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.

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.

The 27-year decline of coral cover on the Great Barrier Reef and its causes.

The world's coral reefs are being degraded, and the need to reduce local pressures to offset the effects of increasing global pressures is now widely recognized. This study investigates the spatial and temporal dynamics of coral cover, identifies the main drivers of coral mortality, and quantifies the rates of potential recovery of the Great Barrier Reef. Based on the world's most extensive time series data on reef condition (2,258 surveys of 214 reefs over 1985-2012), we show a major decline in coral cover from 28.0% to 13.8% (0.53% y(-1)), a loss of 50.7% of initial coral cover. Tropical cyclones, coral predation by crown-of-thorns starfish (COTS), and coral bleaching accounted for 48%, 42%, and 10% of the respective estimated losses, amounting to 3.38% y(-1) mortality rate. Importantly, the relatively pristine northern region showed no overall decline. The estimated rate of increase in coral cover in the absence of cyclones, COTS, and bleaching was 2.85% y(-1), demonstrating substantial capacity for recovery of reefs. In the absence of COTS, coral cover would increase at 0.89% y(-1), despite ongoing losses due to cyclones and bleaching. Thus, reducing COTS populations, by improving water quality and developing alternative control measures, could prevent further coral decline and improve the outlook for the Great Barrier Reef. Such strategies can, however, only be successful if climatic conditions are stabilized, as losses due to bleaching and cyclones will otherwise increase.

The multinomial diversity model: linking Shannon diversity to multiple predictors.

The multinomial diversity model, MDM, is a new method for relating Shannon diversity to complex environmental, spatial, and temporal predictors. It is based on a parameterized formulation of Shannon entropy and diversity, and a novel link between entropy and the log-likelihood of the multinomial model. The MDM relates diversity to the predictors by minimizing the entropy of the estimated species values. Model effects can be expressed as changes in entropy. Entropy can be partitioned within and between sites, species, and models, and changes in entropy can be attributed to model predictors. All entropies translate into diversity for meaningful ecological interpretation. This greatly enhances our capacity to model complex data sets, and yet also provide simple interpretations. By formulating diversity as a statistical model and working in terms of entropy, diversity is simplified both conceptually and analytically, and diversity analyses are extended beyond traditional simple hierarchies of alpha, beta, gamma, and measures of turnover. The MDM inherits the properties of generalized linear models, and thus proven methods can be used for model selection and graphical and numerical interpretation. A weighted version of the Shannon diversity model is proposed in order to extend the MDM to non-Shannon diversities. Two example analyses, based on simulated and field data, illustrate the theoretical concepts and the analytical methods.

Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef.

Degradation of inshore coral reefs due to poor water quality is a major issue, yet it has proved difficult to demonstrate this linkage at other than local scales. This study modeled the relationships between large-scale data on water clarity and chlorophyll and four measures of reef status along the whole Great Barrier Reef, Australia (GBR; 12-24 degrees S). Four biotic groups with different trophic requirements, namely, the cover of macroalgae and the taxonomic richness of hard corals and phototrophic and heterotrophic octocorals, were predicted from water quality and spatial location. Water clarity and chlorophyll showed strong spatial patterns, with water clarity increasing more than threefold from inshore to offshore waters and chlorophyll decreasing approximately twofold from inshore to offshore and approximately twofold from south to north. Richness of hard corals and phototrophic octocorals declined with increasing turbidity and chlorophyll, whereas macroalgae and the richness of heterotrophic octocorals increased. Macroalgal cover experienced the largest water quality effects, increasing fivefold with decreasing water clarity and 1.4-fold with increasing chlorophyll. For each of the four biota, -45% of variation was predictable, with water quality effects accounting for 18-46% of that variation and spatial effects accounting for the remainder. Effects were consistent with the trophic requirements of the biota, suggesting that both macroalgal cover and coral biodiversity are partially controlled by energy supply limitation. Throughout the GBR, mean annual values of >10 m Secchi disk depth (a measure of water clarity) and < 0.45 g/L chlorophyll were associated with low macroalgal cover and high coral richness, indicating these values to be potentially useful water quality guidelines. The models predict that on the 22.8% of GBR reefs where guideline values are currently exceeded, water quality improvement, e.g., by minimizing agricultural runoff, should reduce macroalgal cover on average by 39% and increase the richness of hard corals and phototrophic octocorals on average by 16% and 33%, respectively (all else being equal). Such guidelines may help focus efforts to implement effective pollution reduction and integrated coastal management policies for the GBR and other Indo-Pacific coral reefs.

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.

Boosted trees for ecological modeling and prediction.

Accurate prediction and explanation are fundamental objectives of statistical analysis, yet they seldom coincide. Boosted trees are a statistical learning method that attains both of these objectives for regression and classification analyses. They can deal with many types of response variables (numeric, categorical, and censored), loss functions (Gaussian, binomial, Poisson, and robust), and predictors (numeric, categorical). Interactions between predictors can also be quantified and visualized. The theory underpinning boosted trees is presented, together with interpretive techniques. A new form of boosted trees, namely, "aggregated boosted trees" (ABT), is proposed and, in a simulation study, is shown to reduce prediction error relative to boosted trees. A regression data set is analyzed using ABT to illustrate the technique and to compare it with other methods, including boosted trees, bagged trees, random forests, and generalized additive models. A software package for ABT analysis using the R software environment is included in the Appendices together with worked examples.

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.

Are increased nutrient inputs responsible for more outbreaks of crown-of-thorns starfish? An appraisal of the evidence.

