Disentangling the effect of space, time, and environmental and anthropogenic drivers on coastal macrobenthic ß diversity in contrasting habitats over 15 years.

Coastal zones are biodiversity hotspots and deliver essential ecosystem functions and services, yet they are exposed to multiple and interacting anthropogenic and environmental constraints. The individual and cumulative effects of these constraints on benthic communities, a key component of coastal ecosystems, and their variability across space and time, remains to be thoroughly quantified to guide conservation actions. Here, we explored how the presence of biogenic habitats influences the response of benthic communities to natural and anthropogenic constraints. We investigated this effect in both intertidal and subtidal habitats exposed to different pressures. We used data collected in the North-East Atlantic over 15 years (2005-2019) as part of the REBENT monitoring program, covering 38 sites of bare sediments, intertidal seagrass beds and maerl beds. We collected a range of environmental variables and proxies of anthropogenic pressures and used variation and hierarchical partitioning with redundancy analyses to estimate their relative effect on macrobenthic communities. We used descriptors modeling spatial and temporal structures (dbMEMs) to explore the scale of their effects and potential missing predictors. The selected variables explained between 53 % and 64 % of macrobenthic ß diversity depending on habitat and depth. Fishing pressures, sedimentary and hydrodynamics variables stood out as the most important predictors across all habitats while proxies of anthropogenic pressures were overall more important in intertidal habitats. In the intertidal, presence of biogenic habitat strongly modulated the amount of explained variance and the identity of the selected variable. Across both tidal levels, analysis of models' residuals further indicated that biogenic habitats might mitigate the effect of extreme environmental events. Our study provides a hierarchy of the most important drivers of benthic communities across different habitats and tidal levels, emphasizing the prominence of anthropogenic pressures on intertidal communities and the role of biogenic habitats in mitigating environmental changes.

Changes in maerl-associated macroalgal community dynamics as evidence of anthropogenic pressure.

BACKGROUND AND AIMS: Maerl-associated communities have received considerable attention due to their uniqueness, biodiversity and functional importance. Although the impacts of human activities are well documented for maerl-associated macrofauna, the spatio-temporal variations of macroalgae have comparatively been neglected, and the drivers that influence their dynamics are poorly known. We investigate the links between maerl-associated macroalgal communities, anthropogenic pressures and environmental conditions, and hypothesize that sites under human pressure would exhibit different dynamics when compared to reference sites. METHODS: To better understand community variation through space and time, four subtidal maerl beds under different pressures were consistently monitored over one year in the bay of Brest, Brittany, France. Both macroalgae community monitoring and environmental data were acquired through field sampling and available models. KEY RESULTS: Higher macroalgal biomass was observed within eutrophic sites, especially in summer (more than ten times higher than in the Unimpacted site), caused by free-living forms of opportunistic red macroalgae. The Dredged site also exhibited distinct macroalgal communities during summer from the Unimpacted site. Nutrient concentrations and seasonality proved to be key factors affecting the macroalgal community composition, although dredging and its effects on granulometry also had a strong influence. Over the long term, fewer than half of the species identified during historical surveys were found, indicating major temporal changes. CONCLUSIONS: Human pressures have strong impacts on maerl-associated macroalgal communities. Nutrient concentrations and dredging pressure appear as the main anthropogenic factors shaping maerl-associated macroalgal communities. Additionally, our results suggest historical changes in maerl-associated macroalgal communities over 25 years in response to changes in local human pressure management. This study suggests that maerl-associated macroalgal communities could be used as indicators of anthropogenically driven changes in this habitat.

Seasonal lipid dynamics of four Arctic bivalves: Implications for their physiological capacities to cope with future changes in coastal ecosystems.

