Long-distance facilitation of coastal ecosystem structure and resilience.

Biotic interactions that hierarchically organize ecosystems by driving ecological and evolutionary processes across spatial scales are ubiquitous in our biosphere. Biotic interactions have been extensively studied at local and global scales, but how long-distance, cross-ecosystem interactions at intermediate landscape scales influence the structure, function, and resilience of ecological systems remains poorly understood. We used remote sensing, modeling, and field data to test the hypothesis that the long-distance impact of an invasive species dramatically affects one of the largest tidal flat ecosystems in East Asia. We found that the invasion of exotic cordgrass Spartina alterniflora can produce long-distance effects on native species up to 10 km away, driving decadal coastal ecosystem transitions. The invasive cordgrass at low elevations facilitated the expansion of the native reed Phragmites australis at high elevations, leading to the massive loss and reduced resilience of the iconic Suaeda salsa "Red Beach" marshes at intermediate elevations, largely as a consequence of reduced soil salinity across the landscape. Our results illustrate the complex role that long-distance interactions can play in shaping landscape structure and ecosystem resilience and in bridging the gap between local and global biotic interactions.

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.

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.

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.

Bottom-up and top-down human impacts interact to affect a protected coastal Chilean marsh.

Many ecosystems, even in protected areas, experience multiple anthropogenic impacts. While anthropogenic modification of bottom-up (e.g., eutrophication) and top-down (e.g., livestock grazing) forcing often co-occurs, whether these factors counteract or have additive or synergistic effects on ecosystems is poorly understood. In a Chilean bio-reserve, we examined the interactive impacts of eutrophication and illegal livestock grazing on plant growth with a 4-yr fertilization by cattle exclusion experiment. Cattle grazing generally decreased plant biomass, but had synergistic, additive, and antagonistic interactions with fertilization in the low, middle, and high marsh zones, respectively. In the low marsh, fertilization increased plant biomass by 112%, cattle grazing decreased it by 96%, and together they decreased plant biomass by 77%. In the middle marsh, fertilization increased plant biomass by 47%, cattle grazing decreased it by 37%, and together they did not affect plant biomass. In the high marsh, fertilization and cattle grazing decreased plant biomass by 81% and 92%, respectively, but together they increased plant biomass by 42%. These interactions were also found to be species specific. Different responses of plants to fertilization and cattle grazing were likely responsible for these variable interactions. Thus, common bottom-up and top-down human impacts can interact in different ways to affect communities even within a single ecosystem. Incorporating this knowledge into conservation actions will improve ecosystem management in a time when ecosystems are increasingly challenged by multiple interacting human impacts.

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.

Flowering and biomass allocation in U.S. Atlantic coast Spartina alterniflora.

PREMISE OF THE STUDY: Salt marshes are highly productive and valuable ecosystems, providing many services on which people depend. Spartina alterniflora Loisel (Poaceae) is a foundation species that builds and maintains salt marshes. Despite this species' importance, much of its basic reproductive biology is not well understood, including flowering phenology, seed production, and the effects of flowering on growth and biomass allocation. We sought to better understand these life history traits and use that knowledge to consider how this species may be affected by climate change. METHODS: We examined temporal and spatial patterns in flowering and seed production in S. alterniflora at a latitudinal scale (along the U.S. Atlantic coast), regional scale (within New England), and local scale (among subhabitats within marshes) and determined the impact of flowering on growth allocation using field and greenhouse studies. KEY RESULTS: Flowering stem density did not vary along a latitudinal gradient, while at the local scale plants in the less submerged panne subhabitats produced fewer flowers and seeds than those in more frequently submerged subhabitats. We also found that a shift in biomass allocation from above to belowground was temporally related to flowering phenology. CONCLUSIONS: We expect that environmental change will affect seed production and that the phenological relationship with flowering will result in limitations to belowground production and thus affect marsh elevation gain. Salt marshes provide an excellent model system for exploring the interactions between plant ecology and ecosystem functioning, enabling better predictions of climate change impacts.

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.

Extreme stresses, niches, and positive species interactions along stress gradients.

