Open-sea cultivation by transplanting young fronds of the kelp Saccharina latissima

Saccharina latissima is an economically and ecologically important native kelp. As its limited supply from wild stock cannot meet increasing current and future demands, methods for its cultivation in the ocean need to be developed. This kelp is now beginning to be farmed off the Atlantic coast of Spain using a regular method similar to the “forced cultivation” technique used with Asian kelps (kombu). Its cultivation is also a growing enterprise in other European countries. In this study, the open-sea farming of S. latissima using the transplanting method is tested on a commercial scale. This cultivation method has not been studied with kelp species outside Asian waters. The tested method includes the following steps: indoor production of seedlings, pre-culture in greenhouse tanks, and open-sea cultivation by transplanting young fronds. Results demonstrate that open-sea cultivation using transplanted young fronds is a technically and biologically viable method. The mean yield obtained (7.8 kg fresh wt per meter rope equivalent to 45.6 t fresh wt per hectare farm) is satisfactory, considering the low densities of transplanted fronds (25–30 fronds per meter rope). Moreover, these values are comparable to those reported in previous cultivations with this species, as well as in the farming of similar kelps. The transplanting method used in conjunction with the regular cultivation method has valuable practical applications for the commercial farming of S. latissima.     

Modelling seasonal growth and composition of the kelp Saccharina latissima

A dynamical model for simulating growth of the brown macroalga Saccharina latissima is described. In addition to wet and dry weights, the model simulates carbon and nitrogen reserves, with variable C/N ratio. In effect, the model can be used to emulate seasonal changes in growth and composition of the alga. Simulation results based on published, environmental field data are presented and compared with corresponding data on growth and composition. The model resolves seasonal growth, carbon and nitrogen content well, and may contribute to the understanding of how seasonal growth in S. latissima depends simultaneously on a combination of several environmental factors: light, nutrients, temperature and water motion. The model is applied to aquaculture problems such as estimating the nutrient scavenging potential of S. latissima and estimating the potential of this kelp species as a raw material for bioenergy production.     

Skinny kelp (Saccharina angustissima) provides valuable genetics for the biomass improvement of farmed sugar kelp (Saccharina latissima)

Saccharina latissima (sugar kelp) is one of the most widely cultivated brown marine macroalgae species in the North Atlantic and the eastern North Pacific Oceans. To meet the expanding demands of the sugar kelp mariculture industry, selecting and breeding sugar kelp that is best suited to offshore farm environments is becoming necessary. To that end, a multi-year, multi-institutional breeding program was established by the U.S. Department of Energy's (DOE) Advanced Research Projects Agency-Energy (ARPA-E) Macroalgae Research Inspiring Novel Energy Resources (MARINER) program. Hybrid sporophytes were generated using 203 unique gametophyte cultures derived from wild-collected Saccharina spp. for two seasons of farm trials (2019–2020 and 2020–2021). The wild sporophytes were collected from 10 different locations within the Gulf of Maine (USA) region, including both sugar kelp (Saccharina latissima) and the skinny kelp species (Saccharina angustissima). We harvested 232 common farm plots during these two seasons with available data. We found that farmed kelp plots with skinny kelp as parents had an average increased yield over the mean (wet weight 2.48?±?0.90 kg m^?1 and dry weight 0.32?±?0.10 kg m^?1) in both growing seasons. We also found that blade length positively correlated with biomass in skinny kelp x sugar kelp crosses or pure sugar kelp crosses. The skinny x sugar progenies had significantly longer and narrower blades than the pure sugar kelp progenies in both seasons. Overall, these findings suggest that sugar x skinny kelp crosses provide improved yield compared to pure sugar kelp crosses.

