Top-predator recovery abates geomorphic decline of a coastal ecosystem.

The recovery of top predators is thought to have cascading effects on vegetated ecosystems and their geomorphology1,2, but the evidence for this remains correlational and intensely debated3,4. Here we combine observational and experimental data to reveal that recolonization of sea otters in a US estuary generates a trophic cascade that facilitates coastal wetland plant biomass and suppresses the erosion of marsh edges-a process that otherwise leads to the severe loss of habitats and ecosystem services5,6. Monitoring of the Elkhorn Slough estuary over several decades suggested top-down control in the system, because the erosion of salt marsh edges has generally slowed with increasing sea otter abundance, despite the consistently increasing physical stress in the system (that is, nutrient loading, sea-level rise and tidal scour7-9). Predator-exclusion experiments in five marsh creeks revealed that sea otters suppress the abundance of burrowing crabs, a top-down effect that cascades to both increase marsh edge strength and reduce marsh erosion. Multi-creek surveys comparing marsh creeks pre- and post-sea otter colonization confirmed the presence of an interaction between the keystone sea otter, burrowing crabs and marsh creeks, demonstrating the spatial generality of predator control of ecosystem edge processes: densities of burrowing crabs and edge erosion have declined markedly in creeks that have high levels of sea otter recolonization. These results show that trophic downgrading could be a strong but underappreciated contributor to the loss of coastal wetlands, and suggest that restoring top predators can help to re-establish geomorphic stability.

Climate drives the geography of marine consumption by changing predator communities.

The global distribution of primary production and consumption by humans (fisheries) is well-documented, but we have no map linking the central ecological process of consumption within food webs to temperature and other ecological drivers. Using standardized assays that span 105° of latitude on four continents, we show that rates of bait consumption by generalist predators in shallow marine ecosystems are tightly linked to both temperature and the composition of consumer assemblages. Unexpectedly, rates of consumption peaked at midlatitudes (25 to 35°) in both Northern and Southern Hemispheres across both seagrass and unvegetated sediment habitats. This pattern contrasts with terrestrial systems, where biotic interactions reportedly weaken away from the equator, but it parallels an emerging pattern of a subtropical peak in marine biodiversity. The higher consumption at midlatitudes was closely related to the type of consumers present, which explained rates of consumption better than consumer density, biomass, species diversity, or habitat. Indeed, the apparent effect of temperature on consumption was mostly driven by temperature-associated turnover in consumer community composition. Our findings reinforce the key influence of climate warming on altered species composition and highlight its implications for the functioning of Earth's ecosystems.

Rapid enhancement of multiple ecosystem services following the restoration of a coastal foundation species.

The global decline of marine foundation species (kelp forests, mangroves, salt marshes, and seagrasses) has contributed to the degradation of the coastal zone and threatens the loss of critical ecosystem services and functions. Restoration of marine foundation species has had variable success, especially for seagrasses, where a majority of restoration efforts have failed. While most seagrass restorations track structural attributes over time, rarely do restorations assess the suite of ecological functions that may be affected by restoration. Here we report on the results of two small-scale experimental seagrass restoration efforts in a central California estuary where we transplanted 117 0.25-m2 plots (2,340 shoots) of the seagrass species Zostera marina. We quantified restoration success relative to persistent reference beds, and in comparison to unrestored, unvegetated areas. Within three years, our restored plots expanded ~8,500%, from a total initial area of 29 to 2,513 m2 . The restored beds rapidly began to resemble the reference beds in (1) seagrass structural attributes (canopy height, shoot density, biomass), (2) ecological functions (macrofaunal species richness and abundance, epifaunal species richness, nursery function), and (3) biogeochemical functions (modulation of water quality). We also developed a multifunctionality index to assess cumulative functional performance, which revealed restored plots are intermediate between reference and unvegetated habitats, illustrating how rapidly multiple functions recovered over a short time period. Our comprehensive study is one of few published studies to quantify how seagrass restoration can enhance both biological and biogeochemical functions. Our study serves as a model for quantifying ecosystem services associated with the restoration of a foundation species and demonstrates the potential for rapid functional recovery that can be achieved through targeted restoration of fast-growing foundation species under suitable conditions.

Unexpected resilience of a seagrass system exposed to global stressors.

