Tracking the distribution of persistent and mobile wastewater-derived substances in the southern and central North Sea using anthropogenic gadolinium from MRI contrast agents as a far-field tracer.

The use of the rare earth element gadolinium (Gd) in contrast agents for magnetic resonance imaging has led to a significant (micro-)contamination of riverine and coastal environments in many parts of the world. This study comprises a detailed investigation on the rare earth elements and yttrium inventory of the North Sea and also reports data for the major tributaries Thames, Rhine, Ems, Weser and Elbe. We show that large parts of the southern North Sea, including the Wadden Sea UNESCO Natural World Heritage site, are (micro)contaminated with Gd from Gd-based contrast agents (GBCA). Their dispersion reveals their estuarine input and allows to effectively track water masses and currents. The chemical persistence and conservative behavior of GBCA, coupled with the low detection limits of state-of-the-art analytical methods, makes the anthropogenic Gd a sensitive screening proxy for monitoring similarly stable, but potentially hazardous, persistent chemical/pharmaceutical substances in natural waters.

Frequency-dependent tolerance to aircraft disturbance drastically alters predicted impact on shorebirds.

Anthropogenic disturbance of wildlife is increasing globally. Generalizing impacts of disturbance to novel situations is challenging, as the tolerance of animals to human activities varies with disturbance frequency (e.g. due to habituation). Few studies have quantified frequency-dependent tolerance, let alone determined how it affects predictions of disturbance impacts when these are extrapolated over large areas. In a comparative study across a gradient of air traffic intensities, we show that birds nearly always fled (80%) if aircraft were rare, while birds rarely responded (7%) if traffic was frequent. When extrapolating site-specific responses to an entire region, accounting for frequency-dependent tolerance dramatically alters the predicted costs of disturbance: the disturbance map homogenizes with fewer hotspots. Quantifying frequency-dependent tolerance has proven challenging, but we propose that (i) ignoring it causes extrapolations of disturbance impacts from single sites to be unreliable, and (ii) it can reconcile published idiosyncratic species- or source-specific disturbance responses.

Abundance, biomass and species richness of macrozoobenthos along an intertidal elevation gradient.

Ecology aims to comprehend species distribution and its interaction with environmental factors, from global to local scales. While global environmental changes affect marine biodiversity, understanding the drivers at smaller scales remains crucial. Tidal flats can be found on most of the world's coastlines and are particularly vulnerable to anthropogenic disturbances. They are important transient ecosystems between terrestrial and marine ecosystems, and their biodiversity provides important ecosystem services. Owing to this unique, terrestrial-marine transition, strong environmental gradients of elevation, sediment composition and food availability prevail. Here, we investigated which regional and local environmental factors drive the spatio-temporal dynamics of macrozoobenthos communities on back-barrier tidal flats in the East Frisian Wadden Sea. On the regional level, we found that species composition changed significantly from west to east on the East Frisian islands and that total abundance and species richness decreased from west to east. On the local abiotic level, we found that macrozoobenthos biomass decreased with higher elevation towards the salt marsh and that the total abundance of organisms in the sediment significantly increased with increasing mud content, while biodiversity and biomass were not changing significantly. In contrast to expectations, increasing Chl a availability as a measure of primary productivity did not result in changes in abundance, biomass or biodiversity, but extremely high total organic carbon (TOC) content was associated with a decrease in biomass and biodiversity. In conclusion, we found regional and local relationships that are similar to those observed in previous studies on macrozoobenthos in the Wadden Sea. Macrozoobenthos biomass, abundance and biodiversity are interrelated in a complex way with the physical, abiotic and biotic processes in and above the sediment.

Modelled dispersal pathways of non-indigenous species in the Danish Wadden Sea.

The introduction-rate of non-indigenous species (NIS) to coastal water bodies has accelerated over the last century. We present a model study assessing the fate of NIS released in likely point sources of the Danish Wadden Sea. We show that NIS-particles released in the deep North Sea are generally transported away from the Wadden Sea, while those released in the coastal North Sea and the Wadden Sea show large variability in track pattern and settlement location. Consequently, the introduction of NIS from ships entering the port of Esbjerg pose a threat to the Wadden Sea through primary and secondary spreading, while transport of species from sources in the south likely causes a slow and steady settling of NIS in the Wadden Sea and coastal North Sea. The study points to the importance of enforcing an efficient monitoring system to ensure early detection of changes to the species composition of the Wadden Sea.

