Decline of a distinct coral reef holobiont community under ocean acidification.

BACKGROUND: Microbes play vital roles across coral reefs both in the environment and inside and upon macrobes (holobionts), where they support critical functions such as nutrition and immune system modulation. These roles highlight the potential ecosystem-level importance of microbes, yet most knowledge of microbial functions on reefs is derived from a small set of holobionts such as corals and sponges. Declining seawater pH - an important global coral reef stressor - can cause ecosystem-level change on coral reefs, providing an opportunity to study the role of microbes at this scale. We use an in situ experimental approach to test the hypothesis that under such ocean acidification (OA), known shifts among macrobe trophic and functional groups may drive a general ecosystem-level response extending across macrobes and microbes, leading to reduced distinctness between the benthic holobiont community microbiome and the environmental microbiome. RESULTS: We test this hypothesis using genetic and chemical data from benthic coral reef community holobionts sampled across a pH gradient from CO2 seeps in Papua New Guinea. We find support for our hypothesis; under OA, the microbiome and metabolome of the benthic holobiont community become less compositionally distinct from the sediment microbiome and metabolome, suggesting that benthic macrobe communities are colonised by environmental microbes to a higher degree under OA conditions. We also find a simplification and homogenisation of the benthic photosynthetic community, and an increased abundance of fleshy macroalgae, consistent with previously observed reef microbialisation. CONCLUSIONS: We demonstrate a novel structural shift in coral reefs involving macrobes and microbes: that the microbiome of the benthic holobiont community becomes less distinct from the sediment microbiome under OA. Our findings suggest that microbialisation and the disruption of macrobe trophic networks are interwoven general responses to environmental stress, pointing towards a universal, undesirable, and measurable form of ecosystem changed. Video Abstract.

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.

Macroalgal cover on coral reefs: Spatial and environmental predictors, and decadal trends in the Great Barrier Reef.

Macroalgae are an important component of coral reef ecosystems. We identified spatial patterns, environmental drivers and long-term trends of total cover of upright fleshy and calcareous coral reef inhabiting macroalgae in the Great Barrier Reef. The spatial study comprised of one-off surveys of 1257 sites (latitude 11-24°S, coastal to offshore, 0-18 m depth), while the temporal trends analysis was based on 26 years of long-term monitoring data from 93 reefs. Environmental predictors were obtained from in situ data and from the coupled hydrodynamic-biochemical model eReefs. Macroalgae dominated the benthos (≥50% cover) on at least one site of 40.4% of surveyed inshore reefs. Spatially, macroalgal cover increased steeply towards the coast, with latitude away from the equator, and towards shallow (≤3 m) depth. Environmental conditions associated with macroalgal dominance were: high tidal range, wave exposure and irradiance, and low aragonite saturation state, Secchi depth, total alkalinity and temperature. Evidence of space competition between macroalgal cover and hard coral cover was restricted to shallow inshore sites. Temporally, macroalgal cover on inshore and mid-shelf reefs showed some fluctuations, but unlike hard corals they showed no systematic trends. Our extensive empirical data may serve to parameterize ecosystem models, and to refine reef condition indices based on macroalgal data for Pacific coral reefs.

Expanding ocean food production under climate change.

As the human population and demand for food grow1, the ocean will be called on to provide increasing amounts of seafood. Although fisheries reforms and advances in offshore aquaculture (hereafter 'mariculture') could increase production2, the true future of seafood depends on human responses to climate change3. Here we investigated whether coordinated reforms in fisheries and mariculture could increase seafood production per capita under climate change. We find that climate-adaptive fisheries reforms will be necessary but insufficient to maintain global seafood production per capita, even with aggressive reductions in greenhouse-gas emissions. However, the potential for sustainable mariculture to increase seafood per capita is vast and could increase seafood production per capita under all but the most severe emissions scenario. These increases are contingent on fisheries reforms, continued advances in feed technology and the establishment of effective mariculture governance and best practices. Furthermore, dramatically curbing emissions is essential for reducing inequities, increasing reform efficacy and mitigating risks unaccounted for in our analysis. Although climate change will challenge the ocean's ability to meet growing food demands, the ocean could produce more food than it does currently through swift and ambitious action to reduce emissions, reform capture fisheries and expand sustainable mariculture operations.

