A Pleistocene legacy structures variation in modern seagrass ecosystems.

Distribution of Earth's biomes is structured by the match between climate and plant traits, which in turn shape associated communities and ecosystem processes and services. However, that climate-trait match can be disrupted by historical events, with lasting ecosystem impacts. As Earth's environment changes faster than at any time in human history, critical questions are whether and how organismal traits and ecosystems can adjust to altered conditions. We quantified the relative importance of current environmental forcing versus evolutionary history in shaping the growth form (stature and biomass) and associated community of eelgrass (Zostera marina), a widespread foundation plant of marine ecosystems along Northern Hemisphere coastlines, which experienced major shifts in distribution and genetic composition during the Pleistocene. We found that eelgrass stature and biomass retain a legacy of the Pleistocene colonization of the Atlantic from the ancestral Pacific range and of more recent within-basin bottlenecks and genetic differentiation. This evolutionary legacy in turn influences the biomass of associated algae and invertebrates that fuel coastal food webs, with effects comparable to or stronger than effects of current environmental forcing. Such historical lags in phenotypic acclimatization may constrain ecosystem adjustments to rapid anthropogenic climate change, thus altering predictions about the future functioning of ecosystems.

Trophic niches of macrobenthos: Latitudinal variation indicates climate change impact on ecosystem functioning.

Benthic food-web structure and organic matter (OM) utilization are important for marine ecosystem functioning. In response to environmental changes related to the ongoing climate change, however, many benthic species are shifting their ranges to colder regions, which may lead to altered community composition, but it remains largely unknown how it will affect ecosystem functioning. Here, stable isotope analysis was used to study benthic OM utilization and food-web structure and to assess whether their spatial patterns reflect today's community differentiation among biogeographic regions and depth zones. Benthic fauna and OM mixtures were collected from two depth zones (100-150 m vs. 200-250 m) within a temperate, two sub-Arctic, and an Arctic fjord along a latitudinal gradient (59-78° N) that was used as a space-for-time substitution to assess the impact of climate change. Our results showed that Arctic and temperate communities are functionally different. Arctic communities were characterized by a strong resource partitioning among different feeding types, irrespective of depth zone. In contrast, all feeding types in temperate communities seemed to rely on sedimentary OM. The sub-Arctic presented a transition zone. In the sub-Arctic, shallower communities resembled Arctic communities, suggesting a functional transition between temperate and sub-Arctic regions. Deeper sub-Arctic communities resembled temperate communities, suggesting a functional transition between the sub-Arctic and Arctic regions. This implies that the regions north of the current transitions (deep Arctic and shallow sub-Arctic) are most likely to experience functional changes related to an altered OM utilization in benthic food webs in response to climate change.

The biogeography of community assembly: latitude and predation drive variation in community trait distribution in a guild of epifaunal crustaceans.

While considerable evidence exists of biogeographic patterns in the intensity of species interactions, the influence of these patterns on variation in community structure is less clear. Studying how the distributions of traits in communities vary along global gradients can inform how variation in interactions and other factors contribute to the process of community assembly. Using a model selection approach on measures of trait dispersion in crustaceans associated with eelgrass (Zostera marina) spanning 30° of latitude in two oceans, we found that dispersion strongly increased with increasing predation and decreasing latitude. Ocean and epiphyte load appeared as secondary predictors; Pacific communities were more overdispersed while Atlantic communities were more clustered, and increasing epiphytes were associated with increased clustering. By examining how species interactions and environmental filters influence community structure across biogeographic regions, we demonstrate how both latitudinal variation in species interactions and historical contingency shape these responses. Community trait distributions have implications for ecosystem stability and functioning, and integrating large-scale observations of environmental filters, species interactions and traits can help us predict how communities may respond to environmental change.

Methodological elements for optimising the spatial monitoring design to support regional benthic ecosystem assessments.

