Assessing the influence of sewage outfalls on seagrass meadows using nitrogen isotopes.

Untreated sewage discharged increases the nutrient loads and changes ecosystem functions. It increases the values of the nitrogen isotopic signature (δ15N) of primary producers such as seagrasses. Itaparica Island (Bahia, Brazil) has undergone extensive urbanization over 50 years. Most of the island has no sewage treatment, and a bridge's construction could increase its population ten times. We evaluated the effects of sewage inputs on the δ15N of seagrass (Halodule wrightii) across Itaparica Island in 14 areas of the island with different degrees of urbanization. Average values of δ15N ranged from -3.95 ‰ (±1.04 SD) to 2.73 ‰ (±1.61). The highest human occupation site also has the highest mean value of δ15N, and seagrass shoot density. The significant correlation (p < 0.05) between δ15N values and shoot density may indicate a possible anthropogenic pressure impacting meadow abundance. Despite a positive correlation, increased anthropogenic nutrient supply can support algae growth and harm seagrass ecosystems.

Long range gene flow beyond predictions from oceanographic transport in a tropical marine foundation species.

The transport of passively dispersed organisms across tropical margins remains poorly understood. Hypotheses of oceanographic transportation potential lack testing with large scale empirical data. To address this gap, we used the seagrass species, Halodule wrightii, which is unique in spanning the entire tropical Atlantic. We tested the hypothesis that genetic differentiation estimated across its large-scale biogeographic range can be predicted by simulated oceanographic transport. The alternative hypothesis posits that dispersal is independent of ocean currents, such as transport by grazers. We compared empirical genetic estimates and modelled predictions of dispersal along the distribution of H. wrightii. We genotyped eight microsatellite loci on 19 populations distributed across Atlantic Africa, Gulf of Mexico, Caribbean, Brazil and developed a biophysical model with high-resolution ocean currents. Genetic data revealed low gene flow and highest differentiation between (1) the Gulf of Mexico and two other regions: (2) Caribbean-Brazil and (3) Atlantic Africa. These two were more genetically similar despite separation by an ocean. The biophysical model indicated low or no probability of passive dispersal among populations and did not match the empirical genetic data. The results support the alternative hypothesis of a role for active dispersal vectors like grazers.

Long-term monitoring projects of Brazilian marine and coastal ecosystems.

Biodiversity assessment is a mandatory task for sustainable and adaptive management for the next decade, and long-term ecological monitoring programs are a cornerstone for understanding changes in ecosystems. The Brazilian Long-Term Ecological Research Program (PELD) is an integrated effort model supported by public funds that finance ecological studies at 34 locations. By interviewing and compiling data from project coordinators, we assessed monitoring efforts, targeting biological groups and scientific production from nine PELD projects encompassing coastal lagoons to mesophotic reefs and oceanic islands. Reef environments and fish groups were the most often studied within the long-term projects. PELD projects covered priority areas for conservation but missed sensitive areas close to large cities, as well as underrepresenting ecosystems on the North and Northeast Brazilian coast. Long-term monitoring projects in marine and coastal environments in Brazil are recent (<5 years), not yet integrated as a network, but scientifically productive with considerable relevance for academic and human resources training. Scientific production increased exponentially with project age, despite interruption and shortage of funding during their history. From our diagnosis, we recommend some actions to fill in observed gaps, such as: enhancing projects' collaboration and integration; focusing on priority regions for new projects; broadening the scope of monitored variables; and, maintenance of funding for existing projects.

Environmental settings of seagrass meadows control rare earth element distribution and transfer from soil to plant compartments.

