Seafloor primary production in a changing Arctic Ocean.

Phytoplankton and sea ice algae are traditionally considered to be the main primary producers in the Arctic Ocean. In this Perspective, we explore the importance of benthic primary producers (BPPs) encompassing microalgae, macroalgae, and seagrasses, which represent a poorly quantified source of Arctic marine primary production. Despite scarce observations, models predict that BPPs are widespread, colonizing ~3 million km2 of the extensive Arctic coastal and shelf seas. Using a synthesis of published data and a novel model, we estimate that BPPs currently contribute ~77 Tg C y-1 of primary production to the Arctic, equivalent to ~20 to 35% of annual phytoplankton production. Macroalgae contribute ~43 Tg C y-1, seagrasses contribute ~23 Tg C y-1, and microalgae-dominated shelf habitats contribute ~11 to 16 Tg C y-1. Since 2003, the Arctic seafloor area exposed to sunlight has increased by ~47,000 km2 y-1, expanding the realm of BPPs in a warming Arctic. Increased macrophyte abundance and productivity is expected along Arctic coastlines with continued ocean warming and sea ice loss. However, microalgal benthic primary production has increased in only a few shelf regions despite substantial sea ice loss over the past 20 y, as higher solar irradiance in the ice-free ocean is counterbalanced by reduced water transparency. This suggests complex impacts of climate change on Arctic light availability and marine primary production. Despite significant knowledge gaps on Arctic BPPs, their widespread presence and obvious contribution to coastal and shelf ecosystem production call for further investigation and for their inclusion in Arctic ecosystem models and carbon budgets.

Environmental drivers of Arctic communities based on metabarcoding of marine sediment eDNA.

Our ability to assess biodiversity at relevant spatial and temporal scales for informing management is of increasing importance given this is foundational to identify and mitigate the impacts of global change. Collecting baseline information and tracking ecological changes are particularly important for areas experiencing rapid changes and representing data gaps such as Arctic marine ecosystems. Environmental DNA has the potential to provide such data. We extracted environmental DNA from 90 surface sediment samples to assess eukaryote diversity around Greenland and Svalbard using two separate primer pairs amplifying different sections of the 18S rRNA gene. We detected 27 different phyla and 99 different orders and found that temperature and the change in temperature explained the most variation in the community in a single linear model, while latitude, sea ice cover and change in temperature explained the most variation in the community when assessed by individual non-linear models. We identified potential indicator taxa for Arctic climate change, including a terebellid annelid worm. In conclusion, our study demonstrates that environmental DNA offers a feasible method to assess biodiversity and identifies warming as a key driver of differences in biodiversity across these remote ecosystems.

Global dataset of soil organic carbon in tidal marshes.

Tidal marshes store large amounts of organic carbon in their soils. Field data quantifying soil organic carbon (SOC) stocks provide an important resource for researchers, natural resource managers, and policy-makers working towards the protection, restoration, and valuation of these ecosystems. We collated a global dataset of tidal marsh soil organic carbon (MarSOC) from 99 studies that includes location, soil depth, site name, dry bulk density, SOC, and/or soil organic matter (SOM). The MarSOC dataset includes 17,454 data points from 2,329 unique locations, and 29 countries. We generated a general transfer function for the conversion of SOM to SOC. Using this data we estimated a median (± median absolute deviation) value of 79.2 ± 38.1 Mg SOC ha-1 in the top 30 cm and 231 ± 134 Mg SOC ha-1 in the top 1 m of tidal marsh soils globally. This data can serve as a basis for future work, and may contribute to incorporation of tidal marsh ecosystems into climate change mitigation and adaptation strategies and policies.

Prevalent fingerprint of marine macroalgae in arctic surface sediments.

Macroalgal forests export much of their production, partly supporting food webs and carbon stocks beyond their habitat, but evidence of their contribution in sediment carbon stocks is poor. We test the hypothesis that macroalgae contribute to carbon stocks in arctic marine sediments. We used environmental DNA (eDNA) fingerprinting on a large-scale set of surface sediment samples from Greenland and Svalbard. We evaluated eDNA results by comparing with traditional survey and tracer methods. The eDNA-based survey identified macroalgae in 94 % of the sediment samples covering shallow nearshore areas to 1460 m depth and 350 km offshore, with highest sequence abundance nearshore and with dominance of brown macroalgae. Overall, the eDNA results reflected the potential source communities of macroalgae and eelgrass assessed by traditional surveys, with the most abundant orders being common among different methods. A stable isotope analysis showed a considerable contribution from macroalgae in sediments although with high uncertainty, highlighting eDNA as a great improvement and supplement for documenting macroalgae as a contributor to sediment carbon stocks. Conclusively, we provide evidence for a prevalent contribution of macroalgal forests in arctic surface sediments, nearshore as well as offshore, identifying brown algae as main contributors.

