Temporal and spatial drivers of the structure of macroinvertebrate assemblages associated with Laminaria hyperborea detritus in the northeast Atlantic.

Kelp forests occur on more than a quarter of the world's coastlines, serving as foundation species supporting high levels of biodiversity. They are also a major source of organic matter in coastal ecosystems, with the majority of primary production released and exported as detritus. Kelp detritus also provides food and shelter for macroinvertebrates, which comprise important components of inshore food-webs. Hitherto, research on kelp detritus-associated macroinvertebrate assemblages remains relatively limited. We quantified spatiotemporal variability in the structure of detritus-associated macroinvertebrate assemblages within Laminaria hyperborea forests and evaluated the influence of putative drivers of the observed variability in assemblages across eight study sites within four regions of the United Kingdom in May and September 2015. We documented 5167 individuals from 106 taxa with Malacostraca, Gastropoda, Isopoda and Bivalvia the most abundant groups sampled. Assemblage structure varied across months, sites, and regions, with highest richness in September compared to May. Many taxa were unique to individual regions, with few documented in all regions. Finally, key drivers of assemblage structure included detritus tissue nitrogen content, depth, sea surface temperature, light intensity, as well as L. hyperborea canopy density and canopy biomass. Despite their dynamic composition and transient existence, accumulations of L. hyperborea detritus represent valuable repositories of biodiversity and represent an additional kelp forest component which influences secondary productivity, and potentially kelp forest food-web dynamics.

Impacts of Climate Change on Marine Foundation Species.

Marine foundation species are the biotic basis for many of the world's coastal ecosystems, providing structural habitat, food, and protection for myriad plants and animals as well as many ecosystem services. However, climate change poses a significant threat to foundation species and the ecosystems they support. We review the impacts of climate change on common marine foundation species, including corals, kelps, seagrasses, salt marsh plants, mangroves, and bivalves. It is evident that marine foundation species have already been severely impacted by several climate change drivers, often through interactive effects with other human stressors, such as pollution, overfishing, and coastal development. Despite considerable variation in geographical, environmental, and ecological contexts, direct and indirect effects of gradual warming and subsequent heatwaves have emerged as the most pervasive drivers of observed impact and potent threat across all marine foundation species, but effects from sea level rise, ocean acidification, and increased storminess are expected to increase. Documented impacts include changes in the genetic structures, physiology, abundance, and distribution of the foundation species themselves and changes to their interactions with other species, with flow-on effects to associated communities, biodiversity, and ecosystem functioning. We discuss strategies to support marine foundation species into the Anthropocene, in order to increase their resilience and ensure the persistence of the ecosystem services they provide.

Marine heatwave duration and intensity interact to reduce physiological tipping points of kelp species with contrasting thermal affinities.

BACKGROUND AND AIMS: Marine heatwaves (MHWs) are widely-recognised as pervasive drivers of ecosystem change, yet our understanding of how different MHW properties mediate ecological responses remains largely unexplored. Understanding MHW impacts on foundation species is particularly important, given their structural role in communities and ecosystems. METHODS: We simulated a series of realistic MHWs with different levels of intensity (Control: 14°C, Moderate: 18°C, and Extreme: 22°C) and duration (14 or 28 days) and examined responses of two habitat-forming kelp species in southwest United Kingdom (UK). Here, Laminaria digitata reaches its trailing edge and is undergoing a range contraction, whereas L. ochroleuca reaches its leading edge and is undergoing a range expansion. KEY RESULTS: For both species, sub-lethal stress responses induced by moderate intensity MHWs were exacerbated by longer duration. Extreme intensity MHWs caused dramatic declines in growth and photosynthetic performance, and elevated bleaching, which were again exacerbated by longer MHW duration. Stress responses were most pronounced in L. ochroleuca, where almost complete tissue necrosis was observed by the end of the long duration MHW. This was unexpected due to the greater thermal safety margins assumed with leading edge populations. It is likely that prolonged exposure to sub-lethal thermal stress exceeded a physiological tipping point for L. ochroleuca, presumably due to depletion of internal reserves. CONCLUSIONS: Overall, our study showed that exposure to MHW profiles projected to occur the region in the coming decades can have significant deleterious effects on foundation kelp species, regardless of their thermal affinities and location within respective latitudinal ranges, which would likely have consequences for entire communities and ecosystems.