The Arctic is exposed to unprecedented warming, at least three times higher than the global average, which induces significant melting of the cryosphere. Freshwater inputs from melting glaciers will subsequently affect coastal primary production and organic matter quality. However, due to a lack of basic knowledge on the physiology of Arctic organisms, it remains difficult to understand how these future trophic changes will threaten the long-term survival of benthic species in coastal habitats. This study aimed to gain new insights into the seasonal lipid dynamics of four dominant benthic bivalves (Astarte moerchi, Hiatella arctica, Musculus discors, and Mya truncata) collected before and after sea ice break-up in a high-Arctic fjord (Young Sound, NE Greenland). Total lipid content and fatty acid composition of digestive gland neutral lipids were analyzed to assess bivalve energy reserves while the fatty acid composition of gill polar lipids was determined as a biochemical indicator of interspecies variations in metabolic activity and temperature acclimation. Results showed a decrease in lipid reserves between May and August, suggesting that bivalves have only limited access to fresh organic matter until sea ice break-up. The lack of seasonal variation in the fatty acid composition of neutral lipids, especially essential ω3 fatty acids, indicates that no fatty acid transfer from the digestive glands to the gonads occurs between May and August, and therefore, no reproductive investment takes place during this period. Large interspecies differences in gill fatty acid composition were observed, which appear to be related to differences in species life span and metabolic strategies. Such differences in gill fatty acid composition of polar lipids, which generally influence metabolic rates and energy needs, may imply that not all benthic species will be equally sensitive to future changes in primary production and organic matter quality in Arctic coastal habitats.

Quantifying maerl (rhodolith) habitat complexity along an environmental gradient at regional scale in the Northeast Atlantic.

Maerl beds are ecologically important marine biogenic habitats founded on a few species of free-living coralline algae that aggregate and form highly complex rhodoliths. The high biodiversity found in these habitats have been mainly justified by the structural complexity that they provide. However, few attempts to quantify this complexity have been made. Maerl species distribution, density, rhodolith growth forms, and shapes vary with environmental conditions. Hydrodynamics and depth have been shown to drive morphology. Using species-specific metrics such as sphericity and branching density, as well as diameter and fractal dimension at the rhodolith level, and maerl density at the habitat level, we quantified the habitat complexity within ten maerl beds at a regional scale (along ∼400 km of the coastline of Brittany in Western France). Using both long-term monitoring data and environmental models, we investigated how maerl habitat complexity varies among beds and which environmental conditions drive those differences. The effects of currents, exposure to wind-generated waves, temperature and sediment granulometry were evaluated. We confirmed variations in complexity in maerl beds at the habitat and rhodolith levels at local and regional scales, which might have ecological and conservational implications for their associated biodiversity. The analysed environmental conditions drive around a third of the variance in habitat complexity. Sediment granulometry is the main driver of maerl habitat complexity in Brittany, while the isolated effects of depth and hydrodynamics accounted for less than 5% of the variability each. Our results have important implications for paleoecology, and we suggest that maerl facies should be interpreted carefully. Our study provides a first attempt at explicitly quantifying maerl habitat complexity, and further contributes to the understanding of this fundamental ecological question.

Functional changes in benthic macrofaunal communities along a natural gradient of hypoxia in an upwelling system.

Increasing global concern has been raised about the expansion of hypoxia in coastal waters and its potential to impact benthic ecosystems. Upwelling areas offer opportunities to study the effects of hypoxia on benthic communities under natural conditions. We used a biological trait-based approach and estimated functional diversity indices to assess macrobenthic community functioning along a depth gradient associated with naturally increasing hypoxia and concentrations of organic matter in the upwelling zone of northern Chile (South-East Pacific) over two years. Our results highlighted the increasing dominance of opportunistic biological traits associated with hypoxia and high organic matter content. Habitat filtering was the main process affecting the studied communities. Functional diversity patterns were persistent overtime despite the occurrence of a pulse of oxygenation. This study contributes to our understanding of how natural hypoxia impacts macrobenthic communities, providing useful information in the context of increasing eutrophication due to human influence on coastal areas.

Physiology of maerl algae: Comparison of inter- and intraspecies variations.

