Heidi L. Burdett

The future of the northeast Atlantic benthic flora in a high CO2 world

Seaweed and seagrass communities in the northeast Atlantic have been profoundly impacted by humans, and the rate of change is accelerating rapidly due to runaway CO2 emissions and mounting pressures on coastlines associated with human population growth and increased consumption of finite resources. Here, we predict how rapid warming and acidification are likely to affect benthic flora and coastal ecosystems of the northeast Atlantic in this century, based on global evidence from the literature as interpreted by the collective knowledge of the authorship. We predict that warming will kill off kelp forests in the south and that ocean acidification will remove maerl habitat in the north. Seagrasses will proliferate, and associated epiphytes switch from calcified algae to diatoms and filamentous species. Invasive species will thrive in niches liberated by loss of native species and spread via exponential development of artificial marine structures. Combined impacts of seawater warming, ocean acidification, and increased storminess may replace structurally diverse seaweed canopies, with associated calcified and noncalcified flora, with simple habitats dominated by noncalcified, turf-forming seaweeds.

Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification

Marine pCO2 enrichment via ocean acidification (OA), upwelling and release from carbon capture and storage (CCS) facilities is projected to have devastating impacts on marine biomineralisers and the services they provide. However, empirical studies using stable endpoint pCO2 concentrations find species exhibit variable biological and geochemical responses rather than the expected negative patterns. In addition, the carbonate chemistry of many marine systems is now being observed to be more variable than previously thought. To underpin more robust projections of future OA impacts on marine biomineralisers and their role in ecosystem service provision, we investigate coralline algal responses to realistically variable scenarios of marine pCO2 enrichment. Coralline algae are important in ecosystem function; providing habitats and nursery areas, hosting high biodiversity, stabilizing reef structures and contributing to the carbon cycle. Red coralline marine algae were exposed for 80 days to one of three pH treatments: (i) current pH (control); (ii) low pH (7.7) representing OA change; and (iii) an abrupt drop to low pH (7.7) representing the higher rates of pH change observed at natural vent systems, in areas of upwelling and during CCS releases. We demonstrate that red coralline algae respond differently to the rate and the magnitude of pH change induced by pCO2 enrichment. At low pH, coralline algae survived by increasing their calcification rates. However, when the change to low pH occurred at a fast rate we detected, using Raman spectroscopy, weaknesses in the calcite skeleton, with evidence of dissolution and molecular positional disorder. This suggests that, while coralline algae will continue to calcify, they may be structurally weakened, putting at risk the ecosystem services they provide. Notwithstanding evolutionary adaptation, the ability of coralline algae to cope with OA may thus be determined primarily by the rate, rather than magnitude, at which pCO2 enrichment occurs.

The effect of chronic and acute low pH on the intracellular DMSP production and epithelial cell morphology of red coralline algae

Abstract The release of dimethylsulphoniopropionate (DMSP) by marine algae has major impacts on the global sulphur cycle and may influence local climate through the formation of dimethylsulphide (DMS). However, the effect of global change on DMSP/DMS (DMS(P)) production by algae is not well understood. This study examined the effect of low pH on DMS(P) production and epithelial cell morphology of the free-living red coralline alga Lithothamnion glaciale. Three pH treatments were used in the 80-day experiment: (1) current pH level (8.18, control), (2) low, chronic pH representing a 2100 ocean acidification (OA) scenario (7.70) and (3) low, acute pH (7.75, with a 3-day spike to 6.47), representing acute variable conditions that might be associated with leaks from carbon capture and storage infrastructure, at CO2 vent sites or in areas of upwelling. DMS(P) production was not significantly enhanced under low, stable pH conditions, indicating that red coralline algae may have some resilience to OA. However, intracellular and water column DMS(P) concentrations were significantly higher than the control when pH was acutely spiked. Cracks were observed between the cell walls of the algal skeleton in both low pH treatments. It is proposed that this structural change may cause membrane damage that allows DMS(P) to leak from the cells into the water column, with subsequent implications for the cycling of DMS(P) in coralline algae habitats.