Spatiotemporal variability in population demography and morphology of the habitat-forming macroalga Saccorhiza polyschides in the Western English Channel.

BACKGROUND AND AIMS: Large brown macroalgae serve as foundation organisms along temperate and polar coastlines, providing a range of ecosystem services. Saccorhiza polyschides is a warm-temperate kelp-like species found in the northeast Atlantic, which is suggested to have proliferated in recent decades across the southern United Kingdom (UK), possibly in response to increasing temperatures, physical disturbance, and reduced competition. However, little is known about S. polyschides with regard to ecological functioning and population dynamics across its geographical range. Here we examined the population demography of S. polyschides populations in southwest UK, located within the species' range centre, to address a regional knowledge gap and to provide a baseline against which to detect future changes. METHODS: Intertidal surveys were conducted during spring low tides at three sites along a gradient of wave exposure in Plymouth Sound (Western English Channel) over a period of 15 months. Density, cover, age, biomass, and morphology of S. polyschides were quantified. Additionally, less frequent sampling of shallow subtidal reefs was conducted to compare intertidal and subtidal populations. KEY RESULTS: We recorded pronounced seasonality, with fairly consistent demographic patterns across sites and depths. By late summer, S. polyschides was a dominant habitat-former on both intertidal and subtidal reefs, with maximum standing stock exceeding 13,000 g wet weight m-2. CONCLUSIONS: S. polyschides is a conspicuous and abundant member of rocky reef assemblages in the region, providing complex and abundant biogenic habitat for associated organisms and high rates of primary productivity. However, its short-lived pseudo-annual life strategy is in stark contrast to dominant long-lived perennial Laminarian kelps. As such, any replacement or reconfiguration of habitat-forming macroalgae due to ocean warming will likely have implications for local biodiversity and community composition. More broadly, our study demonstrates the importance of high-resolution cross-habitat surveys to generate robust baselines of kelp population demography, against which the ecological impacts of climate change and other stressors can be reliably detected.

Seasonal development of a tidal mixing front drives shifts in community structure and diversity of bacterioplankton.

Bacterioplankton underpin biogeochemical cycles and an improved understanding of the patterns and drivers of variability in their distribution is needed to determine their wider functioning and importance. Sharp environmental gradients and dispersal barriers associated with ocean fronts are emerging as key determinants of bacterioplankton biodiversity patterns. We examined how the development of the Celtic Sea Front (CF), a tidal mixing front on the Northwest European Shelf affects bacterioplankton communities. We performed 16S-rRNA metabarcoding on 60 seawater samples collected from three depths (surface, 20 m and seafloor), across two research cruises (May and September 2018), encompassing the intra-annual range of the CF intensity. Communities above the thermocline of stratified frontal waters were clearly differentiated and less diverse than those below the thermocline and communities in the well-mixed waters of the Irish Sea. This effect was much more pronounced in September, when the CF was at its peak intensity. The stratified zone likely represents a stressful environment for bacterioplankton due to a combination of high temperatures and low nutrients, which fewer taxa can tolerate. Much of the observed variation was driven by Synechococcus spp. (cyanobacteria), which were more abundant within the stratified zone and are known to thrive in warm oligotrophic waters. Synechococcus spp. are key contributors to global primary productivity and carbon cycling and, as such, variability driven by the CF is likely to influence regional biogeochemical processes. However, further studies are required to explicitly link shifts in community structure to function and quantify their wider importance to pelagic ecosystems.

Multiscale Spatial Variability and Stability in the Structure and Diversity of Bacterial Communities Associated with the Kelp Eisenia cokeri in Peru.

