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).     

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.     

Taxonomic contributions to Hapalidiales (Corallinophycidae,Rhodophyta): Boreolithothamnion gen. nov., Lithothamnion redefined and with three new species and Roseolithon with new combinations

Phylogenetic analyses of rbcL gene sequences and of concatenated rbcL, psbA, and nuclear SSU rRNA gene sequences resolved the generitype of Lithothamnion, L. muelleri, in a clade with three other southern Australian species, L. kraftii sp. nov., L. saundersii sp. nov., and L. woelkerlingii sp. nov. Cold water boreal species currently classified in Lithothamnion and whose type specimens have been sequenced are transferred to Boreolithothamnion gen. nov., with B. glaciale comb. nov. as the generitype. The other species are B. giganteum comb. nov., B. phymatodeum comb. nov., and B. sonderi comb. nov., whose type specimens are newly sequenced, and B. lemoineae comb. nov., B. soriferum comb. nov., and B. tophiforme comb. nov., whose type specimens were already sequenced. Based on rbcL sequences from the type specimens of Lithothamnion crispatum, L. indicum, and L. superpositum, each is recognized as a distinct species and transferred to the recently described Roseolithon as R. crispatum comb. nov., R. indicum comb. nov., and R. superpositum com. nov., respectively. To correctly assign species to these three genera based only on morpho-anatomy, specimens must have multiporate conceptacles and some epithallial cells with flared walls. The discussion provides examples demonstrating that only with phylogenetic analyses of DNA sequences can the evolution of morpho-anatomical characters of non-geniculate corallines be understood and applied at the correct taxonomic rank. Finally, phylogenetic analyses of DNA sequences support recognition of the Hapalidiales as a distinct order characterized by having multiporate tetra/bisporangial conceptacles, and not as a suborder of Corallinales whose tetra/bisporangial conceptacles are uniporate.     

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

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

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.     

PCR fishing for red endophytes in British Columbia Kallymeniaceae (Gigartinales,Florideophyceae) uncovers the species‐rich Kallymenicola gen. nov. (Palmariales,Nemaliophycidae)

Unexpected contaminants uncovered during routine COI‐5P DNA barcoding of British Columbia Kallymeniaceae indicated the presence of a novel lineage allied to the family Meiodiscaceae, Palmariales. Available rbcL data for species of this family were used to design specific primers to screen for the presence of the meiodiscacean species in 534 kallymeniacean specimens primarily from British Columbia, Canada. Ultimately, 43 positive PCR products representing six diverse genetic groups from nine host species were uncovered; three are described here in the new genus Kallymenicola gen. nov., viz., K. invisiblis sp. nov., K penetrans sp. nov., and K superficialis sp. nov. Although genetic groups loosely displayed evidence of host specificity and cospeciation, examples of host switching with interesting biogeographical patterns were also documented.     

DNA sequencing,anatomy, and calcification patterns support a monophyletic,subarctic, carbonate reef‐forming Clathromorphum (Hapalidiaceae,Corallinales, Rhodophyta)

For the first time, morpho‐anatomical characters that were congruent with DNA sequence data were used to characterize several genera in Hapalidiaceae—the major eco‐engineers of Subarctic carbonate ecosystems. DNA sequencing of three genes (SSU, rbcL, ribulose‐1, 5‐bisphosphate carboxylase/oxygenase large subunit gene and psbA, photosystem II D1 protein gene), along with patterns of cell division, cell elongation, and calcification supported a monophyletic Clathromorphum. Two characters were diagnostic for this genus: (i) cell division, elongation, and primary calcification occurred only in intercalary meristematic cells and in a narrow vertical band (1–2 μm wide) resulting in a “meristem split” and (ii) a secondary calcification of interfilament crystals was also produced. Neopolyporolithon was resurrected for N. reclinatum, the generitype, and Clathromorphum loculosum was transferred to this genus. Like Clathromorphum, cell division, elongation, and calcification occurred only in intercalary meristematic cells, but in a wider vertical band (over 10–20 μm), and a “meristem split” was absent. Callilithophytum gen. nov. was proposed to accommodate Clathromorphum parcum, the obligate epiphyte of the northeast Pacific endemic geniculate coralline, Calliarthron. Diagnostic for this genus were epithallial cells terminating all cell filaments (no dorsi‐ventrality was present), and a distinct “foot” was embedded in the host. Leptophytum, based on its generitype, L. laeve, was shown to be a distinct genus more closely related to Clathromorphum than to Phymatolithon. All names of treated species were applied unequivocally by linking partial rbcL sequences from holotype, isotype, or epitype specimens with field‐collected material. Variation in rbcL and psbA sequences suggested that multiple species may be passing under each currently recognized species of Clathromorphum and Neopolyporolithon.     

