Coloring coral larvae allows tracking of local dispersal and settlement.

Quantifying patterns of dispersal and settlement in marine benthic invertebrates is challenging, largely due the complexity of life history traits, small sizes of larvae (<1 mm), and potential for large-scale dispersal (>100 km) in the marine environment. Here, we develop a novel method that allows for immediate differentiation and visual tracking of large numbers of coral larvae (106 to 109) from dispersal to settlement. Neutral red and Nile blue stains were extremely effective in coloring larvae, with minimal impacts on survival and settlement following optimization of incubation times and stain concentrations. Field validation to wild-captured larvae from the Great Barrier Reef demonstrates the efficacy of staining across diverse taxa. The method provides a simple, rapid (<60 minutes), low-cost (approximately USD$1 per 105 larva) tool to color coral larvae that facilitates a wide range of de novo laboratory and field studies of larval behavior and ecology with potential applications for conservation planning and understanding patterns of connectivity.

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.

Limitations to coral recovery along an environmental stress gradient.

Positive feedbacks driving habitat-forming species recovery and population growth are often lost as ecosystems degrade. For such systems, identifying mechanisms that limit the re-establishment of critical positive feedbacks is key to facilitating recovery. Theory predicts the primary drivers limiting system recovery shift from biological to physical as abiotic stress increases, but recent work has demonstrated that this seldom happens. We combined field and laboratory experiments to identify variation in limitations to coral recovery along an environmental stress gradient at Ningaloo Reef and Exmouth Gulf in northwest Australia. Many reefs in the region are coral depauperate due to recent cyclones and thermal stress. In general, recovery trajectories are prolonged due to limited coral recruitment. Consistent with theory, clearer water reefs under low thermal stress appear limited by biological interactions: competition with turf algae caused high mortality of newly settled corals and upright macroalgal stands drove mortality in transplanted juvenile corals. Laboratory experiments showed a positive relationship between crustose coralline algae cover and coral settlement, but only in the absence of sedimentation. Contrary to expectation, coral recovery does not appear limited by the survival or growth of recruits on turbid reefs under higher thermal stress, but to exceptionally low larval supply. Laboratory experiments showed that larval survival and settlement are unaffected by seawater quality across the study region. Rather, connectivity models predicted that many of the more turbid reefs in the Gulf are predominantly self seeded, receiving limited supply under degraded reef states. Overall, we find that the influence of oceanography can overwhelm the influences of physical and biological interactions on recovery potential at locations where environmental stressors are high, whereas populations in relatively benign physical conditions are predominantly structured by local ecological drivers. Such context-dependent information can help guide expectations and assist managers in optimizing strategies for spatial conservation planning for system recovery.

Benthic micro- and macro-community succession and coral recruitment under overfishing and nutrient enrichment.

Herbivory and nutrient availability are fundamental drivers of benthic community succession in shallow marine systems, including coral reefs. Despite the importance of early community succession for coral recruitment and recovery, studies characterizing the impact of top-down and bottom-up drivers on micro- and macrobenthic communities at scales relevant to coral recruitment are lacking. Here, a combination of tank and field experiments were used to assess the effects of herbivore exclusion and nutrient enrichment on micro- to macrobenthic community succession and subsequent coral recruitment success. Herbivore exclusion had the strongest effect on micro- and macrobenthic community succession, including a community shift toward copiotrophic and potentially opportunistic/pathogenic microorganisms, an increased cover of turf and macroalgae, and decreased cover of crustose coralline algae. Yet, when corals settled prior to the development of a macrobenthic community, rates of post-settlement survival increased when herbivores were excluded, benefiting from the predation refugia provided by cages during their vulnerable early post-settlement stage. Interestingly, survival on open tiles was negatively correlated with the relative abundance of the bacterial order Rhodobacterales, an opportunistic microbial group previously associated with stressed and diseased corals. Development of micro- and macrobenthic communities in the absence of herbivory, however, led to reduced coral settlement. In turn, there were no differences in post-settlement survival between open and caged treatments for corals settled on tiles with established benthic communities. As a result, open tiles experienced marginally higher recruitment rates, driven primarily by the higher initial number of settlers on open tiles compared to caged tiles. Overall, we reveal that the primary interaction driving coral recruitment is the positive effect of herbivory in creating crustose coralline algae (CCA)-dominated habitats, free of fleshy algae and associated opportunistic microbes, to enhance coral settlement. The negative direct and indirect impact of fish predation on newly settled corals was outweighed by the positive effect of herbivory on the initial rate of coral settlement. In turn, the addition of nutrients further altered benthic community succession in the absence of herbivory, reducing coral post-settlement survival. However, the overall impact of nutrients on coral recruitment dynamics was minor relative to herbivory.

