Marsh migration and beyond: A scalable framework to assess tidal wetland resilience and support strategic management.

Tidal wetlands are critical but highly threatened ecosystems that provide vital services. Efficient stewardship of tidal wetlands requires robust comparative assessments of different marshes to understand their resilience to stressors, particularly in the face of relative sea level rise. Existing assessment frameworks aim to address tidal marsh resilience, but many are either too localized or too general, and few directly translate resilience evaluations to recommendations for management strategies. In response to the deficiencies in existing frameworks, we identified a set of metrics that influence overall marsh resilience that can be assessed at any spatial scale. We then developed a new comprehensive assessment framework to rank relative marsh resilience using these metrics, which are nested within three categories. We represent resilience as the sum of results across the three metric categories: current condition, adaptive capacity, and vulnerability. Users of this framework can add scores from each category to generate a total resilience score to compare across marshes or take the score from each category and refer to recommended management actions we developed based on expert elicitation for each combination of category results. We then applied the framework across the contiguous United States using publicly available data, and summarized results at multiple spatial scales, from regions to coastal states to National Estuarine Research Reserves to finer scale marsh units, to demonstrate the framework's value across these scales. Our national analysis allowed for comparison of tidal marsh resilience across geographies, which is valuable for determining where to prioritize management actions for desired future marsh conditions. In combination, the assessment framework and recommended management actions function as a broadly applicable decision-support tool that will enable resource managers to evaluate tidal marshes and select appropriate strategies for conservation, restoration, and other stewardship goals.

Use of historical isoscapes to develop an estuarine nutrient baseline.

Coastal eutrophication is a prevalent threat to the healthy functioning of ecosystems globally. While degraded water quality can be detected by monitoring oxygen, nutrient concentrations, and algal abundance, establishing regulatory guidelines is complicated by a lack of baseline data (e.g., pre-Anthropocene). We use historical carbon and nitrogen isoscapes over ~300 years from sediment cores to reconstruct spatial and temporal changes in nutrient dynamics for a central California estuary, Elkhorn Slough, where development and agriculture dramatically enhanced nutrient inputs over the past century. We found strong contrasts between current sediment stable isotopes and those from the recent past, demonstrating shifts exceeding those in previously studied eutrophic estuaries and substantial increases in nutrient inputs. Comparisons of contemporary with historical isoscapes also revealed that nitrogen sources shifted from a historical marine-terrestrial gradient with higher δ15N near the inlet to amplified denitrification at the head and mouth of the modern estuary driven by increased N inputs. Geospatial analysis of historical data suggests that an increase in fertilizer application - rather than population growth or increases in the extent of cultivated land - is chiefly responsible for increasing nutrient loads during the 20th century. This study demonstrates the ability of isotopic and stoichiometric maps to provide important perspectives on long-term shifts and spatial patterns of nutrients that can be used to improve management of nutrient pollution.

Mapping oysters on the Pacific coast of North America: A coast-wide collaboration to inform enhanced conservation.

To conserve coastal foundation species, it is essential to understand patterns of distribution and abundance and how they change over time. We synthesized oyster distribution data across the west coast of North America to develop conservation strategies for the native Olympia oyster (Ostrea lurida), and to characterize populations of the non-native Pacific oyster (Magallana gigas). We designed a user-friendly portal for data entry into ArcGIS Online and collected oyster records from unpublished data submitted by oyster experts and from the published literature. We used the resulting 2,000+ records to examine spatial and temporal patterns and made an interactive web-based map publicly available. Comparing records from pre-2000 vs. post-2000, we found that O. lurida significantly decreased in abundance and distribution, while M. gigas increased significantly. Currently the distribution and abundance of the two species are fairly similar, despite one species being endemic to this region since the Pleistocene, and the other a new introduction. We mapped the networks of sites occupied by oysters based on estimates of larval dispersal distance, and found that these networks were larger in Canada, Washington, and southern California than in other regions. We recommend restoration to enhance O. lurida, particularly within small networks, and to increase abundance where it declined. We also recommend restoring natural biogenic beds on mudflats and sandflats especially in the southern range, where native oysters are currently found most often on riprap and other anthropogenic structures. This project can serve as a model for collaborative mapping projects that inform conservation strategies for imperiled species or habitats.

Burrowing crabs and physical factors hasten marsh recovery at panne edges.