     

In a squeeze: Epibiosis may affect the distribution of kelp forests

The processes limiting the population recovery of the kelp Saccharina latissima after recent large‐scale loss from the south coast of Norway are poorly understood. Previous investigations do, however, suggest that the impacts of biotic interactions (epibiosis and competition) and increased water turbidity are important. We investigated the depth‐related patterns of growth, epibiosis, and mortality in two sample populations of kelp, from the south and the southwest coast of Norway. The investigations were performed over a period of seven months, in a crossed translocational study, where kelps were mounted on rigs at six depths (1, 3, 6, 9, 15, and 24 m). In a second experiment, the amounts of light blocked by different epibiont layers growing on the kelp frond were investigated. While growth decreased with depth in spring and summer, the kelp grew faster at 15 m than at shallower depths in fall. Survival was low both in shallow water and below 15 m depth. Epibionts covered the kelp growing at depths from 1 to 9 m, and the laboratory study showed that the coverage may have deprived the individuals of as much as 90% of the available light. Although the depth‐related results we present apply—in the strictest sense—only to kelp translocated on rigs, we argue that the relative patterns are relevant for natural populations. Growth and survival of S. latissima is likely to be reduced by heavy loads of epibionts, while depths where epibionts are sparse may be close to the lower limit of the kelps depth distribution along the south coast of Norway. This suggests that a vertical squeeze, or narrowing of the distribution range of kelp forests may be occurring in Norway.     

Patterns of Saccharina latissima Recruitment

The lack of recovery in Norwegian populations of the kelp Saccharina latissima (Linnaeus) C. E. Lane, C. Mayes, Druehl & G. W. Saunders after a large-scale disturbance that occurred sometime between the late 1990s and early 2000s has raised considerable concerns. Kelp forests are areas of high production that serve as habitats for numerous species, and their continued absence may represent the loss of an entire ecosystem. Some S. latissima populations remain as scattered patches within the affected areas, but today, most of the areas are completely devoid of kelp. The question is if natural recolonization by kelp and the reestablishment of the associated ecosystem is possible. Previous studies indicate that a high degree of reproductive synchrony in macrophytes has a positive effect on their potential for dispersal and on the connectivity between populations, but little is known about the patterns of recruitment in Norwegian S. latissima. More is, however, known about the development of fertile tissue (sori) on adult individuals, which is easily observed. The present study investigated the degree of coupling between the appearance of sori and the recruitment on clean artificial substrate beneath adult specimens. The pattern of recruitment was linked to the retreat of visible sori (i.e. spore release) and a seasonal component unrelated to the fertility of the adults. The formation and the retreat of visible sori are processes that seem synchronized along the south coast of Norway, and the link between sori development and recruitment may therefore suggest that the potential for S. latissima dispersal is relatively large. These results support the notion that the production and dispersal of viable spores is unlikely to be the bottleneck preventing recolonization in the south of Norway, but studies over larger temporal and spatial scales are still needed to confirm this hypothesis.     

Biomass yield and morphological features of the seaweed Saccharina latissima cultivated at two different sites in a coastal bay in the Atlantic coast of Spain

The kelp Saccharina latissima is an economically important edible seaweed with great potential for use in other applications. The goal of this study was to identify locations in a coastal bay with better conditions for commercial cultivation of this species. We compared the biomass yield and morphological features of S. latissima cultivated at two locations in a bay of Galicia (northwest Spain): in an external moderately exposed site and in an internal sheltered site. Biomass yield was significantly higher at the moderately exposed site than at the sheltered site (16 fresh kg vs. 12 fresh kg per linear meter of rope). Fronds were significantly larger at the moderately exposed site compared to that at the sheltered site. However, the “substantiality value” (around 40 mg cm^?2), which is an index used to assess blade quality for human consumption, did not differ significantly between the two locations. The effect of light exposure and water velocity seemed to be the most important environmental factors that explain the differences in the results obtained at both culture sites. In summary, both the moderately exposed site and the sheltered site were suitable for cultivation of S. latissima, as indicated by the high yields and similar blade quality obtained at both locations.     

