A roadmap to integrating resilience into the practice of coral reef restoration.

Recent warm temperatures driven by climate change have caused mass coral bleaching and mortality across the world, prompting managers, policymakers, and conservation practitioners to embrace restoration as a strategy to sustain coral reefs. Despite a proliferation of new coral reef restoration efforts globally and increasing scientific recognition and research on interventions aimed at supporting reef resilience to climate impacts, few restoration programs are currently incorporating climate change and resilience in project design. As climate change will continue to degrade coral reefs for decades to come, guidance is needed to support managers and restoration practitioners to conduct restoration that promotes resilience through enhanced coral reef recovery, resistance, and adaptation. Here, we address this critical implementation gap by providing recommendations that integrate resilience principles into restoration design and practice, including for project planning and design, coral selection, site selection, and broader ecosystem context. We also discuss future opportunities to improve restoration methods to support enhanced outcomes for coral reefs in response to climate change. As coral reefs are one of the most vulnerable ecosystems to climate change, interventions that enhance reef resilience will help to ensure restoration efforts have a greater chance of success in a warming world. They are also more likely to provide essential contributions to global targets to protect natural biodiversity and the human communities that rely on reefs.

Using resilience assessments to inform the management and conservation of coral reef ecosystems.

Climate change is causing the decline of coral reef ecosystems globally. Recent research highlights the importance of reducing CO2 emissions in combination with implementing local management actions to support reef health and recovery, particularly actions that protect sites which are more resilient to extreme events. Resilience assessments quantify the ecological, social, and environmental context of reefs through the lens of resilience, i.e., the capacity of a system to absorb or withstand stressors such that the system maintains its structure and functions and has the capacity to adapt to future disturbances and changes. Resilience assessments are an important tool to help marine managers and decision makers anticipate changes, identify areas with high survival prospects, and prioritize management actions to support resilience. While being widely implemented, however, there has not yet been an evaluation of whether resilience assessments have informed coral reef management. Here, we assess the primary and gray literature and input from coral reef managers to map where resilience assessments have been conducted. We explore if and how they have been used to inform management actions and provide recommendations for improving the likelihood that resilience assessments will result in management actions and positive conservation outcomes. These recommendations are applicable to other ecosystems in which resilience assessments are applied and will become increasingly important as climate impacts intensify and reduce the window of opportunity for protecting natural ecosystems.

Effects of predation and nutrient enrichment on the success and microbiome of a foundational coral.

By inflicting damage to prey tissues, consumer species may increase stress in prey hosts and reduce overall fitness (i.e., primary effects, such as growth or reproduction) or cause secondary effects by affecting prey interactions with other species such as microbes. However, little is known about how abiotic conditions affect the outcomes of these biotic interactions. In coral reef communities, both nutrient enrichment and predation have been linked to reduced fitness and disease facilitation in corals, yet no study to date has tested their combined effects on corals or their associated microbial communities (i.e., microbiomes). Here, we assess the effects of grazing by a prevalent coral predator (the short coral snail, Coralliophila abbreviata) and nutrient enrichment on staghorn coral, Acropora cervicornis, and its microbiomes using a factorial experiment and high-throughput DNA sequencing. We found that predation, but not nutrients, significantly reduced coral growth and increased mortality, tissue loss, and turf algae colonization. Partial predation and nutrient enrichment both independently altered coral microbiomes such that one bacterial genus came to dominate the microbial community. Nutrient-enriched corals were associated with significant increases in Rickettsia-like organisms, which are currently one of several microbial groups being investigated as a disease agent in this coral species. However, we found no effects of nutrient enrichment on coral health, disease, or their predators. This research suggests that in the several months following coral transplantation (i.e., restoration) or disturbance (i.e., recovery), Caribbean acroporid corals appear to be highly susceptible to negative effects caused by predators, but not or not yet susceptible to nutrient enrichment despite changes to their microbial communities.

Sediment carbon storage differs in native and non-native Caribbean seagrass beds.

Non-native species are expanding globally and can alter ecosystem functions, including food web dynamics, community structure and carbon storage. Seagrass are foundation species that contribute a variety of ecosystem services in near-shore coastal ecosystems, including a significant sink of carbon. In the Caribbean, the rapidly expanding non-native Halophila stipulacea has unknown impacts on carbon storage. To investigate the impacts on carbon storage, we quantified organic carbon (Corg) content in sediment and seagrass tissues from monotypic H. stipulacea beds, mixed native seagrass beds dominated by Thalassia testudinum and Syringodium filiforme, and unvegetated substrate in St. John, USVI. We found native seagrass-vegetated sediment contained 1.3 times more Corg than sediment covered by H. stipulacea, and 1.6 times more Corg than unvegetated areas on average. Whereas, H. stipulacea-dominated substrate stored 1.2 times more Corg than unvegetated substrate. Likewise, native species contained 2.2 times more aboveground biomass and 6.0 times more belowground biomass than H. stipulacea. Since seagrasses are critical sources of carbon sequestration, our results suggest that invading H. stipulacea is associated with lower carbon stocks which has potential implications for conservation activities and climate change mitigation.

Relationships between a common Caribbean corallivorous snail and protected area status, coral cover, and predator abundance.

