Coral reefs benefit from reduced land-sea impacts under ocean warming.

Coral reef ecosystems are being fundamentally restructured by local human impacts and climate-driven marine heatwaves that trigger mass coral bleaching and mortality1. Reducing local impacts can increase reef resistance to and recovery from bleaching2. However, resource managers lack clear advice on targeted actions that best support coral reefs under climate change3 and sector-based governance means most land- and sea-based management efforts remain siloed4. Here we combine surveys of reef change with a unique 20-year time series of land-sea human impacts that encompassed an unprecedented marine heatwave in Hawai'i. Reefs with increased herbivorous fish populations and reduced land-based impacts, such as wastewater pollution and urban runoff, had positive coral cover trajectories predisturbance. These reefs also experienced a modest reduction in coral mortality following severe heat stress compared to reefs with reduced fish populations and enhanced land-based impacts. Scenario modelling indicated that simultaneously reducing land-sea human impacts results in a three- to sixfold greater probability of a reef having high reef-builder cover four years postdisturbance than if either occurred in isolation. International efforts to protect 30% of Earth's land and ocean ecosystems by 2030 are underway5. Our results reveal that integrated land-sea management could help achieve coastal ocean conservation goals and provide coral reefs with the best opportunity to persist in our changing climate.

Prey-size plastics are invading larval fish nurseries.

Life for many of the world's marine fish begins at the ocean surface. Ocean conditions dictate food availability and govern survivorship, yet little is known about the habitat preferences of larval fish during this highly vulnerable life-history stage. Here we show that surface slicks, a ubiquitous coastal ocean convergence feature, are important nurseries for larval fish from many ocean habitats at ecosystem scales. Slicks had higher densities of marine phytoplankton (1.7-fold), zooplankton (larval fish prey; 3.7-fold), and larval fish (8.1-fold) than nearby ambient waters across our study region in Hawai'i. Slicks contained larger, more well-developed individuals with competent swimming abilities compared to ambient waters, suggesting a physiological benefit to increased prey resources. Slicks also disproportionately accumulated prey-size plastics, resulting in a 60-fold higher ratio of plastics to larval fish prey than nearby waters. Dissections of hundreds of larval fish found that 8.6% of individuals in slicks had ingested plastics, a 2.3-fold higher occurrence than larval fish from ambient waters. Plastics were found in 7 of 8 families dissected, including swordfish (Xiphiidae), a commercially targeted species, and flying fish (Exocoetidae), a principal prey item for tuna and seabirds. Scaling up across an ∼1,000 km2 coastal ecosystem in Hawai'i revealed slicks occupied only 8.3% of ocean surface habitat but contained 42.3% of all neustonic larval fish and 91.8% of all floating plastics. The ingestion of plastics by larval fish could reduce survivorship, compounding threats to fisheries productivity posed by overfishing, climate change, and habitat loss.

First genealogy for a wild marine fish population reveals multigenerational philopatry.

Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.

Fire coral clones demonstrate phenotypic plasticity among reef habitats.

Clonal populations are often characterized by reduced levels of genotypic diversity, which can translate into lower numbers of functional phenotypes, both of which impede adaptation. Study of partially clonal animals enables examination of the environmental settings under which clonal reproduction is favoured. Here, we gathered genotypic and phenotypic information from 3,651 georeferenced colonies of the fire coral Millepora platyphylla in five habitats with different hydrodynamic regimes in Moorea, French Polynesia. In the upper slope where waves break, most colonies grew as vertical sheets ("sheet tree") making them more vulnerable to fragmentation. Nearly all fire corals in the other habitats are encrusting or massive. The M. platyphylla population is highly clonal (80% of the colonies are clones), while characterized by the highest genotype diversity ever documented for terrestrial or marine populations (1,064 genotypes). The proportion of clones varies greatly among habitats (≥58%-97%) and clones (328 clonal lineages) are distributed perpendicularly from the reef crest, perfectly aligned with wave energy. There are six clonal lineages with clones dispersed in at least two adjacent habitats that strongly demonstrate phenotypic plasticity. Eighty per cent of the colonies in these lineages are "sheet tree" on the upper slope, while 80%-100% are encrusting or massive on the mid slope and back reef. This is a unique example of phenotypic plasticity among reef-building coral clones as corals typically have wave-tolerant growth forms in high-energy reef areas.

