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.     

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.     

Coralline algae (Rhodophyta) in a changing world: integrating ecological,physiological, and geochemical responses to global change

Coralline algae are globally distributed benthic primary producers that secrete calcium carbonate skeletons. In the context of ocean acidification, they have received much recent attention due to the potential vulnerability of their high‐Mg calcite skeletons and their many important ecological roles. Herein, we summarize what is known about coralline algal ecology and physiology, providing context to understand their responses to global climate change. We review the impacts of these changes, including ocean acidification, rising temperatures, and pollution, on coralline algal growth and calcification. We also assess the ongoing use of coralline algae as marine climate proxies via calibration of skeletal morphology and geochemistry to environmental conditions. Finally, we indicate critical gaps in our understanding of coralline algal calcification and physiology and highlight key areas for future research. These include analytical areas that recently have become more accessible, such as resolving phylogenetic relationships at all taxonomic ranks, elucidating the genes regulating algal photosynthesis and calcification, and calibrating skeletal geochemical metrics, as well as research directions that are broadly applicable to global change ecology, such as the importance of community‐scale and long‐term experiments in stress response.     

Unexpected deep-sea fish species on the Porcupine Bank (NE Atlantic): Biogeographical implications

Four specimens corresponding to three rare deep-water fish species were caught on the Porcupine Bank (Northeast Atlantic) in September 2019. These catches include the new northernmost records of Azores rockling Gaidropsarus granti and deep-water dab Poecilopsetta beanii in the Atlantic Ocean and the second record of the latter species in its eastern zone. Three of the specimens were retained and their molecular identification also allowed the Cataetyx alleni DNA barcode to be obtained for the first time. The appearance of P. beanii, a West Atlantic species, in its eastern zone is discussed in relation to a possible phenomenon of transoceanic drift in the larval stage.     

Discovery of the mineral brucite (magnesium hydroxide) in the tropical calcifying alga Polystrata dura (Peyssonneliales,Rhodophyta)

Red algae of the family Peyssonneliaceae typically form thin crusts impregnated with aragonite. Here, we report the first discovery of brucite in a thick red algal crust (~1 cm) formed by the peyssonnelioid species Polystrata dura from Papua New Guinea. Cells of P. dura were found to be infilled by the magnesium‐rich mineral brucite [Mg(OH)₂]; minor amounts of magnesite and calcite were also detected. We propose that cell infill may be associated with the development of thick (> ~5 mm) calcified red algal crusts, integral components of tropical biotic reefs. If brucite infill within the P. dura crust enhances resistance to dissolution similarly to crustose coralline algae that infill with dolomite, then these crusts would be more resilient to future ocean acidification than crusts without infill.     

Photoacclimation and photoregulation strategies of Corallina (Corallinales,Rhodophyta) across the NE Atlantic

This study characterizes the photoacclimation and photoregulation mechanisms that allow calcified macroalgae of the genus Corallina (Corallinales, Rhodophyta) to dominate rock pool habitats across the NE Atlantic despite the highly variable irradiance regimes experienced. Rapid light curves (RLCs) were performed with pulse amplitude modulation (PAM) fluorometry in situ across a full seasonal cycle in the UK intertidal with C. officinalis and C. caespitosa. Latitudinal comparisons were performed across the full extent of C. officinalis’ range in the NE Atlantic (Iceland–northern Spain), and for C. caespitosa in northern Spain. Ex situ RLCs with dark recovery were further employed to assess the optimal, as compared with actual, photophysiology across seasons and latitudes. Corallina species were shown to photoacclimate at seasonal timescales to changing irradiance, increasing light-harvesting during low-light autumn/winter periods and protecting photosystems during high-light summer conditions. Seasonal photoacclimation was achieved through alteration in the number of photosystem (PS) units (PSII and light harvesting antennae) over time. Non-photochemical quenching (NPQ) served as an important photoregulation mechanism utilized by Corallina to prevent or minimize photoinhibition over shorter time scales (seconds–hours), though the efficiency of NPQ was dependent on the seasonal-acclimated state. With increasing latitude the efficiency of photoregulation decreased, representing potential differential photoadaptation of Corallina across species ranges in the NE Atlantic. In contrast, highly conserved inter-specific patterns in photophysiological responses to irradiance were apparent. This study demonstrates the photophysiological mechanisms allowing Corallina to optimize use of the variable irradiance conditions apparent in rock pool environments, when and how they are employed, and their limitations.     