Despite a growing interest in identifying tipping points in response to environmental change, our understanding of the ecological mechanisms underlying nonlinear ecosystem dynamics is limited. Ecosystems governed by strong species interactions can provide important insight into how nonlinear relationships between organisms and their environment propagate through ecosystems, and the potential for environmentally mediated species interactions to drive or protect against sudden ecosystem shifts. Here, we experimentally determine the functional relationships (i.e., the shapes of the relationships between predictor and response variables) of a seagrass assemblage with well-defined species interactions to ocean acidification (enrichment of CO2 ) in isolation and in combination with nutrient loading. We demonstrate that the effect of ocean acidification on grazer biomass (Phyllaplysia taylori and Idotea resecata) was quadratic, with the peak of grazer biomass at mid-pH levels. Algal grazing was negatively affected by nutrients, potentially due to low grazer affinity for macroalgae (Ulva intestinalis), as recruitment of both macroalgae and diatoms were favored in elevated nutrient conditions. This led to an exponential increase in macroalgal and epiphyte biomass with ocean acidification, regardless of nutrient concentration. When left unchecked, algae can cause declines in seagrass productivity and persistence through shading and competition. Despite quadratic and exponential functional relationships to stressors that could cause a nonlinear decrease in seagrass biomass, productivity of our model seagrass-the eelgrass (Zostera marina)- remained highly resilient to increasing acidification. These results suggest that important species interactions governing ecosystem dynamics may shift with environmental change, and ecosystem state may be decoupled from ecological responses at lower levels of organization.

Impact of multiple stressors on juvenile fish in estuaries of the northeast Pacific.

A key step in identifying global change impacts on species and ecosystems is to quantify effects of multiple stressors. To date, the science of global change has been dominated by regional field studies, experimental manipulation, meta-analyses, conceptual models, reviews, and studies focusing on a single stressor or species over broad spatial and temporal scales. Here, we provide one of the first studies for coastal systems examining multiple stressor effects across broad scales, focused on the nursery function of 20 estuaries spanning 1,600 km of coastline, 25 years of monitoring, and seven fish and invertebrate species along the northeast Pacific coast. We hypothesized those species most estuarine dependent and negatively impacted by human activities would have lower presence and abundances in estuaries with greater anthropogenic land cover, pollution, and water flow stress. We found significant negative relationships between juveniles of two of seven species (Chinook salmon and English sole) and estuarine stressors. Chinook salmon were less likely to occur and were less abundant in estuaries with greater pollution stress. They were also less abundant in estuaries with greater flow stress, although this relationship was marginally insignificant. English sole were less abundant in estuaries with greater land cover stress. Together, we provide new empirical evidence that effects of stressors on two fish species culminate in detectable trends along the northeast Pacific coast, elevating the need for protection from pollution, land cover, and flow stressors to their habitats. Lack of response among the other five species could be related to differing resistance to specific stressors, type and precision of the stressor metrics, and limitations in catch data across estuaries and habitats. Acquiring improved measurements of impacts to species will guide future management actions, and help predict how estuarine nursery functions can be optimized given anthropogenic stressors and climate change scenarios.

Climate mediates hypoxic stress on fish diversity and nursery function at the land-sea interface.

Coastal ecosystems provide numerous important ecological services, including maintenance of biodiversity and nursery grounds for many fish species of ecological and economic importance. However, human population growth has led to increased pollution, ocean warming, hypoxia, and habitat alteration that threaten ecosystem services. In this study, we used long-term datasets of fish abundance, water quality, and climatic factors to assess the threat of hypoxia and the regulating effects of climate on fish diversity and nursery conditions in Elkhorn Slough, a highly eutrophic estuary in central California (United States), which also serves as a biodiversity hot spot and critical nursery grounds for offshore fisheries in a broader region. We found that hypoxic conditions had strong negative effects on extent of suitable fish habitat, fish species richness, and abundance of the two most common flatfish species, English sole (Parophrys vetulus) and speckled sanddab (Citharichthys stigmaeus). The estuary serves as an important nursery ground for English sole, making this species vulnerable to anthropogenic threats. We determined that estuarine hypoxia was associated with significant declines in English sole nursery habitat, with cascading effects on recruitment to the offshore adult population and fishery, indicating that human land use activities can indirectly affect offshore fisheries. Estuarine hypoxic conditions varied spatially and temporally and were alleviated by strengthening of El Niño conditions through indirect pathways, a consistent result in most estuaries across the northeast Pacific. These results demonstrate that changes to coastal land use and climate can fundamentally alter the diversity and functioning of coastal nurseries and their adjacent ocean 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.

