Intra-colony spatial variance of oxyregulation and hypoxic thresholds for key Acropora coral species.

Oxygen (O2) availability is essential for healthy coral reef functioning, yet how continued loss of dissolved O2 via ocean deoxygenation impacts performance of reef building corals remains unclear. Here, we examine how intra-colony spatial geometry of important Great Barrier Reef (GBR) coral species Acropora may influence variation in hypoxic thresholds for upregulation, to better understand capacity to tolerate future reductions in O2 availability. We first evaluate the application of more streamlined models used to parameterise Hypoxia Response Curve data, models that have been used historically to identify variable oxyregulatory capacity. Using closed-system respirometry to analyse O2 drawdown rate, we show that a two-parameter model returns similar outputs as previous 12th-order models for descriptive statistics such as the average oxyregulation capacity (Tpos) and the ambient O2 level at which the coral exerts maximum regulation effort (Pcmax), for diverse Acropora species. Following an experiment to evaluate whether stress induced by coral fragmentation for respirometry affected O2 drawdown rate, we subsequently identify differences in hypoxic response for the interior and exterior colony locations for the species Acropora abrotanoides, Acropora cf. microphthalma and Acropora elseyi. Average regulation capacity across species was greater (0.78-1.03 ± SE 0.08) at the colony interior compared with exterior (0.60-0.85 ± SE 0.08). Moreover, Pcmax occurred at relatively low pO2 of <30% (±1.24; SE) air saturation for all species, across the colony. When compared against ambient O2 availability, these factors corresponded to differences in mean intra-colony oxyregulation, suggesting that lower variation in dissolved O2 corresponds with higher capacity for oxyregulation. Collectively, our data show that intra-colony spatial variation affects coral oxyregulation hypoxic thresholds, potentially driving differences in Acropora oxyregulatory capacity.

Impacts of plastic-free materials on coral-associated bacterial communities during reef restoration.

Coral propagation and out-planting based restoration approaches are increasingly being applied to assist natural recovery of coral reefs. However, many restoration methods rely on plastic zip-ties to secure coral material which is potentially problematic for the marine environment. Plastic-free biodegradable alternatives may however pose unique risks to coral-associated bacterial communities integral to coral health. Therefore, to identify whether biodegradable materials differentially impact coral-associated bacterial communities we examined Acropora millepora coral-associated bacterial communities during propagation in two experiments on the Great Barrier Reef. Coral fragments were secured to coral nurseries with conventional plastic, metal, or biodegradable (polyester and polycaprolactone) ties. Tie failure and coral-associated bacterial communities were then characterized over six months. Minimal coral mortality was observed (3.6%-8%) and all ties had low failure rates (0%-4.2%) except for biodegradable polyester ties (29.2% failure). No differences were observed between coral-associated bacterial communities of fragments secured with different ties, and no proliferation of putatively pathogenic bacteria was recorded. Overall, our findings suggest that reducing reliance on conventional plastic is feasible through transitions to biodegradable materials, without any notable impacts on coral-associated bacterial communities. However, we caution the need to examine more coral taxa of different morphologies and new plastic-free materials prior to application.

Distinct emissions of biogenic volatile organic compounds from temperate benthic taxa.

INTRODUCTION: Biogenic volatile organic compounds (BVOCs) are emitted by all organisms as intermediate or end-products of metabolic processes. Individual BVOCs perform important physiological, ecological and climatic functions, and collectively constitute the volatilome-which can be reflective of organism taxonomy and health. Although BVOC emissions of tropical benthic reef taxa have recently been the focus of multiple studies, emissions derived from their temperate counterparts have never been characterised. OBJECTIVES: Characterise the volatilomes of key competitors for benthic space among Australian temperate reefs. METHODS: Six fragments/fronds of a temperate coral (Plesiastrea versipora) and a macroalga (Ecklonia radiata) from a Sydney reef site were placed within modified incubation chambers filled with seawater. Organism-produced BVOCs were captured on thermal desorption tubes using a purge-and-trap methodology, and were then analysed using GC × GC - TOFMS and multivariate tests. RESULTS: Analysis detected 55 and 63 BVOCs from P. versipora and E. radiata respectively, with 30 of these common between species. Each taxon was characterised by a similar relative composition of chemical classes within their volatilomes. However, 14 and 10 volatiles were distinctly emitted by either E. radiata or P. versipora respectively, including the halogenated compounds iodomethane, tribromomethane, carbon tetrachloride and trichloromonofluoromethane. While macroalgal cover was 3.7 times greater than coral cover at the sampling site, P. versipora produced on average 17 times more BVOCs per cm2 of live tissue, resulting in an estimated contribution to local BVOC emission that was 4.7 times higher than E. radiata. CONCLUSION: Shifts in benthic community composition could disproportionately impact local marine chemistry and affect how ecosystems contribute to broader BVOC emissions.

