Phylogenetic relationships of corallinaceae (Corallinales,Rhodophyta): taxonomic implications for reef‐building corallines

A new, more complete, five‐marker (SSU, LSU, psbA, COI, 23S) molecular phylogeny of the family Corallinaceae, order Corallinales, shows a paraphyletic grouping of seven well‐supported monophyletic clades. The taxonomic implications included the amendment of two subfamilies, Neogoniolithoideae and Metagoniolithoideae, and the rejection of Porolithoideae as an independent subfamily. Metagoniolithoideae contained Harveylithon gen. nov., with H. rupestre comb. nov. as the generitype, and H. canariense stat. nov., H. munitum comb. nov., and H. samoënse comb. nov. Spongites and Pneophyllum belonged to separate clades. The subfamily Neogoniolithoideae included the generitype of Spongites, S. fruticulosus, for which an epitype was designated. Pneophyllum requires reassesment. The generitype of Hydrolithon, H. reinboldii, was a younger heterotypic synonym of H. boergesenii. The evolutionary novelty of the subfamilies Hydrolithoideae, Metagoniolithoideae, and Lithophylloideae was the development of tetra/bisporangial conceptacle roofs by filaments surrounding and interspersed among the sporangial initials.     

Phylogenetic analysis of rhodolith formation in the Corallinales (Rhodophyta)

Although the ecological importance of rhodolith (maerl, free-living coralline algae) beds is well-known, rhodolith-forming species have been neglected in molecular phylogenetic studies. This is the first molecular systematic study aimed at understanding whether the rhodolith habit is a fixed feature in lineages and determining the relationship (phylogenetic vs. environmental) between rhodolith and crustose habits. Phylogenetic relationships of rhodolith-forming species and encrusting coralline algae at generic and species levels were analysed using SSU rDNA and psbA sequences. Extensive sampling in the European North Atlantic, Pacific and Caribbean Mexico of Phymatolithon, Lithothamnion, Lithophyllum and Neogoniolithon taxa forming rhodoliths and crusts was accompanied by examination of type or topotype material. Phylogenetic reconstruction showed that Neogoniolithon contained a monophyletic group of rhodolith-forming species whereas other rhodolith-formers were closely related to encrusting forms in the genera Phymatolithon, Lithothamnion, Mesophyllum, Hydrolithon, Spongites and Sporolithon. DNA analysis showed that the crust-forming Lithophyllum cf. incrustans/dentatum also forms rhodoliths with a stone nucleus that occur on rocky shores. In contrast, species that form beds of non-nucleate rhodoliths (e.g. Neogoniolithon spectabile, N. strictum, Lithophyllum cf. incrustans/dentatum or sp. 1 and Phymatolithon calcareum) rarely form crusts. The rhodolith habit cannot be used to delimit species for taxonomic or identification purposes. Extensive taxonomic revision will be required to deal with problems such as the position of specimens identified as Lithophyllum margaritae in two unrelated lineages.     

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.     

Inventario delle Corallinales del Mar Mediterraneo: considerazioni tassonomiche

Abstract

Inventory of Corallinales of the Mediterranean Sea: taxonomic aspects. - The aim of the present work is the drawing up of a critical inventory of Corallinales of the Mediterranean Sea. This research has been based upon a census of 320 works published since 175 years, upon direct collections and sample exchanges. A census of 88 species of Corallinales (with forms and varieties), made up on the basis of about 5000 records, has been taken. 34 of the 88 species are considered “species dubiae aut rariter inventae”, it has been reported also “species inquirendae” and “species addendae”. From this census it results that there are some taxonomic problems about genera attributions (Lithophyllum, Pseudolithophyllum, Titanoderma, Neogoniolithon, Spongites, Goniolithion, Leptophytum), species attributions of articulated Corallinales (Corallina elongata, C. officinalis e Haliptilon squamatum) and non-articulated Corallinales (Fosliella ischitana, Lithophyllum (Titanoderma) trochanter, Spongites fruticulosus). Definition of these taxonomic attributions might condition not only studies of phytogeographical distribution of these algae but also every successive interpretation.     

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.     

