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Understanding the ecological interactions that enhance the resilience of threatened ecosystems is essential in assuring their conservation and restoration. Top-down trophic interactions can increase resilience to bottom-up nutrient enrichment, however, as many seagrass ecosystems are threatened by both eutrophication and trophic modifications, understanding how these processes interact is important. Using a combination of approaches, we explored how bottom-up and top-down processes, acting individually or in conjunction, can affect eelgrass meadows and associated communities in the northern Baltic Sea. Field surveys along with fish diet and stable isotope analyses revealed that the eelgrass trophic network included two main top predatory fish species, each of which feeds on a separate group of invertebrate mesograzers (crustaceans or gastropods). Mesograzer abundance in the study area was high, and capable of mitigating the effects of increased algal biomass that resulted from experimental nutrient enrichment in the field. When crustacean mesograzers were experimentally excluded, gastropod mesograzers were able to compensate and limit the effects of nutrient enrichment on eelgrass biomass and growth. Our results suggest that top-down processes (i.e., suppression of algae by different mesograzer groups) may ensure eelgrass resilience to nutrient enrichment in the northern Baltic Sea, and the existence of multiple trophic pathways can provide additional resilience in the face of trophic modifications. However, the future resilience of these meadows is likely threatened by additional local stressors and global environmental change. Understanding the trophic links and interactions that ensure resilience is essential for managing and conserving these important ecosystems and the services they provide.

Motivation The BioTIME database contains raw data on species identities and abundances in ecological assemblages through time. These data enable users to calculate temporal trends in biodiversity within and amongst assemblages using a broad range of metrics. BioTIME is being developed as a community-led open-source database of biodiversity time series. Our goal is to accelerate and facilitate quantitative analysis of temporal patterns of biodiversity in the Anthropocene. Main types of variables included The database contains 8,777,413 species abundance records, from assemblages consistently sampled for a minimum of 2 years, which need not necessarily be consecutive. In addition, the database contains metadata relating to sampling methodology and contextual information about each record. Spatial location and grain BioTIME is a global database of 547,161 unique sampling locations spanning the marine, freshwater and terrestrial realms. Grain size varies across datasets from 0.0000000158 km2 (158 cm2) to 100 km2 (1,000,000,000,000 cm2). Time period and grain BioTIME records span from 1874 to 2016. The minimal temporal grain across all datasets in BioTIME is a year. Major taxa and level of measurement BioTIME includes data from 44,440 species across the plant and animal kingdoms, ranging from plants, plankton and terrestrial invertebrates to small and large vertebrates. Software format .csv and .SQL., Global Ecology and Biogeography, 27 (7), ISSN:1466-822X, ISSN:1466-8238

We tested the relative effects of nutrient loading, reduced predation, and reduced grazing on eelgrass community dynamics in Chesapeake Bay and found evidence supporting the “mutualistic mesograzer model” in which small invertebrate grazers control accumulation of epiphytic algae, buffer eutrophication effects, and thus facilitate seagrass dominance. Experimental reduction of crustacean grazers in the field stimulated a nearly sixfold increase in epiphytic algae, and reduced seagrass biomass by 65% compared to controls with grazers. Nutrient fertilization generally had much weaker effects, but an interaction with mesograzers was key in changing the sign of fertilization effects on the system: aboveground eelgrass biomass was reduced by fertilization under reduced grazing, but increased by fertilization under ambient grazing. When protected from predators in field cages, these mesograzers limited epiphyte blooms even with nutrient enrichment, and nutrients instead enhanced grazer secondary production. Crustacean mesograzers play a key role in maintaining macrophyte (seagrass) dominance in Chesapeake Bay, in buffering eelgrass against eutrophication, and in efficiently transferring nitrogen to higher trophic levels. Yet, these crustacean grazers are also highly sensitive to predator abundance. Reducing nutrient pollution alone is unlikely to restore seagrass meadows where alterations to food webs have reduced populations of algae-feeding mesograzers. Integration of both water quality and fishery management will be more effective in restoring and maintaining healthy coastal ecosystems.