Optimizing coral reef recovery with context-specific management actions at prioritized reefs.

Assisting the natural recovery of coral reefs through local management actions is needed in response to increasing ecosystem disturbances in the Anthropocene. There is growing evidence that commonly used resilience-based passive management approaches may not be sufficient to maintain coral reef key functions. We synthesize and discuss advances in coral reef recovery research, and its application to coral reef conservation and restoration practices. We then present a framework to guide the decision-making of reef managers, scientists and other stakeholders, to best support reef recovery after a disturbance. The overall aim of this management framework is to catalyse reef recovery, to minimize recovery times, and to limit the need for ongoing management interventions into the future. Our framework includes two main stages: first, a prioritization method for assessment following a large-scale disturbance, which is based on a reef's social-ecological values, and on a classification of the likelihood of recovery or succession resulting in degraded, novel, hybrid or historical states. Second, a flow chart to assist with determining management actions for highly valued reefs. Potential actions are chosen based on the ecological attributes of the disturbed reef, defined during ecological assessments. Depending on the context, management actions may include (1) substrata rehabilitation actions to facilitate natural coral recruitment, (2) repopulating actions using active restoration techniques, (3) resilience-based management actions and (4) monitoring coral recruitment and growth to assess the effectiveness of management interventions. We illustrate the proposed decision framework with a case study of typhoon-damaged eastern outer reefs in Palau, Micronesia. The decisions made following this framework lead to the conclusion that some reefs may not return to their historical state for many decades. However, if motivation and funds are available, new management approaches can be explored to assist coral reefs at valued locations to return to a functional state providing key ecosystem services.

An Indo-Pacific coral spawning database.

The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology.

Bright Spots in Coastal Marine Ecosystem Restoration.

The United Nations General Assembly calls for ecosystem restoration to be a primary intervention strategy used to counter the continued loss of natural habitats worldwide, while supporting human health and wellbeing globally. Restoration of coastal marine ecosystems is perceived by many to be expensive and prone to failure, in part explaining its low rates of implementation compared with terrestrial ecosystems. Yet, marine ecosystem restoration is a relatively new field, and we argue that assessments of its potential to answer this call should not rely on typical outcomes, but also to learn from successful outliers. Here, we review successful restoration efforts across a suite of metrics in coastal marine systems to highlight 'bright spots'. We find that, similar to terrestrial systems, restoration interventions can be effective over large spatial expanses (1,000s-100,000s ha), persist for decades, rapidly expand in size, be cost-effective, and generate social and economic benefits. These bright spots clearly demonstrate restoration of coastal marine systems can be used as a nature-based solution to improve biodiversity and support human health and wellbeing. Examining coastal marine restoration through a historical lens shows that it has developed over a shorter period than restoration in terrestrial systems, partially explaining lower efficiencies. Given these bright spots and the relative immaturity of coastal marine ecosystem restoration, it is likely to advance rapidly over the coming decades and become a common intervention strategy that can reverse marine degradation, contribute to local economies, and improve human wellbeing at a scale relevant to addressing global threats.

Relative roles of biological and physical processes influencing coral recruitment during the lag phase of reef community recovery.

Following disturbances, corals recolonize space through the process of recruitment consisting of the three phases of propagule supply, settlement, and post-settlement survival. Yet, each phase is influenced by biophysical factors, leading to recruitment success variability through space. To resolve the relative contributions of biophysical factors on coral recruitment, the recovery of a 150 km long coral reefs in Palau was investigated after severe typhoon disturbances. Overall, we found that benthic organisms had a relatively weak interactive influence on larval settlement rates at the scale of individual tiles, with negative effects mainly exerted from high wave exposure for Acropora corals. In contrast, juvenile coral densities were well predicted by biophysical drivers, through both direct and indirect pathways. High densities of Acropora and Poritidae juveniles were directly explained by the availability of substrata free from space competitors. Juvenile Montipora were found in higher densities where coralline algae coverage was high, which occurred at reefs with high wave exposure, while high densities of juvenile Pocilloporidae occurred on structurally complex reefs with high biomass of bioeroder fish. Our findings demonstrate that strengths of biophysical interactions were taxon-specific and had cascading effects on coral recruitment, which need consideration for predicting reef recovery and conservation strategies.

Setting priorities for conservation at the interface between ocean circulation, connectivity, and population dynamics.