Salt marsh loss is projected to increase as sea-level rise accelerates with global climate change. Salt marsh loss occurs along both lateral creek and channel edges and in the marsh interior, when pannes expand and coalesce. Often, edge loss is attributed to erosive processes whereas dieback in the marsh interior is linked to excessive inundation or deposition of wrack, but remains poorly understood. We conducted a two-year field investigation in a central California estuary to identify key factors associated with panne contraction or expansion. Our study explored how an abundant burrowing crab, shown to have strong negative effects on marsh biomass near creek edges, affects panne dynamics. We also explored which physical panne attributes best predicted their dynamics. To our knowledge, ours is the first study of panne dynamics in a California marsh, despite how ubiquitous pannes are as a feature of marshes in the region and how often extensive marsh dieback occurs via panne expansion. Overall, we found that pannes contracted during the study period, but with variable rates of marsh recovery across pannes. Our model incorporating both physical and biological factors explained 86% of the variation in panne contraction. The model revealed a positive effect of crab activity, sediment accretion, and a composite of depth and elevation on panne contraction, and a negative effect of panne size and distance to nearest panne. The positive crab effects detected in pannes contrast with negative effects we detected near creek edges in a previous study, highlighting the context-dependence of top-down and bioturbation effects in marshes. As global change continues and the magnitude and frequency of disturbances increases, understanding the dynamics of marsh loss in the marsh interior as well as creek banks will be critical for the management of these coastal habitats.

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.

Conservation aquaculture as a tool for imperiled marine species: Evaluation of opportunities and risks for Olympia oysters, Ostrea lurida.

Conservation aquaculture is becoming an important tool to support the recovery of declining marine species and meet human needs. However, this tool comes with risks as well as rewards, which must be assessed to guide aquaculture activities and recovery efforts. Olympia oysters (Ostrea lurida) provide key ecosystem functions and services along the west coast of North America, but populations have declined to the point of local extinction in some estuaries. Here, we present a species-level, range-wide approach to strategically planning the use of aquaculture to promote recovery of Olympia oysters. We identified 12 benefits of culturing Olympia oysters, including identifying climate-resilient phenotypes that add diversity to growers' portfolios. We also identified 11 key risks, including potential negative ecological and genetic consequences associated with the transfer of hatchery-raised oysters into wild populations. Informed by these trade-offs, we identified ten priority estuaries where aquaculture is most likely to benefit Olympia oyster recovery. The two highest scoring estuaries have isolated populations with extreme recruitment limitation-issues that can be addressed via aquaculture if hatchery capacity is expanded in priority areas. By integrating social criteria, we evaluated which project types would likely meet the goals of local stakeholders in each estuary. Community restoration was most broadly suited to the priority areas, with limited commercial aquaculture and no current community harvest of the species, although this is a future stakeholder goal. The framework we developed to evaluate aquaculture as a tool to support species recovery is transferable to other systems and species globally; we provide a guide to prioritizing local knowledge and developing recommendations for implementation by using transparent criteria. Our collaborative process engaging diverse stakeholders including managers, scientists, Indigenous Tribal representatives, and shellfish growers can be used elsewhere to seek win-win opportunities to expand conservation aquaculture where benefits are maximized for both people and imperiled species.

Top-down and sideways: Herbivory and cross-ecosystem connectivity shape restoration success at the salt marsh-upland ecotone.

Wetland restoration provides remarkable opportunities to understand vegetation dynamics and to inform success of future projects through rigorous restoration experiments. Salt marsh restoration typically focuses on physical factors such as sediment dynamics and elevation. Despite many demonstrations of strong top-down effects on salt marshes, the potential for consumers to affect salt marsh restoration projects has rarely been quantified. Recently, major restoration projects at the Elkhorn Slough National Estuarine Research Reserve in central California, USA provided an opportunity to examine how herbivory influences restoration success. We quantified the strength of consumer effects by comparing caged to uncaged plantings, and compared effects among plant species and sites. We used camera traps to detect which herbivores were most common and how their abundance varied spatially. Beyond characterizing consumer effects, we also tested management strategies for reducing negative effects of herbivory at the restoration sites, including caging, mowing, and acoustic playbacks of predator sounds. We found extremely strong consumer effects at sites with extensive stands of exotic forbs upland of the high marsh; uncaged restoration plants suffered heavy herbivory and high mortality, while most caged plants survived. Brush rabbits (Sylvilagus bachmani) were by far the most frequent consumers of these high marsh plants. Our work thus provides the first evidence of mammal consumers affecting salt marsh restoration success. Mowing of tall exotic forb cover adjacent to the marsh at one restoration site greatly reduced consumption, and nearly all monitored plantings survived at a second restoration site where construction had temporarily eliminated upland cover. Playbacks of predator sounds did not significantly affect restoration plantings, but restoration efforts in marsh communities vulnerable to terrestrial herbivory may benefit from concurrent restoration of predator communities in the upland habitats surrounding the marsh. A landscape approach is thus critical for recognizing linkages between terrestrial and marine vegetation.

