Accounting for uncertainty in predictions of a marine species: Integrating population genetics to verify past distributions

We develop a new perspective on the uncertainties affecting the predictions of coastal species distributions using patterns of genetic diversity to assess the congruence of hindcasted distribution models. We model the niche of the subtidal seagrass Cymodocea nodosa, for which previous phylogeographic findings are used to contrast hypotheses for the Last Glacial Maximum (LGM) in the Mediterranean and adjacent Atlantic coastal regions. We focus on amelioration of sampling bias, and explore the influence of other sources of uncertainty such as the number of variables, Ocean General Circulation Models (OGCMs), and thresholds used. To do that, we test geographical and environmental filtering of presences, and a species-specific weighted filter related to political boundaries for background data. Contrary to our initial hypothesis that reducing sampling bias by means of geographical, environmental or background filtering would enhance predictive power and reliability of the models, none of these approaches consistently improved performance. These counter-intuitive results might be explained by the higher relative occurrence area (ROA) inherent to linear coastal study areas in relation to terrestrial regions, which may cause worse predictions and, thus, higher variability among models. We found that the Ocean General Circulation Models (OGCMs), the threshold and, to a smaller extent, the number of variables used, conditioned greatly the variability of the predictions in both accuracy and geographic range. Despite these uncertainties, all models achieved the goal of identifying long-term persistence regions (glacial refugia) where the highest genetic diversity for Cymodocea nodosa is found nowadays. However, only the CCSM corroborated the hypothesis, raised in previous studies, of a vicariant process in shaping the species' genetic structure. (C) 2017 Elsevier B.V. All rights reserved.Fundacao para a Ciencia e a Tecnologia (FCT, Portugal) [SFRH/BPD/85040/2012]Pew Foundation (USA)[UID/Multi/04326/2013]info:eu-repo/semantics/publishedVersio

Sexual reproduction vs. clonal propagation in the recovery of a seagrass meadow after an extreme weather event

Marine flowering plants can reproduce sexually and clonally, and the relative contribution of these two modes can be dependent on the environmental conditions. Zostera marina, a seagrass widely distributed in the northern hemisphere, can form annual and perennial meadows with different proportions of sexual versus clonal propagation depending on the environmental disturbance regime. We study the hypothesis that the contribution of sexual propagation varies during the recovery of a seagrass meadow. In this case study, we compare the proportion of sexual versus clonal propagation of a perennial Z. marina meadow before its disappearance due to winter storms and after recovery. Before disturbance, genotypic diversity was high, indicating frequent sexual reproduction events likely to create an abundant seed bank. Seedling germination allowed the population to recover after the extreme disturbance. As months passed, seedlings became rare and finally absent, giving place to adult shoots. In an advanced stage of colonization, the shoots colonized the area by vegetative growth, which lowered the genotypic diversity. Despite this reduction over time, the genotypic diversity of the new meadow is still high, demonstrating the importance of sexual reproduction in meadow recovery and persistence.info:eu-repo/semantics/publishedVersio

Polyploid lineages in the genus Porphyra

Whole genome duplication is now accepted as an important evolutionary force, but the genetic factors and the life history implications affecting the existence and abundance of polyploid lineages within species are still poorly known. Polyploidy has been mainly studied in plant model species in which the sporophyte is the dominant phase in their life history. In this study, we address such questions in a novel system (Porphyra, red algae) where the gametophyte is the dominant phase in the life history. Three Porphyra species (P. dioica, P. umbilicalis, and P. linearis) were used in comparisons of ploidy levels, genome sizes and genetic differentiation using flow cytometry and 11 microsatellite markers among putative polyploid lineages. Multiple ploidy levels and genome sizes were found in Porphyra species, representing different cell lines and comprising several cytotype combinations among the same and different individuals. In P. linearis, genetic differentiation was found among three polyploid lineages: triploid, tetraploid and mixoploids, representing different evolutionary units. We conclude that the gametophytic phase (n) in Porphyra species is not haploid, contradicting previous theories. New hypotheses for the life histories of Porphyra species are discussed.FCT (Fundacao para a Ciencia e a Tecnologia, Portugal) [SFRH/BPD/109452/2015, NORIGENOMICS - PTDC/MAR/099698/2008, UID/Multi/04326/2013, BIODIVERSA/004/2015-MARFOR