Free-living red coralline algae play an important role in the carbon and carbonate cycles of coastal environments. In this study, we examined the physiology of free-living coralline algae-forming maerl beds in the Bay of Brest (Brittany, France), where Lithothamnion corallioides is the dominant maerl (i.e., rhodolith) species. Phymatolithon calcareum and Lithophyllum incrustans are also present (in lower abundances) at a specific site in the bay. We aimed to assess how maerl physiology is affected by seasonality and/or local environmental variations at the inter- and intraspecific levels. Physiological measurements (respiration, photosynthetic, and calcification rates) were performed using incubation chambers in winter and summer to compare (1) the dominant maerl species at three sites and (2) three coexisting maerl species at one site. Comparison of the three coexisting maerl species suggests that L. corallioides is the best adapted to the current environmental conditions in the Bay of Brest, because this species is the most robust to dissolution in the dark in winter and has the highest calcification efficiency in the light. Comparisons of L. corallioides metabolic rates between stations showed that morphological variations within this species are the main factor affecting its photosynthetic and calcification rates. Environmental factors such as freshwater inputs also affect its calcification rates in the dark. In addition to interspecies variation in maerl physiology, there were intraspecific variations associated with direct (water physico-chemistry) or indirect (morphology) local environmental conditions. This study demonstrates the plasticity of maerl physiology in response to environmental changes, which is fundamental for maerl persistence.

Green macroalgae blooms (Ulva spp.) influence trophic ecology of juvenile flatfish differently in sandy beach nurseries.

Opportunistic green macroalgae blooms increasingly affect coastal areas worldwide. Understanding their impacts on organisms that use this zone, such as juvenile flatfish, is critical. By combining stable isotope data, digestive tract contents and community analyses of flatfish and their potential prey (benthic macroinvertebrates) from two North-East Atlantic sandy beaches (one impacted by blooms and one not), we detected similar and species-specific trophic changes among three co-occurring species (sand sole, plaice and turbot). Across flatfish species, juveniles displayed more opportunistic foraging behavior at the impacted site. Differently, plaice and sand sole relied more on the additional basal resource (Ulva spp.) than turbot. Finally, sand sole and turbot presented a stronger diet shift at the impacted site than plaice. We hypothesize that the species-specific response to the blooms are mostly driven by how the flatfish detect their prey (using visual and/or chemical cues) and when they forage (diurnal or nocturnal foraging).

Declining maerl vitality and habitat complexity across a dredging gradient: Insights from in situ sediment profile imagery (SPI).

Maerl beds form complex biogenic benthic habitats, characterized by high productivity as well as diverse biological communities. Disturbances associated with extraction and/or fishing activities using mobile bottom-contacting gears such as clam-dredges induce the most severe and long-term effects on these fragile habitats. We here investigated the effects of dredge-fishing on maerl in the bay of Brest (France). We quantified maerl beds structure and vitality across a fine scale quantified dredging intensity gradient through the acquisition of in-situ images of beds cross-section using Sediment Profile Imaging system (SPI). Declines in the proxies of maerl vitality and habitat complexity were measured across the gradient, and were associated with significant changes in the vertical distribution of live and dead maerl as well as of interstitial space. Fishing with dredges caused maerl mortality, substratum compaction, and decreasing habitat complexity. SPI imaging techniques also allowed for an assessment of changes in spatial heterogeneity that dredging created on several aspects of the structure and vitality of maerl beds. It suggests that direct and indirect disturbances induced by dredging are not acting at the same spatial scale, and can thereby differentially affect the ecosystem functions linked to vitality and habitat complexity.

Guess who? On the importance of using appropriate name: case study of Marphysasanguinea (Montagu, 1813).

