Spatio-temporal variation in the growth of coral fragments of opportunity in the Eastern Tropical Pacific: implications for coral reef restoration

Introduction: Coral-reef communities are considered one of the most biodiverse, but also most threatened, marine ecosystems, and the accelerating loss of habitat over the past decades warrants active intervention. Objective: The present study demonstrates the successful implementation of a low-impact restoration technique in three Central Mexican Pacific degraded coral communities, using a protocol based on natural fragmentation (''fragments of opportunity") of the branching coral Pocillopora spp., considered the most abundant and primary carbonate-producing coral species of the Eastern Tropical Pacific. Methods: The restoration program was implemented in two offshore and one inshore coraline areas. The relationships between seawater temperature and coral survival, growth, and attachment rate were assessed over one year, with 183 fragments monitored each month. Results: The mean coral growth rate was 3.3 ± 0.1 mm mo-1, with annual growth rates in length and width of 39.9 ± 14.2 and 36.5 ± 19.5 mm yr-1, respectively. Self-attachment efficiency was 78 % and the survival rate was high (84 %). The growth rate differed significantly among reefs. Conclusions: Upon monitoring directly fragmented corals over a year, growth rates were deemed high enough to merit active restoration in the region. However, our data show that structural and abiotic differences and seasonal variability must be considered overall in successful long-term coral community restoration initiatives in the eastern Pacific region.

Introducción: Las comunidades de arrecifes de coral se consideran uno de los ecosistemas marinos con mayor biodiversidad, pero también los más amenazados, y la pérdida acelerada de hábitat en las últimas décadas justifica la implementación de una intervención activa. Objetivo: El presente estudio demuestra la implementación exitosa de una técnica de restauración de bajo impacto basada en la fragmentación natural (''fragmentos de oportunidad") del coral ramificado Pocillopora spp., la cual es la especie coralina más abundante y principal productora de carbonato del Pacífico Oriental Tropical. Métodos: El programa de restauración se implementó en dos sitios lejos de la costa y un sitio cercano a la costa, con comunidades coralinas degradadas. Las relaciones entre la temperatura del agua de mar y la supervivencia, el crecimiento y la tasa de adhesión de los corales se evaluaron durante un año con 183 fragmentos monitoreados cada mes. Resultados: La tasa media de crecimiento coralino fue de 3.3 ± 0.1 mm mo-1, con tasas de crecimiento anual en largo y ancho de 39.9 ± 14.2 y 36.5 ± 19.5 mm año-1, respectivamente. La eficiencia de la auto-adherencia fue del 78 % y la tasa de supervivencia fue alta (84 %). La tasa de crecimiento difirió significativamente entre los arrecifes. Conclusiones: Al monitorear directamente los corales fragmentados durante un año, las tasas de crecimiento se consideraron lo suficientemente altas como para merecer una restauración activa en la región. Sin embargo, nuestros datos muestran que las diferencias estructurales y abióticas y la variabilidad estacional deben considerarse en general en las iniciativas exitosas de restauración de comunidades de coral a largo plazo en la región del Pacífico oriental.

Evaluating biodiversity for coral reef reformation and monitoring on complex 3D structures using environmental DNA (eDNA) metabarcoding.

Quantifying coral reef biodiversity is challenging for cryptofauna and organisms in early life stages. We demonstrate the utility of eDNA metabarcoding as a tool for comprehensively evaluating invertebrate communities on complex 3D structures for reef reformation, and the role these structures play in provisioning habitat for organisms. 3D design and printing were used to create 18 complex tiles, which were used to form artificial reef structures. eDNA was collected from scraping tile surfaces for organismal biomass and from seawater samples around the artificial reefs in the Gulf of Eilat/Aqaba, Red Sea. Metabarcoding targeted the mitochondrial COI gene with specific primers for marine biodiversity. We provide the first eDNA biodiversity baseline for the Gulf of Eilat/Aqaba, capturing extensive information on species abundance, richness, and diversity. Tile tops had higher phylogenetic diversity and richness, despite a higher abundance of organisms on tile bottoms, highlighting the detection of cryptic organisms with eDNA. We recommend eDNA metabarcoding for reef restoration initiatives, especially for complex marine structures, to improve success and evaluation of biodiversity.

Assessing the potential for demographic restoration and assisted evolution to build climate resilience in coral reefs.