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.     

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.     

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.     

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.     

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.     

Photosynthesis and calcification in the articulated coralline alga Ellisolandia elongata (Corallinales,Rhodophyta) from intertidal rock pools

Calcifying coralline algae are functionally important in many ecosystems but their existence is now threatened by global climate change. The aim of this study is to improve our understanding of coralline algal metabolic functions and their interactions by assessing the respiration, photosynthesis and calcification rates in an articulated (geniculate) coralline alga, Ellisolandia elongata. Algal samples selected for this case study were collected from an intertidal rock-pool on the coast of Brittany (France). Physiological rates were assessed in summer and winter by measuring the concentration of oxygen, dissolved inorganic carbon and total alkalinity fluxes at five irradiance levels and in the dark using incubation chambers.

Respiration, photosynthetic and calcification rates were strongly affected by seasonal changes. Respiration increased with temperature, being ten-fold higher in summer than in winter. Photosynthetic parameters of the photosynthesis-irradiance (P-E) curve, P_g^max, P_n^max and E_k, were two- to three-fold higher in summer relative to winter. Photoinhibition was observed under high irradiance indicating an acclimation of E. elongata to low irradiance levels. Parameters of the calcification-irradiance (G-E) curve, G^max and E_k, were approximately two-fold higher in summer compared with winter. In summer, calcification rates were more strongly inhibited under high irradiance than photosynthetic rates, suggesting a dynamic relationship between these metabolic processes. By inhabiting intertidal rock pools, E. elongata exhibits tolerance to a dynamic physico-chemical environment. Information on respiration, photosynthesis and calcification rates in a calcifying coralline alga inhabiting such dynamic environments in terms of pH and temperature is important in order to better understand how ocean acidification and warming will affect coralline algae in the future.     

A new species of the genus Lightiella: the first record of Cephalocarida (Crustacea) in Europe

A new species of Cephalocarida belonging to the genus Lightiella is described. Like all known species of Lightiella , the new species is characterized by reduction of trunk segment 8, which also lacks both pleura and thoracopods. The diagnostic characters of the species are: (1) one seta on the inner distal corner of the penultimate endopodal segment of second maxilla and thoracopods 1–5; (2) only one claw on the distal segment of the endopod of thoracopod 6. A cladistic analysis of 27 morphological characters was used to estimate the phylogeny of all species of Lightiella , with all other cephalocarid species used as outgroups. The discovery of this species in the Mediterranean fills a gap in the distribution of the genus and of the entire class.  © 2006 The Linnean Society of London, Zoological Journal of the Linnean Society , 2006, 148 , 209–220.     

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.     

Multiple phases of mg‐calcite in crustose coralline algae suggest caution for temperature proxy and ocean acidification assessment: lessons from the ultrastructure and biomineralization in Phymatolithon (Rhodophyta,Corallinales)1

Magnesium content, strongly correlated with temperature, has been developed as a climate archive for the late Holocene without considering anatomical controls on Mg content. In this paper, we explore the ultrastructure and cellular scale Mg‐content variations within four species of North Atlantic crust‐forming Phymatolithon. The cell wall has radial grains of Mg‐calcite, whereas the interfilament (middle lamella) has grains aligned parallel to the filament axis. The proportion of interfilament and cell wall carbonate varies by tissue and species. Three distinct primary phases of Mg‐calcite were identified: interfilament Mg‐calcite (mean 8.9 mol% MgCO₃), perithallial cell walls Mg‐calcite (mean 13.4 mol% MgCO₃), and hypothallium Mg‐calcite (mean 17.1 mol% MgCO₃). Magnesium content for the bulk crust, an average of all phases present, showed a strongly correlated (R² = 0.975) increase of 0.31 mol% MgCO₃ per °C. Of concern for climate reconstructions is the potential for false warming signals from undetected postgrazing wound repair carbonate that is substantially enriched in Mg, unrelated to temperature. Within a single crust, Mg‐content of component carbonates ranged from 8 to 20 mol% MgCO₃, representing theoretical thermodynamic stabilities from aragonite‐equivalent to unstable higher‐Mg‐calcite. It is unlikely that existing current predictions of ocean acidification impact on coralline algae, based on saturation states calculated using average Mg contents, provide an environmentally relevant estimate.     