Ecological communities are structured by a range of processes that operate over a range of spatial scales. While our understanding of such biodiversity patterns in macro-communities is well studied, our understanding at the microbial level is still lacking. Bacteria can be free living or associated with host eukaryotes, forming part of a wider "microbiome," which is fundamental for host performance and health. For habitat forming foundation-species, host-bacteria relationships likely play disproportionate roles in mediating processes for the wider ecosystem. Here, we describe host-bacteria communities across multiple spatial scales (i.e., from 10s of m to 100s of km) in the understudied kelp, Eisenia cokeri, in Peru. We found that E. cokeri supports a distinct bacterial community compared to the surrounding seawater, but the structure of these communities varied markedly at the regional (~480 km), site (1-10 km), and individual (10s of m) scale. The marked regional-scale differences we observed may be driven by a range of processes, including temperature, upwelling intensity, or regional connectivity patterns. However, despite this variability, we observed consistency in the form of a persistent core community at the genus level. Here, the genera Arenicella, Blastopirellula, Granulosicoccus, and Litorimonas were found in >80% of samples and comprised ~53% of total sample abundance. These genera have been documented within bacterial communities associated with kelps and other seaweed species from around the world and may be important for host function and wider ecosystem health in general.

Seasonal and spatial variability in rates of primary production and detritus release by intertidal stands of Laminaria digitata and Saccharina latissima on wave-exposed shores in the northeast Atlantic.

Coastal habitats are increasingly recognized as fundamentally important components of global carbon cycles, but the rates of carbon flow associated with marine macrophytes are not well resolved for many species in many regions. We quantified density, rates of primary productivity, and detritus production of intertidal stands of two common intertidal kelp species-Laminaria digitata (oarweed) and Saccharina latissima (sugar kelp)-on four NE Atlantic rocky shores over 22 months. The density of L. digitata was greater at exposed compared to moderately exposed shores but remained consistently low for S. latissima throughout the survey period. Individual productivity and erosion rates of L. digitata did not differ between exposed and moderately exposed shores but differed across exposure levels throughout the year at moderately exposed sites only. Productivity and erosion of S. latissima remained low on moderately exposed shores and showed no clear seasonal pattern. Patterns of productivity and total detrital production (erosion and dislodgement) per m2 of both L. digitata and S. latissima followed closely that of densities per m2, peaking in May during both survey years. Temperature and light were key factors affecting the productivity rates of L. digitata and S. latissima. Erosion rates of L. digitata were affected by wave exposure, temperature, light, grazing, and epiphyte cover, but only temperature-affected erosion of S. latissima. Production of biomass and detritus was greater in L. digitata than in S. latissima and exceeded previous estimates for subtidal and warmer-water affinity kelp populations (e.g., Laminaria ochroleuca). These biogenic habitats are clearly important contributors to the coastal carbon cycle that have been overlooked previously and should be included in future ecosystem models. Further work is required to determine the areal extent of kelp stands in intertidal and shallow subtidal habitats, which is needed to scale up local production estimates to entire coastlines.

Marine heatwaves and decreased light availability interact to erode the ecophysiological performance of habitat-forming kelp species.

Coastal marine ecosystems are threatened by a range of anthropogenic stressors, operating at global, local, and temporal scales. We investigated the impact of marine heatwaves (MHWs) combined with decreased light availability over two seasons on the ecophysiological responses of three kelp species (Laminaria digitata, L. hyperborea, and L. ochroleuca). These species function as important habitat-forming foundation organisms in the northeast Atlantic and have distinct but overlapping latitudinal distributions and thermal niches. Under low-light conditions, summertime MHWs induced significant declines in biomass, blade surface area, and Fv/Fm values (a measure of photosynthetic efficiency) in the cool-water kelps L. digitata and L. hyperborea, albeit to varying degrees. Under high-light conditions, all species were largely resistant to simulated MHW activity. In springtime, MHWs had minimal impacts and in some cases promoted kelp performance, while reduced light availability resulted in lower growth rates. While some species were negatively affected by summer MHWs under low-light conditions (particularly L. digitata), they were generally resilient to MHWs under high-light conditions. As such, maintaining good environmental quality and water clarity may increase resilience of populations to summertime MHWs. Our study informs predictions of how habitat-forming foundation kelp species will be affected by interacting, concurrent stressors, typical of compound events that are intensifying under anthropogenic climate change.