Potential role of seaweeds in climate change mitigation.

Seaweed (macroalgae) has attracted attention globally given its potential for climate change mitigation. A topical and contentious question is: Can seaweeds' contribution to climate change mitigation be enhanced at globally meaningful scales? Here, we provide an overview of the pressing research needs surrounding the potential role of seaweed in climate change mitigation and current scientific consensus via eight key research challenges. There are four categories where seaweed has been suggested to be used for climate change mitigation: 1) protecting and restoring wild seaweed forests with potential climate change mitigation co-benefits; 2) expanding sustainable nearshore seaweed aquaculture with potential climate change mitigation co-benefits; 3) offsetting industrial CO2 emissions using seaweed products for emission abatement; and 4) sinking seaweed into the deep sea to sequester CO2. Uncertainties remain about quantification of the net impact of carbon export from seaweed restoration and seaweed farming sites on atmospheric CO2. Evidence suggests that nearshore seaweed farming contributes to carbon storage in sediments below farm sites, but how scalable is this process? Products from seaweed aquaculture, such as the livestock methane-reducing seaweed Asparagopsis or low carbon food resources show promise for climate change mitigation, yet the carbon footprint and emission abatement potential remains unquantified for most seaweed products. Similarly, purposely cultivating then sinking seaweed biomass in the open ocean raises ecological concerns and the climate change mitigation potential of this concept is poorly constrained. Improving the tracing of seaweed carbon export to ocean sinks is a critical step in seaweed carbon accounting. Despite carbon accounting uncertainties, seaweed provides many other ecosystem services that justify conservation and restoration and the uptake of seaweed aquaculture will contribute to the United Nations Sustainable Development Goals. However, we caution that verified seaweed carbon accounting and associated sustainability thresholds are needed before large-scale investment into climate change mitigation from seaweed projects.

Macroalgal habitats support a sustained flux of floating biomass but limited carbon export beyond a Greenland fjord.

Despite growing attention on the contribution of macroalgae to carbon cycling and sequestration (blue carbon), more observational data is needed to constrain current estimates. In this study, we estimate the floating macroalgal carbon flux within and beyond a large sub-Arctic fjord system, Nuup Kangerlua, Greenland, which could potentially reach carbon sinks. Our study estimates 1) the fjord-scale area with macroalgal coverage and barrens caused by sea urchin grazing, 2) the floating macroalgal biomass in the fjord, and 3) the annual export flux of floating macroalgae out of the fjord system. ROV surveys documented that macroalgal habitats cover 32 % of the seafloor within the photic zone (0-30 m) with an average coverage of 39.6, 22, and 7.2 % in the depth intervals 0-10, 10-20, and 20-30 m, respectively. 15 % of the area suitable for macroalgae was denuded by sea urchin grazing. Floating macroalgae were common with an average biomass of 55 kg wet weight km-2. Densities and species composition varied seasonally with the highest levels after storms. The floating biomass was composed of intertidal macroalgal species (58 %) (Fucus vesiculosus, Fucus distichus, and Ascophyllum nodosum) and kelps (42 %) (Saccharina longicruris, S. latissima, and Alaria esculenta). We deployed surface GPS drifters to simulate floating macroalgal trajectories and velocity. Data indicated that 80 % of the floating biomass is retained in the fjord where its fate in relation to long-term sequestration is unknown. Export beyond the fjord was limited and indicated an annual floating macroalgal export beyond the fjord of only 6.92 t C yr-1, which is equal to ~0.02 % of the annual net primary production. Our findings suggest that floating macroalgae support a limited blue carbon potential beyond this fjord and that future research should focus on the fate of retained floating macroalgae and subsurface export to resolve the connectivity between macroalgal habitats and long-term carbon sinks.

Mapping intertidal macrophytes in fjords in Southwest Greenland using Sentinel-2 imagery.

