Ecosystem functioning impacts of the invasive seaweed Sargassum muticum (Fucales,Phaeophyceae)

Ongoing changes in natural diversity due to anthropogenic activities can alter ecosystem functioning. Particular attention has been given to research on biodiversity loss and how those changes can affect the functioning of ecosystems, and, by extension, human welfare. Few studies, however, have addressed how increased diversity due to establishment of nonindigenous species (NIS) may affect ecosystem function in the recipient communities. Marine algae have a highly important role in sustaining nearshore marine ecosystems and are considered a significant component of marine bioinvasions. Here, we examined the patterns of respiration and light‐use efficiency across macroalgal assemblages with different levels of species richness and evenness. Additionally, we compared our results between native and invaded macroalgal assemblages, using the invasive brown macroalga Sargassum muticum (Yendo) Fensholt as a model species. Results showed that the presence of the invader increased the rates of respiration and production, most likely as a result of the high biomass of the invader. This effect disappeared when S. muticum lost most of its biomass after senescence. Moreover, predictability–diversity relationships of macroalgal assemblages varied between native and invaded assemblages. Hence, the introduction of high‐impact invasive species may trigger major changes in ecosystem functioning. The impact of S. muticum may be related to its greater biomass in the invaded assemblages, although species interactions and seasonality influenced the magnitude of the impact.     

Haplotypic differentiation between seasonal populations of Sargassum horneri (Fucales,Phaeophyceae) in Japan

Conspecific populations with different life‐cycle seasonality, particularly of their reproductive season, have been reported for many seaweed species. However, the number of genetic analyses of such seasonal populations is limited. Herein, based on the mitochondrial cytochrome oxidase subunit 3 gene (cox3) haplotype, we evaluated the genetic diversity of winter (January–March) and spring (April–June) fertile populations of the brown alga Sargassum horneri in Sado Island, Japan. Obviously, dominant cox3 haplotypes were different between seasons (even at a single site), and the N _ST values indicated the presence of a strong genetic differentiation between the two seasonal populations. AMOVA analyses confirmed that most of the genetic diversity was between seasons rather than between regions. Herein, the possibility of allochronic isolation is discussed. Considering the phylogeny of the mitochondrial cox3 DNA sequence, autumn or winter seasonal populations such as those in this investigation have evolved independently at least twice in the species. The present study shows that a shift in breeding season could be expected to conserve the genetic diversity of S. horneri in a certain region.     

Born migrators: Historical biogeography of the cosmopolitan family Cannabaceae

Dispersal scenarios have been favored over tectonic vicariance as an explanation for disjunct distributions in many plant taxa during the last two decades. However, this argument has been insufficiently addressed in cosmopolitan groups showing disjunct patterns in both the temperate and tropical regions. In this study, we used the Cannabaceae, an angiosperm family distributed in tropical and temperate regions of both the New World and the Old World, to explore the role of dispersal in shaping disjunct patterns and species diversification of cosmopolitan plants. We reconstructed the phylogenetic relationships of all 10 genera and 75 species of Cannabaceae (ca. 64.1% of recognized species) based on eight DNA regions. Based on fossil calibrations, we estimated the divergence times and net diversification rates. We further inferred the ancestral geographical ranges with several models and compared the fitness of different models. The Cannabaceae and most genera were strongly supported as monophyletic except for the Parasponia being embedded within the Trema. The Celtis were resolved into two strongly supported clades primarily corresponding to temperate and tropical regions. We inferred that the Cannabaceae originated at ca. 93 Ma, and that subsequent rampant and widespread dispersals shaped the intercontinentally disjunct distribution of the Cannabaceae. Dispersal coincides with adaptation to drier and colder climate in the Northern Hemisphere, or humid and warm climate in the tropical regions, followed by rapid species diversification. This study advances our understanding as to the formation of distribution patterns and species diversification of a plant family with tropical to temperate disjunct distributions.     

Egg release and germling development in Sargassum horneri (Fucales, Phaeophyceae)

The mature female conceptacle of Sargassum horneri (Turner) C. Agardh has an ostiole filled with a gelatinous plug. The oogonium in the conceptacle has cell walls that can be differentiated into a dense outer and a less dense inner microfibrillar layer. Just prior to egg release, stalk material is produced inside the outer layer and the inner layer disappears. At this stage the gelatinous plug is extruded and mucilage is released through the ostiole. The released eggs are retained on the receptacle by the stalk and are surrounded by a large amount of the mucilage. Three-celled germlings form a primary wall with a polylamellated structure of microfibril layers. In multicellular germlings that have differentiated into thallus and rhizoids, the peripheral thallus cells have an outer cell wall consisting of a microfibril layer under the primary wall, while the cell wall of the rhizoid tip has an amorphous structure. The germlings are released from the stalk and become attached to the substratum by an adhesive substance secreted from rhizoidal cells.     

Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae,Heterokontophyta) in northwestern Pacific

Sargassum hemiphyllum is commonly found in Japan and Korea, with a variety, var. chinense, that is found distributed in the southern Chinese coast. We previously reported distinct genetic differentiation between the two taxa based on the PCR‐RFLP data of plastid RubiscoL‐S spacer. The present study aims at elucidating the phylogeographic pattern of S. hemiphyllum based on more markers in the nuclear and extranuclear genomes, with a view to reveal the occurrence of hybridization. The two allopatrically distributed taxa were found to be genetically distinct in nuclear ITS2, plastidial Rubisco (Rbc) and mitochondrial TrnW_I (Trn) spacers. Their divergence was postulated to be attributable to the vicariant event which resulted from the isolation of the Sea of Japan during the late Miocene (6.58–11.25 Mya). Divergence within both S. hemiphyllum and the chinense variety was observed based on Trn spacer, while the divergence in S. hemiphyllum was further confirmed in Rbc spacer. This divergence appears to correspond to the separation of the Japanese populations between the Sea of Japan and the Pacific that occurred around 0.92–2.88 Mya (the early Pleistocene). The presence of an ITS2 clone resembling var. chinense sequences in a Japanese population of S. hemiphyllum (JpNS) raises the possibility of the introgression of var. chinense individuals into S. hemiphyllum population. Compared to that between S. hemiphyllum and the chinense variety, hybridization among the Japanese and Korean populations of S. hemiphyllum is highly probable as all these individuals share a pool of nuclear ITS2 sequences, possibly attributable to incomplete concerted evolution of ITS2.     

Sargassum boreale sp. nov. (Fucales, Phaeophyceae) from Hokkaido, Japan

A new species, Sargassum boreale Yoshida et Horiguchi is described. It belongs to the subgenus Bactrophycus section Teretia, with cylindrical receptacles and is distinct from Sargassum confusum C. Agardh, S. pallidum (Turner) C. Agardh and Sargassum microceratium (Turner) C. Agardh in having a rather elongated stem with smooth surface and distantly issuing main branches, with narrow leaves. The distinction between S. boreale and these species is also revealed by a difference in internal transcribed spacer 2 (ITS‐2) sequences. In addition to the base substitutions, the existence of a large gap in S. boreale distinguishes this species from others. Sargassum boreale is distributed around Hokkaido and Saghalien to 50°N latitude. A key to the species of section Teretia is provided.     

Comparison of antifouling properties of native and invasive Sargassum (Fucales,Phaeophyceae) species

The invasiveness of algal species can be facilitated by chemo-ecological traits that allow the establishment of invasive species in a highly competitive environment. Anti-bacterial, anti-quorum sensing, anti-diatom and anti-larval properties of the invasive brown macroalga Sargassum muticum and three native Sargassum species from Oman waters were compared in laboratory and field experiments to assess whether these traits have the potential to facilitate the invasion process. Only the extract of S. muticum inhibited bacterial growth of four marine bacterial strains and quorum sensing in the reporter strain Chromobacterium violaceum CV017. Settlement, growth and survival of the diatom Cylindrotheca closterium and larvae of the bryozoan Bugula neritina were significantly inhibited by all Sargassum extracts in laboratory experiments. However, crude extracts of S. muticum had the strongest antifouling effect. Natural tissue-level concentrations of S. muticum extract reduced diatom density to about 20% compared with the controls. Larval mortality increased by 80–90% compared with controls with S. muticum extract diluted to one-third natural levels. Significant anti-diatom activity of S. muticum was confirmed in the field experiments with Sargassum extracts embedded in a phytagel matrix. Comparison of non-polar compounds by gas chromatography–mass spectrometry demonstrated that S. muticum extracts had overall fewer secondary metabolites but more species-unique compounds than extracts of native Sargassum spp. The greater antifouling defence of invasive vs. native Sargassum species indicates a selective trait that may contribute to the invasion success of S. muticum.     

