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- Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentaceaPublication . Buonomo, Roberto; Assis, J.; Fernandes, Francisco; Engelen, Aschwin H.; Airoldi, Laura; Serrao, Ester A.Effective predictive and management approaches for species occurring in a metapopulation structure require good understanding of interpopulation connectivity. In this study, we ask whether population genetic structure of marine species with fragmented distributions can be predicted by stepping-stone oceanographic transport and habitat continuity, using as model an ecosystem-structuring brown alga, Cystoseira amentacea var. stricta. To answer this question, we analysed the genetic structure and estimated the connectivity of populations along discontinuous rocky habitat patches in southern Italy, using microsatellite markers at multiple scales. In addition, we modelled the effect of rocky habitat continuity and ocean circulation on gene flow by simulating Lagrangian particle dispersal based on ocean surface currents allowing multigenerational stepping-stone dynamics. Populations were highly differentiated, at scales from few metres up to thousands of kilometres. The best possible model fit to explain the genetic results combined current direction, rocky habitat extension and distance along the coast among rocky sites. We conclude that a combination of variable suitable habitat and oceanographic transport is a useful predictor of genetic structure. This relationship provides insight into the mechanisms of dispersal and the role of life-history traits. Our results highlight the importance of spatially explicit modelling of stepping-stone dynamics and oceanographic directional transport coupled with habitat suitability, to better describe and predict marine population structure and differentiation. This study also suggests the appropriate spatial scales for the conservation, restoration and management of species that are increasingly affected by habitat modifications.
- A meta-analysis of seaweed impacts on seagrasses: generalities and knowledge gapsPublication . Thomsen, Mads S.; Wernberg, Thomas; Engelen, Aschwin; Tuya, Fernando; Vanderklift, Mat A.; Holmer, Marianne; McGlathery, Karen J.; Arenas, Francisco; Kotta, Jonne; Sillimann, Brian R.Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than 'rooted' seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that 'rooted' seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds.
- Fast sporophyte replacement after removal suggests banks of latent microscopic stages of Laminaria Ochroleuca (phaeophyceae) in tide pools in northern PortugalPublication . Barradas, Ana; Alberto, F.; Engelen, Aschwin; Serrão, EsterThis study investigated the effects of a physical disturbance consisting of the removal of adult kelps (Laminaria ochroleuca Bachelot de la Pylaie)and their corresponding understorey turf assemblage in tide pools in northern Portugal.
- Temperature effects on the microscopic haploid stage development of laminaria ochroleuca and sacchoriza polyschides, kelps with contrasting life historiesPublication . Pereira, T. R.; Engelen, Aschwin; Pearson, G. A.; Serrão, Ester; Destombe, C.; Valero, MyriamKelp forests are one of the most diverse and productive ecosystems worldwide. Global climate change and human exploitation threaten the stability of many of these ecosystems.
- Host differentiation and compartmentalization of microbial communities in the Azooxanthellate Cupcorals Tubastrea coccinea and Rhizopsammia goesi in the CaribbeanPublication . Engelen, Aschwin; Aires, Tânia; Vermeij, Mark J. A.; Herndl, Gerhard J.; Serrao, Ester; Rodrigues Frade, PedroWe investigated the microbial communities associated with surface mucus layer, tissue, and gastrovascular cavity of two azooxanthellate Caribbean cup corals (Tubastrea coccinea and Rhizopsammia goesi) to explore potential differences in microbial community composition within and among these azooxanthellate scleractinian corals. Using next-generation sequencing of the V3-V6 region of the 16S rRNA gene we found that while alpha-diversity was overall very similar, the relative abundance of microbial taxa differed between host species and among locations within a polyp (i.e., compartments). The interspecific differentiation of microbial assemblages is only challenged by the relatively high similarity among mucus samples of both species. This suggests a stronger signal of the surrounding environment and weaker host control over the mucus compartment compared with the tissue and gastrovascular cavity. T. coccinea harbored four indicator OTUs (including a Pseudoalteromonas species, an unidentified Gammaproteobacteria, an unidentified OTU in the family Comamonadaceae and one in the genus Burkholderia). The single indicator for R. goesi was another undetermined OTU in the Comamonadaceae. The microbial communities of the gastrovascular cavity and the mucus overlapped substantially in indicator OTUs. None of these were exclusive of the gastrovascular cavity or mucus, while an OTU of the order Thiohalorhabdales occurred uniquely in the tissue. In contrast to the gastrovascular cavity and mucus, the tissue of both coral species was rich in chloroplasts of different algal taxa (mainly Ulvophyceae and Stramenopiles), and an OTU of the genus Roseivirga (family Flammeovirgaceae). The two coral species shared most indicator OTUs for microbial communities residing in their mucus and tissue, but not in their gastrovascular cavities. However, Endozoicomonadaceae occurred in the tissue of both coral species. The genus Pseudomonas was found in R. goesi but was virtually absent in .T coccinea. This study demonstrates the influence of coral compartments and species identities on the composition of microbial communities associated with azooxanthellate cup corals and emphasizes the important effects of within-polyp microhabitats in structuring the coral microbiome.