Adeylithon bosencei gen. et sp. nov. (Corallinales,Rhodophyta): a new reef‐building genus with anatomical affinities with the fossil Aethesolithon

Adeylithon gen. nov. with one species, A. bosencei sp. nov., belonging to the subfamily Hydrolithoideae is described from Pacific coral reefs based on psbA sequences and morpho‐anatomy. In contrast with Hydrolithon, A. bosencei showed layers of large polygonal “cells,” which resulted from extensive lateral fusions of perithallial cells, interspersed among layers of vegetative cells. This anatomical feature is shared with the fossil Aethesolithon, but lacking DNA sequences from the fossils and the fragmentary nature of Aethesolithon type material, we cannot ascertain if Adeylithon and Aethesolithon are congeneric. Morpho‐anatomical features of A. bosencei were generally congruent with diagnostic features of the subfamily Hydrolithoideae: (i) outline of cell filaments entirely lost in large portions due to pervasive and extensive cell fusions, (ii) trichocytes not arranged in tightly packed horizontal fields, (iii) basal layer without palisade cells, and (iv) cells lining the canal pore oriented more or less perpendicular to roof surface and not protruding into the canal. However, it showed a predominant monomerous thallus organization and trichocytes were disposed in large pustulate, horizontal fields, although they were not tightly packed and did not become distinctly buried in the thallus. Only mature tetrasporangial conceptacles were observed, therefore the type of conceptacle roof formation remained undetermined. Adeylithon bosencei occurs on shallow coral reefs, in Australia, Papua New Guinea, and South Pacific islands (Fiji, Vanuatu). Fossil Aethesolithon is considered an important component of shallow coral reefs since the Miocene; fossil records showed a broad Indo‐Pacific distribution, but a long‐term process of range contraction in the last 2.6 million years, resulting in an overlap with the distribution of the extant Adeylithon. While the congeneric nature of extant and fossil taxa remained uncertain, similarities in morpho‐anatomy, habitat, and distribution may indicate that both taxa likely shared a common ancestor.     

Sequencing type material resolves the identity and distribution of the generitype Lithophyllum incrustans,and related European species L. hibernicum and L. bathyporum (Corallinales,Rhodophyta)

DNA sequences from type material in the nongeniculate coralline genus Lithophyllum were used to unambiguously link some European species names to field‐collected specimens, thus providing a great advance over morpho‐anatomical identifi‐cation. In particular, sequence comparisons of rbcL, COI and psbA genes from field‐collected specimens allowed the following conclusion: the generitype species, L. incrustans, occurs mostly as subtidal rhodoliths and crusts on both Atlantic and Mediterranean coasts, and not as the common, NE Atlantic, epilithic, intertidal crust reported in the literature. The heterotypic type material of L. hibernicum was narrowed to one rhodolith belonging in Lithophyllum. As well as occurring as a subtidal rhodolith, L. hibernicum is a common, epilithic and epizoic crust in the intertidal zone from Ireland south to Mediterranean France. A set of four features distinguished L. incrustans from L. hibernicum, including epithallial cell diameter, pore canal shape of sporangial conceptacles and sporangium height and diameter. An rbcL sequence of the lectotype of Lithophyllum bathyporum, which was recently proposed to accommodate Atlantic intertidal collections of L. incrustans, corresponded to a distinct taxon hitherto known only from Brittany as the subtidal, bisporangial, lectotype, but also occurs intertidally in Atlantic Spain. Specimens from Ireland and France morpho‐anatomically identified as L. fasciculatum and a specimen from Cornwall likewise identified as L. duckerae were resolved as L. incrustans and L. hibernicum, respectively.     

Molecular and morphological evidence for Sheathia gen. nov. (Batrachospermales,Rhodophyta) and three new species

The freshwater red algal genus Batrachospermum has been shown to be paraphyletic since the first molecular studies of the Batrachospermales. Previous research, along with this study, provides strong support for the clade Batrachospermum section Helminthoidea. This study has found that heterocortication, the presence of both cylindrical and bulbous cells on the main axis, is an underlying synapomorphy of this clade. Based on support from DNA sequences of the rbcL gene, the COI barcode region and the rDNA ITS 1 and 2, along with morphological studies, the new genus Sheathia is proposed. Seven heterocorticate species were recognized from the molecular clades. Sheathia boryana and S. exigua sp. nov. appear to be restricted to Europe, whereas S. confusa occurs in Europe and New Zealand. Sheathia involuta is widespread in the USA and reported for the first time from Europe. Sheathia americana sp. nov., has been collected in the USA and Canada, and S. heterocortica and S. grandis sp. nov. have been collected only in the USA. Sheathia confusa and S. grandis can be distinguished based on morphological characters, whereas DNA sequence data are required to conclusively distinguish the other species. Sheathia fluitans and S. carpoinvolucra also are placed within this genus based on the presence of heterocortication. These data also hint at greater diversity among non‐heterocorticate Sheathia than is recognized by the single species name S. arcuata.     