First description of seagrass distribution and abundance in Sao Tome and Principe

Seagrass meadows in Sao Tome and Principe, eastern Atlantic Ocean, are described here for the first time. Specifically, we quantified the biomass and density of seagrasses, characterized the plant morphology and measure their nutrient content as a proxy of the nutrient environmental conditions where the meadows develop. The seagrass Halodule wrightii was found in two locations of the northeastern coast of the island of Sao Tome: 1) developing throughout an estimated area of 1500 ha surrounding Cabras islet, at a depth range of 4-10 m, on sandy bottom; and 2) at Santana bay with an area of 1500 m(2) at 5-10 m depth, on sandy bottom. A highly morphologically different population of Halodule wrightii was found on the northeastern coast of the island of Principe, off Abade beach, covering an area of 135 m2 at 4 m depth. Further research is needed to assess if this is a different species. Shoot biomass and density was 10 and 4-fold higher in Sao Tome than in Principe, respectively. CN ratios of above and belowground tissues of plants collected in Sao Tome were also significantly higher than in Principe. The carbon content of Halodule leaves from Sao Tome and Principe (41%) was much higher than that reported for other Halodule species, suggesting that meadows may have an important ecological role for carbon fixation. The presence of H. wrightii in Sao Tome and Principe raises ecological and evolutionary questions that warrant further research.PADI Foundation [21670

Some don't like it hot: microhabitat-dependent thermal and water stresses in a trailing edge population

The distributional limits of species in response to environmental change are usually studied at large temporal and/or geographical scales. However, organismal scale habitat variation can be overlooked when investigating large-scale averages of key factors such as temperature. We examine how microhabitat thermal conditions relate to physiological limits, which may contribute to recent range shifts in an intertidal alga. We defined the onset and maximum temperatures of the heat-shock response (HSR) for a southern edge population of Fucus vesiculosus, which has subsequently become extinct. The physiological threshold for resilience (assayed using chlorophyll fluorescence) coincided with declining HSR, determined from the temperature-dependent induction of seven heat-shock protein transcripts. In intertidal habitats, temperature affects physiology directly by controlling body temperature and indirectly through evaporative water loss. We investigated the relationship between the thermal environment and in situ molecular HSR at microhabitat scales. Over cm to m scales, four distinct microhabitats were defined in algal patches (canopy surface, patch edge, subcanopy, submerged channels), revealing distinct thermal and water stress environments during low-tide emersion. The in situ HSR agreed with estimated tissue temperatures in all but one microhabitat. Remarkably, in the most thermally extreme microhabitat (canopy surface), the HSR was essentially absent in desiccated tissue, providing a potential escape from the cellular metabolic costs of thermal stress. Meteorological records, microenvironmental thermal profiles and HSR data indicate that the maximum HSR is approached or exceeded in hydrated tissue during daytime low tides for much of the year. Furthermore, present-day summer seawater temperatures are sufficient to induce HSR during high-tide immersion, preventing recovery and resulting in continuous HSR during daytime low-tide cycles over the entire summer. HSR in the field matched microhabitat temperatures more closely than local seawater or atmospheric data, suggesting that the impacts of climatic change are best understood at the microhabitat scale, particularly in intertidal areas.FCT - Portuguese Science Foundation [POCTI/MAR/61105/2004, EXCL/AAG-GLO/0661/2012, SFRH/BPD/63/03/2009, SFRH/BD/74436/2010]info:eu-repo/semantics/publishedVersio

Seaweed loads cause stronger bacterial community shifts in coastal lagoon sediments than nutrient loads

