Thermal stress affects bioturbators' burrowing behavior: A mesocosm experiment on common cockles (Cerastoderma edule).

The intensity of marine heatwaves is increasing due to climate change. Heatwaves may affect macroinvertebrates' bioturbating behavior in intertidal areas, thereby altering the deposition-erosion balance at tidal flats. Moreover, small-scale topographic features on tidal flats can create tidal pools during the low tide, thus changing the heat capacity of tidal flats. These pools could then potentially operate as refuge environments during marine heatwaves. We studied behavior responses to heat waves using the well-known bioturbating cockle Cerastoderma edule as a model species. Different temperature regimes (i.e., fluctuating between 20 and 40 °C) and micro-topographies (i.e., presence vs. absence of tidal water pools) were mimicked in a mesocosm experiment with regular tidal regimes. Our results demonstrate that behavioral responses to heat stress strongly depend on the site-specific morphological features. Cockles covered by shallow water pools moved up when exposed to thermal stress, while burrowing deeper into the sediment in the absence of water pools. But in both cases, their migratory behavior increased under heat stress compared to regular ambient treatments. Moreover, long-term cumulative heat stress increased cockles' respiration rates and decreased their health conditions, causing mass mortality after four weeks of gradually increasing heat exposure. Overall, the present findings provide the first insights into how bioturbating behavior on tidal flats may change in response to global warming.

Modelling spatial and temporal patterns in bioturbator effects on sediment resuspension: A biophysical metabolic approach.

Tidal flats are biogeomorphic landscapes, shaped by physical forces and interaction with benthic biota. We used a metabolic approach to assess the overarching effect of bioturbators on tidal landscapes. The benthic bivalve common cockle (Cerastoderma edule) was used as model organism. The effect of C. edule on sediment resuspension was approximated as a function of the overall population metabolic rate per unit of area. We combined i) laboratory observations on how C. edule affect sediment resuspension along gradients of bioturbation activity, sediment cohesiveness and hydrodynamic force with ii) spatial data on the natural distribution of intertidal C. edule populations. This allowed us to build an integrated model of the C. edule effect on sediment resuspension along the tidal gradient. Owing to the temperature dependence of metabolic rate, the model also accounted for seasonal variation in bioturbators activity. Laboratory experiments indicated that sediment resuspension is positively related to the metabolic rate of the C. edule population especially in cohesive sediments. Based on this observation, we predicted a clear spatial and seasonal pattern in the relative importance of C. edule contribution to sediment resuspension along a tidal transect. At lower elevations, our model indicates that hydrodynamics overrules biotic effects; at higher elevations, inter-tidal hydrodynamics should be too low to suspend bioturbated sediments. The influence of C. edule on sediment resuspension is expected to be maximal at the intermediate elevation of a mudflat, owing to the combination of moderate hydrodynamic stress and high bioturbator activity. Also, bio-mediated sediment resuspension is predicted to be particularly high in the warm season. Research into metabolic dependency of bio-mediated sediment resuspension may help to place phenomenological observations in the broader framework of metabolic theories in ecology and to formulate general expectations on the coastal ecosystem functioning.

Seasonal variability in ecosystem functioning across estuarine gradients: The role of sediment communities and ecosystem processes.

Functional trait approaches advance the understanding of biodiversity-ecosystem function (BDEF) relationships and its control by the environmental context. Application of these insights into management remains constrained due to lack of evidence from real-world ecosystems that capture the natural spatial and temporal gradients at which biodiversity and environmental conditions operate. In this study we measured macrofauna community traits, ecosystem processes and abiotic properties at 9 locations during 4 months, spanning a wide gradient in sedimentary habitats and salinity in the Scheldt estuary, and quantified the (a)biotic contribution to sediment community oxygen consumption, as a measure of ecosystem function. We found that functional attributes of the macrofauna community and its effect on bio-irrigation can predict ecosystem function, but especially during the colder period of the year. This result highlights that generalizations about BDEF relationships, and biodiversity loss on ecosystem functions, are limited whenever this temporal component is not acknowledged.

