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- Fine‐scale genetic structure and flowering output of the seagrass Enhalus acoroides undergoing disturbancePublication . Yu, Shuo; Wu, Yunchao; Serrao, Ester A.; Zhang, Jingping; Jiang, Zhijian; Huang, Chi; Cui, Lijun; Thorhaug, Anitra; Huang, XiaopingSeagrass are under great stress in the tropical coast of Asia, where Enhalus acoroides is frequently the dominant species with a large food web. Here, we investigate the question of the fine-scale genetic structure of this ecologically important foundation species, subject to severe anthropogenic disturbance in China. The genetic structure will illuminate potential mechanisms for population dynamics and sustainability, which are critical for preservation of biodiversity and for decision-making in management and restoration. We evaluated the fine-scale spatial genetic structure (SGS) and flowering output of E. acoroides, and indirectly estimated the relative importance of sexual versus asexual reproduction for population persistence using spatial autocorrelation analysis. Results reveal high clonal diversity for this species, as predicted from its high sexual reproduction output. The stronger Sp statistic at the ramet-level compared with genet-level indicates that clonality increases the SGS pattern for E. acoroides. Significant SGS at the genet-level may be explained by the aggregated dispersal of seed/pollen cohorts. The estimated gene dispersal variance suggests that dispersal mediated by sexual reproduction is more important than clonal growth in this study area. The ongoing anthropogenic disturbance will negatively affect the mating pattern and the SGS patterns in the future due to massive death of shoots, and less frequency of sexual reproduction.
- Comparative analysis of stability-genetic diversity in seagrass (Posidonia oceanica) meadows yields unexpected resultsPublication . ARNAUD-HAOND, Sophie; Marbà, N.; Diaz-Almela, E.; Serrão, Ester; Duarte, C. M.The diversity–stability relationship is the subject of a long-standing debate in ecology, but the genetic component of diversity has seldom been explored. In this study, we analyzed the interplay between genetic diversity and demographic responses to environmental pressures. This analysis included 30 meadows formed by the Mediterranean endemic seagrass, Posidonia oceanica, showing a wide range of population dynamics ranging from a near equilibrium state to steep decline due to strong environmental pressures close to aquaculture installations. Our results show that sedimentation rates are much better predictors of mortality than clonal or genetic components. An unexpected positive trend was observed between genotypic diversity and mortality, along with a negative relationship between allelic richness and net population growth. Yet such trends disappeared when excluding the most extreme cases of disturbance and mortality, suggesting the occurrence of a threshold below which no relationship exists. These results contrast with the positive relationship between genotypic diversity and resistance or resilience observed in previous manipulative experiments on seagrass. We discuss the reasons for this discrepancy, including the difficulties in designing experiments reflecting the complexity of natural meadows.
- New microsatellite markers for the endemic Mediterranean seagrass Posidonia oceanicaPublication . Alberto, F.; Correia, L.; ARNAUD-HAOND, Sophie; Billot, C.; Duarte, C. M.; Serrão, EsterThe seagrass Posidonia oceanica is endemic to the Mediterranean Sea, where it plays an important role in coastal ecosystem dynamics. Because of this important role and concerns about the observed regression of some meadows, population genetic studies of this species have been promoted. However, the markers used until now were not polymorphic enough to efficiently assess the level and spatial pattern of genetic variability. Hypervariable molecular markers were obtained by screening a genomic library enriched for microsatellite dinucleotide repeats. Among 25 primer pairs defined, eight amplified polymorphic microsatellites with an encouraging level of variability at the two geographical scales sampled.
