A cockle-induced bioturbation model and its impact on sediment erodibility: A meta-analysis.

Modelling the dynamics of an estuary and the evolution of its morphology requires a process-based description not only of the physical processes, but also of the influence of benthic fauna on sediment characteristics at ecosystem scale. A meta-analysis was tested as an approach for modelling the effect of bioturbation exerted by the cockle Cerastoderma edule on sediment erodibility. Six different erosion flume datasets were collected to ensure a broad range of experimental conditions including bed shear stress, population characteristics, and sediment composition. First, a model was built to describe the biogenic fluff layer created by C. edule activity in relation to (i) bioturbation activity using the population metabolic rate [mW·m-2] as a proxy for faunal metabolic energy, and (ii) the silt content [%] of the sediment. Second, different erosion models were compared by testing parameterization steps incorporating both erosion of the fluff layer and/or mass erosion of the sediment bed. Structural differences in the flumes and in the preparation of samples in the six different datasets makes it difficult to propose a single model that satisfactorily simulates all the data and encompasses both types of subsequent erosion, that of the fluff layer and that of the underlying consolidated bed. However, a generic model is proposed for the surficial fluff layer erosion covering a moderate range of bed shear stress (<1 Pa). This study shows that including several datasets covering a wide range of environmental conditions is a key to the robustness of this model, and that new insights can be gained by integrating the complexity of sediment features. We expect that this two-part model can be used in broad contexts in terms of cockle populations, estuarine habitats, and climatic conditions and can combined with various hydro-morpho-sedimentary models that include these biological effects.

Influence of nutrient enrichment on colonisation and photosynthetic parameters of hard substrate marine microphytobenthos.

This study aimed to assess the influence of nutrient enrichment on the development of microalgal biofilm on concrete and PVC cubes. Three mesocosms were utilized to create a nutrient gradient over a period of 28 days. Various parameters including biomass, photosynthetic activity, microtopography, and extracellular polymeric substances (EPS) were measured. Imaging PAM techniques were employed to obtain surface-wide data. Results revealed that nutrient availability had no significant impact on Chl a biomass and the maximum quantum efficiency of PSII (Fv/Fm). The photosynthetic capacity and efficiency were minimally affected by nutrient availability. Interestingly, the relationship between microphytobenthic (MPB) biomass and photosynthesis and surface rugosity exhibited distinct patterns. Negative reliefs showed a strong correlation with Fv/Fm, while no clear pattern emerged for biomass on rough concrete structures. Overall, our findings demonstrate that under conditions of heightened eutrophication, biofilm photosynthesis thrives in the fissures and crevasses of colonized structures regardless of nutrient levels. This investigation provides valuable insights into the interplay between nutrient availability and surface rugosity.

Heterogeneous microgeographic genetic structure of the common cockle (Cerastoderma edule) in the Northeast Atlantic Ocean: biogeographic barriers and environmental factors.

Knowledge of genetic structure at the finest level is essential for the conservation of genetic resources. Despite no visible barriers limiting gene flow, significant genetic structure has been shown in marine species. The common cockle (Cerastoderma edule) is a bivalve of great commercial and ecological value inhabiting the Northeast Atlantic Ocean. Previous population genomics studies demonstrated significant structure both across the Northeast Atlantic, but also within small geographic areas, highlighting the need to investigate fine-scale structuring. Here, we analysed two geographic areas that could represent opposite models of structure for the species: (1) the SW British Isles region, highly fragmented due to biogeographic barriers, and (2) Galicia (NW Spain), a putative homogeneous region. A total of 9250 SNPs genotyped by 2b-RAD on 599 individuals from 22 natural beds were used for the analysis. The entire SNP dataset mostly confirmed previous observations related to genetic diversity and differentiation; however, neutral and divergent SNP outlier datasets enabled disentangling physical barriers from abiotic environmental factors structuring both regions. While Galicia showed a homogeneous structure, the SW British Isles region was split into four reliable genetic regions related to oceanographic features and abiotic factors, such as sea surface salinity and temperature. The information gathered supports specific management policies of cockle resources in SW British and Galician regions also considering their particular socio-economic characteristics; further, these new data will be added to those recently reported in the Northeast Atlantic to define sustainable management actions across the whole distribution range of the species.