Three quarters of the global human population will live in coastal areas in the coming decades and will continue to develop these areas as population density increases. Anthropogenic stressors from this coastal development may lead to fragmented habitats, altered food webs, changes in sediment characteristics, and loss of near-shore vegetated habitats. Seagrass systems are important vegetated estuarine habitats that are vulnerable to anthropogenic stressors, but provide valuable ecosystem functions. Key to maintaining these habitats that filter water, stabilize sediments, and provide refuge to juvenile animals is an understanding of the impacts of local coastal development. To assess development impacts in seagrass communities, we surveyed 20 seagrass beds in lower Chesapeake Bay, VA. We sampled primary producers, consumers, water quality, and sediment characteristics in seagrass beds, and characterized development along the adjacent shoreline using land cover data. Overall, we could not detect effects of local coastal development on these seagrass communities. Seagrass biomass varied only between sites, and was positively correlated with sediment organic matter. Epiphytic algal biomass and epibiont (epifauna and epiphyte) community composition varied between western and eastern regions of the bay. But, neither eelgrass (Zostera marina) leaf nitrogen (a proxy for integrated nitrogen loading), crustacean grazer biomass, epifaunal predator abundance, nor fish and crab abundance differed significantly among sites or regions. Overall, factors operating on different scales appear to drive primary producers, seagrass-associated faunal communities, and sediment properties in these important submerged vegetated habitats in lower Chesapeake Bay.

We characterized the seasonal and interannual variation in macrophytes, epiphytes, invertebrate herbivores, small demersal predators, and physicochemical characteristics of an eelgrass (Zostera marina) bed in Chesapeake Bay, Virginia, over 10 yr, to explore the relative importance of abiotic and biotic forcing on community composition and abundance. Our hypotheses were (1) physicochemical drivers affect community structure directly, (2) bottom-up trophic control is evidenced by positive covariance among trophic levels, (3) top-down control generates inverse patterns of abundance at adjacent trophic levels, and (4) species diversity among herbivores contributes to temporal stability. Composition and abundance of eelgrass-associated species varied strongly among seasons and years. Much of this variation correlated with temperature and salinity anomalies, and multivariate analysis grouped communities roughly by season, supporting our first hypothesis. Severe seagrass loss during the hot summer of 2005 shifted the community toward a novel composition, but community structure rebounded within a year. Evidence for trophic control was mixed: selected taxa showed patterns consistent with top-down or bottom-up control, but these patterns generally disappeared at the level of whole years and entire trophic levels. Our ability to detect trophic effects may have been limited, however, by consumer movement or changing behavioral responses to resource availability and predation. There was also little evidence that diversity stabilized total herbivore abundance. Although consumer effects on lower levels were inconsistent, the strong physicochemical forcing of community structure supports suggestions that eelgrass communities are highly vulnerable to natural and anthropogenic changes in climate and hydrography.

Eutrophication and fishing are common perturbations in aquatic ecosystems that have pervasive effects on community structure, including species diversity and abundance. While sedi- ment biogeochemical processes probably respond to these stressors, the linkages to ecosystem func- tioning remain poorly understood. To explore these linkages, we experimentally manipulated water column nutrient levels and food web composition (i.e. predator and grazer presence and absence) in a factorial design using field enclosures situated in a natural eelgrass Zostera marina bed. After 28 d, we quantified sediment organic matter (SOM) abundance and composition using measures of total organic carbon and nitrogen as well as fatty acid (FA) biomarkers. Nutrient enrichment led to a rapid increase of epiphytes and a decline in Z. marina biomass. Responding to the available algae, grazers reduced epiphytes and the abundance of microalgal FAs in the sediment. Predators reduced Z. marina abundance and possibly its ability to trap particulate organic matter (OM), leading to lower sediment organic carbon content and total FA abundance. There was evidence of a trophic cascade as FA contributions to sediments from epiphytes and diatoms were higher in treatments with both grazers and predators than in treatments with grazers only. Predators increased contributions of labile diatom-derived OM, which probably resulted in higher proportions of bacterial FA. Inter- actions between nutrient additions and food web composition indicated that SOM responses were complex and not predictable from single variables. Changes in SOM composition, combined with a rapid heterotrophic bacterial response, suggest that resource levels and aboveground community structure are important to sediment biogeochemistry in natural seagrass systems.

