Research priorities for the sustainability of coral-rich western Pacific seascapes.

Nearly a billion people depend on tropical seascapes. The need to ensure sustainable use of these vital areas is recognised, as one of 17 policy commitments made by world leaders, in Sustainable Development Goal (SDG) 14 ('Life below Water') of the United Nations. SDG 14 seeks to secure marine sustainability by 2030. In a time of increasing social-ecological unpredictability and risk, scientists and policymakers working towards SDG 14 in the Asia-Pacific region need to know: (1) How are seascapes changing? (2) What can global society do about these changes? and (3) How can science and society together achieve sustainable seascape futures? Through a horizon scan, we identified nine emerging research priorities that clarify potential research contributions to marine sustainability in locations with high coral reef abundance. They include research on seascape geological and biological evolution and adaptation; elucidating drivers and mechanisms of change; understanding how seascape functions and services are produced, and how people depend on them; costs, benefits, and trade-offs to people in changing seascapes; improving seascape technologies and practices; learning to govern and manage seascapes for all; sustainable use, justice, and human well-being; bridging communities and epistemologies for innovative, equitable, and scale-crossing solutions; and informing resilient seascape futures through modelling and synthesis. Researchers can contribute to the sustainability of tropical seascapes by co-developing transdisciplinary understandings of people and ecosystems, emphasising the importance of equity and justice, and improving knowledge of key cross-scale and cross-level processes, feedbacks, and thresholds.

Interventions to help coral reefs under global change-A complex decision challenge.

Climate change is impacting coral reefs now. Recent pan-tropical bleaching events driven by unprecedented global heat waves have shifted the playing field for coral reef management and policy. While best-practice conventional management remains essential, it may no longer be enough to sustain coral reefs under continued climate change. Nor will climate change mitigation be sufficient on its own. Committed warming and projected reef decline means solutions must involve a portfolio of mitigation, best-practice conventional management and coordinated restoration and adaptation measures involving new and perhaps radical interventions, including local and regional cooling and shading, assisted coral evolution, assisted gene flow, and measures to support and enhance coral recruitment. We propose that proactive research and development to expand the reef management toolbox fast but safely, combined with expedient trialling of promising interventions is now urgently needed, whatever emissions trajectory the world follows. We discuss the challenges and opportunities of embracing new interventions in a race against time, including their risks and uncertainties. Ultimately, solutions to the climate challenge for coral reefs will require consideration of what society wants, what can be achieved technically and economically, and what opportunities we have for action in a rapidly closing window. Finding solutions that work for coral reefs and people will require exceptional levels of coordination of science, management and policy, and open engagement with society. It will also require compromise, because reefs will change under climate change despite our best interventions. We argue that being clear about society's priorities, and understanding both the opportunities and risks that come with an expanded toolset, can help us make the most of a challenging situation. We offer a conceptual model to help reef managers frame decision problems and objectives, and to guide effective strategy choices in the face of complexity and uncertainty.

Reduced diversity and stability of coral-associated bacterial communities and suppressed immune function precedes disease onset in corals.

Disease is an emerging threat to coral reef ecosystems worldwide, highlighting the need to understand how environmental conditions interact with coral immune function and associated microbial communities to affect holobiont health. Increased coral disease incidence on reefs adjacent to permanently moored platforms on Australia's Great Barrier Reef provided a unique case study to investigate environment-host-microbe interactions in situ. Here, we evaluate coral-associated bacterial community (16S rRNA amplicon sequencing), immune function (protein-based prophenoloxidase-activating system), and water quality parameters before, during and after a disease event. Over the course of the study, 31% of tagged colonies adjacent to platforms developed signs of white syndrome (WS), while all control colonies on a platform-free reef remained visually healthy. Corals adjacent to platforms experienced significant reductions in coral immune function. Additionally, the corals at platform sites that remained visually healthy throughout the study had reduced bacterial diversity compared to healthy colonies at the platform-free site. Interestingly, prior to the observation of macroscopic disease, corals that would develop WS had reduced bacterial diversity and significantly greater community heterogeneity between colonies compared to healthy corals at the same location. These results suggest that activities associated with offshore marine infrastructure impacts coral immunocompetence and associated bacterial community, which affects the susceptibility of corals to disease.

