Faunal engineering stimulates landscape-scale accretion in southeastern US salt marshes.

The fate of coastal ecosystems depends on their ability to keep pace with sea-level rise-yet projections of accretion widely ignore effects of engineering fauna. Here, we quantify effects of the mussel, Geukensia demissa, on southeastern US saltmarsh accretion. Multi-season and -tidal stage surveys, in combination with field experiments, reveal that deposition is 2.8-10.7-times greater on mussel aggregations than any other marsh location. Our Delft-3D-BIVALVES model further predicts that mussels drive substantial changes to both the magnitude (±<0.1 cm·yr-1) and spatial patterning of accretion at marsh domain scales. We explore the validity of model predictions with a multi-year creekshed mussel manipulation of >200,000 mussels and find that this faunal engineer drives far greater changes to relative marsh accretion rates than predicted (±>0.4 cm·yr-1). Thus, we highlight an urgent need for empirical, experimental, and modeling work to resolve the importance of faunal engineers in directly and indirectly modifying the persistence of coastal ecosystems globally.

Wrack enhancement of post-hurricane vegetation and geomorphological recovery in a coastal dune.

Coastal ecosystems such as sand dunes, mangrove forests, and salt marshes provide natural storm protection for vulnerable shorelines. At the same time, storms erode and redistribute biological materials among coastal systems via wrack. Yet how such cross-ecosystem subsidies affect post-storm recovery is not well understood. Here, we report an experimental investigation into the effect of storm wrack on eco-geomorphological recovery of a coastal embryo dune in north-eastern Florida, USA, following hurricane Irma. We contrasted replicated 100-m2 wrack-removal and unmanipulated (control) plots, measuring vegetation and geomorphological responses over 21 months. Relative to controls, grass cover was reduced 4-fold where diverse storm wrack, including seagrass rhizomes, seaweed, and wood, was removed. Wrack removal was also associated with a reduction in mean elevation, which persisted until the end of the experiment when removal plots had a 14% lower mean elevation than control plots. These results suggest that subsides of wrack re-distributed from other ecosystem types (e.g. seagrasses, macroalgae, uplands): i) enhances the growth of certain dune-building grasses; and ii) boosts the geomorphological recovery of coastal dunes. Our study also indicates that the practice of post-storm beach cleaning to remove wrack-a practice widespread outside of protected areas-may undermine the resilience of coastal dunes and their services.

A large invasive consumer reduces coastal ecosystem resilience by disabling positive species interactions.

Invasive consumers can cause extensive ecological damage to native communities but effects on ecosystem resilience are less understood. Here, we use drone surveys, manipulative experiments, and mathematical models to show how feral hogs reduce resilience in southeastern US salt marshes by dismantling an essential marsh cordgrass-ribbed mussel mutualism. Mussels usually double plant growth and enhance marsh resilience to extreme drought but, when hogs invade, switch from being essential for plant survival to a liability; hogs selectively forage in mussel-rich areas leading to a 50% reduction in plant biomass and slower post-drought recovery rate. Hogs increase habitat fragmentation across landscapes by maintaining large, disturbed areas through trampling of cordgrass during targeted mussel consumption. Experiments and climate-disturbance recovery models show trampling alone slows marsh recovery by 3x while focused mussel predation creates marshes that may never recover from large-scale disturbances without hog eradication. Our work highlights that an invasive consumer can reshape ecosystems not just via competition and predation, but by disrupting key, positive species interactions that underlie resilience to climatic disturbances.

Mussels drive polychlorinated biphenyl (PCB) biomagnification in a coastal food web.

Despite international regulation, polychlorinated biphenyls (PCBs) are routinely detected at levels threatening human and environmental health. While previous research has emphasized trophic transfer as the principle pathway for PCB accumulation, our study reveals the critical role that non-trophic interactions can play in controlling PCB bioavailability and biomagnification. In a 5-month field experiment manipulating saltmarsh macro-invertebrates, we show that suspension-feeding mussels increase concentrations of total PCBs and toxic dioxin-like coplanars by 11- and 7.5-fold in sediment and 10.5- and 9-fold in cordgrass-grazing crabs relative to no-mussel controls, but do not affect PCB bioaccumulation in algae-grazing crabs. PCB homolog composition and corroborative dietary analyses demonstrate that mussels, as ecosystem engineers, amplify sediment contamination and PCB exposure for this burrowing marsh crab through non-trophic mechanisms. We conclude that these ecosystem engineering activities and other non-trophic interactions may have cascading effects on trophic biomagnification pathways, and therefore exert strong bottom-up control on PCB biomagnification up this coastal food web.