The role of seagrass meadows in the cycling and accumulation of rare earth elements and yttrium (REEY) is unknown. Here, we measured the concentration of REEY in the different compartments of Halodule wrightii (shoots, rhizomes, and roots) and soils in seagrass meadows near sandy beaches, mangroves, and coral reefs in the Todos os Santos Bay, Brazil. We provide data on the accumulation dynamics of REEY in seagrass compartments and demonstrate that plant compartments and soil properties determine accumulation patterns. The ∑REEY in soils were ~1.7-fold higher near coral reefs (93.0 ±â€¯5.61 mg kg-1) than near mangrove sites (53.9 ±â€¯31.5 mg kg-1) and were slightly higher than in sandy beaches (81.7 ±â€¯49.1 mg kg-1). The ∑REEY in seagrasses varied between 35.4 ±â€¯28.1 mg kg-1 near coral reefs to 59.2 ±â€¯21.3 mg kg-1 near sandy beaches, respectively. The ∑REE bioaccumulation factor (BAF) was highest in seagrass roots near sandy beaches (BAF = 0.67 ±â€¯0.48). All values of ∑REE translocation are <1, indicating inefficient translocation of REE from roots to rhizome to shoot. PAAS normalized REE was enriched in light REE (LREE) over heavy REE (HREE). The REEY accumulation in Halodule wrightii revealed a low potential of the seagrass to act as a sink for these elements. However, their bioavailability and potential uptake may change with soil properties. Our results serve as a basis for a better understanding of REE biogeochemical cycling and its fate in the marine environment. REE have experienced increased use as they are central to new technologies revealing an urgent need for further investigations of potential impacts on coastal ecosystems.

Generalized Linear Models outperform commonly used canonical analysis in estimating spatial structure of presence/absence data.

BACKGROUND: Ecological communities tend to be spatially structured due to environmental gradients and/or spatially contagious processes such as growth, dispersion and species interactions. Data transformation followed by usage of algorithms such as Redundancy Analysis (RDA) is a fairly common approach in studies searching for spatial structure in ecological communities, despite recent suggestions advocating the use of Generalized Linear Models (GLMs). Here, we compared the performance of GLMs and RDA in describing spatial structure in ecological community composition data. We simulated realistic presence/absence data typical of many ß-diversity studies. For model selection we used standard methods commonly used in most studies involving RDA and GLMs. METHODS: We simulated communities with known spatial structure, based on three real spatial community presence/absence datasets (one terrestrial, one marine and one freshwater). We used spatial eigenvectors as explanatory variables. We varied the number of non-zero coefficients of the spatial variables, and the spatial scales with which these coefficients were associated and then compared the performance of GLMs and RDA frameworks to correctly retrieve the spatial patterns contained in the simulated communities. We used two different methods for model selection, Forward Selection (FW) for RDA and the Akaike Information Criterion (AIC) for GLMs. The performance of each method was assessed by scoring overall accuracy as the proportion of variables whose inclusion/exclusion status was correct, and by distinguishing which kind of error was observed for each method. We also assessed whether errors in variable selection could affect the interpretation of spatial structure. RESULTS: Overall GLM with AIC-based model selection (GLM/AIC) performed better than RDA/FW in selecting spatial explanatory variables, although under some simulations the methods performed similarly. In general, RDA/FW performed unpredictably, often retaining too many explanatory variables and selecting variables associated with incorrect spatial scales. The spatial scale of the pattern had a negligible effect on GLM/AIC performance but consistently affected RDA's error rates under almost all scenarios. CONCLUSION: We encourage the use of GLM/AIC for studies searching for spatial drivers of species presence/absence patterns, since this framework outperformed RDA/FW in situations most likely to be found in natural communities. It is likely that such recommendations might extend to other types of explanatory variables.

Atlantia, a new genus of Dendrophylliidae (Cnidaria, Anthozoa, Scleractinia) from the eastern Atlantic.