Microbial indicators of environmental perturbations in coral reef ecosystems.

BACKGROUND: Coral reefs are facing unprecedented pressure on local and global scales. Sensitive and rapid markers for ecosystem stress are urgently needed to underpin effective management and restoration strategies. Although the fundamental contribution of microbes to the stability and functioning of coral reefs is widely recognised, it remains unclear how different reef microbiomes respond to environmental perturbations and whether microbiomes are sensitive enough to predict environmental anomalies that can lead to ecosystem stress. However, the lack of coral reef microbial baselines hinders our ability to study the link between shifts in microbiomes and ecosystem stress. In this study, we established a comprehensive microbial reference database for selected Great Barrier Reef sites to assess the diagnostic value of multiple free-living and host-associated reef microbiomes to infer the environmental state of coral reef ecosystems. RESULTS: A comprehensive microbial reference database, originating from multiple coral reef microbiomes (i.e. seawater, sediment, corals, sponges and macroalgae), was generated by 16S rRNA gene sequencing for 381 samples collected over the course of 16 months. By coupling this database to environmental parameters, we showed that the seawater microbiome has the greatest diagnostic value to infer shifts in the surrounding reef environment. In fact, 56% of the observed compositional variation in the microbiome was explained by environmental parameters, and temporal successions in the seawater microbiome were characterised by uniform community assembly patterns. Host-associated microbiomes, in contrast, were five-times less responsive to the environment and their community assembly patterns were generally less uniform. By applying a suite of indicator value and machine learning approaches, we further showed that seawater microbial community data provide an accurate prediction of temperature and eutrophication state (i.e. chlorophyll concentration and turbidity). CONCLUSION: Our results reveal that free-living microbial communities have a high potential to infer environmental parameters due to their environmental sensitivity and predictability. This highlights the diagnostic value of microorganisms and illustrates how long-term coral reef monitoring initiatives could be enhanced by incorporating assessments of microbial communities in seawater. We therefore recommend timely integration of microbial sampling into current coral reef monitoring initiatives.

High spatio-temporal variability in Acroporidae settlement to inshore reefs of the Great Barrier Reef.

Recovery of coral reefs after disturbance relies heavily on replenishment through successful larval settlement and their subsequent survival. As part of an integrated study to determine the potential effects of water quality changes on the resilience of inshore coral communities, scleractinian coral settlement was monitored between 2006 and 2012 at 12 reefs within the inshore Great Barrier Reef. Settlement patterns were only analysed for the family Acroporidae, which represented the majority (84%) of settled larvae. Settlement of Acroporidae to terracotta tiles averaged 0.11 cm-2, representing 34 ± 31.01 (mean ± SD) spat per tile, indicating an abundant supply of competent larvae to the study reefs. Settlement was highly variable among reefs and between years. Differences in settlement among locations partly corresponded to the local cover of adult Acroporidae, while substantial reductions in Acroporidae cover caused by tropical cyclones and floods resulted in a clear reduction in settlement. Much of the observed variability remained unexplained, although likely included variability in both connectivity to, and the fecundity of, adult Acroporidae. The responsiveness of settlement patterns to the decline in Acroporidae cover across all four regions indicates the importance of supply and connectivity, and the vulnerability towards region-wide disturbance. High spatial and temporal variability, in addition to the resource-intensive nature of sampling with settlement tiles, highlights the logistical difficulty of determining coral settlement over large spatial and temporal scales.

Support for improved quality control but misplaced criticism of GBR science. Reply to viewpoint "The need for a formalised system of Quality Control for environmental policy-science" by P. Larcombe and P. Ridd (Marine Pollution Bulletin 126: 449-461, 2018).

