Diversity of European seagrass indicators: patterns within and across regions

Seagrasses are key components of coastal marine ecosystems and many monitoring programmes worldwide assess seagrass health and apply seagrasses as indicators of environmental status. This study aims at identifying the diversity and characteristics of seagrass indicators in use within and across European ecoregions in order to provide an overview of seagrass monitoring effort in Europe. We identified 49 seagrass indicators used in 42 monitoring programmes and including a total of 51 metrics. The seagrass metrics represented 6 broad categories covering different seagrass organizational levels and spatial scales. The large diversity is particularly striking considering that the pan-European Water Framework Directive sets common demands for the presence and abundance of seagrasses and related disturbance-sensitive species. The diversity of indicators reduces the possibility to provide pan-European overviews of the status of seagrass ecosystems. The diversity can be partially justified by differences in species, differences in habitat conditions and associated communities but also seems to be determined by tradition. Within each European region, we strongly encourage the evaluation of seagrass indicator–pressure responses and quantification of the uncertainty of classification associated to the indicator in order to identify the most effective seagrass indicators for assessing ecological quality of coastal and transitional water bodies.     

A biotic index using the seagrass Posidonia oceanica (BiPo), to evaluate ecological status of coastal waters

The development of ecologically based indices that respond to disturbances in a predictable manner has been stressed by the EU Water Framework Directive. The seagrass Posidonia oceanica, given its ecological indicator characteristics, has been identified as one of the elements to determine ecological status under the EU Water Framework Directive. The purpose of this study is therefore to develop a biotic index based on P. oceanica (BiPo), focussing on: (i) the necessity of an index that may be applied over the largest geographical extent possible, (ii) the necessity of a tool for a baseline evaluation of P. oceanica status in the Mediterranean, (iii) the compliance with WFD requirements, (iv) the efficiency of the method in terms of reliability and cost. The BiPo index is developed on the basis of all P. oceanica monitoring data available in the western Mediterranean and on a standard assessment of anthropogenic pressures. The index metrics are selected and evaluated on the basis of this pressures assessment, and are subsequently integrated for the evaluation of ecological status. The index is then tested on 15 sites around Corsica (France). The results show that the BiPo well reflects meadow health status and ecological status. Furthermore it is reliable, standard and cost-effective, and can be applied to a wide array of management and conservation purposes.     

Modelling seagrass growth and development to evaluate transplanting strategies for restoration

Background and Aims

Seagrasses are important marine plants that are under threat globally. Restoration by transplanting vegetative fragments or seedlings into areas where seagrasses have been lost is possible, but long-term trial data are limited. The goal of this study is to use available short-term data to predict long-term outcomes of transplanting seagrass.

Methods

A functional–structural plant model of seagrass growth that integrates data collected from short-term trials and experiments is presented. The model was parameterized for the species Posidonia australis, a limited validation of the model against independent data and a sensitivity analysis were conducted and the model was used to conduct a preliminary evaluation of different transplanting strategies.

Key Results

The limited validation was successful, and reasonable long-term outcomes could be predicted, based only on short-term data.

Conclusions

This approach for modelling seagrass growth and development enables long-term predictions of the outcomes to be made from different strategies for transplanting seagrass, even when empirical long-term data are difficult or impossible to collect. More validation is required to improve confidence in the model''s predictions, and inclusion of more mechanism will extend the model''s usefulness. Marine restoration represents a novel application of functional–structural plant modelling.     

A new procedure for comparing class boundaries of biological assessment methods: A case study from the Danube Basin

For the implementation of the European Water Framework Directive class boundaries of biological assessment methods need to be intercalibrated. The most commonly applied intercalibration approach of national river assessment methods in Europe requires data on near-natural reference sites; however, these data are generally scarce. We developed an alternative approach based on sites impacted by similar levels of disturbance and tested it with national assessment methods based on diatoms and benthic invertebrates from countries in the Danube River Basin. Using environmental variables we screened for sampling sites of at least good environmental status. Relations between different assessment methods were established by common metrics, and we standardized these metrics by “biological benchmarks” obtained from the screened datasets. This approach allows for intercalibration even if near-natural reference sites are absent; relatively few and easily available data are required.     

