Timothy F. Cooper

The role of deep reefs in shallow reef recovery: an assessment of vertical connectivity in a brooding coral from west and east Australia.

Approximately one quarter of zooxanthellate coral species have a depth distribution from shallow waters (<30 m) down to mesophotic depths of 30–60 m. The deeper populations of such species are less likely to be affected by certain environmental perturbations, including high temperature/high irradiance causing coral bleaching. This has led to the hypothesis that deep populations may serve as refuges and a source of recruits for shallow reef habitats. The extent of vertical connectivity of reef coral species, however, is largely unquantified. Using 10 coral host microsatellite loci and sequences of the host mtDNA putative control region, as well as ribosomal DNA (rDNA) ITS2 sequences of the coral’s algal endosymbionts (Symbiodinium), we examine population structure, connectivity and symbiont specificity in the brooding coral Seriatopora hystrix across a depth profile in both northwest (Scott Reef) and northeast Australia (Yonge Reef). Strong genetic structuring over depth was observed in both regions based on the microsatellite loci; however, Yonge Reef exhibited an additional partitioning of mtDNA lineages (associated with specific symbiont ITS2 types), whereas Scott Reef was dominated by a single mtDNA lineage (with no apparent host‐symbiont specificity). Evidence for recruitment of larvae of deep water origin into shallow habitats was found at Scott Reef, suggesting that recovery of shallow water habitats may be aided by migration from deep water refuges. Conversely, no migration from the genetically divergent deep slope populations into the shallow habitats was evident at Yonge Reef, making recovery of shallow habitats from deeper waters at this location highly unlikely.

Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes

Effective environmental management requires monitoring programmes that provide specific links between changes in environmental conditions and ecosystem health. This article reviews the suitability of a range of bioindicators for use in monitoring programmes that link changes in water quality to changes in the condition of coral-reef ecosystems. From the literature, 21 candidate bioindicators were identified, whose responses to changes in water quality varied spatially and temporally; responses ranged from rapid (hours) changes within individual corals to long-term (years) changes in community composition. From this list, the most suitable bioindicators were identified by determining whether responses were (i) specific, (ii) monotonic, (iii) variable, (iv) practical and (v) ecologically relevant to management goals. For long-term monitoring programmes that aim to quantify the effects of chronic changes in water quality, 11 bioindicators were selected: symbiont photophysiology, colony brightness, tissue thickness and surface rugosity of massive corals, skeletal elemental and isotopic composition, abundance of macro-bioeroders, micro- and meiobenthic organisms such as foraminifera, coral recruitment, macroalgal cover, taxonomic richness of corals and the maximal depth of coral-reef development. For short-term monitoring programmes, or environmental impact assessments that aim to quantify the effects of acute changes in water quality, a subset of seven of these bioindicators were selected, including partial mortality. Their choice will depend on the specific objectives and the timeframe available for each monitoring programme. An assessment framework is presented to assist in the selection of bioindicators to quantify the effects of changing water quality on coral-reef ecosystems.

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.

Niche specialization of reef-building corals in the mesophotic zone: metabolic trade-offs between divergent Symbiodinium types

The photobiology of two reef corals and the distribution of associated symbiont types were investigated over a depth gradient of 0–60 m at Scott Reef, Western Australia. Pachyseris speciosa hosted mainly the same Symbiodinium C type similar to C3 irrespective of sampling depth. By contrast, Seriatopora hystrix hosted predominantly Symbiodinium type D1a or D1a-like at shallow depths while those in deeper water were dominated by a Symbiodinium C type closely related to C1. The photosynthesis/respiration (P/R) ratio increased consistently with depth at the two sampling times (November 2008 and April 2009) for P. speciosa and in November 2008 only for S. hystrix, suggesting a reduction in metabolic energy expended for every unit of energy obtained from photosynthesis. However, in April 2009, shallow colonies of S. hystrix exhibited decreased P/R ratios down to depths of approximately 23 m, below which the ratio increased towards the maximum depth sampled. This pattern was mirrored by changes in tissue biomass determined as total protein content. The depth of change in the direction of the P/R ratio correlated with a shift from Symbiodinium D to C-dominated colonies. We conclude that while photobiological flexibility is vital for persistence in contrasting light regimes, a shift in Symbiodinium type may also confer a functional advantage albeit at a metabolic cost with increased depth.

