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.

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.

Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow.

Ocean acidification threatens many marine organisms, especially marine calcifiers. The only global-scale solution to ocean acidification remains rapid reduction in CO2 emissions. Nevertheless, interest in localized mitigation strategies has grown rapidly because of the recognized threat ocean acidification imposes on natural communities, including ones important to humans. Protection of seagrass meadows has been considered as a possible approach for localized mitigation of ocean acidification due to their large standing stocks of organic carbon and high productivity. Yet much work remains to constrain the magnitudes and timescales of potential buffering effects from seagrasses. We developed a biogeochemical box model to better understand the potential for a temperate seagrass meadow to locally mitigate the effects of ocean acidification. Then we parameterized the model using data from Tomales Bay, an inlet on the coast of California, USA which supports a major oyster farming industry. We conducted a series of month-long model simulations to characterize processes that occur during summer and winter. We found that average pH in the seagrass meadows was typically within 0.04 units of the pH of the primary source waters into the meadow, although we did find occasional periods (hours) when seagrass metabolism may modify the pH by up to ±0.2 units. Tidal phasing relative to the diel cycle modulates localized pH buffering within the seagrass meadow such that maximum buffering occurs during periods of the year with midday low tides. Our model results suggest that seagrass metabolism in Tomales Bay would not provide long-term ocean acidification mitigation. However, we emphasize that our model results may not hold in meadows where assumptions about depth-averaged net production and seawater residence time within the seagrass meadow differ from our model assumptions. Our modeling approach provides a framework that is easily adaptable to other seagrass meadows in order to evaluate the extent of their individual buffering capacities. Regardless of their ability to buffer ocean acidification, seagrass meadows maintain many critically important ecosystem goods and services that will be increasingly important as humans increasingly affect coastal ecosystems.

Coast-wide recruitment dynamics of Olympia oysters reveal limited synchrony and multiple predictors of failure.

Recruitment of new propagules into a population can be a critical determinant of adult density. We examined recruitment dynamics in the Olympia oyster (Ostrea lurida), a species occurring almost entirely in estuaries. We investigated spatial scales of interannual synchrony across 37 sites in eight estuaries along 2,500 km of Pacific North American coastline, predicting that high vs. low recruitment years would coincide among neighboring estuaries due to shared exposure to regional oceanographic factors. Such synchrony in recruitment has been found for many marine species and some migratory estuarine species, but has never been examined across estuaries in a species that can complete its entire life cycle within the same estuary. To inform ongoing restoration efforts for Olympia oysters, which have declined in abundance in many estuaries, we also investigated predictors of recruitment failure. We found striking contrasts in absolute recruitment rate and frequency of recruitment failure among sites, estuaries, and years. Although we found a positive relationship between upwelling and recruitment, there was little evidence of synchrony in recruitment among estuaries along the coast, and only limited synchrony of sites within estuaries, suggesting recruitment rates are affected more strongly by local dynamics within estuaries than by regional oceanographic factors operating at scales encompassing multiple estuaries. This highlights the importance of local wetland and watershed management for the demography of oysters, and perhaps other species that can complete their entire life cycle within estuaries. Estuaries with more homogeneous environmental conditions had greater synchrony among sites, and this led to the potential for estuary-wide failure when all sites had no recruitment in the same year. Environmental heterogeneity within estuaries may thus buffer against estuary-wide recruitment failure, analogous to the portfolio effect for diversity. Recruitment failure was correlated with lower summer water temperature, higher winter salinity, and shorter residence time: all indicators of stronger marine influence on estuaries. Recruitment failure was also more common in estuaries with limited networks of nearby adult oysters. Large existing oyster networks are thus of high conservation value, while estuaries that lack them would benefit from restoration efforts to increase the extent and connectivity of sites supporting oysters.

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.

Historical ecology with real numbers: past and present extent and biomass of an imperilled estuarine habitat.

Historic baselines are important in developing our understanding of ecosystems in the face of rapid global change. While a number of studies have sought to determine changes in extent of exploited habitats over historic timescales, few have quantified such changes prior to late twentieth century baselines. Here, we present, to our knowledge, the first ever large-scale quantitative assessment of the extent and biomass of marine habitat-forming species over a 100-year time frame. We examined records of wild native oyster abundance in the United States from a historic, yet already exploited, baseline between 1878 and 1935 (predominantly 1885-1915), and a current baseline between 1968 and 2010 (predominantly 2000-2010). We quantified the extent of oyster grounds in 39 estuaries historically and 51 estuaries from recent times. Data from 24 estuaries allowed comparison of historic to present extent and biomass. We found evidence for a 64 per cent decline in the spatial extent of oyster habitat and an 88 per cent decline in oyster biomass over time. The difference between these two numbers illustrates that current areal extent measures may be masking significant loss of habitat through degradation.

Joint effects of patch edges and habitat degradation on faunal predation risk in a widespread marine foundation species.