The common bait worm Marphysasanguinea (Montagu, 1813), originally described from the south coast of England, is the type species of the genus. This species has been widely reported from all around the world and has been considered as cosmopolitan until recently. This is partly because the original description was very brief and poorly illustrated, and also because all species superficially look similar. In order to clarify the situation, M.sanguinea was redescribed and a neotype was designated by Hutchings and Karageorgpoulos in 2003. Recently, specimens from Cornwall, close to the type locality, were sampled, examined morphologically, and used to obtain COI gene sequences for this species. Molecular results permitted us to confirm the identity and presence of M.sanguinea along the French coasts and to highlight the presence of inaccurate sequences of this species on GenBank. Use of this "false" cosmopolitan species at a worldwide scale by many biologists is also discussed in this paper.

Combined effects of global climate change and nutrient enrichment on the physiology of three temperate maerl species.

Made up of calcareous coralline algae, maerl beds play a major role as ecosystem engineers in coastal areas throughout the world. They undergo strong anthropogenic pressures, which may threaten their survival. The aim of this study was to gain insight into the future of maerl beds in the context of global and local changes. We examined the effects of rising temperatures (+3°C) and ocean acidification (-0.3 pH units) according to temperature and pH projections (i.e., the RCP 8.5 scenario), and nutrient (N and P) availability on three temperate maerl species (Lithothamnion corallioides, Phymatolithon calcareum, and Lithophyllum incrustans) in the laboratory in winter and summer conditions. Physiological rates of primary production, respiration, and calcification were measured on all three species in each treatment and season. The physiological response of maerl to global climate change was species-specific and influenced by seawater nutrient concentrations. Future temperature-pH scenario enhanced maximal gross primary production rates in P. calcareum in winter and in L. corallioides in both seasons. Nevertheless, both species suffered an impairment of light harvesting and photoprotective mechanisms in winter. Calcification rates at ambient light intensity were negatively affected by the future temperature-pH scenario in winter, with net dissolution observed in the dark in L. corallioides and P. calcareum under low nutrient concentrations. Nutrient enrichment avoided dissolution under future scenarios in winter and had a positive effect on L. incrustans calcification rate in the dark in summer. In winter conditions, maximal calcification rates were enhanced by the future temperature-pH scenario on the three species, but P. calcareum suffered inhibition at high irradiances. In summer conditions, the maximal calcification rate dropped in L. corallioides under the future global climate change scenario, with a potential negative impact on CaCO3 budget for maerl beds in the Bay of Brest where this species is dominant. Our results highlight how local changes in nutrient availability or irradiance levels impact the response of maerl species to global climate change and thus point out how it is important to consider other abiotic parameters in order to develop management policies capable to increase the resilience of maerl beds under the future global climate change scenario.

Correction to 'Marine soundscape shaped by fishing activity'.

[This corrects the article DOI: 10.1098/rsos.160606.].

Marine soundscape shaped by fishing activity.

Marine communities face anthropogenic pressures that degrade ecosystems. Because underwater soundscapes carry information about habitat quality, we explored whether destructive impacts of fishing could be evaluated via the soundscape. Maerl beds are recognized as biodiversity hotspots and they experience major worldwide degradation owing to fishing. We collected field acoustic recordings in maerl beds exposed to different fishing practices. We found that unfished maerl beds were threefold louder and exhibited sound frequencies more diversified than those recorded in fished maerl beds. Analyses of associated fauna samples indicated that snapping shrimps provided a major contribution to the maerl bed soundscape. Moreover, sea urchins and squat lobsters most likely contributed to differences between the soundscapes of unfished and fished maerl beds. Our results supported the idea that the soundscape can provide valuable information on maerl bed ecosystem health related to fishing activity.

Human activities and climate variability drive fast-paced change across the world's estuarine-coastal ecosystems.

