Kelp forests collapse reduces understorey seaweed ß-diversity.

BACKGROUND AND AIMS: Kelps are the primary foundation species in temperate subtidal rocky shores worldwide. However, global change is causing their decline with consequences for the organisms that rely on them. An accurate assessment of these consequences may depend on which attributes of the associated community are considered. This study shows that conventional α-diversity approaches may overlook some of these consequences compared to spatially explicit approaches such as with ß-diversity. METHODS: A 1-year seasonal study was conducted to compare the macroalgal understorey between healthy reefs with a Laminaria ochroleuca canopy and degraded reefs where the canopy collapsed years ago due to excessive fish herbivory. At each reef, the understorey seaweed assemblage was recorded in five replicate quadrats to estimate α-diversity (total richness, species density, Shannon index) and ß-diversity (intra- and inter-reef scale). KEY RESULTS: The understorey assemblage exhibited a distinct seasonal dynamic in both healthy and degraded reefs. α-Diversity attributes increased in spring and summer; turf-forming algae were particularly dominant in degraded reefs during summer. ß-Diversity also showed seasonal variability, but mostly due to the changes in degraded reefs. None of the α-diversity estimates differed significantly between healthy and degraded reefs. In contrast, spatial ß-diversity was significantly lower in degraded reefs. CONCLUSIONS: Although the loss of the kelp canopy affected the composition of the macroalgal understorey, none of the conventional indicators of α-diversity detected significant differences between healthy and degraded reefs. In contrast, small-scale spatial ß-diversity decreased significantly as a result of deforestation, suggesting that the loss of kelp canopy may not significantly affect the number of species but still have an effect on their spatial arrangement. Our results suggest that small-scale ß-diversity may be a good proxy for a more comprehensive assessment of the consequences of kelp forest decline.

Resolving the taxonomy of the Polysiphonia scopulorum complex and the Bryocladia lineage (Rhodomelaceae, Rhodophyta).

Cryptic diversity is common among marine macroalgae, with molecular tools leading to the discovery of many new species. To assign names to these morphologically similar species, the type and synonyms have to be examined, and if appropriate, new species must be described. The turf-forming red alga Polysiphonia scopulorum was originally described from Rottnest Island, Australia, and subsequently widely reported in tropical and temperate coasts based on morphological identifications. A recent study of molecular species delineation revealed a complex of 12 species in Australia, South Africa, and Europe. These species are placed in a taxonomically unresolved lineage of the tribe Polysiphonieae. The aim of this study was to resolve the genus- and species-level taxonomy of this complex and related species using molecular and morphological information. Three morphologically indistinguishable species of the complex were found at the type locality of P. scopulorum, preventing a straightforward assignment of the name to any of the molecular lineages. Therefore, we propose a molecularly characterized epitype. Polysiphonia caespitosa is reinstated for the only species found in its type locality in South Africa. We describe seven new species. Only one species of the complex can be morphologically recognized, with the other eight species indistinguishable based on morphometric analysis. The studied complex, together with another seven species currently placed in Polysiphonia and two Bryocladia species, formed a clade distinct from Polysiphonia sensu stricto. Based on observations of Bryocladia cervicornis (the generitype), we describe our seven new species in the genus Bryocladia and transfer another nine species from Polysiphonia to Bryocladia.

Gene-rich plastid genomes of two parasitic red algal species, Laurencia australis and L. verruciformis (Rhodomelaceae, Ceramiales), and a taxonomic revision of Janczewskia.

Parasitic red algae are an interesting system for investigating the genetic changes that occur in parasites. These parasites have evolved independently multiple times within the red algae. The functional loss of plastid genomes can be investigated in these multiple independent examples, and fine-scale patterns may be discerned. The only plastid genomes from red algal parasites known so far are highly reduced and missing almost all photosynthetic genes. Our study assembled and annotated plastid genomes from the parasites Janczewskia tasmanica and its two Laurencia host species (Laurencia elata and one unidentified Laurencia sp. A25) from Australia and Janczewskia verruciformis, its host species (Laurencia catarinensis), and the closest known free-living relative (Laurencia obtusa) from the Canary Islands (Spain). For the first time we show parasitic red algal plastid genomes that are similar in size and gene content to free-living host species without any gene loss or genome reduction. The only exception was two pseudogenes (moeB and ycf46) found in the plastid genome of both isolates of J. tasmanica, indicating potential for future loss of these genes. Further comparative analyses with the three highly reduced plastid genomes showed possible gene loss patterns, in which photosynthetic gene categories were lost followed by other gene categories. Phylogenetic analyses did not confirm monophyly of Janczewskia, and the genus was subsumed into Laurencia. Further investigations will determine if any convergent small-scale patterns of gene loss exist in parasitic red algae and how these are applicable to other parasitic systems.