As coral populations decline across the Caribbean, it is becoming increasingly important to understand the forces that inhibit coral survivorship and recovery. Predation by corallivores, such as the short coral snail Coralliophila abbreviata, are one such threat to coral health and recovery worldwide, but current understanding of the factors controlling corallivore populations, and therefore predation pressure on corals, remains limited. To examine the extent to which bottom-up forces (i.e., coral prey), top-down forces (i.e., predators), and marine protection relate to C. abbreviata distributions, we surveyed C. abbreviata abundance, percent coral cover, and the abundance of potential snail predators across six protected and six unprotected reefs in the Florida Keys. We found that C. abbreviata abundance was lower in protected areas where predator assemblages were also more diverse, and that across all sites snail abundance generally increased with coral cover. C. abbreviata abundance had strong, negative relationships with two gastropod predators-the Caribbean spiny lobster (Panulirus argus) and the grunt black margate (Anisotremus surinamensis), which may be exerting top-down pressure on C. abbreviata populations. Further, we found the size of C. abbreviata was also related to reef protection status, with larger C. abbreviata on average in protected areas, suggesting that gape-limited predators such as P. argus and A. surinamensis may alter size distributions by targeting small snails. Combined, these results provide preliminary evidence that marine protection in the Florida Keys may preserve critical trophic interactions that indirectly promote coral success via control of local populations of the common corallivorous snail C. abbreviata.

Correction: Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov.

Bacterial symbionts are integral to the health and homeostasis of invertebrate hosts. Notably, members of the Rickettsiales genus Wolbachia influence several aspects of the fitness and evolution of their terrestrial hosts, but few analogous partnerships have been found in marine systems. We report here the genome, phylogenetics, and biogeography of a ubiquitous and novel Rickettsiales species that primarily associates with marine organisms. We previously showed that this bacterium was found in scleractinian corals, responds to nutrient exposure, and is associated with reduced host growth and increased mortality. This bacterium, like other Rickettsiales, has a reduced genome indicative of a parasitic lifestyle. Phylogenetic analysis places this Rickettsiales within a new genus we define as "Candidatus Aquarickettsia." Using data from the Earth Microbiome Project and SRA databases, we also demonstrate that members of "Ca. Aquarickettsia" are found globally in dozens of invertebrate lineages. The coral-associated "Candidatus A. rohweri" is the first finished genome in this new clade. "Ca. A. rohweri" lacks genes to synthesize most sugars and amino acids but possesses several genes linked to pathogenicity including Tlc, an antiporter that exchanges host ATP for ADP, and a complete Type IV secretion system. Despite its inability to metabolize nitrogen, "Ca. A. rohweri" possesses the NtrY-NtrX two-component system involved in sensing and responding to extracellular nitrogen. Given these data, along with visualization of the parasite in host tissues, we hypothesize that "Ca. A. rohweri" reduces coral health by consuming host nutrients and energy, thus weakening and eventually killing host cells. Last, we hypothesize that nutrient enrichment, which is increasingly common on coral reefs, encourages unrestricted growth of "Ca. A. rohweri" in its host by providing abundant N-rich metabolites to be scavenged.

Publisher Correction: Local management actions can increase coral resilience to thermally-induced bleaching.

In the version of this Brief Communication originally published, the two instances of 'natural-to-high' in the sixth and seventh paragraphs were incorrect; they should have read 'naturally high'.

Local management actions can increase coral resilience to thermally-induced bleaching.

Recent large-scale analyses suggest that local management actions may not protect coral reefs from climate change, yet most local threat-reduction strategies have not been tested experimentally. We show that removing coral predators is a common local action used by managers across the world, and that removing the corallivorous snail Coralliophila abbreviata from Caribbean brain corals (Pseudodiploria and Diploria species) before a major warming event increased coral resilience by reducing bleaching severity (resistance) and post-bleaching tissue mortality (recovery). Our results highlight the need for increased evaluation and identification of local interventions that improve coral reef resilience.

Time to cash in on positive interactions for coral restoration.

Coral reefs are among the most biodiverse and productive ecosystems on Earth, and provide critical ecosystem services such as protein provisioning, coastal protection, and tourism revenue. Despite these benefits, coral reefs have been declining precipitously across the globe due to human impacts and climate change. Recent efforts to combat these declines are increasingly turning to restoration to help reseed corals and speed-up recovery processes. Coastal restoration theory and practice has historically favored transplanting designs that reduce potentially harmful negative species interactions, such as competition between transplants. However, recent research in salt marsh ecosystems has shown that shifting this theory to strategically incorporate positive interactions significantly enhances restoration yield with little additional cost or investment. Although some coral restoration efforts plant corals in protected areas in order to benefit from the facilitative effects of herbivores that reduce competitive macroalgae, little systematic effort has been made in coral restoration to identify the entire suite of positive interactions that could promote population enhancement efforts. Here, we highlight key positive species interactions that managers and restoration practitioners should utilize to facilitate the restoration of corals, including (i) trophic facilitation, (ii) mutualisms, (iii) long-distance facilitation, (iv) positive density-dependence, (v) positive legacy effects, and (vi) synergisms between biodiversity and ecosystem function. As live coral cover continues to decline and resources are limited to restore coral populations, innovative solutions that increase efficiency of restoration efforts will be critical to conserving and maintaining healthy coral reef ecosystems and the human communities that rely on them.