Dynamic photoinhibition exhibited by red coralline algae in the red sea

BackgroundRed coralline algae are critical components of tropical reef systems, and their success and development is, at least in part, dependent on photosynthesis. However, natural variability in the photosynthetic characteristics of red coralline algae is poorly understood. This study investigated diurnal variability in encrusting Porolithon sp. and free-living Lithophyllum kotschyanum. Measured parameters included: photosynthetic characteristics, pigment composition, thallus reflectance and intracellular concentrations of dimethylsulphoniopropionate (DMSP), an algal antioxidant that is derived from methionine, an indirect product of photosynthesis. L. kotschyanum thalli were characterised by a bleached topside and a pigmented underside.ResultsMinimum saturation intensity and intracellular DMSP concentrations in Porolithon sp. were characterised by significant diurnal patterns in response to the high-light regime. A smaller diurnal pattern in minimum saturation intensity in the topside of L. kotschyanum was also evident. The overall reflectance of the topside of L. kotschyanum also exhibited a diurnal pattern, becoming increasingly reflective with increasing ambient irradiance. The underside of L. kotschyanum, which is shaded from ambient light exposure, exhibited a much smaller diurnal variability.ConclusionsThis study highlights a number of dynamic photoinhibition strategies adopted by coralline algae, enabling them to tolerate, rather than be inhibited by, the naturally high irradiance of tropical reef systems; a factor that may become more important in the future under global change projections. In this context, this research has significant implications for tropical reef management planning and conservation monitoring, which, if natural variability is not taken into account, may become flawed. The information provided by this research may be used to inform future investigations into the contribution of coralline algae to reef accretion, ecosystem service provision and palaeoenvironmental reconstruction.

Evidence for phosphonate usage in the coral holobiont

Phosphonates are characterized by a stable carbon–phosphorus bond and commonly occur as lipid conjugates in invertebrate cell membranes. Phosphonoacetate hydrolase encoded by the phnA gene, catalyses the cleavage of phosphonoacetate to acetate and phosphate. In this study, we demonstrate the unusually high phnA diversity in coral-associated bacteria. The holobiont of eight coral species tested positive when screened for phnA using degenerate primers. In two soft coral species, Sinularia and Discosoma, sequencing of the phnA gene showed 13 distinct groups on the basis of 90% sequence identity across 100% of the sequence. A total of 16 bacterial taxa capable of using phosphonoacetate as the sole carbon and phosphorus source were isolated; 8 of which had a phnA+ genotype. This study enhances our understanding of the wide taxonomic and environmental distribution of phnA, and highlights the importance of phosphonates in marine ecosystems.

Spatiotemporal Variability of Dimethylsulphoniopropionate on a Fringing Coral Reef: The Role of Reefal Carbonate Chemistry and Environmental Variability

Oceanic pH is projected to decrease by up to 0.5 units by 2100 (a process known as ocean acidification, OA), reducing the calcium carbonate saturation state of the oceans. The coastal ocean is expected to experience periods of even lower carbonate saturation state because of the inherent natural variability of coastal habitats. Thus, in order to accurately project the impact of OA on the coastal ocean, we must first understand its natural variability. The production of dimethylsulphoniopropionate (DMSP) by marine algae and the release of DMSP’s breakdown product dimethylsulphide (DMS) are often related to environmental stress. This study investigated the spatiotemporal response of tropical macroalgae (Padina sp., Amphiroa sp. and Turbinaria sp.) and the overlying water column to natural changes in reefal carbonate chemistry. We compared macroalgal intracellular DMSP and water column DMSP+DMS concentrations between the environmentally stable reef crest and environmentally variable reef flat of the fringing Suleman Reef, Egypt, over 45-hour sampling periods. Similar diel patterns were observed throughout: maximum intracellular DMSP and water column DMS/P concentrations were observed at night, coinciding with the time of lowest carbonate saturation state. Spatially, water column DMS/P concentrations were highest over areas dominated by seagrass and macroalgae (dissolved DMS/P) and phytoplankton (particulate DMS/P) rather than corals. This research suggests that macroalgae may use DMSP to maintain metabolic function during periods of low carbonate saturation state. In the reef system, seagrass and macroalgae may be more important benthic producers of dissolved DMS/P than corals. An increase in DMS/P concentrations during periods of low carbonate saturation state may become ecologically important in the future under an OA regime, impacting larval settlement and increasing atmospheric emissions of DMS.

