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.

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.

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.

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.

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.

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.

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.

Negative effects of a zoanthid competitor limit coral calcification more than ocean acidification.

Ocean acidification (OA) threatens the persistence of reef-building corals and the habitat they provide. While species-specific effects of OA on marine organisms could have cascading effects on ecological interactions like competition, few studies have identified how benthic reef competitors respond to OA. We explored how two common Caribbean competitors, branching Porites and a colonial zoanthid (Zoanthus), respond to the factorial combination of OA and competition. In the laboratory, we exposed corals, zoanthids and interacting corals and zoanthids to ambient (8.01 ± 0.03) and OA (7.68 ± 0.07) conditions for 60 days. The OA treatment had no measured effect on zoanthids or coral calcification but decreased Porites maximum PSII efficiency. Conversely, the competitive interaction significantly decreased Porites calcification but had minimal-to-no countereffects on the zoanthid. Although this interaction was not exacerbated by the 60-day OA exposure, environmental changes that enhance zoanthid performance could add to the dominance of zoanthids over corals. The lack of effects of OA on coral calcification indicates that near-term competitive interactions may have more immediate consequences for some corals than future global change scenarios. Disparate consequences of competition have implications for community structure and should be accounted for when evaluating local coral reef trajectories.

The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs.

Environmental degradation has the potential to alter key mutualisms that underlie the structure and function of ecological communities. How microbial communities associated with fishes vary across populations and in relation to habitat characteristics remains largely unknown despite their fundamental roles in host nutrition and immunity. We find significant differences in the gut microbiome composition of a facultative coral-feeding butterflyfish (Chaetodon capistratus) across Caribbean reefs that differ markedly in live coral cover (∼0-30%). Fish gut microbiomes were significantly more variable at degraded reefs, a pattern driven by changes in the relative abundance of the most common taxa potentially associated with stress. We also demonstrate that fish gut microbiomes on severely degraded reefs have a lower abundance of Endozoicomonas and a higher diversity of anaerobic fermentative bacteria, which may suggest a less coral dominated diet. The observed shifts in fish gut bacterial communities across the habitat gradient extend to a small set of potentially beneficial host associated bacteria (i.e., the core microbiome) suggesting essential fish-microbiome interactions may be vulnerable to severe coral degradation.

Novel coexisting mangrove-coral habitats: Extensive coral communities located deep within mangrove canopies of Panama, a global classification system and predicted distributions.

Marine ecosystems are structured by coexisting species occurring in adjacent or nested assemblages. Mangroves and corals are typically observed in adjacent assemblages (i.e., mangrove forests and coral reefs) but are increasingly reported in nested mangrove-coral assemblages with corals living within mangrove habitats. Here we define these nested assemblages as "coexisting mangrove-coral" (CMC) habitats and review the scientific literature to date to formalize a baseline understanding of these ecosystems and create a foundation for future studies. We identify 130 species of corals living within mangrove habitats across 12 locations spanning the Caribbean Sea, Red Sea, Indian Ocean, and South Pacific. We then provide the first description, to our knowledge, of a canopy CMC habitat type located in Bocas del Toro, Panama. This canopy CMC habitat is one of the most coral rich CMC habitats reported in the world, with 34 species of corals growing on and/or among submerged red mangrove aerial roots. Based on our literature review and field data, we identify biotic and abiotic characteristics common to CMC systems to create a classification framework of CMC habitat categories: (1) Lagoon, (2) Inlet, (3) Edge, and (4) Canopy. We then use the compiled data to create a GIS model to suggest where additional CMC habitats may occur globally. In a time where many ecosystems are at risk of disappearing, discovery and description of alternative habitats for species of critical concern are of utmost importance for their conservation and management.

Predator control of marine communities increases with temperature across 115 degrees of latitude.

Early naturalists suggested that predation intensity increases toward the tropics, affecting fundamental ecological and evolutionary processes by latitude, but empirical support is still limited. Several studies have measured consumption rates across latitude at large scales, with variable results. Moreover, how predation affects prey community composition at such geographic scales remains unknown. Using standardized experiments that spanned 115° of latitude, at 36 nearshore sites along both coasts of the Americas, we found that marine predators have both higher consumption rates and consistently stronger impacts on biomass and species composition of marine invertebrate communities in warmer tropical waters, likely owing to fish predators. Our results provide robust support for a temperature-dependent gradient in interaction strength and have potential implications for how marine ecosystems will respond to ocean warming.