Detection of Novel Poxvirus from Gray Seal (Halichoerus grypus), Germany.

We detected a novel poxvirus from a gray seal (Halichoerus grypus) from the North Sea, Germany. The juvenile animal showed pox-like lesions and deteriorating overall health condition and was finally euthanized. Histology, electron microscopy, sequencing, and PCR confirmed a previously undescribed poxvirus of the Chordopoxvirinae subfamily, tentatively named Wadden Sea poxvirus.

Effect of predation risk on parasite transmission from first to second intermediate trematode hosts.

Predators can affect parasite-host interactions when directly preying on hosts or their parasites. However, predators may also have non-consumptive indirect effects on parasite-host interactions when hosts adjust their behaviour or physiology in response to predator presence. In this study, we examined how chemical cues from a predatory marine crab affect the transmission of a parasitic trematode from its first (periwinkle) to its second (mussel) intermediate host. Laboratory experiments revealed that chemical cues from crabs lead to a threefold increase in the release of trematode cercariae from periwinkles as a result of increased periwinkle activity. This positive effect on transmission was contrasted by a 10-fold reduction in cercarial infection rates in the second intermediate host when we experimentally exposed mussels to cercariae and predator cues. The low infection rates were caused by a substantial reduction in mussel filtration activity in the presence of predator cues, preventing cercariae from entering the mussels. To assess the combined net effect of both processes, we conducted a transmission experiment between infected periwinkles and uninfected mussels. Infection levels of mussels in the treatments with crab cues were sevenfold lower than in mussels without crab chemical cues. This suggests that predation risk effects on mussel susceptibility can counteract the elevated parasite release from first intermediate hosts, with negative net effects on parasite transmission. These experiments highlight that predation risk effects on parasite transmission can have opposing directions at different stages of the parasite's life cycle. Such complex non-consumptive predation risk effects on parasite transmission may constitute an important indirect mechanism affecting prevalence and distribution patterns of parasites in different hosts across their life cycle.

Conceptions of prospective biology teachers about the Wadden Sea ecosystem.

The present study contributes to the thematization of the UNESCO World Heritage Site Wadden Sea in biology didactics. Despite the uniqueness and high potential of the Wadden Sea ecosystem, especially for out-of-school learning, it has hardly been considered in biology didactics so far. The overall aim of this study is to gain insight into prospective biology teachers' existing conceptions regarding the Wadden Sea. Students are not only learners in their role at the university but prospective teachers as well due to their intended professional goal. Therefore, they can be considered the intersection of these two perspectives and are of particular interest to relevant research projects. In this paper, prospective biology teachers (n = 209, mean age 22.89 years) from Germany were surveyed using a word association test. Associations to the stimulus words Wadden Sea, mudflat hiking tour, tides, national park, and UNESCO World Heritage Site were collected. In the analysis, a category system was developed as literally as possible from the associations. This paper uses mind maps to provide a detailed overview of the identified associations. There was a wide range of identified associations: In addition to subject-area-related and subject-didactic associations, there were experience-oriented associations as well as associations unrelated to the subject. To place these results in context, secondary school students' associations to the same stimulus words are used for comparison. A central commonality is associations that encompass the experience possibilities at the Wadden Sea. In contrast to the secondary school students, the prospective teachers focus more on the school context. Conclusions are drawn regarding the education of biology teachers. In addition to identifying possible future research projects, this study suggests the need to consider the Wadden Sea in university teacher training.

Body condition and energy content of the shore crab Carcinus maenas L. in a temperate coastal system: the cost of barnacle epibiosis.