Experimental bottom trawling finds resilience in large-bodied infauna but vulnerability for epifauna and juveniles in the Frisian Front.

In this study, we analysed the benthic effects of two in situ fisheries disturbance experiments using a combination of side-scan sonar, high definition underwater video, sediment profile imagery, and box core sampling techniques after conventional beam trawling and box core sampling after electric pulse trawling in a southern North Sea habitat. Acoustic and optical methods visualised the morphological changes induced by experimental beam trawling, showing the flattening and homogenisation of surface sediments. Video transects found a 94% decrease in epibenthos in beam trawled sediments compared to an untrawled control site and a 74% decrease in untrawled sediments of the same transect. Box core samples taken 5.5 h, 29 h and 75 h after trawling detected a downward trend in infaunal densities and species richness that continued after the initial impact with small-bodied and juvenile taxa being especially prone to depletion. Data from shallow sediment samples showed trawl resilience in large mud shrimps and evidence of their upward movement towards the sediment surface after disturbance. Both trawl gears induced significant changes to infaunal communities, with no differential effect between the two gears. Our results suggest that in the Frisian Front, trawling may favour the survival of deep burrowers while removing surficial macrofauna.

Aligning biodiversity conservation and ecosystem services in spatial planning: Focus on ecosystem processes.

Although the consideration of socio-economic demands with biodiversity conservation is now high on the environmental policy agenda, it is not yet standard practice in spatial planning. This is argued to be related, among others, to a lack of awareness among stakeholders and practitioners of the underpinning role of ecosystem functioning and biodiversity to support human well-being. Meanwhile, there is mounting critique on the absolute focus of biodiversity conservation on static properties such as species and habitats. The establishment of more ecologically sensible objectives that include ecosystem processes besides species and habitats is put forward as a more effective way of environmental conservation. Methodological approaches increasingly consider ecosystem processes. However, the processes that are included mostly relate to aspects of biodiversity such as dispersal and productivity, and rarely do they include abiotic mechanisms that underlie biodiversity. We here report on the development of a method that integrates two principles which we identify as key to advance the integration of ecosystem services with biodiversity conservation in planning practice: (1) consider the variety of ecosystem processes, biotic as well as abiotic, that support biodiversity and ecosystem services, and (2) link the ecosystem processes to biodiversity and to socio-economic benefits to identify the common ground between seemingly conflicting objectives. The methodology uses a stepwise approach and is based on an extensive review of available knowledge on ecosystem functioning, expert consultation and stakeholder involvement. We illustrate how the methodology supports the setting of strategic goals to accomplish a healthy coastal ecosystem in Belgium, and exemplify how this may affect spatial plans. The aim of this paper is to demonstrate how including processes opens opportunities to align biodiversity and ecosystem services and how this increases chances to provide long-term benefits for biodiversity and human well-being. The paper may provide inspiration to advance current spatial planning approaches.

Ecosystem engineering creates a new path to resilience in plants with contrasting growth strategies.

Plant species can be characterized by different growth strategies related to their inherent growth and recovery rates, which shape their responses to stress and disturbance. Ecosystem engineering, however, offers an alternative way to cope with stress: modifying the environment may reduce stress levels. Using an experimental study on two seagrass species with contrasting traits, the slow-growing Zostera marina vs. the fast-growing Zostera japonica, we explored how growth strategies versus ecosystem engineering may affect their resistance to stress (i.e. addition of organic material) and recovery from disturbance (i.e. removal of above-ground biomass). Ecosystem engineering was assessed by measuring sulphide levels in the sediment porewater, as seagrass plants can keep sulphide levels low by aerating the rhizosphere. Consistent with predictions, we observed that the fast-growing species had a high capacity to recover from disturbance. It was also more resistant to stress and still able to maintain high standing stock with increasing stress levels because of its ecosystem engineering capacity. The slow-growing species was not able to maintain its standing stock under stress, which we ascribe to a weak capacity for ecosystem engineering regarding this particular stress. Overall, our study suggests that the combination of low-cost investment in tissues with ecosystem engineering to alleviate stress creates a new path in the growth trade-off between investment in strong tissues or fast growth. It does so by being both fast in recovery and more resistant. As such low-cost ecosystem engineering may occur in more species, we argue that it should be considered in assessing plant resilience.