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.

Heterogeneity within and among co-occurring foundation species increases biodiversity.

Habitat heterogeneity is considered a primary causal driver underpinning patterns of diversity, yet the universal role of heterogeneity in structuring biodiversity is unclear due to a lack of coordinated experiments testing its effects across geographic scales and habitat types. Furthermore, key species interactions that can enhance heterogeneity, such as facilitation cascades of foundation species, have been largely overlooked in general biodiversity models. Here, we performed 22 geographically distributed experiments in different ecosystems and biogeographical regions to assess the extent to which variation in biodiversity is explained by three axes of habitat heterogeneity: the amount of habitat, its morphological complexity, and capacity to provide ecological resources (e.g. food) within and between co-occurring foundation species. We show that positive and additive effects across the three axes of heterogeneity are common, providing a compelling mechanistic insight into the universal importance of habitat heterogeneity in promoting biodiversity via cascades of facilitative interactions. Because many aspects of habitat heterogeneity can be controlled through restoration and management interventions, our findings are directly relevant to biodiversity conservation.

Differential susceptibility of reef-building corals to deoxygenation reveals remarkable hypoxia tolerance.

Ocean deoxygenation threatens the persistence of coastal ecosystems worldwide. Despite an increasing awareness that coastal deoxygenation impacts tropical habitats, there remains a paucity of empirical data on the effects of oxygen limitation on reef-building corals. To address this knowledge gap, we conducted laboratory experiments with ecologically important Caribbean corals Acropora cervicornis and Orbicella faveolata. We tested the effects of continuous exposure to conditions ranging from extreme deoxygenation to normoxia (~ 1.0 to 6.25 mg L-1 dissolved oxygen) on coral bleaching, photophysiology, and survival. Coral species demonstrated markedly different temporal resistance to deoxygenation, and within a species there were minimal genotype-specific treatment effects. Acropora cervicornis suffered tissue loss and mortality within a day of exposure to severe deoxygenation (~ 1.0 mg L-1), whereas O. faveolata remained unaffected after 11 days of continuous exposure to 1.0 mg L-1. Intermediate deoxygenation treatments (~ 2.25 mg L-1, ~ 4.25 mg L-1) elicited minimal responses in both species, indicating a low oxygen threshold for coral mortality and coral resilience to oxygen concentrations that are lethal for other marine organisms. These findings demonstrate the potential for variability in species-specific hypoxia thresholds, which has important implications for our ability to predict how coral reefs may be affected as ocean deoxygenation intensifies. With deoxygenation emerging as a critical threat to tropical habitats, there is an urgent need to incorporate deoxygenation into coral reef research, management, and action plans to facilitate better stewardship of coral reefs in an era of rapid environmental change.

Rapid ecosystem-scale consequences of acute deoxygenation on a Caribbean coral reef.

Loss of oxygen in the global ocean is accelerating due to climate change and eutrophication, but how acute deoxygenation events affect tropical marine ecosystems remains poorly understood. Here we integrate analyses of coral reef benthic communities with microbial community sequencing to show how a deoxygenation event rapidly altered benthic community composition and microbial assemblages in a shallow tropical reef ecosystem. Conditions associated with the event precipitated coral bleaching and mass mortality, causing a 50% loss of live coral and a shift in the benthic community that persisted a year later. Conversely, the unique taxonomic and functional profile of hypoxia-associated microbes rapidly reverted to a normoxic assemblage one month after the event. The decoupling of ecological trajectories among these major functional groups following an acute event emphasizes the need to incorporate deoxygenation as an emerging stressor into coral reef research and management plans to combat escalating threats to reef persistence.

Seagrass structural and elemental indicators reveal high nutrient availability within a tropical lagoon in Panama.