Successional dynamics of the cultivated kelp microbiome

Kelp are important primary producers that are colonized by diverse microbes that can have both positive and negative effects on their hosts. The kelp microbiome could support the burgeoning kelp cultivation sector by improving host growth, stress tolerance, and resistance to disease. Fundamental questions about the cultivated kelp microbiome still need to be addressed before microbiome-based approaches can be developed. A critical knowledge gap is how cultivated kelp microbiomes change as hosts grow, particularly following outplanting to sites that vary in abiotic conditions and microbial source pools. In this study we assessed if microbes that colonize kelp in the nursery stage persist after outplanting. We characterized microbiome succession over time on two species of kelp, Alaria marginata and Saccharina latissima, outplanted to open ocean cultivation sites in multiple geographic locations. We tested for host-species specificity of the microbiome and the effect of different abiotic conditions and microbial source pools on kelp microbiome stability during the cultivation process. We found the microbiome of kelp in the nursery is distinct from that of outplanted kelp. Few bacteria persisted on kelp following outplanting. Instead, we identified significant microbiome differences correlated with host species and microbial source pools at each cultivation site. Microbiome variation related to sampling month also indicates that seasonality in host and/or abiotic factors may influence temporal succession and microbiome turnover in cultivated kelps. This study provides a baseline understanding of microbiome dynamics during kelp cultivation and highlights research needs for applying microbiome manipulation to kelp cultivation.     

Comparing salinity tolerance in early stages of the sporophytes of a non-indigenous kelp (Undaria pinnatifida) and a native kelp (Saccharina latissima)

The short-term effects of low salinities on the survival of germlings of an introduced kelp Undaria pinnatifida and a native kelp Saccharina latissima were assessed under laboratory conditions. This experiment was designed to compare the differential stress tolerance to salinity of the early life history stages of sporophytes of these two kelps that co-occur on European Atlantic coasts. Germlings (young sporophytes) of both species were exposed for 4 days to salinities ranging from 31 (control) to 26, 21, 16, 11, and 6 psu. Afterwards, they were post-cultured in control seawater (31 psu) for another 4 days to corroborate the viability of injured germlings. Results showed that germlings of the introduced kelp were less resistant to low salinity, surviving to as low as 16 psu; whereas the germlings of the native kelp survived in salinities as low as 11 psu. Despite the observed differences, both species are relatively tolerant to low salinity. Our observations also indicated that, at least in a short term, gametophytes of both species were able to survive in salinities as low as 6 psu. The significance of low-salinity tolerance to the distribution of these kelps and for their offshore cultivation is discussed.     

Offshore cultivation methods affects blade features of the edible seaweed <Emphasis Type="Italic">Saccharina latissima</Emphasis> in a bay of Galicia,Northwest Spain

Variation in blade morphology of Saccharina latissima may be of importance for its commercial cultivation. Blade features were compared between offshore cultivation on horizontal ropes versus hanging ropes during its reproduction period (early autumn and early spring of the following year). Cultivation experiments were conducted in February 2002 in a sheltered coastal area of a bay of Galicia (Northwest Spain). Significant differences were found between methods in blade area, which in turn affected blade biomass. However, the differences were only significant during the reproduction period in early spring. The cultivation method also significantly affected the “substantiality value”, which is an index that expresses the blade quality for human consumption. The observed variations in morphological features of S. latissima blades likely were caused by the different hydrodynamics of the two cultivation methods.     

The challenge of estimating kelp production in a turbid marine environment

Coastal kelp forests produce substantial marine carbon due to high annual net primary production (NPP) rates, but upscaling of NPP estimates over time and space remains difficult. We investigated the impact of variable underwater photosynthetically active radiation (PAR) and photosynthetic parameters on photosynthetic oxygen production of Laminaria hyperborea, the dominant NE-Atlantic kelp species, throughout summer 2014. Collection depth of kelp had no effect on chlorophyll a content, pointing to a high photoacclimation potential of L. hyperborea towards incident light. However, chlorophyll a and photosynthesis versus irradiance parameters differed significantly along the blade gradient when normalized to fresh mass, potentially introducing large uncertainties in NPP upscaling to whole thalli. Therefore, we recommend a normalization to kelp tissue area, which is stable over the blade gradient. Continuous PAR measurements revealed a highly variable underwater light climate at our study site (Helgoland, North Sea) in summer 2014, reflected by PAR attenuation coefficients (K_d) between 0.28 and 0.87 m⁻¹. Our data highlight the importance of continuous underwater light measurements or representative average values using a weighted K_d to account for large PAR variability in NPP calculations. Strong winds in August increased turbidity, resulting in a negative carbon balance at depths >3–4 m over several weeks, considerably impacting kelp productivity. Estimated daily summer NPP over all four depths was 1.48 ± 0.97 g C · m⁻² seafloor · d⁻¹ for the Helgolandic kelp forest, which is in the range of other kelp forests along European coastlines.     