A new method to assess water trophy and organic pollution – the Macrophyte Biological Index for Rivers (IBMR): its application to different types of river and pollution

The paper presents a new index for assessing water trophy and organic pollution. It is based on only true aquatic macrophytes – being calculated on species score, coefficient of ecological amplitude and degree of cover. The method was tested in an acidic lowland river and an alkaline mountain river, and is shown to be validated by bio-indication scales based on macrophyte communities. The practical interest is discussed regarding the Water Framework Directive. Electronic Supplementary Material Electronic supplementary material is available for this article atand accessible for authorised users.     

Estimating confidence of European WFD ecological status class and WISER Bioassessment Uncertainty Guidance Software (WISERBUGS)

The Water Framework Directive (WFD) requires estimates of the confidence and precision associated with any scheme for assessing and monitoring the ecological status class of any European rivers, lakes, transitional or coastal waters. This is a complex important issue, especially for waterbody assessments based on multiple metrics and/or two or more taxonomic groups. This paper aims to contribute towards improving understanding and providing practical approaches to assessing confidence of class by (i) discussing the various sources and causes of uncertainty, (ii) using UK rivers macroinvertebrate datasets to illustrate the estimation of replicate, temporal and spatial variance components and the implications for water body metric precision, confidence of class and optimal sampling design, (iii) introducing new freely available general software WISER Bioassessment Uncertainty Guidance Software (WISERBUGS) which uses prior sampling uncertainty estimates with user-specified metrics, class limits and metric combination rules to simulate the joint sampling uncertainty in metric EQR values and provide estimates of confidence of class based on individual metrics, (optionally weighted) multi-metric indices and/or multi-metric classification rules (worst case, mean or median class) based on one or more WFD biological quality elements.     

Response of fish-based metrics to anthropogenic pressures in temperate rocky reefs

The increasing degradation of marine ecosystems as a result of increasing impact caused by anthropogenic pressures, urges for well-founded knowledge to develop efficient tools to appraise the quality status of fish assemblages, as required by the “Marine Strategy Framework Directive”. This study analyzed the structural and functional response of rocky fish assemblages to several pressures on the Portuguese coast, i.e. fishing, sewage discharges, port activities and thermal effluent, by selecting fish-based metrics that best distinguished disturbed from control areas. One of the novel aspects of this research is the integrated assessment made through the analysis of several metrics representing numerous attributes of fish assemblages (namely diversity, abundance, trophic structure, mobility, resilience, habitat association, nursery function), which contrasts with the most commonly used approaches that in general focus on fish species/families. PERMANOVA results showed significant differences on metrics composition for all pressures with the exception of the thermal effluent. Moreover, two major patterns of stress were identified: (1) selective pressure, which affects differentially the fish assemblages (fishing); (2) broad-range pressure, which affects the entire fish assemblage with metrics of several attributes (e.g. structure, resilience, trophic guilds, nursery function) responding to its presence (sewage discharges, port activities). Taking into account the sensitivity results (discriminant analysis and Mann–Whitney test), biological meaning and redundancy with other metrics (Spearman correlations), the following metrics were selected as the most suitable to detect changes on temperate reef fish assemblages: “density of generalist individuals”, “density of territorial individuals”, “density of large individuals with medium to high commercial value (>20 cm)”, “density of juveniles” and metrics relative to trophic guild (except zooplanktivores). Since metrics grouped species that have some degree of functional overlap, the present approach was useful to understand human-induced changes at the assemblage level, contributing for the future use of marine fishes as biological indicators.     

Marine angiosperm indices used to assess ecological status within the Water Framework Directive and South African National Water Act: Learning from differences and common issues

This paper reviews and discusses the methods and metrics used for the assessment of the ecological status of marine angiosperms comparing the European with the South African situation. In Europe salt marsh and seagrasses are an important biological element for establishing the ecological quality status of transitional waters and in South Africa changes over time in the salt marsh and submerged macrophyte habitats (species richness, abundance and community composition) is used nationally to assess the health of estuaries. In Europe several studies have developed metrics that include salt marsh species composition and community structure to assess the ecological quality status. Deviation of taxonomic composition and abundance from a reference situation is investigated. Multi-metric approaches have been shown to provide a more holistic view of the ecological status of the ecosystem. Many indices are highly dependent on historical data to assess the deviation from reference conditions. Within the WFD spirit one widely used approach for salt marsh assessment, the Best’s method, the baseline can be determined based on the first sampling effort, by the largest previously recorded size of the salt marsh or using the “maximum potential size” of the salt marsh from habitat prediction models. In South Africa all habitat below the 5 m contour line is considered estuary habitat and any land occupied here by agricultural or other developments is considered as a loss of habitat from the reference condition. For seagrasses European metrics are based on attributes from the community (e.g., taxonomic composition, epiphytes), the population (e.g., bed extent, shoots density), but also quantified at individual species (e.g., leaves length) or physiological levels (e.g., stable isotopic signatures). Seagrass habitats in South African estuaries are highly dynamic in response to floods and an understanding of this is needed before present ecological status can be assessed.     