Symbiodiniaceae photophysiology and stress resilience is enhanced by microbial associations.

Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species (Symbiodinium microadriaticum and Breviolum minutum) cultured under acute temperature and light stress with specific bacterial partners from their microbiome (Labrenzia (Roseibium) alexandrii, Marinobacter adhaerens or Muricauda aquimarina). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp.) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae.

Coral endosymbiont growth is enhanced by metabolic interactions with bacteria.

Bacteria are key contributors to microalgae resource acquisition, competitive performance, and functional diversity, but their potential metabolic interactions with coral microalgal endosymbionts (Symbiodiniaceae) have been largely overlooked. Here, we show that altering the bacterial composition of two widespread Symbiodiniaceae species, during their free-living stage, results in a significant shift in their cellular metabolism. Indeed, the abundance of monosaccharides and the key phytohormone indole-3-acetic acid (IAA) were correlated with the presence of specific bacteria, including members of the Labrenzia (Roseibium) and Marinobacter genera. Single-cell stable isotope tracking revealed that these two bacterial genera are involved in reciprocal exchanges of carbon and nitrogen with Symbiodiniaceae. We identified the provision of IAA by Labrenzia and Marinobacter, and this metabolite caused a significant growth enhancement of Symbiodiniaceae. By unravelling these interkingdom interactions, our work demonstrates how specific bacterial associates fundamentally govern Symbiodiniaceae fitness.

Symbiont Identity Impacts the Microbiome and Volatilome of a Model Cnidarian-Dinoflagellate Symbiosis.

The symbiosis between cnidarians and dinoflagellates underpins the success of reef-building corals in otherwise nutrient-poor habitats. Alterations to symbiotic state can perturb metabolic homeostasis and thus alter the release of biogenic volatile organic compounds (BVOCs). While BVOCs can play important roles in metabolic regulation and signalling, how the symbiotic state affects BVOC output remains unexplored. We therefore characterised the suite of BVOCs that comprise the volatilome of the sea anemone Exaiptasia diaphana ('Aiptasia') when aposymbiotic and in symbiosis with either its native dinoflagellate symbiont Breviolum minutum or the non-native symbiont Durusdinium trenchii. In parallel, the bacterial community structure in these different symbiotic states was fully characterised to resolve the holobiont microbiome. Based on rRNA analyses, 147 unique amplicon sequence variants (ASVs) were observed across symbiotic states. Furthermore, the microbiomes were distinct across the different symbiotic states: bacteria in the family Vibrionaceae were the most abundant in aposymbiotic anemones; those in the family Crocinitomicaceae were the most abundant in anemones symbiotic with D. trenchii; and anemones symbiotic with B. minutum had the highest proportion of low-abundance ASVs. Across these different holobionts, 142 BVOCs were detected and classified into 17 groups based on their chemical structure, with BVOCs containing multiple functional groups being the most abundant. Isoprene was detected in higher abundance when anemones hosted their native symbiont, and dimethyl sulphide was detected in higher abundance in the volatilome of both Aiptasia-Symbiodiniaceae combinations relative to aposymbiotic anemones. The volatilomes of aposymbiotic anemones and anemones symbiotic with B. minutum were distinct, while the volatilome of anemones symbiotic with D. trenchii overlapped both of the others. Collectively, our results are consistent with previous reports that D. trenchii produces a metabolically sub-optimal symbiosis with Aiptasia, and add to our understanding of how symbiotic cnidarians, including corals, may respond to climate change should they acquire novel dinoflagellate partners.

Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Metabolomic signatures of corals thriving across extreme reef habitats reveal strategies of heat stress tolerance.

