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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.
- Microbiome dynamics in the tissue and mucus of acroporid corals differ in relation to host and environmental parametersPublication . Marchioro, Giulia Manso; Glasl, Bettina; Engelen, Aschwin; Serrao, Ester; Bourne, David G.; Webster, Nicole; Rodrigues Frade, PedroCorals are associated with diverse microbial assemblages; however, the spatial-temporal dynamics of intra-species microbial interactions are poorly understood. The coral-associated microbial community varies substantially between tissue and mucus microhabitats; however, the factors controlling the occurrence, abundance, and distribution of microbial taxa over time have rarely been explored for different coral compartments simultaneously. Here, we test (1) differentiation in microbiome diversity and composition between coral compartments (surface mucus and tissue) of two Acropora hosts (A. tenuis and A. millepora) common along inshore reefs of the Great Barrier Reef, as well as (2) the potential linkage between shifts in individual coral microbiome families and underlying host and environmental parameters. Amplicon based 16S ribosomal RNA gene sequencing of 136 samples collected over 14 months, revealed significant differences in bacterial richness, diversity and community structure among mucus, tissue and the surrounding seawater. Seawater samples were dominated by members of the Synechococcaceae and Pelagibacteraceae bacterial families. The mucus microbiome of Acropora spp. was dominated by members of Flavobacteriaceae, Synechococcaceae and Rhodobacteraceae and the tissue was dominated by Endozoicimonaceae. Mucus microbiome in both Acropora species was primarily correlated with seawater parameters including levels of chlorophyll a, ammonium, particulate organic carbon and the sum of nitrate and nitrite. In contrast, the correlation of the tissue microbiome to the measured environmental (i.e., seawater parameters) and host health physiological factors differed between host species, suggesting host-specific modulation of the tissue-associated microbiome to intrinsic and extrinsic factors. Furthermore, the correlation between individual coral microbiome members and environmental factors provides novel insights into coral microbiome-by-environment dynamics and hence has potential implications for current reef restoration and management efforts (e.g. microbial monitoring and observatory programs).
- From plates to baits: using a remote video foraging system to study the impact of foraging on fouling non-indigenous speciesPublication . Chebaane, Sahar; Canning-Clode, João; Ramalhosa, Patrício; Belz, Janina; Castro, Nuno; Órfão, Inês; Sempere-Valverde, Juan; Engelen, Aschwin; Pais, Miguel Pessanha; Monteiro, João GamaMarinas are a gateway for the introduction and establishment of non-indigenous species (NIS). In these habitats, competition and predation are crucial determinants for NIS establishment and invasiveness. However, fish trophic preferences and biotic effects inside marinas are poorly known. This study proposes a novel method that combines the deployment of settlement plates to recruit different assemblages, followed by their use as bait in remote underwater video systems. This combined approach, addressed as a remote video foraging system (RVFS), can record fish foraging behaviour, including feeding choices and their impacts on fouling assemblage composition. An experimental RVFS trial carried out in a marina of Madeira Island, Portugal (NE Atlantic), identified the Mediterranean parrotfish, Sparisoma cretense, as the most important fouling grazer in the area. S. cretense behaved as a generalist and increased the heterogeneity of fouling assemblages, which can hamper NIS dominance of the fouling and reduce the pressure of propagules from the marina to the natural environment. The RVFS tool was useful to understand the trophic links between foragers and fouling and has the potential to provide relevant information for the management of NIS introductions, establishment and spread.