Sea-level rise and the emergence of a keystone grazer alter the geomorphic evolution and ecology of southeast US salt marshes.

Keystone species have large ecological effects relative to their abundance and have been identified in many ecosystems. However, global change is pervasively altering environmental conditions, potentially elevating new species to keystone roles. Here, we reveal that a historically innocuous grazer-the marsh crab Sesarma reticulatum-is rapidly reshaping the geomorphic evolution and ecological organization of southeastern US salt marshes now burdened by rising sea levels. Our analyses indicate that sea-level rise in recent decades has widely outpaced marsh vertical accretion, increasing tidal submergence of marsh surfaces, particularly where creeks exhibit morphologies that are unable to efficiently drain adjacent marsh platforms. In these increasingly submerged areas, cordgrass decreases belowground root:rhizome ratios, causing substrate hardness to decrease to within the optimal range for Sesarma burrowing. Together, these bio-physical changes provoke Sesarma to aggregate in high-density grazing and burrowing fronts at the heads of tidal creeks (hereafter, creekheads). Aerial-image analyses reveal that resulting "Sesarma-grazed" creekheads increased in prevalence from 10 ± 2% to 29 ± 5% over the past <25 y and, by tripling creek-incision rates relative to nongrazed creekheads, have increased marsh-landscape drainage density by 8 to 35% across the region. Field experiments further demonstrate that Sesarma-grazed creekheads, through their removal of vegetation that otherwise obstructs predator access, enhance the vulnerability of macrobenthic invertebrates to predation and strongly reduce secondary production across adjacent marsh platforms. Thus, sea-level rise is creating conditions within which Sesarma functions as a keystone species that is driving dynamic, landscape-scale changes in salt-marsh geomorphic evolution, spatial organization, and species interactions.

Geomorphology and Species Interactions Control Facilitation Cascades in a Salt Marsh Ecosystem.

Facilitation cascades are chains of positive interactions that occur as frequently as trophic cascades and are equally important drivers of ecosystem function, where they involve the overlap of primary and secondary, or dependent, habitat-forming foundation species [1]. Although it is well recognized that the size and configuration of secondary foundation species' patches are critical features modulating the ecological effects of facilitation cascades [2], the mechanisms governing their spatial distribution are often challenging to discern given that they operate across multiple spatial and temporal scales [1, 3]. We therefore combined regional surveys of southeastern US salt marsh geomorphology and invertebrate communities with a predator exclusion experiment to elucidate the drivers, both geomorphic and biotic, controlling the establishment, persistence, and ecosystem functioning impacts of a regionally abundant facilitation cascade involving habitat-forming marsh cordgrass and aggregations of ribbed mussels. We discovered a hierarchy of physical and biological factors predictably controlling the strength and self-organization of this facilitation cascade across creekshed, landscape, and patch scales. These results significantly enhance our capacity to spatially predict coastal ecosystem function across scales based on easily identifiable metrics of geomorphology that are mechanistically linked to ecological processes. Replication of this approach across vegetated coastal ecosystems has the potential to support management efforts by elucidating the multi-scale linkages between geomorphology and ecology that, in turn, define spatially explicit patterns in community assembly and ecosystem functioning.

Optimizing coastal restoration with the stress gradient hypothesis.

Restoration efforts have been escalating worldwide in response to widespread habitat degradation. However, coastal restoration attempts notoriously vary in their ability to establish resilient, high-functioning ecosystems. Conventional restoration attempts disperse transplants in competition-minimizing arrays, yet recent studies suggest that clumping transplants to maximize facilitative interactions may improve restoration success. Here, we modify the stress gradient hypothesis to generate predictions about where each restoration design will perform best across environmental stress gradients. We then test this conceptual model with field experiments manipulating transplant density and configuration across dune elevations and latitudes. In hurricane-damaged Georgia (USA) dunes, grass transplanted in competition-minimizing (low-density, dispersed) arrays exhibited the highest growth, resilience to disturbance and dune formation in low-stress conditions. In contrast, transplants survived best in facilitation-maximizing (high-density, clumped) arrays in high-stress conditions, but these benefits did not translate to higher transplant growth or resilience. In a parallel experiment in Massachusetts where dune grasses experience frequent saltwater inundation, fewer transplants survived, suggesting that there are thresholds above which intraspecific facilitation cannot overcome local stressors. These results suggest that ecological theory can be used to guide restoration strategies based on local stress regimes, maximizing potential restoration success and return-on-investment of future efforts.

