Christoffer Boström

North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L.

As the most widespread seagrass in temperate waters of the Northern Hemisphere, Zostera marina provides a unique opportunity to investigate the extent to which the historical legacy of the last glacial maximum (LGM18 000–10 000 years bp) is detectable in modern population genetic structure. We used sequences from the nuclear rDNA–internal transcribed spacer (ITS) and chloroplast matK‐intron, and nine microsatellite loci to survey 49 populations (> 2000 individuals) from throughout the species’ range. Minimal sequence variation between Pacific and Atlantic populations combined with biogeographical groupings derived from the microsatellite data, suggest that the trans‐Arctic connection is currently open. The east Pacific and west Atlantic are more connected than either is to the east Atlantic. Allelic richness was almost two‐fold higher in the Pacific. Populations from putative Atlantic refugia now represent the southern edges of the distribution and are not genetically diverse. Unexpectedly, the highest allelic diversity was observed in the North Sea–Wadden Sea–southwest Baltic region. Except for the Mediterranean and Black Seas, significant isolation‐by‐distance was found from ~150 to 5000 km. A transition from weak to strong isolation‐by‐distance occurred at ~150 km among northern European populations suggesting this scale as the natural limit for dispersal within the metapopulation. Links between historical and contemporary processes are discussed in terms of the projected effects of climate change on coastal marine plants. The identification of a high genetic diversity hotspot in Northern Europe provides a basis for restoration decisions.

Community structure and spatial variation of benthic invertebrates associated with Zostera marina (L.) beds in the northern Baltic Sea

Abstract The distribution and bed structure of eelgrass ( Zostera marina L.), and its importance for associated faunal communities in the coastal areas of the northern Baltic Sea are poorly known. The spatial distribution of the fauna associated with Zostera was studied at five localities in SW Finland in 1993–1994. Zostera was common on all localities, but the beds varied in terms of area (1–5 m diameter), density (50–500 shoots/m 2 ) and blade length (20–110 cm). A total of about 40 species or taxa were recorded. The zoobenthic infauna showed significant spatial differences, and total abundance and species diversity were significantly higher in the Zostera beds than in adjacent bare sand. The total abundance in Zostera ranged from 25 000 to 50 000 ind/m 2 and in sand from 2500 to 15 000 ind/m 2 The mean number of species in Zostera ranged from 5.9 to 8.8 spp ( H ′ = 1.76–2.54) and in sand from 2.2 to 5.5 spp ( H ′ = 1.67–2.31). The epifauna in Zostera was numerically dominated by grazing gastropods (Hydrobiidae) and copepods. The epifauna is an important community component, which contributes to the total diversity of the Zostera assemblage. These systems are among the most species-rich components of the shallow soft-bottom ecosystems in the northern Baltic Sea. The mechanisms structuring both the Zostera and the ambient sand-bottom habitats are presented.

The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea

Seagrasses colonized the sea on at least three independent occasions to form the basis of one of the most productive and widespread coastal ecosystems on the planet. Here we report the genome of Zostera marina (L.), the first, to our knowledge, marine angiosperm to be fully sequenced. This reveals unique insights into the genomic losses and gains involved in achieving the structural and physiological adaptations required for its marine lifestyle, arguably the most severe habitat shift ever accomplished by flowering plants. Key angiosperm innovations that were lost include the entire repertoire of stomatal genes, genes involved in the synthesis of terpenoids and ethylene signalling, and genes for ultraviolet protection and phytochromes for far-red sensing. Seagrasses have also regained functions enabling them to adjust to full salinity. Their cell walls contain all of the polysaccharides typical of land plants, but also contain polyanionic, low-methylated pectins and sulfated galactans, a feature shared with the cell walls of all macroalgae and that is important for ion homoeostasis, nutrient uptake and O2/CO2 exchange through leaf epidermal cells. The Z. marina genome resource will markedly advance a wide range of functional ecological studies from adaptation of marine ecosystems under climate warming, to unravelling the mechanisms of osmoregulation under high salinities that may further inform our understanding of the evolution of salt tolerance in crop plants.