Taxonomic and biostratigraphical re-assessments of Subterraniphyllum Elliott (Corallinales, Rhodophyta)

A taxonomic and biostratigraphical re‐assessment of Subterraniphyllum Elliott (Corallinales, Rhodophyta) is presented. Results from studies of the type collection and of newly collected material from north‐eastern Italy and northern Slovenia have shown that this taxon is not a geniculate coralline red alga as originally suggested by Elliott and most subsequent authors. Vegetatively, Subterraniphyllum most closely resembles certain living members of the Corallinales; however, the phenetic and phylogenetic relationships of Subterraniphyllum to other Corallinales cannot be determined with greater certainty. The exclusion of Subterraniphyllum from any group of Corallinaceae with genicula is based on unequivocal evidence that branch formation does not involve the occurrence of genicula. Subterraniphyllum seems to be restricted to the Oligocene. Reports of occurrences in Upper Eocene and Lower Miocene sediments cannot be substantiated. Subterraniphyllum, however, cannot be considered a useful stratigraphical marker until further data on its occurrence in well‐dated carbonate sequences are acquired. This study illustrates the problems associated with placing fossil coralline algal specimens into geniculate genera without the preservation of relevant morphological characters. This is especially true in the absence of the careful assessment of fossil material with respect to current taxonomic concepts of geniculate coralline genera, all of which are based on studies of living species. According to the current concepts for geniculate coralline genera, the placing of fossil specimens into geniculate genera without appropriate evidence must be avoided by grouping all potentially geniculate fragments under the informal group ‘Geniculate sensu lato’. Furthermore, for all those many fossil specimens where unequivocal evidence is not present, it is possible to utilize ‘form genera’ based on characters that are normally preserved. This leads to creating a consistent, workable system of applying names to most fossil corallines so that they can be reliably used in relation to stratigraphical and palaeoecological studies.     

RE-ASSESSMENT OF THE TYPE COLLECTIONS OF CORALLINALEAN GENERA (CORALLINALES, RHODOPHYTA) DESCRIBED BY V. P. MASLOV

Abstract:  From 1935 to 1962 Maslov published two monographs and several other papers on the taxonomy of fossil calcareous algae of diverse ages from the large geographical area of the former USSR. Among many other taxa, he described five new genera ( Solenophyllum , Palaeophyllum , Mesolithon , Bicorium and Tomilithon , as a subgenus of Parachaetetes Deninger) which he attributed to the Corallinaceae, and the new genus Karpathia , which he included in the Squamariaceae. Type material of these taxa, except for Mesolithon , is housed in the Geological Institute of the Russian Academy of Sciences, Moscow. Re-examination of the genus types from a modern perspective of coralline algal taxonomy shows that Karpathia is a validly published genus of corallinaceans (subfamily Mastophoroideae) to which several Cenozoic fossil species can be assigned. In contrast, the holotype of P. elegans , the type species of Palaeophyllum , cannot be assigned to any subfamily within the Corallinaceae and its preserved features are inadequate for confidently delimiting a separate genus. Solenophyllum is a valid genus in which Palaeozoic representatives of Corallinales formerly attributed to Parachaetetes Deninger can be included. Tomilithon is considered a younger heterotypic synonym of Solenophyllum . The algal nature of the bioclasts in the type of Bicorium is uncertain.     

The population and community structure of Hawaiian fringing-reef crustose Corallinaceae (Rhodophyta,Cryptonemiales)

Measurements of cover, relative density, and frequency are given for the major reefbuilders on the Waikiki fringing reef. Crustose coralline algae cover 39% of the reef surface and exceed all other organisms as the major builders and consolidators of reef materials. An unidentified coralline (melobesioid C) covers the greatest area (17 %), but Hydrollthon reinboldii (Weber-van Bosse & Foslie) Foslie (11 % cover) because of its thicker thalli and higher relative density (45 %) and frequency (68 %) values is the primary limestone former. Melobesioid C ranks second and Sporolithon erythraeum (Rothpletz) Kylin (6 % cover) third in relative importance. Porolithon onkodes (Heydrich) Foslie (3 % cover), although shown by its low density (4 %) and frequency (6 %) to have a comparatively restricted distribution, is more important than P. gardineri (Foslie) Foslie (2 % cover). P. onkodes maintains and provides the surf-resistant reef edge and is, therefore, of great ecological importance. Coelenterate corals cover less than 1 % of the total area and are relatively unimportant on the fringing reef. The hypothesis is developed that the high ratio (200 : 1) of crustose corallines to corals at Waikiki may be partly due to increases in eutrophication.Experimental evidence shows that P. onkodes can withstand intense illumination and is thereby unique among Hawaiian crustose Corallinaceae. Sporolithon erythraeum is more typical of other crustose corallines since it is physiologically adapted to low-light habitats.     

