Thresholds of seascape fauna composition along gradients of human pressures and natural conditions to inform marine spatial planning.

Knowledge about the cumulative impacts of anthropogenic activities and environmental conditions on marine ecosystems is incomplete and details are lacking. Compositional community changes can occur along gradients, and community data can be used to assess the state of community resilience against combined impacts of variables representing human pressures and environmental conditions. Here we use a machine learning approach, i.e., Gradient Forest, to identify explanatory variable thresholds and select relevant epibenthic fauna and demersal fish species, which can be used to inform an integrated management of multiple human pressures and conservation planning in the southern North Sea. We show that a broad selection of anthropogenic and environmental variables, such as natural disturbance of the seafloor and euphotic depth, determined community composition thresholds of 67 epibenthic fauna and 39 demersal fish species along environmental conditions and human pressure gradients in the southern North Sea between 2010 and 2020. This has the potential to inform resilience assessments under the Marine Strategy Framework Directive to promote and retain a good environmental status of marine ecosystems.

Benthic microbial biogeographic trends in the North Sea are shaped by an interplay of environmental drivers and bottom trawling effort.

Microbial composition and diversity in marine sediments are shaped by environmental, biological, and anthropogenic processes operating at different scales. However, our understanding of benthic microbial biogeography remains limited. Here, we used 16S rDNA amplicon sequencing to characterize benthic microbiota in the North Sea from the top centimeter of 339 sediment samples. We utilized spatially explicit statistical models, to disentangle the effects of the different predictors, including bottom trawling intensity, a prevalent industrial fishing practice which heavily impacts benthic ecosystems. Fitted models demonstrate how the geographic interplay of different environmental and anthropogenic drivers shapes the diversity, structure and potential metabolism of benthic microbial communities. Sediment properties were the primary determinants, with diversity increasing with sediment permeability but also with mud content, highlighting different underlying processes. Additionally, diversity and structure varied with total organic matter content, temperature, bottom shear stress and bottom trawling. Changes in diversity associated with bottom trawling intensity were accompanied by shifts in predicted energy metabolism. Specifically, with increasing trawling intensity, we observed a transition toward more aerobic heterotrophic and less denitrifying predicted metabolism. Our findings provide first insights into benthic microbial biogeographic patterns on a large spatial scale and illustrate how anthropogenic activity such as bottom trawling may influence the distribution and abundances of microbes and potential metabolism at macroecological scales.

CRITTERBASE, a science-driven data warehouse for marine biota.

Data on marine biota exist in many formats and sources, such as published literature, data repositories, and unpublished material. Due to this heterogeneity, information is difficult to find, access and combine, severely impeding its reuse for further scientific analysis and its long-term availability for future generations. To address this challenge, we present CRITTERBASE, a publicly accessible data warehouse and interactive portal that currently hosts quality-controlled and taxonomically standardized presence/absence, abundance, and biomass data for 18,644 samples and 3,664 benthic taxa (2,824 of which at species level). These samples were collected by grabs, underwater imaging or trawls in Arctic, North Sea and Antarctic regions between the years 1800 and 2014. Data were collated from literature, unpublished data, own research and online repositories. All metadata and links to primary sources are included. We envision CRITTERBASE becoming a valuable and continuously expanding tool for a wide range of usages, such as studies of spatio-temporal biodiversity patterns, impacts and risks of climate change or the evidence-based design of marine protection policies.

Co-occurrence patterns and the large-scale spatial structure of benthic communities in seagrass meadows and bare sand.

