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Coastal Microbial Respiration in a Climate Change Perspective

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Coastal Microbial Respiration in a Climate Change Perspective Coastal microbial respiration in a climate change perspective Anna Nydahl Department of Ecology and Environmental Science Umeå 2012 Copyright © Anna Nydahl ISBN: 978-91-7459-517-8 Cover photo: Norrbyn archipelago, Anna Nydahl Electronic version available at: http://umu.diva-portal.org/ Printed by: KBC Service center Umeå, Sweden 2012 To my family List of papers This thesis is based on the following papers, which will be referred to in the text by their roman numerals I. Nydahl, A., Tengberg, A., Lundberg, E., Båmstedt, U., Wikner, J. Precise microbial respiration rate in coastal waters by a continuous multi-sample sensor dish reader. Manuscript II. Nydahl, A., Panigrahi, S., Wikner, J. Increased microbial activity in a warmer and wetter climate enhance the risk of coastal hypoxia. In revision FEMS Microbiology Ecology III. Wikner, J., Panigrahi, S., Nydahl, A., Lundberg, E., Båmstedt, U., Tengberg, A. Precise continuous measurements of pelagic respiration in coastal waters with an Optode sensor. Conditionally accepted: Limnology and Oceanography Methods IV. Panigrahi, S., Nydahl A., Wikner, J. Strong seasonal effect on plankton respiration by moderate experimental warming in a temperate estuarine plankton community. Manuscript Contributions Paper/ I II III IV Contribution Original idea AN, JW AN, JW, SP JW, AN JW, SP Study design AN, JW AN, JW, SP AN, JW, SP JW, SP and methods Data AN AN, SP SP, JW AN, SP collection Data analysis AN AN, SP SP, JW SP,AN,JW Contributions AN, JW, EL, AN, SP, JW JW, AN, AT, SP, AN, JW for UB, AT SP, EL, UB interpretation of the result and manuscript preparation Responsible AN AN JW SP for the manuscript preparation AN: Anna Nydahl, SP: Satya Panigrahi, JW: Johan Wikner, EL: Erik Lundberg, UB: Ulf Båmstedt, AT: Anders Tengberg i ii Table of Contents List of papers Contributions Table of Contents Abstract Introduction 1 Expanding hypoxia in the Sea 1 Future climate projections 1 The marine microbial food web 2 Marine respiration 3 Respiration measurements 4 Objectives of this thesis 5 Major findings and Discussions 5 Climate effects on respiration (paper II and IV) 5 Methods for respiration measurements (paper I and III) 8 Conclusions 10 Acknowledgements 10 References 11 Sammanfattning (Swedish summary) 16 Tack! 17 iii Abstract In a climate change perspective increased precipitation and temperature are expected which should influence the coastal microbial food web. Precipitation will have a strong impact on river flow and thereby increase the carbon input to the coastal zone as well as lowering the marine salinity by dilution with freshwater. Simultaneously temperature may increase by 2-5 °C, potentially influencing e.g. metabolic processes. Consequences of this have been evaluated in this thesis with focus on microbial respiration in paper II and IV. A temperature increase of 3 °C will have a marked effect on microbial respiration rates in the coastal zone. The effect of temperature on microbial respiration showed a median Q10 value of 25 with markedly higher values during winter conditions (around 0°C). These Q10 values are several-fold higher than found in oceanic environments. The conclusion was in accordance with a consistent temperature limitation of microbial respiration during an annual field study, however, shifting to DOC limitation at the elevated temperature. Neither bacterial production nor phytoplankton production showed a consistent temperature effect, suggesting that the biomass production at the base of the food web is less sensitive to a temperature increase. Results from both a field study and a fully factorial microcosm experiment supported the conclusion. Our results suggested that areas dealing with hypoxia today will most likely expand in the future, due to increased respiration caused by higher temperatures and larger riverine output of dissolved organic carbon. Pelagic respiration measurements in the sea are relatively scarce in the literature, mainly due to the lack of sufficiently good and user friendly techniques. New methods such as the dynamic luminescence quenching technique for oxygen concentration have been developed. This makes it possible to obtain continuous measurements of oxygen in an enclosed vial. Two different commercially available systems based on the dynamic luminescence quenching technique were evaluated from the aspect of precision, accuracy and detection limit when applied to respiration measurements in natural pelagic samples. The Optode setup in paper III showed a practical detection limit of 0.30 mmol m-3 d-1, which can be applied to measure respiration in productive coastal waters (used in paper IV). This included development of a stopper where the sensor was attached, stringent temperature control, proper stirring and compensation for an observed system drift. For controlled laboratory experiments with organisms smaller than 1 µm the Sensor Dish Reader (paper I) has sufficient detection limit of (4.8 mmol m-3 d-1). This required a stringent temperature control