Assessing the condition of lake habitats: a test of methods for surveying aquatic macrophyte communities

The European Union requires member states to monitor the conservation status of water bodies designated under the Habitats and Species Directive. In the UK, macrophytes were identified as useful indicators of conservation status but it was recognised that sampling methods required assessment before nationwide survey work began. At eight lakes, which varied in size (0.9–2797 ha) and trophic status (oligotrophic–eutrophic), we tested a method which uses a combination of three techniques (boat transects, wader transects and perimeter strandline searches) to characterise repeat sectors (six or fewer). The combination of techniques used at a particular lake depended on the accessibility of each sector, the safety of applying the method, expediency and target flora. Species richness and abundance were recorded. By applying indicator metrics/rules to data produced by the method it was possible to categorise the conservation and trophic status of the lakes. Power analysis revealed that the data were statistically robust and could potentially be used to track significant, lake-specific changes in macrophyte flora through time. This analysis also revealed a decreasing return in statistical certainty with increased sampling effort (number of sectors sampled). Little additional certainty was added when more than 4 sectors were sampled per lake. The wader transects proved the most practical means of collecting quantitative data while perimeter surveys were an efficient means of adding useful supplementary semi-quantitative data. Boat surveys, although useful in some situations, particularly in assessing deeper water vegetation, were more time consuming than wader surveys. The potential applications and limitations of these methods are discussed and further tests suggested.     

Back to the sea twice: identifying candidate plant genes for molecular evolution to marine life

Background  

Seagrasses are a polyphyletic group of monocotyledonous angiosperms that have adapted to a completely submerged lifestyle in marine waters. Here, we exploit two collections of expressed sequence tags (ESTs) of two wide-spread and ecologically important seagrass species, the Mediterranean seagrass Posidonia oceanica (L.) Delile and the eelgrass Zostera marina L., which have independently evolved from aquatic ancestors. This replicated, yet independent evolutionary history facilitates the identification of traits that may have evolved in parallel and are possible instrumental candidates for adaptation to a marine habitat.     

Seagrass Quality Index (SQI), a Water Framework Directive compliant tool for the assessment of transitional and coastal intertidal areas

This work describes a new method for assessing the ecological quality of intertidal seagrass in estuaries and coastal systems, the Seagrass Quality Index (SQI). The design of the SQI aims to fulfil the Water Framework Directive requirements in terms of compliance (e.g., metrics, sampling procedure, pressure relationship, uncertainty of misclassification and comparability to other methodologies in terms of concept). The index includes three common and easy-to-measure structural parameters of seagrass (i.e., the no. of taxa, bed extent and shoot density) combined in a calculation rule that allows the index to report all five of the quality classes (i.e., high, good, moderate, poor and bad). The present study contains analyses of the relationships between the ecosystem-quality results produced by the index and the pressures measured in the system as well as the relationships between the SQI and the seagrass parameters composing it (both the correlation between the SQI and metrics and the SQI sensitivity to the individual variation of each metric). These relationships were tested using a Spearman rank-correlation analysis, producing significant correlations between the biological metrics and the index results as well as between the index results and the environmental quality-pressure category (i.e., the concentration of winter DIN and turbidity). In terms of management, it is possible to apply the methodology on a broad geographical scale in systems where the reference condition for the number of taxa is even higher than one (for the Mondego studied here, the reference value was one species). The tool fulfilled the WFD requirements, had a robust sampling design and proved to be able to track the inertia that usually exists from the moment the pressure is alleviated as well as the biological response that characterises the recovery phase in systems under restoration.     