- Timing and success of reproductive stages in the seagrass Zostera noltiiPublication . Alexandre, Ana; Cabaço, Susana; Santos, Rui; Serrão, EsterThe timing and success of sexual reproduction of the seagrass Zostera noltii was investigated at the Ria Formosa lagoon, Portugal. Thirty plants were tagged and monitored individually through time to determine in situ the development time of each maturation stage, from the emergence of the flowers to the production of seeds. The overall process of flowering and fruiting lasted 47 ± 4 days, during which formation and maturation of the fruits was the most time-consuming stage (27 ± 2 days). Spathe success, i.e. the percentage of spathes that produced seeds, was 22 ± 4% while spathe mortality was 34 ± 6%. A considerable percentage of spathes (37 ± 7%) was lost through leaf detachment, but some of these may still add to the reproductive success of the species by contributing to the species recruitment within the source meadow or elsewhere. Meadow seed production (MSP) of Z. noltii was estimated to be 312 ± 66 seeds m−2, whereas the potential seed production of the studied meadow was 2623 seeds m−2. Under laboratory conditions, 70% of Z. noltii seeds germinated within 26 days, but only 10% reached the seedling stage due to the high mortality of germlings. Fertility, defined as the probability of a seed to originate a new plant, was estimated to be 14 × 10−4, which is higher than what is expected for most seagrasses.
- Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean-Atlantic transition regionPublication . Alberto, F.; Massa, S. I.; Manent, P.; Diaz-Almela, E.; ARNAUD-HAOND, Sophie; Duarte, C. M.; Serrão, EsterAim A central question in evolutionary ecology is the nature of environmental barriers that can limit gene flow and induce population genetic divergence, a first step towards speciation. Here we study the geographical barrier constituted by the transition zone between the Atlantic Ocean and the Mediterranean Sea, using as our model Cymodocea nodosa, a seagrass distributed throughout the Mediterranean and in the Atlantic, from central Portugal to Mauritania. We also test predictions about the genetic footprints of Pleistocene glaciations. Location The Atlantic–Mediterranean transition region and adjacent areas in the Atlantic (Mauritania to south-west Portugal) and the Mediterranean. Methods We used eight microsatellite markers to compare 20 seagrass meadows in the Atlantic and 27 meadows in the Mediterranean, focusing on the transition between these basins. Results Populations from these two regions form coherent groups containing several unique, high-frequency alleles for the Atlantic and for the Mediterranean, with some admixture west of the Almeria–Oran Front (Portugal, south-west Spain and Morocco). These are populations where only one or a few genotypes were found, for all but Cadiz, but remarkably still show the footprint of a contact zone. This extremely low genotypic richness at the Atlantic northern edge contrasts with the high values (low clonality) at the Atlantic southern edge and in most of the Mediterranean. The most divergent populations are those at the higher temperature range limits: the southernmost Atlantic populations and the easternmost Mediterranean, both potential footprints of vicariance. Main conclusions A biogeographical transition region occurs close to the Almeria–Oran front. A secondary contact zone in Atlantic Iberia and Morocco results from two distinct dispersal sources: the Mediterranean and southernmost Atlantic populations, possibly during warmer interglacial or post-glacial periods. The presence of high-frequency diagnostic alleles in present-day disjunct populations from the southernmost Atlantic region indicates that their separation from all remaining populations is ancient, and suggests an old, stable rear edge.
- Seagrass connectivity on the West Coast of Africa supports the Hypothesis of Grazer-Mediated Seed DispersalPublication . Tavares, Ana I; Assis, Jorge; Patrício, A. R.; Ferreira, Rogério; Cheikh, Mohamed Ahmed Sidi; Bandeira, Salomão; Regalla, Aissa; Santos, Iderlindo; Potouroglou, Maria; Nicolau, Suzana; Teodosio, Maria; Almada, Carmen; Santos, Rui; Pearson, Gareth; Serrao, EsterPopulation connectivity influences the distribution of genetic diversity and divergence along a species range, as the likelihood of extinction or differentiation increases in isolated populations. However, there is still poor understanding of the processes mediating inter-population dispersal in marine species that are sessile and lack planktonic life stages. One such case is the seagrass species Halodule wrightii, which produces basal seeds, although detached plants can drift. Along the tropical western coast of Africa, this species occurs in distant discontinuous habitats, raising the question of how interpopulation dispersal is mediated. The species is a key source of ecosystem functions including feeding large migratory grazers. This study aims to infer whether genetic differentiation of the seagrass H. wrightii along the western coast of Africa supports a hypothesis of predominant transportation of rafting seagrass by ocean currents, versus the hypothesis of biotic vectors of dispersal. Additional hypotheses were addressed concerning range-wide clonality and genetic diversity, assessed with microsatellite markers on populations of the west coast of Africa from Mauritania to Angola. Population genetic diversity and structure were compared with predictions from biophysical models of dispersal by oceanographic currents. The genetic data revealed low divergence among most populations, in strong contrast with predictions of very low probability of connectivity mediated by currents along the western African coastline. Moderate to high genotypic diversity showed important seed recruitment, but genetic and genotypic diversities were lower at range edges. Populations north and south of the equator were differentiated, and remarkably, so were neighboring equatorial populations despite their proximity. These results reveal independent sources of colonization of meadows in these islands, which are major habitat for migratory grazing green turtles, also supporting the hypothesis of biotically mediated seed transport. The importance of seagrass for conservation of endangered macrofauna has been widely reported; here we report evidence supporting the reciprocal role, that macrofauna protection can also plays a role in long-term survival and reproductive success of seagrass.