Foundation species patch configuration mediates salt marsh biodiversity, stability and multifunctionality.

Foundation species enhance biodiversity and multifunctionality across many systems; however, whether foundation species patch configuration mediates their ecological effects is unknown. In a 6-month field experiment, we test which attributes of foundation species patch configuration - i.e. patch size, total patch area, perimeter, area-perimeter ratio, or connectivity - control biodiversity, stability and multifunctionality by adding a standardised density of mussel foundation species in patches of 1, 5, 10, 30, 60, 90 or 180 individuals to a southeastern US salt marsh. Over 67% of response variables increased with clustering of mussels, responses that were driven by increases in area-perimeter ratio (33%), decreases in perimeter (29%), or increases in patch size (5%), suggesting sensitivity to external stressors and/or dependence on foundation species-derived niche availability and segregation. Thus, mussel configuration - by controlling the relative distribution of multidimensional patch interior and edge niche space - critically modulates this foundation species' effects on ecosystem structure, stability and function.

A natural history model of New England salt marsh die-off.

Natural history gave birth to ecology and evolutionary biology, but today its importance is sometimes marginalized. Natural history provides context for ecological research, a concept that we illustrate using a consumer-driven vegetation die-off case study. For three decades, local predator depletion promoted the formation of high-density crab (Sesarma reticulatum) grazing and burrowing fronts, resulting in the spread of vegetation die-off through southern New England and Long Island marshes. We review results from a decade of research on this phenomenon and synthesize these findings with new field surveys, experiments, and historical reconstructions to test the hypothesis that the locations and processes of vegetation die-off and recovery are spatially predictable. We discovered that crab-driven die-off consistently begins on marsh creek heads, where peat and high flow conditions overlap, before spreading to inner creeks following peat availability, stunted cordgrass, and flow. Eventually, die-off eliminates most low marsh vegetation, leaving behind unvegetated substrate too soft to support burrows. Vegetation recovery exhibits the reverse patterns of die-off; it consistently begins in the low marsh within inner creeks, where soft substrate and low flow conditions overlap, before spreading to creek heads. This spatially explicit, substrate-dependent recovery eventually leads to ungrazed cordgrass abutting grazed cordgrass on the high marsh border. We present a conceptual model of die-off through recovery progression to provide managers and landowners with a diagnostic tool for identifying marsh die-off and recovery status. Collectively, this work illustrates the fundamental importance of long-term, natural history-based investigations of ecosystem dynamics in informing ecology, conservation, and management practices.

Multiple stressors and the potential for synergistic loss of New England salt marshes.

Climate change and other anthropogenic stressors are converging on coastal ecosystems worldwide. Understanding how these stressors interact to affect ecosystem structure and function has immediate implications for coastal planning, however few studies quantify stressor interactions. We examined past and potential future interactions between two leading stressors on New England salt marshes: sea-level rise and marsh crab (Sesarma reticulatum) grazing driven low marsh die-off. Geospatial analyses reveal that crab-driven die-off has led to an order of magnitude more marsh loss than sea-level rise between 2005 and 2013. However, field transplant experimental results suggest that sea-level rise will facilitate crab expansion into higher elevation marsh platforms by inundating and gradually softening now-tough high marsh peat, exposing large areas to crab-driven die-off. Taking interactive effects of marsh softening and concomitant overgrazing into account, we estimate that even modest levels of sea-level rise will lead to levels of salt marsh habitat loss that are 3x greater than the additive effects of sea-level rise and crab-driven die-off would predict. These findings highlight the importance of multiple stressor studies in enhancing mechanistic understanding of ecosystem vulnerabilities to future stress scenarios and encourage managers to focus on ameliorating local stressors to break detrimental synergisms, reduce future ecosystem loss, and enhance ecosystem resilience to global change.

Direct and indirect trophic effects of predator depletion on basal trophic levels.