Aluminium-based galvanic anode impacts the photosynthesis of microphytobenthos and supports the bioaccumulation of metals released.

Very few studies have looked at the potential biological effects of degradation products of galvanic anodes particularly on primary producers which are central to food webs in marine ecosystems. The galvanic anode cathodic protection system (GACP) is widely used to protect submerged metallic structures from corrosion. Aluminium (Al) and zinc (Zn) are the main constituents of galvanic anodes and are therefore released in the marine environment by oxidation process to form ions or oxy-hydroxides. The main objective of our study was to evaluate the effects of the metals released from an aluminium-based galvanic anode on microphytobenthos performance in term of biofilm growing through the analysis of photosynthetic parameters, the determination of chlorophyll and extracellular polymeric substances (EPS). The bioaccumulation of Al and Zn were measured in the microphytobenthic compartment collected at the surface of polyvinyl chloride (PVC) plates exposed during 13 days to seawaters enriched in different concentrations of metals released from dissolution of one anode. Determination of bioconcentration factors confirmed that the microphytobenthos has incorporated Al. A significative effect was observed on the Chl a concentration for the higher tested concentration ([Al] = 210.1 ± 60.2 µg L - 1; [Zn] = 20.2 ± 1.4 µg L - 1). The seawater exposed to the anode affected the MPB productivity (ETRIImax) with consequences on acclimatation light (Ek), absorption cross section of PSII (σPII), Fv/Fm and NPQ. Regarding the EPS production, the anode degradation presented an impact on high and low molecular weight of both carbohydrates and protein fractions of microphytobenthos suggesting that EPS play an essential role in sequestering metal contaminants to maintain the integrity of the biological membranes and the functionality of the cellular organelles. The accumulation of Al released by GACP in microphytobenthos cells could lead to physiologic problems in photosynthetic organisms.

Colonisation of artificial structures by primary producers: competition and photosynthetic behaviour.

Colonisation of artificial structures by primary producers is an important determinant for eco-engineering projects. In this context, interactions between the colonisation by microphytobenthic biofilm and macroalgae were explored on 48 samples of marine infrastructures (MI) immersed for one year in the English Channel. Marine infrastructures samples with smooth and rough surface were compared to evaluate the influence of surface micro-scale rugosity. Microphytobenthos biomass (MPB), macroalgal diversity and photosynthetic parameters of both were assessed during colonisation. No significant differences were found as a function of the surface rugosity of MI samples, which was unexpected, but can be explained by biogenic rugosity provided by barnacles. Marine infrastructures were largely colonised by a red encrusting alga, Phymatolithon purpureum, which showed poor photosynthetic capacity compared to the microphytobenthos present next to it. Colonisation by monospecific encrusting algae tended to reduce the primary productivity of hard substrate.

Influence of infrastructure material composition and microtopography on marine biofilm growth and photobiology.

The impact of concrete composition and roughness on the formation of microalgal biofilms and their photobiology were studied on marine infrastructures presenting four different compositions combined with two degrees of roughness (rough and smooth). The structures were first inoculated with a natural microphytobenthic biofilm and immersed in sterilised seawater with a controlled photoperiod for six days. Photosynthetic activity was assessed with an imaging PAM-(Pulse Amplitude Modulated) fluorometer and microtopography was monitored in parallel with a 3-D camera. The results indicated that roughness had an impact on the biofilm biomass, its physiological status and its photosynthetic efficiency and capacity. The assessment of surface roughness indicated that negative reliefs were preferably colonised by MPB (microphytobenthic) cells with better photosynthetic performances. Moreover, MPB biofilms showed better photoacclimation in these microhabitats than on the positive and smooth reliefs. This study confirms the importance of microhabitat for biofilm formation and their photobiology.