Human activities degrade and fragment coastal marine habitats, reducing their structural complexity and making habitat edges a prevalent seascape feature. Though habitat edges frequently are implicated in reduced faunal survival and biodiversity, results of experiments on edge effects have been inconsistent, calling for a mechanistic approach to the study of edges that explicitly includes indirect and interactive effects of habitat alteration at multiple scales across biogeographic gradients. We used an experimental network spanning 17 eelgrass (Zostera marina) sites across the Atlantic and Pacific oceans and the Mediterranean Sea to determine (1) if eelgrass edges consistently increase faunal predation risk, (2) whether edge effects on predation risk are altered by habitat degradation (shoot thinning), and (3) whether variation in the strength of edge effects among sites can be explained by biogeographical variability in covarying eelgrass habitat features. Contrary to expectations, at most sites, predation risk for tethered crustaceans (crabs or shrimps) was lower along patch edges than in patch interiors, regardless of the extent of habitat degradation. However, the extent to which edges reduced predation risk, compared to the patch interior, was correlated with the extent to which edges supported higher eelgrass structural complexity and prey biomass compared to patch interiors. This suggests an indirect component to edge effects in which the impact of edge proximity on predation risk is mediated by the effect of edges on other key biotic factors. Our results suggest that studies on edge effects should consider structural characteristics of patch edges, which may vary geographically, and multiple ways that humans degrade habitats.

Environmental quality of Korean coasts as determined by modified Shannon-Wiener evenness proportion.

The coast of the Korean peninsula experiences a range of human impacts, including pollution, shipping, reclamation, and aquaculture, that have motivated numerous local studies of macrobenthic organisms. In this paper, 1,492 subtidal stations were compiled from 23 studies (areas) to evaluate environmental quality on a broader scale. A common index in biomonitoring, Shannon-Wiener evenness proportion (SEP), could not incorporate azoic or single-species samples. This shortcoming was overcome by developing an inverse function of SEP (ISEP), which was positively correlated with independent measures of water quality available for nine sites and was not biased by the size of the sampling unit. Additionally, at Shihwa Dike, where samples were collected before and after reinstating a tidal connection with the ocean, ISEP values improved over time, as expected. Thus, it is now possible to assign Korean subtidal sites to seven ISEP "grades" and to use their values and trends to guide coastal management.

Ecosystem metabolism drives pH variability and modulates long-term ocean acidification in the Northeast Pacific coastal ocean.

Ocean acidification poses serious threats to coastal ecosystem services, yet few empirical studies have investigated how local ecological processes may modulate global changes of pH from rising atmospheric CO2. We quantified patterns of pH variability as a function of atmospheric CO2 and local physical and biological processes at 83 sites over 25 years in the Salish Sea and two NE Pacific estuaries. Mean seawater pH decreased significantly at -0.009 ± 0.0005 pH yr-1 (0.22 pH over 25 years), with spatially variable rates ranging up to 10 times greater than atmospheric CO2-driven ocean acidification. Dissolved oxygen saturation (%DO) decreased by -0.24 ± 0.036% yr-1, with site-specific trends similar to pH. Mean pH shifted from <7.6 in winter to >8.0 in summer concomitant to the seasonal shift from heterotrophy (%DO < 100) to autotrophy (%DO > 100) and dramatic shifts in aragonite saturation state critical to shell-forming organisms (probability of undersaturation was >80% in winter, but <20% in summer). %DO overwhelmed the influence of atmospheric CO2, temperature and salinity on pH across scales. Collectively, these observations provide evidence that local ecosystem processes modulate ocean acidification, and support the adoption of an ecosystem perspective to ocean acidification and multiple stressors in productive aquatic habitats.

Comparison of shallow-water seston among biogenic habitats on tidal flats.

Aquatic structure-formers have the potential to establish mosaics of seston in shallow water if they modify the relative amounts of deposition (or filtration) and resuspension of particles. By sampling surface water adjacent to Lagrangian drifters traveling 0.1 to 2 m above the bottom, we tested the modification of seston in water masses flowing over two biogenic marine species (native eelgrass, Zostera marina; introduced oysters, Crassostrea gigas) in comparison to unstructured tidal flats. Water properties were examined at five intertidal sites in Washington State, USA, each with 27 drifts (three drifts at different stages of the tidal cycle in each of three patches of three habitat types; drift distance 116 m (109SD), duration 24 min (15SD)). At the initiation of each drift, habitat differences in water properties were already apparent: chlorophyll-a and total suspended solid (TSS) concentrations were greater in structured habitats than bare, and TSS was also inversely related to water depth. Water flowed more slowly across eelgrass than other habitat types. As water flowed across each habitat type, TSS generally increased, especially in shallow water, but without habitat differences; chlorophyll-a in these surface-water samples showed no consistent change during drifts. At higher TSS concentrations, quality in terms of organic content declined, and this relationship was not habitat-specific. However, quality in terms of chlorophyll-a concentration increased with TSS, as well as being greater in water over eelgrass than over other habitat types. These results support widespread mobilization of seston in shallow water ebbing or flooding across Washington State's tidal flats, especially as water passes into patches of biogenic species.