Time series of environmental measurements are essential for detecting, measuring and understanding changes in the Earth system and its biological communities. Observational series have accumulated over the past 2-5 decades from measurements across the world's estuaries, bays, lagoons, inland seas and shelf waters influenced by runoff. We synthesize information contained in these time series to develop a global view of changes occurring in marine systems influenced by connectivity to land. Our review is organized around four themes: (i) human activities as drivers of change; (ii) variability of the climate system as a driver of change; (iii) successes, disappointments and challenges of managing change at the sea-land interface; and (iv) discoveries made from observations over time. Multidecadal time series reveal that many of the world's estuarine-coastal ecosystems are in a continuing state of change, and the pace of change is faster than we could have imagined a decade ago. Some have been transformed into novel ecosystems with habitats, biogeochemistry and biological communities outside the natural range of variability. Change takes many forms including linear and nonlinear trends, abrupt state changes and oscillations. The challenge of managing change is daunting in the coastal zone where diverse human pressures are concentrated and intersect with different responses to climate variability over land and over ocean basins. The pace of change in estuarine-coastal ecosystems will likely accelerate as the human population and economies continue to grow and as global climate change accelerates. Wise stewardship of the resources upon which we depend is critically dependent upon a continuing flow of information from observations to measure, understand and anticipate future changes along the world's coastlines.

Food web of a confined and anthropogenically affected coastal basin (the Mar Piccolo of Taranto) revealed by carbon and nitrogen stable isotopes analyses.

Carbon and nitrogen stable isotope analysis was used to examine the food web of the Mar Piccolo of Taranto, a coastal basin experiencing several anthropogenic impacts. Main food sources (algal detritus, seaweeds, particulate organic matter (POM) and sediment organic matter (SOM)) and benthic and pelagic consumers were collected during two contrasting seasons (June and April), at four sites distributed over two inlets, and characterized by different level of confinements, anthropogenic inputs and the presence of mussels farming. δ(13)C values of organic sources revealed an important contribution of POM to both planktonic and benthic pathways, as well as the influence of terrigenous inputs within both inlets, probably due to high seasonal land runoff. Although δ(13)C of both sources and consumers varied little between sampling sites and dates, δ(15)N spatial variability was higher and clearly reflected the organic enrichment in the second inlet as well as the uptake of anthropogenically derived material by benthic consumers. On the other hand, within the first inlet, the isotopic composition of consumers did not change in response to chemical contamination. However, the impact of polluted sediments near the Navy Arsenal in the first inlet was detectable at the level of the macrobenthic trophic structure, showing high dominance of motile, upper level consumers capable to face transient conditions and the reduction of the more resident deposit feeders. We therefore underline the great potential of matching stable isotope analysis with quantitative studies of community structure to assess the effects of multiple anthropogenic stressors.

Metabarcoding is powerful yet still blind: a comparative analysis of morphological and molecular surveys of seagrass communities.

In the context of the sixth wave of extinction, reliable surveys of biodiversity are increasingly needed to infer the cause and consequences of species and community declines, identify early warning indicators of tipping points, and provide reliable impact assessments before engaging in activities with potential environmental hazards. DNA metabarcoding has emerged as having potential to provide speedy assessment of community structure from environmental samples. Here we tested the reliability of metabarcoding by comparing morphological and molecular inventories of invertebrate communities associated with seagrasses through estimates of alpha and beta diversity, as well as the identification of the most abundant taxa. Sediment samples were collected from six Zostera marina seagrass meadows across Brittany, France. Metabarcoding surveys were performed using both mitochondrial (Cytochrome Oxidase I) and nuclear (small subunit 18S ribosomal RNA) markers, and compared to morphological inventories compiled by a long-term benthic monitoring network. A sampling strategy was defined to enhance performance and accuracy of results by preventing the dominance of larger animals, boosting statistical support through replicates, and using two genes to compensate for taxonomic biases. Molecular barcodes proved powerful by revealing a remarkable level of diversity that vastly exceeded the morphological survey, while both surveys identified congruent differentiation of the meadows. However, despite the addition of individual barcodes of common species into taxonomic reference databases, the retrieval of only 36% of these species suggest that the remaining were either not present in the molecular samples or not detected by the molecular screening. This finding exemplifies the necessity of comprehensive and well-curated taxonomic reference libraries and multi-gene surveys. Overall, results offer methodological guidelines and support for metabarcoding as a powerful and repeatable method of characterizing communities, while also presenting suggestions for improvement, including implementation of pilot studies prior to performing full "blind" metabarcoding assessments to optimize sampling and amplification protocols.