Human population growth and development have heavily degraded coastal ecosystems with cascading impacts across multiple trophic levels. Understanding both the direct and indirect trophic effects of human activities is important for coastal conservation. In New England, recreational overfishing has triggered a regional trophic cascade. Predator depletion releases the herbivorous purple marsh crab from consumer control and leads to overgrazing of marsh cordgrass and salt marsh die-off. The direct and indirect trophic effects of predator depletion on basal trophic levels, however, are not understood. Using observational and experimental data, we examined the hypotheses that (1) direct trophic effects of predator depletion decrease meiofaunal abundance by releasing deposit feeding fiddler crabs from consumer control, and/or (2) indirect trophic effects of predator depletion increase meiofaunal abundance by releasing blue carbon via the erosion of centuries of accreted marsh peat. Experimental deposit feeder removal led to 23% higher meiofaunal density at die-off than at healthy sites, while reciprocally transplanting sediment from die-off and healthy sites revealed that carbon-rich die-off sediment increased meiofauna density by over 164%: six times stronger than direct trophic effects. Recovering sites had both carbon-rich sediment and reduced deposit feeding leading to higher meiofauna densities than both die-off and healthy sites. This suggests that consequences of the trophic downgrading of coastal habitats can be driven by both direct and indirect trophic mechanisms that may vary in direction and magnitude, making their elucidation dependent on experimental manipulations.

Positive interactions expand habitat use and the realized niches of sympatric species.

Niche theory, the oldest, most established community assembly model, predicts that in sympatry, the realized niche will contract due to negative interspecific interactions, but fails to recognize the effects of positive interactions on community assembly. The stress gradient hypothesis predicts that positive interactions expand realized niches in stressful habitats. We tested the predictions of the stress gradient hypothesis in a cobble beach model system across both physical and biological stress gradients. We transplanted seven common littoral species within, adjacent to, and below Spartina alterniflora cordgrass stands in control, cage control, predator exclusion cage, shade, and shaded predator exclusion cage treatments to test the hypothesis that cordgrass expands intertidal organism habitats. On cobble beaches, cordgrass ameliorates physical and predation stresses, expanding the distribution and realized niches of species to habitats in which they cannot live without facilitation, suggesting that niche theory and species distribution models should be amended to accommodate the role of positive interactions in community assembly.

Indirect human impacts turn off reciprocal feedbacks and decrease ecosystem resilience.

Creek bank salt marsh die-off is a conservation problem in New England, driven by predator depletion, which releases herbivores from consumer control. Many marshes, however, have begun to recover from die-off. We examined the hypothesis that the loss of the foundation species Spartina alterniflora has decreased facilitator populations, weakening reciprocal positive plant/animal feedbacks, resilience, and slowing recovery. Field surveys and experiments revealed that loss of Spartina leads to decreased biodiversity, and increased mortality and decreased growth of the ribbed mussel Geukensia demissa, a key facilitator of Spartina. Experimental addition of Geukensia facilitators to creek banks accelerated Spartina recovery, showing that their loss limits recovery and the reciprocal feedbacks that drive community resilience. Reciprocal positive feedbacks involving foundation species, often lost to human impacts, may be a common, but generally overlooked mechanism of ecosystem resilience, making their reestablishment a valuable restoration tool.

Experimental predator removal causes rapid salt marsh die-off.

Salt marsh habitat loss to vegetation die-offs has accelerated throughout the western Atlantic in the last four decades. Recent studies have suggested that eutrophication, pollution and/or disease may contribute to the loss of marsh habitat. In light of recent evidence that predators are important determinants of marsh health in New England, we performed a total predator exclusion experiment. Here, we provide the first experimental evidence that predator depletion can cause salt marsh die-off by releasing the herbivorous crab Sesarma reticulatum from predator control. Excluding predators from a marsh ecosystem for a single growing season resulted in a >100% increase in herbivory and a >150% increase in unvegetated bare space compared to plots with predators. Our results confirm that marshes in this region face multiple, potentially synergistic threats.

Herbivory drives the spread of salt marsh die-off.

Salt marsh die-off is a Western Atlantic conservation problem that has recently spread into Narragansett Bay, Rhode Island, USA. It has been hypothesized to be driven by: 1) eutrophication decreasing plant investment into belowground biomass causing plant collapse, 2) boat wakes eroding creek banks, 3) pollution or disease affecting plant health, 4) substrate hardness controlling herbivorous crab distributions and 5) trophic dysfunction releasing herbivorous crabs from predator control. To distinguish between these hypotheses we quantified these variables at 14 Narragansett Bay salt marshes where die-off intensity ranged from <5% to nearly 98%. Nitrogen availability, wave intensity and plant growth did not explain any variation in die-off. Herbivory explained 73% of inter-site variation in die-off and predator control of herbivores and substrate hardness also varied significantly with die-off. This suggests that salt marsh die-off is being largely driven by intense herbivory via the release of herbivorous crabs from predator control. Our results and those from other marsh systems suggest that consumer control may not simply be a factor to consider in marsh conservation, but with widespread predator depletion impacting near shore habitats globally, trophic dysfunction and runaway consumption may be the largest and most urgent management challenge for salt marsh conservation.