Coral mass spawning predicted by rapid seasonal rise in ocean temperature.

Coral spawning times have been linked to multiple environmental factors; however, to what extent these factors act as generalized cues across multiple species and large spatial scales is unknown. We used a unique dataset of coral spawning from 34 reefs in the Indian and Pacific Oceans to test if month of spawning and peak spawning month in assemblages of Acropora spp. can be predicted by sea surface temperature (SST), photosynthetically available radiation, wind speed, current speed, rainfall or sunset time. Contrary to the classic view that high mean SST initiates coral spawning, we found rapid increases in SST to be the best predictor in both cases (month of spawning: R(2) = 0.73, peak: R(2) = 0.62). Our findings suggest that a rapid increase in SST provides the dominant proximate cue for coral mass spawning over large geographical scales. We hypothesize that coral spawning is ultimately timed to ensure optimal fertilization success.

Coral reef fish populations can persist without immigration.

Determining the conditions under which populations may persist requires accurate estimates of demographic parameters, including immigration, local reproductive success, and mortality rates. In marine populations, empirical estimates of these parameters are rare, due at least in part to the pelagic dispersal stage common to most marine organisms. Here, we evaluate population persistence and turnover for a population of orange clownfish, Amphiprion percula, at Kimbe Island in Papua New Guinea. All fish in the population were sampled and genotyped on five occasions at 2-year intervals spanning eight years. The genetic data enabled estimates of reproductive success retained in the same population (reproductive success to self-recruitment), reproductive success exported to other subpopulations (reproductive success to local connectivity), and immigration and mortality rates of sub-adults and adults. Approximately 50% of the recruits were assigned to parents from the Kimbe Island population and this was stable through the sampling period. Stability in the proportion of local and immigrant settlers is likely due to: low annual mortality rates and stable egg production rates, and the short larval stages and sensory capacities of reef fish larvae. Biannual mortality rates ranged from 0.09 to 0.55 and varied significantly spatially. We used these data to parametrize a model that estimated the probability of the Kimbe Island population persisting in the absence of immigration. The Kimbe Island population was found to persist without significant immigration. Model results suggest the island population persists because the largest of the subpopulations are maintained due to having low mortality and high self-recruitment rates. Our results enable managers to appropriately target and scale actions to maximize persistence likelihood as disturbance frequencies increase.

Operationalizing resilience for adaptive coral reef management under global environmental change.

Cumulative pressures from global climate and ocean change combined with multiple regional and local-scale stressors pose fundamental challenges to coral reef managers worldwide. Understanding how cumulative stressors affect coral reef vulnerability is critical for successful reef conservation now and in the future. In this review, we present the case that strategically managing for increased ecological resilience (capacity for stress resistance and recovery) can reduce coral reef vulnerability (risk of net decline) up to a point. Specifically, we propose an operational framework for identifying effective management levers to enhance resilience and support management decisions that reduce reef vulnerability. Building on a system understanding of biological and ecological processes that drive resilience of coral reefs in different environmental and socio-economic settings, we present an Adaptive Resilience-Based management (ARBM) framework and suggest a set of guidelines for how and where resilience can be enhanced via management interventions. We argue that press-type stressors (pollution, sedimentation, overfishing, ocean warming and acidification) are key threats to coral reef resilience by affecting processes underpinning resistance and recovery, while pulse-type (acute) stressors (e.g. storms, bleaching events, crown-of-thorns starfish outbreaks) increase the demand for resilience. We apply the framework to a set of example problems for Caribbean and Indo-Pacific reefs. A combined strategy of active risk reduction and resilience support is needed, informed by key management objectives, knowledge of reef ecosystem processes and consideration of environmental and social drivers. As climate change and ocean acidification erode the resilience and increase the vulnerability of coral reefs globally, successful adaptive management of coral reefs will become increasingly difficult. Given limited resources, on-the-ground solutions are likely to focus increasingly on actions that support resilience at finer spatial scales, and that are tightly linked to ecosystem goods and services.

Blacktip reef sharks, Carcharhinus melanopterus, have high genetic structure and varying demographic histories in their Indo-Pacific range.