Temporal dynamics in coral bioindicators for water quality on coastal coral reefs of the Great Barrier Reef

There is a need to identify effective coral bioindicators that provide quantifiable links between changes in water quality and the condition of coastal coral reefs. Temporal variation in a range of coral bioindicators including symbiont density, concentration of chlorophyll a, skeletal density and colony brightness of Pocillopora damicornis, as well as colony brightness and density of macro-bioeroders of massive Porites spp. was examined for 2 years on a coastal coral reef of the Great Barrier Reef. The specificity to changes in water quality varied among bioindicators. For example, a 2.5-fold variation in symbiont density of P. damicornis was related strongly to mean 14-day sea surface temperature and seasonal changes in water quality, suggesting medium specificity to changes in water quality. In contrast, the density of macro-bioeroders in Porites did not vary seasonally but there were consistently more macro-bioeroders at the coastal than mid-shelf reference locations, suggesting high specificity of spatial differences in water quality. In situ measurements of benthic irradiance and turbidity allowed the quantification of potential stress thresholds for coastal corals. Our data suggest long-term turbidity >3 NTU leads to sublethal stress, whereas long-term turbidity >5 NTU corresponds to severe stress effects on corals at shallow depths.

Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts

Understanding the sedimentation and turbidity thresholds for corals is critical in assessing the potential impacts of dredging projects in tropical marine systems. In this study, we exposed two species of coral sampled from offshore locations to six levels of total suspended solids (TSS) for 16 weeks in the laboratory, including a 4 week recovery period. Dose-response relationships were developed to quantify the lethal and sub-lethal thresholds of sedimentation and turbidity for the corals. The sediment treatments affected the horizontal foliaceous species (Montipora aequituberculata) more than the upright branching species (Acropora millepora). The lowest sediment treatments that caused full colony mortality were 30 mg l−1 TSS (25 mg cm−2 day−1) for M. aequituberculata and 100 mg l−1 TSS (83 mg cm−2 day−1) for A. millepora after 12 weeks. Coral mortality generally took longer than 4 weeks and was closely related to sediment accumulation on the surface of the corals. While measurements of damage to photosystem II in the symbionts and reductions in lipid content and growth indicated sub-lethal responses in surviving corals, the most reliable predictor of coral mortality in this experiment was long-term sediment accumulation on coral tissue.

Environmental factors controlling the distribution of symbiodinium harboured by the coral acropora millepora on the great barrier reef

Background The Symbiodinium community associated with scleractinian corals is widely considered to be shaped by seawater temperature, as the corals upper temperature tolerance is largely contingent on the Symbiodinium types harboured. Few studies have challenged this paradigm as knowledge of other environmental drivers on the distribution of Symbiodinium is limited. Here, we examine the influence of a range of environmental variables on the distribution of Symbiodinium associated with Acropora millepora collected from 47 coral reefs spanning 1,400 km on the Great Barrier Reef (GBR), Australia. Methodology/Principal Findings The environmental data included Moderate Resolution Imaging Spectroradiometer (MODIS) satellite data at 1 km spatial resolution from which a number of sea surface temperature (SST) and water quality metrics were derived. In addition, the carbonate and mud composition of sediments were incorporated into the analysis along with in situ water quality samples for a subset of locations. Analyses were conducted at three spatio-temporal scales [GBR (regional-scale), Whitsunday Islands (local-scale) and Keppel Islands/Trunk Reef (temporal)] to examine the effects of scale on the distribution patterns. While SST metrics were important drivers of the distribution of Symbiodinium types at regional and temporal scales, our results demonstrate that spatial variability in water quality correlates significantly with Symbiodinium distribution at local scales. Background levels of Symbiodinium types were greatest at turbid inshore locations of the Whitsunday Islands where SST predictors were not as important. This was not the case at regional scales where combinations of mud and carbonate sediment content coupled with SST anomalies and mean summer SST explained 51.3% of the variation in dominant Symbiodinium communities. Conclusions/Significance Reef corals may respond to global-scale stressors such as climate change through changes in their resident symbiont communities, however, management of local-scale stressors such as altered water quality is also necessary for maintenance of coral-Symbiodinium associations.

