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Burdett, Heidi L. (2013) DMSP dynamics in marine coralline algal habitats. PhD thesis. http://theses.gla.ac.uk/4108/ Copyright and moral rights for this thesis are retained by the author A copy can be downloaded for personal non-commercial research or study This thesis cannot be reproduced or quoted extensively from without first obtaining permission in writing from the Author The content must not be changed in any way or sold commercially in any format or medium without the formal permission of the Author When referring to this work, full bibliographic details including the author, title, awarding institution and date of the thesis must be given Glasgow Theses Service http://theses.gla.ac.uk/ [email protected] DMSP Dynamics in Marine Coralline Algal Habitats Heidi L. Burdett MSc BSc (Hons) University of Plymouth Submitted in fulfilment of the requirements for the Degree of Doctor of Philosophy School of Geographical and Earth Sciences College of Science and Engineering University of Glasgow March 2013 © Heidi L. Burdett, 2013 ii Dedication In loving memory of my Grandads; you may not get to see this in person, but I hope it makes you proud nonetheless. John Hewitson Burdett 1917 – 2012 and Denis McCarthy 1923 - 1998 Heidi L. Burdett March 2013 iii Abstract Dimethylsulphoniopropionate (DMSP) is a dimethylated sulphur compound that appears to be produced by most marine algae and is a major component of the marine sulphur cycle. The majority of research to date has focused on the production of DMSP and its major breakdown product, the climatically important gas dimethylsulphide (DMS) (collectively DMS/P), by phytoplankton in the open ocean. A number of functions for intracellular DMSP (DMSPi) in phytoplankton have been identified and the cycling of DMS/P appears to be critical for ecosystem function. However, mechanisms for the production and release of DMS/P in the coastal ocean are poorly understood, despite the region’s economic and ecological importance. Coralline algal habitats (e.g. maerl beds, coral reefs, seagrass meadows, kelp forests) are distributed throughout the coastal oceans worldwide. Their three-dimensional structure supports high biodiversity and provides numerous services, generating considerable economic wealth. DMSPi in coralline algae is known to be high, thus coralline algal habitats may be critical components of the coastal sulphur cycle. This research aimed to improve our understanding of the production of DMS/P by coralline algal habitats by investigating (1) natural spatiotemporal variation and (2) the influence of environmental pressures. This was achieved through a number of laboratory and field-based studies, utilising modern and well-established techniques. The first objective of this research was to better understand the photosynthesis of red coralline algae (Chapter 3), as the algal precursor to DMSPi is methionine, a product of photosynthesis. The photosynthetic characteristics of coralline algae exhibited acclimation to changing light conditions (e.g. over a diurnal cycle or between natural and static lighting conditions). Further, for the species tested, coralline algae are often subjected to light-saturating natural conditions, therefore requiring efficient photo-protective mechanisms, which may include DMSPi regulation. On a global scale, DMSPi in coralline algae may decline with latitude, reinforcing the role of DMSPi as an antioxidant (Chapter 4). At smaller spatial Heidi L. Burdett March 2013 iv scales, DMS/P production, release and recycling mechanisms were apparent in a number of habitat types (Chapter 4). A strong seasonal trend in DMS/P was also observed at a Scottish maerl bed, driven by water temperature and cloud cover (Chapter 5). Annually averaged DMS and DMSP concentrations were 230% and 700% respectively higher than the open ocean, highlighting the potential importance of the coastal ocean in the marine sulphur cycle (Chapter 5). The influence of environmental pressures (decreased salinity, variable pH and grazing) on DMS/P production by coralline algal habitats was examined (Chapters 6 – 8). In agreement with the phytoplankton literature, a chronic, but not acute, reduction in salinity led to a significant decline in coralline algal DMSPi concentrations and a sinking of the surface epithelial cells but no apparent impact on photosynthesis (Chapter 6). In the naturally variable tropical reef environment, calcifying algae continually regulated DMSPi concentrations in response to the diurnal cycling of carbonate saturation state (Chapter 7), suggesting that DMSPi may be enhanced under low pH regimes to compensate for enhanced oxidant production. Under low pH conditions, cracks were observed between the surface epithelial cells of coralline algae, potentially allowing DMSPi to leak from the cells (Chapter 7). In the field, grazing by urchins appeared to facilitate the release of DMS/P from kelp in coralline algal habitats (Chapter 8). In the laboratory, DMSPi in coralline algae increased in response to chemical cues from grazers rather than direct grazing activity, as had been previously proposed. Prior to this research, little information was available on DMS/P concentrations in coralline algal habitats. The marine sulphur cycle may impact climate regulation and ecosystem function on a global scale. This research provides a comprehensive source of information on the importance of coralline algal habitats in the marine sulphur cycle by examining natural variability and potential changes in response to environmental perturbations. This work will form a baseline for continued research in this field, investigating, for example, the impact of multiple stressors on DMS/P production, release and recycling in coastal marine habitats. Heidi L. Burdett March 2013 v Table of contents Dedication .................................................................................. ii Abstract .................................................................................... iii List of figures .............................................................................. xii List of tables ............................................................................... xv Publications arising from this research ............................................. xvi International conference presentations ........................................... xviii Acknowledgements ...................................................................... xix Author’s declaration .................................................................... xxi Definitions and abbreviations ........................................................ xxii Chapter 1 Introduction ............................................................ 25 1.1 The oceanic sulphur cycle ................................................ 25 1.1.1 Dimethylsulphide .......................................................... 26 1.1.1.1 The CLAW hypothesis ..................................................... 26 1.1.2 Dimethylsulphoniopropionate............................................ 28 1.1.2.1 The production of DMSP .................................................. 29 1.1.2.2 The release of DMSP ...................................................... 30 1.1.2.3 The degradation of DMSP ................................................ 31 1.1.3 Cycling of dimethylated compounds in the ocean .................... 33 1.1.4 Dimethylated sulphur production in the coastal ocean .............. 35 1.2 Non-geniculate red coralline algae ..................................... 36 1.2.1 Distribution of coralline algal habitats ................................. 37 1.2.1.1 Maerl and rhodolith beds ................................................. 37 1.2.1.2 Coralligène ................................................................. 39 1.2.1.3 Kelp forests ................................................................ 39 1.2.1.4 Coral Reefs ................................................................. 40 1.2.1.5 Seagrass meadows ......................................................... 40 1.2.2 Taxonomy ................................................................... 41 1.2.3 Growth ...................................................................... 42 1.2.3.1 Morphology ................................................................. 42 1.2.3.2 Growth banding ............................................................ 43 1.2.4 Red algal photosynthesis ................................................. 45 1.2.4.1 Red algal chloroplasts .................................................... 47 1.2.4.2 Phycobiliprotein pigments ............................................... 47 1.2.5 Importance of coralline algal habitats ................................. 52 1.2.5.1 Ecosystem service provision ............................................. 52 1.2.5.2 Carbon sequestration and cycling ....................................... 53 1.2.5.3 Palaeoclimatic proxies ................................................... 53 1.2.6 Threats to coralline algal habitats ...................................... 54 1.2.6.1 Fishing ...................................................................... 54 1.2.6.2 Harvesting .................................................................. 54 1.2.6.3 Eutrophication ............................................................. 55 1.2.6.4 Climate change ............................................................ 55 1.3 Aims of this research ...................................................... 56 Heidi L. Burdett March 2013
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