Kallymenia crouaniorum (Kallymeniaceae,Rhodophyta), a new red algal species from the Laminaria hyperborea understorey community

In this paper we describe Kallymenia crouaniorum Vergés & Le Gall, sp. nov. (Kallymeniaceae), a new marine red alga from the north-eastern Atlantic Ocean. rbcL and LSU sequences of this species, previously misidentified in the field as Kallymenia reniformis, diverged from those of other Kallymenia species by at least 7.5% and 5.2%, respectively. Kallymenia crouaniorum also has a set of distinctive vegetative and reproductive characteristics, including a deeply lacerate frond, a short stipe, dentate margins, large cortical cells up to 110 μm in diameter, highly refractive stellate medullary cells with arms up to 1000 μm in length, and a monocarpogonial branch system. Molecular phylogenies inferred from rbcL and LSU data indicated, albeit with weak support, that this new species is a sister taxon of a lineage encompassing the generitype K. reniformis, as well as most species of Kallymenia included in the phylogenetic analysis. The main morphological characters that delineate monocarpogonial Kallymenia species are presented. Moreover, after reviewing the literature and several herbarium specimens, we found in the Weber-van Bosse Herbarium a specimen collected at Roscoff in August 1894 with the anatomical characters of the species described here, confirming that this newly described species has in fact been overlooked and is not a recent introduction.     

Note floristique et repartition de Rhodophycees rares (Kallymeniacees et Sebdeniacees) de la Mediterranee occidentale

Abstract

Floristic notes and geographical distribution of some rare Rhodophyta (Kallymeniaceae and Sebdeniaceae) of the western Mediterranean. Callophyllis laciniata, Kallymenia requienii and Kallymenia lacerata (Kallymeniaceae) and Sebdenia rodrigueziana (Sebdeniaceae) are recorded for the first time in the bay of Naples. For each species systematic and distribution data are also given.     

Schizymenia jonssonii sp. nov. (Nemastomatales,Rhodophyta): a relict or an introduction into the North Atlantic after the last glacial maximum?

North-Atlantic records of Schizymenia dubyi extend along the eastern shores of the North Atlantic from Morocco to southern Britain and Ireland, and the species is also recorded from Iceland. A study was undertaken to confirm the identity of the specimens from Iceland that were geographically separate from the main distribution of S. dubyi and in contrast to other species of the genus did not have gland cells. We analyzed rbcL and COI molecular sequence data from Icelandic specimens and compared the results with those for Schizymenia specimens available in GenBank. For both markers, Schizymenia was shown to be a monophyletic genus. The Icelandic specimens were clearly genetically distinct from S. dubyi and formed a well-supported clade with Schizymenia species from the Northern Pacific. Based on these results, we have described a new species, Schizymenia jonssonii, which can be distinguished by molecular phylogeny, its lack of gland cells and by being strictly intertidal. Crustose tetrasporophytes with identical COI and rbcL sequences were found at the same locations as foliose plants. Schizymenia apoda is reported for the first time in the UK, its identity confirmed by rbcL sequence data. In light of these findings, it is likely that by further molecular analysis of the genus Schizymenia in the north-eastern Atlantic and the Mediterranean, a higher diversity of Schizymenia spp. will be discovered in this region.     

Collections from the mesophytic zone off Bermuda reveal three species of Kallymeniaceae (Gigartinales,Rhodophyta) in genera with transoceanic distributions

A molecular survey of red algae collected by technical divers and submersibles from 90 m in the mesophotic zone off the coast of Bermuda revealed three species assignable to the Kallymeniaceae. Two of the species are representative of recently described genera centered in the western Pacific in Australia and New Zealand, Austrokallymenia and Psaromenia and the third from the Mediterranean Sea and the eastern Atlantic, Nothokallymenia. A phylogenetic analysis of concatenated mitochondrial (COI‐5P) and chloroplast (rbcL) genes, as well as morphological characteristics, revealed that two are shown to be new species with distant closest relatives (N. erosa and Psaromenia septentrionalis), while the third represents a deep water western Atlantic species now moved to an Australasian genus (A. westii).     