Atlantia is described as a new genus pertaining to the family Dendrophylliidae (Anthozoa, Scleractinia) based on specimens from Cape Verde, eastern Atlantic. This taxon was first recognized as Enallopsammia micranthus and later described as a new species, Tubastraea caboverdiana, which then changed the status of the genus Tubastraea as native to the Atlantic Ocean. Here, based on morphological and molecular analyses, we compare fresh material of T. caboverdiana to other dendrophylliid genera and describe it as a new genus named Atlantia in order to better accommodate this species. Evolutionary reconstruction based on two mitochondrial and one nuclear marker for 67 dendrophylliids and one poritid species recovered A. caboverdiana as an isolated clade not related to Tubastraea and more closely related to Dendrophyllia cornigera and Leptopsammia pruvoti. Atlantia differs from Tubastraea by having a phaceloid to dendroid growth form with new corallites budding at an acute angle from the theca of a parent corallite. The genus also has normally arranged septa (not Portualès Plan), poorly developed columella, and a shallow-water distribution all supporting the classification as a new genus. Our results corroborate the monophyly of the genus Tubastraea and reiterate the Atlantic non-indigenous status for the genus. In the light of the results presented herein, we recommend an extensive review of shallow-water dendrophylliids from the Eastern Atlantic.

Trends in the detection of aquatic non-indigenous species across global marine, estuarine and freshwater ecosystems: A 50-year perspective.

Aim: The introduction of aquatic non-indigenous species (ANS) has become a major driver for global changes in species biogeography. We examined spatial patterns and temporal trends of ANS detections since 1965 to inform conservation policy and management. Location: Global. Methods: We assembled an extensive dataset of first records of detection of ANS (1965-2015) across 49 aquatic ecosystems, including the (a) year of first collection, (b) population status and (c) potential pathway(s) of introduction. Data were analysed at global and regional levels to assess patterns of detection rate, richness and transport pathways. Results: An annual mean of 43 (±16 SD) primary detections of ANS occurred-one new detection every 8.4 days for 50 years. The global rate of detections was relatively stable during 1965-1995, but increased rapidly after this time, peaking at roughly 66 primary detections per year during 2005-2010 and then declining marginally. Detection rates were variable within and across regions through time. Arthropods, molluscs and fishes were the most frequently reported ANS. Most ANS were likely introduced as stowaways in ships' ballast water or biofouling, although direct evidence is typically absent. Main conclusions: This synthesis highlights the magnitude of recent ANS detections, yet almost certainly represents an underestimate as many ANS go unreported due to limited search effort and diminishing taxonomic expertise. Temporal rates of detection are also confounded by reporting lags, likely contributing to the lower detection rate observed in recent years. There is a critical need to implement standardized, repeated methods across regions and taxa to improve the quality of global-scale comparisons and sustain core measures over longer time-scales. It will be fundamental to fill in knowledge gaps given that invasion data representing broad regions of the world's oceans are not yet readily available and to maintain knowledge pipelines for adaptive management.

A meta-analysis shows that seaweeds surpass plants, setting life-on-Earth's limit for biomass packing.

BACKGROUND: As plants, algae and some sessile invertebrates may grow in nearly monospecific assemblies, their collective biomass increases and if they compete hard enough some die, freeing up space. The concurrent increase in biomass and decrease in density is called self-thinning, and its trajectory over time or maximum values represent a boundary condition. For a single stand developing over time the boundary defines the carrying capacity of the environment but the most extreme trajectories emulate the efficiency of species in packing biomass into space. RESULTS: Here we present a meta-analysis of compiled data on biomass and density from 56 studies of 42 species of seaweeds from 8 orders within 3 phyla scattered through the world's oceans. Our analysis shows that, with respect to biomass, seaweeds are the most efficient space occupiers on Earth because they transgress previously fixed limits derived from land plants. This is probably because seaweeds are not limited by water and do not need structures for its transport or for transpiration; they photosynthesise and uptake nutrients over their entire surface; they are attached to the substrate by holdfasts that are small proportional to their volume or weight compared to roots; water provides them better support, reducing the need for tissues for rigidity. We also identified a biomass concentration common to plants and seaweeds which represents the threshold that no life on the planet can pass. Using each stand's distance to the biomass-density boundary, we determined that within the seaweeds the efficiency of space occupation differed amongst taxonomic and functional groups as well as with clonality and latitude. CONCLUSIONS: Algae occupy space more efficiently than plants, most likely because the watery environment facilitates the physical processes and integration of space occupation. The distance-to-the-boundary proves a good metric to discriminate among groups and may be useful for comparison of the most efficient biomass producing systems, or for the identification of systems impacted by pollution.