Assimilation of inorganic nutrients from salmon (Salmo salar) farming by the macroalgae (Saccharina latissima) in an exposed coastal environment: implications for integrated multi-trophic aquaculture

This paper investigated the assimilation of dissolved inorganic nitrogen (DIN) in Saccharina latissima in proximity to salmon cages in coastal waters. The bioassays were performed on plants from three stations located in the vicinity of a salmon farm (Salmo salar) in exposed waters at Tristein (63° 52′ N, 9° 37′ E) in Central Norway. The growth, the C and N content, and the nitrogen isotope ratios (δ¹⁵N) of S. latissima were monitored over 1 year. The DIN concentrations in seawater were higher at the salmon farm stations than at the reference station during the winter, and the N/P ratio at the salmon farm stations was higher from September to January and in June. S. latissima at the salmon farm stations grew faster than at the reference station. The length of S. latissima increased by 50 % when integrated with the salmon farm compared to the reference station. The N content of S. latissima was positively correlated to the DIN concentration in seawater (p?<?0.05), but the increased N supply from salmon did not result in N accumulation in S. latissima at the salmon farm station because of the dilution by a higher growth rate. The δ¹⁵N in S. latissima was higher at the salmon farm station from April to June and changed in the direction of the δ¹⁵N signature in urine. This indicated that N in S. latissima at the salmon farm station partly originated from the salmon. One hectare of S. latissima may absorb 0.8～1.2 t N during one growth season. Large-scale cultivation of S. latissima should be considered to mitigate the environmental effects of DIN wastes from salmon farms.     

qPCR-based relative quantification of the brown algal endophyte <Emphasis Type="Italic">Laminarionema elsbetiae</Emphasis> in <Emphasis Type="Italic">Saccharina latissima</Emphasis>: variation and dynamics of host—endophyte interactions

Morphological changes—such as dark spots, twisted stipes and deformed blades—have been observed in wild and cultivated Saccharina latissima. The putative cause for the disease symptoms is the filamentous endophytic brown alga Laminarionema elsbetiae, which is known to invade stipes and fronds of its hosts. Little is known about this interaction and its occurrence in the field, although former studies indicated high endophyte prevalence in kelp populations. Previous epidemiological studies on kelp endophytes were mainly based on the examination of microscopic sections, followed by time-consuming isolation and cultivation steps in order to identify the endophyte and a reliable method to quantify endophyte infections was missing. As a novel approach, we established and validated a qPCR assay for relative quantification of the endophyte L. elsbetiae within its host S. latissima, which allows to examine both, the prevalence of endophytic algae and the severity of infections. The assay was shown to be highly specific and suitable to reliably detect small amounts of endophyte DNA in the host. Using this method, we detected very high endophyte prevalence in the investigated kelp populations, up to 100% in young S. latissima sporophytes in Brittany during spring. Furthermore, our results suggest that Saccharina sporophytes are infected early in their life and that seasonality and environmental factors have a significant impact on infection rates. In the future, this approach could also be applied to study other host-endophyte pairs using specific primers.     

Sugar kelp (Saccharina latissima) inhibits hepatic inflammation and fibrosis in a mouse model of diet-induced nonalcoholic steatohepatitis