Species recovery and recolonization of past habitats: lessons for science and conservation from sea otters in estuaries.

Recovering species are often limited to much smaller areas than they historically occupied. Conservation planning for the recovering species is often based on this limited range, which may simply be an artifact of where the surviving population persisted. Southern sea otters (Enhydra lutris nereis) were hunted nearly to extinction but recovered from a small remnant population on a remote stretch of the California outer coast, where most of their recovery has occurred. However, studies of recently-recolonized estuaries have revealed that estuaries can provide southern sea otters with high quality habitats featuring shallow waters, high production and ample food, limited predators, and protected haul-out opportunities. Moreover, sea otters can have strong effects on estuarine ecosystems, fostering seagrass resilience through their consumption of invertebrate prey. Using a combination of literature reviews, population modeling, and prey surveys we explored the former estuarine habitats outside the current southern sea otter range to determine if these estuarine habitats can support healthy sea otter populations. We found the majority of studies and conservation efforts have focused on populations in exposed, rocky coastal habitats. Yet historical evidence indicates that sea otters were also formerly ubiquitous in estuaries. Our habitat-specific population growth model for California's largest estuary-San Francisco Bay-determined that it alone can support about 6,600 sea otters, more than double the 2018 California population. Prey surveys in estuaries currently with (Elkhorn Slough and Morro Bay) and without (San Francisco Bay and Drakes Estero) sea otters indicated that the availability of prey, especially crabs, is sufficient to support healthy sea otter populations. Combining historical evidence with our results, we show that conservation practitioners could consider former estuarine habitats as targets for sea otter and ecosystem restoration. This study reveals the importance of understanding how recovering species interact with all the ecosystems they historically occupied, both for improved conservation of the recovering species and for successful restoration of ecosystem functions and processes.

Pattern and scale: evaluating generalities in crab distributions and marsh dynamics from small plots to a national scale.

The generality of ecological patterns depends inextricably on the scale at which they are examined. We investigated patterns of crab distribution and the relationship between crabs and vegetation in salt marshes at multiple scales. By using consistent monitoring protocols across 15 U.S. National Estuarine Research Reserves, we were able to synthesize patterns from the scale of quadrats to the entire marsh landscape to regional and national scales. Some generalities emerged across marshes from our overall models, and these are useful for informing broad coastal management policy. We found that crab burrow distribution within a marsh could be predicted by marsh elevation, distance to creek and soil compressibility. While these physical factors also affected marsh vegetation cover, we did not find a strong or consistent overall effect of crabs at a broad scale in our multivariate model, though regressions conducted separately for each site revealed that crab burrows were negatively correlated with vegetation cover at 4 out of 15 sites. This contrasts with recent smaller-scale studies and meta-analyses synthesizing such studies that detected strong negative effects of crabs on marshes, likely because we sampled across the entire marsh landscape, while targeted studies are typically limited to low-lying areas near creeks, where crab burrow densities are highest. Our results suggest that sea-level rise generally poses a bigger threat to marshes than crabs, but there will likely be interactions between these physical and biological factors. Beyond these generalities across marshes, we detected some regional differences in crab community composition, richness, and abundance. However, we found striking differences among sites within regions, and within sites, in terms of crab abundance and relationships to marsh integrity. Although generalities are broadly useful, our findings indicate that local managers cannot rely on data from other nearby systems, but rather need local information for developing salt marsh management strategies.

Timing of stressors alters interactive effects on a coastal foundation species.

The effects of climate-driven stressors on organismal performance and ecosystem functioning have been investigated across many systems; however, manipulative experiments generally apply stressors as constant and simultaneous treatments, rather than accurately reflecting temporal patterns in the natural environment. Here, we assessed the effects of temporal patterns of high aerial temperature and low salinity on survival of Olympia oysters (Ostrea lurida), a foundation species of conservation and restoration concern. As single stressors, low salinity (5 and 10 psu) and the highest air temperature (40°C) resulted in oyster mortality of 55.8, 11.3, and 23.5%, respectively. When applied on the same day, low salinity and high air temperature had synergistic negative effects that increased oyster mortality. This was true even for stressor levels that were relatively mild when applied alone (10 psu and 35°C). However, recovery times of two or four weeks between stressors eliminated the synergistic effects. Given that most natural systems threatened by climate change are subject to multiple stressors that vary in the timing of their occurrence, our results suggest that it is important to examine temporal variation of stressors in order to more accurately understand the possible biological responses to global change.

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.

Testing local and global stressor impacts on a coastal foundation species using an ecologically realistic framework.