This is a response to the published Viewpoint by Larcombe and Ridd (2018). We agree with Larcombe and Ridd (2018) that scientific merit goes hand in hand with rigorous quality control. However, we are responding here to several points raised by Larcombe and Ridd (2018) which in our view were misrepresented. We describe the formal and effective science review, synthesis and advice processes that are in place for science supporting decision-making in the Great Barrier Reef. We also respond in detail to critiques of selected publications that were used by Larcombe and Ridd (2018) as a case study to illustrate shortcomings in science quality control. We provide evidence that their representation of the published research and arguments to support the statement that "many (…) conclusions are demonstrably incorrect" is based on misinterpretation, selective use of data and over-simplification, and also ignores formal responses to previously published critiques.

Shifting paradigms in restoration of the world's coral reefs.

Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine-protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014-2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.

Correction: Sediment and Turbidity Associated with Offshore Dredging Increase Coral Disease Prevalence on Nearby Reefs.

[This corrects the article DOI: 10.1371/journal.pone.0102498.].

Towards protecting the Great Barrier Reef from land-based pollution.

The Great Barrier Reef (GBR) is an iconic coral reef system extending over 2000 km along the north-east coast of Australia. Global recognition of its Outstanding Universal Value resulted in the listing of the 348 000 km(2) GBR World Heritage Area (WHA) by UNESCO in 1981. Despite various levels of national and international protection, the condition of GBR ecosystems has deteriorated over the past decades, with land-based pollution from the adjacent catchments being a major and ongoing cause for this decline. To reduce land-based pollution, the Australian and Queensland Governments have implemented a range of policy initiatives since 2003. Here, we evaluate the effectiveness of existing initiatives to reduce discharge of land-based pollutants into the waters of the GBR. We conclude that recent efforts in the GBR catchments to reduce land-based pollution are unlikely to be sufficient to protect the GBR ecosystems from declining water quality within the aspired time frames. To support management decisions for desired ecological outcomes for the GBR WHA, we identify potential improvements to current policies and incentives, as well as potential changes to current agricultural land use, based on overseas experiences and Australia's unique potential. The experience in the GBR may provide useful guidance for the management of other marine ecosystems, as reducing land-based pollution by better managing agricultural sources is a challenge for coastal communities around the world.

Marine microbial communities of the Great Barrier Reef lagoon are influenced by riverine floodwaters and seasonal weather events.

The role of microorganisms in maintaining coral reef health is increasingly recognized. Riverine floodwater containing herbicides and excess nutrients from fertilizers compromises water quality in the inshore Great Barrier Reef (GBR), with unknown consequences for planktonic marine microbial communities and thus coral reefs. In this baseline study, inshore GBR microbial communities were monitored along a 124 km long transect between 2011 and 2013 using 16S rRNA gene amplicon sequencing. Members of the bacterial orders Rickettsiales (e.g., Pelagibacteraceae) and Synechococcales (e.g., Prochlorococcus), and of the archaeal class Marine Group II were prevalent in all samples, exhibiting a clear seasonal dynamics. Microbial communities near the Tully river mouth included a mixture of taxa from offshore marine sites and from the river system. The environmental parameters collected could be summarized into four groups, represented by salinity, rainfall, temperature and water quality, that drove the composition of microbial communities. During the wet season, lower salinity and a lower water quality index resulting from higher river discharge corresponded to increases in riverine taxa at sites near the river mouth. Particularly large, transient changes in microbial community structure were seen during the extreme wet season 2010-11, and may be partially attributed to the effects of wind and waves, which resuspend sediments and homogenize the water column in shallow near-shore regions. This work shows that anthropogenic floodwaters and other environmental parameters work in conjunction to drive the spatial distribution of microorganisms in the GBR lagoon, as well as their seasonal and daily dynamics.

Informing policy to protect coastal coral reefs: insight from a global review of reducing agricultural pollution to coastal ecosystems.