Nonalcoholic steatohepatitis (NASH), closely associated with obesity, is a health concern worldwide. We investigated whether the consumption of U.S.-grown sugar kelp (Saccharina latissima), an edible brown alga, can prevent obesity-associated metabolic disturbances and NASH in a mouse model of diet-induced NASH. Male C57BL/6J mice were fed a low-fat diet, a high-fat/high-sucrose/high-cholesterol diet (HF), or a HF diet containing sugar kelp (HF-Kelp) for 14 weeks. HF-Kelp group showed lower body weight with increased O₂ consumption, CO₂ production, physical activity, and energy expenditure compared with the HF. In the liver, there were significant decreases in weight, triglycerides, total cholesterol, and steatosis with HF-Kelp. The HF-Kelp group decreased hepatic expression of a macrophage marker adhesion G protein-coupled receptor E1 (Adgre1) and an M1 macrophage marker integrin alpha x (Itgax). HF-Kelp group also exhibited decreased liver fibrosis, as evidenced by less expression of fibrogenic genes and collagen accumulation than those of HF group. In epididymal white adipose tissue (eWAT), HF-Kelp group exhibited decreases in eWAT weight and adipocyte size compared with those of the HF. HF-Kelp group showed decreased expression of collagen type VI alpha 1 chain, Adgre1, Itgax, and tumor necrosis factor α in eWAT. We demonstrated, for the first time, that the consumption of U.S-grown sugar kelp prevented the development of obesity and its associated metabolic disturbances, steatosis, inflammation, and fibrosis in the liver and eWAT of a diet-induced NASH mouse model.     

Bacterial diversity in relation to secondary production and succession on surfaces of the kelp Laminaria hyperborea

Kelp forests worldwide are known as hotspots for macroscopic biodiversity and primary production, yet very little is known about the biodiversity and roles of microorganisms in these ecosystems. Secondary production by heterotrophic bacteria associated to kelp is important in the food web as a link between kelp primary production and kelp forest consumers. The aim of this study was to investigate the relationship between bacterial diversity and two important processes in this ecosystem; bacterial secondary production and primary succession on kelp surfaces. To address this, kelp, Laminaria hyperborea, from southwestern Norway was sampled at different geographical locations and during an annual cycle. Pyrosequencing (454-sequencing) of amplicons of the 16S rRNA gene of bacteria was used to study bacterial diversity. Incorporation of tritiated thymidine was used as a measure of bacterial production. Our data show that bacterial diversity (richness and evenness) increases with the age of the kelp surface, which corresponds to the primary succession of its bacterial communities. Higher evenness of bacterial operational taxonomical units (OTUs) is linked to higher bacterial production. Owing to the dominance of a few abundant OTUs, kelp surface biofilm communities may be characterized as low-diversity habitats. This is the first detailed study of kelp-associated bacterial communities using high-throughput sequencing and it extends current knowledge on microbial community assembly and dynamics on living surfaces.     

Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales,Phaeophyceae)

Kelps, seaweeds and seagrasses provide important ecosystem services in coastal areas, and loss of these macrophytes is a global concern. Recent surveys have documented severe declines in populations of the dominant kelp species, Saccharina latissima, along the south coast of Norway. S. latissima is a cold‐temperate species, and increasing seawater temperature has been suggested as one of the major causes of the decline. Several studies have shown that S. latissima can acclimate to a wide range of temperatures. However, local adaptations may render the extrapolation of existing results inappropriate. We investigated the potential for thermal acclimation and heat tolerance in S. latissima collected from three locations along the south coast of Norway. Plants were kept in laboratory cultures at three different growth temperatures (10, 15, and 20°C) for 4–6 weeks, after which their photosynthetic performance, fluorescence parameters, and pigment concentrations were measured. S. latissima obtained almost identical photosynthetic characteristics when grown at 10 and 15°C, indicating thermal acclimation at these temperatures. In contrast, plants grown at 20°C suffered substantial tissue deterioration, and showed reduced net photosynthetic capacity caused by a combination of elevated respiration and reduced gross photosynthesis due to lowered pigment concentrations, altered pigment composition, and reduced functionality of Photo‐system II. Our results support the hypothesis that extraordinarily high temperatures, as observed in 1997, 2002, and 2006, may have initiated the declines in S. latissima populations along the south coast of Norway. However, observations of high mortality in years with low summer temperatures suggest that reduced population resilience or other factors may have contributed to the losses.     

