Assessing ocean acidification impacts on the reef building properties of crustose coralline algae

Crustose coralline algae (CCA), and in particular Porolithon onkodes, play an important reef-building role in modern tropical coral reefs. CCA form thick crusts of Mg-calcite and grow over corals and loose substrate to bind these together. This binding and cementing process is fundamental to the development of structural reefs that are capable of withstanding the high-energy waves in the shallow to inter-tidal areas of the reef. As anthropogenic CO2 emissions continue to increase, the oceans absorb part of this extra CO2 and become more acidic, a process known as Ocean Acidification (OA). There are concerns that OA will have a negative affect on the reef-building capacity of coral reef organisms, in particular on CCA. This is because Mg-calcite is meta-stable and more susceptible to dissolution than aragonite, the mineral used by corals to build skeletons. The goal of this thesis work was to firstly understand the physical and mechanical properties that enable the CCA to cement the reef and withstand damage from high-energy waves, bioerosion and chemical dissolution. Secondly, to anticipate how OA may interfere with these reef-building properties. These goals were pursued by setting clear aims with associated specific objectives designed to elucidate information relevant to these questions. Methods were developed for X-ray diffraction to identify the mineral composition of CCA. Nanoindentation was investigated as a tool for determining the mechanical properties of CCA and the measurement of fracture toughness was found to return physically meaningful information relevant to structural reef development. Study of CCA calcification showed that cell wall Mg-calcite exhibited radial crystal morphology in agreement with published studies on temperate species. However, high-resolution imaging showed the radial crystals were made of banded stacked sub-micron grains within an organic framework. Dolomite was found not only as cell lining by submicron rhombs, but also as the primary calcification of hypothallial cell walls. Dolomite is shown to be resistant to bacterial erosion. A model is developed whereby it is proposed that dolomite formation is dependent on polysaccharide accumulation. Using nanoindentation, P. onkodes are found to be extraordinarily tough, on par with the measured fracture toughness for metamorphic minerals quartz and corundum. The fracture toughness is enabled by the presence of dolomite cell lining. Contrary to the literature, bacterial erosion is found to be a constructive, not destructive, process. A survey of P. onkodes from Heron Island fore reef and reef flat showed that dolomite was present in all the fore reef crusts but none of the reef flat crusts. The reef flat crusts did not have fracture resistance except where remineralised. The presence of dolomite cell lining was shown to decrease skeletal dissolution rates by an order of magnitude. OA experiments showed that skeletal dissolution rates increased with elevated pCO2, but dolomite continued to confer resistance to dissolution. pCO2 levels did not affect the skeletal Mg content or dolomite formation in living CCA. Of concern, and in agreement with the literature, bacterial erosion is accelerated under a combination of elevated pCO2 and temperatures, suggesting this may be the main threat to CCA reef-building in the future. The experimental findings were corroborated by results of a field survey along a natural pCO2 gradient. In summary, dolomite was found to be an essential component of modern reef development via its contribution to enabling CCA P. onkodes thick crust development and persistence. Reef building by CCA P. onkodes is likely to continue as pCO2 rises up until a tipping point is reached whereby bacterial erosion switches from constructive to destructive