Effects of low pH on the coral reef cryptic invertebrate communities near CO2 vents in Papua New Guinea.

Small cryptic invertebrates (the cryptofauna) are extremely abundant, ecologically important, and species rich on coral reefs. Ongoing ocean acidification is likely to have both direct effects on the biology of these organisms, as well as indirect effects through cascading impacts on their habitats and trophic relationships. Naturally acidified habitats have been important model systems for studying these complex interactions because entire communities that are adapted to these environmental conditions can be analyzed. However, few studies have examined the cryptofauna because they are difficult to census quantitatively in topographically complex habitats and are challenging to identify. We addressed these challenges by using Autonomous Reef Monitoring Structures (ARMS) for sampling reef-dwelling invertebrates >2 mm in size and by using DNA barcoding for taxonomic identifications. The study took place in Papua New Guinea at two reef localities, each with three sites at varying distances from carbon dioxide seeps, thereby sampling across a natural gradient in acidification. We observed sharp overall declines in both the abundance (34-56%) and diversity (42-45%) of organisms in ARMS under the lowest pH conditions sampled (7.64-7.75). However, the overall abundance of gastropods increased slightly in lower pH conditions, and crustacean and gastropod families exhibited varying patterns. There was also variability in response between the two localities, despite their close proximity, as one control pH site displayed unusually low diversity and abundances for all invertebrate groups. The data illustrate the complexity of responses of the reef fauna to pH conditions, and the role of additional factors that influence the diversity and abundance of cryptic reef invertebrates.

Coral micro- and macro-morphological skeletal properties in response to life-long acclimatization at CO2 vents in Papua New Guinea.

This study investigates the effects of long-term exposure to OA on skeletal parameters of four tropical zooxanthellate corals naturally living at CO2 seeps and adjacent control sites from two locations (Dobu and Upa Upasina) in the Papua New Guinea underwater volcanic vent system. The seeps are characterized by seawater pH values ranging from 8.0 to about 7.7. The skeletal porosity of Galaxea fascicularis, Acropora millepora, massive Porites, and Pocillopora damicornis was higher (up to ~ 40%, depending on the species) at the seep sites compared to the control sites. Pocillopora damicornis also showed a decrease of micro-density (up to ~ 7%). Thus, further investigations conducted on this species showed an increase of the volume fraction of the larger pores (up to ~ 7%), a decrease of the intraskeletal organic matrix content (up to ~ 15%), and an increase of the intraskeletal water content (up to ~ 59%) at the seep sites. The organic matrix related strain and crystallite size did not vary between seep and control sites. This multi-species study showed a common phenotypic response among different zooxanthellate corals subjected to the same environmental pressures, leading to the development of a more porous skeletal phenotype under OA.

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.

A benthic light index of water quality in the Great Barrier Reef, Australia.

Good water quality is essential to the health of marine ecosystems, yet current metrics used to track water quality in the Great Barrier Reef are not strongly tied to ecological outcomes. There is a need for a better water quality index (WQI). Benthic irradiance, the amount of light reaching the seafloor, is critical for coral and seagrass health and is strongly affected by water quality. It therefore represents a strong candidate for use as a water quality indicator. Here, we introduce a new index based on remote sensing benthic light (bPAR) from ocean color. Resulting bPAR index timeseries, based on the extent to which the observed bPAR fell short of the locally- and seasonally-specific optimum, showed strong spatial and temporal variability, which was consistent with the dynamics that govern changes in water clarity in the Great Barrier Reef. Our new index is ecologically relevant, responsive to changes in light availability and provides a robust metric that may complement current Great Barrier Reef water quality metrics.

Knowledge Gaps in the Biology, Ecology, and Management of the Pacific Crown-of-Thorns Sea Star Acanthaster sp. on Australia's Great Barrier Reef.

