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.

Low-frequency noise pollution impairs burrowing activities of marine benthic invertebrates.

Sounds from human activities such as shipping and seismic surveys have been progressively invading natural soundscapes and pervading oceanic ambient sounds for decades. Benthic invertebrates are important ecosystem engineers that continually rework the sediment they live in. Here, we tested how low-frequency noise (LFN), a significant component of noise pollution, affects the sediment reworking activities of selected macrobenthic invertebrates. In a controlled laboratory setup, the effects of acute LFN exposure on the behavior of three abundant bioturbators on the North Atlantic coasts were explored for the first time by tracking their sediment reworking and bioirrigation activities in noisy and control environments via luminophore and sodium bromide (NaBr) tracers, respectively. The amphipod crustacean Corophium volutator was negatively affected by LFN, exhibiting lower bioturbation rates and shallower luminophore burial depths compared to controls. The effect of LFN on the polychaete Arenicola marina and the bivalve Limecola balthica remained inconclusive, although A. marina displayed greater variability in bioirrigation rates when exposed to LFN. Furthermore, a potential stress response was observed in L. balthica that could reduce bioturbation potential. Benthic macroinvertebrates may be in jeopardy along with the crucial ecosystem-maintaining services they provide. More research is urgently needed to understand, predict, and manage the impacts of anthropogenic noise pollution on marine fauna and their associated ecosystems.

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.

Small suspension-feeding amphipods play a pivotal role in carbon dynamics around offshore man-made structures.

The establishment of artificial hard substrates (i.e. offshore wind farms and oil and gas platforms) on marine soft sediments increases the available habitat for invertebrate communities that would otherwise be restricted to natural hard bottoms. Suspension feeding invertebrates clear a significant amount of particles from the water column and release organic matter in the form of feces, influencing the basis of marine food webs and affecting surrounding environments. Artificial structures in the southern North Sea are dominated by a suspension-feeding crustacean in terms of abundance and sometimes even biomass: the amphipod Jassa herdmani. Animal densities of this tiny biofouler are known to exceed 1 million individuals per m2. Despite their small body sizes and their simple filter apparatus, we hypothesized that J. herdmani is a highly effective suspension feeder with a significant impact on neighboring communities due to its high abundances. In a feeding experiment, individuals of J. herdmani were provided with either an algal or an animal diet under two different temperature regimes. Clearance rates and fecal-pellet carbon (FPC) were measured. The results revealed high clearance rates and subsequent FPC, which were more pronounced at the higher temperature. Furthermore, clearance rates and FPC varied insignificantly with different food items. We further used the current findings for upscaling calculations to the total number of offshore windfarms and oil and gas platforms in the southern North Sea. Our calculations indicated that J. herdmani alone clears 0.33-4.71 km3 water per year in the southern North Sea. At the same time, these amphipods release 255-547 tons of carbon per year by means of defecation, thus enriching the surrounding soft sediments with organic matter. Our study highlights that tiny amphipods can mediate indirect effects of man-made structures in the North Sea, which could have a profound impact on pelagic and benthic habitats.

Generalized changes of benthic communities after construction of wind farms in the southern North Sea.

Over the last years, the development of offshore renewable energy installations such as offshore wind farms led to an increasing number of man-made structures in marine environments. Since 2009, benthic impact monitoring programs were carried out in wind farms installed in the southern North Sea. We collated and analyzed data sets from three major monitoring programs. Our analysis considered a total of 2849 sampling points converted to a set of biodiversity response metrics. We analyzed biodiversity changes related to the implementation of offshore wind farms and generalized the correlation of these changes with spatial and temporal patterns. Our results demonstrate that depth, season and distance to structure (soft-bottom community) consistently determined diversity indicators and abundance parameters, whereas the age and the country affiliation were significantly related to some but not all indices. The water depth was the most important structuring factor for fouling communities while seasonal effects were driving most of the observed changes in soft-sediment communities. We demonstrate that a meta-analysis can provide an improved level of understanding of ecological patterns on large-scale effects of anthropogenic structures on marine biodiversity, which were not visible in single monitoring studies. We believe that meta-analyses should become an indispensable tool for management of offshore wind farm effects in the future, particularly in the view of the foreseen development of offshore renewable energies. This might lead to a better picture and more comprehensive view on potential alterations. However, this requires a modern open-source data policy and data management, across institutions and across national borders.

Jassa (Crustacea: Amphipoda): a new morphological and molecular assessment of the genus.

