A Pleistocene legacy structures variation in modern seagrass ecosystems.

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

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

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

Integrating genetics, biophysical, and demographic insights identifies critical sites for seagrass conservation.

The eelgrass Zostera marina is an important foundation species of coastal areas in the Northern Hemisphere, but is continuing to decline, despite management actions. The development of new management tools is therefore urgent in order to prioritize limited resources for protecting meadows most vulnerable to local extinctions and identifying most valuable present and historic meadows to protect and restore, respectively. We assessed 377 eelgrass meadows along the complex coastlines of two fjord regions on the Swedish west coast-one is currently healthy and the other is substantially degraded. Shoot dispersal for all meadows was assessed with Lagrangian biophysical modeling (scale: 100-1,000 m) and used for barrier analysis and clustering; a subset (n = 22) was also assessed with population genetic methods (20 microsatellites) including diversity, structure, and network connectivity. Both approaches were in very good agreement, resulting in seven subpopulation groupings or management units (MUs). The MUs correspond to a spatial scale appropriate for coastal management of "waterbodies" used in the European Water Framework Directive. Adding demographic modeling based on the genetic and biophysical data as a third approach, we are able to assess past, present, and future metapopulation dynamics to identify especially vulnerable and valuable meadows. In a further application, we show how the biophysical approach, using eigenvalue perturbation theory (EPT) and distribution records from the 1980s, can be used to identify lost meadows where restoration would best benefit the present metapopulation. The combination of methods, presented here as a toolbox, allows the assessment of different temporal and spatial scales at the same time, as well as ranking of specific meadows according to key genetic, demographic and ecological metrics. It could be applied to any species or region, and we exemplify its versatility as a management guide for eelgrass along the Swedish west coast.

Variation of carbon contents in eelgrass ( Zostera marina) sediments implied from depth profiles.

Seagrass meadows are able to store significant amounts of organic carbon in their underlying sediment, but global estimates are uncertain partly owing to spatio-temporal heterogeneity between and within areas and species. In order to provide robust estimates, there is a need to better understand the fate of, and mechanisms behind, organic carbon storage. In this observational study, we analyse a suite of biotic and abiotic parameters in sediment cores from 47 different eelgrass ( Zostera marina) beds spanning the distributional range of the Northern Hemisphere. Depth profiles of particulate organic carbon (POC) revealed three patterns of vertical distribution where POC either increased, decreased or showed no pattern with sediment depth. These categories exhibited distinct profiles of δ13C and C:N ratios, where high POC profiles had a proportionally larger storage of eelgrass-derived material whereas low POC profiles were dominated by phytoplanktonic and macroalgal material. However, high POC did not always translate into high carbon density. Nevertheless, this large-scale dataset provides evidence that the variability in organic matter source in response to natural and anthropogenic environmental changes affects the potential role of eelgrass beds as POC sinks, particularly where eelgrass decline is observed.

Latitude, temperature, and habitat complexity predict predation pressure in eelgrass beds across the Northern Hemisphere.

Latitudinal gradients in species interactions are widely cited as potential causes or consequences of global patterns of biodiversity. However, mechanistic studies documenting changes in interactions across broad geographic ranges are limited. We surveyed predation intensity on common prey (live amphipods and gastropods) in communities of eelgrass (Zostera marina) at 48 sites across its Northern Hemisphere range, encompassing over 37° of latitude and four continental coastlines. Predation on amphipods declined with latitude on all coasts but declined more strongly along western ocean margins where temperature gradients are steeper. Whereas in situ water temperature at the time of the experiments was uncorrelated with predation, mean annual temperature strongly positively predicted predation, suggesting a more complex mechanism than simply increased metabolic activity at the time of predation. This large-scale biogeographic pattern was modified by local habitat characteristics; predation declined with higher shoot density both among and within sites. Predation rates on gastropods, by contrast, were uniformly low and varied little among sites. The high replication and geographic extent of our study not only provides additional evidence to support biogeographic variation in predation intensity, but also insight into the mechanisms that relate temperature and biogeographic gradients in species interactions.

No barrier to emergence of bathyal king crabs on the Antarctic shelf.