Testing systematic concepts of Sargassum (Fucales, Phaeophyceae) using portions of the rbcLS operon

The taxonomic and phylogenetic concepts within the Sargassum C. Agardh (Sargassaceae) species complex were evaluated through molecular phylogenetic analyses using portions of the chloroplast encoded rbcLS Operon. According to more conservative sequences (rbcL), Turbinaria (Turner) J. Agardh is a close and well‐supported sister lineage to the Sargassum species complex and an appropriate external outgroup for analyses of subgenera and subsections within Sargassum. Both rbcL and more rapidly evolving rbcLS spacer sequences indicated that the East Asiatic genus Myagropsis (Mertens et Turner) Fensholt, along with Sargassum sinicola Setchell et Gardner, represent the closest lineage to Sargassum and form appropriate internal outgroups. The rbcLS spacer region supported three of four subgeneric designations by J. Agardh and sectional levels within the subgenus Sargassum. However, some aspects of Agardh's system were not supported: many of the subsectional ranks or the phyletic concepts; Phyllotrichia was not monophyletic as a subgenus, and its species were also not the most ancestral of Sargassum; and subgenus Sargassum was not the most derived subgenus within the genus. This modern phylogeny suggests a deep evolutionary history for subgenus Sargassum with rapid speciation in closely related subsections and series, and a sister relationship between subgenera Arthrophycus and Bactrophycus.     

Distributional range shifts of Western Atlantic benthic Sargassum species (Fucales,Phaeophyceae) under future climate change scenarios

Climate change is altering the world’s marine biota, in particular, their geographic distribution. Sargassum species are foundation species that play critical ecological roles in tropical benthic communities, providing food, habitat heterogeneity and shelter for a wide range of marine organisms. To understand how future changes in abiotic variables could affect the distribution of Sargassum species along the Western Atlantic Ocean, we performed Ecological Niche Models (ENM) for 12 benthic Sargassum species. We projected present and future habitat suitability distributions under the RCP 4.5 and RCP 8.5 IPCC scenarios. We fit ENM and created ensembles from different algorithms. Our results predict changes in species latitudinal range (niche suitability) in the order of 0.5˚ to 8.1˚ northward, and 0˚ to 5.5˚ southward. Six species are likely to reduce their suitability area from 10% to 80%, while other six species are likely to expand their suitability area from 4% to 168%. Overall, changes in suitability area and latitudinal ranges will increase at larger latitudes for most species while suitability areas will decrease at lower latitudes for half of the species. This pattern is consistent with the expected tropicalization of temperate latitudes following global warming. Such changes can produce considerable losses in ecosystem services maintained by healthy Sargassum beds, particularly at lower latitudes. Our findings highlight the need to improve Sargassum conservation policies and management strategies to avoid the negative effects caused by losses in Sargassum forests.     

Boomeranging around Australia: Historical biogeography and population genomics of the anti‐equatorial fish Microcanthus strigatus (Teleostei: Microcanthidae)

The geographic distributions of marine fishes have been shaped by ancient vicariance and ongoing dispersal events. Some species exhibit anti‐equatorial distributions, inhabiting temperate regions on both sides of the tropics while being absent from equatorial latitudes. The perciform fish Microcanthus strigatus (the stripey) exhibits such a distribution with disjunct populations occurring in East Asia, Hawaii, Western Australia, and the southwest Pacific. Here, we examine the historical biogeography and evolutionary history of M. strigatus, based on more than 80 specimens sampled from the four major populations. We analysed 36 morphological characters, three mitochondrial markers, and two sets of 7,120 and 12,771 single‐nucleotide polymorphisms from the nuclear genome. Our results suggest that M. strigatus represents a cryptic species complex comprising at least two genetically distinct populations worthy of species‐level recognition, with one population exhibiting strong genetic structuring but with intermittent, historical gene flow. We provide evidence for a southwest Pacific origin for the ancestral Microcanthus and explain how past connectivity between these regions might have given rise to the relationships observed in present‐day marine fauna. Our ancestral range reconstructions and molecular‐clock analyses support a southwest Pacific centre of origin for Microcanthus, with subsequent colonization of Western Australia through the Bass Strait followed by transequatorial dispersals to the Northern Hemisphere during the Pleistocene. Our results detail an anti‐tropical dispersal pattern that is highly unusual and previously undocumented, thereby emphasizing the importance of integrative systematics in the evaluation of widespread species.     

Morphological changes of sperm nuclei during spermatogenesis in the brown alga Cystoseira hakodatensis (Fucales, Phaeophyceae)

Morphological changes and chromatin condensation of sperm nuclei were observed during spermatogenesis in the fucalean brown alga Cystoseira hakodatensis (Yendo) Fensholt. Ultrastructural studies have shown that the mature spermatozoid has an elongated and concave nucleus with condensed chromatin. The morphological changes and the chromatin condensation process during spermatogenesis was observed. Nuclear size decreased in two stages during spermatogenesis. During the first stage, spherical nuclei decreased in size as they were undergoing meiotic divisions and the subsequent mitoses within the antheridium. During the second stage, the morphological transformation from a spherical into an elongated nucleus occurred. Afterwards, chromatin condensed at the periphery in each nucleus, and chromatin‐free regions were observed in the center of the nucleus. These chromatin‐free regions in the center of nucleus were compressed by the peripheral chromatin‐condensed region. As the result, the elongated and concave nucleus of the mature sperm consisted of uniformly well‐condensed chromatin.     