The impact of barnacle epibionts on the condition of the shore crab Carcinus maenas was studied for the western Wadden Sea population. Approximately 39% of the crabs were fouled with the barnacle Balanus crenatus. Although the morphological Fulton's K condition decreased by 5.8% in fouled crabs, Linear Mixed-Effects Models (LMM) showed that only the energetic condition of the crabs was significantly affected by fouling. The energy density of fouled crabs was consistently poorer (4.1% in AFDW; 8.7% in dry weight) than that of non-fouled crabs, especially in females and green forms in dry weight (12.8% and 11.4% reduction, respectively). Cumulative infection with Sacculina carcini, detected in 4.5% of the fouled crabs, additionally reduced by 14.3% the energy density in dry weight and almost to half of the total energy of the fouled crabs. Impacts of energy density reduction on crabs' growth and reproduction are discussed.

Sacculina carcini impact on energy content of the shore crab Carcinus maenas L.

The impact of Sacculina carcini infection on the nutritional status of the shore crab Carcinus maenas was investigated in the western Dutch Wadden Sea for a period of 20 months. About 3.3% of the population was sacculinized, i.e. externally infected with S. carcini and only 0.7% presented scars of previous infection. The results of mixed linear models showed that sacculinized and non-sacculinized crabs had similar morphometric condition, while the energy density of parasitized crabs (externa excluded) was significantly reduced by about 4.3% overall, and by up to 5.8% in crabs under 40 mm carapace width. However, when Sacculina externa was included in the energy determinations, the difference in energy density decreased to 1.2%, while total energy content of the pair infected crab-parasite including externa was 30.8% higher than non-sacculinized crabs of similar size. The total energy content of ovigerous females (eggs included) was even higher, near doubling the energy of similar-sized crabs. The same way, total energy content of Sacculina externa was about 4 times lower than total energy of egg mass. The results suggest that the rhizocephalan parasite is efficient in consuming the energy that the host may allocate for growth and maintenance, but require future studies to disentangle the impact of the degree of internal infection and the implications for the dynamics of the population.

Nanoplastics and ultrafine microplastic in the Dutch Wadden Sea - The hidden plastics debris?

Plastic pollution in the marine environment has been identified as a global problem; different polymer types and fragment sizes have been detected across all marine regions, from sea ice to the equator and the surface to the deep sea. However, quantification of marine plastics debris in the size range of nanoplastics (<1 µm) and ultrafine microplastics (<10 µm) is not constrained, because such minuscule particles are challenging to measure. In this work, we applied a novel analytical assay using Thermal Desorption - Proton Transfer Reaction - Mass Spectrometry (TD-PTR-MS), which is suitable to detect and identify plastics in the nanogram range. From two stations in the Wadden Sea (the Netherlands), we measured nanoplastics directly from seawater aliquots, and from filters with different mesh sizes. Our results show the presence of Polystyrene (PS) and Polyethylene terephthalate (PET) nanopalstics as well as ultrafine microplastics in the Wadden Sea water column. The mass concentration of PS nanoplastics was 4.2 µg/L on average, indicating a substantial contribution of nanoplastics to the Wadden Sea's total plastic budget.

The application of an environmental performance framework for climate adaptation innovations on two nature-based adaptations.

In this paper, we introduce and test a framework to qualitatively assess the environmental impact of climate adaptation innovations with the ambition to facilitate the implementation of these adaptations. The framework was designed to enable continuous environmentally conscious benchmarking based on three environmental performance indicators: sustainable design, environmental impact and ecological impact. It was pilot tested by uninvolved experts and key-persons for two large-scale nature-based flood adaptation innovations in the Netherlands and discussed with environmental assessment professionals. Our findings indicate how the inclusion of our framework helps to identify important knowledge gaps regarding environmental co-benefits and trade-offs, and can be beneficial to both those developing the innovation and the local authorities charged with assessing the suitability of innovations. We conclude by noting how the incorporation of environmental impact assessment from the design stage of adaptations could supplement existing environmental assessment regulations pre-empting concerns rather than reacting to them.

Out-of-School Learning in the Wadden Sea: The Influence of a Mudflat Hiking Tour on the Environmental Attitudes and Environmental Knowledge of Secondary School Students.