We tested the singular and interactive effects of resource availability (light) and community composition (food chain length and herbivore species richness) on eelgrass (Zostera marina) ecosystem properties and functioning with an experimental mesocosm system. Food chain length was manipulated through the presence or absence of blue crab (Callinectes sapidus) predators, whereas grazer species richness varied across three levels (zero, two, or four crustacean species). We found important and interacting effects of bottom-up and top-down forcings on sediment organic matter (SOM) composition. Light increased eelgrass and algal biomass and sediment organic carbon and nitrogen content. Increasing grazer diversity generally decreased algal biomass and ecosystem production but interacted with food chain length (i.e., presence of predatory crabs) and light. Predators generally increased algal biomass and ecosystem production through a trophic cascade, which was stronger at high grazer diversity and under ambient light. SOM composition, determined with fatty acid (FA) biomarkers, was sensitive to all manipulated variables. Increasing grazer species richness often decreased the contributions of FAs derived from plant and algal sources, whereas increasing light had the opposite effect. Food chain length was generally a less important determinant of SOM composition than light, although predators did increase FAs representative of heterotrophic bacteria. Overall, resource availability and epibenthic community composition strongly influenced organic matter cycling, SOM composition, and the bacterial community in seagrass-bed sediments.

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. National Science Foundation [OCE-1031061] info:eu-repo/semantics/publishedVersion

Biodiversity and food chain length each can strongly influence ecosystem functioning, yet their interactions rarely have been tested. We manipulated grazer diversity in seagrass mesocosms with and without a generalist predator and monitored community development. Changing food chain length altered biodiversity effects: higher grazer diversity enhanced secondary production, epiphyte grazing, and seagrass biomass only with predators present. Conversely, changing diversity altered top-down control: predator impacts on grazer and seagrass biomass were weaker in mixed-grazer assemblages. These interactions resulted in part from among-species trade-offs between predation resistance and competitive ability. Despite weak impact on grazer abundance at high diversity, predators nevertheless enhanced algal biomass through a behaviourally mediated trophic cascade. Moreover, predators influenced every measured variable except total plant biomass, suggesting that the latter is an insensitive metric of ecosystem functioning. Thus, biodiversity and trophic structure interactively influence ecosystem functioning, and neither factor’s impact is predictable in isolation.

High plant species richness can enhance primary production, animal diversity, and invasion resistance. Yet theory predicts that plant and herbivore diversity, which often covary in nature, should have countervailing effects on ecosystem properties. Supporting this, we show in a seagrass system that increasing grazer diversity reduced both algal biomass and total community diversity, and facilitated dominance of a grazer-resistant invertebrate. In parallel with previous plant results, however, grazer diversity enhanced secondary production, a critical determinant of fish yield. Although sampling explained some diversity effects, only the most diverse grazer assemblage maximized multiple ecosystem properties simultaneously, producing a distinct ecosystem state. Importantly, ecosystem responses at high grazer diversity often differed in magnitude and sign from those predicted from summed impacts of individual species. Thus, complex interactions, often opposing plant diversity effects, arose as emergent consequences of changing consumer diversity, advising caution in extrapolating conclusions from plant diversity experiments to food webs.

Background: Food web composition and resource levels can influence ecosystem properties such as productivity and elemental cycles. In particular, herbivores occupy a central place in food webs as the species richness and composition of this trophic level may simultaneously influence the transmission of resource and predator effects to higher and lower trophic levels, respectively. Yet, these interactions are poorly understood. Methodology/Principal Findings: Using an experimental seagrass mesocosm system, we factorially manipulated water column nutrient concentrations, food chain length, and diversity of crustacean grazers to address two questions: (1) Does food web composition modulate the effects of nutrient enrichment on plant and grazer biomasses and stoichiometry? (2) Do ecosystem fluxes of dissolved oxygen and nutrients more closely reflect above-ground biomass and community structure or sediment processes? Nutrient enrichment and grazer presence generally had strong effects on biomass accumulation, stoichiometry, and ecosystem fluxes, whereas predator effects were weaker or absent. Nutrient enrichment had little effect on producer biomass or net ecosystem production but strongly increased seagrass nutrient content, ecosystem flux rates, and grazer secondary production, suggesting that enhanced production was efficiently transferred from producers to herbivores. Gross ecosystem production (oxygen evolution) correlated positively with above-ground plant biomass, whereas inorganic nutrient fluxes were unrelated to plant or grazer biomasses, suggesting dominance by sediment microbial processes. Finally, grazer richness significantly stabilized ecosystem processes, as predators decreased ecosystem production and respiration only in the zero- and one- species grazer treatments. Conclusions/Significance: Overall, our results indicate that consumer presence and species composition strongly influence ecosystem responses to nutrient enrichment, and that increasing herbivore diversity can stabilize ecosystem flux rates in the face of perturbations.