For free-swimming marine species like sharks, only population genetics and demographic history analyses can be used to assess population health/status as baseline population numbers are usually unknown. We investigated the population genetics of blacktip reef sharks, Carcharhinus melanopterus; one of the most abundant reef-associated sharks and the apex predator of many shallow water reefs of the Indian and Pacific Oceans. Our sampling includes 4 widely separated locations in the Indo-Pacific and 11 islands in French Polynesia with different levels of coastal development. Four-teen microsatellite loci were analysed for samples from all locations and two mitochondrial DNA fragments, the control region and cytochrome b, were examined for 10 locations. For microsatellites, genetic diversity is higher for the locations in the large open systems of the Red Sea and Australia than for the fragmented habitat of the smaller islands of French Polynesia. Strong significant structure was found for distant locations with FST values as high as ~0.3, and a smaller but still significant structure is found within French Polynesia. Both mitochondrial genes show only a few mutations across the sequences with a dominant shared haplotype in French Polynesia and New Caledonia suggesting a common lineage different to that of East Australia. Demographic history analyses indicate population expansions in the Red Sea and Australia that may coincide with sea level changes after climatic events. Expansions and flat signals are indicated for French Polynesia as well as a significant recent bottleneck for Moorea, the most human-impacted lagoon of the locations in French Polynesia.

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline.

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.

A framework for responding to coral disease outbreaks that facilitates adaptive management.

Predicted increases in coral disease outbreaks associated with climate change have implications for coral reef ecosystems and the people and industries that depend on them. It is critical that coral reef managers understand these implications and have the ability to assess and reduce risk, detect and contain outbreaks, and monitor and minimise impacts. Here, we present a coral disease response framework that has four core components: (1) an early warning system, (2) a tiered impact assessment program, (3) scaled management actions and (4) a communication plan. The early warning system combines predictive tools that monitor the risk of outbreaks of temperature-dependent coral diseases with in situ observations provided by a network of observers who regularly report on coral health and reef state. Verified reports of an increase in disease prevalence trigger a tiered response of more detailed impact assessment, targeted research and/or management actions. The response is scaled to the risk posed by the outbreak, which is a function of the severity and spatial extent of the impacts. We review potential management actions to mitigate coral disease impacts and facilitate recovery, considering emerging strategies unique to coral disease and more established strategies to support reef resilience. We also describe approaches to communicating about coral disease outbreaks that will address common misperceptions and raise awareness of the coral disease threat. By adopting this framework, managers and researchers can establish a community of practice and can develop response plans for the management of coral disease outbreaks based on local needs. The collaborations between managers and researchers we suggest will enable adaptive management of disease impacts following evaluating the cost-effectiveness of emerging response actions and incrementally improving our understanding of outbreak causation.

Making a model meaningful to coral reef managers in a developing nation: a case study of overfishing and rock anchoring in Indonesia.

Most of the world's coral reefs line the coasts of developing nations, where impacts from intense and destructive fishing practices form critical conservation issues for managers. Overfishing of herbivorous fishes can cause phase shifts to macroalgal dominance, and fishers' use of rocks as anchors lowers coral cover, giving further competitive advantage to macroalgae. Overfishing and anchoring have been studied extensively, but the role of their interaction in lowering coral reef resilience has not been quantified formally. We analyzed the combined effects of overfishing and rock anchoring on a range of reef habitat types--varying from high coral and low macroalgae cover to low coral and high macroalgae cover--in a marine park in Indonesia. We parameterized a model of coral and algal dynamics with three intensities of anchoring and fishing pressure. Results of the model indicated that damage caused by rock anchoring was equal to or possibly more devastating to coral reefs in the area than the impact of overfishing. This is an important outcome for local managers, who usually have the funds to distribute less-damaging anchors, but normally are unable to patrol regularly and effectively enough to reduce the impact of overfishing. We translated model results into an interactive visual tool that allows managers to explore the benefits of reducing anchoring frequency and fishing pressure. The potential consequences of inaction were made clear: the likelihood that any of the reef habitats will be dominated in the future by macroalgae rather than corals depends on reducing anchoring frequency, fishing pressure, or both. The tool provides a platform for strengthened relationships between managers and conservationists and can facilitate the uptake of recommendations regarding resource allocation and management actions. Conservation efforts for coral reefs in developing nations are likely to benefit from transforming model projections of habitat condition into tools local managers can understand and interact with.