The photosynthetic characteristics of red coralline algae, determined using pulse amplitude modulation (PAM) fluorometry

Abstract Interest in red coralline algae is increasing due to their projected sensitivity to ocean acidification and their utility as palaeoenvironmental proxies. Thus, it is crucial to obtain a thorough understanding of their basic photosynthetic characteristics and appropriate techniques for use in both laboratory and in situ studies. This study provides fluorescence methodology and data for the ecologically important red coralline alga Lithothamnion glaciale using pulse amplitude modulation (PAM) fluorometry. Lithothamnion glaciale was sufficiently dark-acclimated for in situ work following 10 s of quasi-darkness, attaining 95–98% of the maximum photochemical efficiency (Fv/Fm). Rapid light curves conducted in situ and in the laboratory determined a low light adaptation, with a saturation intensity of 4.45–54.6 μmol photons m-2 s-1. Intra-thallus heterogeneity was observed between branch tips and bases (i.e., within the thallus) using a custom-made 2 mm fibre optic probe (the heterogeneity could not be detected using the standard 5 mm probe). Branch bases were lower light acclimated than the tips, with higher maximum effective quantum yield (Fq′/Fm′max) and lower non-photochemical quenching. Samples measured in May were higher light acclimated than in March, which suggests a degree of seasonal acclimation. Light history and photon irradiance levels were thus found to significantly affect the photosynthetic characteristics of L. glaciale.

Effects of reduced salinity on the photosynthetic characteristics and intracellular DMSP concentrations of the red coralline alga, Lithothamnion glaciale

Abstract Mid- to high-latitude fjordic coastal environments experience naturally variable salinity regimes. Climate projections suggest that freshwater input into the coastal ocean will increase in the future, exposing coastal organisms to further periods of reduced salinity. This study investigated the effect of low salinity on Lithothamnion glaciale, a red coralline alga found in mid- to high-latitude fjordic regions, during a 21-day experiment. Specific measurements included: the intracellular concentration of dimethylsulphoniopropionate (DMSP, an algal secondary metabolite and major precursor to the climatically active gas dimethylsulphide), pigment composition and photosynthetic characteristics. No significant difference in intracellular DMSP concentrations was observed between treatments, suggesting that the primary function for DMSP in L. glaciale is not as a compatible solute, perhaps favouring an antioxidant role . Photosynthetic parameters (including pigment composition) exhibited a mixed response, suggesting some degree of photosynthetic resilience to reduced salinity. This study provides evidence of intracellular mechanisms adopted by L. glaciale in response to reduced salinity. This has significant implications for the survival of L. glaciale under a projected freshening scenario and provides organism-level detail to ecosystem-level projected changes should lower-salinity conditions become more frequent and more intense in the future.

Coralline Algae as Recorders of Past Climatic and Environmental Conditions

Calcifying marine organisms can be used as recorders, or proxies, of past environmental conditions if they lock physical or chemical signals within their skeletal material. Coralline algae lay down regular growth bands and the study of their structure and composition has gained increasing attention as a technique for reconstructing past environments in tropical, temperate and polar regions. Structurally, growth band width and percentage calcification have been used as records of historic light availability (e.g. due to cloud cover and sea ice extent). The chemical composition of their high Mg calcite skeleton has received significantly more attention, being used to reconstruct temperature, salinity, dissolved inorganic carbon, upwelling patterns and wider climate indices. At the ecosystem level, such reconstructions have been used to shed light on the drivers of past changes in marine productivity. Against a backdrop of projected ocean acidification coralline algae show significant potential for reconstructing historic changes in ocean acidification-driven marine carbonate chemistry. Due to their global distribution, coralline algae are becoming a regularly used tool for understanding environmental and ecosystem change, particularly in areas where other proxies are not available or instrumental records are sparse.

Coralline algae as a globally significant pool of marine dimethylated sulfur

Marine algae are key sources of the biogenic sulfur compound dimethylsulphoniopropionate (DMSP), a vital component of the marine sulfur cycle. Autotrophic ecosystem engineers such as red coralline algae support highly diverse and biogeochemically active ecosystems and are known to be high DMSP producers, but their importance in the global marine sulfur cycle has not yet been appreciated. Using a global sampling approach, we show that red coralline algae are a globally significant pool of DMSP in the oceans, estimated to be ~110 × 1012 moles worldwide during the summer months. Latitude was a major driver of observed regional-scale variations, with peaks in polar and tropical climate regimes, reflecting the varied cellular functions for DMSP (e.g., as a cryoprotectant and antioxidant). A temperate coralline algal bed was investigated in more detail to also identify local-scale temporal variations. Here, water column DMSP was driven by water temperature, and to a lesser extent, cloud cover; two factors which are also vital in controlling coralline algal growth. This study demonstrates that coralline algae harbor a large pool of dimethylated sulfur, thereby playing a significant role in both the sulfur and carbon marine biogeochemical cycles. However, coralline algal habitats are severely threatened by projected climate change; a loss of this habitat may thus detrimentally impact oceanic sulfur and carbon biogeochemical cycling.