Molecular analyses of turf algae reveal a new species and an undetected introduction in the Pterosiphonieae (Rhodomelaceae, Rhodophyta).

Introduced seaweeds and undescribed species often remain undetected because marine regional floras are as yet poorly understood. DNA sequencing facilitates their detection, but databases are incomplete, so their improvement will continue to lead the discovery of these species. Here we aim to clarify the taxonomy of two turf-forming red algal Australian species that morphologically resemble the European Aphanocladia stichidiosa. We also aim to elucidate whether either of these species could have been introduced in Europe or Australia. We studied their morphology, analyzed 17 rbcL sequences of European and Australian specimens, examined their generic assignment using a phylogeny based on 24 plastid genomes, and investigated their biogeography using a taxon-rich phylogeny including 52 rbcL sequences of species in the Pterosiphonieae. The rbcL sequences of one of the Australian species were identical to A. stichidiosa from Europe, considerably expanding its known distribution. Unexpectedly, our phylogenetic analyses resolved this species in the Lophurella clade rather than in Aphanocladia and the new combination L. stichidiosa is proposed. The other Australian species is described as L. pseudocorticata sp. nov. Although L. stichidiosa was originally described in the Mediterranean ca. 70 years ago, our phylogenetic analyses placed it in a lineage restricted to the southern hemisphere, showing that it is native to Australia and introduced to Europe. This study confirms that further work using molecular tools is needed to characterize seaweed diversity, especially among the poorly explored algal turfs, and showcases the usefulness of phylogenetic approaches to uncover introduced species and to determine their native ranges.

Phylogenomic analysis of pseudocryptic diversity reveals the new genus Deltalsia (Rhodomelaceae, Rhodophyta).

Molecular analyses, in combination with morphological studies, provide invaluable tools for delineating red algal taxa. However, molecular datasets are incomplete and taxonomic revisions are often required once additional species or populations are sequenced. The small red alga Conferva parasitica was described from the British Isles in 1762 and then reported from other parts of Europe. Conferva parasitica was traditionally included in the genus Pterosiphonia (type species P. cloiophylla in Schmitz and Falkenberg 1897), based on its morphological characters, and later transferred to Symphyocladia and finally to Symphyocladiella using molecular data from an Iberian specimen. However, although morphological differences have been observed between specimens of Symphyocladiella parasitica from northern and southern Europe they have yet to be investigated in a phylogenetic context. In this study, we collected specimens from both regions, studied their morphology and analyzed rbcL and cox1 DNA sequences. We determined the phylogenetic position of a British specimen using a phylogenomic approach based on mitochondrial and plastid genomes. Northern and southern European populations attributed to S. parasitica represent different species. Symphyocladiella arecina sp. nov. is proposed for specimens from southern Europe, but British specimens were resolved as a distant sister lineage to the morphologically distinctive Amplisiphonia, so we propose the new genus Deltalsia for this species. Our study highlights the relevance of using materials collected close to the type localities for taxonomic reassessments, and showcases the utility of genome-based phylogenies for resolving classification issues in the red algae.

Meridionella gen. nov., a New Genus of Cystocloniaceae (Gigartinales, Rhodophyta) from the Southern Hemisphere, Including M. obtusangula comb. nov. and M. antarctica sp. nov.