Seagrass meadows are valued coastal habitats that provide ecological and economic benefits around the world. Despite their importance, many meadows are in decline, driven by a variety of anthropogenic impacts. While these declines have been well documented in some regions, other locations (particularly within the tropics) lack long-term monitoring programs needed to resolve seagrass trends over time. Effective and spatially-expansive monitoring within under-represented regions is critical to provide an accurate perspective on seagrass status and trends. We present a comprehensive dataset on seagrass coverage and composition across 24 sites in Bahía Almirante, a lagoon along the Caribbean coast of Panama. Using a single survey, we focus on capturing spatial variation in seagrass physical and elemental characteristics and provide data on key seagrass bio-indicators, such as leaf morphology (length and width), elemental content (% nitrogen and phosphorus) and stable isotopic signatures (δ 13C and δ 15N). We further explore relationships between these variables and water depth (proxy for light availability) and proximity to shore (proxy for terrestrial inputs). The seagrass assemblage was mostly monospecific (dominated by Thalassia testudinum) and restricted to shallow water (<3 m). Above-ground biomass varied widely, averaging 71.7 g dry mass m-2, yet ranging from 24.8 to 139.6 g dry mass m-2. Leaf nitrogen content averaged 2.2%, ranging from 1.76 to 2.57%, while phosphorus content averaged 0.19% and ranged from 0.15 to 0.23%. These values were high compared to other published reports for T. testudinum, indicating elevated nutrient availability within the lagoon. Seagrass stable isotopic characteristics varied slightly and were comparable with other published values. Leaf carbon signatures (δ 13C) ranged from -11.74 to -6.70‰ and were positively correlated to shoreline proximity, suggesting a contribution of terrestrial carbon to seagrass biomass. Leaf nitrogen signatures (δ 15N) ranged from -1.75 to 3.15‰ and showed no correlation with shoreline proximity, suggesting that N sources within the bay were not dominated by localized point-source discharge of treated sewage. Correlations between other seagrass bio-indicators and environmental metrics were mixed: seagrass cover declined with depth, while biomass was negatively correlated with N, indicating that light and nutrient availability may jointly regulate seagrass cover and biomass. Our work documents the response of seagrass in Bahía Almirante to light and nutrient availability and highlights the eutrophic status of this bay. Using the broad spatial coverage of our survey as a baseline, we suggest the future implementation of a continuous and spatially expansive seagrass monitoring program within this region to assess the health of these important systems subject to global and local stressors.

Seasonal upwelling reduces herbivore control of tropical rocky intertidal algal communities.

Communities are shaped by a variety of ecological and environmental processes, each acting at different spatial scales. Seminal research on rocky shores highlighted the effects of consumers as local determinants of primary productivity and community assembly. However, it is now clear that the species interactions shaping communities at local scales are themselves regulated by large-scale oceanographic processes that generate regional variation in resource availability. Upwelling events deliver nutrient-rich water to coastal ecosystems, influencing primary productivity and algae-herbivore interactions. Despite the potential for upwelling to alter top-down control by herbivores, we know relatively little about the coupling between oceanographic processes and herbivory on tropical rocky shores, where herbivore effects on producers are considered to be strong and nutrient levels are considered to be limiting. By replicating seasonal molluscan herbivore exclusion experiments across three regions exposed to varying intensity of seasonal upwelling, separated by hundreds of kilometers along Panama's Pacific coast, we examine large-scale environmental determinants of consumer effects and community structure on tropical rocky shores. At sites experiencing seasonal upwelling, grazers strongly limited macroalgal cover when upwelling was absent, leading to dominance by crustose algae. As nutrients increased and surface water cooled during upwelling events, increases in primary productivity temporarily weakened herbivory, allowing foliose, turf and filamentous algae to replace crusts. Meanwhile, grazer effects were persistently strong at sites without seasonal upwelling. Our results confirm that herbivores are key determinants of tropical algal cover, and that the mollusk grazing guild can control initial stages of macroalgal succession. However, our focus on regional oceanographic conditions revealed that bottom-up processes regulate top-down control on tropical shorelines. This study expands on the extensive body of work highlighting the influence of upwelling on local ecological processes by demonstrating that nutrient subsidies delivered by upwelling events can weaken herbivory in tropical rocky shores.

Resilience of Tropical Ecosystems to Ocean Deoxygenation.

The impacts of ocean deoxygenation on biodiversity and ecosystem function are well established in temperate regions, and here we illustrate how the study of hypoxia in tropical ecosystems can offer insights of general importance. We first describe how mechanisms of resilience have developed in response to naturally occurring hypoxia across three tropical ecosystems: coral reefs, seagrass beds, and mangrove forests. We then suggest that the vulnerability of these systems to deoxygenation lies in interactions with other stressors that are increasing rapidly in the Anthropocene. Finally, we advocate for the adoption of a broader community- and ecosystem-level perspective that incorporates mutualisms, feedbacks, and mechanisms of self-rescue and recovery to develop a better predictive understanding of the effects of deoxygenation in coastal ecosystems.