Dimethyl sulphide biogeochemistry within a coccolithophore bloom (DISCO): an overview

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Abstract

This paper presents an overview of dimethyl sulphide biogeochemistry within a coccolithophore bloom (DISCO), an integrated, multidisciplinary Lagrangian process study of the routes, rates and controls on the biogeochemical cycling of dimethyl sulphide (DMS) within a growing bloom of the coccolithophorid alga, Emiliania huxleyi. The Lagrangian study took place between 16 and 26 June 1999 in the northern North Sea. It was preceded by an 8-d survey of ∼52,000 km2 of the region to locate an E. huxleyi bloom suitable for study. Although not originally planned, the survey was carried out because heavy cloud cover precluded use of remote sensing to locate a suitable bloom. E. huxleyi blooms, typically common in the region during mid-summer, were unusually sparse in the study area. The bloom chosen for the process study was initially centred ∼58°56′N 02°52′E, and a 40-km2 patch of water was labelled for study with ∼30 g sulphur hexafluoride (SF6) on 16 June. The original patch was reinfused with further SF6 on 24 June. During the process study, the SF6-labelled patch moved in a south-easterly direction and the study ended when the patch subducted underneath less dense Norwegian coastal water.

The process study comprised analyses of the time-varying biological, optical and physical properties of the patch as well as studies of DMS, dimethylsulphonioproprionate (DMSP), dimethylsulphoxide, nutrients, halocarbons, methylamines, carbon monoxide, dissolved organic carbon, and total dissolved nitrogen. The role of viruses, bacteria, phytoplankton, microzooplankton, and mesozooplankton, together with the dynamics of primary, new and bacterial production, plankton respiration, microzooplankton grazing, and sedimentation, were studied in relation to the biogeochemical cycling of DMS. Although the coccolithophore bloom water exhibited high optical backscatter, the algal community present was highly heterogeneous. Flagellates other than E. huxleyi were found to dominate the phytoplankton. A budget of the DMSP pools suggested that E. huxleyi accounted for only 13% of the stocks of particulate DMSP, showing that in this “E. huxleyi bloom”, taxa other than E. huxleyi were important sources of DMSP. In this young bloom, particulate and dissolved DMSP and DMS concentrations averaged 1360, 155 and 60 μM m−2, respectively, in the surface mixed layer. Surface-water particulate DMSP concentrations increased during the study at a net rate of 13% d−1, as did concentrations of phytoplankton including E. huxleyi, confirming that the bloom was developing. Nutrient conditions were low in the mixed layer throughout the study, maintained by a strong pycnocline across which nitrate upflux was estimated to be ∼2 nM dm−3 d−1. Primary production was fuelled by regenerated nutrients, although nitrification rates in surface waters were found to be significant. Microzooplankton grazing accounted for 91% of the particulate DMSP degradation and was considered to be a major control on the DMSP concentration. Vigorous microzooplankton grazing together with rapid uptake of dissolved DMSP by bacteria suggest that microzooplankton were the main route for the production of dissolved DMSP. The bacterial community was dominated by one taxon, an α proteobacteria related to Roseobacter that satisfied its entire sulphur demand by metabolising dissolved DMSP. Bacteriogenic DMS production amounted to 2 nM d−1 and was considered the main route for DMS production. In vitro DMSPlyase activity was very high, but there was little evidence for high in situ activity. Over the study period, DMS flux to the atmosphere was estimated to be 7 μM m−2 d−1, equivalent to ∼1% of the DMSP sulphur produced in the surface mixed layer. A budget for DMS cycling in the upper mixed layer is presented based on the analytical and experimental measurements made in the DISCO study.

Introduction

Dimethyl sulphide (DMS: formula (CH3)2S) is the main natural source of atmospheric sulphur (Lovelock et al., 1972; Bonsang et al., 1980; Andreae, 1986). Originating primarily in seawater, DMS diffuses readily to the atmosphere where it is oxidised by hydroxyl and nitrate radicals to form a cocktail of sulphur dioxide, methanesulphonic acid and other acidic compounds within submicron aerosols (Andreae and Crutzen, 1997). This cocktail influences various climatically important processes (Bates et al., 1987; Ayers and Gras, 1991). Sulphate rich aerosols increase the backscatter of sunlight and form cloud condensation nuclei (CCN) that generate low stratiform clouds over the ocean. Both processes contribute to planetary cooling by increasing the Earth's albedo and hence influence our climate (Charlson et al., 1987; Charlson, 1993). The cocktail also influences the acidity of atmospheric water, which can fall as “acid rain” (Charlson and Wigley, 1994). Such processes can be globally significant (Wigley, 1994). DMS has been estimated to contribute ca. 60% of the natural emissions of sulphur to the atmosphere. Although anthropogenic sulphur emissions may be approximately three times higher than natural emissions on a global basis, they are restricted to industrialised regions and hence are largely localised to the Northern Hemisphere (Bates et al., 1992; Malin, 1996).