Despite the abundance of literature on organismal responses to multiple environmental stressors, most studies have not matched the timing of experimental manipulations with the temporal pattern of stressors in nature. We test the interactive effects of diel-cycling hypoxia with both warming and decreased salinities using ecologically realistic exposures. Surprisingly, we found no evidence of negative synergistic effects on Olympia oyster growth; rather, we found only additive and opposing effects of hypoxia (detrimental) and warming (beneficial). We suspect that diel-cycling provided a temporal refuge that allowed physiological compensation. We also tested for latent effects of warming and hypoxia to low-salinity tolerance using a seasonal delay between stressor events. However, we did not find a latent effect, rather a threshold survival response to low salinity that was independent of early life-history exposure to warming or hypoxia. The absence of synergism is likely the result of stressor treatments that mirror the natural timing of environmental stressors. We provide environmental context for laboratory experimental data by examining field time series environmental data from four North American west coast estuaries and find heterogeneous environmental signals that characterize each estuary, suggesting that the potential stressor exposure to oysters will drastically differ over moderate spatial scales. This heterogeneity implies that efforts to conserve and restore oysters will require an adaptive approach that incorporates knowledge of local conditions. We conclude that studies of multiple environmental stressors can be greatly improved by integrating ecologically realistic exposure and timing of stressors found in nature with organismal life-history traits.

Biodiversity effects and rates of spread of nonnative eucalypt woodlands in central California.

Woodlands comprised of planted, nonnative trees are increasing in extent globally, while native woodlands continue to decline due to human activities. The ecological impacts of planted woodlands may include changes to the communities of understory plants and animals found among these nonnative trees relative to native woodlands, as well as invasion of adjacent habitat areas through spread beyond the originally planted areas. Eucalypts (Eucalyptus spp.) are among the most widely planted trees worldwide, and are very common in California, USA. The goals of our investigation were to compare the biological communities of nonnative eucalypt woodlands to native oak woodlands in coastal central California, and to examine whether planted eucalypt groves have increased in size over the past decades. We assessed site and habitat attributes and characterized biological communities using understory plant, ground-dwelling arthropod, amphibian, and bird communities as indicators. Degree of difference between native and nonnative woodlands depended on the indicator used. Eucalypts had significantly greater canopy height and cover, and significantly lower cover by perennial plants and species richness of arthropods than oaks. Community composition of arthropods also differed significantly between eucalypts and oaks. Eucalypts had marginally significantly deeper litter depth, lower abundance of native plants with ranges limited to western North America, and lower abundance of amphibians. In contrast to these differences, eucalypt and oak groves had very similar bird community composition, species richness, and abundance. We found no evidence of "invasional meltdown," documenting similar abundance and richness of nonnatives in eucalypt vs. oak woodlands. Our time-series analysis revealed that planted eucalypt groves increased 271% in size, on average, over six decades, invading adjacent areas. Our results inform science-based management of California woodlands, revealing that while bird communities would probably not be affected by restoration of eucalypt to oak woodlands, such a restoration project would not only stop the spread of eucalypts into adjacent habitats but would also enhance cover by western North American native plants and perennials, enhance amphibian abundance, and increase arthropod richness.

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.

Impacts and interactions of multiple human perturbations in a California salt marsh.

Multiple disturbances to ecosystems can influence community structure by modifying resistance to and recovery from invasion by non-native species. Predicting how invasibility responds to multiple anthropogenic impacts is particularly challenging due to the variety of potential stressors and complex responses. Using manipulative field experiments, we examined the relative impact of perturbations that primarily change abiotic or biotic factors to promote invasion in coastal salt marsh plant communities. Specifically we test the hypotheses that nitrogen enrichment and human trampling facilitate invasion of upland weeds into salt marsh, and that the ability of salt marsh communities to resist and/or recover from invasion is modified by hydrological conditions. Nitrogen enrichment affected invasion of non-native upland plants at only one of six sites, and increased aboveground native marsh biomass at only two sites. Percent cover of native marsh plants declined with trampling at all sites, but recovered earlier at tidally flushed sites than at tidally restricted sites. Synergistic interactions between trampling and restricting tidal flow resulted in significantly higher cover of non-native upland plants in trampled plots at tidally restricted sites. Percent cover of non-native plants recovered to pre-trampling levels in fully tidal sites, but remained higher in tidally restricted sites after 22 months. Thus, perturbations that reduce biotic resistance interact with perturbations that alter abiotic conditions to promote invasion. This suggests that to effectively conserve or restore native biodiversity in altered systems, one must consider impacts of multiple human disturbances, and the interactions between them.