- Salinity and host drive Ulva‐associated bacterial communities across the Atlantic–Baltic Sea gradientPublication . Van der Loos, Luna M.; D’hondt, Sofie; Engelen, Aschwin; Pavia, Henrik; Toth, Gunilla B.; Willems, Anne; Weinberger, Florian; De Clerck, Olivier; Steinhagen, SophieThe green seaweed Ulva is a model system to study seaweed-bacteria interactions, but the impact of environmental drivers on the dynamics of these interactions is little understood. In this study, we investigated the stability and variability of the seaweed-associated bacteria across the Atlantic-Baltic Sea salinity gradient. We characterized the bacterial communities of 15 Ulva sensu lato species along 2,000 km of coastline in a total of 481 samples. Our results demonstrate that the Ulva-associated bacterial composition was strongly structured by both salinity and host species (together explaining between 34% and 91% of the variation in the abundance of the different bacterial genera). The largest shift in the bacterial consortia coincided with the horohalinicum (5-8 PSU, known as the transition zone from freshwater to marine conditions). Low-salinity communities especially contained high relative abundances of Luteolibacter, Cyanobium, Pirellula, Lacihabitans and an uncultured Spirosomaceae, whereas high-salinity communities were predominantly enriched in Litorimonas, Leucothrix, Sulfurovum, Algibacter and Dokdonia. We identified a small taxonomic core community (consisting of Paracoccus, Sulfitobacter and an uncultured Rhodobacteraceae), which together contributed to 14% of the reads per sample, on average. Additional core taxa followed a gradient model, as more core taxa were shared between neighbouring salinity ranges than between ranges at opposite ends of the Atlantic-Baltic Sea gradient. Our results contradict earlier statements that Ulva-associated bacterial communities are taxonomically highly variable across individuals and largely stochastically defined. Characteristic bacterial communities associated with distinct salinity regions may therefore facilitate the host's adaptation across the environmental gradient.
- Spatiotemporal variation of the epifaunal assemblages associated to Sargassum muticum on the NW Atlantic coast of MoroccoPublication . Belattmania, Zahira; Chaouti, Abdellatif; Engelen, Aschwin; Serrao, Ester; Machado, Margarida; Reani, Abdeltif; Sabour, BrahimEpifaunal assemblages inhabiting the non-indigenous macroalga Sargassum muticum (Yendo) Fensholt were investigated on two physically distinct intertidal rocky (S1) and sandy (S2) sites along the Atlantic coast of Morocco. The objective of this study was to test whether the habitat-forming marine alga S. muticum invasive in these sites supported different epifaunal assemblages under different environmental conditions and through time. The gastropods Steromphala umbilicalis, S. pennanti, and Rissoa parva and the isopod Dynamene bidentata were the most contributive species to the dissimilarity of epifaunal assemblage structure between both sites throughout seasons. SIMPER analysis showed a dissimilarity of 58.3-78.5% in the associated species composition of S. muticum between study sites with respect to sampling season. Species diversity and total abundance were significantly higher at the rocky site compared to the sandy site. PERMANOVA analyses showed significant differences of associated epifaunal assemblage structure for the season and site interaction. Accordingly, site and season were determinant factors conditioning the role of habitat in structuring epifaunal assemblages.
- 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.
- Regional microbiome differentiation of the invasive Sargassum muticum (Fucales, Phaeophyceae) follows the generalist host hypothesis across the North East AtlanticPublication . Aires, Tânia; Kläui, Anita; Hillebrand Engelen, AschwinOver 90% of introduced marine species are seaweeds. Seaweeds rely on their microbiome for host settlement, nutrition, development and health. As such, it is likely that microbiomes are involved in seaweed invasions. Sargassum muticum, indigenous to Southeast Asia, inhabits the North-east Atlantic from Norway to Morocco. This is the only known successful case of a non-clonal marine invader with almost no genetic variation over its large NE Atlantic introduced range. This makes it a very interesting model to study an invasive seaweeds microbiome, as it practically uncouples host genetic variation from microbiome variation. Associated bacteria potentially contribute to the plasticity and acclimation of S. muticum leading to its success over the last 50 years. Dispersing host organisms can either bring their acquired microbes along or obtain new ones locally, following the mutualist and generalist host hypothesis, respectively. We used partial 16S rRNA gene amplicon sequencing to characterize the total and core microbiome across S. muticum structures/tissues from five NE Atlantic regions, from Norway to Morocco, covering over 30 degrees of latitude. In contrast to host genotypes, highly diverse, regional, total and core microbiomes, with differentiation levels depending on tissue, bacterial community structure were detected. Atlantic S. muticum follows the generalist host hypothesis, possibly recruiting a new microbiome in each new region. This host promiscuity may promote the invasiveness of S. muticum. Diversity was lower in the young/annual tissues compared with the older tissues for the total bacterial community, suggesting that these are mostly transitory bacteria accumulating over time in the older parts. The total core microbiome included 10 OTUs, representing dominant community members commonly found in other seaweeds' cores. The core Granulosicoccus OTU followed a clear regional pattern where northern and southern regions clustered differentially, suggesting a regional signature even at an OTU level.
- 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.