Since proposed two decades ago, the stress-gradient hypothesis (SGH), suggesting that species interactions shift from competition to facilitation with stress, has been widely examined. Despite broad support across species and ecosystems, ecologists debate whether the SGH applies to extreme environments, arguing that species interactions switch to competition or collapse under extreme stress. We show that facilitation often expands distributions on species borders. SGH exceptions occur when weak stress gradients or stresses outside of species' niches are examined, multiple stresses co-occur canceling out their effects, temporally dependent effects are involved, or results are improperly analyzed. We suggest that ecologists resolve debates by standardizing key SGH terms, such as fundamental and realized niche, stress gradients vs. environmental gradients, by quantitatively defining extreme stress, and by critically evaluating the functionality of stress gradients. We also suggest that new research examine the breadth and relevance of the SGH. More rigor needs to be applied to SGH tests to identify actual exceptions rather than those due to failures to meet its underlying assumptions, so that the general principles of the SGH and its exceptions can be incorporated into ecological theory, conservation strategies, and environmental change predictions.

Dead foundation species drive ecosystem dynamics.

Foundation species facilitate communities, modulate energy flow, and define ecosystems, but their ecological roles after death are frequently overlooked. Here, we reveal the widespread importance of their dead structures as unique, interacting components of ecosystems that are vulnerable to global change. Key metabolic activity, mobility, and morphology traits of foundation species either change or persist after death with important consequences for ecosystem functions, biodiversity, and subsidy dynamics. Dead foundation species frequently mediate ecosystem stability, resilience, and transitions, often through feedbacks, and harnessing their structural and trophic roles can improve restoration outcomes. Enhanced recognition of dead foundation species and their incorporation into habitat monitoring, ecological theory, and ecosystem forecasting can help solve the escalating conservation challenges of the Anthropocene.

Harnessing ecological theory to enhance ecosystem restoration.

Ecosystem restoration can increase the health and resilience of nature and humanity. As a result, the international community is championing habitat restoration as a primary solution to address the dual climate and biodiversity crises. Yet most ecosystem restoration efforts to date have underperformed, failed, or been burdened by high costs that prevent upscaling. To become a primary, scalable conservation strategy, restoration efficiency and success must increase dramatically. Here, we outline how integrating ten foundational ecological theories that have not previously received much attention - from hierarchical facilitation to macroecology - into ecosystem restoration planning and management can markedly enhance restoration success. We propose a simple, systematic approach to determining which theories best align with restoration goals and are most likely to bolster their success. Armed with a century of advances in ecological theory, restoration practitioners will be better positioned to more cost-efficiently and effectively rebuild the world's ecosystems and support the resilience of our natural resources.

Global shifts towards positive species interactions with increasing environmental stress.

The study of positive species interactions is a rapidly evolving field in ecology. Despite decades of research, controversy has emerged as to whether positive and negative interactions predictably shift with increasing environmental stress as hypothesised by the stress-gradient hypothesis (SGH). Here, we provide a synthesis of 727 tests of the SGH in plant communities across the globe to examine its generality across a variety of ecological factors. Our results show that plant interactions change with stress through an outright shift to facilitation (survival) or a reduction in competition (growth and reproduction). In a limited number of cases, plant interactions do not respond to stress, but they never shift towards competition with stress. These findings are consistent across stress types, plant growth forms, life histories, origins (invasive vs. native), climates, ecosystems and methodologies, though the magnitude of the shifts towards facilitation with stress is dependent on these factors. We suggest that future studies should employ standardised definitions and protocols to test the SGH, take a multi-factorial approach that considers variables such as plant traits in addition to stress, and apply the SGH to better understand how species and communities will respond to environmental change.

An invasive species facilitates the recovery of salt marsh ecosystems on Cape Cod.