MOLECULAR PHYLOGENY OF THE GENUS KUMANOA (BATRACHOSPERMALES,RHODOPHYTA)1

Species belonging to the newly established genus Kumanoa were sampled from locations worldwide. DNA sequence data from the rbcL gene, cox1 barcode region, and universal plastid amplicon (UPA) were collected. The new sequence data for the rbcL were combined with the extensive batrachospermalean rbcL data available in GenBank. Single gene rbcL results showed the genus Kumanoa to be a well‐supported clade, and there was high statistical support for many of the terminal nodes. However, with this gene alone, there was very little support for any of the internal nodes. Analysis of the concatenated data set (rbcL, cox1, and UPA) provided higher statistical support across the tree. The taxa K. vittata and K. amazonensis formed a basal grade, and both were on relatively long branches. Three new species are proposed, K. holtonii, K. gudjewga, and K. novaecaledonensis; K. procarpa var. americana is raised to species level. In addition, the synonymy of K. capensis and K. breviarticulata is proposed, with K. capensis having precedence. Five new combinations are made, bringing the total number of accepted species in Kumanoa to 31. The phylogenetic analyses did not reveal any interpretable biogeographic patterns within the genus (e.g., K. spermatiophora from the tropical oceanic island Maui, Hawaii, was sister to K. faroensis from temperate midcontinental Ohio in North America). Previously hypothesized relationships among groups of species were not substantiated in the phylogenetic analyses, and no intrageneric classification is recommended based on current knowledge.     

CLASSIFICATION OF THE GENUS ISHIGE (ISHIGEALES,PHAEOPHYCEAE) IN THE NORTH PACIFIC OCEAN WITH RECOGNITION OF ISHIGE FOLIACEA BASED ON PLASTID rbcl AND MITOCHONDRIAL cox3 GENE SEQUENCES1

The taxonomy and biogeography of a genus with species that occur in geographically isolated regions is interesting. The brown algal genus Ishige Yendo is a good example, with species that apparently inhabit warm regions of both the northwestern and northeastern Pacific Ocean. We determined the sequences of mitochondrial cox3 and plastid rbcL genes from specimens of the genus collected over its distributional range. Analyses of the 86 cox3 and 97 rbcL sequences resulted in congruent trees in which Ishige sinicola (Setch. et N. L. Gardner) Chihara consisted of two distinct clades: one comprising samples from Korea and Japan, and the other comprising samples from the Gulf of California. Additional observations of the morphology and anatomy of the specimens agree with the molecular data. On the basis of results, we reinstated Ishige foliacea S. Okamura (considered a synonym of I. sinicola from the Gulf of California) for plants from the northwest Pacific region and designated a specimen in the Yendo Herbarium (SAP) as the lectotype. I. foliacea is distinguished by large (up to 20 cm) and wide (up to 20 mm) thalli, with a cortex of 4–7 cells, and a medulla composed of long, tangled hyphal cells. Both cox3 and rbcL sequence data strongly support the sister‐area relationship between the northwest Pacific region and the Gulf of California. A likely explanation for this pattern would be the presence of a species ancestral to contemporary species of Ishige in both regions during the paleogeological period, with descendants later isolated by distance.     

Wilsonosiphonia gen. nov. (Rhodomelaceae,Rhodophyta) based on molecular and morpho‐anatomical characters

Morphological, anatomical, and molecular sequence data were used to assess the establishment and phylogenetic position of the genus Wilsonosiphonia gen. nov. Phylogenies based on rbcL and concatenated rbcL and cox1 loci support recognition of Wilsonosiphonia gen. nov., sister to Herposiphonia. Diagnostic features for Wilsonosiphonia are rhizoids located at distal ends of pericentral cells and taproot‐shaped multicellular tips of rhizoids. Wilsonosiphonia includes three species with diagnostic rbcL and cox1 sequences, Wilsonosiphonia fujiae sp. nov. (the generitype), W. howei comb. nov., and W. indica sp. nov. These three species resemble each other in external morphology, but W. fujiae is distinguished by having two tetrasporangia per segment rather than one, W. indica by having abundant and persistent trichoblasts, and W. howei by having few and deciduous trichoblasts.     

The monospecific genus Meredithia (Kallymeniaceae,Gigartinales) is species rich and geographically widespread with species from temperate Atlantic,Pacific, and Indian Oceans

Using sequences of 5′ region of the cytochrome oxidase subunit 1 gene, large subunit rDNA, and ribulose‐1,5‐bisphosphate carboxylase/oxygenase large subunit gene as genetic markers to elucidate their phylogenetic positions, six unknown species from Western Australia, Tasmania, Lord Howe Is., and Norfolk Is. cluster with Meredithia in the Kallymeniaceae (Gigartinales), and are described as new members of this previously monospecific genus. Specimens from Bermuda referable to Kallymenia limminghei Mont. in the 20th century also clustered with this genetic grouping, not with the generitype of Kallymenia. The Bermudian specimens are further shown to be morphologically distinct from the type of K. limminghei (Guadeloupe, Caribbean Sea) and are described as a new species, Meredithia crenata. Using these Indo‐Pacific and Bermudian collections, our analyses further show that Psaromenia is closely related to Meredithia, and that Cirrulicarpus nanus sensu stricto should be returned to Meredithia.     