Planctomycetes dominate biofilms on surfaces of the kelp <Emphasis Type="Italic">Laminaria hyperborea</Emphasis>

Background  

Bacteria belonging to Planctomycetes display several unique morphological and genetic features and are found in a wide variety of habitats on earth. Their ecological roles in these habitats are still poorly understood. Planctomycetes have previously been detected throughout the year on surfaces of the kelp Laminaria hyperborea from southwestern Norway. We aimed to make a detailed investigation of the abundance and phylogenetic diversity of planctomycetes inhabiting these kelp surfaces.     

Habitat characteristics can influence fish assemblages in high latitude kelp forests

Kelp forests are patchy fish-associated habitats, which can vary greatly in their size, foundation species, and several physical habitat attributes. The structure of fish assemblages can vary with these characteristics and with the location of the assemblage within the forest, i.e. edges versus interiors. This study quantified the biological and physical heterogeneity within different sized kelp forests and identified which factors are important in structuring the associated fish assemblages. Fish and habitat surveys were conducted at the edge and interiors of ten kelp forests of varying sizes in Kachemak Bay, south-central Alaska. Fish assemblage structure was not correlated with the species composition of surface canopy forming foundation kelps (Nereocystis leutkeana and Eualaria fistulosa) or with kelp forest size. Instead, it correlated with the abundances of two understory foundation kelps (Agarum clathratum and Saccharina latissima), substratum rugosity, and water depth. Together these benthic attributes explained 53.6 % of the fish assemblage variability. Additionally, significantly different fish assemblages were found at edge compared to interior locations with the relative abundance of seven species (Artedius fenestralis, Ammodytes hexapterus, Blepsias cirrhosis, Gadus macrocephalus, Hexagrammos stelleri, Pholis laeta, and Sebastes melanops) explaining 91.4 % of the variability. This study highlights the importance of habitat characteristics such as understory foundation species, substratum rugosity, water depth and location within a patch on the variability of fish assemblages in high latitude kelp forests.     

Allocation of blade surface to reproduction in Laminaria longicruris of Long Island Sound (USA)

Sorus formation in the kelp Laminaria longicruris de la Pylaie (Phaeophyta) was quantified for a biennial population in Long Island Sound (Connecticut, USA), at the southern limit of its biogeographical range in the Western Atlantic Ocean. The allocation of blade surface to reproduction was measured monthly during two years, with additional samples taken at times of peak growth and reproduction. Sporophytes produced sori year-round, with the highest percentages of fertile plants (75 to 95 percent) occurring from October to December. The mean percentage of sorus area to blade ranged from 1 to 37 percent, remaining low and fairly constant during the spring and summer, but reaching much higher levels in the fall (when growth is minimal) and early winter. The comparatively low mean annual allocation of blade surface to reproduction (5 percent), was postulated to be due to temperature stress on these plants at the southern limit of distribution, but may instead be typical of the species. Such a small allocation of resources to reproduction nevertheless results in billions of spores per m² of substrate, making a major contribution of material potentially available to grazing food webs.     

Status,trends and drivers of kelp forests in Europe: an expert assessment

A comprehensive expert consultation was conducted in order to assess the status, trends and the most important drivers of change in the abundance and geographical distribution of kelp forests in European waters. This consultation included an on-line questionnaire, results from a workshop and data provided by a selected group of experts working on kelp forest mapping and eco-evolutionary research. Differences in status and trends according to geographical areas, species identity and small-scale variations within the same habitat where shown by assembling and mapping kelp distribution and trend data. Significant data gaps for some geographical regions, like the Mediterranean and the southern Iberian Peninsula, were also identified. The data used for this study confirmed a general trend with decreasing abundance of some native kelp species at their southern distributional range limits and increasing abundance in other parts of their distribution (Saccharina latissima and Saccorhiza polyschides). The expansion of the introduced species Undaria pinnatifida was also registered. Drivers of observed changes in kelp forests distribution and abundance were assessed using experts’ opinions. Multiple possible drivers were identified, including global warming, sea urchin grazing, harvesting, pollution and fishing pressure, and their impact varied between geographical areas. Overall, the results highlight major threats for these ecosystems but also opportunities for conservation. Major requirements to ensure adequate protection of coastal kelp ecosystems along European coastlines are discussed, based on the local to regional gaps detected in the study.