Evolutionary history of the Corallinales (Corallinophycidae, Rhodophyta) inferred from nuclear, plastidial and mitochondrial genomes

Systematics of the red algal order Corallinales has a long and convoluted history. In the present study, molecular approaches were used to assess the phylogenetic relationships based on the analyses of two datasets: a large dataset of SSU sequences including mainly sequences from GenBank; and a combined dataset including four molecular markers (two nuclear: SSU, LSU; one plastidial: psbA; and one mitochondrial: COI). Phylogenetic analyses of both datasets re-affirmed the monophyly of the Corallinales as well as the two families (Corallinaceae and Hapalidiaceae) currently recognized within the order. Three of the four subfamilies of the Corallinaceae (Corallinoideae, Lithophylloideae, Metagoniolithoideae) were also resolved as a monophyletic lineage whereas members of the Mastophoroideae were resolved as four distinct lineages. We therefore propose to restrict the Mastophoroideae to the genera Mastophora, Metamastophora, and possibly Lithoporella in the aim of rendering this subfamily monophyletic. In addition, our phylogenies resolved the genus Hydrolithon in two unrelated lineages, one containing the generitype Hydrolithon reinboldii and the second containing Hydrolithon onkodes, which used to be the generitype of the now defunct genus Porolithon. We therefore propose to resurrect the genus Porolithon for the second lineage encompassing those species with primarily monomerous thalli, and trichocyte arrangements in large pustulate horizontal rows. Moreover, our phylogenetic analyses revealed the presence of cryptic diversity in several taxa, shedding light on the need for further studies to better circumscribe species frontiers within the diverse order Corallinales, especially in the genera Mesophyllum and Neogoniolithon.     

Ordovician and Silurian coralline red algae

Solenopora gotlandica Rothpletz, hitherto placed in the Solenoporaceae Pia, is locally common in the mid-Silurian of Gotland and Wales. It possesses small cells, radial monomerous thallus organization, trichocytes, and sporangia arranged in irregular sori. Solenopora gotlandica is not congeneric with S. spongioides , the type species of Solenopora. It closely resembles the extant coralline red alga Sporolithon Heydrich. S. gotlandica is here transferred to Craticula gen. nov., and Craticula is placed in the Craticulaceae fam. nov., which morphologically closely resembles the Mesozoic-Cenozoic family Sporolithaceae. The Craticulaceae is placed in the extant rhodophyte order Corallinales. Middle-Late Ordovician Petrophyton kiaeri Høeg resembles Late Ordovician Solenopora richmondense Blackwell et al. , which has sporangia in calcified compartments arranged in sori. These fossils may be craticulaceans. The apparent gap in the fossil record between Silurian Craticula and Cretaceous Sporolithon favours separation of these genera at family level. However, future work may demonstrate that the Craticulaceae is a junior synonym of the Sporolithaceae. Recognition of the Craticulaceae extends the earliest record of the Corallinales from Cretaceous to Silurian, and possibly Ordovician.     

Crusticorallina gen. nov., a nongeniculate genus in the subfamily Corallinoideae (Corallinales,Rhodophyta)