Discovery of dolomite and magnesite in living coralline algae

This Masters started as a consideration of the impacts of ocean acidification on high-magnesium calcite coralline algae. I shifted focus part way through to consider the composition of magnesium calcite sediments from the Great Barrier Reef. While investigating some inconsistencies in X-ray diffraction (XRD) results, I discovered that the coralline algae Hydrolithon onkodes samples I had analysed contained significant amounts of dolomite and magnesite and that this explained inconsistent results not only from my work but also possibly most published work on coralline mineralogy for the past 50 years. My focus again shifted to investigate the occurrence of this dolomite and magnesite, and the final paper presented herein details the discovery of dolomite and magnesite in coralline algae. Early research into coralline algae mineralogy noted the discrepancy between bulk magnesium measurements for mol % MgCO{u2083} and results of those calculated from XRD. This offset was attributed to the presence of amorphous magnesium hydroxide (brucite) or magnesium calcites ranging up to 30 mol % MgCO{u2083}. Some earlier researchers considered that dolomite might be present, but this was unable to be proven. Sedimentary dolomite has been thought to form by a post-depositional diagenetic process that converts limestone to dolomite over long periods of time, perhaps up to millions of years. Marine sedimentary dolomite in fossil coral reefs is typically found in association with coralline algae. Our discovery revealed that dolomite and magnesite can form within living coralline algae. Chemical micro-analysis of the coralline skeleton reveals that not only are the cell walls calcified, but that cell spaces are typically filled with magnesite, rimmed by dolomite or both. Our results are consistent with dolomite occurrences in coralline algae rich environments in fossil reefs of the last 60 million years. Furthermore, this discovery demonstrates that dolomitisation, rather than being a lengthy process over thousands of years or more, can take place contemporaneously with living processes in coralline algae. The question of why this prolific dolomite mineralisation hadn't been discovered previously is considered and comparative treatment tests reveal that the standard process of bleaching prior to XRD analysis can result in a decrease of the intensity of dolomite and magnesite diffraction patterns. Consideration is given to the role of dominant paradigms in obscuring scientific progress in this area of study, and I reflect on how that may have impacted previous research. Finally, I conclude that the XRD method is suitable for estimating mol % MgCO{u2083} for tropical coralline algae cell wall Mg-calcite, that dolomite formed by coralline algae can account for primary dolomite found in Cenozoic reefs, and that the role of biologically formed dolomite needs to be considered when reconstructing past environments

High Magnesium Calcite and Dolomite composition carbonate in Amphiroa (Lithophyllaceae, Corallinales, Rhodophyta): further documentation of elevated Mg in Corallinales with climate change implications

Species of the calcified, articulate coralline Amphiroa are key components of many shallow marine ecosystems. Understanding their mineral composition is important as their susceptibility to dissolution, due to ocean acidification, may vary with mineral composition. We studied the distribution of Mg-calcite, very high magnesium calcite (VHMC), and dolomite within Amphiroa species to elucidate their mineral properties and susceptibility to dissolution. Results revealed that the asymmetrical X-ray diffraction (XRD) pattern typical of Amphiroa globally represents high levels of VHMC and dolomite composition carbonate. The dolomite seems most likely to be disordered, but higher resolution XRD is required for confirmation. The calcified long sides of medullary cells have predominantly VHMC/dolomite and the corners have bands of VHMC/dolomite. Epithallial cell walls are low Mg-calcite, and cortical cells are low Mg-calcite with bands of VHMC. VHMC/dolomite is more stable than Mg-calcite, and this may provide a competitive advantage for Amphiroa species as seawater pH declines. Further work is required to determine the metabolic controls on VHMC/dolomite mineral formation

Ocean acidification: assessing the vulnerability of socioeconomic systems in Small Island Developing States

Ocean acidification poses an increasing threat to marine ecosystems and also interacts with other anthropogenic environmental drivers. A planned response strategy could minimize exposure of socioeconomic systems to potential hazards and may even offer wider advantages. Response strategies can be informed by understanding the hazards, assessing exposure and assessing risks and opportunities. This paper assesses exposure of key socioeconomic systems to the hazards of ocean acidification and analyzes the risks and opportunities of this exposure from Small Island Developing States (SIDS) perspectives. Key socioeconomic systems that are likely to be affected by ocean acidification are identified. A risk analysis matrix is developed to evaluate the risks or opportunities arising from ocean acidification. Analysis of the matrix reveals similarities and differences in potential adaptive responses at global and regional levels. For example, while ocean acidification poses significant threats to SIDS from more frequent toxic wild-caught seafood events and, potentially destruction of coral reef structure and habitat, SIDS may have a relative advantage in aquaculture and an important role to play in global marine ecosystem conservation.This work received funding from the ANU Australian Postgraduate Award (APA) to K.S and LD