Oyster breakwater reefs promote adjacent mudflat stability and salt marsh growth in a monsoon dominated subtropical coast.

Oyster reefs have the potential as eco-engineers to improve coastal protection. A field experiment was undertaken to assess the benefit of oyster breakwater reefs to mitigate shoreline erosion in a monsoon-dominated subtropical system. Three breakwater reefs with recruited oysters were deployed on an eroding intertidal mudflat at Kutubdia Island, the southeast Bangladesh coast. Data were collected on wave dissipation by the reef structures, changes in shoreline profile, erosion-accretion patterns, and lateral saltmarsh movement and related growth. This was done over four seasons, including the rainy monsoon period. The observed wave heights in the study area ranged 0.1-0.5 m. The reefs were able to dissipate wave energy and act as breakwaters for tidal water levels between 0.5-1.0 m. Waves were totally blocked by the vertical relief of the reefs at water levels <0.5 m. On the lee side of the reefs, there was accretion of 29 cm clayey sediments with erosion reduction of 54% as compared to control sites. The changes caused by the deployed reefs also facilitated seaward expansion of the salt marsh. This study showed that breakwater oyster reefs can reduce erosion, trap suspended sediment, and support seaward saltmarsh expansion demonstrating the potential as a nature-based solution for protecting the subtropical coastlines.

A verified habitat suitability model for the intertidal rock oyster, Saccostrea cucullata.

There is growing interest to restore oyster populations and develop oyster reefs for their role in ecosystem health and delivery of ecosystem services. Successful and sustainable oyster restoration efforts largely depend on the availability and selection of suitable sites that can support long-term growth and survival of oysters. Hence, in the present study a habitat suitability index (HSI) model was developed for the intertidal rock oyster (Saccostrea cucullata), with special attention: (1) to the role of the monsoon in the suitability of oyster habitats, and (2) to identify potential suitable sites along the south-eastern Bangladesh coast. Seven habitat factors were used as input variables for the HSI model: (1) water temperature; (2) salinity; (3) dissolved oxygen; (4) particulate inorganic matter (PIM); (5) pH; (6) Chlorophyll-a; and (7) water flow velocity. Seven field surveys were conducted at 80 locations to collect geo-spatial environmental data, which were then used to determine HSI scores using habitat suitability functions. The model results showed that the areas suitable (HSI >0.50) for oyster settlement and growth were characterized by relatively high salinities, Chlorophyll-a, dissolved oxygen and pH values. In contrast, freshwater dominated estuaries and nearby coastal areas with high suspended sediment were found less suitable (HSI <0.50) for oysters. HSI model results were validated with observed oyster distribution data. There was strong correlation between the HSI calculated by the model and observed oyster densities (r = 0.87; n = 53), shell height (r = 0.95; n = 53) and their condition index (r = 0.98; n = 53). The good correspondence with field data enhances the applicability of the HSI model as a quantitative tool for evaluating the quality of a site for oyster restoration and culture.

A process based model of cohesive sediment resuspension under bioturbators' influence.