Trichocytes in Lithophyllum kotschyanum and Lithophyllum spp. (Corallinales,Rhodophyta) from the NW Indian Ocean

The current diagnosis of the genus Lithophyllum includes absent or rare trichocyte occurrence. After examining holotype material, single trichocytes have been revealed to occur abundantly in Lithophyllum kotschyanum Unger, and in freshly collected specimens of Lithophyllum spp. from the Red Sea, Gulf of Aden and Socotra Island (Yemen). Trichocyte occurrence is not considered a diagnostic character at specific or supraspecific levels in the Lithophylloideae, and the ecological significance of trichocyte formation is discussed. The generitype species, L. incrustans Philippi, does not show trichocytes nor do many other Lithophyllum species from diverse geographic localities, but the presence of abundant trichocytes in other congeneric taxa requires emendation of the genus diagnosis. Therefore, the diagnosis of Lithophyllum is here emended by eliminating the adjective “rare” in the sentence concerning trichocyte occurrence, as follows: “Trichocytes present or absent, if present occurring singly.”     

Morphology of the crustose coralline alga Pseudolithophyllum muricatum (Corallinales,Rhodophyta) responds to 30 years of ocean acidification in the Northeast Pacific

As the process of ocean acidification alters seawater carbon chemistry, physiological processes such as skeletal accretion are expected to become more difficult for calcifying organisms. The crustose coralline red algae (Corallinales, Rhodophyta) form an important guild of calcifying primary producers in the temperate Northeast Pacific. The morphology of important ecological traits, namely, skeletal density and thallus thickness near the growing edge, was evaluated in Pseudolithophyllum muricatum (Foslie) Steneck & R.T. Paine, the competitively dominant alga within this guild. P. muricatum shows a morphological response to increased ocean acidification in the temperate Northeast Pacific. Comparing historical (1981–1997) and modern (2012) samples from the field, crust thickness near the growing edge was approximately half as thick in modern samples compared with historical samples, while crust calcite density showed no significant change between the two sample groups. Morphological changes at the growing edge have important consequences for mediating competitive interactions within this guild of algae, and may affect the role of crustose coralline algal beds as hosts to infaunal communities and facilitators of recruitment in many invertebrate and macroalgal species.     

Cyanomargarita gen. nov. (Nostocales,Cyanobacteria): convergent evolution resulting in a cryptic genus

Two populations of Rivularia‐like cyanobacteria were isolated from ecologically distinct and biogeographically distant sites. One population was from an unpolluted stream in the Kola Peninsula of Russia, whereas the other was from a wet wall in the Grand Staircase‐Escalante National Monument, a desert park‐land in Utah. Though both were virtually indistinguishable from Rivularia in field and cultured material, they were both phylogenetically distant from Rivularia and the Rivulariaceae based on both 16S rRNA and rbcLX phylogenies. We here name the new cryptic genus Cyanomargarita gen. nov., with type species C. melechinii sp. nov., and additional species C. calcarea sp. nov. We also name a new family for these taxa, the Cyanomargaritaceae.     

Beneath the hairy look: the hidden reproductive diversity of the Gibsmithia hawaiiensis complex (Dumontiaceae,Rhodophyta)

The tropical alga previously recognized as Gibsmithia hawaiiensis (Dumontiaceae, Rhodophyta) was recently suggested to represent a complex of species distributed throughout the Indo‐Pacific Ocean and characterized by a peculiar combination of hairy (pilose) gelatinous lobes growing on cartilaginous stalks. Phylogenetic reconstructions based on three genetic markers are presented here with the inclusion of new samples. Further diversity is reported within the complex, with nine lineages spread in four major phylogenetic groups. The threshold between intra‐ and interspecific relationships was assessed by species delimitation methods, which indicate the existence of 8–10 putative species in the complex. Two species belonging to the G. hawaiiensis complex are described here: Gibsmithia malayensis sp. nov. from the Coral Triangle and Gibsmithia indopacifica sp. nov., widely distributed in the Central and Eastern Indo‐Pacific. Morphological differences in the vegetative and reproductive structures of the newly described species are provided and compared to the previously described species of the complex. Additional lineages represent putative species, which await further investigation to clarify their taxonomic status. Gibsmithia hawaiiensis sensu stricto is confirmed to be endemic to the Hawaiian Islands, and Gibsmithia eilatensis is apparently confined to the Red Sea, with an expanded distribution in the region. New records of the G. hawaiiensis complex are reported from Egypt, Saudi Arabia, Indonesia, Philippines, and the Federated States of Micronesia, indicating that the complex is more broadly distributed than previously considered. The isolated position of Gibsmithia within the Dumontiaceae is corroborated by molecular data.     