The continuing degradation of coral reefs has serious consequences for the provision of ecosystem goods and services to local and regional communities. While climate change is considered the most serious risk to coral reefs, agricultural pollution threatens approximately 25% of the total global reef area with further increases in sediment and nutrient fluxes projected over the next 50 years. Here, we aim to inform coral reef management using insights learned from management examples that were successful in reducing agricultural pollution to coastal ecosystems. We identify multiple examples reporting reduced fluxes of sediment and nutrients at end-of-river, and associated declines in nutrient concentrations and algal biomass in receiving coastal waters. Based on the insights obtained, we recommend that future protection of coral reef ecosystems demands policy focused on desired ecosystem outcomes, targeted regulatory approaches, up-scaling of watershed management, and long-term maintenance of scientifically robust monitoring programs linked with adaptive management.

Sediment and turbidity associated with offshore dredging increase coral disease prevalence on nearby reefs.

In recent decades, coral reef ecosystems have declined to the extent that reefs are now threatened globally. While many water quality parameters have been proposed to contribute to reef declines, little evidence exists conclusively linking specific water quality parameters with increased disease prevalence in situ. Here we report evidence from in situ coral health surveys confirming that chronic exposure to dredging-associated sediment plumes significantly increase the prevalence of white syndromes, a devastating group of globally important coral diseases. Coral health surveys were conducted along a dredging-associated sediment plume gradient to assess the relationship between sedimentation, turbidity and coral health. Reefs exposed to the highest number of days under the sediment plume (296 to 347 days) had two-fold higher levels of disease, largely driven by a 2.5-fold increase in white syndromes, and a six-fold increase in other signs of compromised coral health relative to reefs with little or no plume exposure (0 to 9 days). Multivariate modeling and ordination incorporating sediment exposure level, coral community composition and cover, predation and multiple thermal stress indices provided further confirmation that sediment plume exposure level was the main driver of elevated disease and other compromised coral health indicators. This study provides the first evidence linking dredging-associated sedimentation and turbidity with elevated coral disease prevalence in situ. Our results may help to explain observed increases in global coral disease prevalence in recent decades and suggest that minimizing sedimentation and turbidity associated with coastal development will provide an important management tool for controlling coral disease epizootics.

A bioindicator system for water quality on inshore coral reefs of the Great Barrier Reef.

Responses of bioindicator candidates for water quality were quantified in two studies on inshore coral reefs of the Great Barrier Reef (GBR). In Study 1, 33 of the 38 investigated candidate indicators (including coral physiology, benthos composition, coral recruitment, macrobioeroder densities and FORAM index) showed significant relationships with a composite index of 13 water quality variables. These relationships were confirmed in Study 2 along four other water quality gradients (turbidity and chlorophyll). Changes in water quality led to multi-faceted shifts from phototrophic to heterotrophic benthic communities, and from diverse coral dominated communities to low-diversity communities dominated by macroalgae. Turbidity was the best predictor of biota; hence turbidity measurements remain essential to directly monitor water quality on the GBR, potentially complemented by our final calibrated 12 bioindicators. In combination, this bioindicator system may be used to assess changes in water quality, especially where direct water quality data are unavailable.

Water quality in the inshore Great Barrier Reef lagoon: Implications for long-term monitoring and management.

Coastal and inshore areas of the Great Barrier Reef lagoon receive substantial amounts of material from adjacent developed catchments, which can affect the ecological integrity of coral reefs and other inshore ecosystems. A 5-year water quality monitoring dataset provides a 'base range' of water quality conditions for the inshore GBR lagoon and illustrates the considerable temporal and spatial variability in this system. Typical at many sites were high turbidity levels and elevated chlorophyll a and phosphorus concentrations, especially close to river mouths. Water quality variability was mainly driven by seasonal processes such as river floods and sporadic wind-driven resuspension as well as by regional differences such as land use. Extreme events, such as floods, caused large and sustained increases in water quality variables. Given the highly variable climate in the GBR region, long-term monitoring of marine water quality will be essential to detect future changes due to improved catchment management.

Assessing the additive risks of PSII herbicide exposure to the Great Barrier Reef.

