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.     

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.     

Timing of the evolutionary history of Corallinaceae (Corallinales,Rhodophyta)

The temporal dimension of the most recent Corallinaceae (order Corallinales) phylogeny was presented here, based on first occurrence time estimates from the fossil record. Calibration of the molecular clock of the genetic marker SSU entailed a separation of Corallinales from Hapalidiales in the Albian (Early Cretaceous ~105 mya). Neither the calibration nor the fossil record resolved the succession of appearance of the first three emerging subfamilies: Mastophoroideae, Corallinoideae, and Neogoniolithoideae. The development of the tetra/bisporangial conceptacle roofs by filaments surrounding and interspersed among the sporangial initials was an evolutionary novelty emerging at the Cretaceous–Paleogene boundary (~66 mya). This novelty was shared by the subfamilies Hydrolithoideae, Metagoniolithoideae, and Lithophylloideae, which diverged in the early Paleogene. Subclades within the Metagoniolithoideae and Lithophylloideae diversified in the late Oligocene–middle Miocene (~28–12 mya). The most common reef corallinaceans (Hydrolithon, Porolithon, Harveylithon, “Pneophyllum” conicum, and subclades within Lithophylloideae) appeared in this interval in the Indo‐Australian Archipelago.     

Revision of Corallinaceae (Corallinales,Rhodophyta): recognizing Dawsoniolithon gen. nov., Parvicellularium gen. nov. and Chamberlainoideae subfam. nov. containing Chamberlainium gen. nov. and Pneophyllum

A multi‐gene (SSU, LSU, psbA, and COI) molecular phylogeny of the family Corallinaceae (excluding the subfamilies Lithophylloideae and Corallinoideae) showed a paraphyletic grouping of six monophyletic clades. Pneophyllum and Spongites were reassessed and recircumscribed using DNA sequence data integrated with morpho‐anatomical comparisons of type material and recently collected specimens. We propose Chamberlainoideae subfam. nov., including the type genus Chamberlainium gen. nov., with C. tumidum comb. nov. as the generitype, and Pneophyllum. Chamberlainium is established to include several taxa previously ascribed to Spongites, the generitype of which currently resides in Neogoniolithoideae. Additionally we propose two new genera, Dawsoniolithon gen. nov. (Metagoniolithoideae), with D. conicum comb. nov. as the generitype and Parvicellularium gen. nov. (subfamily incertae sedis), with P. leonardi sp. nov. as the generitype. Chamberlainoideae has no diagnostic morpho‐anatomical features that enable one to assign specimens to it without DNA sequence data, and it is the first subfamily to possess both Type 1 (Chamberlainium) and Type 2 (Pneophyllum) tetra/bisporangial conceptacle roof development. Two characters distinguish Chamberlainium from Spongites: tetra/biasporangial conceptacle chamber diameter (<300 μm in Chamberlainium vs. >300 μm in Spongites) and tetra/bisporangial conceptacle roof thickness (<8 cells in Chamberlainium vs. >8 cells in Spongites). Two characters also distinguish Pneophyllum from Dawsoniolithon: tetra/bisporangial conceptacle roof thickness (<8 cells in Pneophyllum vs. >8 cells in Dawsoniolithon) and thallus construction (dimerous in Pneophyllum vs. monomerous in Dawsoniolithon).     

Misleading morphologies and the importance of sequencing type specimens for resolving coralline taxonomy (Corallinales,Rhodophyta): Pachyarthron cretaceum is Corallina officinalis

Coralline red algae play a key role in the ecology of near shore marine ecosystems and are increasingly being used to study the effects of climate change in the marine environment. Corallines are very difficult to identify to species, and even to genus, using morpho‐anatomy, likely complicating studies of their ecology, physiology, and biodiversity. We sequenced a 296 base pair fragment of chloroplast DNA from a 187‐year‐old isolectotype specimen of Pachyarthron cretaceum, a morphologically distinct geniculate species, to demonstrate that coralline morphology is often misleading and that species names can only be applied unequivocally by comparing DNA sequences from type material with sequences from field‐collected specimens. Our results indicate that Pachyarthron cretaceum is synonymous with Corallina officinalis.     

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.     