Interest is growing in developing conservation strategies to restore and maintain coral reef ecosystems in the face of mounting anthropogenic stressors, particularly climate warming and associated mass bleaching events. One such approach is to propagate coral colonies ex situ and transplant them to degraded reef areas to augment habitat for reef-dependent fauna, prevent colonization from spatial competitors, and enhance coral reproductive output. In addition to such "demographic restoration" efforts, manipulating the thermal tolerance of outplanted colonies through assisted relocation, selective breeding, or genetic engineering is being considered for enhancing rates of evolutionary adaptation to warming. Although research into such "assisted evolution" strategies has been growing, their expected performance remains unclear. We evaluated the potential outcomes of demographic restoration and assisted evolution in climate change scenarios using an eco-evolutionary simulation model. We found that supplementing reefs with pre-existing genotypes (demographic restoration) offers little climate resilience benefits unless input levels are large and maintained for centuries. Supplementation with thermally resistant colonies was successful at improving coral cover at lower input levels, but only if maintained for at least a century. Overall, we found that, although demographic restoration and assisted evolution have the potential to improve long-term coral cover, both approaches had a limited impact in preventing severe declines under climate change scenarios. Conversely, with sufficient natural genetic variance and time, corals could readily adapt to warming temperatures, suggesting that restoration approaches focused on building genetic variance may outperform those based solely on introducing heat-tolerant genotypes.

Coral reef restoration for coastal protection: Crafting technical and financial solutions.

Coastal erosion, aggravated by coral reef mortality is a major issue for Small Island Developing States. Traditionally gray infrastructure, financed by public budgets has been used to combat beach loss. We examined if three Nature-based Solutions (NbS): (i) coral restoration (green) (ii) restoration + limestone (hybrid) and (iii) restoration + 3D printed concrete (hybrid) could deliver positive outcomes for coastal protection and further incentivize cost sharing for reef conservation, with private beneficiaries. We modelled the impact of restoration on wave attenuation at two reefs off Barbados and simulated up-front and maintenance costs over a 25-year period. All solutions provide additionality when compared to gray infrastructure, especially in mitigating against Sea Level Rise. Restoration was the least costly with the highest risk of failure. The hybrid solutions, were less risky than the green as they provided immediate wave attenuation, alongside complementary services such as increased attractiveness due to the presence of reef fish. Their costs were however between +80% and +450% higher than gray solutions. While this might initially deter the use of NbS, blended finance and in some cases, Payments for Ecosystem Services, could provide options for governments and private beneficiaries to share costs, with ultimately greater benefits for themselves and coral reefs.

Reef Metabolism Monitoring Methods and Potential Applications for Coral Restoration.

Coral reef metabolism measurements have been used by scientists for decades to track reef responses to the globe's changing carbon budget and project shifts in reef function. Here, we propose that metabolism measurement tools and methods could also be used to monitor reef ecosystem change in response to coral restoration. This review paper provides a general introduction to net ecosystem metabolism and carbon chemistry for coral reef ecosystems, followed by a review of five metabolism monitoring methods with potential for application to coral reef restoration monitoring. Selected methodologies included those with measurement scales appropriate to assess outplant arrays and whole reef ecosystem outcomes associated with restoration interventions. Subsequently we discuss how water column and CO2 chemistry could be used to address coral restoration monitoring research gaps and scale up from biological, colony-level metrics to ecosystem-scale function and performance assessments. Such function-based measurements could potentially be used to inform several goal-based monitoring objectives highlighted in the Coral Reef Restoration Monitoring Guide. Lastly, this review discusses important methodological factors, such as scale, reef type, and flow environment, that should be considered when determining which metabolism monitoring technique would be most appropriate for a reef restoration project.

Coral cover and rubble cryptofauna abundance and diversity at outplanted reefs in Okinawa, Japan.