The input of nutrients from anthropogenic sources is the leading cause of coastal eutrophication and is usually coupled with algal/seaweed blooms. Effects may be magnified in semi-enclosed systems, such as highly productive coastal lagoon ecosystems. Eutrophication and seaweed blooms can lead to ecosystem disruption. Previous studies have considered only one of these factors, disregarding possible interactive effects and the effect of the blooming species' identity on sediment bacterial communities. We tested the effect of experimental nutrient loading and two common blooming seaweeds (Ulva rigida and Gracilaria vermiculophylla) in coastal lagoon sediments, on the structure of bacterial communities (using 16S rRNA amplicon sequencing) and corresponding putative functional potential (using PiCRUSt). At the Operational Taxonomic Unit (OTU) level, the addition of nutrients reduced bacterial community α-diversity and decreased the abundance of sulfate reducers (Desulfobacterales) compared to sulfur oxidizers/denitrifiers (Chromatiales and Campylobacterales), whereas this was not the case at the order level. Seaweed addition did not change bacterial α-diversity and the effect on community structure depended on the taxonomic level considered. The addition of Gracilaria increased the abundance of orders and OTUs involved in sulfate reduction and organic matter decomposition (Desulfobacterales, Bacteroidales, and Clostridiales, respectively), an effect which was also detected when only Ulva was added. Nutrients and the seaweeds combined only interacted for Ulva and nutrients, which increased known sulfide oxidizers and denitrifiers (order Campylobacterales). Seaweed enrichment affected putative functional profiles; a stronger increase of sulfur cycling KEGG pathways was assigned to nutrient-disturbed sediments, particularly with the seaweeds and especially Ulva. In contrast, nitrogen and sulfur cycle pathways showed a higher abundance of genes related to dissimilatory nitrate reduction to ammonium (DNRA) in Ulva+nutrients treatments. However, the other seaweed treatments increased the nitrogen fixation genes. Thiosulfate reduction, performed by sulfate-reducing bacteria, increased in seaweed treatments except when Ulva was combined with nutrients. In conclusion, the in situ addition of nutrients and the seaweeds to intertidal sediments affected the bacterial communities differently and independently. The predicted functional profile suggests a shift in relative abundances of putative pathways for nitrogen and sulfur cycles, in line with the taxonomic changes of the bacterial communities.FCT - Foundation for Science and Technology UID/Multi/04326/2019 UID/Multi/04326/2016 SEAS-ERA/0001/2012 SFRH/BPD/107878/2015 SFRH/BPD/116774/2016 research priority area Systems Biology of the University of Amsterdaminfo:eu-repo/semantics/publishedVersio

Less is more: seagrass restoration success using less vegetation per area

Seagrass restoration in open coast environments presents unique challenges. Traditional sod transplant designs, though relatively successful in these environments, are impractical for large-scale restoration due to high biomass requirements. Here, we develop the checkers design, which aims to optimise the usage of biomass by transplanting fewer sods in a checkerboard pattern. We established six plots (9 m2 each) for each species (Zostera marina and Zostera noltei), with 25 sods in each plot. The area, percent cover, density, and leaf length were measured at 1, 6, and 12 months. The plots located on the seaward end of the transplant design vanished over the winter, suggesting location-dependent survival influenced by winter storms. Nevertheless, both species exhibited increased percentages of cover, density, and vegetated area after one year, with variations between species. Z. noltei showed a slower expansion but greater resilience to winter, while Z. marina displayed a higher density and cover over the first 6 months but experienced area loss during the winter. Despite these differences, both species survived and increased vegetated areas after one year, indicating the viability and promise of the checkers method for large-scale restoration. However, careful consideration of location or storm-mitigating measures is essential for the successful implementation of this method.LA/P/0101/2020; CRESC Algarve 2020 and COMPETE 2020 through project EMBRC.PT ALG-01-0145-FEDER-022121info:eu-repo/semantics/publishedVersio