Molecular phylogenetic analyses of 18S rDNA (SSU) gene sequences confirm the placement of Crusticorallina gen. nov. in Corallinoideae, the first nongeniculate genus in an otherwise geniculate subfamily. Crusticorallina is distinguished from all other coralline genera by the following suite of morpho‐anatomical characters: (i) sunken, uniporate gametangial and bi/tetrasporangial conceptacles, (ii) cells linked by cell fusions, not secondary pit connections, (iii) an epithallus of 1 or 2 cell layers, (iv) a hypothallus that occupies 50% or more of the total thallus thickness, (v) elongate meristematic cells, and (vi) trichocytes absent. Four species are recognized based on rbcL, psbA and COI‐5P sequences, C. painei sp. nov., the generitype, C. adhaerens sp. nov., C. nootkana sp. nov. and C. muricata comb. nov., previously known as Pseudolithophyllum muricatum. Type material of Lithophyllum muricatum, basionym of C. muricata, in TRH comprises at least two taxa, and therefore we accept the previously designated lectotype specimen in UC that we sequenced to confirm its identity. Crusticorallina species are very difficult to distinguish using morpho‐anatomical and/or habitat characters, although at specific sites, some species may be distinguished by a combination of morpho‐anatomy, habitat and biogeography. The Northeast Pacific now boasts six coralline endemic genera, far more than any other region of the world.     

Tracking paleoenvironmental changes in coralline algal-dominated carbonates of the Lower Oligocene Calcareniti di Castelgomberto formation (Monti Berici, Italy)

Lower Oligocene, shallow-water carbonates of the Calcareniti di Castelgomberto formation (Monti Berici, Italy, Southern Alps) are studied in detail with respect to fabric and component distributions in order to trace paleoecological changes along a monotonous sedimentary stacking pattern. The carbonates are dominated by coralline algal rudstones with a packstone to wackestone matrix. Non-geniculate coralline algae include six genera: Lithoporella melobesioides, Mesophyllum, Neogoniolithon, Spongites, Sporolithon, and Subterraniphyllum. The algae are found in the form of encrusting thalli, rhodoliths, and coralline debris. Non-algal components include larger, small benthic, and planktonic foraminifera associated with bryozoans, zooxanthellate corals, and echinoderms. Four carbonate facies are distinguished: (1) coralline algal facies, (2) coralline algal-coral facies, (3) coralline algal-larger foraminiferal facies, and (4) coralline algal debris facies. Marly horizons also occur in the section. The facies and coralline algal content are interpreted with respect to light intensity, hydrodynamic energy, biotic interactions, and substrate stability. Facies development along the studied section shows systematic variations, suggesting asymmetric sea-level changes with rapid regressions and gradual transgressions.     

Taxonomic biodiversity of geniculate coralline red algae (Corallinales,Rhodophyta) from the Macaronesian region: summary and analysis

A catalog and critical review of species and infraspecific taxa of non-fossil geniculate coralline red algae (Corallinales, Rhodophyta) previously reported from the Macaronesian region are presented along with an assessment of species diversity in the region. Published records of geniculate coralline algae are included along with comments relating to type material. Within the catalog, taxa are organized alphabetically by genus and within this by final epithet. From the 31 taxa recorded, 4 are based on type collections from Macaronesian localities. The types of most species and infraspecific taxa reported from the region have yet to be re-examined in a modern context, and most Macaronesian records require verification. The biodiversity of Macaronesian geniculate coralline algae may be lower than current information indicates.     

Japanese marine algae: New combinations, new names and new species

Several new species, combinations and names are described or proposed for the following species of algae reported from Japan: Gloiocladia japonica comb. nov. (=Gloioderma japonicum Okamura), Mazzaella hemisphaerica comb. nov. (=Rhodoglos-sum hemisphaericum Mikami), Melanamansia mitsuii comb. nov. (=Amansia mitsuii Segawa), Ptilo-cladia divaricata comb. nov. (=Crouania divaricata Okamura), Analipus gunjii comb. nov. (=Chordaria gunjii Yendo), Elachista okarnurae nom. nov. (=Elachista globosa Takamatsu), Gelidium inagakii nom. nov. (=Gelidium nanum Inagaki), Mastocarpus yendoisp. nov. (=Gigartina mamillosa sensu Yendo), Melobesia masakii nom. nov. (=Metobesia pacifica Masaki) and Porphyra yamadae sp. nov. (=Porphyra crispata sensu Okamura and Ueda).     

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.     

