CO2-driven ocean acidification reduces larval feeding efficiency and change food selectivity in the mollusk Concholepas concholepas

We present experimental data obtained from an experiment with newly hatched veliger larvae of the gastropod Concholepas concholepas exposed to three pCO₂ levels. Egg capsules were collected from two locations in northern and central Chile, and then incubated throughout their entire intra-capsular life cycle at three nominal pCO₂ levels, ∼400, 700 and 1000 ppm (i.e. corresponding to ∼8.0, 7.8 and 7.6 pH units, respectively). Hatched larvae were fed with natural food assemblages. Food availability at time zero did not vary significantly with pCO₂ level. Our results clearly showed a significant effect of elevated pCO₂ on the intensity of larval feeding, which dropped by >60%. Incubation also showed that pCO₂-driven ocean acidification (OA) may radically impact the selectivity of ingested food by C. concholepas larvae. Results also showed that larvae switched their clearance rate based on large cells, such as diatoms and dinoflagellates to tiny and highly abundant nanoflagellates and cyanobacteria as pCO₂ levels increased. Thus, this study reveals the important effect of low pH conditions on larval feeding behavior, in terms of both ingestion magnitude and selectivity. These findings support the notion that larval feeding is a key physiological process susceptible to the effects of OA.

Occurrence of a cold-water coral along natural pH gradients (Patagonia, Chile)

Increasing dissolution of anthropogenic-released carbon dioxide into the world’s oceans is causing ocean acidification (OA). OA is thought to negatively affect most marine-calcifying organisms, notably cold-water corals (CWC), which may be especially sensitive due to the deep and cold waters they normally thrive in. However, the impact of OA on CWC is difficult to predict. Recorded distributions of CWC are rarely linked to in situ water chemistry, and the boundaries of their distributions are not clearly defined. The fjord Comau in Chilean Patagonia features pronounced pH gradients, and up to 0.5 pH units have been recorded both vertically (at some sites within 50 m depth) and less distinct horizontally (from head to mouth). The cosmopolite coral Desmophyllum dianthus grows along the course of the fjord and of the entire pH range. It occurs in shallow depths (below 12 m, pH 8.1) as part of a deep-water emergence community, but also in 225 m depth at a pH of 7.4. Based on pH and total alkalinity, data calculations of the associated carbonate chemistry revealed that this CWC thrives commonly close the aragonite (the orthogonal crystal form of calcium carbonate, the mineral structure of coral skeletons) saturation horizon and even below. This suggests a high adaptation potential of D. dianthus to adjust its calcification performance to conditions thermodynamically unfavourable for the precipitation of aragonite.

The global impacts of climate change on fish

Climate change is a global issue and the effects on fish populations remain largely unknown. It is thought that climate change could affect fish at all levels of biological organisation, from cellular,
individual, population and community. This thesis has taken a holistic approach to examine the ways in which climate change could affect fish from both tropical, marine ecosystems (Great Barrier Reef,
Australia) and temperate, freshwater ecosystems (non-tidal River Thames, Britain). Aerobic scope of coral reef fish tested on the Great Barrier Reef was significantly reduced by just a 2°C rise in water temperature (31, 32 and 33°C, compared to the current summer mean of 29°C) due to increased resting oxygen consumption and an inability to increase the maximal oxygen uptake. A 0.3 unit decline in pH, representative of ocean acidification, caused the same percentage loss in aerobic scope as did a 3°C warming. Interfamilial differences in ability to cope aerobically with warming waters will likely lead to changes in the community structure on coral reefs with damselfish replacing cardinalfish.

Concerning Britain, there is evidence of gradual warming and increased rainfall in winter months over a 150 year period, suggesting that British fish are already experiencing climate change. It was evident from an analysis of a 15 year dataset on fish populations in the River Thames, that cyprinid species displayed a different pattern in biomass and density to all the non-cyprinid fish population, suggesting that there will be interfamilial differences in responses to climate change.

Using a Biological Indicator Approach on the three-spined stickleback, Gasterosteus aculeatus, a 2°C rise in water temperature resulted in a stress response at the cellular and whole organism level. A 6°C rise in temperature resulted in a stress response at the biochemical level (higher cortisol and glucose concentrations), cellular level (higher neutrophil: lymphocyte ratio) and whole organism level (higher ventilation rate and lowered condition factor, hepatosomatic index and growth). G. aculeatus is considered to be temperature tolerant; therefore these results indicate that climate change may prove to be stressful for more temperature-sensitive species. This study has demonstrated that climate change will have direct effects on fish populations, whether they are in temperate regions such as Britain or in tropical coral reefs,but with strong interfamilial differences in those responses.

Acid sulfate soil induced acidification of estuarine areas used for the production of Sydney Rock oysters, Saccostrea glomerata

This study investigated estuarine acidification, associated with drainage and excavation of acid sulfate soils, in areas used for commercial cultivation of Sydney rock oysters (Saccostrea glomerata). Regular measurements of pH and electrical conductivity were collected in oyster cultivation areas and acidified reaches of the Hastings River estuary and Port Stephens estuary located on the mid north coast of New South Wales, Australia. Water quality information from acidified floodplain drains was also collected in the Hastings River following heavy rainfall. Both estuaries experienced acidification of tributaries following periods of heavy rainfall. Drain outflow waters were acidic (pH < 3.5); contained elevated concentrations of iron, aluminium, manganese and zinc; and polluted areas used for oyster production. The extent and duration of estuarine acidification events was capable of causing a variety of short- and long-term impacts to oysters as well as other aquatic organisms in affected areas.