Changes in benthic macrofauna in oyster parks during an OsHV-1 µVar oyster spat mortality outbreak.

In intertidal areas, oyster farming creates a crosshatching pattern between oyster tables and aisles. Tables provide a refuge from the current and solar irradiance and the oysters facilitate the accumulation of OM, thereby structuring the spatial organization of the associated macrozoobenthic community at mesoscale. The aim of this study was to describe the quality of the oyster table environment at small scale and the response of the macrozoobenthic community to OsHV-1 µvar oyster mortality. The species assemblage was dominated by Golfingia vulgaris, Tubificoides benedii, Capitella capitata and Scoloplos armiger. The table habitat appeared to be in a bad ecological state throughout the 2-month survey (May and June 2017), whereas in the aisle, eutrophication occurred lately and was clearly related to be due to the massive stranding of dead seaweed at the end of the survey (in early July). So, this disturbance of the species assemblage seemed to occur in two phases: 1) after oyster spat mortality and 2) after seaweed stranding resulted in a bad ecological status, as revealed by macrofaunal indicators. Large quantities of OsHV-1 DNA were also found in some species, including small crabs and amphipods, one week after the mortality crisis, but there is no apparent virus reservoir found in the benthic species.

Contrasted impact of two macrofaunal species (Hediste diversicolor and Scrobicularia plana) on microphytobenthos spatial distribution and photosynthetic activity at microscale.

Microphytobenthos is most often the primary source of carbon for coastal soft-sediment communities, especially in intertidal and shallow subtidal environments. The influence of benthic macrofaunal organisms on microphytobenthic biomass, spatial distribution and photosynthetic capacities is not only resulting from their feeding intensity but also indirectly from their bioturbation activity, which regulates nutrient fluxes and sediment mixing. This study compares the impact of two species (Hediste diversicolor and Scrobicularia plana) that dominate macrofaunal communities in estuarine intertidal mudflats on microphytobenthic biomass and photosynthetic activity. Imaging-PAM fluorescence was used to non-invasively map the development of microphytobenthic biomass and to assess its spatial extent. Our results showed that, due to intense deposit feeding, Scrobicularia plana quickly limited microphytobenthos growth and photosynthetic activity, even at low density (<250 ind m-2). In contrast, the negative impact of Hediste diversicolor on microphytobenthos development due to direct consumption was very low. Thereby, the stimulation of nutrient fluxes at the sediment-water interface resulting from bioirrigation seems to enhance microphytobenthos growth and photosynthesis.

Sediment stability: can we disentangle the effect of bioturbating species on sediment erodibility from their impact on sediment roughness?

Benthic organisms, in particular bioturbators, can influence erosion processes either by affecting sediment roughness through their mere presence and/or activities, or by modulating sediment characteristics (e.g., silt content, granulometry), thus altering its erodibility. To date, it was not possible to distinguish the influence of bioturbating species on sediment roughness from their impact on sediment erodibility. Consequently, uncertainties remain regarding the role played by benthic species on sediment dynamics. In this study, we used a canal flume which allows to record the bed shear stress at the surface of a non-cohesive sediment (4% of mud) during erosion experiments, thus allowing to disentangle the influence of bioturbators, here the common cockle Cerastoderma edule, on the two erosion mechanisms. In order to assess the influence of bioturbators on sediment stability in different environmental situations, we additionally tested for the effects of three factors, i.e. bivalve density, availability of suspended food (i.e. phytoplankton presence) and microphytobenthos (MPB) occurrence, which may modulate the behavior of cockles. We observed that cockles promote the erosion of the sediment surficial layer by increasing its roughness as a consequence of their sediment reworking activity and/or presence at the sediment surface (emerging shell). In contrast, we calculated similar critical bed shear stress for erosion with and without bivalves suggesting that cockles have a minor influence on the erodibility of non-cohesive substrates with a low silt content. The destabilizing effect of cockles increased with the bivalve density whereas it was attenuated by the presence of phytoplankton. We hypothesize that the magnitude of cockles' bioturbation activity was lower when a high proportion of suspended food is available. High concentrations of suspended food may also have enhanced the filtration and biodeposition rates of cockles, thus rapidly leading to the 'muddification' of the sediment bed and consequently counteracting with the own destabilizing effect of the bivalves. Finally, the sole presence of MPB did not significantly affect the resuspension dynamics of non-cohesive sediments with a low proportion of mud.

