian reefal carbonates of the Llàcova Formation (Maestrat Basin, Iberian Chain, E Spain) contain Sporolithon phylloideum (Bucur and Dragastan) Tomás, Aguirre, Braga and Martín-Closas comb. nov. and Sporolithon rude (Lemoine) Ghosh and Maithy (1996). Moussavian et al. (1993) identified them as Parakymalithon phylloideum (Bucur and Dragastan) Moussavian 1987 and Archaeolithothamnium rude Lemoine 1925. The re-assessment of the type of P. phylloideum and additional material indicate that the diagnostic characters of the genus do not warrant separation from Sporolithon and the new combination Sporolithon phylloideum is proposed. The lectotype of Sporolithon rude presents sporangial cavities grouped in sori that can be merged originating a structure that resembles the multiporate tetrasporangial conceptacles of the Hapalidiaceae. We hypothesize that multiporate tetrasporangial conceptacles could have originated from the fusion of several sporangial cavities, suggesting a phylogenetic linkage between Sporolithaceae and Hapalidiaceae supported by other anatomical features, molecular phylogeny and the fossil record.     

VEGETATIVE AND REPRODUCTIVE MORPHOLOGY OF EUCHEUMA ISIFORME (SOLIERIACEAE,GIGARTINALES, RHODOPHYTA)1

Eucheuma isiforme (C. Agardh) J. Agardh exhibits a combination of vegetative and reproductive features that distinguish it from other critically studied genera in the Solieriaceae. The development of the multiaxial thallus, emphasizing the arrangement of periaxial cells around each axial file; presence of reproductive nemathecia that contain carpogonial branches and auxiliary cells; and post-diploidization stages, including gonimoblast and pericarp initiation, stages of fusion cell formation, and carposporophyte development are described and illustrated for the first time in this species. The vegetative and reproductive features observed in E. isiforme are not diagnostic of any of the recently erected tribes in the Solieriaceae. Eucheuma appears most closely related to the Indian Ocean genus, Sarconema.     

MESOPHYLLUM SPHAERICUM SP. NOV. (CORALLINALES,RHODOPHYTA): A NEW MAËRL‐FORMING SPECIES FROM THE NORTHEAST ATLANTIC1

Mesophyllum sphaericum sp. nov. is described based on spherical maërl individuals (up to 10 cm) collected in a shallow subtidal maërl bed in Galicia (NW Spain). The thalli of these specimens are radially organized, composed of arching tiers of compact medullary filaments. Epithallial cells have flattened to rounded outermost walls, and they occur in a single layer. Subepithallial initials are as long as, or longer than the daughter cells that subtend them. Cell fusions are abundant. Multiporate asexual conceptacles are protruding, mound‐like with a flattened pore plate, lacking a peripheral raised rim. Filaments lining the pore canal and the conceptacle roof are composed of five to six cells with straight elongate and narrow cells at their base. Carposporangial conceptacles are uniporate, protruding, and conical. Spermatangial conceptacles were not observed. Molecular results placed M. sphaericum near to M. erubescens, but M. sphaericum is anatomically close to M. canariense. The examination of the holotype and herbarium specimens of M. canariense indicated that both species have pore canal filaments with elongate basal cells, but they differ in number of cells (five to six in M. sphaericum vs. four in M. canariense). Based on the character of pore canal filaments, M. canariense shows similarities with M. erubescens (three to five celled). The outermost walls of epithallial cells of M. canariense are flared compared to the round to flattened ones of M. erubescens, the latter being widely accepted for the genus Mesophyllum. The addition of M. sphaericum as new maërl‐forming species suggests that European maërl beds are more biodiverse than previously understood.     

Lectotypifícation of Lithophyllum arcticum (Corallinales, Rhodophyta) and a study of its relationships within the Melobesioideae

Three separate collections of the type material of Kjellman's Lithophyllum arcticum are re‐examined and a lectotype is selected. It is confirmed that the thallus is unattached, at least 4.5 cm in diameter, composed of up to eight superimposed more or less discoidal lamellae, provided with concentric striations on the surface. Individual lamellae are usually 100 to 200 μm thick (reaching 1 mm), developing dorsally from the main thallus and expanding centrifugally. The internal organization is dorsiventral with a polystromatic hypothallium, giving rise to an ascending perithallium with small subepithallial initials and rectangular (in TS) epithallial cells. It is found that patches of coaxial‐like growth occur sporadically in the hypothallium and the perithallium, and that ventral lamellae may grow back‐to‐back. Somatic cells exhibit both large and narrow cell fusions. Pore plates of the raised multiporate conceptacles are slightly sunken to flattened and perforated by 16 to 31 pores. Pore canals are conical (narrowing towards the top) and are bordered by filaments composed of both undifferentiated and slender‐elongate cells. Old conceptacles are overgrown by vegetative filaments and empty chambers are embedded in the perithallium. Collectively these features indicate that L. arcticum belongs to the subfamily Melobesioideae. The development of an unattached‐superimposed thallus, patches of coaxial growth, short subepithallial initials and specialized pore cells suggest a position either in Mesophyllum, or in an amended Leptophytum to include even species with coaxial patches and unattached‐superimposed habit (characters presently segregating Leptophytum from Synarthrophytorn). The holotype of Lithophyllum zonatum from East‐Finnmark, previously considered to be related to L. arcticum, is re‐examined and shown to belong to a different species. A previous Arctic record of Mesophyllum lichenoides from Spitsbergen is abolished, and thus the disjunct distribution of I. arcticum in relation to Mesophyllum suggests a position in the Synarthrophyton‐Leptophytum complex which shows a bipolar to temperate distribution.     