Anthropogenic stressors continue to escalate worldwide, driving unprecedented declines in reef environmental conditions and coral health. One approach to better understand how corals can function in the future is to examine coral populations that thrive within present day naturally extreme habitats. We applied untargeted metabolomics (gas chromatography-mass spectrometry (GC-MS)) to contrast metabolite profiles of Pocillopora acuta colonies from hot, acidic and deoxygenated mangrove environments versus those from adjacent reefs. Under ambient temperatures, P. acuta predominantly associated with endosymbionts of the genera Cladocopium (reef) or Durusdinium (mangrove), exhibiting elevated metabolism in mangrove through energy-generating and biosynthesis pathways compared to reef populations. Under transient heat stress, P. acuta endosymbiont associations were unchanged. Reef corals bleached and exhibited extensive shifts in symbiont metabolic profiles (whereas host metabolite profiles were unchanged). By contrast, mangrove populations did not bleach and solely the host metabolite profiles were altered, including cellular responses in inter-partner signalling, antioxidant capacity and energy storage. Thus mangrove P. acuta populations resist periodically high-temperature exposure via association with thermally tolerant endosymbionts coupled with host metabolic plasticity. Our findings highlight specific metabolites that may be biomarkers of heat tolerance, providing novel insight into adaptive coral resilience to elevated temperatures.

Coral restoration and adaptation in Australia: The first five years.

While coral reefs in Australia have historically been a showcase of conventional management informed by research, recent declines in coral cover have triggered efforts to innovate and integrate intervention and restoration actions into management frameworks. Here we outline the multi-faceted intervention approaches that have developed in Australia since 2017, from newly implemented in-water programs, research to enhance coral resilience and investigations into socio-economic perspectives on restoration goals. We describe in-water projects using coral gardening, substrate stabilisation, coral repositioning, macro-algae removal, and larval-based restoration techniques. Three areas of research focus are also presented to illustrate the breadth of Australian research on coral restoration, (1) the transdisciplinary Reef Restoration and Adaptation Program (RRAP), one of the world's largest research and development programs focused on coral reefs, (2) interventions to enhance coral performance under climate change, and (3) research into socio-cultural perspectives. Together, these projects and the recent research focus reflect an increasing urgency for action to confront the coral reef crisis, develop new and additional tools to manage coral reefs, and the consequent increase in funding opportunities and management appetite for implementation. The rapid progress in trialling and deploying coral restoration in Australia builds on decades of overseas experience, and advances in research and development are showing positive signs that coral restoration can be a valuable tool to improve resilience at local scales (i.e., high early survival rates across a variety of methods and coral species, strong community engagement with local stakeholders). RRAP is focused on creating interventions to help coral reefs at multiple scales, from micro scales (i.e., interventions targeting small areas within a specific reef site) to large scales (i.e., interventions targeting core ecosystem function and social-economic values at multiple select sites across the Great Barrier Reef) to resist, adapt to and recover from the impacts of climate change. None of these interventions aim to single-handedly restore the entirety of the Great Barrier Reef, nor do they negate the importance of urgent climate change mitigation action.

Deoxygenation lowers the thermal threshold of coral bleaching.

Exposure to deoxygenation from climate warming and pollution is emerging as a contributing factor of coral bleaching and mortality. However, the combined effects of heating and deoxygenation on bleaching susceptibility remain unknown. Here, we employed short-term thermal stress assays to show that deoxygenated seawater can lower the thermal limit of an Acropora coral by as much as 1 °C or 0.4 °C based on bleaching index scores or dark-acclimated photosynthetic efficiencies, respectively. Using RNA-Seq, we show similar stress responses to heat with and without deoxygenated seawater, both activating putative key genes of the hypoxia-inducible factor response system indicative of cellular hypoxia. We also detect distinct deoxygenation responses, including a disruption of O2-dependent photo-reception/-protection, redox status, and activation of an immune response prior to the onset of bleaching. Thus, corals are even more vulnerable when faced with heat stress in deoxygenated waters. This highlights the need to integrate dissolved O2 measurements into global monitoring programs of coral reefs.

Cellular adaptations leading to coral fragment attachment on artificial substrates in Acropora millepora (Am-CAM).