and manual temperature correction. The Sensor Dish Reader gives the opportunity to perform multiple treatments at low cost (used in paper II), but the precision is too low for field studies due to the between ampule variation. iv Introduction Expanding hypoxia in the Sea Dissolved oxygen levels in coastal waters have changed drastically over the last decades (Diaz and Rosenberg 2008). Literature shows that the number of coastal sites where hypoxia has been reported have increased with a rate of 5,4 % year-1 (Vaquer-Sunyer and Duarte 2008). Hypoxia in the coastal zones of the Baltic Sea has increased during the past 50 years and 20% of all known hypoxic sites around the world is located in the Baltic Sea (Conley et al. 2011). Local, regional and global changes in dissolved oxygen levels will have fundamental effects on ecosystems and have been more intensively studied during recent years (Körtzinger et al. 2004, Diaz and Rosenberg 2008, Riser and Johnson 2008, Keeling et al. 2010). Hypoxia i.e. oxygen concentrations under 2 mg ml-1 will have impact and kill bottom living organisms (Vaquer-Sunyer and Duarte 2008) and the consequences of hypoxia on nutrient biogeochemical cycles are substantial (Conley et al. 2002). The large-scale hypoxia is an inherent property of the Baltic Sea caused by geographically and climatically determined insufficiency of oxygen supply to the deep water layers (Savchuk 2010). To understand occurrence of hypoxic waters respiration plays a fundamental part. Respiration is one of the most important processes in the biosphere, from the level of individual organisms to regulation of CO2 an O2 levels in the atmosphere. Further, the balance between auto- and heterotrophic processes may be measured by light and dark changes in oxygen, It is of importance to study the downward transport of biomass through sedimentation, and thereby the role of the sea as a global sink or source for CO2 (g). (Karl et al. 2003, Stramma et al. 2008, Reid et al. 2009). The development of hypoxia as well as emissions of CO2 is thought to be promoted by future climate driven increase in temperature and discharge of freshwater (Conley et al. 2002, Zillén et al. 2008). Future climate projections Climate change projections suggest some changes in ocean physics and chemistry such as higher sea surface temperature and CO2 concentration, lower pH and enhanced upper ocean stratification (Solomon et al. 2007). Furthermore, precipitation may increase by approximately 20 % by the end of this century, leading to a larger riverine discharge to the sea, potentially resulting in higher inputs of riverine dissolved organic matter (rDOM) and lower salinity in the coastal zone (Meier 2006, Raymond and Saiers 2010). In addition, a temperature increase of approximately 2-5 ˚C is projected for northern Scandinavia. Microbial activity will likely be influenced by these climate related land-sea drivers individually or in concert. This change may in turn have a profound impact on food-web efficiency, carbon flow and nutrient recycling in marine surface waters (Wikner and Andersson 2012). These potential changes motivate the study of the effects of the major environmental drivers for microbial growth and respiration. 1 The marine microbial food web Life in the oceans is dominated by microbes (e.g. < 0.1 mm in size), comprising viruses, bacteria, protozoa and some phytoplankton. In fact microorganisms are thought to account for 90 % of the respiration in the water column (Robinson and Williams 2005). These small, singled-celled organisms constitute the base of the marine food web and catalyze the transformation of energy and matter in the sea. The role that the microbial community plays in the global marine carbon cycle was recognized in the end of the 1970-ies, partly as a result of a large share of marine respiration occurring in the microbial size fraction (Pomeroy 1974, Williams 1981, Azam et al. 1983). In the microbial food web heterotrophic bacteria use dissolved organic carbon and nutrients, primary Nitrogen (N) and Phosphorous (P) as their energy source. The carbon can either be derived autochthonusly from phytoplankton (or other planktonic organism groups) (Azam et al. 1983) or from allochtonous sources such as riverine input (Sandberg et al. 2004, Findlay et al. 1991).The bacteria are grazed on by heterotrophic flagellates and ciliates and they are in turn eaten by zooplankton, creating a link between bacteria and zooplankton (Fig. 1). The largest fraction of the carbon taken up by bacteria is respired to CO2 during consumption of oxygen, but the production of bacterial biomass is also an important process to make dissolved carbon available to the food web. (Kirchman 2000). Fig 1. Illustration of the aquatic food web and carbon transfer. Illustration by Kristina Viklund. 2 Marine respiration As mentioned above microorganisms are responsible for the major part (90%) of respiration in the water column and respiration is a fundamental part of biospheric metabolism. In a physiological perspective, respiration encompasses electron flow through membrane-associated transport systems from donors to acceptors, creating a proton gradient.
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