Effects of water quality on the health and condition of inshore corals

Coral species are threatened by environmental change, both from global pressures, particularly ocean warming and acidification, and local pressures, such as poor water quality and pollution. Species with broad distributions experience a range of different environments. For example, distribution ranges that span the continental shelf expose coral populations to oligotrophic offshore conditions and turbid, nutrient-rich inshore reef waters. Such study systems provide a unique opportunity to understand how species modify their biochemical and molecular phenotype in response to varying environmental conditions. Organisms can optimise their performance and fitness (i.e. growth, survival and reproduction) under local environmental regimes through physiological acclimatisation within their lifetimes and/or through genetic adaptation at the population or species level across generations. Studies of species with broad habitat distributions can provide insights into the fundamental mechanisms that underpin acclimatisation and adaptation, which collectively enable corals to respond to changing environments in the future. Biochemical attributes of corals, and estimates of their growth and survival, can be used to describe the health of the coral holobiont under different environmental conditions. In Chapter 2, I compared survival, growth, and five biochemical health attributes of Acropora tenuis among habitats characterised by different water quality regimes in the central Great Barrier Reef, Australia. Health attributes of the coral host and its' Symbiodinium were monitored over three seasons along a strong and a weak inshore water quality gradient, each with three locations at increasing distances from the coast and major rivers. Along the strong water quality gradient, corals had the highest symbiont densities and tissue energetic concentrations closest to the coast and river source, where particulate concentrations were the highest. In contrast, corals found at the site with clearer water had slower growth and increased skeletal density. Differences in coral and Symbiodinium attributes were less pronounced along the weaker gradient. According to most of the physiological and biochemical attributes measured, high concentrations of dissolved and particulate nutrients were not detrimental to this robust coral species over the timeframe of the study. Decreased skeletal densities associated with higher growth rates at more turbid sites are likely to cause higher susceptibility to physical damage from storms, which occur seasonally and are predicted to increase in frequency in the future. These results highlight the importance of assessing multiple coral attributes when monitoring coral health. Fatty acids (FA), the building blocks of lipids, have been proposed as biomarkers of coral health and stress, as they play a vital role in the metabolism and stress resistance of a broad range of organisms. In corals, FA can also potentially reveal sources of nutrition and host-symbiont resource sharing, which can elucidate basal mechanisms of biochemical and physiological functioning of corals. In Chapter 3, I explore seasonal and spatial variation in tissue concentrations and composition of FA in Acropora tenuis along the two aforementioned water quality gradients. FA health indicator ratios varied similarly within both regions along the respective water quality gradients. Corals exposed to clear, nutrient-poor conditions at sites along the afore studied water quality gradients (defined as good or very good water quality by the Reef Rescue Marine Monitoring Program at the Australian Institute of Marine Science) had the highest ratios, while corals from sites of moderate WQ had the lowest ratios, suggesting heterotrophic food sources within turbid, nutrient-enriched conditions along these same water quality gradients can supplement reduced autotrophy. Percentages of essential FA (EPA and ARA) were highest in corals from clearer water and were negatively correlated with Symbiodinium density. Strong seasonal divergence occurred in polyunsaturated fatty acid (PUFA) concentrations, with greater percentage of n-3 PUFA found in the dry seasons (June 2013 and October 2013) compared to greater percentage of n-6 PUFA found during the wet seasons (February 2013 and February 2014). This study demonstrated essential FA and their derived health ratios respond to changes in seasonal and environmental conditions supporting FA as biomarkers of coral holobiont health. Predation is a major source of coral mortality, and corallivorous fishes can significantly influence growth and survival of coral populations. In Chapter 4, I document how corals transplanted from a highly turbid and nutrient-enriched environment of moderate water quality to a low turbidity, non-nutrient-enriched environment of good water quality suffered high mortality and skeletal loss from predation. Specifically, colonies of Acropora tenuis transplanted from the site closest to the coast and river source to the site with clearer water along the stronger water quality gradient sustained significantly greater loss of coral skeleton, when compared to control colonies and their reciprocally transplanted counterparts. These results suggest marked intraspecific differences in the physiological condition and palatability of coral colonies underlying selective predation on corals originating from a high turbidity, nutrient-enriched environment. Further studies are needed to understand the underlying biochemical or physiological attributes that incite selective predation within coral populations and their ecological consequences. To investigate drivers of plasticity in the biochemical and physiological attributes of A. tenuis, a suite of FA and biochemical attributes were monitored over the course of the reciprocal transplant experiment described in Chapter 4. In Chapter 5, I evaluated the degree to which coral populations from different environmental regimes acclimated to a novel environment four months after transplantation. To partition the effects of source population genetics, long-term acclimatisation and the environment, I quantified variation in global gene expression (GE) and FA composition of surviving experimental fragments. There was a strong influence of source population on GE profiles enriched with higher relative expression of genes associated with translation, ribosome biogenesis and ribosome cellular components in corals sourced from moderate water quality compared to lower relative expression in corals sourced from an environment defined by good water quality. Environment was a major driver of change in FA composition; all major FA classes, with the exception of short-chain PUFA, decreased in concentration when corals were exposed to moderate water quality and increased in concentration when corals were exposed to a good water quality environment, regardless of source population. There was also evidence of plasticity in the responses of coral genes relating to elevated health and immunity due to environmental change. This chapter demonstrates the plasticity of corals in response to environmental change, but also a limit to that plasticity dictated by their source population either as a consequence of underlying genetic differences or long-term acclimatisation. Therefore, there may be potential hope for future corals, if we can reduce anthropogenic water quality stressors on coral health and condition. In summary, comparisons of a range of molecular and biochemical health attributes among experimental colonies of Acropora tenuis originating from a range of water quality regimes reveal new insights into environmental drivers and the underlying genetic basis of coral health. This research demonstrates that common coral species on inshore reefs, such as A. tenuis, can grow rapidly under water quality conditions characterised by high concentrations of particulate and dissolved nutrients. However, negative correlations among attributes commonly associated with good health (e.g. growth rate and skeletal density) highlight the need to carefully define health attributes. Inshore populations of the coral A. tenuis can acclimatise and/or adapt to local conditions through variation in growth rate, symbiont type and density, skeletal density and organic tissue components, including FA composition. Yet, coral populations still maintain a genetic signature of their origins, which enables differentiation and identification of inshore populations. By integrating physiological attributes, biochemical composition and genomics, this research improves our understanding of the capacity of corals to acclimatise and/or adapt to a range of environmental conditions, most notably terrestrial runoff and climate change into the future