Development and Diversity of Epibiont Assemblages on Cultivated Sugar Kelp (Saccharina latissima) in Relation to Farming Schedules and Harvesting Techniques.

Seaweed farming in Europe is growing and may provide environmental benefits, including habitat provisioning, coastal protection, and bioremediation. Habitat provisioning by seaweed farms remains largely unquantified, with previous research focused primarily on the detrimental effects of epibionts, rather than their roles in ecological functioning and ecosystem service provision. We monitored the development and diversity of epibiont assemblages on cultivated sugar kelp (Saccharina latissima) at a farm in Cornwall, southwest UK, and compared the effects of different harvesting techniques on epibiont assemblage structure. Increases in epibiont abundance (PERMANOVA, F4,25 = 100.56, p < 0.001) and diversity (PERMANOVA, F4,25 = 27.25, p < 0.001) were found on cultivated kelps over and beyond the growing season, reaching an average abundance of >6000 individuals per kelp plant with a taxonomic richness of ~9 phyla per kelp by late summer (August). Assemblages were dominated by crustaceans (mainly amphipods), molluscs (principally bivalves) and bryozoans, which provide important ecological roles, despite reducing crop quality. Partial harvesting techniques maintained, or increased, epibiont abundance and diversity beyond the farming season; however, these kelp plants were significantly fouled and would not be commercially viable in most markets. This paper improves understanding of epibiont assemblage development at European kelp farms, which can inform sustainable, ecosystem-based approaches to aquaculture.

Consistency and Variation in the Kelp Microbiota: Patterns of Bacterial Community Structure Across Spatial Scales.

Kelp species are distributed along ~ 25% of the world's coastlines and the forests they form represent some of the world's most productive and diverse ecosystems. Like other marine habitat-formers, the associated microbial community is fundamental for host and, in turn, wider ecosystem functioning. Given there are thousands of bacteria-host associations, determining which relationships are important remains a major challenge. We characterised the associated bacteria of two habitat-forming kelp species, Laminaria hyperborea and Saccharina latissima, from eight sites across a range of spatial scales (10 s of metres to 100 s of km) in the northeast Atlantic. We found no difference in diversity or community structure between the two kelps, but there was evidence of regional structuring (across 100 s km) and considerable variation between individuals (10 s of metres). Within sites, individuals shared few amplicon sequence variants (ASVs) and supported a very small proportion of diversity found across the wider study area. However, consistent characteristics between individuals were observed with individual host communities containing a small conserved "core" (8-11 ASVs comprising 25 and 32% of sample abundances for L. hyperborea and S. latissima, respectively). At a coarser taxonomic resolution, communities were dominated by four classes (Planctomycetes, Gammaproteobacteria, Alphaproteobacteria and Bacteroidia) that made up ~ 84% of sample abundances. Remaining taxa (47 classes) made up very little contribution to overall abundance but the majority of taxonomic diversity. Overall, our study demonstrates the consistent features of kelp bacterial communities across large spatial scales and environmental gradients and provides an ecologically meaningful baseline to track environmental change.

Core Community Persistence Despite Dynamic Spatiotemporal Responses in the Associated Bacterial Communities of Farmed Pacific Oysters.