The relative importance of food and shelter for seagrass-associated invertebrates: a latitudinal comparison of habitat choice by isopod grazers

Abstract The generality of mechanisms affecting habitat choice and grazing in seagrass meadows was evaluated in a latitudinal comparison of seagrass grazers from the temperate (60°N) Baltic Sea and the subtropical (30°N) Gulf of Mexico. Using similar habitat choice experiment set-ups in Finland and the USA, the role of food type, habitat complexity and predation hazard on habitat choice of the isopods Idotea baltica (Pallas) and Erichsonella attenuata Harger were tested. When shelter was provided by both living and artificial seagrass, epiphytic food resources on artificial vegetation were clearly preferred by both species, although Idotea was attracted to epiphyte-free seagrass when no alternative food was present. When choosing between food and shelter, both species preferred epiphytic food over shelter. However, under predation hazard of fish, Erichsonella clearly switched to the habitat offering shelter, while the presence of a predatory fish produced no preference for shelter by Idotea. Food type may be considered as an universal mechanism that partly determines the presence of grazers in seagrass habitats and is, in the absence of a predator, more important than shelter. Predation risk affected the behaviour of the grazers, but the response varied between species possibly due to varying importance of fish predation in the areas studied.

Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative‐experimental approach

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Distribution, structure and function of Nordic eelgrass (Zostera marina) ecosystems: implications for coastal management and conservation

This paper focuses on the marine foundation eelgrass species, Zostera marina, along a gradient from the northern Baltic Sea to the north-east Atlantic. This vast region supports a minimum of 1480 km2 eelgrass (maximum >2100 km2), which corresponds to more than four times the previously quantified area of eelgrass in Western Europe. Eelgrass meadows in the low salinity Baltic Sea support the highest diversity (4–6 spp.) of angiosperms overall, but eelgrass productivity is low (<2 g dw m-2 d-1) and meadows are isolated and genetically impoverished. Higher salinity areas support monospecific meadows, with higher productivity (3–10 g dw m-2 d-1) and greater genetic connectivity. The salinity gradient further imposes functional differences in biodiversity and food webs, in particular a decline in number, but increase in biomass of mesograzers in the Baltic. Significant declines in eelgrass depth limits and areal cover are documented, particularly in regions experiencing high human pressure. The failure of eelgrass to re-establish itself in affected areas, despite nutrient reductions and improved water quality, signals complex recovery trajectories and calls for much greater conservation effort to protect existing meadows. The knowledge base for Nordic eelgrass meadows is broad and sufficient to establish monitoring objectives across nine national borders. Nevertheless, ensuring awareness of their vulnerability remains challenging. Given the areal extent of Nordic eelgrass systems and the ecosystem services they provide, it is crucial to further develop incentives for protecting them.

Distribution, structure and function of Nordic eelgrass (Zostera marina) ecosystems

This paper focuses on the marine foundation eelgrass species, Zostera marina, along a gradient from the northern Baltic Sea to the north-east Atlantic. This vast region supports a minimum of 1480 km2 eelgrass (maximum >2100 km2), which corresponds to more than four times the previously quantified area of eelgrass in Western Europe. Eelgrass meadows in the low salinity Baltic Sea support the highest diversity (4–6 spp.) of angiosperms overall, but eelgrass productivity is low (<2 g dw m-2 d-1) and meadows are isolated and genetically impoverished. Higher salinity areas support monospecific meadows, with higher productivity (3–10 g dw m-2 d-1) and greater genetic connectivity. The salinity gradient further imposes functional differences in biodiversity and food webs, in particular a decline in number, but increase in biomass of mesograzers in the Baltic. Significant declines in eelgrass depth limits and areal cover are documented, particularly in regions experiencing high human pressure. The failure of eelgrass to re-establish itself in affected areas, despite nutrient reductions and improved water quality, signals complex recovery trajectories and calls for much greater conservation effort to protect existing meadows. The knowledge base for Nordic eelgrass meadows is broad and sufficient to establish monitoring objectives across nine national borders. Nevertheless, ensuring awareness of their vulnerability remains challenging. Given the areal extent of Nordic eelgrass systems and the ecosystem services they provide, it is crucial to further develop incentives for protecting them.