Population genetics of the Manila clam (Ruditapes philippinarum) introduced in North America and Europe.

Globally, the Manila clam (Ruditapes philippinarum) stands as the second most important bivalve species in fisheries and aquaculture. Native to the Pacific coast of Asia, it is now well-established in North America and Europe, where its on-going management reflects local economic interests. The historic record of transfers spans the 20th century and suggests sequential movement from Japan to North America, as a hitch-hiker on oysters, and then intentional introduction in Europe, but global genetic data are missing. We have studied mitochondrial DNA and microsatellite markers in nine populations from Asia, North America and Europe. The results from the two types of markers indicated a good concordance of present-day genetic structure with the reported history of clam transfers across continents, and no evidence of relevant concealed introductions from continental Asia in Europe and North America. However, European populations showed a loss of genetic variability and significant genetic differentiation as compared to their American counterparts. Our study shows that in spite of the increasing ease for species to spread out of their native range, in the case of the Manila clam this has not resulted in new invasion waves in the two studied continents.

Meta-Analysis of Reciprocal Linkages between Temperate Seagrasses and Waterfowl with Implications for Conservation.

Multi-trophic conservation and management strategies may be necessary if reciprocal linkages between primary producers and their consumers are strong. While herbivory on aquatic plants is well-studied, direct top-down control of seagrass populations has received comparatively little attention, particularly in temperate regions. Herein, we used qualitative and meta-analytic approaches to assess the scope and consequences of avian (primarily waterfowl) herbivory on temperate seagrasses of the genus Zostera. Meta-analyses revealed widespread evidence of spatio-temporal correlations between Zostera and waterfowl abundances as well as strong top-down effects of grazing on Zostera. We also documented the identity and diversity of avian species reported to consume Zostera and qualitatively assessed their potential to exert top-down control. Our results demonstrate that Zostera and their avian herbivores are ecologically linked and we suggest that bird herbivory may influence the spatial structure, composition, and functioning of the seagrass ecosystem. Therefore, the consequences of avian herbivory should be considered in the management of seagrass populations. Of particular concern are instances of seagrass overgrazing by waterfowl which result in long-term reductions in seagrass biomass or coverage, with subsequent impacts on local populations of waterfowl and other seagrass-affiliated species. While our results showed that bird density and type may affect the magnitude of the top-down effects of avian herbivory, empirical research on the strength, context-dependency, and indirect effects of waterfowl-Zostera interactions remains limited. For example, increased efforts that explicitly measure the effects of different functional groups of birds on seagrass abundance and/or document how climate change-driven shifts in waterfowl migratory patterns impact seagrass phenology and population structure will advance research programs for both ecologists and managers concerned with the joint conservation of both seagrasses and their avian herbivores.

Impact of supply-side ecology on consumer-mediated coexistence: evidence from a meta-analysis.

Studies of marine nearshore hard substrates have demonstrated that consumers and abiotic disturbances can remove biomass, clearing space for species that are competitively subordinate and subsequently increasing diversity. However, studies often examine the impact of these space-opening forces on diversity in isolation from other potentially interacting factors. In marine systems, space can be closed by recruitment decoupled from local populations. Therefore, we investigated how recruitment influences the impacts of consumers on diversity with a meta-analysis of 27 experiments of community development involving sessile species on marine hard substrates. These studies allowed quantification of recruitment rates, consumer pressure, and species richness of primary space occupants. This meta-analysis demonstrated that consumers generally increase diversity at high levels of recruitment but decrease diversity at low levels of recruitment. Therefore, species diversity of sessile species is controlled by the interaction between forces that open (predation and herbivory) and close (recruitment) space.

Restricted ranges in physical factors may constitute subtle stressors for estuarine biota.

Biotic trends along estuarine gradients can be affected by co-varying processes ranging from large-scale oceanographic to local-scale physico-chemical effects. As a baseline for future process studies, we investigated the distinct gradients in species richness and biomass in pebble-sand shorelines along the estuarine axis of Puget Sound, and the scales of variation of some of their physical correlates. Higher richness and biomass at beaches at the more marine end of the Sound are temporally consistent and seen in all trophic groups. Variables that correlate with biotic patterns include relatively subtle increases in beach surface and sediment temperatures and decreases in nearshore salinity near the head of the estuary, but not more localized parameters such as sediment grain size or porewater salinity. To understand whether these variables are true forcing functions of community structure, we are performing experimental work.

Extinction and ecosystem function in the marine benthos.

Rapid changes in biodiversity are occurring globally, yet the ecological impacts of diversity loss are poorly understood. Here we use data from marine invertebrate communities to parameterize models that predict how extinctions will affect sediment bioturbation, a process vital to the persistence of aquatic communities. We show that species extinction is generally expected to reduce bioturbation, but the magnitude of reduction depends on how the functional traits of individual species covary with their risk of extinction. As a result, the particular cause of extinction and the order in which species are lost ultimately govern the ecosystem-level consequences of biodiversity loss.