ANALYSIS OF ANCIENT DNA FROM FOSSIL CORALLINES (CORALLINALES,RHODOPHYTA)1

The field of molecular paleontology has recently made significant contributions to anthropology and biology. Hundreds of ancient DNA studies have been published, but none has targeted fossil coralline algae. Using regions of the SSU gene, we analyzed rDNA from fossil coralline algae of varying ages and states of preservation from Spain, Papua New Guinea (PNG), and the Great Barrier Reef (GBR). Specimens from PNG, GBR, and some localities from Spain did not contain endogenous ancient DNA. Reproducible sequence data were obtained from specimens ～550 years old from near Cadiz, Spain, and from rocky‐shore deposits in Carboneras, Almeria Province of Spain (～78,000 years before present [YBP]). Based on BLAST searches and a phylogenetic analysis of sequences, an undescribed coralline alga belonging to the Melobesioideae was discovered in the Carboneras material as well as the following coralline genera: Jania, Lithophyllum, Lithothamnion, Mesophyllum, and Phymatolithon. DNA from fleshy brown and red macroalgae was also discovered in the specimens from Carboneras. The coralline algae identified using molecular techniques were in agreement with those based on morphological methods. The identified taxa are common in the present‐day southeastern Spain littoral zone. Amino acid racemization, concentration ratios, and specific concentrations failed to show a correlation between biomolecular preservation and PCR amplification success. Results suggest that molecular investigations on fossil algae, although limited by technical difficulties, are feasible. Validity of our results was established using authentication criteria and a self‐critical approach to compliance.     

3-D distribution of nongeniculate corallinales: a case study from a reef crest of South Sinai (Red Sea,Egypt)

An innovative technique for the estimation of species and growth-form abundance of coralline algae, including information on their vitality, was adopted on the reef crest of Ras Nosrani and Coral Bay, South Sinai. Data of coralline abundance from visual census and collection of voucher specimens were plotted on a 3-D sketched representation of the horizontal and vertical planes of the reef crest and of its crannies. Coralline dominance at the two investigated sites was not significantly different, with values ranging from 8.55 and 10.06% on the vertical plane and from 5.3 to 7.17% on the horizontal plane. About one-third of total corallines of the South Sinai reef crest was located in crannies, where the algae are completely overlooked by routine field surveys. Pink to violet, healthy corallines with encrusting growth-form, mainly belonging to Hydrolithon onkodes and Neogoniolithon, with subordinate fruticose Lithophyllum kotschyanum dominated the reef crest at both sites. The fruticose growth form, usually associated with L. kotschyanum, was more common in the horizontal than in the vertical plane. Purple, healthy, encrusting Sporolithon uncommonly occurred. Whitish, gray or green unhealthy or dead corallines were more common on the horizontal plane at both sites, possibly resulting from excessive solar radiation.     

AN SEM‐BASED ANALYSIS OF THE MORPHOLOGY,ANATOMY, AND REPRODUCTION OF LITHOTHAMNION TOPHIFORME (ESPER) UNGER (CORALLINALES,RHODOPHYTA), WITH A COMPARATIVE STUDY OF ASSOCIATED NORTH ATLANTIC ARCTIC/SUBARCTIC MELOBESIOIDEAE1

Lithothamnion tophiforme (Esper) Unger is a dominant, arctic, saxicolous species that extends southward, albeit with reduced cover, into the deeper colder waters of the North Atlantic subarctic, where it also occurs in significant rhodolith deposits with L. glaciale. The external appearance of L. tophiforme is distinctive, but typification, anatomy, reproduction, ecology, and biogeography have not been previously analyzed. These topics are now addressed, with extensive use of SEM, in comparison with other North Atlantic arctic and subarctic melobesioid genera and species. The species considered in this article comprise 95% of the coralline biomass of the colder North Atlantic and adjacent arctic (i.e. less than 12° C summer and less than 0° C winter). In the outer thallus region of coralline algae, crust extension proceeds, calcification develops, surface sloughing and grazing occur, and reproductive structures are initiated. Analysis of the ultrastructure of the outer thallus region (epithallium, meristem, and perithallium) of L. tophiforme shows distinctive generic similarities and specific differences from the other Lithothamnion species discussed here. Considerable generic differences from the Clathromorpum and Leptophytum species also encountered in the region considered are highlighted as well. We discuss the functional and taxonomic implications of these distinguishing features and recommend that they be more widely considered in future research on coralline algae to understand more fully the ecology and evolution of the Corallinales.