Benthic habitat condition assessments are a requirement under various environmental directives. The Marine Strategy Framework Directive (MSFD), for example, challenges member states in a European sea region to perform comparable assessments of good environmental status and improve coherence of their monitoring programmes by 2020. Currently, North Sea countries operate independent monitoring programmes using nationally defined assessment areas. Lack of an agreed OSPAR or EU scale monitoring method and programme has been identified as a priority science need. This paper proposes a method for the development of a coherent and efficient spatial sampling design for benthic habitats on regional level and gives advice on optimal monitoring effort to get more accurate assessments. We use ecologically relevant assessment areas (strata) across national borders and test spatial sample allocation methods. Furthermore, we investigate the number of samples needed in each stratum to reduce the variance for estimating mean number of taxa and abundance. The stratification needs to take into account the spatial heterogeneity of the entire ecosystem. The total sample effort is optimal when sample allocation takes into account the size and benthic variability within those strata. Change point analysis helps to find a balance between sampling effort and precision of the benthic parameter estimate. A joint sampling design for the North Sea could be generated by combining current efforts, and where needed adapting existing national programmes. This serves a coordinated, region-wide, benthic condition status assessment and strengthens regional cooperation to fulfil multiple monitoring tasks, with a scientifically underpinned common approach.

Thyasirid species composition (Bivalvia: Thyasiridae) and genetic connectivity of Parathyasira equalis (A. E. Verrill & K. J. Bush, 1898) in deep basins of sub-Arctic fjords.

BACKGROUND: Thyasirid bivalves are often recorded as a dominant component of macrobenthic infaunal communities in depositional environments such as fjord basins. Fjord basins comprise patchy soft-bottom habitats bounded by steep walls and sills; however, little is known how this semi-isolated nature of fjords affects benthic populations. Accordingly, data on the composition and population connectivity of thyasirids can provide valuable information on the ecology of these ecosystems. RESULTS: The species composition of thyasirid bivalves has been studied in the basins of three sub-Arctic fjords (Nordland, Northern Norway). Overall, six thyasirid species were recorded: Parathyasira equalis, Parathyasira dunbari, Mendicula ferruginosa, Genaxinus eumyarius, Thyasira sarsii, and Thyasira obsoleta. The species composition remained stable within the basins during the sampling period (2013-2020) and suggested the importance of local reproduction over advection of individuals for population dynamics. Only one species, Parathyasira equalis, was common in all fjords. We have further investigated the population genetics of this species by combining two types of genetic markers: a 579 bp fragment of the cytochrome c oxidase subunit I (COI) gene and 4043 single-nucleotide polymorphisms (SNPs) generated by genotyping-by-sequencing. The latter provided a more in-depth resolution on the population genetics of this species and revealed a weak but significant differentiation of populations within fjords, further indicating limited connectivity between basins. CONCLUSION: Based on our findings, we conclude that limited dispersal between the basin communities results in weakly connected populations and might be an important structuring factor for macrobenthic communities.

Future trends of marine fish biomass distributions from the North Sea to the Barents Sea.

Climate warming is one of the facets of anthropogenic global change predicted to increase in the future, its magnitude depending on present-day decisions. The north Atlantic and Arctic Oceans are already undergoing community changes, with warmer-water species expanding northwards, and colder-water species retracting. However, the future extent and implications of these shifts remain unclear. Here, we fitted a joint species distribution model to occurrence data of 107, and biomass data of 61 marine fish species from 16,345 fishery independent trawls sampled between 2004 and 2022 in the northeast Atlantic Ocean, including the Barents Sea. We project overall increases in richness and declines in relative dominance in the community, and generalised increases in species' ranges and biomass across three different future scenarios in 2050 and 2100. The projected decline of capelin and the practical extirpation of polar cod from the system, the two most abundant species in the Barents Sea, drove an overall reduction in fish biomass at Arctic latitudes that is not replaced by expanding species. Furthermore, our projections suggest that Arctic demersal fish will be at high risk of extinction by the end of the century if no climate refugia is available at eastern latitudes.