The cause(s) of primary outbreaks of the coral-eating crown-of-thorns starfish (Acanthaster planci) are still subject to scientific controversy. The possibility of primary outbreaks being linked to terrestrial runoff has been postulated a number of times, suggesting that enhanced nutrient supply is critical for enhanced A. planci larval development. This paper examines the evidence for such a cause, focussing particularly on the Great Barrier Reef (GBR). Nutrient discharges from rivers have increased at least four-fold in the central GBR over the last century, and concentrations of large phyto-plankton (>2 microm) of the inshore central GBR shelf in the wet season when A. planci larvae develop, is double that of other places and times. Larval development, growth and survival increase almost ten-fold with doubled concentrations of large phyto-plankton. This and other lines of evidence suggest that frequent A. planci outbreaks on the GBR may indeed be a result of increased nutrient delivery from the land.

Changes in algal, coral and fish assemblages along water quality gradients on the inshore Great Barrier Reef.

Macroalgae, hard corals, octocorals, and fish were surveyed on 10 to 13 inshore coral reefs of the Great Barrier Reef, along a water quality gradient in two regions with contrasting agricultural land use. A water quality index was calculated for each reef based on available data of particulate and dissolved nutrients, chlorophyll and suspended solids. Strong gradients in ecological attributes occurred along the water quality gradient. Macroalgae of the divisions Rhodophyta and Chlorophyta increased with increasing nutrients, while Phaeophyta remained similar. Octocoral richness and abundances of many hard coral and octocoral taxa decreased, and none of the hundreds of species increased. At reefs in higher nutrient environments, hard coral and octocoral assemblages were composed of subsets of the many species found in lower nutrient environments, whereas fish and macroalgal assemblages consisted of contrasting suites of species. The study identifies species groups that are likely to increase or decrease in abundance with changing water quality.

Does trophic status enhance or reduce the thermal tolerance of scleractinian corals? A review, experiment and conceptual framework.

Global warming, and nutrient and sediment runoff from coastal development, both exert increasing pressures on coastal coral reefs. The objective of this study was to resolve the question of whether coastal eutrophication may protect corals from thermal stress by improving their nutritional status, or rather diminish their thermal tolerance through the synergy of dual stressors. A review of previous studies on the topic of combined trophic status and heat exposure on the thermal tolerance of corals reveals a broad range of outcomes, including synergistic, additive and antagonistic effects. We conducted a 90-day long experiment exposing corals to realistic levels of elevated nutrients and sediments, and heat stress. Colonies of two common scleractinian corals (Acropora millepora and Montipora tuberculosa) were kept in coastal seawater, or coastal seawater that was further organically and nutrient enriched (OE), and/or enriched with nitrate. Batches of OE were created daily, facilitating nutrient uptake, plankton succession and organic enrichment as observed in coastal waters. After 10 days of acclimation, 67% of the colonies had their temperature gradually increased from 27° to 31.2°C. After 3-7 weeks of heat stress, colonies of both species had significantly greater reductions in fluorescence yields and lower survival in OE than without addition of OE. Furthermore, photophysiological recovery was incomplete 31-38 days after ending the heat stress only in the OE treatments. Nitrate alone had no measurable effect on survival, bleaching and recovery in either species. Skeletal growth rates were reduced by 45% in heat-stressed A. millepora and by 24% in OE-exposed M. tuberculosa. We propose a conceptual trophic framework that resolves some of the apparently contradictory outcomes revealed by the review. Our study shows that management actions to reduce coastal eutrophication can improve the resistance and resilience of vulnerable coastal coral reefs to warming temperatures.

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.

Declining coral calcification on the Great Barrier Reef.

Reef-building corals are under increasing physiological stress from a changing climate and ocean absorption of increasing atmospheric carbon dioxide. We investigated 328 colonies of massive Porites corals from 69 reefs of the Great Barrier Reef (GBR) in Australia. Their skeletal records show that throughout the GBR, calcification has declined by 14.2% since 1990, predominantly because extension (linear growth) has declined by 13.3%. The data suggest that such a severe and sudden decline in calcification is unprecedented in at least the past 400 years. Calcification increases linearly with increasing large-scale sea surface temperature but responds nonlinearly to annual temperature anomalies. The causes of the decline remain unknown; however, this study suggests that increasing temperature stress and a declining saturation state of seawater aragonite may be diminishing the ability of GBR corals to deposit calcium carbonate.

Genetic traces of recent long-distance dispersal in a predominantly self-recruiting coral.

BACKGROUND: Understanding of the magnitude and direction of the exchange of individuals among geographically separated subpopulations that comprise a metapopulation (connectivity) can lead to an improved ability to forecast how fast coral reef organisms are likely to recover from disturbance events that cause extensive mortality. Reef corals that brood their larvae internally and release mature larvae are believed to show little exchange of larvae over ecological times scales and are therefore expected to recover extremely slowly from large-scale perturbations. METHODOLOGY/PRINCIPAL FINDINGS: Using analysis of ten DNA microsatellite loci, we show that although Great Barrier Reef (GBR) populations of the brooding coral, Seriatopora hystrix, are mostly self-seeded and some populations are highly isolated, a considerable amount of sexual larvae (up to approximately 4%) has been exchanged among several reefs 10 s to 100 s km apart over the past few generations. Our results further indicate that S. hystrix is capable of producing asexual propagules with similar long-distance dispersal abilities (approximately 1.4% of the sampled colonies had a multilocus genotype that also occurred at another sampling location), which may aid in recovery from environmental disturbances. CONCLUSIONS/SIGNIFICANCE: Patterns of connectivity in this and probably other GBR corals are complex and need to be resolved in greater detail through genetic characterisation of different cohorts and linkage of genetic data with fine-scale hydrodynamic models.