The seafloor from a trait perspective. A comprehensive life history dataset of soft sediment macrozoobenthos.

Biological trait analysis (BTA) is a valuable tool for evaluating changes in community diversity and its link to ecosystem processes as well as environmental and anthropogenic perturbations. Trait-based analytical techniques like BTA rely on standardised datasets of species traits. However, there are currently only a limited number of datasets available for marine macrobenthos that contain trait data across multiple taxonomic groups. Here, we present an open-access dataset of 16 traits for 235 macrozoobenthic species recorded throughout multiple sampling campaigns of the Dutch Wadden Sea; a dynamic soft bottom system where humans have long played a substantial role in shaping the coastal environment. The trait categories included in this dataset cover a variety of life history strategies that are tightly linked to ecosystem functioning and the resilience of communities to (anthropogenic) perturbations and can advance our understanding of environmental changes and human impacts on the functioning of soft bottom systems.

The metamicrobiome: key determinant of the homeostasis of nutrient recycling.

The metamicrobiome is an integrated concept to study carbon and nutrient recycling in ecosystems. Decomposition of plant-derived matter by free-living microbes and fire - two key recycling pathways - are highly sensitive to global change. Mutualistic associations of microbes with plants and animals strongly reduce this sensitivity. By solving a fundamental allometric trade-off between metabolic and homeostatic capacity, these mutualisms enable continued recycling of plant matter where and when conditions are unfavourable for the free-living microbiome. A diverse metamicrobiome - where multiple plant- and animal-associated microbiomes complement the free-living microbiome - thus enhances homeostasis of ecosystem recycling rates in variable environments. Research into metamicrobiome structure and functioning in ecosystems is therefore important for progress towards understanding environmental change.

The importance of marshes providing soil stabilization to resist fast-flow erosion in case of a dike breach.

Salt marshes provide valuable ecosystem services including coastal protection by reducing wave loading on dikes and seawalls. If the topsoil is erosion resistant to fast-flowing water, it may also reduce breach depth if a dike fails. In this experiment, we quantified the topsoil erosion resistance from marshes and bare tidal flats with different soil types to understand the extent to which they can help reduce breach depth. Intact soil samples were collected from 11 locations in the Netherlands at different tidal elevations and then exposed for 3 h to 2.3 m/s currents. To the samples that remained stable after flow exposure, an artificial crack was made to test their stability following soil disturbance. All samples from the tidal flats were completely eroded, regardless of sediment type. In contrast, all samples from well-established marsh plateaus were stable as long as no disturbances were made, including those with sandy subsoils. After creating artificial cracks, samples with a thin cohesive top layer on top of sandy subsoil collapsed, while marshes with silty subsoils remained stable. Pioneer marshes on sandy substrate without a cohesive top layer were the only vegetated soils that completely eroded. The lower erosion of marshes with either sandy or silty soils compared to bare tidal flats was best explained by the presence of a top layer with belowground biomass, high organic content, high water content, and low bulk density. When analyzing the erodibility of marshes only, fine root density was the best predictor of erosion resistance. This study demonstrates the importance of preserving, restoring, or creating salt marshes, to obtain a topsoil that is erosion resistant under fast-flowing water, which helps reduce breach dimensions if a dike fails. The probability of topsoil erosion in established marshes with sandy subsoil is higher than in silty marshes. A silty layer of cohesive sediment on top of the sand provides extra erosion resistance as long as it does not break. Pioneer marshes that have not developed a cohesive top layer are erosion sensitive, especially in sandy soils. For future marsh creations, using fine-grained sediments or a mixture of sand with silt or clay is recommended.

Small herbivores and abiotic heterogeneity promote trait variation of a saltmarsh plant in local communities.