Benthic remineralization under future Arctic conditions and evaluating the potential for changes in carbon sequestration in warming sediments.

Benthic (seafloor) remineralization of organic material determines the fate of carbon in the ocean and its sequestration. Bottom water temperature and labile carbon supply to the seafloor are expected to increase in a warming Arctic and correspondingly, benthic remineralization rates. We provide some of the first experimental data on the response of sediment oxygen demand (SOD), an established proxy for benthic remineralization, to increased temperature and/or food supply across a range of Arctic conditions and regimes. Each factor significantly increased SOD rates (with different degrees of variability); however the largest increases were seen with both factors combined (50% to ten-fold increases), consistently across the four seasons and the spatial gradient covering shelf to deep basin included in our study. This ability of the Arctic benthos to process increased pulses of carbon suggests that increased sedimented carbon under warming conditions is likely to be utilized and processed, not accumulated, impacting carbon storage and decreasing the Arctic's role as a global carbon sink.

Seasonality of primary production explains the richness of pioneering benthic communities.

A pattern of increasing species richness from the poles to the equator is frequently observed in many animal taxa. Ecological limits, determined by the abiotic conditions and biotic interactions within an environment, are one of the major factors influencing the geographical distribution of species diversity. Energy availability is often considered a crucial limiting factor, with temperature and productivity serving as empirical measures. However, these measures may not fully explain the observed species richness, particularly in marine ecosystems. Here, through a global comparative approach and standardised methodologies, such as Autonomous Reef Monitoring Structures (ARMS) and DNA metabarcoding, we show that the seasonality of primary production explains sessile animal richness comparatively or better than surface temperature or primary productivity alone. A Hierarchical Generalised Additive Model (HGAM) is validated, after a model selection procedure, and the prediction error is compared, following a cross-validation approach, with HGAMs including environmental variables commonly used to explain animal richness. Moreover, the linear effect of production magnitude on species richness becomes apparent only when considered jointly with seasonality, and, by identifying world coastal areas characterized by extreme values of both, we postulate that this effect may result in a positive relationship in environments with lower seasonality.

Over 20% of marine fishes shifting in the North and Barents Seas, but not in the Norwegian Sea.

Climate warming generally induces poleward range expansions and equatorward range contractions of species' environmental niches on a global scale. Here, we examined the direction and magnitude of species biomass centroid geographic shifts in relation to temperature and depth for 83 fish species in 9,522 standardised research trawls from the North Sea (1998-2020) to the Norwegian (2000-2020) and Barents Sea (2004-2020). We detected an overall significant northward shift of the marine fish community biomass in the North Sea, and individual species northward shifts in the Barents and North Seas, in 20% and 25% of the species' biomass centroids in each respective region. We did not detect overall community shifts in the Norwegian Sea, where two species (8%) shifted in each direction (northwards and southwards). Among 9 biological traits, species biogeographic assignation, preferred temperature, age at maturity and maximum depth were significant explanatory variables for species latitudinal shifts in some of the study areas, and Arctic species shifted significantly faster than boreal species in the Barents Sea. Overall, our results suggest a strong influence of other factors, such as biological interactions, in determining several species' recent geographic shifts.

Seafloor warm water temperature anomalies impact benthic macrofauna communities of a high-Arctic cold-water fjord.

