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.

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.

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.

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.

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.

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.

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.

Quantifying pCO2 in biological ocean acidification experiments: A comparison of four methods.

Quantifying the amount of carbon dioxide (CO2) in seawater is an essential component of ocean acidification research; however, equipment for measuring CO2 directly can be costly and involve complex, bulky apparatus. Consequently, other parameters of the carbonate system, such as pH and total alkalinity (AT), are often measured and used to calculate the partial pressure of CO2 (pCO2) in seawater, especially in biological CO2-manipulation studies, including large ecological experiments and those conducted at field sites. Here we compare four methods of pCO2 determination that have been used in biological ocean acidification experiments: 1) Versatile INstrument for the Determination of Total inorganic carbon and titration Alkalinity (VINDTA) measurement of dissolved inorganic carbon (CT) and AT, 2) spectrophotometric measurement of pHT and AT, 3) electrode measurement of pHNBS and AT, and 4) the direct measurement of CO2 using a portable CO2 equilibrator with a non-dispersive infrared (NDIR) gas analyser. In this study, we found these four methods can produce very similar pCO2 estimates, and the three methods often suited to field-based application (spectrophotometric pHT, electrode pHNBS and CO2 equilibrator) produced estimated measurement uncertainties of 3.5-4.6% for pCO2. Importantly, we are not advocating the replacement of established methods to measure seawater carbonate chemistry, particularly for high-accuracy quantification of carbonate parameters in seawater such as open ocean chemistry, for real-time measures of ocean change, nor for the measurement of small changes in seawater pCO2. However, for biological CO2-manipulation experiments measuring differences of over 100 µatm pCO2 among treatments, we find the four methods described here can produce similar results with careful use.

Low recruitment due to altered settlement substrata as primary constraint for coral communities under ocean acidification.

The future of coral reefs under increasing CO2 depends on their capacity to recover from disturbances. To predict the recovery potential of coral communities that are fully acclimatized to elevated CO2, we compared the relative success of coral recruitment and later life stages at two volcanic CO2 seeps and adjacent control sites in Papua New Guinea. Our field experiments showed that the effects of ocean acidification (OA) on coral recruitment rates were up to an order of magnitude greater than the effects on the survival and growth of established corals. Settlement rates, recruit and juvenile densities were best predicted by the presence of crustose coralline algae, as opposed to the direct effects of seawater CO2 Offspring from high CO2 acclimatized parents had similarly impaired settlement rates as offspring from control parents. For most coral taxa, field data showed no evidence of cumulative and compounding detrimental effects of high CO2 on successive life stages, and three taxa showed improved adult performance at high CO2 that compensated for their low recruitment rates. Our data suggest that severely declining capacity for reefs to recover, due to altered settlement substrata and reduced coral recruitment, is likely to become a dominant mechanism of how OA will alter coral reefs.

Effects of suspended sediments and nutrient enrichment on juvenile corals.

Three to six-month-old juveniles of Acropora tenuis, A. millepora and Pocillopora acuta were experimentally co-exposed to nutrient enrichment and suspended sediments (without light attenuation or sediment deposition) for 40days. Suspended sediments reduced survivorship of A. millepora strongly, proportional to the sediment concentration, but not in A. tenuis or P. acuta juveniles. However, juvenile growth of the latter two species was reduced to less than half or to zero, respectively. Additionally, suspended sediments increased effective quantum yields of symbionts associated with A. millepora and A. tenuis, but not those associated with P. acuta. Nutrient enrichment did not significantly affect juvenile survivorship, growth or photophysiology for any of the three species, either as a sole stressor or in combination with suspended sediments. Our results indicate that exposure to suspended sediments can be energetically costly for juveniles of some coral species, implying detrimental longer-term but species-specific repercussions for populations and coral cover.

A diver-operated hyperspectral imaging and topographic surveying system for automated mapping of benthic habitats.

We developed a novel integrated technology for diver-operated surveying of shallow marine ecosystems. The HyperDiver system captures rich multifaceted data in each transect: hyperspectral and color imagery, topographic profiles, incident irradiance and water chemistry at a rate of 15-30 m2 per minute. From surveys in a coral reef following standard diver protocols, we show how the rich optical detail can be leveraged to generate photopigment abundance and benthic composition maps. We applied machine learning techniques, with a minor annotation effort (<2% of pixels), to automatically generate cm-scale benthic habitat maps of high taxonomic resolution and accuracy (93-97%). The ability to efficiently map benthic composition, photopigment densities and rugosity at reef scales is a compelling contribution to modernize reef monitoring. Seafloor-level hyperspectral images can be used for automated mapping, avoiding operator bias in the analysis and deliver the degree of detail necessary for standardized environmental monitoring. The technique can deliver fast, objective and economic reef survey results, making it a valuable tool for coastal managers and reef ecologists. Underwater hyperspectral surveying shares the vantage point of the high spatial and taxonomic resolution restricted to field surveys, with analytical techniques of remote sensing and provides targeted validation for aerial monitoring.

Pontellid copepods, Labidocera spp., affected by ocean acidification: A field study at natural CO2 seeps.

CO2 seeps in coral reefs were used as natural laboratories to study the impacts of ocean acidification on the pontellid copepod, Labidocera spp. Pontellid abundances were reduced by ∼70% under high-CO2 conditions. Biological parameters and substratum preferences of the copepods were explored to determine the underlying causes of such reduced abundances. Stage- and sex-specific copepod lengths, feeding ability, and egg development were unaffected by ocean acidification, thus changes in these physiological parameters were not the driving factor for reduced abundances under high-CO2 exposure. Labidocera spp. are demersal copepods, hence they live amongst reef substrata during the day and emerge into the water column at night. Deployments of emergence traps showed that their preferred reef substrata at control sites were coral rubble, macro algae, and turf algae. However, under high-CO2 conditions they no longer had an association with any specific substrata. Results from this study indicate that even though the biology of a copepod might be unaffected by high-CO2, Labidocera spp. are highly vulnerable to ocean acidification.

