Towards achieving circularity and sustainability in feeds for farmed blue foods

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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

Transplantation of corals into a new environment results in substantial skeletal loss in Acropora tenuis

The degradation of coral reefs, specifically the loss of structural biomass created by coral skeletons, is an important issue in coral reef science. In this study, we give evidence for high skeletal loss in corals transplanted from a high turbidity environment to a low turbidity environment. Specifically, we show that in colonies of Acropora tenuis, significantly higher skeletal loss occurred in colonies from Geoffrey Bay (Magnetic Island, Australia, ∼8 km offshore) transplanted to Pelorus Island (Palm Islands, Australia, ∼16 km offshore), when compared to control colonies and their reciprocally transplanted counterparts. These results may suggest marked intraspecific differences in the physiological condition of coral colonies, possibly causing selective predation by corallivorous organisms, strengthening the need for detailed investigations of the underlying causes as well as the consequences of skeletal loss in an important branching species of coral, Acropora tenuis

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

Thermal stress-related gene expression in corals with different Symbiodinium types

The endosymbiotic relationship between scleractinian corals and Symbiodinium spp underpins the biodiversity and productivity of coral reefs worldwide. The genetic and physiological characteristics of Symbiodinium have large effects on coral host physiology and thermal tolerance; however, the degree to which molecular responses to thermal and oxidative stress vary among corals with different symbiont types is still not well understood. We examine gene expression in response to laboratory-based thermal stress in 1 year-old juveniles of Acropora millepora hosting different dominant Symbiodinium types. We detected significant changes in symbiont dominance through time, with 59.7% of coral juveniles changing their symbiont type during a 12-month growth period in the wild and 22% hosting two types simultaneously. Only three of 50 genes with a putative role in heat and oxidative stress were differentially expressed. Heat Shock Proteins 70 and 90 were expressed at higher levels in juveniles hosting multiple symbiont types during early stages of heat stress, whereas a NOS-interacting gene (a gene regulating nitric oxide production) was up-regulated concurrently with a decline in maximum quantum yield during heat stress. Our results support an important role for symbiont complements in the transcriptomes of corals and highlight high variability among individuals

Reef location has a greater impact than coral bleaching severity on the microbiome of Pocillopora acuta

Coral reefs are increasingly threatened by heat stress events leading to coral bleaching. In 2016, a mass bleaching event affected large parts of the Great Barrier Reef (GBR). Whilst bleaching severity and coral mortality are usually monitored throughout major bleaching events, other health indicators, such as changes in microbial partners, are rarely assessed. We examined the impact of the 2016 bleaching event on the composition of the microbial communities in the coral Pocillopora acuta at Havannah Island Pandora reef, separated by 12 km on the inshore central GBR. Corals experienced moderate heat stress (3.6 and 5.3 degree heating weeks), inducing major bleaching (30–60%) at the coral community level. Samples were partitioned according to Symbiodiniaceae densities into three bleaching severity categories (mild, moderate, and severe). Whilst Symbiodiniaceae densities were similar at both reef locations, sequencing of the Symbiodiniaceae ITS2 and prokaryotic 16S rRNA genes revealed that microbial communities were significantly different between reefs, but not according to bleaching severity. Symbiodiniaceae composition was dominated by the genus Cladocopium with low abundances of Durusdinium detected in moderately and severely bleached colonies at both sites, despite site-specific ITS2 profiles. Bacterial communities were dominated by Proteobacteria and were almost entirely lacking the common Pocilloporid associate Endozoicomonas regardless of bleaching severity. Strikingly, only 11.2% of the bacterial Amplicon Sequencing Variants (ASVs) were shared between sites. This reef specificity was driven by 165 ASVs, mainly from the family Rhodobacteraceae. Comparison with previous studies suggests that the moderate heat stress experienced on the central GBR in 2016 caused the near-complete absence of Endozoicomonas. Symbiodiniaceae and bacteria (particularly Rhodobacteraceae) can be vertically transmitted in P. acuta, and larval propagation can be spatially restricted for this brooding species. Our results demonstrate that, unlike bleaching severity, location-specific factors and species-specific life history traits might have been paramount in shaping the P. acuta microbiome

