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  • Linking ecology to genetics to better understand adaptation and evolution: a review in marine macrophytes
    Publication . Hu, Zi-Min; Zhong, Kai-Le; Weinberger, Florian; Duan, De-Lin; Draisma, Stefano G. A.; Serrao, Ester
    Ecological processes and intra-specific genetic diversity reciprocally affect each other. While the importance of uniting ecological variables and genetic variation to understand species’ plasticity, adaptation, and evolution is increasingly recognized, only few studies have attempted to address the intersection of population ecology and genetics using marine macrophyte as models. Representative empirical case studies on genetic diversity are reviewed that explore ecological and evolutionary processes in marine macrophytes. These include studies on environment-induced phenotypic plasticity and associated ecological adaptation; population genetic variation and structuring driven by ecological variation; and ecological consequences mediated by intraspecific and interspecific diversity. Knowledge gaps are also discussed that impede the connection of ecology and genetics in macrophytes and possible approaches to address these issues. Finally, an eco-evolutionary perspective is advocated, by incorporating structural-tofunctional genomics and life cycle complexity, to increase the understanding of the adaptation and evolution of macrophytes in response to environmental heterogeneity.
  • Setting preliminary biometric baselines for new target sea cucumbers species of the NE Atlantic and Mediterranean fisheries
    Publication . González-Wangüemert, Mercedes; Valente, Sara; Henriques, Filipe; Domínguez-Godino, Jorge A.; Serrao, Ester
    Commercial interest on sea cucumber species from the NE Atlantic and the Mediterranean is increasing.Holothuria polii, Holothuria tubulosa, Holothuria mammata and Holothuria arguinensis are the new targetspecies. The scarce biological and ecological knowledge on these species along their geographical distri-bution, is a major problem for their fisheries management. To address it, we carried out a morphometricstudy to describe the baseline population size structure, focused on the length–weight relationship andsize–weight distribution.In the NE Atlantic, the largest mean size and heaviest mean weight of H. mammata and H. arguinensiswere found in localities with upwelling, but another factors could be influencing on these results. In theMediterranean, Girona and Mallorca showed the heaviest specimens of H. polii, H. tubulosa and H. mam-mata, and the smallest were registered in Crete and Kusadasi. Significant differences in length and weightbetween populations were found for each species. These results could be linked with local environmentalconditions. Size frequency distribution was multimodal for all species except for H. mammata; the weightfrequency distribution was only unimodal for H. polii and H. mammata.This study provides novel data, helpful for stock and population assessment which could support theimplementation of effective management for the European sea cucumber target species.
  • Do hatchery-reared sea urchins pose a threat to genetic diversity in wild populations?
    Publication . Segovia-Viadero, M.; Serrao, Ester; Canteras-Jordana, J. C.; Gonzalez-Wangueemert, Mercedes
    In salmonids, the release of hatchery-reared fish has been shown to cause irreversible genetic impacts on wild populations. However, although responsible practices for producing and releasing genetically diverse, hatchery-reared juveniles have been published widely, they are rarely implemented. Here, we investigated genetic differences between wild and early-generation hatchery-reared populations of the purple sea urchin Paracentrotus lividus (a commercially important species in Europe) to assess whether hatcheries were able to maintain natural levels of genetic diversity. To test the hypothesis that hatchery rearing would cause bottleneck effects (that is, a substantial reduction in genetic diversity and differentiation from wild populations), we compared the levels and patterns of genetic variation between two hatcheries and four nearby wild populations, using samples from both Spain and Ireland. We found that hatchery-reared populations were less diverse and had diverged significantly from the wild populations, with a very small effective population size and a high degree of relatedness between individuals. These results raise a number of concerns about the genetic impacts of their release into wild populations, particularly when such a degree of differentiation can occur in a single generation of hatchery rearing. Consequently, we suggest that caution should be taken when using hatchery-reared individuals to augment fisheries, even for marine species with high dispersal capacity, and we provide some recommendations to improve hatchery rearing and release practices. Our results further highlight the need to consider the genetic risks of releasing hatchery-reared juveniles into the wild during the establishment of restocking, stock enhancement and sea ranching programs.
  • Microbiome dynamics in the tissue and mucus of acroporid corals differ in relation to host and environmental parameters
    Publication . Marchioro, Giulia Manso; Glasl, Bettina; Engelen, Aschwin; Serrao, Ester; Bourne, David G.; Webster, Nicole; Rodrigues Frade, Pedro
    Corals 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).
  • Predicted regime shift in the seagrass ecosystem of the Gulf of Arguin driven by climate change
    Publication . Chefaoui, Rosa M.; Duarte, Carlos M.; Tavares, Ana I; Frade, Duarte; Sidi Cheikh, M.A.; Abdoull Ba, M.; Serrao, Ester
    The Banc d′Arguin is a marine ecosystem of global conservation significance, the largest bird sanctuary of western Africa, supported by one of the most extensive seagrass beds in the world composed by three seagrass species, two temperate near their southern limit (Zostera noltei and Cymodocea nodosa) and one tropical at its northern limit (Halodule wrightii). Here we predict the fate of this seagrass ecosystem under climate change scenarios during the 21st century, using species distribution models and sea level rise estimates. We forecast a probable decline in total seagrass area of 3340 Km2 (78%) by 2100, involving the loss of both temperate seagrasses (Z. noltei, C. nodosa), the foundational ecosystem components. By 2050, only the tropical species (H. wrightii) would remain, which forms thin and sparse shallow stands functionally distinct from the previous tall dense meadows that span wider vertical ranges. Intertidal flats, the essential bird foraging habitats, would become unvegetated and also suffer a major reduction in area (114 km2 by 2050, 587 km2 by 2100). The large projected loss of foundational seagrass species portends a collapse of major ecosystem functions with profound impacts on biodiversity, fishery resources and ecosystem services.