Reproductive propagation by asexual fragmentation in the reef-building coral Acropora millepora depends on (1) successful attachment to the reef substrate through modification of soft tissues and (2) a permanent bond with skeletal encrustation. Despite decades of research examining asexual propagation in corals, the initial response, cellular reorganisation, and development leading to fragment substrate attachment via a newly formed skeleton has not been documented in its entirety. Here, we establish the first "coral attachment model" for this species ("Am-CAM") by developing novel methods that allow correlation of fluorescence and electron microscopy image data with in vivo microscopic time-lapse imagery. This multi-scale imaging approach identified three distinct phases involved in asexual propagation: (1) the contact response of the coral fragment when contact with the substrate, followed by (2) fragment stabilisation through anchoring by the soft tissue, and (3) formation of a "lappet-like appendage" structure leading to substrate bonding of the tissue for encrustation through the onset of skeletal calcification. In developing Am-CAM, we provide new biological insights that can enable reef researchers, managers and coral restoration practitioners to begin evaluating attachment effectiveness, which is needed to optimise species-substrate compatibility and achieve effective outplanting.

The diversity and ecology of Symbiodiniaceae: A traits-based review.

Among the most successful microeukaryotes to form mutualisms with animals are dinoflagellates in the family Symbiodiniaceae. These photosynthetic symbioses drive significant primary production and are responsible for the formation of coral reef ecosystems but are particularly sensitive when environmental conditions become extreme. Annual episodes of widespread coral bleaching (disassociation of the mutualistic partnership) and mortality are forecasted from the year 2060 under current trends of ocean warming. However, host cnidarians and dinoflagellate symbionts display exceptional genetic and functional diversity, and meaningful predictions of the future that embrace this biological complexity are difficult to make. A recent move to trait-based biology (and an understanding of how traits are shaped by the environment) has been adopted to move past this problem. The aim of this review is to: (1) provide an overview of the major cnidarian lineages that are symbiotic with Symbiodiniaceae; (2) summarise the symbiodiniacean genera associated with cnidarians with reference to recent changes in taxonomy and systematics; (3) examine the knowledge gaps in Symbiodiniaceae life history from a trait-based perspective; (4) review Symbiodiniaceae trait variation along three abiotic gradients (light, nutrients, and temperature); and (5) provide recommendations for future research of Symbiodiniaceae traits. We anticipate that a detailed understanding of traits will further reveal basic knowledge of the evolution and functional diversity of these mutualisms, as well as enhance future efforts to model stability and change in ecosystems dependent on cnidarian-dinoflagellate organisms.

Symbiosis induces unique volatile profiles in the model cnidarian Aiptasia.

The establishment and maintenance of the symbiosis between a cnidarian host and its dinoflagellate symbionts is central to the success of coral reefs. To explore the metabolite production underlying this symbiosis, we focused on a group of low molecular weight secondary metabolites, biogenic volatile organic compounds (BVOCs). BVOCs are released from an organism or environment, and can be collected in the gas phase, allowing non-invasive analysis of an organism's metabolism (i.e. 'volatilomics'). We characterised volatile profiles of the sea anemone Aiptasia (Exaiptasia diaphana), a model system for cnidarian-dinoflagellate symbiosis, using comprehensive two-dimensional gas chromatography coupled with time-of-flight mass spectrometry. We compared volatile profiles between: (1) symbiotic anemones containing their native symbiont, Breviolum minutum; (2) aposymbiotic anemones; and (3) cultured isolates of B. minutum. Overall, 152 BVOCs were detected, and classified into 14 groups based on their chemical structure, the most numerous groups being alkanes and aromatic compounds. A total of 53 BVOCs were differentially abundant between aposymbiotic anemones and B. minutum cultures; 13 between aposymbiotic and symbiotic anemones; and 60 between symbiotic anemones and cultures of B. minutum. More BVOCs were differentially abundant between cultured and symbiotic dinoflagellates than between aposymbiotic and symbiotic anemones, suggesting that symbiosis may modify symbiont physiology more than host physiology. This is the first volatilome analysis of the Aiptasia model system and provides a foundation from which to explore how BVOC production is perturbed under environmental stress, and ultimately the role they play in this important symbiosis.

Widespread oxyregulation in tropical corals under hypoxia.