Warming Trends and Bleaching Stress of the World's Coral Reefs 1985-2012.

Coral reefs across the world's oceans are in the midst of the longest bleaching event on record (from 2014 to at least 2016). As many of the world's reefs are remote, there is limited information on how past thermal conditions have influenced reef composition and current stress responses. Using satellite temperature data for 1985-2012, the analysis we present is the first to quantify, for global reef locations, spatial variations in warming trends, thermal stress events and temperature variability at reef-scale (~4 km). Among over 60,000 reef pixels globally, 97% show positive SST trends during the study period with 60% warming significantly. Annual trends exceeded summertime trends at most locations. This indicates that the period of summer-like temperatures has become longer through the record, with a corresponding shortening of the 'winter' reprieve from warm temperatures. The frequency of bleaching-level thermal stress increased three-fold between 1985-91 and 2006-12 - a trend climate model projections suggest will continue. The thermal history data products developed enable needed studies relating thermal history to bleaching resistance and community composition. Such analyses can help identify reefs more resilient to thermal stress.

A robust operational model for predicting where tropical cyclone waves damage coral reefs.

Tropical cyclone (TC) waves can severely damage coral reefs. Models that predict where to find such damage (the 'damage zone') enable reef managers to: 1) target management responses after major TCs in near-real time to promote recovery at severely damaged sites; and 2) identify spatial patterns in historic TC exposure to explain habitat condition trajectories. For damage models to meet these needs, they must be valid for TCs of varying intensity, circulation size and duration. Here, we map damage zones for 46 TCs that crossed Australia's Great Barrier Reef from 1985-2015 using three models - including one we develop which extends the capability of the others. We ground truth model performance with field data of wave damage from seven TCs of varying characteristics. The model we develop (4MW) out-performed the other models at capturing all incidences of known damage. The next best performing model (AHF) both under-predicted and over-predicted damage for TCs of various types. 4MW and AHF produce strikingly different spatial and temporal patterns of damage potential when used to reconstruct past TCs from 1985-2015. The 4MW model greatly enhances both of the main capabilities TC damage models provide to managers, and is useful wherever TCs and coral reefs co-occur.

Overfishing and nutrient pollution interact with temperature to disrupt coral reefs down to microbial scales.

Losses of corals worldwide emphasize the need to understand what drives reef decline. Stressors such as overfishing and nutrient pollution may reduce resilience of coral reefs by increasing coral-algal competition and reducing coral recruitment, growth and survivorship. Such effects may themselves develop via several mechanisms, including disruption of coral microbiomes. Here we report the results of a 3-year field experiment simulating overfishing and nutrient pollution. These stressors increase turf and macroalgal cover, destabilizing microbiomes, elevating putative pathogen loads, increasing disease more than twofold and increasing mortality up to eightfold. Above-average temperatures exacerbate these effects, further disrupting microbiomes of unhealthy corals and concentrating 80% of mortality in the warmest seasons. Surprisingly, nutrients also increase bacterial opportunism and mortality in corals bitten by parrotfish, turning normal trophic interactions deadly for corals. Thus, overfishing and nutrient pollution impact reefs down to microbial scales, killing corals by sensitizing them to predation, above-average temperatures and bacterial opportunism.

Changes in bleaching susceptibility among corals subject to ocean warming and recurrent bleaching in Moorea, French Polynesia.