In this study, the Wadden Sea, as an out-of-school learning site, is considered from an empirical-research perspective of environmental education. The Wadden Sea in Germany is part of the largest contiguous mudflat area in the world. Although much evidence is already available on different teaching and learning processes at various out-of-school learning sites, this is not yet the case for the Wadden Sea. This research gap was taken up. In this paper, 427 students (mean age: 11.74 years) participated in a mudflat hiking tour. A pre-post-test design followed by a retention test was used to determine the impact of this on participants' environmental attitudes and environmental knowledge. The single factor analyses of variance with repeated measures demonstrated that the mudflat hiking tour had both a positive short-term and a positive long-term impact on environmental attitudes, as well as on environmental knowledge. All three constructs could, therefore, be positively influenced by the intervention. Correlation analyses revealed a positive relationship between environmental attitudes and environmental knowledge at three measurement time points. These results empirically confirm the potential of the Wadden Sea as an out-of-school learning site for environmental education with students from secondary schools. The effectiveness of non-formal education in this ecological environment can be proven.

No evidence for reduced growth in resident fish species in the era of de-eutrophication in a coastal area in NW Europe.

Coastal areas in north-western Europe have been influenced by elevated nutrient levels starting in the 1960s. Due to efficient measures, both nitrate and phosphate levels decreased since the mid-1980s. The co-occurring declines in nutrient loadings and fish productivity are often presumed to be causally linked. We investigated whether four resident fish species (twaite shad, bull-rout, thick-lipped grey mullet and eelpout), that spend the majority of their life in the vicinity of the coast, differed in growth between the historic eutrophication period compared to the recent lower nutrient-level period. Based on Von Bertalanffy growth models of length at age, and the analysis of annual otolith increments, we investigated the difference in sex-specific growth patterns and related these to temperature, eutrophication level (Chlorophyll a), growth window and fish density. In all four species, annual otolith growth rates during the early life stages differed between the two periods, mostly resulting in larger lengths at age in the recent period. All species showed significant correlations between increment size and temperature, explaining the observed period differences. The lack of an effect of total fish biomass provided no evidence for density dependent growth. A correlation with chlorophyll was found in bull-rout, but the relationship was negative, thus not supporting the idea of growth enhanced by high nutrient levels. In conclusion, we found no evidence for reduced growth related to de-eutrophication. Our results indicate that temperature rise due to climate change had a greater impact on growth than reduced food availability due to de-eutrophication. We discuss potential consequences of growth changes for length-based indicators used in management.

Migrating curlews on schedule: departure and arrival patterns of a long-distance migrant depend on time and breeding location rather than on wind conditions.

BACKGROUND: Departure decisions in long-distance migratory bird species may depend on favourable weather conditions and beneficial resources at the destination location, overarched by genetic triggers. However, few studies have tried to validate the significance of these three concepts simultaneously, and long-term, high-resolution tagging datasets recording individual movements across consecutive years are scarce. We used such a dataset to explore intraspecific and intra-individual variabilities in departure and arrival decisions from/to wintering grounds in relation to these three different concepts in bird migration. METHODS: We equipped 23 curlews (Numenius arquata) wintering in the Wadden Sea with Global Positioning System data loggers to record their spatio-temporal patterns of departure from and arrival at their wintering site, and the first part of their spring migration. We obtained data for 42 migrations over 6 years, with 12 individuals performing repeat migrations in consecutive years. Day of year of departure and arrival was related to 38 meteorological and bird-related predictors using the least absolute shrinkage and selection operator (LASSO) to identify drivers of departure and arrival decisions. RESULTS: Curlews migrated almost exclusively to Arctic and sub-Arctic Russia for breeding. They left their wintering site mainly during the evening from mid- to late April and returned between the end of June and mid-July. There was no difference in departure times between the sexes. Weather parameters did not impact departure decisions; if departure days coincided with headwind conditions, the birds accounted for this by flying at higher altitudes of up to several kilometres. Curlews breeding further away in areas with late snowmelt departed later. Departures dates varied by only < 4 days in individual curlews tagged over consecutive years. CONCLUSIONS: These results suggest that the trigger for migration in this long-distance migrant is largely independent of weather conditions but is subject to resource availability in breeding areas. The high intra-individual repeatability of departure days among subsequent years and the lack of relationship to weather parameters suggest the importance of genetic triggers in prompting the start of migration. Further insights into the timing of migration in immatures and closely related birds might help to further unravel the genetic mechanisms triggering migration patterns.