- Is asexual reproduction more important at geographical limits? A genetic study of the seagrass Zostera marina in the Ria Formosa, PortugalPublication . Billingham, M. R.; Reusch, T. B. H.; Alberto, F.; Serrão, EsterIn populations of species that are able to reproduce both sexually and asexually, there may be local differences with regard to the relative importance of the 2 modes of reproduction. Studies of plant species with such a life history have shown that the contribution of sexual reproduction to population maintenance may be lower at the geographical margins, with genotypic diversity often used as an indicator of the relative importance of vegetative and sexual reproduction. This hypothesis was examined in a collection of samples of eelgrass Zostera marina (a marine flowering plant) from its eastern Atlantic southern limit (Ria Formosa, Portugal). Samples from 12 sites were genotyped using 9 microsatellite loci to compare within-site clonal and genetic diversity, and among-site distribution of genetic diversity, with previously published values from central sites. Sites within the Ria Formosa had lower clonal diversities (mean = 0.29, range = 0.07 to 0.68) than the central sites (mean = 0.86, range = 0.33 to 1.00), lower levels of expected heterozygosity (He = 0.423 vs 0.486) and exhibited heterozygote excesses rather than deficits. Similarly, genetic differentiation was found to be much greater in the Ria Formosa, with the FST of 0.233 being over 10-fold greater than that reported for populations in the Baltic Sea. Results from this study were consistent with previous findings of reduced sexual reproduction, genotypic diversity and among-population gene flow at species limits.
- Toward a coordinated global observing system for seagrasses and marine macroalgaePublication . Duffy, J. Emmett; Benedetti-Cecchi, Lisandro; Trinanes, Joaquin; Muller-Karger, Frank E.; Ambo-Rappe, Rohani; Boström, Christoffer; Buschmann, Alejandro H.; Byrnes, Jarrett; Coles, Robert G.; Creed, Joel; Cullen-Unsworth, Leanne C.; Diaz-Pulido, Guillermo; Duarte, Carlos M.; Edgar, Graham J.; Fortes, Miguel; Goni, Gustavo; Hu, Chuanmin; Huang, Xiaoping; Hurd, Catriona L.; Johnson, Craig; Konar, Brenda; Krause-Jensen, Dorte; Krumhansl, Kira; Macreadie, Peter; Marsh, Helene; McKenzie, Len J.; Mieszkowska, Nova; Miloslavich, Patricia; Montes, Enrique; Nakaoka, Masahiro; Norderhaug, Kjell Magnus; Norlund, Lina M.; Orth, Robert J.; Prathep, Anchana; Putman, Nathan F.; Samper-Villarreal, Jimena; Serrao, Ester; Short, Frederick; Pinto, Isabel Sousa; Steinberg, Peter; Stuart-Smith, Rick; Unsworth, Richard K. F.; van Keulen, Mike; van Tussenbroek, Brigitta I.; Wang, Mengqiu; Waycott, Michelle; Weatherdon, Lauren V.; Wernberg, Thomas; Yaakub, Siti MaryamIn coastal waters around the world, the dominant primary producers are benthic macrophytes, including seagrasses and macroalgae, that provide habitat structure and food for diverse and abundant biological communities and drive ecosystem processes. Seagrass meadows and macroalgal forests play key roles for coastal societies, contributing to fishery yields, storm protection, biogeochemical cycling and storage, and important cultural values. These socio-economically valuable services are threatened worldwide by human activities, with substantial areas of seagrass and macroalgal forests lost over the last half-century. Tracking the status and trends in marine macrophyte cover and quality is an emerging priority for ocean and coastal management, but doing so has been challenged by limited coordination across the numerous efforts to monitor macrophytes, which vary widely in goals, methodologies, scales, capacity, governance approaches, and data availability. Here, we present a consensus assessment and recommendations on the current state of and opportunities for advancing global marine macrophyte observations, integrating contributions from a community of researchers with broad geographic and disciplinary expertise. With the increasing scale of human impacts, the time is ripe to harmonize marine macrophyte observations by building on existing networks and identifying a core set of common metrics and approaches in sampling design, field