Evidence for better microphytobenthos dynamics in mixed sand/mud zones than in pure sand or mud intertidal flats (Seine estuary, Normandy, France).

Understanding the dynamics of microphytobenthos biomass and photosynthetic performances in intertidal ecosystems will help advance our understanding of how trophic networks function in order to optimize ecological management and restoration projects. The main objective of this study was to investigate microphytobenthic biomass and photosynthetic performances as a function of the sedimentary and environmental variabilities in the range of intertidal habitats in the downstream Seine estuary (Normandy, France). Our results highlight higher biomass associated with more stratified biofilms and better photosynthetic performances in areas characterized by a sand/mud mixture (40-60% of mud) compared to pure sand or pure mud environments. This type of sediment probably offers an efficient trade-off between the favorable characteristics of the two types of sediments (sand and mud) with respect to light penetration and nutrient accessibility. Moreover, the large quantities of exopolysaccharides produced in sand/mud mixtures emphasizes the functional role played by microphytobenthos in promoting sediment stability against erosion. This allows us to show that despite the strong increase in sand content of the downstream Seine estuary, intertidal flats are still productive since microphytobenthic biomass, photosynthetic performances and exopolysaccharides secretion are highest in sand-mud mixtures. This study also underlines the impact of ecosystem modifications due to human disturbance and climate change on the dynamics of key primary producers in estuaries.

Ecosystem services provided by a non-cultured shellfish species: The common cockle Cerastoderma edule.

Coastal habitats provide many important ecosystem services. The substantial role of shellfish in delivering ecosystem services is increasingly recognised, usually with a focus on cultured species, but wild-harvested bivalve species have largely been ignored. This study aimed to collate evidence and data to demonstrate the substantial role played by Europe's main wild-harvested bivalve species, the common cockle Cerastoderma edule, and to assess the ecosystem services that cockles provide. Data and information are synthesised from five countries along the Atlantic European coast with a long history of cockle fisheries. The cockle helps to modify habitat and support biodiversity, and plays a key role in the supporting services on which many of the other services depend. As well as providing food for people, cockles remove nitrogen, phosphorus and carbon from the marine environment, and have a strong cultural influence in these countries along the Atlantic coast. Preliminary economic valuation of some of these services in a European context is provided, and key knowledge gaps identified. It is concluded that the cockle has the potential to become (i) an important focus of conservation and improved sustainable management practices in coastal areas and communities, and (ii) a suitable model species to study the integration of cultural ecosystem services within the broader application of 'ecosystem services'.

Does parasitism influence sediment stability? Evaluation of trait-mediated effects of the trematode Bucephalus minimus on the key role of cockles Cerastoderma edule in sediment erosion dynamics.