New branched Porolithon species (Corallinales,Rhodophyta) from the Great Barrier Reef,Coral Sea,and Lord Howe Island

Porolithon is one of the most ecologically important genera of tropical and subtropical crustose (non-geniculate) coralline algae growing abundantly along the shallow margins of coral reefs and functioning to cement reef frameworks. Thalli of branched, fruticose Porolithon specimens from the Indo-Pacific Ocean traditionally have been called P. gardineri, while massive, columnar forms have been called P. craspedium. Sequence comparisons of the rbcL gene both from type specimens of P. gardineri and P. craspedium and from field-collected specimens demonstrate that neither species is present in east Australia and instead resolve into four unique genetic lineages. Porolithon howensis sp. nov. forms columnar protuberances and loosely attached margins and occurs predominantly at Lord Howe Island; P. lobulatum sp. nov. has fruticose to clavate forms and free margins that are lobed and occurs in the Coral Sea and on the Great Barrier Reef (GBR); P. parvulum sp. nov. has short (<2 cm), unbranched protuberances and attached margins and is restricted to the central and southern GBR; and P. pinnaculum sp. nov. has a mountain-like, columnar morphology and occurs on oceanic Coral Sea reefs. A rbcL gene sequence of the isotype of P. castellum demonstrates it is a different species from other columnar species. In addition to the diagnostic rbcL and psbA marker sequences, the four new species may be distinguished by a combination of features including thallus growth form, margin shape (attached or unattached), and medullary system (coaxial or plumose). Porolithon species, because of their ecological importance and sensitivity to ocean acidification, need urgent documentation of their taxonomic diversity.     

Polychaete meets octopus: symbiotic relationship between Spathochaeta octopodis gen. et sp. nov. (Annelida: Chrysopetalidae) and Octopus sp. (Mollusca: Octopodidae)

Marine annelids in the subfamily Calamyzinae (family Chrysopetalidae) are either symbiotic or free-living forms that have been mainly reported from deep-sea chemosynthetic systems. Symbiotic calamyzines mainly live in the mantle cavity of bivalves in hydrothermal vents or cold seeps, but one species is also found to be inserted into the epidermis of polychaetes. We found a single specimen of calamyzine polychaete on the body surface of Octopus sp. collected in the Sea of Kumano (Japan), which represents the first known record of symbiotic association between polychaetes and octopuses. We described the specimen as Spathochaeta octopodis gen. et sp. nov. Spathochaeta gen. nov. can be discriminated from other genera in Calamyzinae by the presence of spatula-shaped notochaetae and dorsal chaetal lobes. We also provided the phylogenetic position of S. octopodis gen. et sp. nov. within Chrysopetalidae based on four gene markers (COI, 16S, 18S, H3). www.zoobank.org/urn:lsid:zoobank.org:pub:A8FB15C1-31A7-4487-966B-13F10E19A373.     

Neosiphonia flavimarina gen. et sp. nov. with a taxonomic reassessment of the genus Polysiphonia (Rhodomelaceae, Rhodophyta)

Vegetative and reproductive development of Neosiphonia flavimarina gen. et sp. nov. (Rhodomelaceae, Ceramiales) from Bangpo on the western coast of Korea was investigated. This species is superficially similar to Polysiphonia, but differs distinctly from the latter in vegetative and reproductive structures. The plants attach by a solid disk composed of a dense cluster of rhizoids cut off from the pericentral cell wall, and bear erect indeterminate branches producing the lateral-branch initials from successive segments in a spiral arrangement. The procarps have a three-celled carpo-gonial branch. Spermatangial branches are formed on a primary branch of the trichoblasts, terminating in a single or occasionally two large, sterile cells. Tetra-sporangia are produced from the second pericentral cell adjacent to the trichoblast basal cell on indeterminate branches, and arranged spirally. Comparing several taxonomic characters among related genera, Neosiphonia occupies an independent phylogenetic position from Polysiphonia and leads to the conclusion that the genus may have a strong link with Fernandosiphonia which has a unilateral branching system. Relevant nomenclatural changes for several Polysiphonia species are also proposed.     