measurements, governance, capacity building, and data management. We recommend a tiered observation system, with improvement of remote sensing and remote underwater imaging to expand capacity to capture broad-scale extent at intervals of several years, coordinated with strati fied in situ sampling annually to characterize the key variables of cover and taxonomic or functional group composition, and to provide ground-truth. A robust networked system of macrophyte observations will be facilitated by establishing best practices, including standard protocols, documentation, and sharing of resources at all stages of work flow, and secure archiving of open-access data. Because such a network is necessarily distributed, sustaining it depends on close engagement of local stakeholders and focusing on building and long-term maintenance of local capacity, particularly in the developing world. Realizing these recommendations will producemore effective, efficient, and responsive observing, a more accurate global picture of change in vegetated coastal systems, and stronger international capacity for sustaining observations.
- Microsatellite markers developed through pyrosequencing allow clonal discrimination in the invasive alga Caulerpa taxifoliaPublication . ARNAUD-HAOND, Sophie; Candeias, Rui; Serrão, Ester; Teixeira, SaraPolymorphic microsatellites were developed for the invasive green algae Caulerpa taxifolia using next generation DNA sequencing. Results showed a limited rate of microsatellites for the amount of sequences, possibly explaining failure of previous attempts for microsatellite development through classical methods. Eight polymorphic loci were selected that exhibited polymorphism and a null or negligible rate of amplification failure. The number of alleles per locus ranged from two to seven. The reconstruction of Multi Locus Genotypes and the heterozygosity and departure from Hardy–Weinberg equilibrium confirmed the influence of clonal reproduction and showed the usefulness of this set of markers to successfully discriminate clonal lineages and analyze the clonal and genetic composition of algal beds. These markers will be used to further investigate the clonal composition and genetic structure in populations of C. taxifolia and to attempt retracing the origin of and pathways followed by invasive clonal lineages.
- Genetic diversity of a clonal angiosperm near its range limit: The case of Cymodocea nodosa at the Canary IslandsPublication . Alberto, F.; ARNAUD-HAOND, Sophie; Duarte, C. M.; Serrão, EsterThe seagrass Cymodocea nodosa forms a unique community in the Canary Islands, where it is classified as an endangered species. Biogeographic theory predicts that clonal species on islands near their distributional limits might show lower proportions of sexual (versus clonal) reproduction, lower genetic diversity, and higher differentiation. We addressed these hypotheses by comparing the genetic structure of C. nodosa from 10 meadows in the 4 main Canary Islands with2Iberian sites (Atlantic and Mediterranean) using microsatellites. A resampling method was proposed to standardize, among samples, genetic variability statistics estimating genotypic richness (R) and allelic richness (Â). A high degree of genotypic richness at the Canary Islands (R = 0.30 – 0.94, mean = 0.67) relative to Iberian sites revealed that C. nodosa performs effective sexual reproduction here. In contrast, lower  suggested a founder effect during the colonization of the archipelago, and similar allelic composition across all islands indicated colonization from a single source. A hotspot of genetic diversity was observed in El Medano (Tenerife), probably associated with lower drift in this meadow, the largest of the archipelago. Predominant north-south surface currents and a greater distance to the mainland could explain lower allelic richness of 2 northwestern sites on different islands and greater similarity between them. All meadows were differentiated from each other and there was no correlation between genetic and geographic distances. This non-equilibrium migration-mutation system was therefore mostly influenced by diversity resulting from genetic drift, and less by the homogenizing effects of gene flow.