No apparent trade-offs associated with heat tolerance in a reef-building coral.

As marine species adapt to climate change, their heat tolerance will likely be under strong selection. Yet trade-offs between heat tolerance and other life history traits could compromise natural adaptation or assisted evolution. This is particularly important for ecosystem engineers, such as reef-building corals, which support biodiversity yet are vulnerable to heatwave-induced mass bleaching and mortality. Here, we exposed 70 colonies of the reef-building coral Acropora digitifera to a long-term marine heatwave emulation experiment. We tested for trade-offs between heat tolerance and three traits measured from the colonies in situ - colony growth, fecundity, and symbiont community composition. Despite observing remarkable within-population variability in heat tolerance, all colonies were dominated by Cladocopium C40 symbionts. We found no evidence for trade-offs between heat tolerance and fecundity or growth. Contrary to expectations, positive associations emerged with growth, such that faster-growing colonies tended to bleach and die at higher levels of heat stress. Collectively, our results suggest that these corals exist on an energetic continuum where some high-performing individuals excel across multiple traits. Within populations, trade-offs between heat tolerance and growth or fecundity may not be major barriers to natural adaptation or the success of assisted evolution interventions.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Small-scale genetic structure of coral populations in Palau based on whole mitochondrial genomes: Implications for future coral resilience.

The ability of local populations to adapt to future climate conditions is facilitated by a balance between short range dispersal allowing local buildup of adaptively beneficial alleles, and longer dispersal moving these alleles throughout the species range. Reef building corals have relatively low dispersal larvae, but most population genetic studies show differentiation only over 100s of km. Here, we report full mitochondrial genome sequences from 284 tabletop corals (Acropora hyacinthus) from 39 patch reefs in Palau, and show two signals of genetic structure across reef scales from 1 to 55 km. First, divergent mitochondrial DNA haplotypes exist in different proportions from reef to reef, causing PhiST values of 0.02 (p = 0.02). Second, closely related sequences of mitochondrial Haplogroups are more likely to be co-located on the same reefs than expected by chance alone. We also compared these sequences to prior data on 155 colonies from American Samoa. In these comparisons, many Haplogroups in Palau were disproportionately represented or absent in American Samoa, and inter-regional PhiST = 0.259. However, we saw three instances of identical mitochondrial genomes between locations. Together, these data sets suggest two features of coral dispersal revealed by occurrence patterns in highly similar mitochondrial genomes. First, the Palau-American Samoa data suggest that long distance dispersal in corals is rare, as expected, but that it is common enough to deliver identical mitochondrial genomes across the Pacific. Second, higher than expected co-occurrence of Haplogroups on the same Palau reefs suggests greater retention of coral larvae on local reefs than predicted by many current oceanographic models of larval movement. Increased attention to local scales of coral genetic structure, dispersal, and selection may help increase the accuracy of models of future adaptation of corals and of assisted migration as a reef resilience intervention.

Coral bleaching resistance variation is linked to differential mortality and skeletal growth during recovery.

The prevalence of global coral bleaching has focused much attention on the possibility of interventions to increase heat resistance. However, if high heat resistance is linked to fitness tradeoffs that may disadvantage corals in other areas, then a more holistic view of heat resilience may be beneficial. In particular, overall resilience of a species to heat stress is likely to be the product of both resistance to heat and recovery from heat stress. Here, we investigate heat resistance and recovery among individual Acropora hyacinthus colonies in Palau. We divided corals into low, moderate, and high heat resistance categories based on the number of days (4-9) needed to reach significant pigmentation loss due to experimental heat stress. Afterward, we deployed corals back onto a reef in a common garden 6-month recovery experiment that monitored chlorophyll a, mortality, and skeletal growth. Heat resistance was negatively correlated with mortality during early recovery (0-1 month) but not late recovery (4-6 months), and chlorophyll a concentration recovered in heat-stressed corals by 1-month postbleaching. However, moderate-resistance corals had significantly greater skeletal growth than high-resistance corals by 4 months of recovery. High- and low-resistance corals on average did not exhibit skeletal growth within the observed recovery period. These data suggest complex tradeoffs may exist between coral heat resistance and recovery and highlight the importance of incorporating multiple aspects of resilience into future reef management programs.

Functional and phylogenetic responses of motile cryptofauna to habitat degradation.