False-positive enterococci counts in seawater with the IDEXX Enterolert-E most probable number technique caused by Bacillus licheniformis.

Enterolert-E is an easy-to-use method for the enumeration of enterococci in water samples as an indicator of fecal pollution. This most probable number technique replaced the laborious and more time-consuming MEA-BEA plating method, and it is used extensively in ballast water testing and monitoring. In spring 2018, the Control Union Water ballast water test facility measured high enterococci concentrations in Wadden Sea water without any correlation with polluted freshwater input. By isolating bacteria from samples incubated in Enterolert-E culture medium, followed by analyses of colony morphology and DNA, it is shown that these erroneously high concentrations were caused by Bacillus licheniformis, a gram-positive rod-shaped chlorine-resistant bacterium. It is concluded that control analyses or the MEA-BEA method or dilution to reduce salinity must be performed when high enterococci concentrations are measured in water samples that are not suspected to be polluted.

High prevalences of disseminated neoplasia in the Baltic tellin Limecola balthica in the Wadden Sea.

The Baltic tellin Limecola balthica is one of the most common bivalves in intertidal areas in the Northern Hemisphere. Over the last 2 decades, the species has been suffering from a decrease in adult survival in the European Wadden Sea. While several factors such as global warming and fisheries have been suggested to influence the population dynamics of this bivalve mollusc, the potential role of diseases has never been investigated. In this study, we investigated whether disseminated neoplasia, a common proliferative disorder in bivalve molluscs, could play a potential role in the recent population decline of Baltic tellins in the Wadden Sea. We conducted a field survey in the Dutch Wadden Sea to (1) determine whether the disease occurs in Baltic tellins in the Wadden Sea and (2) quantify the occurrence and severity of the disease via histology. Disseminated neoplasia occurred in L. balthica at each of the 10 sampled locations with very high prevalences (21-89%) compared to those reported elsewhere for this species. The highest severity category was found in 8 to 87% of affected individuals, with severity generally increasing with prevalence. Disseminated neoplasia usually increases mortality among affected individuals and may also be associated with important sub-lethal effects, especially regarding gametogenesis. Thus, we suggest that disseminated neoplasia may play a key role in the population dynamics of the Baltic tellin, the extent of which remains to be investigated in future studies.

Molecular Targets for Coevolutionary Interactions Between Pacific Oyster Larvae and Their Sympatric Vibrios.

Bacteria of the Vibrio genus are the most predominant infectious agents threatening marine wildlife and aquaculture. Due to the large genetic diversity of these pathogens, the molecular determinants of Vibrio virulence are only poorly understood. Furthermore, studies tend to ignore co-evolutionary interactions between different host populations and their locally encountered Vibrio communities. Here, we explore the molecular targets of such co-evolutionary interactions by analyzing the genomes of nine Vibrio strains from the Splendidus-clade showing opposite virulence patterns towards two populations of Pacific oysters introduced into European Wadden Sea. By contrasting Vibrio phylogeny to their host specific virulence patterns, we could identify two core genome genes (OG1907 and OG 3159) that determine the genotype by genotype (G × G) interactions between oyster larvae and their sympatric Vibrio communities. Both genes show positive selection between locations targeting only few amino acid positions. Deletion of each gene led to a loss of the host specific virulence patterns while complementation with OG3159 alleles from both locations could recreate the wild type phenotypes matching the origin of the allele. This indicates that both genes can act as a genetic switch for Vibrio-oyster coevolution demonstrating that local adaptation in distinct Vibrio lineages can rely on only few genes independent of larger pathogenicity islands or plasmids.

How invasive oysters can affect parasite infection patterns in native mussels on a large spatial scale.