BACKGROUND: Climate-induced coral bleaching poses a major threat to coral reef ecosystems, mostly because of the sensitivities of key habitat-forming corals to increasing temperature. However, susceptibility to bleaching varies greatly among coral genera and there are likely to be major changes in the relative abundance of different corals, even if the wholesale loss of corals does not occur for several decades. Here we document variation in bleaching susceptibility among key genera of reef-building corals in Moorea, French Polynesia, and compare bleaching incidence during mass-bleaching events documented in 1991, 1994, 2002 and 2007. METHODOLOGY/PRINCIPAL FINDINGS: This study compared the proportion of colonies that bleached for four major genera of reef-building corals (Acropora, Montipora, Pocillopora and Porites), during each of four well-documented bleaching events from 1991 to 2007. Acropora and Montipora consistently bleached in far greater proportions (up to 98%) than Pocillopora and Porites. However, there was an apparent and sustained decline in the proportion of colonies that bleached during successive bleaching events, especially for Acropora and Montipora. In 2007, only 77% of Acropora colonies bleached compared with 98% in 1991. Temporal variation in the proportion of coral colonies bleached may be attributable to differences in environmental conditions among years. Alternately, the sustained declines in bleaching incidence among highly susceptible corals may be indicative of acclimation or adaptation. CONCLUSIONS/SIGNIFICANCE: Coral genera that are highly susceptible to coral bleaching, and especially Acropora and Montipora, exhibit temporal declines in their susceptibility to thermal anomalies at Moorea, French Polynesia. One possible explanation for these findings is that gradual removal of highly susceptible genotypes (through selective mortality of individuals, populations, and/or species) is producing a coral assemblage that is more resistant to sustained and ongoing ocean warming.

Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress.

BACKGROUND: Coral bleaching events vary in severity, however, to date, the hierarchy of susceptibility to bleaching among coral taxa has been consistent over a broad geographic range and among bleaching episodes. Here we examine the extent of spatial and temporal variation in thermal tolerance among scleractinian coral taxa and between locations during the 2010 thermally induced, large-scale bleaching event in South East Asia. METHODOLOGY/PRINCIPAL FINDINGS: Surveys to estimate the bleaching and mortality indices of coral genera were carried out at three locations with contrasting thermal and bleaching histories. Despite the magnitude of thermal stress being similar among locations in 2010, there was a remarkable contrast in the patterns of bleaching susceptibility. Comparisons of bleaching susceptibility within coral taxa and among locations revealed no significant differences between locations with similar thermal histories, but significant differences between locations with contrasting thermal histories (Friedman = 34.97; p<0.001). Bleaching was much less severe at locations that bleached during 1998, that had greater historical temperature variability and lower rates of warming. Remarkably, Acropora and Pocillopora, taxa that are typically highly susceptible, although among the most susceptible in Pulau Weh (Sumatra, Indonesia) where respectively, 94% and 87% of colonies died, were among the least susceptible in Singapore, where only 5% and 12% of colonies died. CONCLUSIONS/SIGNIFICANCE: The pattern of susceptibility among coral genera documented here is unprecedented. A parsimonious explanation for these results is that coral populations that bleached during the last major warming event in 1998 have adapted and/or acclimatised to thermal stress. These data also lend support to the hypothesis that corals in regions subject to more variable temperature regimes are more resistant to thermal stress than those in less variable environments.

Prioritizing key resilience indicators to support coral reef management in a changing climate.

Managing coral reefs for resilience to climate change is a popular concept but has been difficult to implement because the empirical scientific evidence has either not been evaluated or is sometimes unsupportive of theory, which leads to uncertainty when considering methods and identifying priority reefs. We asked experts and reviewed the scientific literature for guidance on the multiple physical and biological factors that affect the ability of coral reefs to resist and recover from climate disturbance. Eleven key factors to inform decisions based on scaling scientific evidence and the achievability of quantifying the factors were identified. Factors important to resistance and recovery, which are important components of resilience, were not strongly related, and should be assessed independently. The abundance of resistant (heat-tolerant) coral species and past temperature variability were perceived to provide the greatest resistance to climate change, while coral recruitment rates, and macroalgae abundance were most influential in the recovery process. Based on the 11 key factors, we tested an evidence-based framework for climate change resilience in an Indonesian marine protected area. The results suggest our evidence-weighted framework improved upon existing un-weighted methods in terms of characterizing resilience and distinguishing priority sites. The evaluation supports the concept that, despite high ecological complexity, relatively few strong variables can be important in influencing ecosystem dynamics. This is the first rigorous assessment of factors promoting coral reef resilience based on their perceived importance, empirical evidence, and feasibility of measurement. There were few differences between scientists' perceptions of factor importance and the scientific evidence found in journal publications but more before and after impact studies will be required to fully test the validity of all the factors. The methods here will increase the feasibility and defensibility of including key resilience metrics in evaluations of coral reefs, as well as reduce costs. Adaptation, marine protected areas, priority setting, resistance, recovery.