Cold-water conditions have excluded durophagous (skeleton-breaking) predators from the Antarctic seafloor for millions of years. Rapidly warming seas off the western Antarctic Peninsula could now facilitate their return to the continental shelf, with profound consequences for the endemic fauna. Among the likely first arrivals are king crabs (Lithodidae), which were discovered recently on the adjacent continental slope. During the austral summer of 2010 ‒ 2011, we used underwater imagery to survey a slope-dwelling population of the lithodid Paralomis birsteini off Marguerite Bay, western Antarctic Peninsula for environmental or trophic impediments to shoreward expansion. The population density averaged ∼ 4.5 individuals × 1,000 m(-2) within a depth range of 1,100 ‒ 1,500 m (overall observed depth range 841-2,266 m). Images of juveniles, discarded molts, and precopulatory behavior, as well as gravid females in a trapping study, suggested a reproductively viable population on the slope. At the time of the survey, there was no thermal barrier to prevent the lithodids from expanding upward and emerging on the outer shelf (400- to 550-m depth); however, near-surface temperatures remained too cold for them to survive in inner-shelf and coastal environments (<200 m). Ambient salinity, composition of the substrate, and the depth distribution of potential predators likewise indicated no barriers to expansion of lithodids onto the outer shelf. Primary food resources for lithodids--echinoderms and mollusks--were abundant on the upper slope (550-800 m) and outer shelf. As sea temperatures continue to rise, lithodids will likely play an increasingly important role in the trophic structure of subtidal communities closer to shore.

Genome architecture enables local adaptation of Atlantic cod despite high connectivity.

Adaptation to local conditions is a fundamental process in evolution; however, mechanisms maintaining local adaptation despite high gene flow are still poorly understood. Marine ecosystems provide a wide array of diverse habitats that frequently promote ecological adaptation even in species characterized by strong levels of gene flow. As one example, populations of the marine fish Atlantic cod (Gadus morhua) are highly connected due to immense dispersal capabilities but nevertheless show local adaptation in several key traits. By combining population genomic analyses based on 12K single nucleotide polymorphisms with larval dispersal patterns inferred using a biophysical ocean model, we show that Atlantic cod individuals residing in sheltered estuarine habitats of Scandinavian fjords mainly belong to offshore oceanic populations with considerable connectivity between these diverse ecosystems. Nevertheless, we also find evidence for discrete fjord populations that are genetically differentiated from offshore populations, indicative of local adaptation, the degree of which appears to be influenced by connectivity. Analyses of the genomic architecture reveal a significant overrepresentation of a large ~5 Mb chromosomal rearrangement in fjord cod, previously proposed to comprise genes critical for the survival at low salinities. This suggests that despite considerable connectivity with offshore populations, local adaptation to fjord environments may be enabled by suppression of recombination in the rearranged region. Our study provides new insights into the potential of local adaptation in high gene flow species within fine geographical scales and highlights the importance of genome architecture in analyses of ecological adaptation.

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.

Ocean current patterns drive the worldwide colonization of eelgrass (Zostera marina).

Currents are unique drivers of oceanic phylogeography and thus determine the distribution of marine coastal species, along with past glaciations and sea-level changes. Here we reconstruct the worldwide colonization history of eelgrass (Zostera marina L.), the most widely distributed marine flowering plant or seagrass from its origin in the Northwest Pacific, based on nuclear and chloroplast genomes. We identified two divergent Pacific clades with evidence for admixture along the East Pacific coast. Two west-to-east (trans-Pacific) colonization events support the key role of the North Pacific Current. Time-calibrated nuclear and chloroplast phylogenies yielded concordant estimates of the arrival of Z. marina in the Atlantic through the Canadian Arctic, suggesting that eelgrass-based ecosystems, hotspots of biodiversity and carbon sequestration, have only been present there for ~243 ky (thousand years). Mediterranean populations were founded ~44 kya, while extant distributions along western and eastern Atlantic shores were founded at the end of the Last Glacial Maximum (~19 kya), with at least one major refuge being the North Carolina region. The recent colonization and five- to sevenfold lower genomic diversity of the Atlantic compared to the Pacific populations raises concern and opportunity about how Atlantic eelgrass might respond to rapidly warming coastal oceans.

Effects of pesticides and metals on penaeid shrimps in Maputo Bay, Mozambique - A field study.