Finding of regeneration in a large number of wounded receptacles in Sargassum ringgoldianum (Phaeophyceae,Fucales)

Sargassum ringgoldianm is a canopy‐forming perennial macroalga dominant in a shallow waters along the central Pacific coast of Honshu, Japan, where macroalgal forests have been drastically declining by browsing of herbivorous fish since the 1990s. Accordingly, we tried to reveal seasonal fluctuation of browsing damage on S. ringgoldianum. In the course of the investigation, we found signs of receptacle regeneration in S. rinngoldianum, which has been reported in a few species of the order Fucales. Regenerations occurred most frequently from 3.0 mm to 3.9 mm of the basal part of original receptacles and were also observed at the tips of remaining stalks as well as branchlets that seemed to lose original receptacles. The regenerated receptacles formed antheridia and oogonia, and released eggs from them, suggesting that regenerated receptacles are functional. In addition, no regeneration was observed in only three individuals among 51 plants observed. We show herein a high regenerative ability of wounded receptacles in S. ringgoldianum. This frequent regeneration of functional receptacles is important for the persistence of the population.     

Phylogenetic relationships within the genus Sargassum (Fucales, Phaeophyceae), inferred from ITS-2 nrDNA, with an emphasis on the taxonomic subdivision of the genus

Sequences from the ribosomal DNA internal transcribed spacer‐2 (ITS‐2) were compared among species of Sargassaceae including the genera Sargassum and Hizikia. Species of different subgenera and sections of Sargassum were used to assess the taxonomic relationships within the genus, especially the subdivisions of the subgenus Bactrophycus. Sequences were aligned in accordance with their common secondary structure. Phylogenetic trees were constructed using neighbor‐joining, maximum likelihood and maximum parsimony methods with three species of Turbinaria as outgroups. The resulting phylogenetic trees showed that the genus Sargassum is divided into three clades corresponding to the subgenera Phyllotrichia, Sargassum and Bactrophycus. This last subgenus is further divided into four distinct groups: a Spongocarpus clade, a Teretia clade, a Hizikia clade, and a Halochloa/ Repentia clade. The position of the section Phyllo‐cystae, excluded from the subgenus Bactrophycus and included within the subgenus Sargassum is once again confirmed by the present study. Current results strongly support the assignation of Hizikia fusiformis to the genus Sargassum. Based on morphological differences and a distinct position in the molecular trees, Hizikia should be recognized as a section in the subgenus Bactrophycus so that Hizikia (Okamura) Yoshida, stat. nov. is proposed. A remarkably low divergence of ITS‐2 sequences was observed for the species in the sections Repentia and Halochloa, suggesting very recent radiation of these species. The subgenus Sargassum is divided into three clades corresponding to the three known sections: Acanthocarpicae, Malacocarpicae and Zygocarpicae, previously recognized by the morphology of receptacles. The position of Sargassum duplicatum, S. carpophyllum, S.yendoi, S. piluliferum and S. patens within the subgenus Sargassum is discussed.     

Phylogeographic analysis of the brown alga Cutleria multifida (Tilopteridales,Phaeophyceae) suggests a complicated introduction history

In depth genetic comparisons of populations of Cutleria multifida (Tilopteridales, Phaeophyceae) collected from Europe, the northwestern Pacific Ocean, Australia and New Zealand using the DNA sequences of four gene regions (the mitochondrial cox2 and cox3 genes, the intergeneric spacer region adjacent to cox3, and the open reading frame) suggested that the northwestern European and Japanese populations were considerably greater in terms of their genetic divergence than Mediterranean, Australian or New Zealand populations. The haplotypes of the populations in northwestern European (distribution range including the type locality, seven haplotypes) and Japanese populations (seven haplotypes) were unique except for one shared haplotype. There were weak but positive correlations between the geographical distance and the genetic divergence among northwestern European and Japanese populations. Moreover, both female and male gametophytes occurred in eight of the nine Japanese localities, suggesting Japanese populations showed normal sexual heteromorphic life history of the species. In light of these results, it appears that Japanese populations were native to the area despite earlier hypothesis. In contrast, Australian and New Zealand populations were composed of only one haplotype that is very close to those found in northwestern Europe and Japan, suggesting a recent introduction history from Europe (or from northeastern Asia via Europe) by ship transport to Australia and New Zealand. The Mediterranean populations included two haplotypes identical to those found in northwestern Europe and Japan, and it is suggestive of transoceanic introductions of some populations between Mediterranean and Japanese coasts.