BACKGROUND: Species distribution models are commonly used tools to describe diversity patterns and support conservation measures. There is a wide range of approaches to developing SDMs, each highlighting different characteristics of both the data and the ecology of the species or assemblages represented by the data. Yet, signals of species co-occurrences in community data are usually ignored, due to the assumption that such structuring roles of species co-occurrences are limited to small spatial scales and require experimental studies to be detected. Here, our aim is to explore associations among marine sandy-bottom sediment inhabitants and test for the structuring effect of seagrass on co-occurrences among these species across a New Zealand intertidal sandflat, using a joint species distribution model (JSDM). RESULTS: We ran a JSDM on a total of 27 macrobenthic species co-occurring in 300,000 m2 of sandflat. These species represented all major taxonomic groups, i.e. polychaetes, bivalves and crustaceans, collected in 400 sampling locations. A number of significant co-occurrences due to shared habitat preferences were present in vegetated areas, where negative and positive correlations were approximately equally common. A few species, among them the gastropods Cominella glandiformis and Notoacmea scapha, co-occurred randomly with other seagrass benthic inhabitants. Residual correlations were less apparent and mostly positive. In bare sand flats shared habitat preferences resulted in many significant co-occurrences of benthic species. Moreover, many negative and positive residual patterns between benthic species remained after accounting for habitat preferences. Some species occurring in both habitats showed similarities in their correlations, such as the polychaete Aglaophamus macroura, which shared habitat preferences with many other benthic species in both habitats, yet no residual correlations remained in either habitat. CONCLUSIONS: Firstly, analyses based on a latent variable approach to joint distributions stressed the structuring role of species co-occurrences beyond experimental scales. Secondly, results showed context dependent interactions, highlighted by species having more interconnected networks in New Zealand bare sediment sandflats than in seagrass meadows. These findings stress the critical importance of natural history to modelling, as well as incorporating ecological reality in SDMs.

Changes in the location of biodiversity-ecosystem function hot spots across the seafloor landscape with increasing sediment nutrient loading.

Declining biodiversity and loss of ecosystem function threatens the ability of habitats to contribute ecosystem services. However, the form of the relationship between biodiversity and ecosystem function (BEF) and how relationships change with environmental change is poorly understood. This limits our ability to predict the consequences of biodiversity loss on ecosystem function, particularly in real-world marine ecosystems that are species rich, and where multiple ecosystem functions are represented by multiple indicators. We investigated spatial variation in BEF relationships across a 300 000 m2 intertidal sandflat by nesting experimental manipulations of sediment pore water nitrogen concentration into sites with contrasting macrobenthic community composition. Our results highlight the significance of many different elements of biodiversity associated with environmental characteristics, community structure, functional diversity, ecological traits or particular species (ecosystem engineers) to important functions of coastal marine sediments (benthic oxygen consumption, ammonium pore water concentrations and flux across the sediment-water interface). Using the BEF relationships developed from our experiment, we demonstrate patchiness across a landscape in functional performance and the potential for changes in the location of functional hot and cold spots with increasing nutrient loading that have important implications for mapping and predicating change in functionality and the concomitant delivery of ecosystem services.

In situ soft sediment nutrient enrichment: A unified approach to eutrophication field experiments.

Adding fertiliser to sediments is an established way of studying the effects of eutrophication but a lack of consistent methodology, reporting on enrichment levels, or guidance on application rates precludes rigorous synthesis and meta-analysis. We developed a simple enrichment technique then applied it to 28 sites across an intertidal sandflat. Fertiliser application rates of 150 and 600gNm(-2) resulted in pore water ammonium concentrations respectively 1-110 and 4-580×ambient, with greater elevations observed in deeper (5-7cm) than surface (0-2cm) sediments. These enrichment levels were similar to eutrophic estuaries and were maintained for at least seven weeks. The high between-site variability could be partially explained by the sedimentary environment and macrofaunal community (42%), but only at the high application rate. We suggest future enrichment studies should be conducted in situ across large environmental gradients to incorporate real world complexity and increase generality of conclusions.

Cross-Scale Variation in Biodiversity-Environment Links Illustrated by Coastal Sandflat Communities.