A model for the biomass-density dynamics of seagrasses developed and calibrated on global data.

BACKGROUND: Seagrasses are foundation species in estuarine and lagoon systems, providing a wide array of services for the ecosystem and the human population. Understanding the dynamics of their stands is essential in order to better assess natural and anthropogenic impacts. It is usually considered that healthy seagrasses aim to maximize their stand biomass (g DW m-2) which may be constrained by resource availability i.e., the local environment sets a carrying capacity. Recently, this paradigm has been tested and reassessed, and it is believed that seagrasses actually maximize their efficiency of space occupation-i.e., aim to reach an interspecific boundary line (IBL)-as quick as possible. This requires that they simultaneously grow in biomass and iterate new shoots to increase density. However, this strategy depresses their biomass potential. RESULTS: to comply with this new paradigm, we developed a seagrass growth model that updates the carrying capacities for biomass and shoot density from the seagrass IBL at each time step. The use of a joint biomass and density growth rates enabled parameter estimation with twice the sample sizes and made the model less sensitive to episodic error in either of the variables. The use of instantaneous growth rates enabled the model to be calibrated with data sampled at widely different time intervals. We used data from 24 studies of six seagrass species scattered worldwide. The forecasted allometric biomass-density growth trajectories fit these observations well. Maximum growth and decay rates were found consistently for each species. The growth rates varied seasonally, matching previous observations. CONCLUSIONS: State-of-art models predicting both biomass and shoot density in seagrass have not previously incorporated our observation across many seagrass species that dynamics depend on current state relative to IBL. Our model better simulates the biomass-density dynamics of seagrass stands while shedding light on its intricacies. However, it is only valid for established patches where dynamics involve space-filling, not for colonization of new areas.

The biomass-density relationship in seagrasses and its use as an ecological indicator.

BACKGROUND: Biomass-density relations have been at the centre of a search for an index which describes the health of seagrass meadows. However, this search has been complicated by the intricacy of seagrass demographics and their complex biomass-density relations, a consequence mainly of their modular growth and clonality. Concomitantly, biomass-density upper boundaries have been determined for terrestrial plants and algae, reflecting their asymptotic maximum efficiencies of space occupation. Each stand's distance to its respective biomass-density upper boundary reflects its effective efficiency in packing biomass, which has proved a reliable ecological indicator in order to discriminate between taxonomic groups, functional groups and clonal vs. non-clonal growth. RESULTS: We gathered data from 32 studies on 10 seagrass species distributed worldwide and demonstrated that seagrasses are limited by their own boundary line, placed below the boundaries previously determined for algae and terrestrial plants. Then, we applied a new metric-dgrass: each stand's perpendicular distance to the seagrass boundary-and used this parameter to review fundamental aspects such as clonal growth patterns, depth distribution, seasonality, interspecific competition, and the effects of light, temperature and nutrients. CONCLUSIONS: Seagrasses occupy space less efficiently than algae and terrestrial plants. Using only their biomass and density data we established a new and efficient tool to describe space occupation by seagrasses. This was used with success to evaluate their meadows as an ecological indicator for the health of coastal ecosystems.

Seagrass ecosystem services - What's next?