Trophic cascades on the edge: fostering seagrass resilience via a novel pathway.

Despite widespread degradation, some coastal ecosystems display remarkable resilience. For seagrasses, a century-old paradigm has implicated macroalgal blooms stimulated by anthropogenic nutrient, loading as a primary driver of seagrass decline, yet relatively little attention has been given to drivers of seagrass resilience. In Elkhorn Slough, CA, an estuarine system characterized by extreme anthropogenic nutrient loading and macroalgal (Ulva spp.) blooms, seagrass (Zostera marina) beds have recovered concurrent with colonization of the estuary by top predators, sea otters (Enhydra lutris). Here, we follow up on the results of a previous experiment at the seagrass interior, showing how sea otters can generate a trophic cascade that promotes seagrass. We conducted an experiment and constructed structural equation models to determine how sea otters, through a trophic cascade, might affect the edge of seagrass beds where expansion occurs. We found that at the edge, sea otters promoted both seagrass and ephemeral macroalgae, with the latter contributing beneficial grazers to the seagrass. The surprising results that sea otters promote two potentially competing vegetation types, and a grazer assemblage at their boundary provides a mechanism by which seagrasses can expand in eutrophic environments, and contributes to a growing body of literature demonstrating that ephemeral macroalgae are not always negatively associated with seagrass. Our results highlight the potential for top predator recovery to enhance ecosystem resilience to anthropogenic alterations through several cascading mechanisms.

Recovery of a top predator mediates negative eutrophic effects on seagrass.

A fundamental goal of the study of ecology is to determine the drivers of habitat-forming vegetation, with much emphasis given to the relative importance to vegetation of "bottom-up" forces such as the role of nutrients and "top-down" forces such as the influence of herbivores and their predators. For coastal vegetation (e.g., kelp, seagrass, marsh, and mangroves) it has been well demonstrated that alterations to bottom-up forcing can cause major disturbances leading to loss of dominant vegetation. One such process is anthropogenic nutrient loading, which can lead to major changes in the abundance and species composition of primary producers, ultimately affecting important ecosystem services. In contrast, much less is known about the relative importance of apex predators on coastal vegetated ecosystems because most top predator populations have been depleted or lost completely. Here we provide evidence that an unusual four-level trophic cascade applies in one such system, whereby a top predator mitigates the bottom-up influences of nutrient loading. In a study of seagrass beds in an estuarine ecosystem exposed to extreme nutrient loading, we use a combination of a 50-y time series analysis, spatial comparisons, and mesocosm and field experiments to demonstrate that sea otters (Enhydra lutris) promote the growth and expansion of eelgrass (Zostera marina) through a trophic cascade, counteracting the negative effects of agriculturally induced nutrient loading. Our results add to a small but growing body of literature illustrating that significant interactions between bottom-up and top-down forces occur, in this case with consequences for the conservation of valued ecosystem services provided by seagrass.

Sediment carbon storage differs in native and non-native Caribbean seagrass beds.

Non-native species are expanding globally and can alter ecosystem functions, including food web dynamics, community structure and carbon storage. Seagrass are foundation species that contribute a variety of ecosystem services in near-shore coastal ecosystems, including a significant sink of carbon. In the Caribbean, the rapidly expanding non-native Halophila stipulacea has unknown impacts on carbon storage. To investigate the impacts on carbon storage, we quantified organic carbon (Corg) content in sediment and seagrass tissues from monotypic H. stipulacea beds, mixed native seagrass beds dominated by Thalassia testudinum and Syringodium filiforme, and unvegetated substrate in St. John, USVI. We found native seagrass-vegetated sediment contained 1.3 times more Corg than sediment covered by H. stipulacea, and 1.6 times more Corg than unvegetated areas on average. Whereas, H. stipulacea-dominated substrate stored 1.2 times more Corg than unvegetated substrate. Likewise, native species contained 2.2 times more aboveground biomass and 6.0 times more belowground biomass than H. stipulacea. Since seagrasses are critical sources of carbon sequestration, our results suggest that invading H. stipulacea is associated with lower carbon stocks which has potential implications for conservation activities and climate change mitigation.