There are surprisingly few field studies on the role of invasive species on parasite infection patterns in native hosts. We investigated the role of invasive Pacific oysters (Magallana gigas) in determining parasite infection levels in native blue mussels (Mytilus edulis) in relation to other environmental and biotic factors. Using hierarchical field sampling covering three spatial scales along a large intertidal ecosystem (European Wadden Sea), we found strong spatial differences in infection levels of five parasite species associated with mussels and oysters. We applied mixed models to analyse the associations between parasite prevalence and abundance in mussels and oysters, and 12 biological and environmental factors. For each parasite-host relationship, an optimal model (either a null, one-factor or two-factor model) was selected based on AIC scores. We found that the density of invasive oysters contributed to three of the 12 models. Other biological factors such as host size (six models), and the density of target or alternative host species (five models) contributed more frequently to the best models. Furthermore, for parasite species infecting both mussels and oysters, parasite population densities were higher in native mussels, attributed to the higher densities of mussels. Our results indicate that invasive species can affect parasite infection patterns in native species in the field, but that their relative contribution may be further mediated by other biological and environmental parameters. These results stress the usefulness of large-scale field studies for detailed assessments of the mechanisms underlying the impacts of invasive species on native host communities.

Infection by invasive parasites increases susceptibility of native hosts to secondary infection via modulation of cellular immunity.

Parasite spillover from invasive aliens to native species increases the risk of disease emergence within native biota-either by direct harm to the new host or by indirect effects like increased risks of secondary infection. One example for such a detrimental effect is the parasitic copepod Mytilicola intestinalis that infected blue mussels Mytilus edulis after being introduced into the North Sea in the early 20th century. Since 1949, the parasite was blamed for multiple mass mortalities of infested blue mussels but evidence for a direct causal involvement of M. intestinalis remained circumstantial. Here, we now examine the potential effects of primary infections by the invasive parasite on the susceptibility to secondary infections with virulent bacteria (Vibrio spp.) in a full factorial infection experiment combining parasite infection (control vs. infected) with different Vibrio infection treatments (control, bath challenge, injection) in environmental conditions that either favoured the host (ambient temperature) or the bacterium (elevated temperature). The influence of primary and secondary infections on cellular immunity (phagocytosis) and Vibrio load in the haemolymph was used to correlate these results to host survival. Our results suggest that the rate of secondary Vibrio infection is increased due to lower efficiency of the cellular immune response. As a consequence, the failure of clearing Vibrio from the haemolymph might increase mortality of mussels infected by M. intestinalis. This demonstrates that indirect effects of parasite invasions can outweigh direct effects of the infection highlighting the need for a more integrative approach to understand and predict the consequences of parasite invasions.

Benthic primary producers are key to sustain the Wadden Sea food web: stable carbon isotope analysis at landscape scale.

Coastal food webs can be supported by local benthic or pelagic primary producers and by the import of organic matter. Distinguishing between these energy sources is essential for our understanding of ecosystem functioning. However, the relative contribution of these components to the food web at the landscape scale is often unclear, as many studies lack good taxonomic and spatial resolution across large areas. Here, using stable carbon isotopes, we report on the primary carbon sources for consumers and their spatial variability across one of the world's largest intertidal ecosystems (Dutch Wadden Sea; 1460 km2 intertidal surface area), at an exceptionally high taxonomic (178 species) and spatial resolution (9,165 samples from 839 locations). The absence of overlap in δ13 C values between consumers and terrestrial organic matter suggests that benthic and pelagic producers dominate carbon input into this food web. In combination with the consistent enrichment of benthic primary producers (δ13 C -16.3‰) relative to pelagic primary producers (δ13 C -18.8) across the landscape, this allowed the use of a two-food-source isotope-mixing model. This spatially resolved modelling revealed that benthic primary producers (microphytobenthos) are the most important energy source for the majority of consumers at higher trophic levels (worms, molluscs, crustaceans, fish, and birds), and thus to the whole food web. In addition, we found large spatial heterogeneity in the δ13 C values of benthic primary producers (δ13 C -19.2 to -11.5‰) and primary consumers (δ13 C -25.5 to -9.9‰), emphasizing the need for spatially explicit sampling of benthic and pelagic primary producers in coastal ecosystems. Our findings have important implications for our understanding of the functioning of ecological networks and for the management of coastal ecosystems.