Seagrasses, marine flowering plants, provide a wide range of ecosystem services, defined here as natural processes and components that directly or indirectly benefit human needs. Recent research has shown that there are still many gaps in our comprehension of seagrass ecosystem service provision. Furthermore, there seems to be little public knowledge of seagrasses in general and the benefits they provide. This begs the questions: how do we move forward with the information we have? What other information do we need and what actions do we need to take in order to improve the situation and appreciation for seagrass? Based on the outcomes from an international expert knowledge eliciting workshop, three key areas to advance seagrass ecosystem service research were identified: 1) Variability of ecosystem services within seagrass meadows and among different meadows; 2) Seagrass ecosystem services in relation to, and their connection with, other coastal habitats; and 3) Improvement in the communication of seagrass ecosystem services to the public. Here we present ways forward to advance seagrass ecosystem service research in order to raise the profile of seagrass globally, as a means to establish more effective conservation and restoration of these important coastal habitats around the world.

Clone wars: asexual reproduction dominates in the invasive range of Tubastraea spp. (Anthozoa: Scleractinia) in the South-Atlantic Ocean.

Although the invasive azooxanthellate corals Tubastraea coccinea and T. tagusensis are spreading quickly and outcompeting native species in the Atlantic Ocean, there is little information regarding the genetic structure and path of introduction for these species. Here we present the first data on genetic diversity and clonal structure from these two species using a new set of microsatellite markers. High proportions of clones were observed, indicating that asexual reproduction has a major role in the local population dynamics and, therefore, represents one of the main reasons for the invasion success. Although no significant population structure was found, results suggest the occurrence of multiple invasions for T. coccinea and also that both species are being transported along the coast by vectors such as oil platforms and monobouys, spreading these invasive species. In addition to the description of novel microsatellite markers, this study sheds new light into the invasive process of Tubastraea.

Correction: Seagrass Ecosystem Services and Their Variability across Genera and Geographical Regions.

[This corrects the article DOI: 10.1371/journal.pone.0163091.].

Seagrass Ecosystem Services and Their Variability across Genera and Geographical Regions.

Threats to and loss of seagrass ecosystems globally, impact not only natural resources but also the lives of people who directly or indirectly depend on these systems. Seagrass ecosystems play a multi-functional role in human well-being, e.g. food through fisheries, control of erosion and protection against floods. Quantifying these services reveals their contributions to human well-being and helps justify seagrass conservation. There has been no comprehensive assessment as to whether seagrass ecosystem services are perceived to vary over the globe or amongst genera. Our study compiles the most complete list of ecosystem services provided by seagrasses so far, including bioregional- and genus-specific information from expert opinion and published studies. Several seagrass ecosystem services vary considerably in their (known) provision across genera and over the globe. Seagrasses genera are clearly not all equal with regard to the ecosystem services they provide. As seagrass genera are not evenly distributed over all bioregions, the presence of an ecosystem service sometimes depends on the genera present. Larger sized seagrass genera (e.g. Posidonia, Enhalus) are perceived to provide more substantial and a wider variety of ecosystem services than smaller species (e.g. Halophila, Lepilaena). Nevertheless, smaller species provide important services. Our findings point out data gaps, provide new insight for more efficient management and recommend caution in economic valuation of seagrass services worldwide.

Occurrence of an invasive coral in the southwest Atlantic and comparison with a congener suggest potential niche expansion.

Tubastraea tagusensis, a coral native to the Galapagos Archipelago, has successfully established and invaded the Brazilian coast where it modifies native tropical rocky shore and coral reef communities. In order to understand the processes underlying the establishment of T. tagusensis, we tested whether Maxent, a tool for species distribution modeling, based on the native range of T. tagusensis correctly forecasted the invasion range of this species in Brazil. The Maxent algorithm was unable to predict the Brazilian coast as a suitable environment for the establishment of T. tagusensis. A comparison between these models and a principal component analysis (PCA) allowed us to examine the environmental dissimilarity between the two occupied regions (native and invaded) and to assess the species' occupied niche breadth. According to the PCA results, lower levels of chlorophyll-a and nitrate on the Atlantic coast segregate the Brazilian and Galapagos environments, implying that T. tagusensis may have expanded its realized niche during the invasion process. We tested the possible realized niche expansion in T. tagusensis by assuming that Tubastraea spp. have similar fundamental niches, which was supported by exploring the environmental space of T. coccinea, a tropical-cosmopolitan congener of T. tagusensis. We believe that the usage of Maxent should be treated with caution, especially when applied to biological invasion (or climate change) scenarios where the target species has a highly localized native (original) distribution, which may represent only a small portion of its fundamental niche, and therefore a violation of a SDM assumption.