With global increases in human impacts, invasive species have become a major threat to ecosystems worldwide. While they have been traditionally viewed as harmful, invasive species may facilitate the restoration of degraded ecosystems outside their native ranges. In New England (USA) overfishing has depleted salt marsh predators, allowing the herbivorous crab Sesarma reticulatum to denude hundreds of hectares of low marsh. Here, using multiple site surveys and field caging experiments, we show that the subsequent invasion of green crabs, Carcinus maenas, into heavily burrowed marshes partially reverses decades of cordgrass die-off. By consuming Sesarma, eliciting a nonlethal escape response, and evicting Sesarma from burrows, Carcinus reduces Sesarma herbivory and promotes cordgrass recovery. These results suggest that invasive species can contribute to restoring degraded ecosystems and underscores the potential for invasive species to return ecological functions lost to human impacts.

Feedbacks underlie the resilience of salt marshes and rapid reversal of consumer-driven die-off.

Understanding ecosystem resilience to human impacts is critical for conservation and restoration. The large-scale die-off of New England salt marshes was triggered by overfishing and resulted from decades of runaway crab grazing. In 2009, however, cordgrass began to recover, decreasing die-off -40% by 2010. We used surveys and experiments to test whether plant-substrate feedbacks underlie marsh resilience. Initially, grazer-generated die-off swept through the cordgrass, creating exposed, stressful peat banks that inhibited plant growth. This desertification cycle broke when banks eroded and peat transitioned into mud with fewer herbivores, less grazing, and lower physical stress. Cordgrass reestablished in these areas through a feedback where it engineered a recovery zone by further ameliorating physical stresses and facilitating additional revegetation. Our results reveal that feedbacks can play a critical role in rapid, reversible ecosystem shifts associated with human impacts, and that the interplay of facilitative and consumer interactions should be incorporated into resilience theory.

Regional ontogeny of New England salt marsh die-off.

Coastal areas are among the world's most productive and highly affected ecosystems. Centuries of human activity on coastlines have led to overexploitation of marine predators, which in turn has led to cascading ecosystem-level effects. Human effects and approaches to mediating them, however, differ regionally due to gradients in biotic and abiotic factors. Salt marsh die-off on Cape Cod, Massachusetts (U.S.A.), triggered by a recreational-fishing-induced trophic cascade that has released herbivorous crabs from predator control, has been ongoing since 1976. Similar salt marsh die-offs have been reported in Long Island Sound and Narragansett Bay (U.S.A.), but the driving mechanism of these die-offs has not been examined. We used field experiments to assess trophic interactions and historical reconstructions of 24 New England marshes to test the hypotheses that recreational fishing and predator depletion are a regional trigger of salt marsh die-off in New England and that die-offs in Long Island Sound and Narragansett Bay are more recent than those on Cape Cod. Predator depletion was the general trigger of marsh die-off and explained differences in herbivorous crab abundance and the severity of die-off across regions. Die-offs in Long Island Sound and Narragansett Bay are following a trajectory similar to die-off on Cape Cod, but are approximately 20 years behind those on Cape Cod. As a result, die-off currently affects 31.2% (SE 2.2) of low-marsh areas in Long Island Sound and Narragansett Bay, less than half the severity of die-off on Cape Cod. Our results contribute to the growing evidence that recreational fishing is an increasing threat to coastal ecosystems and that studying the effects of human activity at regional scales can provide insight into local effects and aid in early detection and potential remediation.

Shorebirds-driven trophic cascade helps restore coastal wetland multifunctionality.

Ecosystem restoration has traditionally focused on re-establishing vegetation and other foundation species at basal trophic levels, with mixed outcomes. Here, we show that threatened shorebirds could be important to restoring coastal wetland multifunctionality. We carried out surveys and manipulative field experiments in a region along the Yellow Sea affected by the invasive cordgrass Spartina alterniflora. We found that planting native plants alone failed to restore wetland multifunctionality in a field restoration experiment. Shorebird exclusion weakened wetland multifunctionality, whereas mimicking higher predation before shorebird population declines by excluding their key prey - crab grazers - enhanced wetland multifunctionality. The mechanism underlying these effects is a simple trophic cascade, whereby shorebirds control crab grazers that otherwise suppress native vegetation recovery and destabilize sediments (via bioturbation). Our findings suggest that harnessing the top-down effects of shorebirds - through habitat conservation, rewilding, or temporary simulation of consumptive or non-consumptive effects - should be explored as a nature-based solution to restoring the multifunctionality of degraded coastal wetlands.