Mineralogical response of the Mediterranean crustose coralline alga Lithophyllum cabiochae to near-future ocean acidification and warming

Red calcareous coralline algae are thought to be among the organisms most vulnerable to ocean acidification due to the high solubility of their magnesium calcite skeleton. Although skeletal mineralogy is proposed to change as CO2 and temperature continue to rise, there is currently very little information available on the response of coralline algal carbonate mineralogy to near-future changes in pCO2 and temperature. Here we present results from a 1-year controlled laboratory experiment to test mineralogical responses to pCO2 and temperature in the Mediterranean crustose coralline alga (CCA) Lithophyllum cabiochae. Our results show that Mg incorporation is mainly constrained by temperature (+1 mol % MgCO3 for an increase of 3 °C), and there was no response to pCO2. This suggests that L. cabiochae thalli have the ability to buffer their calcifying medium against ocean acidification, thereby enabling them to continue to deposit magnesium calcite with a significant mol % MgCO3 under elevated pCO2. Analyses of CCA dissolution chips showed a decrease in Mg content after 1 year for all treatments, but this was affected neither by pCO2 nor by temperature. Our findings suggest that biological processes exert a strong control on calcification on magnesium calcite and that CCA may be more resilient under rising CO2 than previously thought. However, previously demonstrated increased skeletal dissolution with ocean acidification will still have major consequences for the stability and maintenance of Mediterranean coralligenous habitats

Ocean acidification does not affect magnesium composition or dolomite formation in living crustose coralline algae, Porolithon onkodes in an experimental system

There are concerns that Mg-calcite crustose coralline algae (CCA), which are key reef builders on coral reefs, will be most susceptible to increased rates of dissolution under higher pCO2 and ocean acidification. Due to the higher solubility of Mg-calcite, it has been hypothesised that magnesium concentrations in CCA Mg-calcite will decrease as the ocean acidifies, and that this decrease will make their skeletons more chemically stable. In addition to Mg-calcite, CCA Porolithon onkodes, the predominant encrusting species on tropical reefs, can have dolomite (Ca0.5Mg0.5CO3) infilling cell spaces which increases their stability. However, nothing is known about how bio-mineralised dolomite formation responds to higher pCO2. Using P. onkodes grown for 3 and 6 months in tank experiments, we aimed to determine (1) if mol % MgCO3 in new crust and new settlement was affected by increasing CO2 levels (365, 444, 676 and 904 μatm), (2) whether bio-mineralised dolomite formed within these time frames, and (3) if so, whether this was effected by CO2. Our results show that there was no significant effect of CO2 on mol % MgCO3 in any sample set, indicating an absence of a plastic response under a wide range of experimental conditions. Dolomite within the CCA cells formed within 3 months and dolomite abundance did not vary significantly with CO2 treatment. While evidence mounts that climate change will impact many sensitive coral and CCA species, the results from this study indicate that reef-building P. onkodes will continue to form stabilising dolomite infill under near-future acidification conditions, thereby retaining its higher resistance to dissolution

Presence of skeletal banding in a reef-building tropical crustose coralline alga

The presence of banding in the skeleton of coralline algae has been reported in many species, primarily from temperate and polar regions. Similar to tree rings, skeletal banding can provide information on growth rate, age, and longevity; as well as records of past environmental conditions and the coralline alga’s growth responses to such changes. The aim of this study was to explore the presence and characterise the nature of banding in the tropical coralline alga Porolithon onkodes, an abundant and key reef-building species on the Great Barrier Reef (GBR) Australia, and the Indo-Pacific in general. To achieve this we employed various methods including X-ray diffraction (XRD) to determine seasonal mol% magnesium (Mg), mineralogy mapping to investigate changes in dominant mineral phases, scanning electron microscopy–electron dispersive spectroscopy (SEM-EDS), and micro-computed tomography (micro-CT) scanning to examine changes in cell size and density banding, and UV light to examine reproductive (conceptacle) banding. Seasonal variation in the Mg content of the skeleton did occur and followed previously recorded variations with the highest mol% MgCO3 in summer and lowest in winter, confirming the positive relationship between seawater temperature and mol% MgCO3. Rows of conceptacles viewed under UV light provided easily distinguishable bands that could be used to measure vertical growth rate (1.4 mm year-1) and age of the organism. Micro-CT scanning showed obvious banding patterns in relation to skeletal density, and mineralogical mapping revealed patterns of banding created by changes in Mg content. Thus, we present new evidence for seasonal banding patterns in the tropical coralline alga P. onkodes. This banding in the P. onkodes skeleton can provide valuable information into the present and past life history of this important reef-building species, and is essential to assess and predict the response of these organisms to future climate and environmental changes