Amid the alarming atmospheric and oceanic warming rates taking place in the Arctic, western fjords around the Svalbard archipelago are experiencing an increased frequency of warm water intrusions in recent decades, causing ecological shifts in their ecosystems. However, hardly anything is known about their potential impacts on the until recently considered stable and colder northern fjords. We analyzed macrobenthic fauna from four locations in Rijpfjorden (a high-Arctic fjord in the north of Svalbard) along its axis, sampled intermittently in the years 2003, 2007, 2010, 2013 and 2017. After a strong seafloor warm water temperature anomaly (SfWWTA) in 2006, the abundance of individuals and species richness dropped significantly across the entire fjord in 2007, together with diversity declines at the outer parts (reflected in Shannon index drops) and increases in beta diversity between inner and outer parts of the fjord. After a period of three years with stable water temperatures and higher sea-ice cover, communities recovered through recolonization processes by 2010, leading to homogenization in community composition across the fjord and less beta diversity. For the last two periods (2010-2013 and 2013-2017), beta diversity between the inner and outer parts gradually increased again, and both the inner and outer sites started to re-assemble in different directions. A few taxa began to dominate the fjord from 2010 onwards at the outer parts, translating into evenness and diversity drops. The inner basin, however, although experiencing strong shifts in abundances, was partially protected by a fjordic sill from impacts of these temperature anomalies and remained comparatively more stable regarding community diversity after the disturbance event. Our results indicate that although shifts in abundances were behind important spatio-temporal community fluctuations, beta diversity variations were also driven by the occurrence-based macrofauna data, suggesting an important role of rare taxa. This is the first multidecadal time series of soft-bottom macrobenthic communities for a high-Arctic fjord, indicating that potential periodic marine heatwaves might drive shifts in community structure, either through direct effects from thermal stress on the communities or through changes in environmental regimes led by temperature fluctuations (i.e. sea ice cover and glacial runoff, which could lead to shifts in primary production and food supply to the benthos). Although high-Arctic macrobenthic communities might be resilient to some extent, sustained warm water anomalies could lead to permanent changes in cold-water fjordic benthic systems.

Benthic ecosystem functioning under climate change: modelling the bioturbation potential for benthic key species in the southern North Sea.

Climate change affects the marine environment on many levels with profound consequences for numerous biological, chemical, and physical processes. Benthic bioturbation is one of the most relevant and significant processes for benthic-pelagic coupling and biogeochemical fluxes in marine sediments, such as the uptake, transport, and remineralisation of organic carbon. However, only little is known about how climate change affects the distribution and intensity of benthic bioturbation of a shallow temperate shelf sea system such as the southern North Sea. In this study, we modelled and projected changes in bioturbation potential (BPp) under a continuous global warming scenario for seven southern North Sea key bioturbators: Abra alba, Amphiura filiformis, Callianassa subterranea, Echinocardium cordatum, Goniada maculata, Nephtys hombergii, and Nucula nitidosa. Spatial changes in species bioturbation intensity are simulated for the years 2050 and 2099 based on one species distribution model per species driven by bottom temperature and salinity changes using the IPCC SRES scenario A1B. Local mean bottom temperature was projected to increase between 0.15 and 5.4 °C, while mean bottom salinity was projected to moderately decrease by 1.7. Our results show that the considered benthic species are strongly influenced by the temperature increase. Although the total BP remained rather constant in the southern North Sea, the BPp for four out of seven species was projected to increase, mainly due to a simultaneous northward range expansion, while the BPp in the core area of the southern North Sea declined for the same species. Bioturbation of the most important species, Amphiura filiformis and Echinocardium cordatum, showed no substantial change in the spatial distribution, but over time. The BPp of E. cordatum remained almost constant until 2099, while the BPp of A. filiformis decreased by 41%. The northward expansion of some species and the decline of most species in the south led to a change of relative contribution to bioturbation in the southern North Sea. These results indicate that some of the selected key bioturbators in the southern North Sea might partly compensate the decrease in bioturbation by others. But especially in the depositional areas where bioturbation plays a specifically important role for ecosystem functioning, bioturbation potential declined until 2099, which might affect the biochemical cycling in sediments of some areas of the southern North Sea.

Exploring the potential of mRNA for taxonomic delineation of marine benthic eukaryotes.