Spatial variation in the composition of communities is the product of many biotic and environmental interactions. A neglected factor in the analysis of community distribution patterns is the multi-scale nature of the data, which has implications for understanding ecological processes and the development of conservation and environmental management practice. Drawing on recently established multivariate spatial analyses, we investigate whether including relationships between spatial structure and abiotic variables enable us to better discern patterns of species and communities across scales. Data comprised 1200 macrozoobenthic samples collected over an array of distances (30 cm to 1 km) in three New Zealand harbours, as well as commonly used abiotic variables, such as sediment characteristics and chlorophyll a concentrations, measured at the same scales. Moran's eigenvector mapping was used to extract spatial scales at which communities were structured. Benthic communities, representing primarily bivalves, polychaetes and crustaceans, were spatially structured at four spatial scales, i.e. >100 m, 50-100 m, 50-15 m, and < 15 m. A broad selection of abiotic variables contributed to the large-scale variation, whereas a more limited set explained part of the fine-scale community structure. Across all scales, less than 30% of the variation in spatial structure was captured by our analysis. The large number of species (48) making up the 10 highest species scores based on redundancy analyses illustrate the variability of species-scale associations. Our results emphasise that abiotic variables and biodiversity are related at all scales investigated and stress the importance of assessing the relationship between environmental variables and the abundance and distribution of biological assemblages across a range of different scales.

The up-scaling of ecosystem functions in a heterogeneous world.

Earth is in the midst of a biodiversity crisis that is impacting the functioning of ecosystems and the delivery of valued goods and services. However, the implications of large scale species losses are often inferred from small scale ecosystem functioning experiments with little knowledge of how the dominant drivers of functioning shift across scales. Here, by integrating observational and manipulative experimental field data, we reveal scale-dependent influences on primary productivity in shallow marine habitats, thus demonstrating the scalability of complex ecological relationships contributing to coastal marine ecosystem functioning. Positive effects of key consumers (burrowing urchins, Echinocardium cordatum) on seafloor net primary productivity (NPP) elucidated by short-term, single-site experiments persisted across multiple sites and years. Additional experimentation illustrated how these effects amplified over time, resulting in greater primary producer biomass (sediment chlorophyll a content) in the longer term, depending on climatic context and habitat factors affecting the strengths of mutually reinforcing feedbacks [corrected]. The remarkable coherence of results from small and large scales is evidence of real-world ecosystem function scalability and ecological self-organisation. This discovery provides greater insights into the range of responses to broad-scale anthropogenic stressors in naturally heterogeneous environmental settings.

Experimenting with ecosystem interaction networks in search of threshold potentials in real-world marine ecosystems.

Thresholds profoundly affect our understanding and management of ecosystem dynamics, but we have yet to develop practical techniques to assess the risk that thresholds will be crossed. Combining ecological knowledge of critical system interdependencies with a large-scale experiment, we tested for breaks in the ecosystem interaction network to identify threshold potential in real-world ecosystem dynamics. Our experiment with the bivalves Macomona liliana and Austrovenus stutchburyi on marine sandflats in New Zealand demonstrated that reductions in incident sunlight changed the interaction network between sediment biogeochemical fluxes, productivity, and macrofauna. By demonstrating loss of positive feedbacks and changes in the architecture of the network, we provide mechanistic evidence that stressors lead to break points in dynamics, which theory predicts predispose a system to a critical transition.

The role of environmental variables in structuring landscape-scale species distributions in seafloor habitats.

Ongoing statistical sophistication allows a shift from describing species' spatial distributions toward statistically disentangling the possible roles of environmental variables in shaping species distributions. Based on a landscape-scale benthic survey in the Dutch Wadden Sea, we show the merits of spatially explicit generalized estimating equations (GEE). The intertidal macrozoobenthic species, Macoma balthica, Cerastoderma edule, Marenzelleria viridis, Scoloplos armiger, Corophium volutator, and Urothoe poseidonis served as test cases, with median grain-size and inundation time as typical environmental explanatory variables. GEEs outperformed spatially naive generalized linear models (GLMs), and removed much residual spatial structure, indicating the importance of median grain-size and inundation time in shaping landscape-scale species distributions in the intertidal. GEE regression coefficients were smaller than those attained with GLM, and GEE standard errors were larger. The best fitting GEE for each species was used to predict species' density in relation to median grain-size and inundation time. Although no drastic changes were noted compared to previous work that described habitat suitability for benthic fauna in the Wadden Sea, our predictions provided more detailed and unbiased estimates of the determinants of species-environment relationships. We conclude that spatial GEEs offer the necessary methodological advances to further steps toward linking pattern to process.