A breakdown in host-bacteria relationships has been associated with the progression of a number of marine diseases and subsequent mortality events. For the Pacific oyster, Crassostrea gigas, summer mortality syndrome (SMS) is one of the biggest constraints to the growth of the sector and is set to expand into temperate systems as ocean temperatures rise. Currently, a lack of understanding of natural spatiotemporal dynamics of the host-bacteria relationship limits our ability to develop microbially based monitoring approaches. Here, we characterised the associated bacterial community of C. gigas, at two Irish oyster farms, unaffected by SMS, over the course of a year. We found C. gigas harboured spatiotemporally variable bacterial communities that were distinct from bacterioplankton in surrounding seawater. Whilst the majority of bacteria-oyster associations were transient and highly variable, we observed clear patterns of stability in the form of a small core consisting of six persistent amplicon sequence variants (ASVs). This core made up a disproportionately large contribution to sample abundance (34 ± 0.14%), despite representing only 0.034% of species richness across the study, and has been associated with healthy oysters in other systems. Overall, our study demonstrates the consistent features of oyster bacterial communities across spatial and temporal scales and provides an ecologically meaningful baseline to track environmental change.

Biological Impacts of Marine Heatwaves.

Climatic extremes are becoming increasingly common against a background trend of global warming. In the oceans, marine heatwaves (MHWs)-discrete periods of anomalously warm water-have intensified and become more frequent over the past century, impacting the integrity of marine ecosystems globally. We review and synthesize current understanding of MHW impacts at the individual, population, and community levels. We then examine how these impacts affect broader ecosystem services and discuss the current state of research on biological impacts of MHWs. Finally, we explore current and emergent approaches to predicting the occurrence andimpacts of future events, along with adaptation and management approaches. With further increases in intensity and frequency projected for coming decades, MHWs are emerging as pervasive stressors to marine ecosystems globally. A deeper mechanistic understanding of their biological impacts is needed to better predict and adapt to increased MHW activity in the Anthropocene.

Identifying and protecting macroalgae detritus sinks toward climate change mitigation.

Harnessing natural solutions to mitigate climate change requires an understanding of carbon fixation, flux, and sequestration across ocean habitats. Recent studies have suggested that exported seaweed particulate organic carbon is stored within soft-sediment systems. However, very little is known about how seaweed detritus disperses from coastlines, or where it may enter seabed carbon stores, where it could become the target of conservation efforts. Here, focusing on regionally dominant seaweed species, we surveyed environmental DNA (eDNA) from natural coastal sediments, and studied their connectivity to seaweed habitats using a particle tracking model parameterized to reproduce seaweed detritus dispersal behavior based on laboratory observations of seaweed fragment degradation and sinking. Experiments showed that seaweed detritus density changed over time, differently across species. This, in turn, modified distances traveled by released fragments until they reached the seabed for the first time, during model simulations. Dispersal pathways connected detritus from the shore to the open ocean but, importantly, also to coastal sediments, and this was reflected by field eDNA evidence. Dispersion pathways were also affected by hydrodynamic conditions, varying in space and time. Both the properties and timing of released detritus, individual to each macroalgal population, and short-term near-seabed and medium-term water-column transport pathways, are thus seemingly important in determining the connectivity between seaweed habitats and potential sedimentary sinks. Studies such as this one, supported by further field verification of sedimentary carbon sequestration rates and source partitioning, are still needed to help quantify the role of seaweed in the ocean carbon cycle. Such studies will provide vital evidence to inform on the potential need to develop blue carbon conservation mechanisms, beyond wetlands.

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.

Kelp carbon sink potential decreases with warming due to accelerating decomposition.