Changes in the distribution of coastal macrophytes in Greenland, and elsewhere in the Arctic are difficult to quantify as the region remains challenging to access and monitor. Satellite imagery, in particular Sentinel-2 (S2), may enable large-scale monitoring of coastal areas in Greenland but its use is impacted by the optically complex environments and the scarcity of supporting data in the region. Additionally, the canopies of the dominant macrophyte species in Greenland do not extend to the sea surface, limiting the use of indices that exploit the reflection of near-infrared radiation by vegetation due to its absorption by seawater. Three hypotheses are tested: I) 10-m S2 imagery and commonly used detection methods can identify intertidal macrophytes that are exposed at low tide in an optically complex fjord system in Greenland impacted by marine and land terminating glaciers; II) detached and floating macrophytes accumulate in patches that are sufficiently large to be detected by 10-m S2 images; III) iceberg scour and/or turbid meltwater runoff shape the spatial distribution of intertidal macroalgae in fjord systems with marine-terminating glaciers. The NDVI produced the best results in optically complex fjord systems in Greenland. 12 km2 of exposed intertidal macrophytes were identified in the study area at low tide. Floating mats of macrophytes ranged in area from 400 m2 to 326,800 m2 and were most common at the mouth of the fjord. Icebergs and turbidity appear to play a role in structuring the distribution of intertidal macrophytes and the retreat of marine terminating glaciers could allow macrophytes cover to expand. The challenges and solutions presented here apply to most fjords in Greenland and, therefore, the methodology may be extended to produce a Greenland-wide estimate of intertidal macrophytes.

Whole genome population structure of North Atlantic kelp confirms high-latitude glacial refugia.

Coastal refugia during the Last Glacial Maximum (~21,000 years ago) have been hypothesized at high latitudes in the North Atlantic, suggesting marine populations persisted through cycles of glaciation and are potentially adapted to local environments. Here, whole-genome sequencing was used to test whether North Atlantic marine coastal populations of the kelp Alaria esculenta survived in the area of southwestern Greenland during the Last Glacial Maximum. We present the first annotated genome for A. esculenta and call variant positions in 54 individuals from populations in Atlantic Canada, Greenland, Faroe Islands, Norway and Ireland. Differentiation across populations was reflected in ~1.9 million single nucleotide polymorphisms, which further revealed mixed ancestry in the Faroe Islands individuals between putative Greenlandic and European lineages. Time-calibrated organellar phylogenies suggested Greenlandic populations were established during the last interglacial period more than 100,000 years ago, and that the Faroe Islands population was probably established following the Last Glacial Maximum. Patterns in population statistics, including nucleotide diversity, minor allele frequencies, heterozygosity and linkage disequilibrium decay, nonetheless suggested glaciation reduced Canadian Atlantic and Greenlandic populations to small effective sizes during the most recent glaciation. Functional differentiation was further reflected in exon read coverage, which revealed expansions unique to Greenland in 337 exons representing 162 genes, and a modest degree of exon loss (103 exons from 56 genes). Altogether, our genomic results provide strong evidence that A. esculenta populations were resilient to past climatic fluctuations related to glaciations and that high-latitude populations are potentially already adapted to local conditions as a result.

Global seaweed productivity.

The magnitude and distribution of net primary production (NPP) in the coastal ocean remains poorly constrained, particularly for shallow marine vegetation. Here, using a compilation of in situ annual NPP measurements across >400 sites in 72 geographic ecoregions, we provide global predictions of the productivity of seaweed habitats, which form the largest vegetated coastal biome on the planet. We find that seaweed NPP is strongly coupled to climatic variables, peaks at temperate latitudes, and is dominated by forests of large brown seaweeds. Seaweed forests exhibit exceptionally high per-area production rates (a global average of 656 and 1711 gC m-2 year-1 in the subtidal and intertidal, respectively), being up to 10 times higher than coastal phytoplankton in temperate and polar seas. Our results show that seaweed NPP is a strong driver of production in the coastal ocean and call for its integration in the oceanic carbon cycle, where it has traditionally been overlooked.

A network analysis of connected biophysical pathways to advice eelgrass (Zostera marina) restoration.