Intraspecific trait variation (ITV) enables plants to respond to global changes. However, causes for ITV, especially from biotic components such as herbivory, are not well understood. We explored whether small vertebrate herbivores (hares and geese) impact ITV of a dominant clonal plant (Elytrigia atherica) in local communities. Moreover, we looked at the relative importance of their direct (e.g., selective grazing) and indirect effects (altering genotypic richness/diversity and abiotic environment) on ITV. We used exclosures at two successional stages in a Dutch saltmarsh, where grazing pressure at the early successional stage was ca. 1.5 times higher than that of the intermediate successional stage. We measured key functional traits of E. atherica including height, aboveground biomass, flowering (flower or not), specific leaf area, and leaf dry matter content in local communities (1 m × 1 m plots) inside and outside the exclosures. We determined genotypic richness and diversity of each plant using molecular markers. We further measured abiotic variations in topography and clay thickness (a proxy for soil total nitrogen). Structural equation models revealed that small herbivores significantly promoted ITV in height and flowering at the early successional stage, while they marginally promoted ITV in height at the intermediate successional stage. Moreover, the direct effects of herbivores played a major role in promoting ITV. Small herbivores decreased genotypic diversity at the intermediate successional stage, but genotypic richness and diversity did not impact ITV. Small herbivores did not alter topographic variation and variation in clay thickness, but these variations increased ITV in all traits at the early successional stage. Small herbivores may not only impact trait means in plants as studies have shown but also their ITV.

Ontogenetic niche shifts as a driver of seasonal migration.

Ontogenetic niche shifts have helped to understand population dynamics. Here we show that ontogenetic niche shifts also offer an explanation, complementary to traditional concepts, as to why certain species show seasonal migration. We describe how demographic processes (survival, reproduction and migration) and associated ecological requirements of species may change with ontogenetic stage (juvenile, adult) and across the migratory range (breeding, non-breeding). We apply this concept to widely different species (dark-bellied brent geese (Branta b. bernicla), humpback whales (Megaptera novaeangliae) and migratory Pacific salmon (Oncorhynchus gorbuscha) to check the generality of this hypothesis. Consistent with the idea that ontogenetic niche shifts are an important driver of seasonal migration, we find that growth and survival of juvenile life stages profit most from ecological conditions that are specific to breeding areas. We suggest that matrix population modelling techniques are promising to detect the importance of the ontogenetic niche shifts in maintaining migratory strategies. As a proof of concept, we applied a first analysis to resident, partial migratory and fully migratory populations of barnacle geese (Branta leucopsis). We argue that recognition of the costs and benefits of migration, and how these vary with life stages, is important to understand and conserve migration under global environmental change.

Cross-boundary human impacts compromise the Serengeti-Mara ecosystem.

Protected areas provide major benefits for humans in the form of ecosystem services, but landscape degradation by human activity at their edges may compromise their ecological functioning. Using multiple lines of evidence from 40 years of research in the Serengeti-Mara ecosystem, we find that such edge degradation has effectively "squeezed" wildlife into the core protected area and has altered the ecosystem's dynamics even within this 40,000-square-kilometer ecosystem. This spatial cascade reduced resilience in the core and was mediated by the movement of grazers, which reduced grass fuel and fires, weakened the capacity of soils to sequester nutrients and carbon, and decreased the responsiveness of primary production to rainfall. Similar effects in other protected ecosystems worldwide may require rethinking of natural resource management outside protected areas.

North Sea demersal fisheries prefer specific benthic habitats.