AbstractCrown-of-thorns sea stars (Acanthaster sp.) are among the most studied coral reef organisms, owing to their propensity to undergo major population irruptions, which contribute to significant coral loss and reef degradation throughout the Indo-Pacific. However, there are still important knowledge gaps pertaining to the biology, ecology, and management of Acanthaster sp. Renewed efforts to advance understanding and management of Pacific crown-of-thorns sea stars (Acanthaster sp.) on Australia's Great Barrier Reef require explicit consideration of relevant and tractable knowledge gaps. Drawing on established horizon scanning methodologies, this study identified contemporary knowledge gaps by asking active and/or established crown-of-thorns sea star researchers to pose critical research questions that they believe should be addressed to improve the understanding and management of crown-of-thorns sea stars on the Great Barrier Reef. A total of 38 participants proposed 246 independent research questions, organized into 7 themes: feeding ecology, demography, distribution and abundance, predation, settlement, management, and environmental change. Questions were further assigned to 48 specific topics nested within the 7 themes. During this process, redundant questions were removed, which reduced the total number of distinct research questions to 172. Research questions posed were mostly related to themes of demography (46 questions) and management (48 questions). The dominant topics, meanwhile, were the incidence of population irruptions (16 questions), feeding ecology of larval sea stars (15 questions), effects of elevated water temperature on crown-of-thorns sea stars (13 questions), and predation on juveniles (12 questions). While the breadth of questions suggests that there is considerable research needed to improve understanding and management of crown-of-thorns sea stars on the Great Barrier Reef, the predominance of certain themes and topics suggests a major focus for new research while also providing a roadmap to guide future research efforts.

Progressive seawater acidification on the Great Barrier Reef continental shelf.

Coral reefs are highly sensitive to ocean acidification due to rising atmospheric CO2 concentrations. We present 10 years of data (2009-2019) on the long-term trends and sources of variation in the carbon chemistry from two fixed stations in the Australian Great Barrier Reef. Data from the subtropical mid-shelf GBRWIS comprised 3-h instrument records, and those from the tropical coastal NRSYON were monthly seawater samples. Both stations recorded significant variation in seawater CO2 fugacity (fCO2), attributable to seasonal, daytime, temperature and salinity fluctuations. Superimposed over this variation, fCO2 progressively increased by > 2.0 ± 0.3 µatm year-1 at both stations. Seawater temperature and salinity also increased throughout the decade, whereas seawater pH and the saturation state of aragonite declined. The decadal upward fCO2 trend remained significant in temperature- and salinity-normalised data. Indeed, annual fCO2 minima are now higher than estimated fCO2 maxima in the early 1960s, with mean fCO2 now ~ 28% higher than 60 years ago. Our data indicate that carbonate dissolution from the seafloor is currently unable to buffer the Great Barrier Reef against ocean acidification. This is of great concern for the thousands of coral reefs and other diverse marine ecosystems located in this vast continental shelf system.

Model for deriving benthic irradiance in the Great Barrier Reef from MODIS satellite imagery: erratum.

Corrections for equations in our recently published paper [Opt. Express27, A1350 (2019)] are presented.

Shifts in coralline algae, macroalgae, and coral juveniles in the Great Barrier Reef associated with present-day ocean acidification.

Seawater acidification from increasing CO2 is often enhanced in coastal waters due to elevated nutrients and sedimentation. Our understanding of the effects of ocean and coastal acidification on present-day ecosystems is limited. Here we use data from three independent large-scale reef monitoring programs to assess coral reef responses associated with changes in mean aragonite saturation state (Ωar ) in the Great Barrier Reef World Heritage Area (GBR). Spatial declines in mean Ωar are associated with monotonic declines in crustose coralline algae (up to 3.1-fold) and coral juvenile densities (1.3-fold), while non-calcifying macroalgae greatly increase (up to 3.2-fold), additionally to their natural changes across and along the GBR. These three key groups of organisms are important proxies for coral reef health. Our data suggest a tipping point at Ωar 3.5-3.6 for these coral reef health indicators. Suspended sediments acted as an additive stressor. The latter suggests that effective water quality management to reduce suspended sediments might locally and temporarily reduce the pressure from ocean acidification on these organisms.