In coastal environments, bioturbators greatly influence the physical and biogeochemical properties of sediments with consequences for central ecological processes such as erosion dynamics. In addition to their direct impact on sediment stability, bioturbators can have an impact on sediment erosion processes by modulating the growth of microphytobenthic organisms that stabilise the surface layer of sediments. The direct and indirect influences of bioturbators on sediment dynamics depend on the magnitude of their activity and inherently on their physiological state. Bioturbators are infected by various parasites, which have a substantial impact on their physiology and behaviour. However, the knock-on effects of parasites on key ecosystem functions like sediment dynamics remain poorly studied. We conducted flume experiments to investigate the indirect influence of the trematode Bucephalus minimus parasitising the common cockle Cerastoderma edule on the dynamics of sandy sediments enriched or not with microphytobenthos (MPB). Cockles modified bed roughness, sediment surface erodibility and hence destabilised sandy sediments. In sediments not enriched with MPB, both unparasitised and parasitised organisms had a similar impact on the stability of sandy sediments. In contrast, parasitism slightly reduced the destabilisation effect of cockles in MPB-enriched sediments. In the latter, parasitised cockles did not interfere with MPB growth whereas unparasitised organisms constrained the microalgae development. However, the enrichment of the surface layers of sandy sediments with MPB did not modulate the erosion dynamics of these environments. Thus, the lower destabilisation effect of parasitised cockles was not here linked to a stabilisation effect of MPB. When standardised for length, parasitised cockles were lighter than unparasitised organisms. Weakened cockles may have had a lower bioturbation potential than unparasitised conspecifics. If so, the influence parasitised cockles had on sediment erodibility and sediment roughness may have been reduced. The absence of a parasitism effect on the dynamics of MPB-unenriched sediments remains nonetheless unclear.

Key features of intertidal food webs that support migratory shorebirds.

The migratory shorebirds of the East Atlantic flyway land in huge numbers during a migratory stopover or wintering on the French Atlantic coast. The Brouage bare mudflat (Marennes-Oléron Bay, NE Atlantic) is one of the major stopover sites in France. The particular structure and function of a food web affects the efficiency of carbon transfer. The structure and functioning of the Brouage food web is crucial for the conservation of species landing within this area because it provides sufficient food, which allows shorebirds to reach the north of Europe where they nest. The aim of this study was to describe and understand which food web characteristics support nutritional needs of birds. Two food-web models were constructed, based on in situ measurements that were made in February 2008 (the presence of birds) and July 2008 (absence of birds). To complete the models, allometric relationships and additional data from the literature were used. The missing flow values of the food web models were estimated by Monte Carlo Markov Chain--Linear Inverse Modelling. The flow solutions obtained were used to calculate the ecological network analysis indices, which estimate the emergent properties of the functioning of a food-web. The total activities of the Brouage ecosystem in February and July are significantly different. The specialisation of the trophic links within the ecosystem does not appear to differ between the two models. In spite of a large export of carbon from the primary producer and detritus in winter, the higher recycling leads to a similar retention of carbon for the two seasons. It can be concluded that in February, the higher activity of the ecosystem coupled with a higher cycling and a mean internal organization, ensure the sufficient feeding of the migratory shorebirds.

Spatial variability of benthic-pelagic coupling in an estuary ecosystem: consequences for microphytobenthos resuspension phenomenon.

The high degree of physical factors in intertidal estuarine ecosystem increases material processing between benthic and pelagic compartments. In these ecosystems, microphytobenthos resuspension is a major phenomenon since its contribution to higher trophic levels can be highly significant. Understanding the sediment and associated microphytobenthos resuspension and its fate in the water column is indispensable for measuring the food available to benthic and pelagic food webs. To identify and hierarchize the physical/biological factors potentially involved in MPB resuspension, the entire intertidal area and surrounding water column of an estuarine ecosystem, the Bay des Veys, was sampled during ebb tide. A wide range of physical parameters (hydrodynamic regime, grain size of the sediment, and suspended matter) and biological parameters (flora and fauna assemblages, chlorophyll) were analyzed to characterize benthic-pelagic coupling at the bay scale. Samples were collected in two contrasted periods, spring and late summer, to assess the impact of forcing variables on benthic-pelagic coupling. A mapping approach using kriging interpolation enabled us to overlay benthic and pelagic maps of physical and biological variables, for both hydrological conditions and trophic indicators. Pelagic Chl a concentration was the best predictor explaining the suspension-feeders spatial distribution. Our results also suggest a perennial spatio-temporal structure of both benthic and pelagic compartments in the ecosystem, at least when the system is not imposed to intense wind, with MPB distribution controlled by both grain size and bathymetry. The benthic component appeared to control the pelagic one via resuspension phenomena at the scale of the bay. Co-inertia analysis showed closer benthic-pelagic coupling between the variables in spring. The higher MPB biomass observed in summer suggests a higher contribution to filter-feeders diets, indicating a higher resuspension effect in summer than in spring, in turn suggesting an important role of macrofauna bioturbation and filter feeding (Cerastoderma edule).