The classification of Cystoclonium obtusangulum has been questioned since the species was first described by Hooker and Harvey as Gracilaria? obtusangula. The objective of this study was to provide the first comprehensive taxonomic analysis of Cystoclonium obtusangulum, based on DNA sequences coupled with morphological observations made on syntype specimens and new collections. Sequence divergences of rbcL, UPA, and COI-5P, and maximum-likelihood phylogenies for rbcL and 18S demonstrated that specimens identified as Cystoclonium obtusangulum represent a clade of two distinct species that are distantly related to the generitype Cystoclonium purpureum. A new genus, Meridionella gen. nov., is proposed for this clade. The two species placed in this new genus were morphologically indistinguishable cryptic species, but have disjunct distributions, with Meridionella obtusangula comb. nov. found from temperate to cold coasts of South America and the Falkland Islands and Meridionella antarctica sp. nov., occurring in Antarctic waters. Vegetative and reproductive characters of Meridionella gen. nov. are described, and implications of our results for the biogeography of the family Cystocloniaceae are discussed.

A multidisciplinary approach to identify priority areas for the monitoring of a vulnerable family of fishes in Spanish Marine National Parks.

BACKGROUND: Syngnathid fishes (Actinopterygii, Syngnathidae) are flagship species strongly associated with seaweed and seagrass habitats. Seahorses and pipefishes are highly vulnerable to anthropogenic and environmental disturbances, but most species are currently Data Deficient according to the IUCN (2019), requiring more biological and ecological research. This study provides the first insights into syngnathid populations in the two marine Spanish National Parks (PNIA-Atlantic- and PNAC-Mediterranean). Fishes were collected periodically, marked, morphologically identified, analysed for size, weight, sex and sexual maturity, and sampled for stable isotope and genetic identification. Due the scarcity of previous information, habitat characteristics were also assessed in PNIA. RESULTS: Syngnathid diversity and abundance were low, with two species identified in PNIA (Hippocampus guttulatus and Syngnathus acus) and four in PNAC (S. abaster, S. acus, S. typhle and Nerophis maculatus). Syngnathids from both National Parks (NP) differed isotopically, with much lower δ15N in PNAC than in PNIA. The dominant species were S. abaster in PNAC and S. acus in PNIA. Syngnathids preferred less exposed sites in macroalgal assemblages in PNIA and Cymodocea meadows in PNAC. The occurrence of very large specimens, the absence of small-medium sizes and the isotopic comparison with a nearby population suggest that the population of Syngnathus acus (the dominant syngnathid in PNIA) mainly comprised breeders that migrate seasonally. Mitochondrial cytochrome b sequence variants were detected for H. guttulatus, S. acus, and S. abaster, and a novel 16S rDNA haplotype was obtained in N. maculatus. Our data suggest the presence of a cryptic divergent mitochondrial lineage of Syngnathus abaster species in PNAC. CONCLUSIONS: This is the first multidisciplinary approach to the study of syngnathids in Spanish marine NPs. Habitat preferences and population characteristics in both NPs differed. Further studies are needed to assess the occurrence of a species complex for S. abaster, discarding potential misidentifications of genus Syngnathus in PNAC, and evaluate migratory events in PNIA. We propose several preferential sites in both NPs for future monitoring of syngnathid populations and some recommendations for their conservation.

Extensive cryptic diversity in the widely distributed Polysiphonia scopulorum (Rhodomelaceae, Rhodophyta): Molecular species delimitation and morphometric analyses.

Our knowledge of seaweed diversity and biogeography still largely relies on information derived from morphological identifications, but the use of molecular tools is revealing that cryptic diversity is common among algae. Polysiphonia scopulorum is a turf-forming red alga widely reported in tropical and temperate coasts worldwide. The only study based on material collected from its Australian type locality and the Iberian Peninsula indicates that it is a species complex, but the extent of cryptic diversity across its geographical range is not known. To investigate the species diversity in P. scopulorum, the geographical distribution of species-level lineages and their morphological characterization, we collected 135 specimens from Australia, South Africa and southern Europe. Two gene datasets (cox1 and rbcL) were used to delimit species using three methods (GMYC, PTP, ABGD), leading to a consensus result that our collections of the P. scopulorum complex comprise 12 species. Five of these species were resolved in a highly supported clade, while the other seven species were related to other taxonomically accepted species or in unresolved parts of the tree. Morphometric and statistical analysis of a set of ten quantitative characters showed that there are no clear morphological correlates of species boundaries, demonstrating true cryptic diversity in the P. scopulorum complex. Distribution patterns of the 12 species were variable, ranging from species only known from a single site to species with a wide distribution spanning three continents. Our study indicates that a significant level of undiscovered cryptic diversity is likely to be found in algal turfs, a type of seaweed community formed by small entangled species.

