Carbon physiological strategies across dominant Great Barrier Reef crustose coralline algae in the context of evolutionary history and global change

Abstract

Crustose coralline algae (CCA) are calcifying marine red macroalgae that play key ecological roles in building and cementing reef structures, and contribute significantly to the coastal marine carbon cycle. Anthropogenic global change is advancing rapidly and its two main threats in the marine realm, ocean acidification (OA) and ocean warming, have been empirically shown to impair the physiology of CCA. However, the presence of CCA in the geological record dates back to more than 180 million years ago, indicating that CCA have endured periods of substantial fluctuation in oceanic temperature and pCO2. CCA taxa comprise three lineages: Corallinales (most recently evolved), Hapalidiales (intermediate/more basal), and Sporolithales (most basal). Yet, it is still not well understood how their distinct evolutionary histories may have affected selection for certain physiological strategies and how this may shape trends in their responses to OA and warming. Two key carbon physiological processes in CCA are photosynthesis and calcification, and due to their variable and interdependent nature, the observation of a singular physiological response may not suffice in predicting the long-term survival of these reef-building macroalgae. Gaps exist in the knowledge of mechanisms that underpin carbon fixation and biomineralisation across lineages that would ultimately elucidate the fate of CCA taxa under global threats. Thus, I aimed to identify the strategies that exist across various carbon physiological processes: inorganic carbon uptake, carbon partitioning, carbon release, and cell wall organic matrix composition, which allow the movement of carbon into, within, and out of the CCA thallus. I examined six common CCA species from the northern Great Barrier Reef that belong to lineages with distinct evolutionary histories (time and environmental conditions endured). I chose three dominant taxa that pertain to the more basal lineages and occupy low-light habitats, and three dominant taxa that belong to the most recently evolved lineage and occupy high-light environments. I conducted experiments where OA and warming scenarios (largely IPCC 8.5) were simulated in a flow-through mesocosm system, CCA fragments were subjected to treatment for 1-2 months, and physiological strategies and their responses to treatment were quantified. First, to establish the extent of diffusive CO2 and/or HCO3- use, inorganic carbon uptake was characterised by measuring the stable carbon isotope ratio of surficial CCA tissue (Chapter 2). Second, I determined patterns in the quantity of carbon partitioned to surficial organic tissue and inorganic skeleton, as well as the amount of carbon released as dissolved organic carbon (DOC) (Chapter 3). Finally, I examined strategies of the monosaccharide composition of polysaccharides that compose the cell wall in surficial organic tissue, and its relationship with biomineralisation capacity (Chapter 4). The results indicated that CCA possess a range of strategies within each physiological process. In Chapters 2 and 3, I found that CCA from basal lineages that evolved to occupy low-light environments largely possess strategies of greater diffusive CO2 uptake, lower organic:inorganic biomass ratios, and from a zero to positive net efflux of DOC. On the other hand, CCA from the more recently-evolved lineage that occupy high-light environments largely possess greater HCO3- uptake, higher organic:inorganic biomass ratios, and a net DOC influx. Results from Chapter 4 suggest variability in abundance of cellulose, mannan, alginate, and galactan across taxa. Patterns in the abundance of a monomer of alginate indicate a positive correlation between alginate abundance and biomineralisation potential. However, composition is largely not predicted by evolutionary history. In response to OA and warming, Chapter 2 results indicate that CCA largely increase HCO3- uptake across strategies, which is associated with maintained or increased metabolic performance. Chapter 3 results suggest that while low-light CCA tend to retain carbon content in their surficial thallus and switch to a net influx of DOC under global change, high-light taxa largely decrease surficial carbon content and release more DOC. Chapter 4 results demonstrate that monosaccharides were differentially modulated across CCA taxa under OA and warming. Changes in the monosaccharides of the important reef-builder P. cf. onkodes were correlated with lower biomineralisation capacity. Overall, these findings provide a framework for characterising the distinct strategies of carbon acquisition, partitioning, release, and organic matrix composition across dominant reef-building CCA of the Great Barrier Reef. The data suggest that some physiological strategies may be specific to high- or low-light reef environments, showing the importance of the relationship between light availability and carbon fluxes. The data also indicate that the distinct environmental conditions during which each CCA lineage evolved may have played a role in the diversity of carbon physiologies across CCA. Ultimately, the carbon physiological responses of some species were more suitable to maintain metabolic performance, and may potentially be more adaptable to global change than others. These findings suggest that if less robust CCA are not capable of acclimating/adapting relatively quickly, there may be serious repercussions for the integrity and ecology of certain reef environments into the Anthropocene.