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.

Model for deriving benthic irradiance in the Great Barrier Reef from MODIS satellite imagery.

We demonstrate a simple, spectrally resolved ocean color remote sensing model to estimate benthic photosynthetically active radiation (bPAR) for the waters of the Great Barrier Reef (GBR), Australia. For coastal marine environments and coral reefs, the underwater light field is critical to ecosystem health, but data on bPAR rarely exist at ecologically relevant spatio-temporal scales. The bPAR model presented here is based on Lambert-Beer's Law and uses: (i) sea surface values of the downwelling solar irradiance, Es(λ); (ii) high-resolution seafloor bathymetry data; and (iii) spectral estimates of the diffuse attenuation coefficient, Kd(λ), calculated from GBR-specific spectral inherent optical properties (IOPs). We first derive estimates of instantaneous bPAR. Assuming clear skies, these instantaneous values were then used to obtain daily integrated benthic PAR values. Matchup comparisons between concurrent satellite-derived bPAR and in situ values recorded at four optically varying test sites indicated strong agreement, small bias, and low mean absolute error. Overall, the matchup results suggest that our benthic irradiance model was robust to spatial variation in optical properties, typical of complex shallow coastal waters such as the GBR. We demonstrated the bPAR model for a small test region in the central GBR, with the results revealing strong patterns of temporal variability. The model will provide baseline datasets to assess changes in bPAR and its external drivers and may form the basis for a future GBR water-quality index. This model may also be applicable to other coastal waters for which spectral IOP and high-resolution bathymetry data exist.

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.

Contrasting responses of the coral Acropora tenuis to moderate and strong light limitation in coastal waters.

Coastal water quality and light attenuation can detrimentally affect coral health. This study investigated the effects of light limitation and reduced water quality on the physiological performance of the coral Acropora tenuis. Branches of individual colonies were collected in 2 m water depth at six inshore reefs at increasing distances from major river sources in the Great Barrier Reef, along a strong water quality gradient in the Burdekin and a weak gradient in the Whitsunday region. Rates of net photosynthesis, dark respiration, and light and dark calcification were determined at daily light integrals (DLI) of moderate (13.86-16.38 mol photons m-2 d-1), low (7.92-9.36 mol photons m-2 d-1) and no light (0 mol photons m-2 d-1), in both the dry season (October 2013, June 2014) and the wet season (February 2014). Along the strong but not the weak water quality gradient, rates of net photosynthesis, dark respiration and light calcification increased towards the river mouth both in the dry and the wet seasons. Additionally, a ∼50% light reduction (from moderate to low light), as often found in shallow turbid waters in the Burdekin region, reduced rates of net photosynthesis and light calcification by up to 70% and 50%. The data show the acclimation potential in A. tenuis to river derived nutrients and sediments at moderate DLI (i.e., in very shallow water). However, prolonged and frequent periods of low DLI (i.e., in deeper water, especially after high river sediment discharges) will affect the corals' energy balance, and may represent a major factor limiting the depth distribution of these corals in turbid coastal reefs.

Elevated CO2 Has Little Influence on the Bacterial Communities Associated With the pH-Tolerant Coral, Massive Porites spp.