Simple X-ray diffraction techniques to identify mg calcite, dolomite, and magnesite in tropical coralline algae and assess peak asymmetry

Understanding of dolomite development in reef environments has been frustrated by the failure to identify dolomite forming in abundant tropical reef algae. The analytical and sampling techniques presented here will allow fundamental questions about dolom

Spatial variation in mechanical properties of coral reef substrate and implications for coral colony integrity

The physical structure of coral reefs plays a critical role as a barrier to storm waves and tsunamis and as a habitat for living reef-building and reef-associated organisms. However, the mechanical properties of reef substrate (i. e. the non-living benthos) are largely unknown, despite the fact that substrate properties may ultimately determine where organisms can persist. We used a geo-mechanical technique to measure substrate material density and strength over a reef hydrodynamic gradient. Contrary to expectation, we found a weak relationship between substrate strength and wave-induced water flow: flow rates decline sharply at the reef crest, whereas substrate properties are relatively constant over much of the reef before declining by almost an order of magnitude at the reef back. These gradients generate a novel hump-shaped pattern in resistance to mechanical disturbances for live corals, where colonies closer to the back reef are prone to dislodgement because of poorly cemented substrate. Our results help explain an intermediate zone of higher taxonomic and morphological diversity bounded by lower diversity exposed reef crest and unstable reef back zones

Coralline algal calcification: A morphological and process-based understanding.

RESEARCH PURPOSE AND FINDINGS:Coralline algae are key biological substrates of many carbonate systems globally. Their capacity to build enduring crusts that underpin the formation of tropical reefs, rhodolith beds and other benthic substrate is dependent on the formation of a calcified thallus. However, this important process of skeletal carbonate formation is not well understood. We undertook a study of cellular carbonate features to develop a model for calcification. We describe two types of cell wall calcification; 1) calcified primary cell wall (PCW) in the thin-walled elongate cells such as central medullary cells in articulated corallines and hypothallial cells in crustose coralline algae (CCA), 2) calcified secondary cell wall (SCW) with radial Mg-calcite crystals in thicker-walled rounded cortical cells of articulated corallines and perithallial cells of CCA. The distinctive banding found in many rhodoliths is the regular transition from PCW-only cells to SCW cells. Within the cell walls there can be bands of elevated Mg with Mg content of a few mol% higher than radial Mg-calcite (M-type), ranging up to dolomite composition (D-type). MODEL FOR CALCIFICATION:We propose the following three-step model for calcification. 1) A thin (< 0.5 μm) PCW forms and is filled with a mineralising fluid of organic compounds and seawater. Nanometer-scale Mg-calcite grains precipitate on the organic structures within the PCW. 2) Crystalline cellulose microfibrils (CMF) are extruded perpendicularly from the cellulose synthase complexes (CSC) in the plasmalemma to form the SCW. 3) The CMF soaks in the mineralising fluid as it extrudes and becomes calcified, retaining the perpendicular form, thus building the radial calcite. In Clathromorphum, SCW formation lags PCW creating a zone of weakness resulting in a split in the sub-surface crust. All calcification seems likely to be a bioinduced rather than controlled process. These findings are a substantial step forward in understanding how corallines calcify