Easier detection of invertebrate "identification-key characters" with light of different wavelengths.

The marine α-taxonomist often encounters two problems. Firstly, the "environmental dirt" that is frequently present on the specimens and secondly the difficulty in distinguishing key-features due to the uniform colours which fixed animals often adopt.Here we show that illuminating animals with deep-blue or ultraviolet light instead of the normal white-light abrogates both difficulties; dirt disappears and important details become clearly visible. This light regime has also two other advantages. It allows easy detection of very small, normally invisible, animals (0.1 µm range). And as these light wavelengths can induce fluorescence, new identification markers may be discovered by this approach.

Occurrence of the cis-4,7,10, trans-13-22:4 fatty acid in the family Pectinidae (Mollusca: Bivalvia).

The present study aimed to elucidate the effective phylogenetic specificity of distribution of a cis-4,7,10, trans-13-22:4 (22:4(n-9)Delta13trans) among pectinids. For this purpose, we extended the analysis of membrane glycerophospholipids FA composition to 13 species of scallops, covering 11 genera and 7 tribes representatives of the three subfamilies Chlamydinae, Palliolinae and Pectininae and the subgroup Aequipecten. In species belonging to the subfamily Pectininae and the Aequipecten subgroup, 22:4(n-9)Delta13trans was found in substantial amounts, but it was absent in other species belonging to the subfamilies Chlamydinae and Palliolinae. Homologous non-methylene-interrupted (NMI) FA, also hypothesized to differ along phylogenetic lines in bivalves, were totally absent or present only in trace amounts in representatives of the Aequipecten subgroup but ranged from 0.3 to 4.5% of the total FA in Pectinidae, Chlamydinae, and Palliolinae subfamilies. The species-specific occurrence of NMI and 22:4(n-9)Delta13trans FA in membrane lipids of pectinids agrees with the most recent phylogenies based on shell morphology and molecular characteristics. We examined the potential timing of the appearance of 22:4(n-9)Delta13trans in pectinids on a geologic time scale.

Determination of metal and organometal trophic bioaccumulation in the benthic macrofauna of the Adour estuary coastal zone (SW France, Bay of Biscay).

A multidisciplinary approach has been adopted in order to investigate the bioaccumulation of metals and organometals in macrobenthic populations. A complete method coupling a sampling strategy and classification of benthic organisms with a performant analytical procedure for the analysis of both metals and organometals has been developed. A single sample preparation method using a TMAH extraction and species specific isotope dilution makes it possible to analyse metals and organometals in the same extract, which is especially interesting for situations where only a limited amount of sample is available. Low detection limits have been obtained in the range of 12-250 pg g(-1) for mercury and butyltin compounds and 0.4-50 ng g(-1) for metals with good precision (1-10% RSD) even for a very low mass of sample (0.02 g). This method has been applied for monitoring contamination and bioaccumulation of metals and organometals as well as the biodiversity and trophic structure of the macrobenthic population of the Adour Estuary (South-West, France). The benthic macrofauna diversity indicates that inner estuarine stations are moderately polluted whereas outer estuarine stations are less impacted. However, metals concentrations in both sediment and benthic biomass do not change drastically between stations. Moreover, the bioaccumulation has been determined in relation to the feeding guild of benthic organisms. The results demonstrate that higher bioaccumulation is generally observed for deposit feeders directly impacted by sediment contamination compared to suspensive feeders and predators. Biomagnification along the trophic levels was highlighted for MMHg but no significant trend was observed for the other metallic compounds.