Taxonomic circumscription of heterogeneous species Neogoniolithon brassica‐florida (Corallinales,Rhodophyta) in Japan

The nongeniculate species Neogoniolithon brassica‐florida (Harvey) Setchell et Mason is circumscribed as a polymorphic species with various gross morphologies due to it being synonymized with several previous species. However, small subunit rDNA and cox1 analyses showed that N. brassica‐florida was polyphyletic, and strongly imply that crustose species lacking any protuberances such as Neogoniolithon fosliei (Heydrich) Setchell et Mason and species with protuberances or branches such as N. brassica‐florida and N. frutescens (Foslie) Setchell et Mason should be treated as genetically different groups (species). Therefore, we propose the resurrection of N. frutescens. We also confirmed that N. trichotomum was distinguished from N. frutescens by slender uniform diameter branches, a conceptacle with a prominent ostiole, and large cox1 interspecific sequence differences. Male and female reproductive structures of N. trichotomum were illustrated for the first time. Neogoniolithon fosliei, was divided into three clades, each of which was recognized as a species complex based on interspecific level sequence differences within clade and morphological differences. Therefore, we treated the clade most similar to N. fosliei as N. fosliei complex (Clade B), and the other clades as respective complexes of N. cf. fosliei with yellow conceptacles (Clade A) or N. cf. fosliei with large conceptacles (Clade C). Of two species complexes (Clade A and B) were morphologically consistent with two entities of N. fosliei previously reported in the Ryukyu Islands, Japan, which is supported by their niche partitioning. DNA barcoding research of nongeniculate corallines can promote the finding of more reliable taxonomic characters and the understanding of their biological aspects.     

CONCEPTACLE STRUCTURE OF THE PARASITIC CORALLINE RED ALGA CHOREONEMA THURETII (CORALLINALES) AND ITS TAXONOMIC IMPLICATIONS1

The major diagnostic features for erecting the red algal subfamily Choreonematoideae (Corallinales) were a combination of 1) absence of both cell fusions and secondary pit connections, 2) conceptacle roof and wall comprised of a single cell layer, and 3) presence of tetrasporangial pore plugs within a uniporate conceptacle in the monotypic taxon Choreonema thuretii (Bornet) Schmitz. Because this alga is a parasite, the absence of secondary cell connections is most likely an adaptation to a reduced thallus. This study shows that all conceptacles are not composed of a file of cells but rather a single layer of epithallial cells that are underlain by a thick layer of calcified acellular material; both epithallial cells and the calcified layer are produced by peripheral sterile cells. Although the outermost tetrasporangial pore canal is uniporate, there is a calcified acellular multiporate plate recessed just below the rim. The plate is produced by interspersed sterile cells and is continuous with the calcified layer supporting the conceptacle. These unique structures are likely due to parasitism rather than to the ancestral state. Based on these results and a reexamination of published micrographs depicting lenticular cells in Austrolithon intumescens Harvey et Woelkerling, we propose that both subfamily Choreonematoideae and Austrolithoideae are closely allied with subfamily Melobesioideae. This distant relationship to its host (Corallinoideae) plus a combination of unique conceptacle and unusual type of parasitism indicates that C. thuretii is an alloparasite and that it is likely the most ancient red algal parasite studied to date.     

Studies on Metamastophora (Corallinaceae,Rhodophyta). I. M. flabellata (Sonder) Setchell: Morphology and anatomy

A morphological-anatomical study of Australian populations of Metamastophora flabellata (Sonder) Setchell, the type species of Metamastophora (Corallinaceae, Rhodophyta), has revealed that the primarily erect or ascending non-geniculate thallus possesses a dorsi-ventral organization of tissues. All conceptacles are uniporate and arise dorsally. Two distinct vegetative meristems occur: an apical primary meristem from which hypothallial cells are produced basipetally and a sub-epithallial secondary meristem which generates perithallial cells basipetally and secondary epithallial cells acropetally. Primary epithallial cells arise from divisions of subapical hypothallial cells. In younger parts, tissues are produced only dorsal to the hypothallium; in veins and stipes, tissue production occurs both dorsal and ventral to the hypothallium. Mature tetrasporic conceptacles contain peripheral tetrasporangia with zonately divided contents and a central sterile columella. Gametic conceptacles produce fertile tissue across the entire conceptacle chamber floor. After fertilization, the zygotic nucleus or a derivative is transferred (presumably) to an auxiliary cell through cells of the carpogonial branch; no tubular transfer siphon develops. Mature fusion cells are composed of the amalgamated supporting cells of carpogonial branches and are initiated from a single supporting cell which functions as an auxiliary cell. Unbranched 3–4 celled gonimoblast filaments arise from the fusion cell, do not become connected to other cells, and produce terminal carposporangia. Results from this study have led to a redefinition of hypothallium and perithallium in relation to meristems rather than substrate. In addition, carposporophyte ontogeny in the Corallinaceae is considered in terms of the presumed mode of transfer of the zygotic nucleus to the fusion cell, the extent of fusion cell development, and gonimoblast filament production in relation to auxiliary cells and fusion cells.