Estuaries are important nursery areas for many species and these habitats are often affected by anthropogenic activities. We investigate possible negative effects of pesticides and metals on penaeid shrimps in Maputo Bay, Mozambique. Shrimps and water samples were collected in three estuaries and one coastal area for biomarker and chemical analysis. Acetylcholinesterase (AChE) and glutathione-S transferase activities were analysed as biomarkers for pollutants. 37 different pesticides were analysed in water samples and shrimp muscle tissue was analysed for 10 metals. Risk assessment showed that the environmental thresholds were exceeded for several herbicides in three of four of the assessed nursery areas. Lower AChE activities were detected in shrimps captured close to an agriculture area and this location had the lowest shrimp densities. Metal analysis in shrimp showed low levels. Despite localized effects, results highlight the need to improve the regulation of pollutants in the Espírito Santo estuary in Maputo bay.

Seascape genetics and biophysical connectivity modelling support conservation of the seagrass Zostera marina in the Skagerrak-Kattegat region of the eastern North Sea.

Maintaining and enabling evolutionary processes within meta-populations are critical to resistance, resilience and adaptive potential. Knowledge about which populations act as sources or sinks, and the direction of gene flow, can help to focus conservation efforts more effectively and forecast how populations might respond to future anthropogenic and environmental pressures. As a foundation species and habitat provider, Zostera marina (eelgrass) is of critical importance to ecosystem functions including fisheries. Here, we estimate connectivity of Z. marina in the Skagerrak-Kattegat region of the North Sea based on genetic and biophysical modelling. Genetic diversity, population structure and migration were analysed at 23 locations using 20 microsatellite loci and a suite of analytical approaches. Oceanographic connectivity was analysed using Lagrangian dispersal simulations based on contemporary and historical distribution data dating back to the late 19th century. Population clusters, barriers and networks of connectivity were found to be very similar based on either genetic or oceanographic analyses. A single-generation model of dispersal was not realistic, whereas multigeneration models that integrate stepping-stone dispersal and extant and historic distribution data were able to capture and model genetic connectivity patterns well. Passive rafting of flowering shoots along oceanographic currents is the main driver of gene flow at this spatial-temporal scale, and extant genetic connectivity strongly reflects the "ghost of dispersal past" sensu Benzie, 1999. The identification of distinct clusters, connectivity hotspots and areas where connectivity has become limited over the last century is critical information for spatial management, conservation and restoration of eelgrass.

Seed Predation by the Shore Crab Carcinus maenas: A Positive Feedback Preventing Eelgrass Recovery?

There is an increasing interest to restore the ecosystem services that eelgrass provides, after their continuous worldwide decline. Most attempts to restore eelgrass using seeds are challenged by very high seed losses and the reasons for these losses are not all clear. We assess the impact of predation on seed loss and eelgrass establishment, and explore methods to decrease seed loss during restoration in the Swedish northwest coast. In a laboratory study we identified three previously undescribed seed predators, the shore crab Carcinus maenas, the hermit crab Pagurus bernhardus and the sea urchin Strongylocentrotus droebachiensis, of which shore crabs consumed 2-7 times more seeds than the other two species. The importance of shore crabs as seed predators was supported in field cage experiments where one enclosed crab caused 73% loss of seeds over a 1-week period on average (~ 21 seeds per day). Seedling establishment was significantly higher (14%) in cages that excluded predators over an 8-month period than in uncaged plots and cages that allowed predators but prevented seed-transport (0.5%), suggesting that seed predation constitutes a major source of seed loss in the study area. Burying the seeds 2 cm below the sediment surface prevented seed predation in the laboratory and decreased predation in the field, constituting a way to decrease seed loss during restoration. Shore crabs may act as a key feedback mechanism that prevent the return of eelgrass both by direct consumption of eelgrass seeds and as a predator of algal mesograzers, allowing algal mats to overgrow eelgrass beds. This shore crab feedback mechanism could become self-generating by promoting the growth of its own nursery habitat (algal mats) and by decreasing the nursery habitat (seagrass meadow) of its dominant predator (cod). This double feedback-loop is supported by a strong increase of shore crab abundance in the last decades and may partly explain the regime shift in vegetation observed along the Swedish west coast.