Macrozoobenthos may affect sediment stability and erodibility via their bioturbating activities, thereby impacting both the short- and long-term development of coastal morphology. Process-based models accounting for the effect of bioturbation are needed for the modelling of erosion dynamics. With this work, we explore whether the fundamental allometric principles of metabolic activity scaling with individual and population size may provide a framework to derive general patterns of bioturbation effect on cohesive sediment resuspension. Experimental flumes were used to test this scaling approach across different species of marine, soft-sediment bioturbators. The collected dataset encompasses a range of bioturbator functional diversity, individual densities, body sizes and overall population metabolic rates. Measurements were collected across a range of hydrodynamic stress from 0.02 to 0.25 Pa. Overall, we observed that bioturbators are able to slightly reduce the sediment resuspension at low hydrodynamic stress, whereas they noticeably enhance it at higher levels of stress. Along the whole hydrodynamic stress gradient, the quantitative effect of bioturbators on sediment resuspension can be efficiently described by the overall metabolic rate of the bioturbating benthic communities, with significant variations across the bioturbators' taxonomic and functional diversity. One of the tested species (the gallery-builder Polychaeta Hediste diversicolor) had an effect that was partially deviating from the general trend, being able to markedly reduce sediment resuspension at low hydrodynamic stress compared to other species. By combining bioturbators' influence with hydrodynamic force, we were able to produce a process-based model of biota-mediated sediment resuspension.

Functional consumers regulate the effect of availability of subsidy on trophic cascades in the Yellow River Delta, China.

Understanding the environmental context where heterogeneous ecological processes affect biotic interactions is a key aim of ecological research. However, mechanisms underlying spatial variation in trophic interactions linked to resource availability across ecosystem gradients remains unclear. We experimentally manipulated the interactive effects of predator fish and quantitative gradient of leaf detritus on macroinvertebrates and benthic algae. We found that non-linear changes in the strength of trophic cascades were strongly linked to the retention rates of experimental leaf detritus and also determined by predatory consumers. Retention rate of leaf detritus influenced the recruitment of predatory invertebrates and foraging preference of predators, accounting for largely the variations in shift of strengthening and weakening trophic cascades. Our results highlight the importance to identify joint processes of recruitment and foraging responses of functional consumer in understanding the impacts of both anthropogenic and natural alterations in subsidy on trophic interaction of coastal food webs.

The combined influence of body size and density on cohesive sediment resuspension by bioturbators.

We propose an empirical framework to scale the effects of bioturbation on sediment resuspension to population bioturbation activity, approximated as population metabolic rate. Individual metabolic rates have been estimated as functions of body size and extrapolated to population level. We used experimental flumes to test this approach across different types of marine, soft-sediment bioturbators. We observed that a large part of the variance in biota-mediated sediment resuspension can be explained by a positive relationship with population metabolic rate. Other mechanisms can strongly influence the outcome, such as bioturbation of deep sediment strata, biotic interactions with hydrodynamic stress and overlapping areas of influence must be further investigated. By relating the biota-mediated changes in resuspended sediment to metabolism, we can place our observations within the broader context of the metabolic theory of ecology and to formulate general expectations about changes in biota-mediated sediment resuspension in response to changes in population structure and climate change.

Sprouting as a gardening strategy to obtain superior supplementary food: evidence from a seed-caching marine worm.

Only a handful of non-human animals are known to grow their own food by cultivating high-yield fungal or algal crops as staple food. Here we report an alternative strategy utilized by an omnivorous marine worm, Hediste diversicolor, to supplement its diet: gardening by sprouting seeds. In addition to having many other known feeding modes, we showed using video recordings and manipulative mesocosm experiments that this species can also behave like gardeners by deliberately burying cordgrass seeds in their burrows, which has been previously shown to reduce the loss of seeds to water. These seeds, however, are protected by the seed husk, and we used feeding experiments to show that they were not edible for H. diversicolor until they had sprouted or the seed husk had been artificially removed. Additionally, sprouts were shown to be highly nutritious, permitting higher growth rates in H. diversicolor than the low-quality basal food, detritus. We propose both a proximate cause (seed husk as a physical barrier) and ultimate cause (nutritional demand) for this peculiar feeding behavior. Our findings suggest that sprouting may be a common strategy used by seed-collecting animals to exploit nutrients from well-protected seeds.

Cover versus recovery: contrasting responses of two indicators in seagrass beds.