Biodiversity of terrestrial and marine ecosystems, including coral reefs, is dominated by small, often cryptic, invertebrate taxa that play important roles in ecosystem structure and functioning. While cryptofauna community structure is determined by strong small-scale microhabitat associations, the extent to which ecological and environmental factors shape these communities are largely unknown, as is the relative importance of particular microhabitats in supporting reef trophodynamics from the bottom up. The goal of this study was to address these knowledge gaps, provided coral reefs are increasingly exposed to multiple disturbances and environmental gradients that influence habitat complexity, condition and ecosystem functioning. We compared the density, biomass, size range, phylogenetic diversity and functional roles of motile cryptofauna in Palau, Western Micronesia, among four coral-derived microhabitats representing various states of degradation (live coral [Acropora and Pocillopora], dead coral and coral rubble) from reefs along a gradient of effluent exposure. In total, 122 families across ten phyla were identified, dominated by the Arthropoda (Crustacea) and Mollusca. Cryptofauna biomass was greatest in live Pocillopora, while coral rubble contained the greatest density and diversity. Size ranges were broader in live corals than both dead coral and rubble. From a bottom-up perspective, effluent exposure had mixed effects on cryptic communities including a decline in total biomass in rubble. From a top-down perspective, cryptofauna were generally unaffected by predator biomass. Our data show that, as coral reef ecosystems continue to decline in response to more frequent and severe disturbances, habitats other than live coral may become increasingly important in supporting coral reef biodiversity and food webs.

Persistence of phenotypic responses to short-term heat stress in the tabletop coral Acropora hyacinthus.

Widespread mapping of coral thermal resilience is essential for developing effective management strategies and requires replicable and rapid multi-location assays of heat resistance and recovery. One- or two-day short-term heat stress experiments have been previously employed to assess heat resistance, followed by single assays of bleaching condition. We tested the reliability of short-term heat stress resistance, and linked resistance and recovery assays, by monitoring the phenotypic response of fragments from 101 Acropora hyacinthus colonies located in Palau (Micronesia) to short-term heat stress. Following short-term heat stress, bleaching and mortality were recorded after 16 hours, daily for seven days, and after one and two months of recovery. To follow corals over time, we utilized a qualitative, non-destructive visual bleaching score metric that correlated with standard symbiont retention assays. The bleaching state of coral fragments 16 hours post-heat stress was highly indicative of their state over the next 7 days, suggesting that symbiont population sizes within corals may quickly stabilize post-heat stress. Bleaching 16 hours post-heat stress predicted likelihood of mortality over the subsequent 3-5 days, after which there was little additional mortality. Together, bleaching and mortality suggested that rapid assays of the phenotypic response following short-term heat stress were good metrics of the total heat treatment effect. Additionally, our data confirm geographic patterns of intraspecific variation in Palau and show that bleaching severity among colonies was highly correlated with mortality over the first week post-stress. We found high survival (98%) and visible recovery (100%) two months after heat stress among coral fragments that survived the first week post-stress. These findings help simplify rapid, widespread surveys of heat sensitivity in Acropora hyacinthus by showing that standardized short-term experiments can be confidently assayed after 16 hours, and that bleaching sensitivity may be linked to subsequent survival using experimental assessments.

Within-population variability in coral heat tolerance indicates climate adaptation potential.

Coral reefs are facing unprecedented mass bleaching and mortality events due to marine heatwaves and climate change. To avoid extirpation, corals must adapt. Individual variation in heat tolerance and its heritability underpin the potential for coral adaptation. However, the magnitude of heat tolerance variability within coral populations is largely unresolved. We address this knowledge gap by exposing corals from a single reef to an experimental marine heatwave. We found that double the heat stress dosage was required to induce bleaching in the most-tolerant 10%, compared to the least-tolerant 10% of the population. By the end of the heat stress exposure, all of the least-tolerant corals were dead, whereas the most-tolerant remained alive. To contextualize the scale of this result over the coming century, we show that under an ambitious future emissions scenario, such differences in coral heat tolerance thresholds equate to up to 17 years delay until the onset of annual bleaching and mortality conditions. However, this delay is limited to only 10 years under a high emissions scenario. Our results show substantial variability in coral heat tolerance which suggests scope for natural or assisted evolution to limit the impacts of climate change in the short-term. For coral reefs to persist through the coming century, coral adaptation must keep pace with ocean warming, and ambitious emissions reductions must be realized.

