Ignacio Bárbara

SYSTEMATICS OF GRATELOUPIA FILICINA (HALYMENIACEAE, RHODOPHYTA), BASED ON rbcL SEQUENCE ANALYSES AND MORPHOLOGICAL EVIDENCE, INCLUDING THE REINSTATEMENT OF G. MINIMA AND THE DESCRIPTION OF G. CAPENSIS SP. NOV.

Grateloupia filicina (C. Agardh) Lamouroux, originally described from the Mediterranean Sea, has long been considered a textbook example of a marine red alga with a cosmopolitan distribution. An rbcL‐based molecular phylogeny, encompassing samples covering the entire geographic distribution of the species, revealed a plethora of “cryptic” species, whereby the presence of genuine G. filicina is limited to the Mediterranean basin. The phylogeny revealed a strong biogeographic imprint, with specimens from temperate regions resolved in clades composed of species inhabiting the same geographic region. Presence of widely divergent morphologies in the temperate clades indicated that several lineages have converged independently to a G. filicina‐type morphology. Tropical representatives are resolved in a single clade with very uniform G. filicina‐type morphology and pairwise sequence divergences that are lower than the average divergence observed in temperate lineages. This, combined with a lack of clear geographic structure among the tropical lineages, may indicate a more recent divergence with long‐range dispersal capacities. Violations to the biogeographic signal in temperate lineages seemed to be due to either inadequate taxonomy or recent introductions. Grateloupia minima P. & H. Crouan, a taxon placed in synonymy under G. filicina, is reinstated as a separate species distributed in the northeast Atlantic Ocean. Grateloupia capensis sp. nov. is described to accommodate specimens from South Africa with a G. filicina‐type morphology, and G. filicina var. luxurians is elevated to species status. Morphological and anatomical characters were put forward that support the distinctiveness of these three distinct species.

Checklist of benthic marine algae and cyanobacteria of northern Portugal

The northern Portuguese coast is a biogeographic transition zone where many macroalgal species have their distribution limits; it is thus a particularly interesting region for investigating species distribution shifts. An updated and complete list of species for this region is not available in spite of its baseline importance for comparative studies with past and present data. Based on new records, literature references, and herbarium data, we provide an updated checklist of the benthic marine algae of the northern Portuguese coast. This checklist includes 346 species: 26 Cyanobacteria, 200 Rhodophyta, 70 Ochrophyta, and 50 Chlorophyta. From these, 21 species are new records for the Portuguese coast (Lyngbya aestuarii, Lyngbya semiplena, Microcoleus acutirostris, Myxosarcina gloeocapsoides, Aiolocolax pulchella, Antithamnion densum, Antithamnion villosum, Antithamnionella spirographidis, Dasya sessilis, Furcellaria lumbricalis, Neosiphonia harveyi, Porphyrostromium boryanum, Chorda filum, Dictyopteris ambigua, Sphacelaria rigidula, Undaria pinnatifida, Vaucheria coronata, Vaucheria velutina, Ulothrix implexa, Ulva scandinavica, and Umbraulva olivascens) and 33 were recorded for the first time in the north of Portugal. Alien species have increased in number and extended their distribution range over the last 10 years in the study area. Distribution shifts of northern cold water species with southern distribution limit in the north of Portugal were not consistent among species.

A Multilocus Species Delimitation Reveals a Striking Number of Species of Coralline Algae Forming Maerl in the OSPAR Maritime Area

Maerl beds are sensitive biogenic habitats built by an accumulation of loose-lying, non-geniculate coralline algae. While these habitats are considered hot-spots of marine biodiversity, the number and distribution of maerl-forming species is uncertain because homoplasy and plasticity of morphological characters are common. As a result, species discrimination based on morphological features is notoriously challenging, making these coralline algae the ideal candidates for a DNA barcoding study. Here, mitochondrial (COI-5P DNA barcode fragment) and plastidial (psbA gene) sequence data were used in a two-step approach to delimit species in 224 collections of maerl sampled from Svalbard (78°96’N) to the Canary Islands (28°64’N) that represented 10 morphospecies from four genera and two families. First, the COI-5P dataset was analyzed with two methods based on distinct criteria (ABGD and GMYC) to delineate 16 primary species hypotheses (PSHs) arranged into four major lineages. Second, chloroplast (psbA) sequence data served to consolidate these PSHs into 13 secondary species hypotheses (SSHs) that showed biologically plausible ranges. Using several lines of evidence (e.g. morphological characters, known species distributions, sequences from type and topotype material), six SSHs were assigned to available species names that included the geographically widespread Phymatolithon calcareum, Lithothamnion corallioides, and L. glaciale; possible identities of other SSHs are discussed. Concordance between SSHs and morphospecies was minimal, highlighting the convenience of DNA barcoding for an accurate identification of maerl specimens. Our survey indicated that a majority of maerl forming species have small distribution ranges and revealed a gradual replacement of species with latitude.