Despite being a highly valuable key-stone ecosystem, seagrass meadows are threatened and declining worldwide, creating urgent need for indicators of their health status. We compared two indicators for seagrass health: standing leaf area index versus relative recovery from local disturbance. Disturbance was created by removing aboveground biomass and recording the rate of regrowth for Zostera marina meadows exposed to contrasting wave regimes and nutrient stress levels. Within the experimental period, relative regrowth in gaps was around 50% in most plots, except for the ambient nutrient treatment at the sheltered site, where it exceeded 100%. The two indicators showed an opposite response to disturbance: the higher the standing leaf area index, the lower the relative recovery from disturbance. This conflicting response raises the question on the proper interpretation of such indicators to estimate seagrass health and resilience, and how to ideally monitor seagrass ecosystems in order to predict collapse.

A mixed modeling approach to predict the effect of environmental modification on species distributions.

Human infrastructures can modify ecosystems, thereby affecting the occurrence and spatial distribution of organisms, as well as ecosystem functionality. Sustainable development requires the ability to predict responses of species to anthropogenic pressures. We investigated the large scale, long term effect of important human alterations of benthic habitats with an integrated approach combining engineering and ecological modelling. We focused our analysis on the Oosterschelde basin (The Netherlands), which was partially embanked by a storm surge barrier (Oosterscheldekering, 1986). We made use of 1) a prognostic (numerical) environmental (hydrodynamic) model and 2) a novel application of quantile regression to Species Distribution Modeling (SDM) to simulate both the realized and potential (habitat suitability) abundance of four macrozoobenthic species: Scoloplos armiger, Peringia ulvae, Cerastoderma edule and Lanice conchilega. The analysis shows that part of the fluctuations in macrozoobenthic biomass stocks during the last decades is related to the effect of the coastal defense infrastructures on the basin morphology and hydrodynamics. The methodological framework we propose is particularly suitable for the analysis of large abundance datasets combined with high-resolution environmental data. Our analysis provides useful information on future changes in ecosystem functionality induced by human activities.

Ecosystem-based coastal defence in the face of global change.

The risk of flood disasters is increasing for many coastal societies owing to global and regional changes in climate conditions, sea-level rise, land subsidence and sediment supply. At the same time, in many locations, conventional coastal engineering solutions such as sea walls are increasingly challenged by these changes and their maintenance may become unsustainable. We argue that flood protection by ecosystem creation and restoration can provide a more sustainable, cost-effective and ecologically sound alternative to conventional coastal engineering and that, in suitable locations, it should be implemented globally and on a large scale.

On the myths of indicator species: issues and further consideration in the use of static concepts for ecological applications.

The use of static indicator species, in which species are expected to have a similar sensitivity or tolerance to either natural or human-induced stressors, does not account for possible shifts in tolerance along natural environmental gradients and between biogeographic regions. Their indicative value may therefore be considered at least questionable. In this paper we demonstrate how species responses (i.e. abundance) to changes in sediment grain size and organic matter (OM) alter along a salinity gradient and conclude with a plea for prudency when interpreting static indicator-based quality indices. Six model species (three polychaetes, one amphipod and two bivalves) from the North Sea, Baltic Sea and the Mediterranean Sea region were selected. Our study demonstrated that there were no generic relationships between environment and biota and half of the studied species showed different responses in different seas. Consequently, the following points have to be carefully considered when applying static indicator-based quality indices: (1) species tolerances and preferences may change along environmental gradients and between different biogeographic regions, (2) as environment modifies species autecology, there is a need to adjust indicator species lists along major environmental gradients and (3) there is a risk of including sibling or cryptic species in calculating the index value of a species.

Conditional Responses of Benthic Communities to Interference from an Intertidal Bivalve.