The presence of exotic Hypnea flexicaulis (Rhodophyta) in the Mediterranean Sea as indicated by morphology, rbcL and cox1 analyses

Here we report the first finding of Hypnea flexicaulis Yamagishi and Masuda in the Mediterranean Sea (Lagoon of Venice, Italy), identified through molecular analyses using the plastid ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL) and the mitochondrial protein-coding cytochrome c oxidase subunit I (cox1) genes. The phylogenetic reconstruction, based on rbcL + cox1 multiple alignment, showed that all specimens of H. flexicaulis from Venice, Korea, Philippines and Taiwan were included in a monophyletic group supported by a bootstrap value of 100%.It is highly probable that H. flexicaulis has been introduced from Indo-Pacific populations, in particular the Korean one, probably via ship traffic or shellfish transfers.The use of DNA barcoding combined with morphological observations was, in this case, a rapid way to identify this allochthonous species.     

Species Diversity,Phylogeny and Large Scale Biogeographic Patterns of the Genus Padina (Phaeophyceae,Dictyotales)

The brown algal genus Padina (Dictyotales, Phaeophyceae) is distributed worldwide in tropical and temperate seas. Global species diversity and distribution ranges, however, remain largely unknown. Species‐level diversity was reassessed using DNA‐based, algorithmic species delineation techniques based on cox3 and rbcL sequence data from 221 specimens collected worldwide. This resulted in estimates ranging from 39 to 61 putative species (ESUs), depending on the technique as well as the locus. We discuss the merits, potential pitfalls, and evolutionary and biogeographic significance of algorithmic species delineation. We unveil patterns whereby ESUs are in all but one case restricted to either the Atlantic or Indo‐Pacific Ocean. Within ocean basins we find evidence for the vast majority of ESUs to be confined to a single marine realm. Exceptions, whereby ESUs span up to three realms, are located in the Indo‐Pacific Ocean. Patterns of range‐restricted species likely arise by repeated founder events and subsequent peripatric speciation, hypothesized to dominate speciation mechanisms for coastal marine organisms in the Indo‐Pacific. Using a three‐gene (cox3, psaA and rbcL), relaxed molecular clock phylogenetic analysis we estimated divergence times, providing a historical framework to interpret biogeographic patterns.     

Diversity within red algal species : variation in world-wide samples of Spyridia filamentosa (Ceramiaceae) and Murrayella periclados (Rhodomelaceae) using DNA markers and breeding studies

Molecular and breeding studies on two pan-tropical marine red algae reveal vastly different levels of genetic variation and reproductive isolation. Sequenced DNA regions from the nuclear, mitochondrial and plastid genomes (partial LSU rRNA, cox2-3 spacer, RuBisCo spacer, respectively) revealed high genetic variation among individuals of Spyridia filamentosa. An rbcL analysis shows that Spyridia is a monophyletic genus distinct from other Ceramiaceae sampled, suggesting that the Ceramiaceae could be paraphyletic. There is complete congruence between all data sets of S. filamentosa, showing a well-supported phylogeographic pattern with samples from the Pacific distinct from Atlantic and Indian Ocean samples. One western Mediterranean sample is associated with Atlantic specimens, while an eastern Mediterranean sample has closer affinities to Pacific samples, possibly indicating a recent cryptic introduction into the eastern Mediterranean. Limited breeding studies imply that these samples are mostly reproductively isolated, whereas a successful cross demonstrated maternal inheritance of organellar DNA. These data indicate that S. filamentosa exists as several cryptic species. Murrayella periclados exhibits low levels of genetic variation and no phylogeographic structure, and almost complete reproductive compatibility between isolates. This suggests that all M. periclados samples share a recent common ancestor that may have dispersed relatively rapidly, or that rates of base pair substitution between these two species vary greatly. Rapid longdistance dispersal of M. periclados is not indicated by what is known of the biology of M. periclados, especially in comparison with S. filamentosa, which appears to be a much better candidate for long-distance dispersal. These data demonstrate that red algal morphospecies are not equivalent units of diversity, with implications for our view of red algal biodiversity and evolution.     