Hypoxia (low oxygen stress) is increasingly reported on coral reefs, caused by ocean deoxygenation linked to coastal nutrient pollution and ocean warming. While the ability to regulate respiration is a key driver of hypoxia tolerance in many other aquatic taxa, corals' oxyregulatory capabilities remain virtually unexplored. Here, we examine O2-consumption patterns across 17 coral species under declining O2 partial pressure (pO2). All corals showed ability to oxyregulate, but total positive regulation (Tpos) varied between species, ranging from 0.41 (Pocillopora damicornis) to 2.42 (P. acuta). On average, corals performed maximum regulation effort (Pcmax) at low pO2 (30% air saturation, corresponding to lower O2 levels measured on natural reef systems), and exhibited detectable regulation down to as low as <10% air saturation. Our study shows that corals are not oxyconformers as previously thought, suggesting oxyregulation is likely important for survival in dynamic O2 environments of shallow coral reefs subjected to hypoxic events.

Disentangling compartment functions in sessile marine invertebrates.

Sessile invertebrates are frequently sampled and processed whole for downstream analyses. However, their apparent structural simplicity is deceptive as these organisms often harbour discrete compartments. These compartments have physicochemical conditions that differ markedly from neighbouring tissues, and that have likely evolved to support specific functions. Here, we argue that such compartments should be specifically targeted when characterising sessile invertebrate biology and we use the coral gastrovascular cavity to support our argument. This complex compartment displays steep and dynamic chemical gradients, harbours distinct microorganisms, and presumably plays a key role in coral biology. Disentangling the functions played by (and amongst) compartments will likely provide transformative insight into the biology of sessile invertebrates and their future under environmental change.

Micronutrient content drives elementome variability amongst the Symbiodiniaceae.

BACKGROUND: Elements are the basis of life on Earth, whereby organisms are essentially evolved chemical substances that dynamically interact with each other and their environment. Determining species elemental quotas (their elementome) is a key indicator for their success across environments with different resource availabilities. Elementomes remain undescribed for functionally diverse dinoflagellates within the family Symbiodiniaceae that includes coral endosymbionts. We used dry combustion and ICP-MS to assess whether Symbiodiniaceae (ten isolates spanning five genera Breviolum, Cladocopium, Durusdinium, Effrenium, Symbiodinium) maintained under long-term nutrient replete conditions have unique elementomes (six key macronutrients and nine micronutrients) that would reflect evolutionarily conserved preferential elemental acquisition. For three isolates we assessed how elevated temperature impacted their elementomes. Further, we tested whether Symbiodiniaceae conform to common stoichiometric hypotheses (e.g., the growth rate hypothesis) documented in other marine algae. This study considers whether Symbiodiniaceae isolates possess unique elementomes reflective of their natural ecologies, evolutionary histories, and resistance to environmental change. RESULTS: Symbiodiniaceae isolates maintained under long-term luxury uptake conditions, all exhibited highly divergent elementomes from one another, driven primarily by differential content of micronutrients. All N:P and C:P ratios were below the Redfield ratio values, whereas C:N was close to the Redfield value. Elevated temperature resulted in a more homogenised elementome across isolates. The Family-level elementome was (C19.8N2.6 P1.0S18.8K0.7Ca0.1) · 1000 (Fe55.7Mn5.6Sr2.3Zn0.8Ni0.5Se0.3Cu0.2Mo0.1V0.04) mmol Phosphorous-1 versus (C25.4N3.1P1.0S23.1K0.9Ca0.4) · 1000 (Fe66.7Mn6.3Sr7.2Zn0.8Ni0.4Se0.2Cu0.2Mo0.2V0.05) mmol Phosphorous -1 at 27.4 ± 0.4 °C and 30.7 ± 0.01 °C, respectively. Symbiodiniaceae isolates tested here conformed to some, but not all, stoichiometric principles. CONCLUSIONS: Elementomes for Symbiodiniaceae diverge from those reported for other marine algae, primarily via lower C:N:P and different micronutrient expressions. Long-term maintenance of Symbiodiniaceae isolates in culture under common nutrient replete conditions suggests isolates have evolutionary conserved preferential uptake for certain elements that allows these unique elementomes to be identified. Micronutrient content (normalised to phosphorous) commonly increased in the Symbiodiniaceae isolates in response to elevated temperature, potentially indicating a common elemental signature to warming.

Proteome metabolome and transcriptome data for three Symbiodiniaceae under ambient and heat stress conditions.