Biological importance of an Atlantic European maërl bed off Benencia Island (northwest Iberian Peninsula)

We studied the conservation status of a maerl bed off Benencia Island (NW Spain) over a 2-year period using SCUBA and dredging. The maerl bed, which includes a maerl beach, extended from the intertidal to subtidal zones (18 m), and occupied an area of 215 ha. It was composed of a pure unattached coralline algal deposit occasionally mixed with broken shells. The area estimated for the highest maerl cover (76–100%) was greater than reported in previous research. The living maerl layer reached 15 cm in depth and the living/dead maerl ratio was high (80–100% living maerl cover). The dominant maerl-forming species was Phymatolithon calcareum, although unattached plants of Mesophyllum sp. reaching 10 cm in diameter were found in two sites. Both maerl species are fruticose. The proportion of discoidal specimens of P. calcareum was related to depth. The associated flora comprised 137 species whose seasonal variations were very marked, with high floristic richness in summer (71 species) and low in winter (35 species). Crustose and turf-like species were the dominant floral components throughout the year, whereas the presence of other species was restricted to specific periods. We propose that Benencia Island be included in future Atlantic Iberian maerl bed conservation schemes.

Lampisiphonia iberica gen. et sp. nov. (Ceramiales, Rhodophyta) based on morphology and molecular evidence

Bárbara I., Choi H.-G., Secilla A., Díaz-Tapia P., Gorostiaga J.M., Seo T.-K., Jung M.-Y. and Berecibar E. 2013. Lampisiphonia iberica gen. et sp. nov. (Ceramiales, Rhodophyta) based on morphology and molecular evidence. Phycologia 52: 137–155. DOI: 10.2216/12-009.1 Lampisiphonia iberica gen. et sp. nov. is described on the basis of specimens collected from subtidal rocky bottom habitats on the Atlantic coast of the Iberian Peninsula. The new genus was distinguished by an erect habit, pseudodichotomous branching, and 9–11 pericentral cells. Plants were bright red to brown-red in colour, 3–6 cm high, firm at the base but ultimate divisions soft and flaccid. Cortication was thick but restricted to the base of large thalli. Plants were attached to the substratum by discoid holdfasts with the tips of decumbent branches reattaching by secondary discoid holdfasts or rhizoids cut off from pericentral cells. Trichoblasts and scar cells were absent and the branching was exogenous. Tetrasporangia were arranged in straight series of up to 15 segments. Sexual structures were not observed. Lampisiphonia was separated from other groups and genera of Polysiphonia sensu lato and the tribe Polysiphonieae by a combination of features that include the absence of trichoblasts and presence of a compact basal cortication. Furthermore, Lampisiphonia had tetrasporangia in a straight series, a feature to date considered unique to Polysiphonia sensu stricto. The phylogenetic relationship of Lampisiphonia among the three resolved lineages of the Polysiphonia sensu lato was equivocal in our analyses and it was not clearly distinct from the Neosiphonia group and the multipericental group in morphological and molecular characters. Nevertheless, monophyly of Lampisiphonia and the Polysiphonia group was statistically rejected in small-subunit ribosomal DNA, rbcL and combined data with the Shimodaira–Hasegawa test. We therefore proposed Lampisiphonia as a new genus.

MESOPHYLLUM SPHAERICUM SP. NOV. (CORALLINALES, RHODOPHYTA): A NEW MAËRL-FORMING SPECIES FROM THE NORTHEAST ATLANTIC1

Mesophyllum sphaericum sp. nov. is described based on spherical maërl individuals (up to 10 cm) collected in a shallow subtidal maërl bed in Galicia (NW Spain). The thalli of these specimens are radially organized, composed of arching tiers of compact medullary filaments. Epithallial cells have flattened to rounded outermost walls, and they occur in a single layer. Subepithallial initials are as long as, or longer than the daughter cells that subtend them. Cell fusions are abundant. Multiporate asexual conceptacles are protruding, mound‐like with a flattened pore plate, lacking a peripheral raised rim. Filaments lining the pore canal and the conceptacle roof are composed of five to six cells with straight elongate and narrow cells at their base. Carposporangial conceptacles are uniporate, protruding, and conical. Spermatangial conceptacles were not observed. Molecular results placed M. sphaericum near to M. erubescens, but M. sphaericum is anatomically close to M. canariense. The examination of the holotype and herbarium specimens of M. canariense indicated that both species have pore canal filaments with elongate basal cells, but they differ in number of cells (five to six in M. sphaericum vs. four in M. canariense). Based on the character of pore canal filaments, M. canariense shows similarities with M. erubescens (three to five celled). The outermost walls of epithallial cells of M. canariense are flared compared to the round to flattened ones of M. erubescens, the latter being widely accepted for the genus Mesophyllum. The addition of M. sphaericum as new maërl‐forming species suggests that European maërl beds are more biodiverse than previously understood.