INTRODUCTION: The future protection of marine biodiversity through good conservation planning requires both the identification of key habitats with unique ecological characteristics and detailed knowledge of their human utilization through fisheries. Demersal fisheries are important disturbers of benthic habitats. They often have a heterogeneous spatial distribution, pressurizing particular habitats with high abundances of target species. For the North Sea, we quantified the commonness/rarity of habitats in relation to the environmental determinants of so-called fishing hotspots, to support better-informed conservation planning of benthic habitats in this intensively used continental shelf. METHODS: We first distinguished 9 main seascapes in the study area based on seabed morphology. Secondly, we determined average fishing intensity and fishing hotspots using VMS-data for the three dominant Dutch fisheries from 2008 to 2015: beam-trawlers targeting sole Solea solea (Beam-Sole), beam-trawlers targeting plaice Pleuronectes platessa (Beam-Plaice), and otter-trawlers targeting Norway lobster Nephrops norvegicus and demersal fish (Otter-Mix). Within the seascapes subjected to >80% of the fishing activity, nineteen environmental factors (summarized by PCA) were used to ecologically characterize fishing hotspot locations using MaxEnt response modelling. RESULTS: We found that all three fisheries target highly specific, uncommon habitats. Beam-Sole fishers targeted warmer, shallow, dynamic, nearshore habitats, and within these specifically the depressions between sand ridges. Beam-Plaice fishers mainly targeted the exposed, non-muddy flanks of the Dogger Bank and similar large-scale elevations (50-75 km) where especially the ridges of smaller sand banks are used. Otter-Mix fisheries concentrated in areas with low bed shear stress, located in muddy, relatively deeper areas. IMPLICATIONS: This study is the first to provide insight in benthic habitat types that are frequently targeted by fishers in the North Sea. We demonstrated unequal exploitation pressure between seabed habitats, with the majority of hotspots in the less common habitats. Our results hence contribute to a more effective, ecologically informed planning for the protection and monitoring of all seabed habitats and biodiversity of the North Sea.

Evidence for 'critical slowing down' in seagrass: a stress gradient experiment at the southern limit of its range.

The theory of critical slowing down, i.e. the increasing recovery times of complex systems close to tipping points, has been proposed as an early warning signal for collapse. Empirical evidence for the reality of such warning signals is still rare in ecology. We studied this on Zostera noltii intertidal seagrass meadows at their southern range limit, the Banc d'Arguin, Mauritania. We analyse the environmental covariates of recovery rates using structural equation modelling (SEM), based on an experiment in which we assessed whether recovery after disturbances (i.e. seagrass & infauna removal) depends on stress intensity (increasing with elevation) and disturbance patch size (1 m2 vs. 9 m2). The SEM analyses revealed that higher biofilm density and sediment accretion best explained seagrass recovery rates. Experimental disturbances were followed by slow rates of recovery, regrowth occurring mainly in the coolest months of the year. Macrofauna recolonisation lagged behind seagrass recovery. Overall, the recovery rate was six times slower in the high intertidal zone than in the low zone. The large disturbances in the low zone recovered faster than the small ones in the high zone. This provides empirical evidence for critical slowing down with increasing desiccation stress in an intertidal seagrass system.

Organic Amendment Under Increasing Agricultural Intensification: Effects on Soil Bacterial Communities and Plant Productivity.

The soil microbiome is a complex living network that plays essential roles in agricultural systems, regardless of the level of intensification. However, the effects of agricultural management on the soil microbiome and the association with plant productivity remain largely unclear. Here, we studied the responses of three soil systems displaying distinct levels of agriculture intensiveness (i.e., natural, organic, and conventional soil management regimes) to experimentally manipulated organic farming amendments (i.e., dung and earthworms). We aimed at (i) identifying the effect on plant productivity and (ii) elucidating the degree of shifts in bacterial communities in response to the applied organic amendments. We found plant productivity to be lower with increasing agricultural intensification. Bacterial communities shifted distinctively for each soil management regime to the organic amendments applied. In brief, greater changes were observed in the Conventional management comparatively to the Organic and Natural management, an effect largely driven by dung addition. Moreover, we found evidence that the level of agricultural intensiveness also affects the timespan for these shifts. For instance, while the Natural system reached a relatively stable community composition before the end of the experiment, treatments on the conventional soil management regime did not. Random forest analyses further revealed an increasing impact of introduced taxa from dung addition aligned with increasing agricultural intensification. These analyses suggested that earthworms regulate the introduction of species from dung into the soil bacterial community. Collectively, our results contribute to a better understanding of the outcomes of organic amendments on soils under distinct levels of agriculture intensiveness, with implications for further development in soil restorations practices.

