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Benthic Primary Production and Carbon Turnover in Coastal Marine Environments Quantified Using Aquatic Eddy Correlation

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Benthic Primary Production and Carbon Turnover in Coastal Marine Environments Quantified Using Aquatic Eddy Correlation BENTHIC PRIMARY PRODUCTION AND CARBON TURNOVER IN COASTAL MARINE ENVIRONMENTS QUANTIFIED USING AQUATIC EDDY CORRELATION Karl M. Attard Ph.D. thesis September 2014 1 Nordic Centre for Earth Evolution 2 BENTHIC PRIMARY PRODUCTION AND CARBON TURNOVER IN COASTAL MARINE ENVIRONMENTS QUANTIFIED USING AQUATIC EDDY CORRELATION Karl M. Attard A dissertation submitted to the Faculty of Science at the University of Southern Denmark in partial fulfilment of the requirements for the degree of Doctor of Philosophy Department of Biology Nordic Centre for Earth Evolution September 2014 3 Nordic Centre for Earth Evolution 4 Data sheet Title: Benthic primary production and carbon turnover in coastal marine environments quantified using aquatic eddy correlation Author: Karl M. Attard Affiliation: Institute of Biology, Nordic Centre for Earth Evolution, University of Southern Denmark, and Greenland Climate Research Centre, Greenland Institute of Natural Resources Supervisors: Prof. Ronnie N. Glud Asst. Prof. Daniel F. McGinnis Prof. Søren Rysgaard Committee: Assoc. Prof. Erik Kristensen (University of Southern Denmark) Res. Prof. Peter Berg (University of Virginia) Prof. Per Hall (University of Gothenburg) Submitted: September 2014 Cite as: Attard, K. M. 2014. Benthic primary production and carbon turnover in coastal marine environments quantified using aquatic eddy correlation. PhD thesis. University of Southern Denmark and Greenland Climate Research Centre. 197pp. Keywords: Benthic oxygen exchange, benthic primary production, coastal carbon cycling, benthic metabolism, eddy correlation, Greenland, maerl beds, cold water corals, permeable sediments Front page: (Left) Deploying an eddy correlation system by ROV on a cold water coral reef in the NE Atlantic during the JC073 ‘Changing Oceans’ expedition. (Right) The remarkable pristine maerl beds in Loch Sween, Scotland (Photo by Rob Cook, Heriot-Watt University). 5 6 Contents Acknowledgements 09 Abstract 11 Dansk Resumé 13 List of manuscripts 15 1. INTRODUCTION 1.1. The oceanic carbon cycle 17 Benthic primary production 18 Light availability 19 Organic carbon degradation 20 Importance of benthic fauna 21 1.2. The benthic O2 exchange rate 24 The benthic O2 exchange rate as a measure of organic carbon remineralization 24 Estimating benthic primary production from O2 exchange measurements 26 Evaluating the benthic community light response 27 1.3. Estimating the benthic O2 exchange rate 30 The benthic boundary layer 30 Benthic O2 microprofile and chamber measurements 31 The aquatic O2 eddy correlation method 34 1.4. Summary of manuscripts 43 1.5. References 49 2. APPENDIX 57 3. PUBLICATIONS 3.1. Paper I 63 3.2. Paper II 113 3.3. Paper III 143 7 8 ACKNOWLEDGEMENTS I must begin by acknowledging my main advisor, Prof. Ronnie N. Glud, who back in September 2010 saw it fit to offer me a Ph.D. position within his research group. Looking back at the past four years, I couldn’t have hoped for a better set of experiences, both academic and personal, than this Ph.D. project has provided me with. I thank him for being an excellent mentor and for always going the extra mile, whether it was his flexibility in scheduling or in providing honest advice and guidance. I thank my co-adviser, Dr. Daniel F. McGinnis, for introducing me to the world of aquatic eddy correlation, for his valued patience and mentorship, continued encouragement, stimulating conversations, and for many memorable hours in the field. Furthermore I thank my second co-advisor, Prof. Søren Rysgaard, for supporting my research stays in Greenland. These were life-changing experiences for me, and I am proud and happy to have been part of his research group there. I would like to acknowledge the Faculty of Science at the University of Southern Denmark for providing an excellent platform from which to pursue my Ph.D. studies. I would like to express my deep gratitude to colleagues and friends, too long to list, within the Institute of Biology and in particular in the Nordic Centre for Earth Evolution (NordCEE). Special thanks go to the members of the ‘Glud Lab’, to Dr. Kasper Hancke and to my officemate Dr. Lorenzo Rovelli for many stimulating debates and for being great co-fieldworkers. I must express my gratitude to Anni Glud, Mette Andersen, and Lone Nørgaard Bruun, for their help with all matters administration related. A heartfelt ‘Qujanaq!’ to the staff and students at the Greenland Climate Research Centre for a very special 16 month research stay in Nuuk. In particular, thank you to Heidi Sørensen, Lorenz Meire, Dr. Martin Blicher, Dr. Thomas Juul-Pedersen, and Peter Schmidt Mikkelsen. I would like to thank the research groups at the Scottish Association for Marine Sciences (Dr. Henrik Stahl) and Heriot-Watt University (Prof. Murray Roberts) in Scotland, and the MPI-AWI research groups in Germany (Dr. Frank Wenzhöfer and Prof. Antje Boetius), who allowed me to join research expeditions they organized. Much of this work is in progress and therefore is not included in this thesis. Finally I am indebted to those closest to me: my family back home in Malta, who from a time way before starting my Ph.D. degree has been nothing but encouraging and supportive of my (often questionable) endeavours. I am especially indebted to my mother and father, Annette and Joe. This thesis is dedicated to them. And to Lisa, who has always been around to provide reassurance and perspective. Karl Attard Odense, September 2014 9 10 ABSTRACT The benthic environments on the continental shelves are hotspots for carbon turnover in the oceans, hosting a high biomass of heterotrophic microbes and fauna as well as benthic primary producers such as seagrasses, micro- and macro-algae, and corals that contribute substantially to ecosystem primary production. While the importance of quantifying the carbon turnover in shelf environments is clear, the global database remains limited. This is especially true for complex benthic habitats that are widespread on the continental shelf such as consolidated sands and gravels, rocky and uneven substrates, and for those dominated by large macroalgae and macrofauna. The difficulties in applying traditional benthic O2 exchange measurement techniques such as benthic microprofiling and benthic chamber incubations have left many shelf environments practically unstudied in the context of organic carbon turnover. Data is particularly scarce for the massive coastal regions of the Arctic that encompass around 25% of the global continental shelf area. Many of these regions are undergoing dramatic transformations due to climate change that are expected to affect coastal productivity. The primary aim of this thesis was to investigate the organic carbon turnover in complex, understudied benthic environments on the continental shelf using the aquatic O2 eddy correlation (EC) method. In contrast with the traditional measurement techniques, the EC method is not confined to soft sediments, and the measurements integrate a large area of the seabed (typically 10-100 m2) under the natural light and flow conditions. This thesis draws on three case studies. The first study presents a series of high-quality EC measurements from an intensive 13 month study that was carried out to estimate benthic primary production and carbon turnover in a Greenland fjord. The second study investigates the benthic O2 uptake rate of two cold-water coral communities in the North Atlantic using EC. The third study is a seasonal study investigating benthic primary production and carbon turnover in a pristine maerl bed and a nearby sandy habitat in Loch Sween, Scotland. These high-quality novel data document that hard and complex benthic surfaces mediate high carbon turnover rates. These habitats play a key role in the remineralization of organic matter, regeneration of nutrients, and benthic primary production of temperate and polar coastal waters. The EC method estimates the benthic O2 exchange rates over large areas of the seabed in environments where other techniques would likely fail. Altogether, these studies provide a number of exciting and timely avenues for conducting future research. 11 12 DANSK RESUMÉ De bentiske økosystemer på de kontinentale sokler er brændpunkter for karbon omsætning i havet. De opretholder/indeholder en høj biomasse bestående af heterotrofe mikrober, fauna lige såvel som bentisk primær producenter, så som ålegræs, mikro- og makro alger og koraller. Disse bidrager en betydelig del til hele økosystemets primær produktion. På trods af vigtigheden af at kunne kvantificere karbon omsætningen på de kontinentale sokler, er den globale database fortsat begrænset. Dette er især gældende for komplekse bentiske habitater bestående af konsolideret sand og grus, klippe og ujævne overflader som primært er domineret af makroalger og – fauna, da disse udgør en betragtelig andel af de kontinentale sokler. Problematikken i at benytte traditionelle metoder for måling af bentisk ilt udveksling, så som ilt mikroprofilering og iltkamre, har forårsaget at mange områder fortsat ikke er undersøgt i forbindelse med karbon omsætning. Især data/information fra den arktiske region, som udgør 25% af de globale kontinentale sokler, er manglende. Mange af økosystemerne i denne region gennemgår dramatiske forandringer grundet klima forandring, som forventes at påvirke den kystnære primær produktionen. Det primære mål med denne afhandling var at undersøge omsætningen at karbon i de komplekse og relative uudforsket bentiske systemer på de kontinentale sokler ved hjælp af EDDY CORRELATION
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