A fine-tuned global distribution dataset of marine forests

Species distribution records are a prerequisite to follow climate-induced range shifts across space and time. However, synthesizing information from various sources such as peer-reviewed literature, herbaria, digital repositories and citizen science initiatives is not only costly and time consuming, but also challenging, as data may contain thematic and taxonomic errors and generally lack standardized formats. We address this gap for important marine ecosystem-structuring species of large brown algae and seagrasses. We gathered distribution records from various sources and provide a fine-tuned dataset with ~2.8 million dereplicated records, taxonomically standardized for 682 species, and considering important physiological and biogeographical traits. Specifically, a flagging system was implemented to signal potentially incorrect records reported on land, in regions with limiting light conditions for photosynthesis, and outside the known distribution of species, as inferred from the most recent published literature. We document the procedure and provide a dataset in tabular format based on Darwin Core Standard (DwC), alongside with a set of functions in R language for data management and visualization.FCT: (SFRH/BPD/111003/2015) / (SFRH/BSAB/150485/2019) / (SFRH/BD/144878/2019)(PTDC/MAREST/6053/2014) / MARFOR (BIODIVERSA/004/2015) / UIDB/04326/2020info:eu-repo/semantics/publishedVersio

Summer shifts of bacterial communities associated with the invasive brown seaweed Sargassum muticum are location and tissue dependent

Seaweed-associated microbiota experience spatial and temporal shifts in response to changing environmental conditions and seaweed physiology. These shifts may result in structural, functional and behavioral changes in the host with potential consequences for its fitness. They, thus, may help the host to adapt to changing environmental conditions. The current knowledge of seasonal variation of seaweed-associated microbiota is however still limited. In this study, we explored temporal and spatial variation of microbial communities associated with the invasive brown seaweed S. muticum. We sampled in northern and southern Portugal, in September, March and July-August (summer). In addition, as (pseudo-)perennial seaweeds display seasonal reproductive phenology, we sampled various parts of the individuals to disentangle the effect of temporal changes from those due to structural development variations. The diversity and structure of associated microbial communities were determined using next generation sequencing of the variable regions V5-7 of the 16S rDNA. We expected to find differentiation in associated microbial communities between regions and sampling months, but with differences depending on the seaweed structure examined. As expected, the study revealed substantial temporal shifts in S. muticum microbiome, for instance with large abundance of Rhodobacteraceae and Loktanella in September-March but prevalence of Pirellulales during the summer months. Variations between regions and tissues were also observed: in northern Portugal and on basal structures, bacterial diversity was higher as compared to the South and apical parts. All examined seaweed structures showed temporal differences in associated microbial community structure over time, except for holdfasts between September and March. Bacteria contributing to these changes varied spatially. Conversely to all other structures, the holdfast also did not show differences in associated community structure between southern and northern regions. Our study highlights the importance of structural microscale differentiations within seaweeds hosts with regard to their associated microbial communities and their importance across temporal and spatial dimensions.Erasmus Mundus Doctoral Programme MARES on Marine Ecosystem Health Conservation - MARES_13_08 FCT (Portugal) - SFRH/BPD/107878/2015, SFRH/BPD/116774/2016 project EU SEAS-ERA INVASIVES - SEAS-ERA/0001/2012 project MARFOR - FCT-BIODIVERSA/004/2015 CCMAR/Multi/04326/2013info:eu-repo/semantics/publishedVersio

Hologenome theory supported by cooccurrence networks of species-specific bacterial communities in siphonous algae (Caulerpa)

The siphonous algae of the Caulerpa genus harbor internal microbial communities hypothesized to play important roles in development, defense and metabolic activities of the host. Here, we characterize the endophytic bacterial community of four Caulerpa taxa in the Mediterranean Sea, through 16S rRNA amplicon sequencing. Results reveal a striking alpha diversity of the bacterial communities, similar to levels found in sponges and coral holobionts. These comprise (1) a very small core community shared across all hosts ( 70%) species-specific fraction of the community, forming very specific clusters revealed by modularity in networks of cooccurrence, even in areas where distinct Caulerpa taxa occurred in sympatry. Indirect inferences based on sequence homology suggest that these communities may play an important role in the metabolism of their host, in particular on their ability to grow on anoxic sediment. These findings support the hologenome theory and the need for a holistic framework in ecological and evolutionary studies of these holobionts that frequently become invasive.Portuguese Foundation for Science and Technology (FCT); FEDER; project IBISA [PTDC / MAR / 64749 / 2006]; PhD fellowship from FCT [SFRH/BD/30043/2006]; FSEinfo:eu-repo/semantics/publishedVersio