Direct sequencing of mRNA isolated from environmental samples has been commonly used to analyze the functional activity of ambient communities and, occasionally used for taxonomic identification. Here we assess the viability of using mRNA for investigating the species composition of marine benthic eukaryotes. Total RNA was extracted from sediments sampled close to fish farms and mRNA was sequenced after poly-A enrichment on an Illumina MiSeq sequencer. We investigated the origin of both raw reads and assembled contigs by aligning them to the NCBI non-redundant (nr/nt) nucleotide database. Although sequences were predominantly of eukaryotic origin, the analyses were complicated both by experimental and database artefacts. These issues were addressed by applying filtering procedures that removed the majority of ambiguous sequences from downstream analyses. These processes resulted in a set of 436 high-confidence contigs, the vast majority of which mapped to benthic organisms. Our alignments were dominated by annelids, consistent with burrowing groups found in a parallel morphological analysis. This study shows that it is possible to obtain adequate taxonomic information from the RNA of an eukaryotic community from a limited sample at a moderate cost, demonstrates how both laboratory and in silico artefacts can be overcome through appropriate bioinformatic procedures, and finally highlights some of the drawbacks and caveats of using NCBI as a reference database for such a dataset.

Impact of aquaculture and agriculture nutrient sources on macroalgae in a bioassay study.

Eutrophication is a major threat to aquatic ecosystems, because excessive nutrient enrichment may result in the loss of ecosystem services. Fjord systems are specifically under pressure due to nutrient input from land (agriculture) and sea (aquaculture). In this bioassay study, we have analyzed the effect of different nutrient sources, as well as their combination, on growth, nutrient composition and recruitment of habitat-forming and ephemeral macrophytes. We found that agricultural fertilizer increased growth for all algae (except Fucus), while the fish farm effluents mainly increased growth of Ulva. The C:N ratio was hardly affected by the fish farm, but decreased significantly in all algae when agriculture fertilizer was added. Most interestingly, however, distance to the fish farm modulated the algal response to the fertilizer. Our results demonstrate the importance of studying effects of multiple stressors in aquatic ecosystems to sustainably manage the consequences of anthropogenic impacts.

Seasonal dynamics of mesozooplankton biomass over a sub-Arctic continental shelf.

Mesozooplankton research in high latitude ecosystems tends to focus on different life stages of Calanus spp. due to its biomass dominance and trophic roles. However, a complex seasonal succession of abundant smaller mesozooplankton taxa suggests that the ecological functioning of the mesozooplankton communities is more complicated. We studied the year-round taxon-specific biomass measurements and size distributions of mesozooplankton on a sub-Arctic continental shelf based on formalin preserved samples. Our results confirm that Calanus spp. dominate the mesozooplankton biomass (81%). We show that commonly used length-weight relationships underestimate Calanus biomass in autumn and winter, and accordingly, a strong seasonal bias was introduced in our understanding of sub-Arctic plankton communities. We observed two periods with considerable contribution of meroplankton, the planktonic larvae of benthic invertebrates, to the mesozooplankton biomass: (a) Cirripedia nauplii accounted for 17% of total biomass close to the coast in early April and (b) meroplankton comprised up to 12.7% of total biomass in late July. Based on these results, we suggest that meroplankton may play an ecologically important role in addition to their role in dispersal of benthic species. We conclude that the seasonal succession of the biomass of small-sized holoplankton and meroplankton, often obscured by patterns in the Calanus biomass, should receive more attention as these smaller individuals are likely an important functional component of the pelagic food web.

Climate change effects on marine protected areas: Projected decline of benthic species in the North Sea.

Climate change is a global threat for marine ecosystems, their biodiversity and consequently ecosystem services. In the marine realm, marine protected areas (MPAs) were designated to counteract regional pressures, but they might be ineffective to protect vulnerable species and habitats, if their distribution is affected by global climate change. We used six Species Distribution Models (GLM, MARS, FDA, RF, GBM, MAXENT) to project changes in the distribution of eight benthic indicator and key species under climate change in the North Sea MPAs for 2050 and 2099. The projected distribution area of most species will be stable or even increase within the MPAs between 2001 and 2050. Thereafter, the distribution area decreased, especially within MPAs in the central North Sea by 2099, and some key species even disappeared from the MPAs. Consequently, the monitoring and protection of benthic species might not be possible within static MPA borders under climate change.