Infauna fromZostera marina L. meadows in Norway. Differences in vegetated and unvegetated areas

Abstract To investigate the importance of benthic vegetation for shallow infaunal assemblages, macroinvertebrates were sampled inZostera marina meadows and in adjacent bare sand at three sites in the Skagerrak region and one in the Western part of Norway. A total of 3777 individuals were encountered, representing mainly the faunal groups Annelida, Nemertea, Echinodermata, Crustacea and Mollusca. Twice as many individuals were found in theZ. marina meadows compared to the bare sand. Oligochaetes were the most abundant group (29% of total number of individuals), followed by crustaceans (24%), polychaetes (18.5%) and molluscs (16%). Polychaetes showed the highest species number (42), followed by molluscs (30) and crustaceans (26). Multivariate cluster technique showed the highest similarities within sites and thereafter grouping according to the two different habitats;Zostera and sand. No regional differences were evident between the Skagerrak sites and the site in Western Norway, as the site from Western Norway grouped together with one of the Skagerrak sites. The high biodiversity inZostera marina beds should have implications for the management of such areas.

The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems - a review

Seagrass meadows are vital ecosystems in coastal zones worldwide, but are also under global threat. One of the major hurdles restricting the success of seagrass conservation and restoration is our limited understanding of ecological feedback mechanisms. In these ecosystems, multiple, self‐reinforcing feedbacks can undermine conservation efforts by masking environmental impacts until the decline is precipitous, or alternatively they can inhibit seagrass recovery in spite of restoration efforts. However, no clear framework yet exists for identifying or dealing with feedbacks to improve the management of seagrass ecosystems. Here we review the causes and consequences of multiple feedbacks between seagrass and biotic and/or abiotic processes. We demonstrate how feedbacks have the potential to impose or reinforce regimes of either seagrass dominance or unvegetated substrate, and how the strength and importance of these feedbacks vary across environmental gradients. Although a myriad of feedbacks have now been identified, the co‐occurrence and likely interaction among feedbacks has largely been overlooked to date due to difficulties in analysis and detection. Here we take a fundamental step forward by modelling the interactions among two distinct above‐ and belowground feedbacks to demonstrate that interacting feedbacks are likely to be important for ecosystem resilience. On this basis, we propose a five‐step adaptive management plan to address feedback dynamics for effective conservation and restoration strategies. The management plan provides guidance to aid in the identification and prioritisation of likely feedbacks in different seagrass ecosystems.

Widespread genetic mosaicism in the marine angiosperm Zostera marina is correlated with clonal reproduction

Somatic mutations are an underappreciated source of genetic variation within multi-cellular organisms. The resulting genetic mosaicism should be particularly abundant in large clones of vegetatively propagating angiosperms. Little is known on the abundance and ecological correlates of genetic mosaicism in field populations, despite its potential evolutionary significance. Because sexual reproduction restores genetic homogeneity, we predicted that in facultatively clonally reproducing organisms, the prevalence of genetic mosaicism increases with increasing clonality. This was tested among 33 coastal locations colonized by the ecologically important marine angiosperm Zostera marina, ranging from Portugal to Finland. Genetic mosaics were detectable as complex microsatellite genotypes at two hypervariable loci that revealed additional mosaic alleles, suggesting the presence of one or more divergent cell lineages within the same ramet. The proportions of non-mosaic genotypes in a population sharply decreased below a clonal richness of 0.2. Accordingly, more genetic mosaics were found at the southern and northern limit of the distribution of Z. marina in Europe where sexual reproduction is rare or absent. The genetic mosaics observed at neutral microsatellite markers suggest the possibility of within-clone variation at selectively relevant loci and supports the notion that members of clones are seldom genetically identical.