Kalinella bambusicola gen. et sp. nov. (Trebouxiophyceae, Chlorophyta), a novel coccoid Chlorella-like subaerial alga from Southeast Asia

The traditional green algal genus Chlorella , which comprised coccoid algae surrounded by a smooth cell wall and reproducing solely by autosporulation, has proved to be polyphyletic and extremely diverse in phylogenetic terms. We studied a new subaerial Chlorella -like strain CAUP H7901 and morphological, ultrastructural, and molecular phylogenetic investigations indicated that it represents a new lineage of the trebouxiophycean Watanabea clade, dissimilar from other members of this group. The alga has globular coccoid cells with a single parietal pyrenoid-bearing chloroplast. The pyrenoid is transected by multiple radial thylakoid bands. The alga reproduces exclusively by means of asexual autospores of unequal size. In 18S rDNA sequence phylogenies, it was nested within the Watanabea clade close to lineages containing Chlorella saccharophila , Chlorella luteoviridis , Heveochlorella hainangensis , and two uncharacterized strains, but alternative positions within the Watanabea clade could not be rejected by an approximately unbiased (AU) test. Here we describe this organism as a new genus and species Kalinella bambusicola gen. et sp. nov. Furthermore, we describe Heterochlorella gen. nov. to accommodate a species previously referred to as Chlorella luteoviridis .     

Vallodiscus gen. nov., a new fossil resting spore morpho-genus related to the marine diatom genus Chaetoceros (Bacillariophyceae)

A new fossil marine diatom resting spore morphogenus, Vallodiscus Suto gen. nov., is described using samples from Deep Sea Drilling Project Site 338 in the Norwegian Sea, Sites 436 and 438 in the north‐west Pacific Ocean and the onland Newport Beach Section, California. Vallodiscus is characterized by a single ring of veins along the epivalve margin and a hypovalve covered with circular depressions of several sizes with gentle elevation. The morpho‐genus bears three new species and one new combination: Vallodiscus simplexus Suto sp. nov., Vallodiscus complexus Suto sp. nov., Vallodiscus lanceolatus Suto sp. nov. and Vallodiscus chinchae (Mereschkowsky) Suto comb. nov.     

An integrative systematic approach to species diversity and distribution in the genus Mesophyllum (Corallinales,Rhodophyta) in Atlantic and Mediterranean Europe

For the first time, a comprehensive assessment of Mesophyllum species diversity and their distribution in Atlantic Europe and the Mediterranean Sea is presented based on molecular (COI-5P, psbA) and morphological data. The distribution ranges were redefined for the four species collected in this study: M. alternans, M. expansum, M. macroblastum and M. sphaericum. Mesophyllum sphaericum, which was previously known only from a single maerl bed in Galicia (NW Spain), is reported from the Mediterranean Sea. The known range of M. expansum (Mediterranean and Macaronesia) was extended to the Atlantic Iberian Peninsula. The occurrence of M. alternans was confirmed along the Atlantic French coast south to Algarve (southern Portugal). Mesophyllum lichenoides was only recorded from the Atlantic, whereas M. macroblastum appears to be restricted to the Mediterranean Sea. A positive correlation was observed between maximum Sea Surface Temperature (SSTmax) and the depth at which M. expansum was collected, suggesting that this species may compensate for higher SST by growing in deeper habitats where the temperature is lower. The latter indicates that geographic shifts in the distribution of coastal species as a result of global warming can possibly be mitigated by changes in the depth profile at which these species occur. Mesophyllum expansum, an important builder of Mediterranean coralligenous habitats, may be a good target species to assess its response to climate change.     

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.     

Lunachloris lukesovae gen. et sp. nov. (Trebouxiophyceae,Chlorophyta), a novel coccoid green alga isolated from soil in South Bohemia,Czech Republic

