Shifts in the coral microbiome in response to in situ experimental deoxygenation.

IMPORTANCE: Marine hypoxia is a threat for corals but has remained understudied in tropical regions where coral reefs are abundant. Though microbial symbioses can alleviate the effects of ecological stress, we do not yet understand the taxonomic or functional response of the coral microbiome to hypoxia. In this study, we experimentally lowered oxygen levels around Siderastrea siderea and Agaricia lamarcki colonies in situ to observe changes in the coral microbiome in response to deoxygenation. Our results show that hypoxia triggers a stochastic change of the microbiome overall, with some bacterial families changing deterministically after just 48 hours of exposure. These families represent an increase in anaerobic and opportunistic taxa in the microbiomes of both coral species. Thus, marine deoxygenation destabilizes the coral microbiome and increases bacterial opportunism. This work provides novel and fundamental knowledge of the microbial response in coral during hypoxia and may provide insight into holobiont function during stress.

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.

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

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

Governance and the mangrove commons: Advancing the cross-scale, nested framework for the global conservation and wise use of mangroves.

Mangroves provide critical ecosystems services, contributing an estimated 42 billion US dollars to global fisheries, storing 25.5 million tons of carbon per year, and providing flood protection to over 15 million people annually. Yet, they are increasingly threatened by factors ranging from local resource exploitation to global climate change, with an estimated 35% of mangrove forests lost in the past two decades. These threats are difficult to manage due to the intrinsic characteristics of mangrove systems and their provisioning services, and their transboundary and pan-global nature. Due to their unique intertidal ecological niche, mangroves are often treated as a "common pool resource" within national legal frameworks, making them particularly susceptible to exploitation. Moreover, they form ecological connections through numerous biotic and abiotic processes that cross political boundaries. Because of these qualities a cross-scale nested framework of international, regional, and local coordination is necessary to successfully sustain mangrove ecosystems and their valuable services. Although coordination across the geopolitical spectrum is often cited as a need for effective management of common resources such as mangroves, there has been no formal analysis of mangrove multiscale governance. In this paper we address this gap by providing a comprehensive analysis of interactions between and within international, regional, and local mangrove management regimes and examine the challenges and opportunities such multiscale governance frameworks present. We highlight Costa Rica as a case study to demonstrate the universal relevance and potential of multi-scale governance and explore its downscale potential. Using Elinor Ostrom's principles for self-governance of the commons as our touchstone, we identify where improvements to the status quo could be implemented to increase its effectiveness of the current frameworks to meet the ongoing challenge of managing mangrove-derived resources and services in the face of a changing climate and human needs.

Tropical dead zones and mass mortalities on coral reefs.

Degradation of coastal water quality in the form of low dissolved oxygen levels (hypoxia) can harm biodiversity, ecosystem function, and human wellbeing. Extreme hypoxic conditions along the coast, leading to what are often referred to as "dead zones," are known primarily from temperate regions. However, little is known about the potential threat of hypoxia in the tropics, even though the known risk factors, including eutrophication and elevated temperatures, are common. Here we document an unprecedented hypoxic event on the Caribbean coast of Panama and assess the risk of dead zones to coral reefs worldwide. The event caused coral bleaching and massive mortality of corals and other reef-associated organisms, but observed shifts in community structure combined with laboratory experiments revealed that not all coral species are equally sensitive to hypoxia. Analyses of global databases showed that coral reefs are associated with more than half of the known tropical dead zones worldwide, with >10% of all coral reefs at elevated risk for hypoxia based on local and global risk factors. Hypoxic events in the tropics and associated mortality events have likely been underreported, perhaps by an order of magnitude, because of the lack of local scientific capacity for their detection. Monitoring and management plans for coral reef resilience should incorporate the growing threat of coastal hypoxia and include support for increased detection and research capacity.

Bioerosion in a changing world: a conceptual framework.