Habitat-modifying organisms that impact other organisms and local functioning are important in determining ecosystem resilience. However, it is often unclear how the outcome of interactions performed by key species varies depending on the spatial and temporal disturbance context which makes the prediction of disturbance-driven regime shifts difficult. We investigated the strength and generality of effects of the filter feeding cockle Cerastoderma edule on its ambient intertidal benthic physical and biological environment. By comparing the magnitude of the effect of experimental cockle removal between a non-cohesive and a sheltered cohesive sediment in two different periods of the year, we show that the outcome of cockle interference effects relates to differences in physical disturbance, and to temporal changes in suspended sediment load and ontogenetic changes in organism traits. Interference effects were only present in the cohesive sediments, though the effects varied seasonally. Cockle presence decreased only the density of surface-dwelling species suggesting that interference effects were particularly mediated by bioturbation of the surface sediments. Furthermore, density reductions in the presence of cockles were most pronounced during the season when larvae and juveniles were present, suggesting that these life history stages are most vulnerable to interference competition. We further illustrate that cockles may enhance benthic microalgal biomass, most likely through the reduction of surface-dwelling grazing species, especially in periods with high sediment load and supposedly also high bioturbation rates. Our results emphasize that the physical disturbance of the sediment may obliterate biotic interactions, and that temporal changes in environmental stressors, such as suspended sediments, may affect the outcome of key species interference effects at the local scale. Consequently, natural processes and anthropogenic activities that change bed shear stress and sediment dynamics in coastal soft-sediment systems will affect cockle-mediated influences on ecosystem properties and therefore the resilience of these systems to environmental change.

Organism-sediment interactions govern post-hypoxia recovery of ecosystem functioning.

Hypoxia represents one of the major causes of biodiversity and ecosystem functioning loss for coastal waters. Since eutrophication-induced hypoxic events are becoming increasingly frequent and intense, understanding the response of ecosystems to hypoxia is of primary importance to understand and predict the stability of ecosystem functioning. Such ecological stability may greatly depend on the recovery patterns of communities and the return time of the system properties associated to these patterns. Here, we have examined how the reassembly of a benthic community contributed to the recovery of ecosystem functioning following experimentally-induced hypoxia in a tidal flat. We demonstrate that organism-sediment interactions that depend on organism size and relate to mobility traits and sediment reworking capacities are generally more important than recovering species richness to set the return time of the measured sediment processes and properties. Specifically, increasing macrofauna bioturbation potential during community reassembly significantly contributed to the recovery of sediment processes and properties such as denitrification, bedload sediment transport, primary production and deep pore water ammonium concentration. Such bioturbation potential was due to the replacement of the small-sized organisms that recolonised at early stages by large-sized bioturbating organisms, which had a disproportionately stronger influence on sediment. This study suggests that the complete recovery of organism-sediment interactions is a necessary condition for ecosystem functioning recovery, and that such process requires long periods after disturbance due to the slow growth of juveniles into adult stages involved in these interactions. Consequently, repeated episodes of disturbance at intervals smaller than the time needed for the system to fully recover organism-sediment interactions may greatly impair the resilience of ecosystem functioning.

Ecological evaluation of an experimental beneficial use scheme for dredged sediment disposal in shallow tidal waters.

An experiment was performed to test an alternative dredging strategy for the Westerschelde estuary. Clean sand dredged from the navigation channel was disposed seawards of an eroding intertidal flat in order to modify morphology and hydrodynamics, improving the multi-channel system with ecologically productive shallow water habitat. Five years of intensive monitoring revealed that part of the disposed sediment moved slowly towards the flat, increasing the very shallow subtidal and intertidal area, as planned. The sand in the impact zone became gradually finer after disposal, possibly due to reduced current velocities. Nevertheless, no changes in macrobenthic biomass, density, species richness and composition were detected in the subtidal zone, also demonstrating rapid macrobenthic recovery. In the intertidal zone, no ecological effects could be revealed superimposed on trends associated with long-term sediment fining. Thus, despite morphological success and absence of detected negative ecological impacts of the experiment, new beneficial habitat was not created.