Field and culture studies of species of Gelidium (Gelidiales,Rhodophyta) from their northern limit of distribution in Europe

Two species of Gelidium, provisionally referred to as G. pusillum and G. latifolium, are included in the Scandinavian flora and reach their northern limit of distribution on the Norwegian west coast. Small frond sizes due to adverse growth conditions, extreme phenotypic variability and lack of sexual reproduction make identification of specimens very difficult. Both species were isolated into unialgal culture and were compared with cultured strains referable to G. pusillum from Ireland and France. Temperature and salinity requirements and tolerance ranges were determined and discussed in view of distribution along the Norwegian coast. Little or no growth occurs below 9 °C, corresponding to a northern summer growth limit. On the Norwegian Skagerrak coast, low winter temperature rather than reduced salinity is the limiting factor.     

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.”     

Mitochondrial DNA reveals a mosaic pattern of phylogeographical structure in Atlantic and Mediterranean populations of anchovy (Engraulis encrasicolus)

This study extends the geographic coverage of a previous study of mitochondrial DNA restriction fragment length polymorphism in European anchovy. Both studies together include 24 samples representing 17 localities extending from the Black Sea, through the Mediterranean Sea to the eastern Atlantic as far south as Dakar, Senegal. Eighty-eight haplotypes define two clades (A and B) separated by 3.2% sequence divergence. Clade A has a star-like genealogy indicative of a recent population expansion. Clade B has a more complex genealogy, consisting of several haplotypes at intermediate frequencies. The distributions of these clades consist of a mosaic with abrupt changes between some areas and gradients between other areas. Clade A predominates the Black and Aegean seas, but is present throughout the Mediterranean. Unexpectedly, new data show that clade A is also at a high frequency in the Atlantic, from Portugal to at least Senegal. Overall, the level of genetic differentiation among populations is high (F(ST)=0.148, p<0.0001), with the greatest differences between basins. AMOVA reveals four main geographical groups: Atlantic, central Mediterranean, Aegean Sea, and Black Sea. Mismatch distribution clearly indicates historical bottleneck and population expansion for clade A, while for clade B such evidence is equivocal. This difference may reflect a range expansion for both clades, but with higher gene flow (Nm values) between demes for clade A. Both contemporary and historical processes are important in shaping the complex genetic population structure of European anchovy.     

An integrative approach to species delineation incorporating different species concepts: a case study of Limnadopsis (Branchiopoda: Spinicaudata)

The unambiguous delineation and identification of species remain central problems in systematic and taxonomic studies. Species delineation depends on the data utilized and the species concept applied. In recent years, morphology‐based species delineation has been complemented by DNA sequence data, leading to an integrative taxonomy. Such integrative approaches, however, are hampered by the partial incongruence of the various data types with certain species concepts. In this study, we delineated Australian Limnadopsis species employing one mitochondrial (cytochrome c oxidase subunit I, COI) and one nuclear (elongation factor 1α, EF1α) marker and a morphological character apparently part of the specific mate recognition complex, and therefore potentially indicative of reproductive isolation. By integrating the data over various species concepts (e.g. the ‘biological’, ‘Hennigian’, ‘recognition’, ‘phylogenetic’ and ‘evolutionary’ species concepts), the delineation of most species becomes straightforward and unambiguous. Conflicts are particularly interesting as they reveal different aspects of speciation considering the various species concepts. Our study emphasizes the benefits of a truly integrative approach to taxonomy. By combining molecular data with morphological characters indicative of reproductive isolation, it is possible to delineate species integrating not only different data types, but also different underlying species concepts. Overall, 11 Limnadopsis species could be delineated, including all eight currently recognized species, and three so far undescribed species. Most species were congruently delineated under all species concepts. A strict application of the evolutionary species concept, however, would have further split L. parvispinus into two species on the basis of the COI data. In addition, Limnadopsis tatei is consistently split into two sympatrically occurring species under all applied species concepts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 575–599.