The amphipod genus Jassa Leach, 1814 now comprises 24 species that occur in temperate regions of both hemispheres on solid substrates from the lower intertidal zone to 500 m depth. The propensity for some species to form dense colonies in water intake structures and offshore platforms has brought them to attention as an unwanted pest. Based on the examination of ~25,000 specimens from ~1,100 museum and private collections, it is evident that some species of Jassa have been transported by human vectors since at least the 19th century and now occur widely. Their colonial, tube-living habit enables such transport, and collection records document them on ships, buoys and portable water systems as well as on natural movable substrates such as logs, drift algae and larger crustaceans. Because Jassa can be so readily found, but species discrimination has had a problematic history, the purpose of this monograph is to assist researchers to identify species through illustrations, descriptions, keys and habitat summaries. Seven species which were named in the 19th century but whose names have lapsed are placed in the context of currently known species. Two new species, J. laurieae n. sp. and J. kimi n. sp. are described, and J. monodon (Heller, 1866) and J. valida (Dana, 1853) are resurrected. Jassa mendozai Winfield et al., 2021 is submerged under J. valida, and J. cadetta Krapp et al., 2008 and J. trinacriae Krapp et al., 2010 are submerged under J. slatteryi Conlan, 1990. Morphological differences are related to current understanding of growth, behaviour and ecology. CO1 analysis suggests a Southern Hemisphere origin with diversification northward and an evolutionary direction toward greater physiological plasticity, leading to success in long distance transport and establishment in exotic locations. Correct identification of Jassa world-wide will facilitate further research on this ecologically important genus and will allow for differentiation of indigenous from exotic introductions.

Ancient globetrotters-connectivity and putative native ranges of two cosmopolitan biofouling amphipods.

The geographic distributions of some coastal marine species have appeared as cosmopolitan ever since they were first scientifically documented. In particular, for many benthic species that are associated with anthropogenic substrata, there is much speculation as to whether or not their broad distributions can be explained by natural mechanisms of dispersal. Here, we focused on two congeneric coastal crustaceans with cosmopolitan distributions-the tube-dwelling amphipods Jassa marmorata and Jassa slatteryi. Both species are common elements of marine biofouling on nearly all kinds of artificial hard substrata in temperate to warm seas. We hypothesized that the two species' modern occurrences across the oceans are the result of human shipping activities that started centuries ago. Mitochondrial DNA sequences of the CO1 fragment of specimens from distinct marine regions around the world were analysed, evaluating genetic structure and migration models and making inferences on putative native ranges of the two Jassa species. Populations of both species exhibited considerable genetic diversity with differing levels of geographic structure. For both species, at least two dominant haplotypes were shared among several geographic populations. Rapid demographic expansion and high migration rates between geographically distant regions support a scenario of ongoing dispersal all over the world. Our findings indicate that the likely former native range of J. marmorata is the Northwest Atlantic, whereas the likely former native range of J. slatteryi is the Northern Pacific region. As corroborated by the genetic connectivity between populations, shipping still appears to be the more successful vector of the two species' dispersal when compared to natural mechanisms. Historical invasion events that likely started centuries ago, along with current ongoing dispersal, confirm these species' identities as true "neocosmopolitans".

Marine stepping-stones: Connectivity of Mytilus edulis populations between offshore energy installations.

Recent papers have suggested that epifaunal organisms use artificial structures as stepping-stones to spread to areas that are too distant to reach in a single generation. With thousands of artificial structures present in the North Sea, we test the hypothesis that these structures are connected by water currents and act as an interconnected reef. Population genetic structure of the blue mussel, Mytilus edulis, was expected to follow a pattern predicted by a particle tracking model (PTM). Correlation between population genetic differentiation, based on microsatellite markers, and particle exchange was tested. Specimens of M. edulis were found at each location, although the PTM indicated that locations >85 km offshore were isolated from coastal subpopulations. The fixation coefficient FST correlated with the number of arrivals in the PTM. However, the number of effective migrants per generation as inferred from coalescent simulations did not show a strong correlation with the arriving particles. Isolation by distance analysis showed no increase in isolation with increasing distance and we did not find clear structure among the populations. The marine stepping-stone effect is obviously important for the distribution of M. edulis in the North Sea and it may influence ecologically comparable species in a similar way. In the absence of artificial shallow hard substrates, M. edulis would be unlikely to survive in offshore North Sea waters.

Gastropod pedal mucus retains microplastics and promotes the uptake of particles by marine periwinkles.

