Interactive effects of ocean acidification and warming on sediment-dwelling marine calcifiers

The increase in human activities, such as the burning of fossil fuels, has elevated the concentration of atmospheric carbon dioxide and warmed the planet through the greenhouse effect. In addition, approximately 30% of the CO2 produced by human activities has dissolved into the oceans, lowering pH and reducing the abundance, and hence the availability, of carbonate ions (CO3 2-), which are essential for calcium carbonate deposition. Of great concern is the impact to photosynthetic marine calcifiers, elevated CO2 and temperature is expected to have a negative impact on the health and survivorship of calcifying marine organisms. This thesis explores the effects of elevated CO2 and temperature on the microenvironment, photosynthetic efficiency, calcification and biomechanical properties in important sediment producers on coral reefs. The reef-building and sedimentdwelling organisms, Halimeda and symbiont-bearing foraminifera are prominent, coexisting taxa in shallow coral reefs and play a vital role in tropical and subtropical ecosystems as producers of sediment and habitats and food sources for other marine organisms. However, there is limited evidence of the effects of ocean warming and acidification in these two keystone species. Irradiance alone was not found to influence photosynthetic efficiency, photoprotective mechanisms and calcification in Halimeda macroloba, Halimeda cylindracea and Halimeda opuntia (Chapter 2). There is also limited knowledge of foraminiferal biology on coral reefs, especially the symbiotic relationship between the protest host and algal symbionts. Marginopora vertebralis, the dominant tropical foraminifera, shows phototactic behavior, which is a unique mechanism for ensuring symbionts experience an ideal light environment. The diurnal photosynthetic responses of in hospite symbiont photosynthesis was linked to host movement and aided in preventing photoinhibition and bleaching by moving away from over-saturating irradiance, to more optimal light fields (Chapter 3). With this greater understanding of Halimeda and foraminiferan biology and photosynthesis, the impacts of ocean warming and acidification on photosynthesis and calcification were then tested (Chapter 4, 5 and 6). Impacts of ocean acidification and warming were investigated through exposure to a combination of four temperature (28, 30, 32, 34°C) and four pCO2 levels (380, 600, 1000, 2000 µatm; equivalent to future climate change scenarios for the current and the years 2065, 2100 and 2200 and simulating the IPCC A1F1 predictions) (Chapter 4). Elevated CO2 and temperature caused a decline in photosynthetic efficiency (FV/FM), calcification and growth in all species. After five weeks at 34°C under all CO2 levels, all species died. The elevated CO2 and temperature greatly affect the CaCO3 crystal formation with reductions in density and width. M. vertebralis experienced the greatest inhibition to crystal formation, suggesting that this high Mg-calcite depositing species is more sensitive to lower pH and higher temperature than aragonite-forming Halimeda species. Exposure to elevated temperature alone or reduced pH alone decreased photosynthesis and calcification in these species. However, there was a strong synergistic effect of elevated temperature and reduced pH, with dramatic reductions in photosynthesis and calcification in all three species. This study suggested that the elevated temperature of 32°C and the pCO2 concentration of 1000 µatm are the upper limit for survival of these species art our site of collection (Heron Island on the Great Barrier Reef, Australia). Microsensors enabled the detection of O2 surrounding specimens at high spatial and temporal resolutions and revealed a 70-80% in decrease in O2 production under elevated CO2 and temperature (1200 µatm 32°C) in Halimeda (Chapter 5) and foraminifera (Chapter 6). The results from O2 microprofiles support the photosynthetic pigment and chlorophyll fluorescence data, showing decreasing O2 production with declining chlorophyll a and b concentrations and a decrease in photosynthetic efficiency under ocean acidification and/or temperature stress. This revealed that photosynthesis and calcification are closely coupled with reductions in photosynthetic efficiency leading to reductions in calcification. Reductions in carbonate availability reduced calcification and that can lead to weakened calcified structures. Elevations in water temperature is expected to augment this weakening, resulting in decreased mechanical integrity and increased susceptibility to storm- and herbivory-induced mortality in Halimeda sp. The morphological and biomechanical properties in H. macroloba and H. cylindracea at different wave exposures were then investigated in their natural reef habitats (Chapter 7). The results showed that both species have morphological (e.g. blade surface area, holdfast volume) and biomechanical (e.g. force required to uproot, force required to break thalli) adaptations to different levels of hydrodynamic exposure. The mechanical integrity and skeletal mineralogy of Halimeda was then investigated in response to future climate change scenarios (Chapter 7). The biomechanical properties (shear strength and punch strength) significantly declined in the more heavily calcified H. cylindracea at 32ºC and 1000 µatm, whereas were variable in less heavily calcified H. macroloba, indicating different responses between Halimeda species. An increase in less-soluble low Mgcalcite was observed under elevated CO2 conditions. Significant changes in Mg:Ca and Sr:Ca ratios under elevated CO2 and temperature conditions suggested that calcification was affected at the ionic level. It is concluded that Halimeda is biomechanically sensitive to elevated temperature and more acidic oceans and may lead to increasing susceptibility to herbivory and higher risk of thallus breakage or removal from the substrate. Experimental results throughout the thesis revealed that ocean acidification and warming have negative impacts on photosynthetic efficiency, productivity, calcification and mechanical integrity, which is likely to lead to increased mortality in these species under a changing climate. A loss of these calcifying keystone species will have a dramatic impact on carbonate accumulation, sediment turnover, and coral reef community and habitat structure.

Sinutok S., 2013. Interactive effects of ocean acidification and warming on sediment-dwelling marine calcifiers. PhD thesis, University of Technology Sydney, 268 p. Thesis.

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