Plastics are a new threat to Palau's coral reefs.

Plastic pollution of the oceans has long been an ongoing and growing problem. Single-use plastic (plastic bags and microbeads) is responsible for most of this pollution. In recent years, studies have highlighted the importance of the size of plastic particles, and the impact of this pollution source on the environment. We determined the concentration of small marine plastics in seawater, sediments and beach sand around a pristine reef area (Republic of Palau) using very simple tools (plankton net, sieves, organic matter degradation, density separation, Nile red fluorochrome). In this study, we succeeded in detecting microplastic (MPs) particles and microplastic fibers, but also nanoplastic (NPs). These three types of particles were found in all samples with a large heterogeneity, from 0.01 to 0.09 particles L-1 and 0.17 to 32.13 particles g-1 DW for MPs in seawater, sediments and sand, respectively. Even when NPs were identified, the amounts of NPs were underestimated and varied from 0.09 to 0.43 particles L-1 in seawater and from 1.08 to 71.02 particles g-1 DW in sediment and sand, respectively. These variations could be attributed to the environmental characteristics of the different sites. This study shows that plastic pollution must be considered in environmental studies even in the most pristine locations. It also shows that NPs pollution is related to the amount of MPs found at the sites. To understand the effects of this plastic pollution, it is necessary that the next toxicological studies take into account the effects of this fraction that makes up the NPs.

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.

Widespread variation in heat tolerance and symbiont load are associated with growth tradeoffs in the coral Acropora hyacinthus in Palau.

Climate change is dramatically changing ecosystem composition and productivity, leading scientists to consider the best approaches to map natural resistance and foster ecosystem resilience in the face of these changes. Here, we present results from a large-scale experimental assessment of coral bleaching resistance, a critical trait for coral population persistence as oceans warm, in 221 colonies of the coral Acropora hyacinthus across 37 reefs in Palau. We find that bleaching-resistant individuals inhabit most reefs but are found more often in warmer microhabitats. Our survey also found wide variation in symbiont concentration among colonies, and that colonies with lower symbiont load tended to be more bleaching-resistant. By contrast, our data show that low symbiont load comes at the cost of lower growth rate, a tradeoff that may operate widely among corals across environments. Corals with high bleaching resistance have been suggested as a source for habitat restoration or selective breeding in order to increase coral reef resilience to climate change. Our maps show where these resistant corals can be found, but the existence of tradeoffs with heat resistance may suggest caution in unilateral use of this one trait in restoration.

Potential local adaptation of corals at acidified and warmed Nikko Bay, Palau.

Ocean warming and acidification caused by increases of atmospheric carbon dioxide are now thought to be major threats to coral reefs on a global scale. Here we evaluated the environmental conditions and benthic community structures in semi-closed Nikko Bay at the inner reef area in Palau, which has high pCO2 and seawater temperature conditions with high zooxanthellate coral coverage. Nikko Bay is a highly sheltered system with organisms showing low connectivity with surrounding environments, making this bay a unique site for evaluating adaptation and acclimatization responses of organisms to warmed and acidified environments. Seawater pCO2/Ωarag showed strong gradation ranging from 380 to 982 µatm (Ωarag: 1.79-3.66), and benthic coverage, including soft corals and turf algae, changed along with Ωarag while hard coral coverage did not change. In contrast to previous studies, net calcification was maintained in Nikko Bay even under very low mean Ωarag (2.44). Reciprocal transplantation of the dominant coral Porites cylindrica showed that the calcification rate of corals from Nikko Bay did not change when transplanted to a reference site, while calcification of reference site corals decreased when transplanted to Nikko Bay. Corals transplanted out of their origin sites also showed the highest interactive respiration (R) and lower gross photosynthesis (Pg) to respiration (Pg:R), indicating higher energy acquirement of corals at their origin site. The results of this study give important insights about the potential local acclimatization and adaptation capacity of corals to different environmental conditions including pCO2 and temperature.

Predicting coral-reef futures from El Niño and Pacific Decadal Oscillation events.