Cycling of organic carbon in the ocean has the potential to mitigate or exacerbate global climate change, but major questions remain about the environmental controls on organic carbon flux in the coastal zone. Here, we used a field experiment distributed across 28° of latitude, and the entire range of 2 dominant kelp species in the northern hemisphere, to measure decomposition rates of kelp detritus on the seafloor in relation to local environmental factors. Detritus decomposition in both species were strongly related to ocean temperature and initial carbon content, with higher rates of biomass loss at lower latitudes with warmer temperatures. Our experiment showed slow overall decomposition and turnover of kelp detritus and modeling of coastal residence times at our study sites revealed that a significant portion of this production can remain intact long enough to reach deep marine sinks. The results suggest that decomposition of these kelp species could accelerate with ocean warming and that low-latitude kelp forests could experience the greatest increase in remineralization with a 9% to 42% reduced potential for transport to long-term ocean sinks under short-term (RCP4.5) and long-term (RCP8.5) warming scenarios. However, slow decomposition at high latitudes, where kelp abundance is predicted to expand, indicates potential for increasing kelp-carbon sinks in cooler (northern) regions. Our findings reveal an important latitudinal gradient in coastal ecosystem function that provides an improved capacity to predict the implications of ocean warming on carbon cycling. Broad-scale patterns in organic carbon decomposition revealed here can be used to identify hotspots of carbon sequestration potential and resolve relationships between carbon cycling processes and ocean climate at a global scale.

Heterogeneity within and among co-occurring foundation species increases biodiversity.

Habitat heterogeneity is considered a primary causal driver underpinning patterns of diversity, yet the universal role of heterogeneity in structuring biodiversity is unclear due to a lack of coordinated experiments testing its effects across geographic scales and habitat types. Furthermore, key species interactions that can enhance heterogeneity, such as facilitation cascades of foundation species, have been largely overlooked in general biodiversity models. Here, we performed 22 geographically distributed experiments in different ecosystems and biogeographical regions to assess the extent to which variation in biodiversity is explained by three axes of habitat heterogeneity: the amount of habitat, its morphological complexity, and capacity to provide ecological resources (e.g. food) within and between co-occurring foundation species. We show that positive and additive effects across the three axes of heterogeneity are common, providing a compelling mechanistic insight into the universal importance of habitat heterogeneity in promoting biodiversity via cascades of facilitative interactions. Because many aspects of habitat heterogeneity can be controlled through restoration and management interventions, our findings are directly relevant to biodiversity conservation.

The influence of light and temperature on detritus degradation rates for kelp species with contrasting thermal affinities.

Kelp detritus fuels coastal food webs and may play an important role as a source of organic matter for natural carbon sequestration. Here, we conducted ex situ and in situ manipulations to evaluate the role of temperature and light availability in the breakdown of detrital material. We examined degradation rates of two North Atlantic species with contrasting thermal affinities: the 'warm water' kelp Laminaria ochroleuca and the 'cool water' Laminaria hyperborea. Detrital fragments were exposed to different temperatures in controlled conditions and across an in situ gradient of depth, corresponding to light availability. Overall, degradation rates (i.e. changes in Fv/Fm and biomass) were faster under lower light conditions and at higher temperatures, although responses were highly variable between plants and fragments. Crucially, as L. ochroleuca degraded faster than L. hyperborea under some conditions, a climate-driven substitution of the 'cool' for the 'warm' kelp, which has been observed at some locations, will likely increase detritus turnover rates and alter detrital pathways in certain environments. More importantly, ocean warming combined with decreased coastal water quality will likely accelerate kelp detritus decomposition, with potential implications for coastal food webs and carbon cycles.

Socioeconomic impacts of marine heatwaves: Global issues and opportunities.

Extreme climatic events, including marine heatwaves (MHWs), are altering ecosystems globally, often with profound socioeconomic impacts. We examine how MHWs have affected the provision of ecosystem services and evaluate the socioeconomic consequences for human society. Ecological impacts range from harmful algal blooms and mass mortality events to reconfigurations of entire ecosystems, affecting provisioning, habitat, regulating, and cultural ecosystem services globally. Reported economic costs of individual MHW events exceed US$800 million in direct losses or >US$3.1 billion in indirect losses of ecosystem services for multiple years. However, biological responses to MHWs can also increase human-ocean interactions, providing opportunities for coastal societies. Our study provides a global perspective on the far-reaching impacts of MHWs on human societies and highlights the urgent need to develop robust approaches to mitigation and adaptation.