Population persistence in the marine environment is driven by patterns of ocean circulation, larval dispersal, ecological interactions, and demographic rates. For habitat-forming organisms in particular, understanding the relationship between larval connectivity and meta-population dynamics aids in planning for marine spatial management. Here, we estimate networks of connectivity between fringing coral reefs in the northwest shelf of Australia by combining a particle tracking model based on shelf circulation with models of subpopulation dynamics of individual reefs. Coral cover data were used as a proxy for overall habitat quality, which can change as a result of natural processes, human-driven impacts, and management initiatives. We obtain three major results of conservation significance. First, the dynamics of the ecological network result from the interplay between network connectivity and ecological processes on individual reefs. The maximum coral cover a zone can sustain imposes a significant nonlinearity on the role an individual reef plays within the dynamics of the network, and thus on the impact of conservation interventions on specific reefs. Second, the role of an individual reef within these network dynamics changes considerably depending on the overall state of the system: a reef's role in sustaining the system's state can be different from the same reef's role in helping the system recover following major disturbance. Third, patterns of network connectivity change significantly as a function of yearly shelf circulation trends, and nonlinearity in network dynamics make mean connectivity a poor representation of yearly variations. From a management perspective, the priority list of reefs that are targets for management interventions depends crucially on what type of stressors (system-wide vs. localized) need addressing. This choice also depends not only on the ultimate purpose of management, but also on future oceanographic, climate change, and development scenarios that will determine the network connectivity and habitat quality.

Split spawning increases robustness of coral larval supply and inter-reef connectivity.

Many habitat-building corals undergo mass synchronous spawning events. Yet, despite the enormous amounts of larvae produced, larval dispersal from a single spawning event and the reliability of larval supply are highly dependent on vagaries of ocean currents. However, colonies from the same population will occasionally spawn over successive months. These split spawning events likely help to realign reproduction events to favourable environmental conditions. Here, we show that split spawning may benefit corals by increasing the reliability of larval supply. By modelling the dispersal of coral larvae across Australia's Great Barrier Reef, we find that split spawning increased the diversity of sources and reliability of larval supply the reefs could receive, especially in regions with low and intrinsically variable connectivity. Such increased larval supply might help counteract the expected declines in reproductive success associated with split spawning events.

Drivers of recovery and reassembly of coral reef communities.

Understanding processes that drive community recovery are needed to predict ecosystem trajectories and manage for impacts under increasing global threats. Yet, the quantification of community recovery in coral reefs has been challenging owing to a paucity of long-term ecological data and high frequency of disturbances. Here we investigate community re-assembly and the bio-physical drivers that determine the capacity of coral reefs to recover following the 1998 bleaching event, using long-term monitoring data across four habitats in Palau. Our study documents that the time needed for coral reefs to recover from bleaching disturbance to coral-dominated state in disturbance-free regimes is at least 9-12 years. Importantly, we show that reefs in two habitats achieve relative stability to a climax community state within that time frame. We then investigated the direct and indirect effects of drivers on the rate of recovery of four dominant coral groups using a structural equation modelling approach. While the rates of recovery differed among coral groups, we found that larval connectivity and juvenile coral density were prominent drivers of recovery for fast growing Acropora but not for the other three groups. Competitive algae and parrotfish had negative and positive effects on coral recovery in general, whereas wave exposure had variable effects related to coral morphology. Overall, the time needed for community re-assembly is habitat specific and drivers of recovery are taxa specific, considerations that require incorporation into planning for ecosystem management under climate change.

Coralline algal metabolites induce settlement and mediate the inductive effect of epiphytic microbes on coral larvae.

Settlement of invertebrates is a key process affecting the structure of marine communities and underpins the ability of benthic ecosystems to recover from disturbance. While it is known that specific crustose coralline algae (CCA) are important for settlement of some coral species, the role of algal chemical compounds versus surface microbial biofilms has long been ambiguous. Using a model system - a CCA of a genus that has been shown to induce high levels of settlement of Acropora corals (Titanoderma cf. tessellatum) and an abundant coral species (Acropora millepora)- we show that chemical effects of CCA are stronger than those from CCA surface microbial biofilms as drivers of coral settlement. Biofilms contributed to some extent to larval settlement via synergistic effects, where microbial cues were dependent on the CCA primary metabolism (production of dissolved organic carbon). We propose that optimal coral settlement is caused by complex biochemical communications among CCA, their epiphytic microbial community and coral larvae.

Acute drivers influence recent inshore Great Barrier Reef dynamics.

Understanding the dynamics of habitat-forming organisms is fundamental to managing natural ecosystems. Most studies of coral reef dynamics have focused on clear-water systems though corals inhabit many turbid regions. Here, we illustrate the key drivers of an inshore coral reef ecosystem using 10 years of biological, environmental, and disturbance data. Tropical cyclones, crown-of-thorns starfish, and coral bleaching are recognized as the major drivers of coral loss at mid- and offshore reefs along the Great Barrier Reef (GBR). In comparison, little is known about what drives temporal trends at inshore reefs closer to major anthropogenic stress. We assessed coral cover dynamics using state-space models within six major inshore GBR catchments. An overall decline was detected in nearly half (46%) of the 15 reefs at two depths (30 sites), while the rest exhibited fluctuating (23%), static (17%), or positive (13%) trends. Inshore reefs responded similarly to their offshore counterparts, where contemporary trends were predominantly influenced by acute disturbance events. Storms emerged as the major driver affecting the inshore GBR, with the effects of other drivers such as disease, juvenile coral density, and macroalgal and turf per cent cover varying from one catchment to another. Flooding was also associated with negative trends in live coral cover in two southern catchments, but the mechanism remains unclear as it is not reflected in available metrics of water quality and may act through indirect pathways.