Ocean acidification (OA) as a result of increased anthropogenic CO2 input into the atmosphere carries consequences for all ocean life. Low pH can cause a shift in coral-associated microbial communities of pCO2-sensitive corals, however, it remains unknown whether the microbial community is also influenced in corals known to be more tolerant to high pCO2/low pH. This study profiles the bacterial communities associated with the tissues of the pCO2-tolerant coral, massive Porites spp., from two natural CO2 seep sites in Papua New Guinea. Amplicon sequencing of the hypervariable V3-V4 regions of the 16S rRNA gene revealed that microbial communities remained stable across CO2 seep sites (pH = 7.44-7.85) and adjacent control sites (ambient pH = 8.0-8.1). Microbial communities were more significantly influenced by reef location than pH, with the relative abundance of dominant microbial taxa differing between reefs. These results directly contrast with previous findings that increased CO2 has a strong effect on structuring microbial communities. The stable structure of microbial communities associated with the tissues of massive Porites spp. under high pCO2/low pH conditions confirms a high degree of tolerance by the whole Porites holobiont to OA, and suggest that pH tolerant corals such as Porites may dominate reef assemblages in an increasingly acidic ocean.

Effects of variability in daily light integrals on the photophysiology of the corals Pachyseris speciosa and Acropora millepora.

Phototrophic sessile organisms, such as reef corals, adjust their photosynthetic apparatus to optimize the balance of light capture versus protection in response to variable light availability (photoacclimation). In shallow marine environments, daily light integrals (DLI) can vary several-fold in response to water clarity and clouds. This laboratory study investigated the responses of two coral species to fluctuations in DLI. Corals were exposed to four contrasting DLI treatments: 'high-light' (potentially photoinhibiting conditions, 32 mol photons m-2 d-1), 'low-light' (potentially light-limiting conditions, 6 mol photons m-2 d-1), and two 'variable light' treatments that alternated between high and low conditions every 5 days. In the variable treatments, the shade-tolerant coral Pachyseris speciosa displayed cycles of rapid declines in maximum quantum yield during high-light and subsequent recoveries during low-light, showing photoacclimation at a time scale of 3-5 days. In contrast, the shallow-water coral Acropora millepora showed slow (>20 days) photoacclimation, and minimal changes in photosynthetic yields despite contrasting light exposure. However, growth (change in buoyant weight) in A. millepora was significantly slower under variable light, and even more so under low-light conditions, compared with high-light conditions. The responses of yields in P. speciosa match their preference for low-light environments, but suggest a vulnerability to even short periods of high-light exposure. In contrast, A. millepora had better tolerance of high-light conditions, however its slow photoacclimatory responses limit its growth under low and variable conditions. The study shows contrasting photoacclimatory responses in variable light environments, which is important to identify and understand as many coastal and midshelf reefs are becoming increasingly more turbid, and may experience higher variability in light availability.

Ocean acidification alters early successional coral reef communities and their rates of community metabolism.

Ocean acidification is expected to alter community composition on coral reefs, but its effects on reef community metabolism are poorly understood. Here we document how early successional benthic coral reef communities change in situ along gradients of carbon dioxide (CO2), and the consequences of these changes on rates of community photosynthesis, respiration, and light and dark calcification. Ninety standardised benthic communities were grown on PVC tiles deployed at two shallow-water volcanic CO2 seeps and two adjacent control sites in Papua New Guinea. Along the CO2 gradient, both the upward facing phototrophic and the downward facing cryptic communities changed in their composition. Under ambient CO2, both communities were dominated by calcifying algae, but with increasing CO2 they were gradually replaced by non-calcifying algae (predominantly green filamentous algae, cyanobacteria and macroalgae, which increased from ~30% to ~80% cover). Responses were weaker in the invertebrate communities, however ascidians and tube-forming polychaetes declined with increasing CO2. Differences in the carbonate chemistry explained a far greater amount of change in communities than differences between the two reefs and successional changes from five to 13 months, suggesting community successions are established early and are under strong chemical control. As pH declined from 8.0 to 7.8, rates of gross photosynthesis and dark respiration of the 13-month old reef communities (upper and cryptic surfaces combined) significantly increased by 10% and 20%, respectively, in response to altered community composition. As a consequence, net production remained constant. Light and dark calcification rates both gradually declined by 20%, and low or negative daily net calcification rates were observed at an aragonite saturation state of <2.3. The study demonstrates that ocean acidification as predicted for the end of this century will strongly alter reef communities, and will significantly change rates of community metabolism.