Morphological evolution and classification of the red algal order Ceramiales inferred using plastid phylogenomics.

The order Ceramiales contains about one third of red algal diversity and it was classically classified into four families according to morphology. The first phylogenies based on one or two molecular markers were poorly supported and failed to resolve these families as monophyletic. Nine families are currently recognized, but relationships within and among them are poorly understood. We produced a well-resolved phylogeny for the Ceramiales using plastid genomes for 80 (28 newly sequenced) representative species of the major lineages. Three of the previously recognized families were resolved as independent monophyletic lineages: Ceramiaceae, Wrangeliaceae and Rhodomelaceae. By contrast, our results indicated that the other six families require reclassification. We propose the new order Inkyuleeales, a new circumscription of the Callithamniaceae to include the Spyridiaceae, and a new concept of the Delesseriaceae that includes the Sarcomeniaceae and the Dasyaceae. We also investigated the evolution of the thallus structure, which has been important in the classical delineation of families. The ancestor of the Ceramiales was a monosiphonous filament that evolved into more complex morphologies several times independently during the evolutionary history of this hyperdiverse lineage.

Widely distributed red algae often represent hidden introductions, complexes of cryptic species or species with strong phylogeographic structure.

Despite studies suggesting that most seaweeds are poor dispersers, many red algal species are reported to have circumglobal distributions. Such distributions have mostly been based on morphological identifications, but molecular data have revealed a range of issues with morphologically defined species boundaries. Consequently, the real distribution of such reportedly circumglobal species must be questioned. In this study, we analyzed molecular data sets (rbcL gene) of nine species in the Rhodomelaceae for which samples were available from widely spaced geographical locations. Three overall patterns were identified: (i) species showing strong phylogeographic structure (i.e., phylogenetic similarity correlates with geographical provenance), often to the point that populations from different locations could be considered as different species (Lophosiphonia obscura, Ophidocladus simpliciusculus, Polysiphonia villum, and Xiphosiphonia pinnulata); (ii) species with a broad distribution that is explained, in part, by putative human-mediated transport (Symphyocladia dendroidea and Polysiphonia devoniensis); and (iii) non-monophyletic complexes of cryptic species, most with a more restricted distribution than previously thought (Herposiphonia tenella, Symphyocladia dendroidea, and the Xiphosiphonia pennata complex that includes the species Xiphosiphonia pinnulata and Symphyocladia spinifera). This study shows that widely distributed species are the exception in marine red algae, unless they have been spread by humans.

Analysis of chloroplast genomes and a supermatrix inform reclassification of the Rhodomelaceae (Rhodophyta).

With over a thousand species, the Rhodomelaceae is the most species-rich family of red algae. While its genera have been assigned to 14 tribes, the high-level classification of the family has never been evaluated with a molecular phylogeny. Here, we reassess its classification by integrating genome-scale phylogenetic analysis with observations of the morphological characters of clades. In order to resolve relationships among the main lineages of the family we constructed a phylogeny with 55 chloroplast genomes (52 newly determined). The majority of branches were resolved with full bootstrap support. We then added 266 rbcL, 125 18S rRNA gene and 143 cox1 sequences to construct a comprehensive phylogeny containing nearly half of all known species in the family (407 species in 89 genera). These analyses suggest the same subdivision into higher-level lineages, but included many branches with moderate or poor support. The circumscription for nine of the 13 previously described tribes was supported, but the Lophothalieae, Polysiphonieae, Pterosiphonieae and Herposiphonieae required revision, and five new tribes and one resurrected tribe were segregated from them. Rhizoid anatomy is highlighted as a key diagnostic character for the morphological delineation of several lineages. This work provides the most extensive phylogenetic analysis of the Rhodomelaceae to date and successfully resolves the relationships among major clades of the family. Our data show that organellar genomes obtained through high-throughput sequencing produce well-resolved phylogenies of difficult groups, and their more general application in algal systematics will likely permit deciphering questions about classification at many taxonomic levels.