Spatial and temporal dynamics of size-structured photosynthetic parameters (PAM) and primary production (13C) of pico- and nano-phytoplankton in an atoll lagoon.

Atoll lagoons display a high diversity of trophic states due mainly to their specific geomorphology, and probably to their level and mode of human exploitation. We investigated the functioning of the Ahe atoll lagoon, utilized for pearl oyster farming, through estimations of photosynthetic parameters (pulse amplitude modulation fluorometry) and primary production ((13)C incorporation) measurements of the size structured phytoplankton biomass (<2 µm and >2 µm). Spatial and temporal scales of variability were surveyed during four seasons, over 16 months, at four sites within the lagoon. While primary production (P) was dominated by the picophytoplankton, its biomass specific primary productivity (P(B)) was lower than in other atoll lagoons. The variables size fraction of the phytoplankton, water temperature, season, the interaction term station*fraction and site, explained significantly the variance of the data set using redundancy analysis. No significant trends over depth were observed in the range of 0-20 m. A clear spatial pattern was found which was persistent over the seasons: south and north sites were different from the two central stations for most of the measured variables. This pattern could possibly be explained by the existence of water cells showing different water residence time within the lagoon. Photoacclimation strategies of the two size fractions differed through their light saturation coefficient (higher for picophytoplankton), but not through their maximum photosynthetic capacity (ETR(max)). Positive linear relationships between photosynthetic parameters indicated that their dynamic was independent of light availability in this ecosystem, but most probably dependent on nutrient availability and/or rapid changes in the community structure. Spatial and temporal patterns of the measured processes are then further discussed in the context of nutrient availability and the possible role of cultured oysters in nutrient recycling.

Biochemical composition and changes of extracellular polysaccharides (ECPS) produced during microphytobenthic biofilm development (Marennes-Oléron, France).

The main goal of this work was to study the dynamics and biochemical composition of extracellular polysaccharides (ECPS), a fraction of the extracellular polymeric substances (EPS) produced during the development of a microphytobenthic biofilm in a European intertidal mudflat (Marennes-Oléron Bay, France) during winter. Microphytobenthic biomass was surveyed during four consecutive emersion periods to confirm the biofilm growth. Bacteria abundance was also checked considering the importance of heterotrophic bacteria observed by various authors in the dynamics of EPS. Various colorimetric assays, coupled to biochemical chromatographic analysis, were used to characterize the three main fractions of extracted EPS: colloidal, bound, and residual. The monosaccharide distribution of colloidal ECPS highlighted their role of carbon source for bacteria (>50% of glucose) even if no increase of colloidal carbohydrate amounts was observed during the tidal exposure. Bound ECPS were composed of deoxy or specific sugars (30% rhamnose) and uronic acids (18% galacturonic acid). Their levels and dynamics could be correlated to the development of the microphytobenthic biofilm, enhancing the stabilization of the sediment or increasing binding forces accordingly. Residual fractions, containing refractory bound ECPS and other internal polymeric substances, were composed of various carbohydrates. The high ratio of glucose in these fractions (18% to 43%) was interesting, as it was once attributed to colloidal sugars due to poor extraction procedures. Finally, the presence of inositol (15%) was significant since no author has highlighted it before, knowing that inositol is a major growth factor for heterotrophic bacteria.