Landscape-scale experiment demonstrates that Wadden Sea intertidal flats are used to capacity by molluscivore migrant shorebirds.

1. Whether intertidal areas are used to capacity by shorebirds can best be answered by large-scale manipulation of foraging areas. The recent overexploitation of benthic resources in the western Dutch Wadden Sea offers such an 'experimental' setting. 2. We review the effects of declining food abundances on red knot Calidris canutus islandica numbers, based on a yearly large-scale benthic mapping effort, long-term colour-ringing and regular bird-counts from 1996 to 2005. We focus on the three-way relationships between suitable foraging area, the spatial predictability of food and red knot survival. 3. For each benthic sampling position, red knot intake rate (mg AFDM s(-1)) was predicted by a multiple prey species functional response model, based on digestive rate maximization (this model explained diet and intake rate in earlier studies on red knots). This enabled us to derive the spatial distribution of the suitable foraging area, which in each of the 10 years was analysed with a measure of autocorrelation, i.e. Moran's I. 4. Over the 10 years, when accounting for a threshold value to meet energetic demands, red knots lost 55% of their suitable foraging area. This ran parallel to a decrease in red knot numbers by 42%. Although there was also a decrease in patchiness (i.e. less information about the location of the suitable feeding sites), this did not yet lead to additional loss of birds. 5. To cope with these landscape-scale declines in food stocks, an increase in the capacity for instantaneous food processing would be required. Although we show that red knots indeed enlarged their muscular gizzards, the increase in gizzard size was not enough to compensate for the decreased feeding area. 6. Survival of islandica knots in the western Dutch Wadden Sea, based on colour-ring resightings, declined from 89% in the first half of our study period to 82% in the second half of our study period and could account for almost half of the decline in red knot numbers; the rest must have moved elsewhere in winter. 7. Densities of red knots per unit suitable foraging area remained constant at 10 knots ha(-1) between 1996 and 2005, which suggests that red knots have been using the Dutch Wadden Sea to full capacity.

Reversed optimality and predictive ecology: burrowing depth forecasts population change in a bivalve.

Optimality reasoning from behavioural ecology can be used as a tool to infer how animals perceive their environment. Using optimality principles in a 'reversed manner' may enable ecologists to predict changes in population size before such changes actually happen. Here we show that a behavioural anti-predation trait (burrowing depth) of the marine bivalve Macoma balthica can be used as an indicator of the change in population size over the year to come. The per capita population growth rate between years t and t+1 correlated strongly with the proportion of individuals living in the dangerous top 4 cm layer of the sediment in year t: the more individuals in the top layer, the steeper the population decline. This is consistent with the prediction based on optimal foraging theory that animals with poor prospects should accept greater risks of predation. This study is among the first to document fitness forecasting in animals.

Shellfish dredging pushes a flexible avian top predator out of a marine protected area.

There is a widespread concern about the direct and indirect effects of industrial fisheries; this concern is particularly pertinent for so-called "marine protected areas" (MPAs), which should be safeguarded by national and international law. The intertidal flats of the Dutch Wadden Sea are a State Nature Monument and are protected under the Ramsar convention and the European Union's Habitat and Birds Directives. Until 2004, the Dutch government granted permission for ~75% of the intertidal flats to be exploited by mechanical dredgers for edible cockles (Cerastoderma edule). Here we show that dredged areas belonged to the limited area of intertidal flats that were of sufficient quality for red knots (Calidris canutus islandica), a long-distance migrant molluscivore specialist, to feed. Dredging led to relatively lower settlement rates of cockles and also reduced their quality (ratio of flesh to shell). From 1998 to 2002, red knots increased gizzard mass to compensate for a gradual loss in shellfish quality, but this compensation was not sufficient and led to decreases in local survival. Therefore, the gradual destruction of the necessary intertidal resources explains both the loss of red knots from the Dutch Wadden Sea and the decline of the European wintering population. This study shows that MPAs that do not provide adequate protection from fishing may fail in their conservation objectives.