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.     

Diversity and distribution of Laurencia sensu stricto (Rhodomelaceae,Rhodophyta) from the Mexican Pacific,including L. mutueae sp. nov.

The alpha diversity of Laurencia sensu stricto, as well as the majority of the other algal groups along the Mexican Pacific, was underestimated because very few studies had incorporated the use of molecular markers in taxonomic studies, which would allow a more realistic estimation of diversity, incluing new records and new species. The records of Laurencia s.s. for the Eastern Pacific (California, USA to Chile) currently represent 23% of its richness worldwide. In this work, we proposed an updated census of the currently recognized species of Laurencia s.s. for the Mexican Pacific. This checklist reported the occurrence of 22 species that represent 16% of the 137 species worldly recorded. We further included taxonomic remarks, type localities, and a detailed distribution for each species. In addition, we proposed a new species for this region, Laurencia mutueae sp. nov., based on morphological observation as well as phylogenetic analyses. The distribution in the Mexican Pacific revealed that the highest records of species were for the sub‐temperate region, while the localities along the Mexican tropical Pacific were poorly recorded. The scarcity of floristic affinities between the eastern and the western and central parts of the North Pacific Ocean was hypothesized to be a consequence of a strong isolation and hard barriers, such as the water masses between these regions.     

Coralline red algae from the Silurian of Gotland indicate that the order Corallinales (Corallinophycidae,Rhodophyta) is much older than previously thought

Aguirrea fluegelii gen. et sp. nov. (Corallinales, Corallinophycidae, Rhodophyta) is described from the mid‐Silurian of Gotland Island, Sweden (Högklint Formation, lower Wenlock). The holotype is of dimerous construction and includes a uniporate conceptacle with a sporangium, thus providing evidence that taxa of the Corallinales/Corallinaceae existed at least 300 million years earlier than previously documented. Aguirrea fluegelii cannot be unequivocally placed in any of seven currently recognized lineages/subfamilies/groups of the Corallinaceae as not all diagnostic characters are preserved, and thus is accorded incertae sedis status within the family Corallinaceae and order Corallinales. Extant evolutionary history studies of Corallinophycidae involving molecular clocks now require updating using new calibration points to take account of the much earlier unequivocal mid‐Silurian record of uniporate conceptacle‐bearing taxa of Corallinales/Corallinaceae as well as the parallel record of Graticula, a genus attributed to the Sporolithales.     

Diversity of bladed Bangiales (Rhodophyta) in western Mediterranean: recognition of the genus Themis and descriptions of T. ballesterosii sp. nov., T. iberica sp. nov., and Pyropia parva sp. nov.

The diversity of the bladed species of the red algal order Bangiales from the Iberian Mediterranean shores has been reassessed after a detailed study of this region. Prior to this study, 11 bladed species of Bangiales had been reported from Mediterranean waters: Porphyra atropurpurea, P. cordata, P. coriacea, P. dioica, P. linearis, P. purpurea, P. umbilicalis, Pyropia leucosticta, Pyropia koreana (as P. olivii), Py. elongata (as P. rosengurttii) and Py. suborbiculata. A combined analysis of the nuclear nSSU and the plastid rbcL genes together with detailed morphological studies has confirmed the presence of species within the genera Porphyra and Pyropia and also revealed a third, undescribed genus, Themis gen. nov. Porphyra linearis, Pyropia elongata and the introduced Pyropia koreana had been previously listed for the Mediterranean and were recorded in this study. An additional four species, including the introduced Pyropia suborbiculata and three new species: Pyropia parva sp. nov., Themis ballesterosii sp. nov., and Themis iberica sp. nov. were also observed. Hence, most of the Porphyra species traditionally reported along these shores were not reported in this survey. This new floristic Bangiales composition confirms the importance of the Mediterranean basin as a hotspot for biodiversity, possible endemics of ancient origin and high proportion of introductions. Our data also continue to confirm the extent of Bangiales diversity at regional and worldwide levels.