Expression of calcification and metabolism-related genes in response to elevated pCO(2) and temperature in the reef-building coral Acropora millepora

Declining health of scleractinian corals in response to deteriorating environmental conditions is widely acknowledged, however links between physiological and functional genomic responses of corals are less well understood. Here we explore growth and the expression of 20 target genes with putative roles in metabolism and calcification in the branching coral, Acropora millepora, in two separate experiments: 1) elevated pCO(2) (464, 822, 1187 and 1638 mu atm) and ambient temperature (27 degrees C), and 2) elevated pCO(2) (490 and 822 mu atm) and temperature (28 and 31 degrees C). After 14 days of exposure to elevated pCO(2) and ambient temperatures, no evidence of differential expression of either calcification or metabolism genes was detected between control and elevated pCO(2) treatments. After 37 days of exposure to control and elevated pCO(2), Ubiquinol-Cytochrome-C Reductase Subunit 2 gene (QCR2; a gene involved in complex III of the electron chain transport within the mitochondria and critical for generation of ATP) was significantly down-regulated in the elevated pCO(2) treatment in both ambient and elevated temperature treatments. Overall, the general absence of a strong response to elevated pCO(2) and temperature by the other 19 targeted calcification and metabolism genes suggests that corals may not be affected by these stressors on longer time scales (37 days). These results also highlight the potential for QCR2 to act as a biomarker of coral genomic responses to changing environments

Temporal and spatial variation in fatty acid composition in Acropora tenuis corals along water quality gradients on the Great Barrier Reef, Australia

Fatty acids (FA) play a vital role in coral physiology, metabolism and stress resistance. Optimal health requires a balance of fatty acids, and more specifically essential polyunsaturated fatty acids (PUFA), for efficient biochemical and physiological functioning. Therefore, it is necessary to fully assess and evaluate the viability of FA as biomarkers for monitoring the health of coral populations. This study explores seasonal and spatial variation in the abundance of 17 FA in the coral Acropora tenuis, along two water quality gradients on the central Great Barrier Reef. Ratios of key FA varied similarly along the two water quality gradients and were highest in corals from comparatively good water quality conditions. Strong differences in PUFA composition were found between wet and dry seasons, with high percentage n-3 PUFA defining the dry seasons (June 2013 and October 2013) and high percentage n-6 PUFA defining the wet seasons (February 2013 and 2014). Saturated FA and monounsaturated FA concentrations varied with season, positively correlated with Symbiodinium density, and had highest concentrations in corals exposed to relatively poor water quality. Overall, results demonstrate that essential FA and their derived ratios support FA as a potential indicator of coral holobiont health; however, strong seasonal variation may negate FA and their derived ratios as water quality indicators

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

Plasticity in gene expression and fatty acid profiles of Acropora tenuis reciprocally transplanted between two water quality regimes in the central Great Barrier Reef, Australia

To investigate plasticity in biochemical and physiological health attributes of corals, identical colony fragments of the coral Acropora tenuis, from two inshore populations, were exposed to native and novel environmental regimes. Variation in global gene expression (GE) and lipid and fatty acid (FA) composition of surviving colony fragments were quantified after four months. Major FA classes, with the exception of short-chain (C18) polyunsaturated fatty acids (PUFA), decreased in concentration when coral fragments were exposed to lower water quality regardless of their source population. In contrast, a strong effect of source population was detected in the GE profiles of all coral fragments and was enriched with genes associated with translation, ribosome biogenesis and ribosome cellular components. One cluster of co-expressed genes positively correlated with multiple individual FA and included genes involved in developmental processes and cellular pathways. This study demonstrates the strong influence of a source effect defining gene expression relating to basic biological functions, including biosynthetic processing, translation and ribosome biogenesis. However, there is plasticity in FA composition and specific genes relating to elevated health and immunity, which can respond to changes in environmental conditions. These findings suggest hope for future corals, if we can reduce anthropogenic water quality stressors