Characterization of Grateloupia lanceola (Halymeniales, Rhodophyta), an obscure foliose Grateloupia from the Iberian Peninsula, based on morphology, comparative sequence analysis and mycosporine-like amino acid composition

Foliose Grateloupia species are among the most commonly reported introduced species of red algae in European waters. Unequivocal identification at species level, however, has proven exceedingly difficult owing to a relatively low number of clear-cut diagnostic characters and considerable morphological plasticity. Because of their morphological similarity many of these species were placed in synonymy by subsequent generations of phycologists. In the present paper we demonstrate that Gratelopia lanceola, a native European species, is distinct from G. turuturu, a western Pacific alga introduced in European waters. These conclusions are based on comparative gene sequences (rbcL and LSU rDNA) as well as morphology and mycosporine-like amino acid (MAA) signatures. Even though support was largely lacking from rbcL and the combined analysis, G. lanceola was clearly separated from G. turuturu as well as other foliose species. These data, together with earlier accounts on genuine G. doryphora and G. schizophylla, indicate that foliose Grateloupia species display a clear geographic structuring, which has only become obscured by the recent introduction of morphologically similar species (pseudo-cryptic species) along Atlantic coasts and in the Mediterranean Sea. Grateloupia lanceola also showed a different MAA composition when compared with G. turuturu, regardless of spatial-temporal influences. The concentrations were about 3 mg g−1 DW and about 5 mg g−1 DW in G. turuturu and G. lanceola, respectively. The main MAA in Grateloupia lanceola was porphyra-334, which represented almost 100% of these compounds. Only some traces (<1%) of shinorine and palythine were found in this species. On the other hand, the dominant MAA in G. turuturu was shinorine, which represented approximately 92% of the total MAA content; palythine contributed about 7.5% while traces of asterina-330 were also found.

Seasonal patterns in the maërl community of shallow European Atlantic beds and their use as a baseline for monitoring studies

A study of three shallow Atlantic maërl beds (3–6 m depth) in NW Spain (Galicia) sampled beds every 1.5 months for a year. At each study site, temporal variation in the associated flora and two parameters, temperature and photosynthetic photon flux density (PPFD), were recorded in situ and means were calculated for each period. The range of mean periodic temperatures was 11.9–17.5°C, increasing in late spring–summer and decreasing to <12°C in winter. Mean PPFD was 24–160 µmol photons m−2 s−1; the maximum was recorded in spring (up to 571 µmol photons m−2 s−1). The variation in temperature and PPFD was correlated with seasonal changes in the flora. The composition of the associated flora at Benencia Island (Ría de Arousa) showed a strong correlation with day length while at Tambo Island (Ría de Pontevedra), it was correlated with temperature. A total of 127 species was recorded (in seven functional groups), annual algae being the most abundant group. The highest species richness and total percentage cover occurred in spring and summer, and the lowest in autumn and winter. Significant seasonal differences were detected at each site, particularly between summer and autumn–winter, due to variation in cover of the foliose species Ulva rigida and Dictyota dichotoma. We propose that future monitoring of European Atlantic maërl beds should include several study areas and two sampling seasons (preferably summer and late autumn–winter).

Status, trends and drivers of kelp forests in Europe: an expert assessment

A comprehensive expert consultation was conducted in order to assess the status, trends and the most important drivers of change in the abundance and geographical distribution of kelp forests in European waters. This consultation included an on-line questionnaire, results from a workshop and data provided by a selected group of experts working on kelp forest mapping and eco-evolutionary research. Differences in status and trends according to geographical areas, species identity and small-scale variations within the same habitat where shown by assembling and mapping kelp distribution and trend data. Significant data gaps for some geographical regions, like the Mediterranean and the southern Iberian Peninsula, were also identified. The data used for this study confirmed a general trend with decreasing abundance of some native kelp species at their southern distributional range limits and increasing abundance in other parts of their distribution (Saccharina latissima and Saccorhiza polyschides). The expansion of the introduced species Undaria pinnatifida was also registered. Drivers of observed changes in kelp forests distribution and abundance were assessed using experts’ opinions. Multiple possible drivers were identified, including global warming, sea urchin grazing, harvesting, pollution and fishing pressure, and their impact varied between geographical areas. Overall, the results highlight major threats for these ecosystems but also opportunities for conservation. Major requirements to ensure adequate protection of coastal kelp ecosystems along European coastlines are discussed, based on the local to regional gaps detected in the study.

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.