Intertidal seagrass in Ireland: Pressures,WFD status and an assessment of trace element contamination in intertidal habitats using Zostera noltei

Intertidal seagrass has been selected as a Biological Quality Element for the assessment of ecological status under the Water Framework Directive. In Ireland, two species of seagrass, Zostera marina and Z. noltei occur in intertidal habitats. This study presents the first comprehensive assessment of the distribution and Water Framework Directive status of intertidal seagrass in the Republic of Ireland and Northern Ireland. Most of the areas assessed, using the Water Framework Directive-compliant assessment tool, have a status of HIGH or GOOD. Only two areas were found to have a status less than GOOD and in both, the cause for the decline was smothering by opportunistic foliose green macroalgae. Linear regression showed a relationship between pressure index scores and Ecological Quality Ratio, showing the relevance of the index as a metric of anthropogenic pressure. Trace element concentrations were examined in Z. noltei tissues and Trace Element Pollution Index values were calculated. The relationship between Trace Element contamination and Water Framework Directive status was examined but the results showed little correlation. However, a relationship between the pressure index and trace element contamination was obtained. This assessment provides the most comprehensive overview of intertidal seagrass beds in Ireland and establishes a strong baseline for ongoing monitoring and assessment under the Water Framework Directive. The data provide key information on the pressures affecting these valuable habitats which will assist in the development of measures to improve and protect our transitional and coastal waters.     

The DD-carboxypeptidase activity encoded by pbp4B is not essential for the cell growth of Escherichia coli

The gene (pbp4B) encoding a putative DD-carboxypeptidase has been deleted in Escherichia coli and it is shown to be not essential for cell division. Disruption of the gene in a genetic background where all putative activities of DD-carboxypeptidases and/or DD-endopeptidases had been eliminated indicates that these activities are not required for cell growth in enterobacteria. The penicillin-binding capacity and a low DD-carboxypeptidase activity of PBP4B are demonstrated. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Sensitivity analysis to explore responsiveness and dynamic range of multi-metric fish-based indices for assessing the ecological status of estuaries and lagoons

Fish-based multi-metric indices are an integral tool in implementing effective water policy initiatives for transitional waters. This study analysed the behaviour of three fish indices (TFCI in the UK, ELFI in France and EFAI in Portugal) developed for monitoring in line with the European Water Framework Directive, by applying a supervised multi-way sensitivity analysis with national monitoring data. The relative variation in the index outcome was analysed under different simulation scenarios by setting metric values at various levels and accounting for the co-variation between metrics. Subsets of key metrics were identified based on their higher influence in determining the index output. Index results under manipulations of metric scores clearly indicated that metric type, number of metrics used and correlations between metrics are important in determining their behaviour. This has implications for implementing management/conservation plans, for example, by prioritising restoration and/or conservation of metrics influencing more the ecological status. Indices including uncorrelated metrics (e.g. EFAI) or metrics with a skewed distribution (e.g. TFCI) are less affected by extreme metric changes, reducing the effectiveness of management actions aimed at improving the ecological status of a water body and thus adjustments may be needed to increase their sensitivity to changes in their metrics.     

Development of a multimetric approach to assess perturbation of benthic macrofauna in Zostera noltii beds

Biotic indices based on soft-bottom macrozoobenthic communities are currently used throughout Europe to assess the ecological quality of coastal and transitional water bodies according to the European Water Framework Directive. However, the performance of the currently available biotic indices still has to be tested against a variety of different impact sources. In particular, physical perturbations have received much less attention than other kind of disturbances. This study consisted in testing the capacity of currently available uni- (BOPA, AMBI and BENTIX) and multivariate (M-AMBI) Biotic Indices to assess the ecological impact of the destruction of a Zostera noltii seagrass bed in Arcachon Bay (France) following sediment deposits. Changes of habitat after this physical perturbation were hardly assessed by any of these Biotic Indices whereas analysis of the benthic community showed drastic changes of structure following the perturbation and no recovery after 15 months. This study demonstrates that these Biotic Indices must be integrated into a multimetric approach which describes better the biological integrity of the benthic community by including a complementary set of metrics. A new multimetric approach, named MISS (Macrobenthic Index of Sheltered Systems) is proposed. MISS correctly highlighted the destruction of the seagrass beds, by using 16 metrics describing the biological integrity of the macrofauna.     