The North Sea and the Baltic Sea, including Danish coastal waters, have experienced a drastic decline in eelgrass Zostera marina coverage during the past century. Around 1900, eelgrass meadows covered about 6700 km2 of Danish coastal waters while the current potential distribution area is only about one third of this. In some areas, the potential distribution area is far from realized, and restoration efforts are needed to assist recovery. Such efforts are challenging, and resource-demanding and careful site selection is, therefore, important. In the present study, we aim to identify the connectivity of eelgrass populations as a basis for guiding site selection for restoration. We developed a coupled biophysical model to study eelgrass dispersal in the Kattegat. Partly submerged particles simulated the dispersal of reproductive eelgrass shoots containing seeds during the flowering season July-September. We then used network analysis to identify the potential connectivity between populations. We evaluated connectivity based on In-strength, Betweenness and Eigenvector centrality metrics and identified key areas in the Kattegat such as the central part of Aalborg Bay, to be considered to restore the network of Z. marina patches. The study proves the potentials of combining hydrodynamic models and network analysis to support marine conservation and planning, and highlights the importance of collaboration between ecologists, oceanographers, and practitioners in this endeavour.

Whole-genome sequencing reveals forgotten lineages and recurrent hybridizations within the kelp genus Alaria (Phaeophyceae).

The genomic era continues to revolutionize our understanding of the evolution of biodiversity. In phycology, emphasis remains on assembling nuclear and organellar genomes, leaving the full potential of genomic datasets to answer long-standing questions about the evolution of biodiversity largely unexplored. Here, we used whole-genome sequencing (WGS) datasets to survey species diversity in the kelp genus Alaria, compare phylogenetic signals across organellar and nuclear genomes, and specifically test whether phylogenies behave like trees or networks. Genomes were sequenced from across the global distribution of Alaria (including Alaria crassifolia, A. praelonga, A. crispa, A. marginata, and A. esculenta), representing over 550 GB of data and over 2.2 billion paired reads. Genomic datasets retrieved 3,814 and 4,536 single-nucleotide polymorphisms (SNPs) for mitochondrial and chloroplast genomes, respectively, and upwards of 148,542 high-quality nuclear SNPs. WGS revealed an Arctic lineage of Alaria, which we hypothesize represents the synonymized taxon A. grandifolia. The SNP datasets also revealed inconsistent topologies across genomic compartments, and hybridization (i.e., phylogenetic networks) between Pacific A. praelonga, A. crispa, and putative A. grandifolia, and between some lineages of the A. marginata complex. Our analysis demonstrates the potential for WGS data to advance our understanding of evolution and biodiversity beyond amplicon sequencing, and that hybridization is potentially an important mechanism contributing to novel lineages within Alaria. We also emphasize the importance of surveying phylogenetic signals across organellar and nuclear genomes, such that models of mixed ancestry become integrated into our evolutionary and taxonomic understanding.

Century-long records reveal shifting challenges to seagrass recovery.

Global losses over the 20th century placed seagrass ecosystems among the most threatened ecosystems in the world, with eutrophication, and associated deterioration of the submarine light environment identified as the main driver. Growing appreciation of the ecological and societal benefits of healthy seagrass meadows has stimulated efforts to protect and restore them, largely focused on reducing nutrient input to coastal waters. Here we analyze a unique data set spanning 135 years on eelgrass (Zostera marina), the dominant seagrass of the northern hemisphere. We show that meadows in the Western Baltic Sea exhibited major declines relative to historic (1890-1910) reference due to the wasting disease in the 1930s followed by eutrophication peaking in the 1980s, but have only shown modest improvement despite major eutrophication mitigation, halving nitrogen input since the 1980s. Across the past century, we identified generally shallower colonization depths of eelgrass for a given submarine light penetration and, hence, increased apparent light requirements. This suggests that eelgrass recovery is limited by additional stressors. Our study indicates that bottom trawling and intense recent warming (0.5°C per decade, 1985-2018), which impact on deeper and shallower meadows, respectively, suppress eelgrass from fully recovering from eutrophication. Warming is most severe in shallow turbid waters, while clear-water areas offer eelgrass refugia from warming in deeper, cooler waters; but trawling can prevent eelgrass from reaching these refugia. Efforts to reduce nutrient input and thereby improve water clarity have been instrumental in avoiding a catastrophic loss of eelgrass ecosystems. However, local-scale future management must, in addition, reduce bottom trawling to facilitate eelgrass reaching deeper, cooler refugia, and increase resilience toward realized and further warming. Warming needs to be limited by meeting global climate change mitigation goals.

Seagrass fatty acid profiles as a sensitive indicator of climate settings across seasons and latitudes.