El Niño Southern Oscillation (ENSO) events modulate oceanographic processes that control temperature and productivity in tropical waters, yet potential interactions with low frequency climate variability, such as the Pacific Decadal Oscillation (PDO), are poorly understood. We show that ENSO and PDO together predicted (i) maximum sea-surface temperatures (SST), which were associated with coral bleaching and declines in coral cover, and (ii) maximum chlorophyll-a concentrations, which were associated with high densities of coral-predatory Acanthaster starfish, across the tropical north Pacific Ocean since 1980. Asynchrony between the positive PDO and negative ENSO (i.e., La Niña) was associated with peaks in annual SST. By contrast, synchrony between the positive PDO and positive ENSO (i.e., El Niño) was associated with peaks in chlorophyll-a. Both conditions led to ecological disturbances and significant loss of coral cover, however, spatial models revealed where impacts to reefs were expected under varying climate scenarios.  The 2015/17 ENSO event was coupled with a positive PDO and resulted in high SST and Acanthaster abundances in eastern Micronesia, while positive coral growth occurred in western Micronesia.  Our novel approach for forecasting coral growth into the future may be applicable to other oceanic regions with differing oceanographic modulators.

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.

Conservation policies informed by food system feedbacks can avoid unintended consequences.

Understanding the feedbacks between food systems and conservation policies can help avoid unintended environmental consequences. Using a survey-based choice experiment and economic modelling, we quantify the potential impact of tourists' responses to a shift in offshore fish supply after the designation of a large-scale marine protected area in Palau. We find that this conservation policy may increase offshore fish prices and tourists' consumption of reef fish, thereby further endangering local reef ecosystems. However, if tourists are offered a sustainable offshore choice, their demand for fish could be kept at current levels, and environmental impacts from increased reef fish consumption would be avoided.

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.

Addressing Criticisms of Large-Scale Marine Protected Areas.

Designated large-scale marine protected areas (LSMPAs, 100,000 or more square kilometers) constitute over two-thirds of the approximately 6.6% of the ocean and approximately 14.5% of the exclusive economic zones within marine protected areas. Although LSMPAs have received support among scientists and conservation bodies for wilderness protection, regional ecological connectivity, and improving resilience to climate change, there are also concerns. We identified 10 common criticisms of LSMPAs along three themes: (1) placement, governance, and management; (2) political expediency; and (3) social-ecological value and cost. Through critical evaluation of scientific evidence, we discuss the value, achievements, challenges, and potential of LSMPAs in these arenas. We conclude that although some criticisms are valid and need addressing, none pertain exclusively to LSMPAs, and many involve challenges ubiquitous in management. We argue that LSMPAs are an important component of a diversified management portfolio that tempers potential losses, hedges against uncertainty, and enhances the probability of achieving sustainably managed oceans.

Size, age, and habitat determine effectiveness of Palau's Marine Protected Areas.

Palau has a rich heritage of conservation that has evolved from the traditional moratoria on fishing, or "bul", to more western Marine Protected Areas (MPAs), while still retaining elements of customary management and tenure. In 2003, the Palau Protected Areas Network (PAN) was created to conserve Palau's unique biodiversity and culture, and is the country's mechanism for achieving the goals of the Micronesia Challenge (MC), an initiative to conserve ≥30% of near-shore marine resources within the region by 2020. The PAN comprises a network of numerous MPAs within Palau that vary in age, size, level of management, and habitat, which provide an excellent opportunity to test hypotheses concerning MPA design and function using multiple discreet sampling units. Our sampling design provided a robust space for time comparison to evaluate the relative influence of potential drivers of MPA efficacy. Our results showed that no-take MPAs had, on average, nearly twice the biomass of resource fishes (i.e. those important commercially, culturally, or for subsistence) compared to nearby unprotected areas. Biomass of non-resource fishes showed no differences between no-take areas and areas open to fishing. The most striking difference between no-take MPAs and unprotected areas was the more than 5-fold greater biomass of piscivorous fishes in the MPAs compared to fished areas. The most important determinates of no-take MPA success in conserving resource fish biomass were MPA size and years of protection. Habitat and distance from shore had little effect on resource fish biomass. The extensive network of MPAs in Palau likely provides important conservation and tourism benefits to the Republic, and may also provide fisheries benefits by protecting spawning aggregation sites, and potentially through adult spillover.