Colour polymorphism and its role in stress tolerance in the coral Acropora millepora on the Great Barrier Reef

The roles of colour and fluorescence in animal species are wide-ranging, but their roles in non-bioluminescent corals remain unresolved, particularly the question of whether or not fluorescent proteins (FPs) in coral tissues have a photoprotective function. Knowledge of the mechanisms corals use to combat stress associated with a changing climate is paramount to predictions of the persistence and management of the coral reef ecosystem. Through a combination of field-based monitoring and controlled experiments, I investigate the role of FPs in corals, using the common coral Acropora millepora, which is comprised of four distinct colour morphs, as a model species. Variation in the proportional abundance patterns of intraspecific colour morphs of A. millepora among widely separated populations provides clues about their comparative performance under different environmental conditions. In Chapter 2, I document patterns in the abundance and distribution of the four colour morphs in populations of A. millepora located in northern, central and southern Great Barrier Reef (GBR) regions. The highly fluorescent green morph was rare at all sites, despite the postulated advantage of FPs in stress tolerance. Moreover, patterns in the relative abundance of colour morphs were similar across latitudinal regions, depths, and wave regimes. Highly conserved patterns in colour morph abundance across a range of environmental gradients suggest that, in general, environmental parameters are not responsible for patterns in the distribution and abundance of colour morphs in this species. Results presented in Chapter 2 also quantify, for the first time, relative concentrations of the three common fluorescent proteins and one non-fluorescent protein in tissues of A. millepora colour morphs. Total FP concentrations differed among colour morphs, with the highly fluorescent green morph containing up to 7- fold greater concentrations of the Cyan FP (CFP) than the weakly fluorescent red morph. In all morphs, the most abundant FP was CFP, which was present in concentrations that were up to 1600-fold higher at less turbid northern sites compared to more turbid southern sites, a pattern consistent with a role in photoprotection. Variation in FP concentrations among colour morphs revealed in this study also indicate that colour is a function of the proportional abundance of the 3 FPs rather than a reflection of the FP in highest concentration. Despite high expression levels of FPs in corals (up to 14% of total protein) and the various important functions ascribed to these proteins, baseline information on temporal variation within coral populations remains undocumented. In Chapter 3, I document FP content in Acropora millepora colour morphs in response to temporal (seasonal) environmental variation. CFP was the only FP to significantly fluctuate in abundance among colour morphs and between sampling times, presumably representing cyclical maintenance of optimal protein levels, given the lengthy halflives of these proteins. Of 150 colonies monitored in-situ, five (~3%) changed colour within a four-month timeframe. Colour change from a highly fluorescent green morph to a weakly fluorescent red morph corresponded with declining health, suggesting that maintenance of high concentrations of FPs in coral tissues is energetically costly. Understanding the mechanisms that underpin variation in bleaching susceptibility in corals is central to the conservation of reefs, particularly in light of predictions of continued ocean warming. In Chapters 4 and 5, I analyse the bleaching condition of three colour morphs of A. millepora, each characterised by different FP levels, following both a moderate bleaching event in the northern GBR and experimental heat stress in the central GBR. In both studies, fragments of the highly fluorescent green morph had greater bleaching resilience to thermal stress compared with the weakly and intermediately fluorescent red and yellow morphs. This is the first demonstration of differential susceptibility to temperature stress among fluorescent colour morphs from similar habitats, and highlights the functional importance of subtle intraspecific differences in FP content. Substantial variation in the response of colour morphs to thermal stress confirmed that high abundance of FPs correlates well with high thermal stress tolerance and highlights the contribution of host-mediated mechanisms in governing the bleaching susceptibility of corals. Despite the advantages of greater tissue concentrations of coral FPs, the highly fluorescent green morph is consistently rare across a variety of habitat types and following major thermal disturbances. Although coral FPs are long-lived, this unexpected pattern in abundance suggests that maintenance of high FP concentrations may come at the cost of other physiological processes, resulting in the low abundance of the green morph across the GBR. In Chapter 6, I investigated the capacity of A. millepora colour morphs to produce FPs under a prolonged period of resource deprivation in the months leading up to their annual reproductive event. Comparisons of investment in reproduction among healthy (control) colour morphs and their starving counterparts leads me to propose that a physiological trade-off exists between investment of resources in the production of FPs versus reproduction. Weakly fluorescent red colonies invested more heavily in reproduction, as indicated by their significantly higher concentrations of wax esters, than highly fluorescent green colonies. Greater investment in reproduction by red colonies corroborates the highly conserved pattern of consistently greater abundance of the red morph in populations of A millepora, and would explain the low abundance of green colonies despite the environmental advantages of containing higher concentrations of coral FPs