A facultative mutualistic feedback enhances the stability of tropical intertidal seagrass beds.

Marine foundation species such as corals, seagrasses, salt marsh plants, and mangrove trees are increasingly found to engage in mutualistic interactions. Because mutualisms by their very nature generate a positive feedback between the species, subtle environmental impacts on one of the species involved may trigger mutualism breakdown, potentially leading to ecosystem regime shifts. Using an empirically parameterized model, we investigate a facultative mutualism between seagrass and lucinid bivalves with endosymbiotic sulfide-oxidizing gill bacteria in a tropical intertidal ecosystem. Model predictions for our system show that, by alleviating the build-up of toxic sulfide, this mutualism maintains an otherwise intrinsically unstable seagrass ecosystem. However, an increase in seagrass mortality above natural levels, due to e.g. desiccation stress, triggers mutualism breakdown. This pushes the system in collapse-and-recovery dynamics ('slow-fast cycles') characterized by long-term persistent states of bare and seagrass-dominated, with rapid transitions in between. Model results were consistent with remote sensing analyses that suggest feedback-mediated state shifts induced by desiccation. Overall, our combined theoretical and empirical results illustrate the potential of mutualistic feedbacks to stabilize ecosystems, but also reveal an important drawback as small environmental changes may trigger shifts. We therefore suggest that mutualisms should be considered for marine conservation and restoration of seagrass beds.

Dispersal-competition tradeoff in microbiomes in the quest for land colonization.

Ancestor microbes started colonizing inland habitats approximately 2.7 to 3.5 billion years ago. With some exceptions, the key physiological adaptations of microbiomes associated with marine-to-land transitions have remained elusive. This is essentially caused by the lack of suitable systems that depict changes in microbiomes across sufficiently large time scales. Here, we investigate the adaptive routes taken by microbiomes along a contemporary gradient of land formation. Using functional trait-based metagenomics, we show that a switch from a microbial 'dispersal' to a 'competition' response modus best characterizes the microbial trait changes during this eco-evolutionary trajectory. The 'dispersal' modus prevails in microbiomes at the boundary sites between land and sea. It encompasses traits conferring cell chemosensory and motile behaviors, thus allowing the local microbes to exploit short-lived nutritional patches in high-diffusion microhabitats. A systematic transition towards the 'competition' modus occurs progressively as the soil matures, which is likely due to forces of viscosity or strain that favor traits for competition and chemical defense. Concomitantly, progressive increases in the abundances of genes encoding antibiotic resistance and complex organic substrate degradation were found. Our findings constitute a novel perspective on the ecology and evolution of microbiome traits, tracking back one of the most seminal transitions in the evolutionary history of life.

Unexpected dietary preferences of Eurasian Spoonbills in the Dutch Wadden Sea: spoonbills mainly feed on small fish not shrimp.

After an historical absence, over the last decades Eurasian Spoonbills Platalea leucorodia leucorodia have returned to breed on the barrier islands of the Wadden Sea. The area offers an abundance of predator-free nesting habitat, low degrees of disturbance, and an extensive intertidal feeding area with increasing stocks of brown shrimp Crangon crangon, the assumed main prey of P. leucorodia leucorodia. Nevertheless, newly established and expanding colonies of spoonbills have surprisingly quickly reached plateau levels. Here we tested the often stated assertion that spoonbills mainly rely on brown shrimp as food, by quantifying the diet of chicks on the basis of regurgitates and by analysis of blood isotopes using stable isotope Bayesian mixing models. Both methods showed that, rather than brown shrimp being the staple food of spoonbill chicks, small flatfish (especially plaice Pleuronectes platessa) and gobies (Pomatoschistus spp.) were their main prey. Unlike shrimp, small flatfish have been reported to be rather scarce in the Wadden Sea in recent years, which may explain the rapid saturation of colony size due to food-related density-dependent recruitment declines of growing colonies. By way of their diet and colony growth characteristics, spoonbills may thus indicate the availability of small fish in the Wadden Sea. We predict that the recovery to former densities of young flatfish and other juvenile/small fish in the Wadden Sea will be tracked by changing diets (more fish) and an increase in the size of Eurasian Spoonbill colonies across the Wadden Sea.