The rapid dissemination of microplastics in many habitats of the oceans has raised concerns about the consequences for marine biota and ecosystems. Many adverse effects of microplastics on marine invertebrates are consequences of ingestion. Accordingly, the identification of mechanisms that facilitate the uptake of microplastics is essential for the evaluation of possible implications for marine organisms and food webs. Gastropods produce mucus for locomotion. Gastropod pedal mucus naturally retains formerly suspended micro-organisms, such as bacteria, microalgae, and seaweed spores. The retained organisms are consumed by gastropods that forage on pedal mucus. Here, we investigated the potential of gastropod pedal mucus to retain suspended microplastic particles and make them available for ingestion by periwinkles that forage on the contaminated mucus. In laboratory experiments, mucus of the periwinkles Littorina littorea and Littorina obtusata efficiently retained microplastics. Retention of microplastics varied between mucus from conspecifics of different size but not between mucus from either species. The density of microplastics in mucus trails increased concomitantly with the experimental particle concentration but was independent of incubation time. Aging of mucus and, particularly, desiccation affected the retention of microplastics. Periwinkles ingested microplastics when foraging on the contaminated mucus. Our results reveal a functional link between biogenic accumulation of microplastics and their trophic transfer by marine benthic herbivores into marine food webs.

Cryptic species in a well-known habitat: applying taxonomics to the amphipod genus Epimeria (Crustacea, Peracarida).

Taxonomy plays a central role in biological sciences. It provides a communication system for scientists as it aims to enable correct identification of the studied organisms. As a consequence, species descriptions should seek to include as much available information as possible at species level to follow an integrative concept of 'taxonomics'. Here, we describe the cryptic species Epimeria frankei sp. nov. from the North Sea, and also redescribe its sister species, Epimeria cornigera. The morphological information obtained is substantiated by DNA barcodes and complete nuclear 18S rRNA gene sequences. In addition, we provide, for the first time, full mitochondrial genome data as part of a metazoan species description for a holotype, as well as the neotype. This study represents the first successful implementation of the recently proposed concept of taxonomics, using data from high-throughput technologies for integrative taxonomic studies, allowing the highest level of confidence for both biodiversity and ecological research.

Combined effects of predator cues and competition define habitat choice and food consumption of amphipod mesograzers.

Predation has direct impact on prey populations by reducing prey abundance. In addition, predator presence alone can also have non-consumptive effects on prey species, potentially influencing their interspecific interactions and thus the structure of entire assemblages. The performance of potential prey species may, therefore, depend on both the presence of predators and competitors. We studied habitat use and food consumption of a marine mesograzer, the amphipod Echinogammarus marinus, in the presence/absence of a fish mesopredator and/or an amphipod competitor. The presence of the predator affected both habitat choice and food consumption of the grazer, indicating a trade-off between the use of predator-free space and food acquisition. Without the predator, E. marinus were distributed equally over different microhabitats, whereas in the presence of the predator, most individuals chose a sheltered microhabitat and reduced their food consumption. Furthermore, habitat choice of the amphipods changed in the presence of interspecific competitors, also resulting in reduced feeding rates. The performance of E. marinus is apparently driven by trait-mediated direct and indirect effects caused by the interplay of predator avoidance and competition. This highlights the importance of potential non-consumptive impacts of predators on their prey organisms. The flexible responses of small invertebrate consumers to the combined effects of predation and competition potentially lead to changes in the structure of coastal ecosystems and the multiple species interactions therein.

The Application of DNA Barcodes for the Identification of Marine Crustaceans from the North Sea and Adjacent Regions.

During the last years DNA barcoding has become a popular method of choice for molecular specimen identification. Here we present a comprehensive DNA barcode library of various crustacean taxa found in the North Sea, one of the most extensively studied marine regions of the world. Our data set includes 1,332 barcodes covering 205 species, including taxa of the Amphipoda, Copepoda, Decapoda, Isopoda, Thecostraca, and others. This dataset represents the most extensive DNA barcode library of the Crustacea in terms of species number to date. By using the Barcode of Life Data Systems (BOLD), unique BINs were identified for 198 (96.6%) of the analyzed species. Six species were characterized by two BINs (2.9%), and three BINs were found for the amphipod species Gammarus salinus Spooner, 1947 (0.4%). Intraspecific distances with values higher than 2.2% were revealed for 13 species (6.3%). Exceptionally high distances of up to 14.87% between two distinct but monophyletic clusters were found for the parasitic copepod Caligus elongatus Nordmann, 1832, supporting the results of previous studies that indicated the existence of an overlooked sea louse species. In contrast to these high distances, haplotype-sharing was observed for two decapod spider crab species, Macropodia parva Van Noort & Adema, 1985 and Macropodia rostrata (Linnaeus, 1761), underlining the need for a taxonomic revision of both species. Summarizing the results, our study confirms the application of DNA barcodes as highly effective identification system for the analyzed marine crustaceans of the North Sea and represents an important milestone for modern biodiversity assessment studies using barcode sequences.