Symbiodinium Genotypic and Environmental Controls on Lipids in Reef Building Corals

Background Lipids in reef building corals can be divided into two classes; non-polar storage lipids, e.g. wax esters and triglycerides, and polar structural lipids, e.g. phospholipids and cholesterol. Differences among algal endosymbiont types are known to have important influences on processes including growth and the photobiology of scleractinian corals yet very little is known about the role of symbiont types on lipid energy reserves. Methodology/Principal Findings The ratio of storage lipid and structural lipid fractions of Scott Reef corals were determined by thin layer chromatography. The lipid fraction ratio varied with depth and depended on symbiont type harboured by two corals (Seriatopora hystrix and Pachyseris speciosa). S. hystrix colonies associated with Symbiodinium C1 or C1/C# at deep depths (>23 m) had lower lipid fraction ratios (i.e. approximately equal parts of storage and structural lipids) than those with Symbiodinium D1 in shallow depths (<23 m), which had higher lipid fraction ratios (i.e. approximately double amounts of storage relative to structural lipid). Further, there was a non-linear relationship between the lipid fraction ratio and depth for S. hystrix with a modal peak at ∼23 m coinciding with the same depth as the shift from clade D to C types. In contrast, the proportional relationship between the lipid fraction ratio and depth for P. speciosa, which exhibited high specificity for Symbiodinium C3 like across the depth gradient, was indicative of greater amounts of storage lipids contained in the deep colonies. Conclusions/Significance This study has demonstrated that Symbiodinium exert significant controls over the quality of coral energy reserves over a large-scale depth gradient. We conclude that the competitive advantages and metabolic costs that arise from flexible associations with divergent symbiont types are offset by energetic trade-offs for the coral host.

Pigmentation of massive corals as a simple bioindicator for marine water quality

Photo-acclimatisation by the algal endosymbionts of scleractinian corals to changes in environmental conditions may influence their density and/or the concentration of photosynthetic pigments, and hence coral brightness, on short time-scales. To examine coral pigmentation as a bioindicator of water quality, the brightness of massive corals was quantified using colour charts, concentrations of the pigment chlorophyll a and reflectance spectrometry in the field and with manipulative experiments. Along a water quality gradient, massive Porites became progressively lighter as nutrients decreased and irradiance increased. A laboratory experiment showed that Porites nubbins darkened within 25 days following exposure to reduced water quality. The results of a transplantation experiment of Porites nubbins in a manipulation incorporating multiple depths and zones of water quality confirmed colony brightness as a simple tool to monitor changes in marine water quality, provided effects due to other influences on pigmentation, e.g. seawater temperatures, are taken into consideration.

Development and Validation of Computational Fluid Dynamics Models for Prediction of Heat Transfer and Thermal Microenvironments of Corals

We present Computational Fluid Dynamics (CFD) models of the coupled dynamics of water flow, heat transfer and irradiance in and around corals to predict temperatures experienced by corals. These models were validated against controlled laboratory experiments, under constant and transient irradiance, for hemispherical and branching corals. Our CFD models agree very well with experimental studies. A linear relationship between irradiance and coral surface warming was evident in both the simulation and experimental result agreeing with heat transfer theory. However, CFD models for the steady state simulation produced a better fit to the linear relationship than the experimental data, likely due to experimental error in the empirical measurements. The consistency of our modelling results with experimental observations demonstrates the applicability of CFD simulations, such as the models developed here, to coral bleaching studies. A study of the influence of coral skeletal porosity and skeletal bulk density on surface warming was also undertaken, demonstrating boundary layer behaviour, and interstitial flow magnitude and temperature profiles in coral cross sections. Our models compliment recent studies showing systematic changes in these parameters in some coral colonies and have utility in the prediction of coral bleaching.