Global sampling reveals low genetic diversity within Compsopogon (Compsopogonales,Rhodophyta)

Twenty-five specimens of the freshwater red alga Compsopogon were collected from locations in North America, South America, Europe, Asia, Australasia and Oceania, and from an aquarium, with the goal of determining genetic diversity among specimens and ascertaining the number of phylogenetic species. Specimens were morphologically identified as having either the ‘caeruleus’ morphology, with regular polyhedral cortical cells, or the ‘leptoclados’ morphology, with irregular cortical cells with rhizoidal outgrowths. The ‘leptoclados’ morphology has been used by some researchers to distinguish the genus Compsopogonopsis from Compsopogon, or at least to distinguish C. leptoclados from other Compsopogon species. Sequence data for the rbcL gene and cox1 barcoding region were obtained for most specimens. In addition, SSU and partial LSU (barcode) rDNA were explored for a few specimens, but all sequences were identical. For the 25 newly generated and eight previously published rbcL gene data, there were seven unique haplotypes, but the sequence divergence was very low (≤7 bp, ≤ 0.7%). One haplotype was widespread, represented by 21 specimens from diverse locations in all regions sampled. Likewise, the 22 new and one previously published cox1 barcode region sequences yielded seven unique haplotypes with little sequence divergence (≤13 bp, ≤ 2.0%). One haplotype was widespread, being shared among 16 specimens from all regions. The combined molecular and morphological data showed no genetic differentiation between the ‘caeruleus’ and ‘leptoclados’ morphologies. The ubiquitous distribution of Compsopogon in tropical/subtropical regions and its low genetic variation are probably facilitated by the alga's ability to tolerate a wide range of stream conditions and its propagation via asexual spores. Given the findings of previous culture-based studies, morphometric research and field observations, coupled with the results of our study, we conclude there is only a single monospecific genus worldwide and that the species is correctly called C. caeruleus, since this is the oldest validly published name; all other previously described species of Compsopogon and Compsopogonopsis are synonyms.     

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.     

Ulva (Chlorophyta,Ulvales) Biodiversity in the North Adriatic Sea (Mediterranean,Italy): Cryptic Species and New Introductions

Ulva Linnaeus (Ulvophyceae, Ulvales) is a genus of green algae widespread in different aquatic environments. Members of this genus show a very simple morphology and a certain degree of phenotypic plasticity, heavily influenced by environmental conditions, making difficult the delineation of species by morphological features alone. Most studies dealing with Ulva biodiversity in Mediterranean waters have been based only on morphological characters and a modern taxonomic revision of this genus in the Mediterranean is not available. We report here the results of an investigation on the diversity of Ulva in the North Adriatic Sea based on molecular analyses. Collections from three areas, two of which subject to intense shipping traffic, were examined, as well as historical collections of Ulva stored in the Herbarium Patavinum of the University of Padova, Italy. Molecular analyses based on partial sequences of the rbcL and tufA genes revealed the presence of six different species, often with overlapping morphologies: U. californica Wille, U. flexuosa Wulfen, U. rigida C. Agardh, U. compressa Linnaeus, U. pertusa Kjellman, and one probable new taxon. U. californica is a new record for the Mediterranean and U. pertusa is a new record for the Adriatic. Partial sequences obtained from historical collections show that most of the old specimens are referable to U. rigida. No specimens referable to the two alien species were found among the old herbarium specimens. The results indicate that the number of introduced seaweed species and their impact on Mediterranean communities have been underestimated, due to the difficulties in species identification of morphologically simple taxa as Ulva.     

Genetic and morphological variation in an ecosystem engineer,Lithophyllum byssoides (Corallinales,Rhodophyta)

Lithophyllum byssoides is a common coralline alga in the intertidal zone of Mediterranean coasts, where it produces biogenic concretions housing a high algal and invertebrate biodiversity. This species is an ecosystem engineer and is considered a target for conservation efforts, but designing effective conservation strategies currently is impossible due to lack of information about its population structure. The morphological and molecular variation of L. byssoides was investigated using morphoanatomy and DNA sequences (psbA and cox2,3) obtained from populations at 15 localities on the Italian and Croatian coasts. Lithophyllum byssoides exhibited a high number of haplotypes (31 psbA haplotypes and 24 cox2,3 haplotypes) in the central Mediterranean. The psbA and cox2,3 phylogenies were congruent and showed seven lineages. For most of these clades, the distribution was limited to one or a few localities, but one of them (clade 7) was widespread across the central Mediterranean, spanning the main biogeographic boundaries recognized in this area. The central Mediterranean populations formed a lineage separate from Atlantic samples; psbA pair‐wise divergences suggested that recognition of Atlantic and Mediterranean L. byssoides as different species may be appropriate. The central Mediterranean haplotype patterns of L. byssoides were interpreted as resulting from past climatic events in the hydrogeological history of the Mediterranean Sea. The high haplotype diversity and the restricted spatial distribution of the seven lineages suggest that individual populations should be managed as independent units.     