Zostera marina is a dominant meadow-forming seagrass in temperate regions in the northern hemisphere. Here, fatty acid content and composition, and pigmentation, in leaves were evaluated across temporal (April, July, November -2015 and January-2016) and latitudinal (Greenland to southern Spain) environmental gradients. Content of total fatty acids (TFA) in samples collected in Ireland during warmer periods (summer) was 2-3 times lower than in winter and exhibited a lower proportion of polyunsaturated fatty acids (PUFAs), which have high high-nutritional value relative to saturated fatty acids (SAFA). The latitudinal comparison (Greenland to southern Spain) revealed a clear reduction in the proportion n-3 PUFAs and an increase in n-6 PUFA and SAFA, which correlated with the rise in temperature towards southern locations, which correlated with the rise in temperature towards south. Results indicate that future warming may negatively affect its lipid nutritional value. These results demonstrate the capacity of seagrasses to adjust their lipid composition to achieve optimal membrane functionality, suggesting the potential use of FA as an eco-physiological indicator of global change conditions. The results also suggest that future warming may negatively affect the lipid nutritional value of seagrasses.

A DNA mini-barcode for marine macrophytes.

Studies focusing on marine macrophyte metabarcoding from environmental samples are scarce, due to the lack of a universal barcode for these taxa, and to their poor representation in DNA databases. Here, we searched for a short barcode able to identify marine macrophytes from tissue samples; then, we created a DNA reference library which was used to identify macrophytes in eDNA from coastal sediments. Barcoding of seagrasses, mangroves and marine macroalgae (Chlorophyta, Rhodophyta and Phaeophyceae) was tested using 18 primer pairs from six barcoding genes: the plant barcodes rbcL, matK and trnL, plus the genes ITS2, COI and 18S. The 18S gene showed the highest universality among marine macrophytes, amplifying 95%-100% of samples; amplification performance of the other barcodes was limited. Taxonomy was assigned using a phylogeny-based approach to create an 18S DNA reference library. Macrophyte tissue sequences were accurately identified within their phyla (88%), order (76%), genus (71%) and species (23%). Nevertheless, out of 86 macrophytes tested, only 48% and 15% had a reference sequence at genus and at species level, respectively. Identification at these levels can be improved by more inclusive reference libraries. Using the 18S mini-barcode and the reference library, we recovered eDNA from 21 marine macrophytes in sediments, demonstrating the barcode's ability to trace primary producers that contribute to blue carbon. We expect this barcode to also be useful for other ecological questions, such as tracing macro primary producers in marine food webs.

Ecological effects of non-native species in marine ecosystems relate to co-occurring anthropogenic pressures.

Predictors for the ecological effects of non-native species are lacking, even though such knowledge is fundamental to manage non-native species and mitigate their impacts. Current theories suggest that the ecological effects of non-native species may be related to other concomitant anthropogenic stressors, but this has not been tested at a global scale. We combine an exhaustive meta-analysis of the ecological effects of marine non-native species with human footprint proxies to determine whether the ecological changes due to non-native species are modulated by co-occurring anthropogenic impacts. We found that non-native species had greater negative effects on native biodiversity where human population was high and caused reductions in individual performance where cumulative human impacts were large. On this basis we identified several marine ecoregions where non-native species may have the greatest ecological effects, including areas in the Mediterranean Sea and along the northwest coast of the United States. In conclusion, our global assessment suggests coexisting anthropogenic impacts can intensify the ecological effects of non-native species.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The future of Blue Carbon science.

The term Blue Carbon (BC) was first coined a decade ago to describe the disproportionately large contribution of coastal vegetated ecosystems to global carbon sequestration. The role of BC in climate change mitigation and adaptation has now reached international prominence. To help prioritise future research, we assembled leading experts in the field to agree upon the top-ten pending questions in BC science. Understanding how climate change affects carbon accumulation in mature BC ecosystems and during their restoration was a high priority. Controversial questions included the role of carbonate and macroalgae in BC cycling, and the degree to which greenhouse gases are released following disturbance of BC ecosystems. Scientists seek improved precision of the extent of BC ecosystems; techniques to determine BC provenance; understanding of the factors that influence sequestration in BC ecosystems, with the corresponding value of BC; and the management actions that are effective in enhancing this value. Overall this overview provides a comprehensive road map for the coming decades on future research in BC science.

Publisher Correction: Global ecological impacts of marine exotic species.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.