Seasonal variability of benthic indices: an approach to test the applicability of different indices for ecosystem quality assessment.

In recent studies, several benthic biological indices were developed or used to assess the ecological quality status of marine environments. In the present study the seasonal variability of several univariate and multimetric indices was studied on a monthly scale (September 2000 until May 2002) in different areas of the North Sea such as the German Bight, the Oyster Ground and the Dogger Bank. The stations were chosen to reflect a gradient in the hydrographic regime, temperature and organic matter supply. The seasonal variability was highest for the univariate indices such as the Shannon-Wiener Index and the Hurlbert Index. Thus, due to sensitivity to recruitment the corresponding ecological status ranged from 'good' to 'poor' depending on the season. For the multimetric indices such as the AMBI or the BQI the seasonal variability and the corresponding ecological status were low. The results are discussed concerning possible consequences for ecological quality assessment especially related to the Water Framework Directive (WFD).

Effects of aquaculture fallowing on the recovery of macrofauna communities.

The fallowing period is a management measure in aquaculture where the production is paused for a few months to reduce the impact on the benthic environment. We studied the effects of different fallowing periods on the recovery of macrofauna at two salmon farms in Norway. The macrofauna at the farm stations were characterised by high abundances of opportunistic taxa (e.g. Capitella spp.), low diversity and significantly different community structure compared to reference sites. The fallowing initiated macrofauna recovery at both farm stations, indicated by a decline of dominant opportunistic taxa after 2months. Significant changes in taxa composition occurred only after 6months, although indications of disturbance were still evident. Surprisingly, no corresponding spatial or temporal differences were found in the sediment parameters such as redox, TOC and pH. The results suggest that macrofauna is a more sensitive indicator and that the seasonal timing of fallowing may affect recovery dynamics.

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

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

A bioturbation classification of European marine infaunal invertebrates.

Bioturbation, the biogenic modification of sediments through particle reworking and burrow ventilation, is a key mediator of many important geochemical processes in marine systems. In situ quantification of bioturbation can be achieved in a myriad of ways, requiring expert knowledge, technology, and resources not always available, and not feasible in some settings. Where dedicated research programmes do not exist, a practical alternative is the adoption of a trait-based approach to estimate community bioturbation potential (BPc). This index can be calculated from inventories of species, abundance and biomass data (routinely available for many systems), and a functional classification of organism traits associated with sediment mixing (less available). Presently, however, there is no agreed standard categorization for the reworking mode and mobility of benthic species. Based on information from the literature and expert opinion, we provide a functional classification for 1033 benthic invertebrate species from the northwest European continental shelf, as a tool to enable the standardized calculation of BPc in the region. Future uses of this classification table will increase the comparability and utility of large-scale assessments of ecosystem processes and functioning influenced by bioturbation (e.g., to support legislation). The key strengths, assumptions, and limitations of BPc as a metric are critically reviewed, offering guidelines for its calculation and application.

Influence of macrofauna long-term natural variability on benthic indices used in ecological quality assessment.

An essential prerequisite for the assessment of the ecological quality of marine ecosystems is the understanding of the natural variability and its effect on the performance of quality indices. This study is focused on the long-term natural variability of diversity, biotic and multimetric indices by using long-term macrofauna data of a coastal area in the southern North Sea (1978-2005). The univariate and most biotic and multimetric indices respond significantly on specific natural disturbance events such as cold winters, but the strength of response varied between indices as well as between events. As a result, the ecological quality status can decrease over a range of 3 (out of 5) classification units. The overall ecological quality was good to high, but an increase of indices occurred from the mid 1980s onwards due to changes in the climate regime. This long-term variability has to be considered within ecological quality assessment schemes.