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.

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.

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.

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.

An invasive species erodes the performance of coastal wetland protected areas.

The world has increasingly relied on protected areas (PAs) to rescue highly valued ecosystems from human activities, but whether PAs will fare well with bioinvasions remains unknown. By analyzing three decades of seven of the largest coastal PAs in China, including World Natural Heritage and/or Wetlands of International Importance sites, we show that, although PAs are achieving success in rescuing iconic wetlands and critical shorebird habitats from once widespread reclamation, this success is counteracted by escalating plant invasions. Plant invasions were not only more extensive in PAs than non-PA controls but also undermined PA performance by, without human intervention, irreversibly replacing expansive native wetlands (primarily mudflats) and precluding successional formation of new native marshes. Exotic species are invading PAs globally. This study across large spatiotemporal scales highlights that the consequences of bioinvasions for humanity's major conservation tool may be more profound, far reaching, and critical for management than currently recognized.

Consumer regulation of the carbon cycle in coastal wetland ecosystems.

Despite escalating anthropogenic alteration of food webs, how the carbon cycle in ecosystems is regulated by food web processes remains poorly understood. We quantitatively synthesize the effects of consumers (herbivores, omnivores and carnivores) on the carbon cycle of coastal wetland ecosystems, 'blue carbon' ecosystems that store the greatest amount of carbon per unit area among all ecosystems. Our results reveal that consumers strongly affect many processes of the carbon cycle. Herbivores, for example, generally reduce carbon absorption and carbon stocks (e.g. aboveground plant carbon by 53% and aboveground net primary production by 23%) but may promote some carbon emission processes (e.g. litter decomposition by 32%). The average strengths of these effects are comparable with, or even times higher than, changes driven by temperature, precipitation, nitrogen input, CO2 concentration, and plant invasions. Furthermore, consumer effects appear to be stronger on aboveground than belowground carbon processes and vary markedly with trophic level, body size, thermal regulation strategy and feeding type. Despite important knowledge gaps, our results highlight the powerful impacts of consumers on the carbon cycle and call for the incorporation of consumer control into Earth system models that predict anthropogenic climate change and into management strategies of Earth's carbon stocks. This article is part of the theme issue 'Integrative research perspectives on marine conservation'.

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.

Supporting Spartina: Interdisciplinary perspective shows Spartina as a distinct solid genus.

In 2014, a DNA-based phylogenetic study confirming the paraphyly of the grass subtribe Sporobolinae proposed the creation of a large monophyletic genus Sporobolus, including (among others) species previously included in the genera Spartina, Calamovilfa, and Sporobolus. Spartina species have contributed substantially (and continue contributing) to our knowledge in multiple disciplines, including ecology, evolutionary biology, molecular biology, biogeography, experimental ecology, biological invasions, environmental management, restoration ecology, history, economics, and sociology. There is no rationale so compelling to subsume the name Spartina as a subgenus that could rival the striking, global iconic history and use of the name Spartina for over 200 yr. We do not agree with the subjective arguments underlying the proposal to change Spartina to Sporobolus. We understand the importance of both the objective phylogenetic insights and of the subjective formalized nomenclature and hope that by opening this debate we will encourage positive feedback that will strengthen taxonomic decisions with an interdisciplinary perspective. We consider that the strongly distinct, monophyletic clade Spartina should simply and efficiently be treated as the genus Spartina.

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.

Facilitative and competitive interaction components among New England salt marsh plants.

Intra- and interspecific interactions can be broken down into facilitative and competitive components. The net interaction between two organisms is simply the sum of these counteracting elements. Disentangling the positive and negative components of species interactions is a critical step in advancing our understanding of how the interaction between organisms shift along physical and biotic gradients. We performed a manipulative field experiment to quantify the positive and negative components of the interactions between a perennial forb, Aster tenuifolius, and three dominant, matrix-forming grasses and rushes in a New England salt marsh. Specifically, we asked whether positive and negative interaction components: (1) are unique or redundant across three matrix-forming species (two grasses; Distichlis spicata and Spartina patens, and one rush; Juncus gerardi), and (2) change across Aster life stages (seedling, juvenile, and adult). For adult Aster the strength of the facilitative component of the matrix-forb interaction was stronger than the competitive component for two of the three matrix species, leading to net positive interactions. There was no statistically significant variation among matrix species in their net or component effects. We found little difference in the effects of J. gerardi on Aster at later life-history stages; interaction component strengths did not differ between juveniles and adults. However, mortality of seedlings in neighbor removal plots was 100%, indicating a particularly strong and critical facilitative effect of matrix species on this forb during the earliest life stages. Overall, our results indicate that matrix forming grasses and rushes have important, yet largely redundant, positive net effects on Aster performance across its life cycle. Studies that untangle various components of interactions and their contingencies are critical to both expanding our basic understanding of community organization, and predicting how natural communities and their component parts will respond to environmental change.

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.

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.

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.

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.

Economic development and coastal ecosystem change in China.

Despite their value, coastal ecosystems are globally threatened by anthropogenic impacts, yet how these impacts are driven by economic development is not well understood. We compiled a multifaceted dataset to quantify coastal trends and examine the role of economic growth in China's coastal degradation since the 1950s. Although China's coastal population growth did not change following the 1978 economic reforms, its coastal economy increased by orders of magnitude. All 15 coastal human impacts examined increased over time, especially after the reforms. Econometric analysis revealed positive relationships between most impacts and GDP across temporal and spatial scales, often lacking dropping thresholds. These relationships generally held when influences of population growth were addressed by analyzing per capita impacts, and when population density was included as explanatory variables. Historical trends in physical and biotic indicators showed that China's coastal ecosystems changed little or slowly between the 1950s and 1978, but have degraded at accelerated rates since 1978. Thus economic growth has been the cause of accelerating human damage to China's coastal ecosystems. China's GDP per capita remains very low. Without strict conservation efforts, continuing economic growth will further degrade China's coastal ecosystems.

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.

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.