Culture collections of microorganisms can still hold undiscovered biodiversity; with molecular techniques, considerable progress has been made in characterizing microalgae which were isolated in the past and misidentified due to a lack of morphological features. However, many strains are still awaiting taxonomic reassessment. Here we analysed the phylogenetic position, morphology and ultrastructure of the strain CCALA 307 previously identified as Coccomyxa cf. gloeobotrydiformis Reysigl isolated in 1987 from field soil in South Bohemia, Czech Republic. Molecular phylogenetic analyses based on SSU rDNA and the plastid rbcL gene revealed that the strain CCALA 307 formed a distinct sister lineage to Neocystis and Prasiola clades within the Trebouxiophyceae. We describe this strain as a new genus and species, Lunachloris lukesovae. Multiple conserved nucleotide positions identified in the secondary structures of the highly variable ITS2 rDNA barcoding marker provide further evidence of the phylogenetic position of Lunachloris. Minute vegetative cells of this newly recognized species are spherical or ellipsoid, with a single parietal chloroplast without a pyrenoid. Asexually, it reproduces by the formation of 2–6 autospores. Since the majority of recent attention has been paid to algae from the tropics or extreme habitats, the biodiversity of terrestrial microalgae in temperate regions is still notably unexplored and even a ‘common’ habitat like agricultural soil can contain new, as yet unknown species. Moreover, this study emphasizes the importance of culture collections of microorganisms even in the era of culture-independent biodiversity research, because they may harbour novel and undescribed organisms as well as preserving strains for future studies.     

Reef‐building coralline algae from the Southwest Atlantic: filling gaps with the recognition of Harveylithon (Corallinaceae,Rhodophyta) on the Brazilian coast

The Southwest Atlantic is notable for having extensive reef areas cemented by nongeniculate coralline red algae. Based on an analysis of four genetic markers and morpho‐anatomical features, we clarify the species of Harveylithon in the tropical and warm temperate Southwest Atlantic. Species delimitation methods (mBGD, ABGD, SPN, and PTP), using three markers (psbA, rbcL, and COI), support the recognition of three new species: H. catarinense sp. nov., H. maris‐bahiensis sp. nov., and H. riosmenum sp. nov., previously incorrectly called Hydrolithon samoënse. Our findings highlight the importance of using an approach with several lines of evidence to solve the taxonomic status of the cryptic species.     

Parvularia atlantis gen. et sp. nov., a Nucleariid Filose Amoeba (Holomycota,Opisthokonta)

The opisthokonts constitute a eukaryotic supergroup divided into two main clades: the holozoans, which include animals and their unicellular relatives, and the holomycotans, which include fungi, opisthosporidians, and nucleariids. Nucleariids are phagotrophic filose amoebae that phenotypically resemble more their distant holozoan cousins than their holomycotan phylogenetic relatives. Despite their evolutionary interest, the diversity and internal phylogenetic relationships within the nucleariids remain poorly studied. Here, we formally describe and characterize by molecular phylogeny and microscopy observations Parvularia atlantis gen. et sp. nov. (formerly Nuclearia sp. ATCC 50694), and compare its features with those of other nucleariid genera. Parvularia is an amoebal genus characterized by radiating knobbed and branching filopodia. It exhibits prominent vacuoles observable under light microscopy, a cyst‐like stage, and completely lacks cilia. P. atlantis possesses one or two nuclei with a central nucleolus, and mitochondria with flat or discoid cristae. These morphological features, although typical of nucleariids, represent a combination of characters different to those of any other described Nuclearia species. Likewise, 18S rRNA‐based phylogenetic analyses show that P. atlantis represents a distinct lineage within the nucleariids.     

A new fossil flower from the Turonian of New Jersey: Dressiantha bicarpellata gen. et sp. nov. (Capparales)

Recent discoveries of fossil reproductive structures from deposits of the Raritan Formation in New Jersey (Turonian, Upper Cretaceous, ~90 million years BP) include a previously undescribed representative of the Order Capparales. The fossils are usually charcoalified with three-dimensional structure and excellent anatomical details. In the present contribution, we introduce a taxon represented by fossil flowers that have a combination of characters now found in the families of the Order Capparales sensu Cronquist. The fossil species is characterized by an unique suite of characters, such as the presence of a gynophore, arrangement of the sepals, unequal petal size, monothecal anthers, and a bicarpellate gynoecium, that are found in extant families of the Order Capparales. This new taxon constitutes an important addition to our understanding of Cretaceous angiosperm diversity and represents the oldest known fossil record for the Capparales. Heretofore, the oldest known capparalean was from the Late Tertiary sediments of North America.