Variation in the health and biochemical condition of the coral Acropora tenuis along two water quality gradients on the Great Barrier Reef, Australia.

This study explores how plasticity in biochemical attributes, used as indicators of health and condition, enables the coral Acropora tenuis to respond to differing water quality regimes in inshore regions of the Great Barrier Reef. Health attributes were monitored along a strong and weak water quality gradient, each with three reefs at increasing distances from a major river source. Attributes differed significantly only along the strong gradient; corals grew fastest, had the least dense skeletons, highest symbiont densities and highest lipid concentrations closest to the river mouth, where water quality was poorest. High nutrient and particulate loads were only detrimental to skeletal density, which decreased as linear extension increased, highlighting a trade-off. Our study underscores the importance of assessing multiple health attributes in coral reef monitoring. For example, autotrophic indices are poor indicators of coral health and condition, but improve when combined with attributes like lipid content and biomass.

Cumulative effects of suspended sediments, organic nutrients and temperature stress on early life history stages of the coral Acropora tenuis.

Coral reproduction is vulnerable to both declining water quality and warming temperatures, with simultaneous exposures likely compounding the negative impact of each stressor. We investigated how early life processes of the coral Acropora tenuis respond to increasing levels of suspended sediments in combination with temperature or organic nutrients. Fertilization success and embryo development were more sensitive to suspended sediments than to high temperatures or nutrient enrichment, while larval development (after acquisition of cilia) and settlement success were predominantly affected by thermal stress. Fertilization success was reduced 80% by suspended sediments, and up to 24% by temperature, while the addition of nutrients to suspended sediments had no further impact. Larval survivorship was unaffected by any of these treatments. However, settlement success of larvae developing from treatment-exposed embryos was negatively affected by all three stressors (e.g. up to 55% by suspended sediments), while exposure only during later larval stages predominantly responded to temperature stress. Environmentally relevant levels of suspended sediments and temperature had the greatest impacts, affecting more processes than the combined impacts of sediments and nutrients. These results suggest that management strategies to maintain suspended sediments at low concentrations during coral spawning events will benefit coral recruitment, especially with warming climate.

Enhanced macroboring and depressed calcification drive net dissolution at high-CO2 coral reefs.

Ocean acidification (OA) impacts the physiology of diverse marine taxa; among them corals that create complex reef framework structures. Biological processes operating on coral reef frameworks remain largely unknown from naturally high-carbon-dioxide (CO2) ecosystems. For the first time, we independently quantified the response of multiple functional groups instrumental in the construction and erosion of these frameworks (accretion, macroboring, microboring, and grazing) along natural OA gradients. We deployed blocks of dead coral skeleton for roughly 2 years at two reefs in Papua New Guinea, each experiencing volcanically enriched CO2, and employed high-resolution micro-computed tomography (micro-CT) to create three-dimensional models of changing skeletal structure. OA conditions were correlated with decreased calcification and increased macroboring, primarily by annelids, representing a group of bioeroders not previously known to respond to OA. Incubation of these blocks, using the alkalinity anomaly methodology, revealed a switch from net calcification to net dissolution at a pH of roughly 7.8, within Intergovernmental Panel on Climate Change's (IPCC) predictions for global ocean waters by the end of the century. Together these data represent the first comprehensive experimental study of bioerosion and calcification from a naturally high-CO2 reef ecosystem, where the processes of accelerated erosion and depressed calcification have combined to alter the permanence of this essential framework habitat.

Cumulative Effects of Nutrient Enrichment and Elevated Temperature Compromise the Early Life History Stages of the Coral Acropora tenuis.

Inshore coral reefs are experiencing the combined pressures of excess nutrient availability associated with coastal activities and warming seawater temperatures. Both pressures are known to have detrimental effects on the early life history stages of hard corals, but studies of their combined effects on early demographic stages are lacking. We conducted a series of experiments to test the combined effects of nutrient enrichment (three levels) and elevated seawater temperature (up to five levels) on early life history stages of the inshore coral Acropora tenuis, a common species in the Indo-Pacific and Red Sea. Gamete fertilization, larval survivorship and larval settlement were all significantly reduced as temperature increased, but only fertilization was further affected by simultaneous nutrient enrichment. Combined high temperatures and nutrient enrichment affected fertilization in an additive manner, whereas embryo abnormalities increased synergistically. Higher than normal temperatures (32°C) increased coral juvenile growth rates 1.6-fold, but mortality also increased by 50%. The co-occurrence of nutrient enrichment with high temperatures reduced juvenile mortality to 36%, ameliorating temperature stress (antagonistic interaction). Overall, the types of effect (additive vs synergistic or antagonistic) and their magnitude varied among life stages. Gamete and embryo stages were more affected by temperature stress and, in some cases, also by nutrient enrichment than juveniles. The data suggest that coastal runoff events might exacerbate the impacts of warming temperatures on fertilization if these events co-occur during corals spawning. The cumulative impacts of simultaneous exposure to nutrient enrichment and elevated temperatures over all early life history stages increases the likelihood for failure of larval supply and recruitment for this coral species. Our results suggest that improving the water quality of river discharges into coastal areas might help to enhance the thermal tolerances of early life history stages in this common coral species.