Herbicide residues have been measured in the Great Barrier Reef lagoon at concentrations which have the potential to harm marine plant communities. Monitoring on the Great Barrier Reef lagoon following wet season discharge show that 80% of the time when herbicides are detected, more than one are present. These herbicides have been shown to act in an additive manner with regards to photosystem-II inhibition. In this study, the area of the Great Barrier Reef considered to be at risk from herbicides is compared when exposures are considered for each herbicide individually and also for herbicide mixtures. Two normalisation indices for herbicide mixtures were calculated based on current guidelines and PSII inhibition thresholds. The results show that the area of risk for most regions is greatly increased under the proposed additive PSII inhibition threshold and that the resilience of this important ecosystem could be reduced by exposure to these herbicides.

Seasonal rainfall and runoff promote coral disease on an inshore reef.

BACKGROUND: Declining water quality coupled with the effects of climate change are rapidly increasing coral diseases on reefs worldwide, although links between coral diseases and environmental parameters remain poorly understood. This is the first study to document a correlation between coral disease and water quality on an inshore reef. METHODOLOGY/PRINCIPAL FINDINGS: The temporal dynamics of the coral disease atramentous necrosis (AN) was investigated over two years within inshore populations of Montipora aequituberculata in the central Great Barrier Reef, in relation to rainfall, salinity, temperature, water column chlorophyll a, suspended solids, sedimentation, dissolved organic carbon, and particulate nitrogen, phosphorus and organic carbon. Overall, mean AN prevalence was 10-fold greater during summer wet seasons than winter dry seasons. A 2.5-fold greater mean disease abundance was detected during the summer of 2009 (44 ± SE 6.7 diseased colonies per 25 m(2)), when rainfall was 1.6-fold greater than in the summer of 2008. Two water quality parameters explained 67% of the variance in monthly disease prevalence in a Partial Least Squares regression analysis; disease abundance was negatively correlated with salinity (R2 = -0.6) but positively correlated with water column particulate organic carbon concentration (R2 = 0.32). Seasonal temperature patterns were also positively correlated with disease abundance, but explained only a small portion of the variance. CONCLUSIONS/SIGNIFICANCE: The results suggest that rainfall and associated runoff may facilitate seasonal disease outbreaks, potentially by reducing host fitness or by increasing pathogen virulence due to higher availability of nutrients and organic matter. In the future, rainfall and seawater temperatures are likely to increase due to climate change which may lead to decreased health of inshore reefs.

Chemical and physical environmental conditions underneath mat- and canopy-forming macroalgae, and their effects on understorey corals.

Disturbed coral reefs are often dominated by dense mat- or canopy-forming assemblages of macroalgae. This study investigated how such dense macroalgal assemblages change the chemical and physical microenvironment for understorey corals, and how the altered environmental conditions affect the physiological performance of corals. Field measurements were conducted on macroalgal-dominated inshore reefs in the Great Barrier Reef in quadrats with macroalgal biomass ranging from 235 to 1029 g DW m(-2) dry weight. Underneath mat-forming assemblages, the mean concentration of dissolved oxygen was reduced by 26% and irradiance by 96% compared with conditions above the mat, while concentrations of dissolved organic carbon and soluble reactive phosphorous increased by 26% and 267%, respectively. The difference was significant but less pronounced under canopy-forming assemblages. Dissolved oxygen declined and dissolved inorganic carbon and alkalinity increased with increasing algal biomass underneath mat-forming but not under canopy-forming assemblages. The responses of corals to conditions similar to those found underneath algal assemblages were investigated in an aquarium experiment. Coral nubbins of the species Acropora millepora showed reduced photosynthetic yields and increased RNA/DNA ratios when exposed to conditions simulating those underneath assemblages (pre-incubating seawater with macroalgae, and shading). The magnitude of these stress responses increased with increasing proportion of pre-incubated algal water. Our study shows that mat-forming and, to a lesser extent, canopy-forming macroalgal assemblages alter the physical and chemical microenvironment sufficiently to directly and detrimentally affect the metabolism of corals, potentially impeding reef recovery from algal to coral-dominated states after disturbance. Macroalgal dominance on coral reefs therefore simultaneously represents a consequence and cause of coral reef degradation.