- Diversity and origin of the genus Lobophora in the Mediterranean Sea including the description of two new speciesPublication . Vieira, Christophe; Aharonov, Andre; Paz, Guy; Engelen, Aschwin; Tsiamis, Konstantinos; Einav, Rachel; De Clerck, OlivierThe brown algal genus Lobophora is widely reported from the Mediterranean Sea. Contrary to studies in the Indo-Pacific and Caribbean regions, little attention has been given to Lobophora in the Mediterranean Sea, at least using molecular tools. To address this knowledge gap, we sampled specimens across the Mediterranean Sea (Spanish coast, Balearic Islands, Greece and Israel), with an exhaustive effort in the Balearic Islands. Molecular analyses disclosed the presence of three species, none of them conspecific with the name L. variegata, as they were recorded up to now in the Mediterranean Sea. The most common species in the Mediterranean Sea is L. delicata. We here describe L. schneideri sp. nov., so far found only in Haifa Bay (Israel), where it forms large and dense populations. Similar to L. delicata, L. schneideri occurs across the North Atlantic Ocean. Though a recent range expansion or introduction cannot be ruled out, we regard the North Atlantic Ocean, including the Greater Caribbean and the Mediterranean Sea, as the natural range of both L. schneideri and L. delicata. A third species, described here as L. lessepsiana sp. nov., is found along the Israeli coast as well as in the Red Sea and is most probably a recent introduction through the Suez Canal. Further exploration along the North African coast, the Levantine Sea and the Aegean Sea, would probably increase the currently known species diversity for this group in the Mediterranean Sea.
- Metagenomic analysis shows the presence of bacteria related to free-living forms of sulfur-Oxidizing Chemolithoautotrophic Symbionts in the rhizosphere of the seagrass Zostera marinaPublication . Cúcio, Catarina; Overmars, Lex; Engelen, Aschwin; Muyzer, GerardSeagrasses play an important role as ecosystem engineers; they provide shelter to many animals and improve water quality by filtering out nutrients and by controlling pathogens. Moreover, their rhizosphere promotes a myriad of microbial interactions and processes, which are dominated by microorganisms involved in the sulfur cycle. This study provides a detailed insight into the metabolic sulfur pathways in the rhizobiome of the seagrass Zostera marina, a dominant seagrass species across the temperate northern hemisphere. Shotgun metagenomic sequencing revealed the relative dominance of Gamma- and Deltaproteobacteria, and comparative analysis of sulfur genes identified a higher abundance of genes related to sulfur oxidation than sulfate reduction. We retrieved four high-quality draft genomes that are closely related to the gill symbiont of the clam Solemya velum, which suggests the presence of putative free-living forms of symbiotic bacteria. These are potentially highly versatile chemolithoautotrophic bacteria, able to alternate their metabolism between parallel pathways of sulfide oxidation (via sqr and fcc), nitrate reduction (denitrification or DNRA) and carbon fixation (via CBB or TCA cycle), depending on the environmental availability of sulfide. Our results support the hypothesis that seagrass meadows might function as a source of symbionts for invertebrates that inhabit within or around seagrass meadows. While providing ideal conditions for the proliferation of these free-living forms of symbionts, seagrasses would benefit from their genetic versatility, which contributes to sulfide detoxification and ammonium production, the seagrasses' preferred nitrogen source.