Bioerosion, the breakdown of hard substrata by organisms, is a fundamental and widespread ecological process that can alter habitat structure, biodiversity and biogeochemical cycling. Bioerosion occurs in all biomes of the world from the ocean floor to arid deserts, and involves a wide diversity of taxa and mechanisms with varying ecological effects. Many abiotic and biotic factors affect bioerosion by acting on the bioeroder, substratum, or both. Bioerosion also has socio-economic impacts when objects of economic or cultural value such as coastal defences or monuments are damaged. We present a unifying definition and advance a conceptual framework for (a) examining the effects of bioerosion on natural systems and human infrastructure and (b) identifying and predicting the impacts of anthropogenic factors (e.g. climate change, eutrophication) on bioerosion. Bioerosion is responding to anthropogenic changes in multiple, complex ways with significant and wide-ranging effects across systems. Emerging data further underscore the importance of bioerosion, and need for mitigating its impacts, especially at the dynamic land-sea boundary. Generalised predictions remain challenging, due to context-dependent effects and nonlinear relationships that are poorly resolved. An integrative and interdisciplinary approach is needed to understand how future changes will alter bioerosion dynamics across biomes and taxa.

How habitat-modifying organisms structure the food web of two coastal ecosystems.

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.

Herbivory drives zonation of stress-tolerant marsh plants.

Ecological studies of plant distributions along environmental gradients, such as plant zonation in salt marshes, have primarily focused on abiotic stress and plant interactions (competition and facilitation). A decades-old paradigm is that the stressful and benign boundaries of salt marsh plants are determined by abiotic stress and competition, respectively. Although consumers have long been recognized as mediating algal and sessile animal zonation in the rocky intertidal, their role in generating plant zonation in salt marshes remains largely unexplored. We examined the zonation of two annual succulents, Salicornia europaea and Suaeda salsa, along an elevation gradient in a northern Chinese salt marsh, with and without manipulating the common herbivorous crab Helice tientsinensis. Salicornia occupies waterlogged, low-salinity habitats, whereas Suaeda dominates non-waterlogged, hypersaline habitats at higher elevations. We first conducted a pot experiment crossing salinity, waterlogging, and competition, followed by a field experiment with removal of competitors, and found that neither waterlogging nor salinity stress explained the absence of either species from the other's zone, while Suaeda competitively excluded Salicornia from the upper non-waterlogged zone. We then conducted field and lab herbivory experiments, which showed that Helice preferentially grazed Suaeda at waterlogged low elevations and that Helice grazing on Suaeda increased with waterlogging. These results reveal that while competition plays a role in the zonation by excluding Salicornia from the upper Suaeda zone, crab grazing limits the success of Suaeda in the lower Salicornia zone. These findings challenge the idea that plant interactions and abiotic stress are sufficient to explain marsh zonation in all cases, and highlight an overlooked role of consumers, a role potentially general across diverse intertidal ecosystems. Future models of plant distributions should consider how consumer pressure interacts with plant interactions and abiotic stress across environmental gradients.

Climate change and dead zones.

Estuaries and coastal seas provide valuable ecosystem services but are particularly vulnerable to the co-occurring threats of climate change and oxygen-depleted dead zones. We analyzed the severity of climate change predicted for existing dead zones, and found that 94% of dead zones are in regions that will experience at least a 2 °C temperature increase by the end of the century. We then reviewed how climate change will exacerbate hypoxic conditions through oceanographic, ecological, and physiological processes. We found evidence that suggests numerous climate variables including temperature, ocean acidification, sea-level rise, precipitation, wind, and storm patterns will affect dead zones, and that each of those factors has the potential to act through multiple pathways on both oxygen availability and ecological responses to hypoxia. Given the variety and strength of the mechanisms by which climate change exacerbates hypoxia, and the rates at which climate is changing, we posit that climate change variables are contributing to the dead zone epidemic by acting synergistically with one another and with recognized anthropogenic triggers of hypoxia including eutrophication. This suggests that a multidisciplinary, integrated approach that considers the full range of climate variables is needed to track and potentially reverse the spread of dead zones.