Testing the importance of plant strategies on facilitation using congeners in a coastal community.

Much is known about how environmental stress mediates the strength of facilitation, but less is known about how different plant traits affect facilitation. We examined interactions between the shrub Tamarix chinensis and two congeneric forbs (Suaeda salsa and S. glauca) on the Chinese coast. Although S. salsa and S. glauca are both annuals, morphologically similar, and have synchronous phenologies, they have contrasting adaptive strategies. S. glauca is salt intolerant but competitively superior, and S. salsa is salt tolerant but competitively inferior. Field surveys showed that S. glauca was associated with T. chinensis canopies while S. salsa was more abundant in open areas. A T. chinensis removal experiment showed that S. glauca cover was lower and soil salinity higher after two years in removal than in control plots. Transplant experiments showed that S. salsa performance under T. chinensis canopies was reduced by competition from S. glauca and T. chinensis, while in open areas S. glauca was not affected by S. salsa competition. Thus, contrasting competitive abilities and stress tolerances of S. glauca and S. salsa underlie their facilitative and competitive interactions with T. chinensis, suggesting that plant strategies are critical to the outcome of species interactions.

Belowground herbivory increases vulnerability of New England salt marshes to die-off.

Belowground herbivory is commonly overlooked as a mechanism of top-down control in vegetated habitats, particularly in aquatic ecosystems. Recent research has revealed that increased densities of the herbivorous crab Sesarma reticulatum have led to runaway herbivory and widespread salt marsh die-off on Cape Cod, Massachusetts, USA. Aboveground herbivory is a major driver of this cordgrass habitat loss, but the role of belowground grazing is poorly understood. Sesarma live in communal burrows typically consisting of 1-2 openings and containing 2-3 crabs. However, at die-off sites, burrow complexes can cover > 90% of the low marsh zone, with crab densities as high as 50 crabs/m2 and burrow opening densities of 170 openings/m2. The magnitude of belowground Sesarma activity in association with salt marsh die-off provides an excellent opportunity to extend our knowledge of belowground herbivory impacts in coastal wetlands. Since Sesarma burrows allow access to cordgrass roots and rhizomes, and Sesarma are frequently restricted to burrows by thermal stress and predation, we hypothesized that belowground herbivory would be widespread in die-off areas. We experimentally demonstrate that Sesarma readily eat belowground roots and rhizomes in addition to aboveground cordgrass leaves. We then partitioned above- and belowground herbivory with field manipulations and found that belowground grazing is not only common, but can cause total plant mortality. Additional experiments revealed that plants remain vulnerable to belowground herbivory even after reaching a size refuge from aboveground grazing. This suggests that belowground herbivory contributes to salt marsh die-offs and adds to growing evidence that belowground herbivory is a widespread structuring force in plant communities that can limit habitat persistence.

A trophic cascade triggers collapse of a salt-marsh ecosystem with intensive recreational fishing.

Overexploitation of predators has been linked to the collapse of a growing number of shallow-water marine ecosystems. However, salt-marsh ecosystems are often viewed and managed as systems controlled by physical processes, despite recent evidence for herbivore-driven die-off of marsh vegetation. Here we use field observations, experiments, and historical records at 14 sites to examine whether the recently reported die-off of northwestern Atlantic salt marshes is associated with the cascading effects of predator dynamics and intensive recreational fishing activity. We found that the localized depletion of top predators at sites accessible to recreational anglers has triggered the proliferation of herbivorous crabs, which in turn results in runaway consumption of marsh vegetation. This suggests that overfishing may be a general mechanism underlying the consumer-driven die-off of salt marshes spreading throughout the western Atlantic. Our findings support the emerging realization that consumers play a dominant role in regulating marine plant communities and can lead to ecosystem collapse when their impacts are amplified by human activities, including recreational fishing.