Global mismatch of policy and research on drivers of biodiversity loss.

The United Nations 2030 Agenda for Sustainable Development calls for urgent actions to reduce global biodiversity loss. Here, we synthesize >44,000 articles published in the past decade to assess the research focus on global drivers of loss. Relative research efforts on different drivers are not well aligned with their assessed impact, and multiple driver interactions are hardly considered. Research on drivers of biodiversity loss needs urgent realignment to match predicted severity and inform policy goals.

Density-dependent coral recruitment displays divergent responses during distinct early life-history stages.

Population growth involves demographic bottlenecks that regulate recruitment success during various early life-history stages. The success of each early life-history stage can vary in response to population density, interacting with intrinsic (e.g. behavioural) and environmental (e.g. competition, predation) factors. Here, we used the common reef-building coral Acropora millepora to investigate how density-dependence influences larval survival and settlement in laboratory experiments that isolated intrinsic effects, and post-settlement survival in a field experiment that examined interactions with environmental factors. Larval survival was exceptionally high (greater than 80%) and density-independent from 2.5 to 12 days following spawning. By contrast, there was a weak positive effect of larval density on settlement, driven by gregarious behaviour at the highest density. When larval supply was saturated, settlement was three times higher in crevices compared with exposed microhabitats, but a negative relationship between settler density and post-settlement survival in crevices and density-independent survival on exposed surfaces resulted in similar recruit densities just one month following settlement. Moreover, a negative relationship was found between turf algae and settler survival in crevices, whereas gregarious settlement improved settler survival on exposed surfaces. Overall, our findings reveal divergent responses by coral larvae and newly settled recruits to density-dependent regulation, mediated by intrinsic and environmental interactions.

The influence of resilience-based management on coral reef monitoring: A systematic review.

With rapid changes taking place on coral reefs, managers and scientists are faced with prioritising interventions that might avoid undesirable losses in ecosystem health. The property of resilience captures how reefs react and respond to stressors and environmental changes. Therefore, in principle, management goals are more likely to be realised if resilience theory is used to inform decision making and help set realistic expectations for reef outcomes. Indeed, a new approach to reef management has been termed 'resilience-based management' (RBM). Yet, resilience concepts have often been criticised for being vague, difficult to operationalise, and beset by multiple definitions. Here, we evaluate how the advent of RBM has changed one aspect of reef management: assessment and monitoring. We compare the metrics used in conventional monitoring programs with those developed through resilience assessments and find that the latter have a stronger focus on ecological processes and exposure to environmental drivers. In contrast, monitoring tends to focus on metrics of reef state and has greater taxonomic resolution, which provides comprehensive information on the nature of changes but does not predict the future responses of reefs in part because it is difficult to extrapolate statistical trends of complex ecological systems. In addition, metrics measured by resilience studies are more diverse, owing in part to the reliance of state metrics as proxies of processes given the difficulty in quantifying key ecological processes directly. We conclude by describing practical ways of improving resilience assessments, and avenues for future research.

Sensitivity of coral recruitment to subtle shifts in early community succession.

Community succession following disturbance depends on positive and negative interactions, the strength of which change along environmental gradients. To investigate how early succession affects coral reef recovery, we conducted an 18-month experiment in Palau, using recruitment tiles and herbivore exclusion cages. One set of reefs has higher wave exposure and had previously undergone a phase shift to macroalgae following a major typhoon, whereas the other set of reefs have lower wave exposure and did not undergo a macroalgal phase shift. Similar successional trajectories were observed at all sites when herbivores were excluded: turf algae dominated early succession, followed by shifts to foliose macroalgae and heterotrophic invertebrates. However, trajectories differed in the presence of herbivores. At low wave exposure reefs, herbivores promoted coralline algae and limited turf and encrusting fleshy algae in crevice microhabitats, facilitating optimal coral recruitment. Under medium wave exposure, relatively higher but still low coverage of turf and encrusting fleshy algae (15-25%) found in crevice microhabitats inhibited coral recruitment, persisting throughout multiple recruitment events. Our results indicate that altered interaction strength in different wave environments following disturbance can drive subtle changes in early succession that cascade to alter secondary succession to coral recruitment and system recovery.

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp.

Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical-temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.