Global climate change is leading to damage and loss of coral reef ecosystems. On subtropical Okinawa Island in southwestern Japan, the prefectural government is working on coral reef restoration by outplanting coral colonies from family Acroporidae back to reefs after initially farming colonies inside protected nurseries. In order to establish a baseline for future comparisons, in this study we documented the current status of reefs undergoing outplanting at Okinawa Island, and nearby locations where no human manipulation has occurred. We examined three sites on the coast of Onna Village on the west coast of the island; each site included an outplanted and control location. We used (1) coral rubble sampling to measure and compare abundance and diversity of rubble cryptofauna; and (2) coral reef monitoring using Line Intercept Transects to track live coral coverage. Results showed that rubble shape had a positive correlation with the numbers of animals found within rubble themselves and may therefore constitute a reliable abundance predictor. Each outplanted location did not show differences with the corresponding control location in terms of rubble cryptofauna abundance, but outplanted locations had significantly lower coral coverage. Overall, differences between sites (Maeganeku1, Maeganeku2 and Manza, each including both outplanted and control locations) were significant, for both rubble cryptofauna and coral coverage. We recommend (1) to outplant colonies from more stress-resistant genera in place of Acropora, and (2) to conduct regular surveys to monitor the situation closely. With a lack of baseline data preceding impacts, rigorous monitoring over time can highlight trends towards increases or decreases in evaluated variables, allowing to obtain a clearer idea of the effects of transplants and on the trajectory of impacts due to climate change and local stressors . Finally, we also recommend (3) to establish conservation and sustainable practices that could aid the ongoing restoration efforts such as installing anchoring buoys to reduce impacts from anchoring, which could reduce coral mortality of both outplanted and native coral colonies.

Assessing and genotyping threatened staghorn coral Acropora cervicornis nurseries during restoration in southeast Dominican Republic.

Acropora cervicornis is a structurally and functionally important Caribbean coral species. Since the 1980s, it has suffered drastic population losses with no signs of recovery and has been classified as a critically endangered species. Its rapid growth rate makes it an excellent candidate for coral restoration programs. In 2011, the Fundación Dominicana de Estudios Marinos (Dominican Marine Studies Foundation, FUNDEMAR) began an A. cervicornis restoration program in Bayahibe, southeast Dominican Republic. In this study, we present the methodology and results of this program from its conception through 2017, a preliminary analysis of the strong 2016 and 2017 cyclonic seasons in the greater Caribbean, and a genetic characterization of the "main nursery". The mean survival of the fragments over 12 months was 87.45 ± 4.85% and the mean productivity was 4.01 ± 1.88 cm year-1 for the eight nurseries. The mean survival of six outplanted sites over 12 months was 71.55 ± 10.4%, and the mean productivity was 3.03 ± 1.30 cm year-1. The most common cause of mortality during the first 12 months, in both nurseries and outplanted sites, was predation by the fireworm, Hermodice carunculata. We identified 32 multilocus genotypes from 145 total analyzed individuals. The results and techniques described here will aid in the development of current and future nursery and outplanted site restoration programs.

Ecological solutions to reef degradation: optimizing coral reef restoration in the Caribbean and Western Atlantic.

Reef restoration activities have proliferated in response to the need to mitigate coral declines and recover lost reef structure, function, and ecosystem services. Here, we describe the recent shift from costly and complex engineering solutions to recover degraded reef structure to more economical and efficient ecological approaches that focus on recovering the living components of reef communities. We review the adoption and expansion of the coral gardening framework in the Caribbean and Western Atlantic where practitioners now grow and outplant 10,000's of corals onto degraded reefs each year. We detail the steps for establishing a gardening program as well as long-term goals and direct and indirect benefits of this approach in our region. With a strong scientific basis, coral gardening activities now contribute significantly to reef and species recovery, provide important scientific, education, and outreach opportunities, and offer alternate livelihoods to local stakeholders. While challenges still remain, the transition from engineering to ecological solutions for reef degradation has opened the field of coral reef restoration to a wider audience poised to contribute to reef conservation and recovery in regions where coral losses and recruitment bottlenecks hinder natural recovery.

Genetic markers for antioxidant capacity in a reef-building coral.

The current lack of understanding of the genetic basis underlying environmental stress tolerance in reef-building corals impairs the development of new management approaches to confronting the global demise of coral reefs. On the Great Barrier Reef (GBR), an approximately 51% decline in coral cover occurred over the period 1985-2012. We conducted a gene-by-environment association analysis across 12° latitude on the GBR, as well as both in situ and laboratory genotype-by-phenotype association analyses. These analyses allowed us to identify alleles at two genetic loci that account for differences in environmental stress tolerance and antioxidant capacity in the common coral Acropora millepora. The effect size for antioxidant capacity was considerable and biologically relevant (32.5 and 14.6% for the two loci). Antioxidant capacity is a critical component of stress tolerance because a multitude of environmental stressors cause increased cellular levels of reactive oxygen species. Our findings provide the first step toward the development of novel coral reef management approaches, such as spatial mapping of stress tolerance for use in marine protected area design, identification of stress-tolerant colonies for assisted migration, and marker-assisted selective breeding to create more tolerant genotypes for restoration of denuded reefs.