- Genetic and oceanographic tools reveal high population connectivity and diversity in the endangered pen shell Pinna nobilisPublication . Wesselmann, Marlene; Gonzalez-Wanguemert, Mercedes; Serrao, Ester A.; Engelen, Aschwin H.; Renault, Lionel; Garcia-March, Jose R.; Duarte, Carlos M.; Hendriks, IrisFor marine meta-populations with source-sink dynamics knowledge about genetic connectivity is important to conserve biodiversity and design marine protected areas (MPAs). We evaluate connectivity of a Mediterranean sessile species, Pinna nobilis. To address a large geographical scale, partial sequences of cytochrome oxidase I (COI, 590 bp) were used to evaluate phylogeographical patterns in the Western Mediterranean, and in the whole basin using overlapping sequences from the literature (243 bp). Additionally, we combined (1) larval trajectories based on oceanographic currents and early life-history traits and (2) 10 highly polymorphic microsatellite loci collected in the Western Mediterranean. COI results provided evidence for high diversity and low inter-population differentiation. Microsatellite genotypes showed increasing genetic differentiation with oceanographic transport time (isolation by oceanographic distance (IBD) set by marine currents). Genetic differentiation was detected between Banyuls and Murcia and between Murcia and Mallorca. However, no genetic break was detected between the Balearic populations and the mainland. Migration rates together with numerical Lagrangian simulations showed that (i) the Ebro Delta is a larval source for the Balearic populations (ii) Alicante is a sink population, accumulating allelic diversity from nearby populations. The inferred connectivity can be applied in the development of MPA networks in the Western Mediterranean.
- The effects of grazing on the microbiome of an invasive brown seaweed (Sargassum Muticum)Publication . Aires, Tânia; Muyzer, G.; EA, Serrao; Engelen, AH
- Water-Borne Cues of a Non-Indigenous Seaweed Mediate Grazer-Deterrent Responses in Native Seaweeds, but Not Vice VersaPublication . Yun, Hee Young; Engelen, Aschwin H.; Santos, Rui O.; Molis, MarkusPlants optimise their resistance to herbivores by regulating deterrent responses on demand. Induction of anti-herbivory defences can occur directly in grazed plants or from emission of risk cues to the environment, which modifies interactions of adjacent plants with, for instance, their consumers. This study confirmed the induction of anti-herbivory responses by water-borne risk cues between adjoining con-specific seaweeds and firstly examined whether plant-plant signalling also exists among adjacent hetero-specific seaweeds. Furthermore, differential abilities and geographic variation in plant-plant signalling by a non-indigenous seaweed as well as native seaweeds were assessed. Twelve-day induction experiments using the non-indigenous seaweed Sargassum muticum were conducted in the laboratory in Portugal and Germany with one local con-familiar (Portugal: Cystoseira humilis, Germany: Halidrys siliquosa) and hetero-familiar native species (Portugal: Fucus spiralis, Germany: F. vesiculosus). All seaweeds were grazed by a local isopod species (Portugal: Stenosoma nadejda, Germany: Idotea baltica) and were positioned upstream of con-and hetero-specific seaweeds. Grazing-induced modification in seaweed traits were tested in three-day feeding assays between cue-exposed and cue-free (= control) pieces of both fresh and reconstituted seaweeds. Both Fucus species reduced their palatability when positioned downstream of isopod-grazed con-specifics. Yet, the palatability of non-indigenous S. muticum remained constant in the presence of upstream grazed con-specifics and native hetero-specifics. In contrast, both con-familiar (but neither hetero-familiar) native species reduced palatability when located downstream of grazed S. muticum. Similar patterns of grazer-deterrent responses to water-borne cues were observed on both European shores, and were almost identical between assays using fresh and reconstituted seaweeds. Hence, seaweeds may use plant-plant signalling to optimise chemical resistance to consumers, though this ability appeared to be species-specific. Furthermore, this study suggests that native species may benefit more than a non-indigenous species from water-borne cue mediated reduction in consumption as only natives responded to signals emitted by hetero-specifics.