Genome histories clarify evolution of the expansin superfamily: new insights from the poplar genome and pine ESTs

Expansins comprise a superfamily of plant cell wall-loosening proteins that has been divided into four distinct families, EXPA, EXPB, EXLA and EXLB. In a recent analysis of Arabidopsis thaliana and Oryza sativa expansins, we proposed a further subdivision of the families into 17 clades, representing independent lineages in the last common ancestor of monocots and eudicots. This division was based on both traditional sequence-based phylogenetic trees and on position-based trees, in which genomic locations and dated segmental duplications were used to reconstruct gene phylogeny. In this article we review recent work concerning the patterns of expansin evolution in angiosperms and include additional insights gained from the genome of a second eudicot species, Populus trichocarpa, which includes at least 36 expansin genes. All of the previously proposed monocot-eudicot orthologous groups, but no additional ones, are represented in this species. The results also confirm that all of these clades are truly independent lineages. Furthermore, we have used position-based phylogeny to clarify the history of clades EXPA-II and EXPA-IV. Most of the growth of the expansin superfamily in the poplar lineage is likely due to a recent polyploidy event. Finally, some monocot-eudicot clades are shown to have diverged before the separation of the angiosperm and gymnosperm lineages. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Seagrass depth limits

Examination of the depth limit of seagrass communities distributed worldwide showed that sea-grasses may extend from mean sea level down to a depth of 90 m, and that differences in seagrass depth limit (Z_c) are largely attributable to differences in light attenuation underwater (K). This relationship is best described by the equation

log Z_c (m) = 0.26 − 1.07 log K (m⁻)

that holds for a large number of marine angiosperm species, although differences in seagrass growth strategy and architecture also appear to contribute to explain differences in their depth limits. The equation relating seagrass depth limit and light attenuation coefficient is qualitatively similar to previous equations developed for freshwater angiosperms, but predicts that seagrasses will colonize greater depths than freshwater angiosperms in clear (transparency greater than 10 m) waters. Further, the reduction in seagrass biomass from the depth of maximum biomass towards the depth limit is also closely related to the light attenuation coefficient. The finding that seagrasses can extend to depths receiving, on average, about 11% of the irradiance at the surface, together with the use of the equation described, may prove useful in the identification of seagrass meadows that have not reached their potential extension.     

微生物参与海草床元素循环及其生态修复功能

海草是分布在全球海岸带的沉水被子植物,与周围环境共同形成的海草床生态系统是三大典型海洋生态系统之一,具有十分重要的生态功能。20世纪以来,全球海草床衰退严重,研究海草床的生态修复迫在眉睫,现有修复方法未能足够重视微生物在海草床中的重要作用。本文综合阐述了微生物在海草床生态系统有机物矿化和营养流动过程中起到的作用,分析了微生物驱动下的海草床水体与沉积物之间的元素循环,提出了人类活动引起海草床退化的原因,总结了海草床微生物的系统研究方法,并在此基础上提出从微生物生态的角度修复海草床的新思路。     

Strength and uncertainty of phytoplankton metrics for assessing eutrophication impacts in lakes

Phytoplankton constitutes a diverse array of short-lived organisms which derive their nutrients from the water column of lakes. These features make this community the most direct and earliest indicator of the impacts of changing nutrient conditions on lake ecosystems. It also makes them particularly suitable for measuring the success of restoration measures following reductions in nutrient loads. This paper integrates a large volume of work on a number of measures, or metrics, developed for using phytoplankton to assess the ecological status of European lakes, as required for the Water Framework Directive. It assesses the indicator strength of these metrics, specifically in relation to representing the impacts of eutrophication. It also examines how these measures vary naturally at different locations within a lake, as well as between lakes, and how much variability is associated with different replicate samples, different months within a year and between years. On the basis of this analysis, three of the strongest metrics (chlorophyll-a, phytoplankton trophic index (PTI), and cyanobacterial biovolume) are recommended for use as robust measures for assessing the ecological quality of lakes in relation to nutrient-enrichment pressures and a minimum recommended sampling frequency is provided for these three metrics.     

Potent cytotoxins produced by a microbial symbiont protect host larvae from predation

Larvae of the sessile marine invertebrate Bugula neritina (Bryozoa) are protected by an effective chemical defense. From the larvae, we isolated three bryostatin-class macrocyclic polyketides, including the novel bryostatin 20, that deterred feeding by a common planktivorous fish that co-occurs with B. neritina. A unique bacterial symbiont of B. neritina, Endobugula sertula, was hypothesized as the putative source of the bryostatins. We show that: (1) bryostatins are concentrated in B. neritina larvae and protect them against predation by fish; (2) the adults are not defended by bryostatins; and (3) E. sertula produces bryostatins. This study represents the first example from the marine environment of a microbial symbiont producing an anti-predator defense for its host and, in this case, specifically for the hosts larval stage, which is exceptionally vulnerable to predators.Electronic Supplementary Material Supplementary material is available in the online version of this article at