Effect of phase shift from corals to Zoantharia on reef fish assemblages.

Consequences of reef phase shifts on fish communities remain poorly understood. Studies on the causes, effects and consequences of phase shifts on reef fish communities have only been considered for coral-to-macroalgae shifts. Therefore, there is a large information gap regarding the consequences of novel phase shifts and how these kinds of phase shifts impact on fish assemblages. This study aimed to compare the fish assemblages on reefs under normal conditions (relatively high cover of corals) to those which have shifted to a dominance of the zoantharian Palythoa cf. variabilis on coral reefs in Todos os Santos Bay (TSB), Brazilian eastern coast. We examined eight reefs, where we estimated cover of corals and P. cf. variabilis and coral reef fish richness, abundance and body size. Fish richness differed significantly between normal reefs (48 species) and phase-shift reefs (38 species), a 20% reduction in species. However there was no difference in fish abundance between normal and phase shift reefs. One fish species, Chaetodon striatus, was significantly less abundant on normal reefs. The differences in fish assemblages between different reef phases was due to differences in trophic groups of fish; on normal reefs carnivorous fishes were more abundant, while on phase shift reefs mobile invertivores dominated.

Control of invasive marine invertebrates: an experimental evaluation of the use of low salinity for managing pest corals (Tubastraea spp.).

This study investigated the use of low salinity as a killing agent for the invasive pest corals Tubastraea coccinea and Tubastraea tagusensis (Dendrophylliidae). Experiments investigated the efficacy of different salinities, the effect of colony size on susceptibility and the influence of length of exposure. Experimental treatments of colonies were carried out in aquaria. Colonies were then fixed onto experimental plates and monitored in the field periodically over a period of four weeks. The killing effectiveness of low salinity depended on the test salinity and the target species, but was independent of colony size. Low salinity was fast acting and prejudicial to survival: discoloration, necrosis, fragmenting and sloughing, exposure of the skeleton and cover by biofoulers occurred post treatment. For T. tagusensis, 50% mortality (LC50) after three days occurred at eight practical salinity units (PSU); for T. coccinea the LC50 was 2 PSU. Exposure to freshwater for 45-120 min resulted in 100% mortality for T. tagusensis, but only the 120 min period was 100% effective in killing T. coccinea. Freshwater is now routinely used for the post-border management of Tubastraea spp. This study also provides insights as to how freshwater may be used as a routine biosecurity management tool when applied pre-border to shipping vectors potentially transporting non-indigenous marine biofouling species.

Improving the construction of functional models of alternative persistent states in coral reefs using insights from ongoing research programs: a discussion paper.

Extensive degradation of coral reefs makes it imperative to create functional models that demonstrate ecological processes which occur in alternative states that persist over time. These models provide important information that can help in decision making regarding management measures for both the prevention of further degradation and the recovery of these ecosystems. Development of these models requires identifying and testing the ecological processes that will impose the reduction of coral cover and, preferably, identifying the disturbance that triggers this phenomenon. For this reason, research programs are a useful tool which allows a focus on the production of information for modeling. It should start with survey investigations and tests of hypotheses concerning the cause of the reduction of coral cover. Subsequently, projects should be guided by the most probable hypotheses, focusing on one guild or functional group at a time until the "trigger" process which unleashed the disturbance is identified. Even if incomplete, these models already provide information for focusing management steps.