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.

Stony coral tissue loss disease indirectly alters reef communities.

Many Caribbean coral reefs are near collapse due to various threats. An emerging threat, stony coral tissue loss disease (SCTLD), is spreading across the Western Atlantic and Caribbean. Data from the U.S. Virgin Islands reveal how SCTLD spread has reduced the abundance of susceptible coral and crustose coralline algae and increased cyanobacteria, fire coral, and macroalgae. A Caribbean-wide structural equation model demonstrates versatility in reef fish and associations with rugosity independent of live coral. Model projections suggest that some reef fishes will decline due to SCTLD, with the largest changes on reefs that lose the most susceptible corals and rugosity. Mapping these projected declines in space indicates how the indirect effects of SCTLD range from undetectable to devastating.

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.

Microbiomes of Thalassia testudinum throughout the Atlantic Ocean, Caribbean Sea, and Gulf of Mexico are influenced by site and region while maintaining a core microbiome.

Plant microbiomes are known to serve several important functions for their host, and it is therefore important to understand their composition as well as the factors that may influence these microbial communities. The microbiome of Thalassia testudinum has only recently been explored, and studies to-date have primarily focused on characterizing the microbiome of plants in a single region. Here, we present the first characterization of the composition of the microbial communities of T. testudinum across a wide geographical range spanning three distinct regions with varying physicochemical conditions. We collected samples of leaves, roots, sediment, and water from six sites throughout the Atlantic Ocean, Caribbean Sea, and the Gulf of Mexico. We then analyzed these samples using 16S rRNA amplicon sequencing. We found that site and region can influence the microbial communities of T. testudinum, while maintaining a plant-associated core microbiome. A comprehensive comparison of available microbial community data from T. testudinum studies determined a core microbiome composed of 14 ASVs that consisted mostly of the family Rhodobacteraceae. The most abundant genera in the microbial communities included organisms with possible plant-beneficial functions, like plant-growth promoting taxa, disease suppressing taxa, and nitrogen fixers.

Herbivore effects increase with latitude across the extent of a foundational seagrass.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

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.

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.

A wide megafauna gap undermines China's expanding coastal ecosystem conservation.

To fulfill sustainable development goals, many countries are expanding efforts to conserve ecologically and societally critical coastal ecosystems. Although megafauna profoundly affect the functioning of ecosystems, they are neglected as a key component in the conservation scheme for coastal ecosystems in many geographic contexts. We reveal a rich diversity of extant megafauna associated with all major types of coastal ecosystems in China, including 218 species of mammals, birds, reptiles, cephalopods, and fish across terrestrial and marine environments. However, 44% of these species are globally threatened, and 78% have not yet been assessed in China for extinction risk. More worrisome, 73% of these megafauna have not been designated as nationally protected species, and <10% of their most important habitats are protected. Filling this wide "megafauna gap" in China and globally would be a leading step as humanity strives to thrive with coastal ecosystems.

Herbivory limits success of vegetation restoration globally.

Restoring vegetation in degraded ecosystems is an increasingly common practice for promoting biodiversity and ecological function, but successful implementation is hampered by an incomplete understanding of the processes that limit restoration success. By synthesizing terrestrial and aquatic studies globally (2594 experimental tests from 610 articles), we reveal substantial herbivore control of vegetation under restoration. Herbivores at restoration sites reduced vegetation abundance more strongly (by 89%, on average) than those at relatively undegraded sites and suppressed, rather than fostered, plant diversity. These effects were particularly pronounced in regions with higher temperatures and lower precipitation. Excluding targeted herbivores temporarily or introducing their predators improved restoration by magnitudes similar to or greater than those achieved by managing plant competition or facilitation. Thus, managing herbivory is a promising strategy for enhancing vegetation restoration efforts.

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.