The Symbiodiniaceae are a taxonomically and functionally diverse family of marine dinoflagellates. Their symbiotic relationship with invertebrates such as scleractinian corals has made them the focus of decades of research to resolve the underlying biology regulating their sensitivity to stressors, particularly thermal stress. Research to-date suggests that Symbiodiniaceae stress sensitivity is governed by a complex interplay between phylogenetic dependent and independent traits (diversity of characteristics of a species). Consequently, there is a need for datasets that simultaneously broadly resolve molecular and physiological processes under stressed and non-stressed conditions. Therefore, we provide a dataset simultaneously generating transcriptome, metabolome, and proteome data for three ecologically important Symbiodiniaceae isolates under nutrient replete growth conditions and two temperature treatments (ca. 26 °C and 32 °C). Elevated sea surface temperature is primarily responsible for coral bleaching events that occur when the coral-Symbiodiniaceae relationship has been disrupted. Symbiodiniaceae can strongly influence their host's response to thermal stress and consequently it is necessary to resolve drivers of Symbiodiniaceae heat stress tolerance. We anticipate these datasets to expand our understanding on the key genotypic and functional properties that influence the sensitivities of Symbiodiniaceae to thermal stress.

Horizon scan of rapidly advancing coral restoration approaches for 21st century reef management.

Coral reef restoration activity is accelerating worldwide in efforts to offset the rate of reef health declines. Many advances have already been made in restoration practices centred on coral biology (coral restoration), and particularly those that look to employ the high adaptive state and capacity of corals in order to ensure that efforts rebuilding coral biomass also equip reefs with enhanced resilience to future stress. We horizon scan the state-of-play for the many coral restoration innovations already underway across the complex life cycle for corals that spans both asexual and sexual reproduction - assisted evolution (manipulations targeted to the coral host and host-associated microbes), biobanking, as well as scalable coral propagation and planting - and how these innovations are in different stages of maturity to support new 21st century reef management frameworks. Realising the potential for coral restoration tools as management aids undoubtedly rests on validating different approaches as their application continues to scale. Whilst the ecosystem service responses to increased scaling still largely remain to be seen, coral restoration has already delivered immense new understanding of coral and coral-associated microbial biology that has long lagged behind advances in other reef sciences.

Translating the 10 golden rules of reforestation for coral reef restoration.

Efforts are accelerating to protect and restore ecosystems globally. With trillions of dollars in ecosystem services at stake, no clear framework exists for developing or prioritizing approaches to restore coral reefs even as efforts and investment opportunities to do so grow worldwide. Restoration may buy time for climate change mitigation, but it lacks rigorous guidance to meet objectives of scalability and effectiveness. Lessons from restoration of terrestrial ecosystems can and should be rapidly adopted for coral reef restoration. We propose how the 10 golden rules of effective forest restoration can be translated to accelerate efforts to restore coral reefs based on established principles of resilience, management, and local stewardship. We summarize steps to undertake reef restoration as a management strategy in the context of the diverse ecosystem service values that coral reefs provide. Outlining a clear blueprint is timely as more stakeholders seek to undertake restoration as the UN Decade on Ecosystem Restoration begins.

Traducción de las Diez Reglas de Oro de la Reforestación para la Restauración de los Arrecifes de Coral Resumen Cada vez son más los esfuerzos para proteger y restaurar los ecosistemas a nivel mundial. Con billones de dólares en servicios ambientales en juego, no existe un marco de trabajo para desarrollar o priorizar estrategias para la restauración de los arrecifes de coral incluso cuando en todo el mundo aumentan los esfuerzos y las oportunidades de inversión. Puede que la restauración gane tiempo para la mitigación del cambio climático, pero carece de las directrices rigurosas para cumplir los objetivos de adaptabilidad y eficacia. Las lecciones que ha brindado la restauración de los ecosistemas terrestres pueden y deben adoptarse rápidamente en la restauración de arrecifes de coral. Proponemos una traducción de las diez reglas doradas de la restauración forestal efectiva para acelerar los esfuerzos para restaurar los arrecifes de coral con base en los principios establecidos de resiliencia, gestión y administración local. Resumimos pasos para emprender la restauración de arrecifes como una estrategia de manejo en el contexto de los valores diversos de los servicios ambientales. Estamos a tiempo de delinear un proyecto conforme más actores buscan restaurar con el inicio de la Década de la ONU para la Restauración de Ecosistemas.