Herbivore exclusion promotes a more stochastic plant community assembly in a natural grassland.

Both bottom-up (e.g., nutrients) and top-down (e.g., herbivory) forces structure plant communities, but it remains unclear how they affect the relative importance of stochastic and deterministic processes in plant community assembly. Moreover, different-sized herbivores have been shown to have contrasting effects on community structure and function, but their effects on the processes governing community assembly (i.e., how they generate the impacts on structure) remain largely unknown. We evaluated the influence of bottom-up and top-down forces on the relative importance of deterministic and stochastic processes during plant community assembly. We used the data of a 7-yr factorial experiment manipulating nutrient availability (ambient and increased) and the presence of vertebrate herbivores (>1 kg) of different body size in a floodplain grassland in The Netherlands. We used a null model that describes a community composition expected by chance (i.e., stochastic assembly) and compared the plant community composition in the different treatments with this null model (the larger the difference, the more deterministically assembled). Our results showed that herbivore exclusion promoted a more stochastic plant community assembly, whereas increased nutrients played a relatively minor role in determining the relative importance of stochasticity in community assembly. Large herbivores facilitated intermediate-sized mammal herbivores, resulting in synergistic effects of enhanced grazing pressure and a more deterministic and convergent plant community assembly. We conclude that herbivores can act as strong deterministic forces during community assembly in natural systems. Our results also reveal that although large- and intermediate-sized mammal herbivores often have contrasting effects on many community and ecosystem properties, they can also synergistically homogenize plant communities.

Decoupled diversity dynamics in green and brown webs during primary succession in a saltmarsh.

Terrestrial ecosystems are characterized by a strong functional connection between the green (plant-herbivore-based) and brown (detritus-detritivore-based) parts of the food web, which both develop over successional time. However, the interlinked changes in green and brown food web diversity patterns in relation to key ecosystem processes are rarely studied. Here, we demonstrate changes in species richness, diversity and evenness over a wide range of invertebrate green and brown trophic groups during 100 years of primary succession in a saltmarsh ecosystem, using a well-calibrated chronosequence. We contrast two hypotheses on the relationship between green and brown food web diversity across succession: (i) 'coupled diversity hypothesis', which predicts that all trophic groups covary similarly with the main drivers of successional ecosystem assembly vs. (ii) the 'decoupled diversity hypothesis', where green and brown trophic groups diversity respond to different drivers during succession. We found that, while species richness for plants and invertebrate herbivores (green web groups) both peaked at intermediate productivity and successional age, the diversity of macrodetritivores, microarthropod microbivores and secondary consumers (brown web groups) continuously increased towards the latest successional stages. These results suggest that green web trophic groups are mainly driven by vegetation parameters, such as the amount of bare soil, vegetation biomass production and vegetation height, while brown web trophic groups are mostly driven by the production and standing stock of dead organic material and soil development. Our results show that plant diversity cannot simply be used as a proxy for the diversity of all other species groups that drive ecosystem functioning, as brown and green diversity components in our ecosystem responded differently to successional gradients.

Termites promote resistance of decomposition to spatiotemporal variability in rainfall.