Characterization of a Strain of Fukuyoa paulensis (Dinophyceae) from the Western Mediterranean Sea

A single cell of the dinoflagellate genus Fukuyoa was isolated from the island of Formentera (Balearic Islands, west Mediterranean Sea), cultured, and characterized by morphological and molecular methods and toxin analyses. This is the first report of the Gambierdiscus lineage (genera Fukuyoa and Gambierdiscus) from the western Mediterranean Sea, which is cooler than its eastern basin. Molecular analyses revealed that the Mediterranean strain belongs to F. paulensis and that it bears LSU rDNA sequences identical to New Zealand, Australian, and Brazilian strains. It also shared an identical sequence of the more variable ITS‐rDNA with the Brazilian strain. Toxin analyses showed the presence of maitotoxin, 54‐deoxyCTX1B, and gambieric acid A. This is the first observation of the two latter compounds in a Fukuyoa strain. Therefore, both Gambierdiscus and Fukuyoa should be considered when as contributing to ciguatera fish poisoning. Different strains of Fukuyoa form a complex of morphologically cryptic lineages where F. paulensis stands as the most distantly related nominal species. The comparison of the ITS2 secondary structures revealed the absence of CBCs among strains. The study of the morphological and molecular traits depicted an unresolved taxonomic scenario impacted by the low strains sampling.     

Phylogenetic analysis of the north‐east Atlantic and Mediterranean species of the genus Stenosoma (Isopoda,Valvifera, Idoteidae)

Xavier, R., Santos, A. M., Harris, D. J., Sezgin, M., Machado, M., Branco, M. (2012). Phylogenetic analysis of the north‐east Atlantic and Mediterranean species of the genus Stenosoma (Isopoda, Valvifera, Idoteidae). —Zoologica Scripta, 41, 386–399. The marine isopod genus Stenosoma is widespread in the northern hemisphere. However, 12 of its 14 known species are found within the Mediterranean basin and adjacent regions of the north‐east Atlantic and the Black Sea. Such a high level of diversity confined to a limited region of a much larger circumglobal distribution suggests that the Mediterranean region may have played a crucial role in the evolutionary history of this genus. In the present work, the phylogeny of the genus Stenosoma was investigated on the basis of DNA sequencing data from one nuclear (28SrRNA) and two mitochondrial (COI, ND4) gene fragments obtained for nine of 12 Atlantic–Mediterranean species. Divergence time estimates point to a Tethyan origin of Stenosoma and suggest that the speciation events from which stem most of the extant species took place well before the Messinian Salinity Crisis. Stenosoma spinosum and Stenosoma appendiculatum are the only exceptions, as they apparently arose within the Mediterranean during the Pleistocene. Phylogenetic reconstruction agrees with current taxonomic status of most species. However, Stenosoma capito clustered in two distinct and well‐supported clades, one composed of eastern Mediterranean and Black Sea specimens and the other by western Mediterranean and Atlantic ones. Such polyphyly suggests the existence of a previously unrecognized species, Stenosoma sp., which so far has been confounded with S. capito.     

Mediterranean Lithophyllum stictiforme (Corallinales,Rhodophyta) is a genetically diverse species complex: implications for species circumscription,biogeography and conservation of coralligenous habitats

Lithophyllum species in the Mediterranean Sea function as algal bioconstructors, contributing to the formation of biogenic habitats such as coralligenous concretions. In such habitats, thalli of Lithophyllum, consisting of crusts or lamellae with entire or lobed margins, have been variously referred to as either one species, L. stictiforme, or two species, L. stictiforme and L. cabiochiae, in the recent literature. We investigated species diversity and phylogenetic relationships in these algae by sequencing three markers (psbA and rbcL genes, cox2,3 spacer), in conjunction with methods for algorithmic delimitation of species (ABGD and GMYC). Mediterranean subtidal Lithophyllum belong to a well‐supported lineage, hereby called the L. stictiforme complex, which also includes two species described from the Atlantic, L. lobatum and L. searlesii. Our results indicate that the L. stictiforme complex consists of at least 13 species. Among the Mediterranean species, some are widely distributed and span most of the western and central Mediterranean, whereas others appear to be restricted to specific localities. These patterns are interpreted as possibly resulting from allopatric speciation events that took place during the Messinian Salinity Crisis and subsequent glacial periods. A partial rbcL sequence from the lectotype of L. stictiforme unambiguously indicates that this name applies to the most common subtidal Lithophyllum in the central Mediterranean. We agree with recent treatments that considered L. cabiochiae and L. stictiforme conspecific. The diversity of Lithophyllum in Mediterranean coralligenous habitats has been substantially underestimated, and future work on these and other Mediterranean corallines should use identifications based on DNA sequences.