  • Spatiotemporal variation of the epifaunal assemblages associated to Sargassum muticum on the NW Atlantic coast of Morocco
    Publication . Belattmania, Zahira; Chaouti, Abdellatif; Engelen, Aschwin; Serrao, Ester; Machado, Margarida; Reani, Abdeltif; Sabour, Brahim
    Epifaunal 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.
  • eDNA metabarcoding reveals a rich but threatened and declining elasmobranch community in West Africa’s largest marine protected area, the Banc d’Arguin
    Publication . de la Hoz Schilling, Carolina; Jabado, Rima W.; Veríssimo, Ana; Caminiti, Luca; Sidina, Ebaye; Gandega, Cheikhna Yero; Serrao, Ester
    Elasmobranchs (sharks and rays) are the most threatened marine vertebrates, particularly in tropical and subtropical areas. Their population status is often poorly understood due to insufficient information. Despite reportedly harbouring critical elasmobranch habitats, the Banc d'Arguin National Park (PNBA) in Mauritania lacks comprehensive and updated information on the diversity of elasmobranch species in the area. We developed a baseline inventory based on morphological and molecular identification and metabarcoding. DNA barcoding of tissue samples from elasmobranch processing sites and freshly sampled specimens was used to build a genetic reference database of local elasmobranch species. The richness and diversity of species in the PNBA were described via metabarcoding of seawater eDNA samples using an elasmobranch-specific assay and our reference database. We detected 27 species, including 12 new species records for the PNBA. We further uncover potentially undescribed species of Gymnura and Torpedo, while taxonomic corrections are noted for previously reported species. In particular, the reportedly abundant Mustelus mustelus was absent from tissue and eDNA samples, while M. punctulatus was detected instead. Taxa that have anecdotally become regionally extinct or rare (e.g., sawfishes, wedgefishes, lemon sharks) were not detected, highlighting local species diversity shifts within the last few decades. Results show that 67.9% of elasmobranch species in the PNBA are threatened with extinction according to the IUCN Red List of Threatened Species. This study emphasises the importance of taxonomic identification in support of species management and provides a baseline to inform future studies and conservation measures to avoid further species losses.
  • Genetic diversity of a marine foundation species,Laminaria hyperborea(Gunnerus) Foslie, along the coast of Ireland
    Publication . Schoenrock, Kathryn M.; O'Connor, Aisha M.; Mauger, Stephane; Valero, Myriam; MACHADO, JOÃO NEIVA; Serrao, Ester; Krueger-Hadfield, Stacy A.
    Worldwide, kelp populations are stressed by warming, increased storms and other anthropogenic disturbances. Marine population distributions are projected to retreat poleward with climate change if they cannot adapt to changing conditions, which would potentially lead to a regime shift in subtidal habitats. In Northern Europe,Laminaria hyperboreais a subtidal ecosystem engineer whose distribution has shifted over millennia, leaving predicted areas of high genetic diversity from the last glacial maximum (LGM) near its southern distribution limit in the Iberian Peninsula. In Ireland,L. hyperboreastructures communities by supporting diverse faunal assemblages and producing large quantities of organic carbon throughout the year. We investigated the genetic diversity of eight populations, ranging from the southern coast to the north-west of Ireland, using nine microsatellite loci. Diversity was found to be highest in Lough Hyne, a Special Area of Conservation (SAC), near the predicted climate refugium. We found evidence of isolation by distance, with high connectivity between populations that were geographically close, probably driven by short range dispersal ofL. hyperboreapropagules. Genetic diversity (measured as expected heterozygosity and allelic richness) was highest at Lough Hyne, and decreased northwards, as predicted from past range shifts. Expected heterozygosity was highest at Lough Hyne (0.706) and decreased northward, with the lowest value at Bridges of Ross (0.283). Based on these patterns, further fine-scale investigation into population diversity, dispersal and potential resilience in Irish kelp forests are necessary as warming and non-native species are observed more and more frequently.
  • Canopy microclimate modification in central and marginal populations of a marine macroalga
    Publication . Monteiro, Cátia; Zardi, Gerardo I.; McQuaid, Christopher D.; Serrao, Ester; Pearson, Gareth; Nicastro, Katy
    The effects of environmental changes on species distribution are generally studied at large geographical scales. However, aggregations of individuals can significantly moderate the impact of the environment at smaller, organismal scales. We focused on the intertidal macroalga Fucus guiryi and carried out field and laboratory common garden experiments to evaluate how the different individual morphologies and canopy densities typical of central and peripheral populations modify microhabitat conditions and associated levels of stress. We show that F. guiryi canopies significantly alter environmental conditions (i.e., temperature, humidity and light regimes) and mitigate the levels of stress experienced by individuals within the group. Southern algae are more branched and form denser canopies but, unexpectedly, despite these considerable differences, the mitigating effects of northern and southern canopies did not differ significantly. Microhabitat conditions beneath canopies were more stressful at marginal locations, indicating that southern populations are not more effective than northern algae at mitigating the harsher climate at the edge of the species distribution. Our findings highlight the importance of assessing structural changes in aggregating species across their distribution and relating these to local climates to understand the impact of environmental changes at scales relevant to individual organisms.
  • Host differentiation and compartmentalization of microbial communities in the Azooxanthellate Cupcorals Tubastrea coccinea and Rhizopsammia goesi in the Caribbean
    Publication . Engelen, Aschwin; Aires, Tânia; Vermeij, Mark J. A.; Herndl, Gerhard J.; Serrao, Ester; Rodrigues Frade, Pedro
    We 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.