The ecological impact of rapid environmental change will depend on the resistance of key ecosystems processes, which may be promoted by species that exert strong control over local environmental conditions. Recent theoretical work suggests that macrodetritivores increase the resistance of African savanna ecosystems to changing climatic conditions, but experimental evidence is lacking. We examined the effect of large fungus-growing termites and other non-fungus-growing macrodetritivores on decomposition rates empirically with strong spatiotemporal variability in rainfall and temperature. Non-fungus-growing larger macrodetritivores (earthworms, woodlice, millipedes) promoted decomposition rates relative to microbes and small soil fauna (+34%) but both groups reduced their activities with decreasing rainfall. However, fungus-growing termites increased decomposition rates strongest (+123%) under the most water-limited conditions, making overall decomposition rates mostly independent from rainfall. We conclude that fungus-growing termites are of special importance in decoupling decomposition rates from spatiotemporal variability in rainfall due to the buffered environment they create within their extended phenotype (mounds), that allows decomposition to continue when abiotic conditions outside are less favorable. This points at a wider class of possibly important ecological processes, where soil-plant-animal interactions decouple ecosystem processes from large-scale climatic gradients. This may strongly alter predictions from current climate change models.

Grassland structural heterogeneity in a savanna is driven more by productivity differences than by consumption differences between lawn and bunch grasses.

Savanna grasslands are characterized by high spatial heterogeneity in vegetation structure, aboveground biomass and nutritional quality, with high quality short-grass grazing lawns forming mosaics with patches of tall bunch grasses of lower quality. This heterogeneity can arise because of local differences in consumption, because of differences in productivity, or because both processes enforce each other (more production and consumption). However, the relative importance of both processes in maintaining mosaics of lawn and bunch grassland types has not been measured. Also their interplay been not been assessed across landscape gradients. In a South African savanna, we, therefore, measured the seasonal changes in primary production, nutritional quality and herbivore consumption (amount and percentage) of grazing lawns and adjacent bunch grass patches across a rainfall gradient. We found both higher amounts of primary production and, to a smaller extent, consumption for bunch grass patches. In addition, for bunch grasses primary production increased towards higher rainfall while foliar nitrogen concentrations decreased. Foliar nitrogen concentrations of lawn grasses decreased much less with increasing rainfall. Consequently, large herbivores targeted the biomass produced on grazing lawns with on average 75 % of the produced biomass consumed. We conclude that heterogeneity in vegetation structure in this savanna ecosystem is better explained by small-scale differences in productivity between lawn and bunch grass vegetation types than by local differences in consumption rates. Nevertheless, the high nutritional quality of grazing lawns is highly attractive and, therefore, important for the maintenance of the heterogeneity in species composition (i.e. grazing lawn maintenance).

Drought, Mutualism Breakdown, and Landscape-Scale Degradation of Seagrass Beds.

In many marine ecosystems, biodiversity critically depends on foundation species such as corals and seagrasses that engage in mutualistic interactions [1-3]. Concerns grow that environmental disruption of marine mutualisms exacerbates ecosystem degradation, with breakdown of the obligate coral mutualism ("coral bleaching") being an iconic example [2, 4, 5]. However, as these mutualisms are mostly facultative rather than obligate, it remains unclear whether mutualism breakdown is a common risk in marine ecosystems, and thus a potential accelerator of ecosystem degradation. Here, we provide evidence that drought triggered landscape-scale seagrass degradation and show the consequent failure of a facultative mutualistic feedback between seagrass and sulfide-consuming lucinid bivalves that in turn appeared to exacerbate the observed collapse. Local climate and remote sensing analyses revealed seagrass collapse after a summer with intense low-tide drought stress. Potential analysis-a novel approach to detect feedback-mediated state shifts-revealed two attractors (healthy and degraded states) during the collapse, suggesting that the drought disrupted internal feedbacks to cause abrupt, patch-wise degradation. Field measurements comparing degraded patches that were healthy before the collapse with patches that remained healthy demonstrated that bivalves declined dramatically in degrading patches with associated high sediment sulfide concentrations, confirming the breakdown of the mutualistic seagrass-lucinid feedback. Our findings indicate that drought triggered mutualism breakdown, resulting in toxic sulfide concentrations that aggravated seagrass degradation. We conclude that external disturbances can cause sudden breakdown of facultative marine mutualistic feedbacks. As this may amplify ecosystem degradation, we suggest including mutualisms in marine conservation and restoration approaches.