High risk of extinction of benthic foraminifera in this century due to ocean acidification

Increased atmospheric CO₂ concentrations lead to decreased pH and carbonate availability in the ocean (Ocean Acidification, OA). Carbon dioxide seeps serve as ‘windows into the future’ to study the ability of marine invertebrates to acclimatise to OA. We studied benthic foraminifera in sediments from shallow volcanic CO₂ seeps in Papua New Guinea. Conditions follow a gradient from present day pH/pCO₂ to those expected past 2100. We show that foraminiferal densities and diversity declined steeply with increasing pCO_2. Foraminifera were almost absent at sites with pH < 7.9 (>700 μatm pCO₂). Symbiont-bearing species did not exhibit reduced vulnerability to extinction at <7.9 pH. Non-calcifying taxa declined less steeply along pCO₂ gradients, but were also absent in samples at pH < 7.9. Data suggest the possibility of an OA induced ecological extinction of shallow tropical benthic foraminifera by 2100; similar to extinctions observed in the geological past.

Dynamics of seawater carbonate chemistry, production, and calcification of a coral reef flat, Central Great Barrier Reef

Ocean acidification is projected to shift coral reefs from a state of net accretion to one of net dissolution this century. Presently, our ability to predict global-scale changes to coral reef calcification is limited by insufficient data relating seawater carbonate chemistry parameters to in situ rates of reef calcification. Here, we investigate natural trends in carbonate chemistry of the Davies Reef flat in the central Great Barrier Reef on diel and seasonal timescales and relate these trends to benthic carbon fluxes by quantifying net ecosystem calcification (nec) and net community production (ncp). Results show that seawater carbonate chemistry of the Davies Reef flat is highly variable over both diel and seasonal timescales. pH (total scale) ranged from 7.92 to 8.17, pCO₂ ranged from 272 to 542 μatm, and aragonite saturation state (Ω_arag) ranged from 2.9 to 4.1. Diel cycles in carbonate chemistry were primarily driven by ncp, and warming explained 35% and 47% of the seasonal shifts in pCO₂ and pH, respectively. Daytime ncp averaged 36 ± 19 mmol C m⁻² h⁻¹ in summer and 33 ± 13 mmol C m⁻² h⁻¹ in winter; nighttime ncp averaged −22 ± 20 and −7 ± 6 mmol C m⁻² h⁻¹ in summer and winter, respectively. Daytime nec averaged 11 ± 4 mmol CaCO₃ m⁻² h⁻¹ in summer and 8 ± 3 mmol CaCO₃ m⁻² h⁻¹ in winter, whereas nighttime nec averaged 2 ± 4 mmol and −1 ± 3 mmol CaCO₃ m⁻² h⁻¹ in summer and winter, respectively. Net ecosystem calcification was positively correlated with Ω_arag for both seasons. Linear correlations of nec and Ω_arag indicate that the Davies Reef flat may transition from a state of net calcification to net dissolution at Ω_arag values of 3.4 in summer and 3.2 in winter. Diel trends in Ω_arag indicate that the reef flat is currently below this calcification threshold 29.6% of the time in summer and 14.1% of the time in winter.

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.

Carbonate dissolution rates at the deep ocean floor

This paper reexamines experimental data on the seawater dissolution of CaCO₃-bearing sediment beds to establish that the dependence of the calcite dissolution rate is linearly dependent on the calcite saturation state of the overlying water. This linearity is inherent to the original data and is not the result of an error in the solubility product for calcite. A comparison between these linear kinetics and the rate of solute transport across the benthic boundary layer further reveals that the overall rate of dissolution at ocean depths below the saturation horizon is controlled by boundary layer transfer. A carbonate mass-balance model for the sediment-water interface, which includes both kinetics and boundary layer effects, predictively reproduces the currently observed CaCO₃ depth distribution for two test areas in the oceans. These findings allow important simplifications in modeling CO₂ neutralization in the oceans.

Mixed responses of tropical Pacific fisheries and aquaculture to climate change

Pacific Island countries have an extraordinary dependence on fisheries and aquaculture. Maintaining the benefits from the sector is a difficult task, now made more complex by climate change. Here we report how changes to the atmosphere–ocean are likely to affect the food webs, habitats and stocks underpinning fisheries and aquaculture across the region. We found winners and losers—tuna are expected to be more abundant in the east and freshwater aquaculture and fisheries are likely to be more productive. Conversely, coral reef fisheries could decrease by 20% by 2050 and coastal aquaculture may be less efficient. We demonstrate how the economic and social implications can be addressed within the sector—tuna and freshwater aquaculture can help support growing populations as coral reefs, coastal fisheries and mariculture decline.

Elevated CO2 affects predator-prey interactions through altered performance

Recent research has shown that exposure to elevated carbon dioxide (CO₂) affects how fishes perceive their environment, affecting behavioral and cognitive processes leading to increased prey mortality. However, it is unclear if increased mortality results from changes in the dynamics of predator-prey interactions or due to prey increasing activity levels. Here we demonstrate that ocean pCO₂ projected to occur by 2100 significantly effects the interactions of a predator-prey pair of common reef fish: the planktivorous damselfish Pomacentrus amboinensis and the piscivorous dottyback Pseudochromis fuscus. Prey exposed to elevated CO₂ (880 µatm) or a present-day control (440 µatm) interacted with similarly exposed predators in a cross-factored design. Predators had the lowest capture success when exposed to elevated CO₂ and interacting with prey exposed to present-day CO₂. Prey exposed to elevated CO₂ had reduced escape distances and longer reaction distances compared to prey exposed to present-day CO₂ conditions, but this was dependent on whether the prey was paired with a CO₂ exposed predator or not. This suggests that the dynamics of predator-prey interactions under future CO₂ environments will depend on the extent to which the interacting species are affected and can adapt to the adverse effects of elevated CO₂.