The major source of DMS in the oceanic mixed layer is dimethyl sulphoniopropionate (DMSP), a compound synthesised by certain marine algal groups for cellular osmoregulation (Kirst, 1996; Stefels, 2000). DMSP is found in high concentrations within prymnesiophyte and dinoflagellate algae, while other taxa, such as diatoms, generally have low cellular DMSP concentrations (Keller, 1989). Several mechanisms by which DMSP is converted to DMS are known but remain poorly understood. Most healthy cells appear to produce little DMS, but in unhealthy or damaged cells, DMSP can be converted to DMS. This conversion may be brought about by the enzyme, DMSPlyase, which has been found in high concentrations in some algae (Stefels and Dijkhuisen, 1996; Steinke and Kirst, 1996) and bacteria (de Souza and Yoch, 1995). Other factors that are known to influence DMS production include physical turbulence, osmotic shock, pathogen attack by virus and bacteria, and zooplankton grazing (Malin et al., 1994). Once produced, DMS may be photo-oxidised to dimethylsulphoxide (DMSO) at the sea surface (Brimblecombe and Shooter, 1986). DMSP and DMS also may be metabolised to other compounds by microbially mediated demethylation pathways (Kiene and Service, 1991; Kiene and Bates, 1990; van der Maarel et al., 1996). While a variety of pathways for DMSP to DMS conversion are now known to be mediated by pelagic foodwebs, the relative importance of these pathways, the controls and conversion efficiency of DMSP to DMS under natural conditions, is poorly understood.

One of the phytoplankton groups known to contain high DMSP cellular concentrations are members of the algal class Prymnesiophyceae (Green et al., 1990; Liss et al., 1994). A notable group of prymnesiophytes are the coccolithophores. An ecological characteristic of coccolithophores is their ability to form blooms with concentrations >106 cells l−1. The causes of such blooms are poorly understood (Head et al., 1998), but one suggestion is that coccolithophores out-compete other taxa when phosphate levels are low (Egge and Heimdal, 1994; Tyrrell and Taylor, 1996). Although we understand little about the mechanisms that allow coccolithophore blooms to develop, we know that such blooms form a regular pattern in the seasonal succession of phytoplankton in some temperate waters. Indeed, coccolithophore blooms are seasonally predictable in certain areas including the northern North Sea (Holligan et al., 1983). In the waters between southwest Norway and the Shetland Islands (approximately 60°N 02°E), the coccolithophore, Emiliania huxleyi, blooms annually with cell concentrations reaching 115×106 cells l–1 (Thomsen et al., 1994; Head et al., 1998). E. huxleyi is considered the most abundant coccolithophore in the ocean (Green and Leadbeater, 1994). Since E. huxleyi can contain high (but sometimes variable) cellular DMSP content (Matrai and Keller, 1994), the species may be a globally significant source of DMS (Holligan et al., 1993a).

The distinctive nature of E. huxleyi blooms, their widespread occurrence, and their importance to carbon and sulphur cycles mean that they are one of the most intensively studied oceanic plankton communities (Holligan et al., 1993a). Estimates of the flux of DMS to the atmosphere from coccolithophore blooms in temperate and sub-polar waters suggest that they form “hot spots” of DMSP/DMS production in the oceans (Holligan et al., 1993a; Malin et al., 1993; Matrai and Keller, 1993). Previous studies of open-ocean blooms of coccolithophores have surveyed concentrations of DMS and DMSP in relation to phytoplankton composition and estimated rates of DMS flux to the atmosphere in the North Atlantic (Turner et al., 1988; Holligan et al., 1993a; Malin et al., 1993) and Gulf of Maine (Matrai and Keller, 1994). More recently, utilising a Lagrangian experiment in a bloom dominated by E. huxleyi, Simó and Pedrós-Alió (1999) were able to quantify the bulk production and turnover rates of DMSP and DMS in surface waters. They demonstrated that controls on DMS cycling could vary on a daily basis and were driven by short-term variability in meteorological forcing factors. In light of the extensive knowledge gained from these previous oceanic programmes and the wide variety of detailed studies on DMSP and DMS production by E. huxleyi in laboratory cultures (e.g., Keller and Korjeff-Bellows, 1996; Matrai and Keller, 1994; Wolfe et al., 1997; Steinke et al., 1996) or mesocosms (e.g., Bratbak et al., 1995; Levasseur et al., 1996; Wilson et al., 1998), blooms of E. huxleyi provide a relevant and useful model on which to develop our understanding of DMS cycling.

The aim of DISCO was to quantify the pools and processes that influence the biogeochemical cycling of DMS in surface waters during the progression of a bloom of E. huxleyi. The main pools and processes studied are outlined conceptually in Fig. 1, and incorporate the following objectives, which were addressed on the cruise:

  • (a)

    characterisation of the plankton communities (algae, bacteria, virus, microzooplankton, mesozooplankton) associated with the developing bloom and determination of the role of individual components in the biogeochemical synthesis of DMS and related compounds;

  • (b)

    determination of the temporal changes in physical, optical, chemical, and biological parameters that affect the progression of the coccolithophore bloom;

  • (c)

    quantification of DMSPp, DMSPd, DMS, and DMSO and their production, consumption, and transformation processes during the bloom;

  • (d)

    generation of data for testing DMS biogeochemistry models and the models of microzooplankton trophodynamics in DMS generation within the bloom.

The approach adopted centred on a Lagrangian drift study of a coherent water patch, tagged by a deliberate release of the tracer sulphur hexafluoride (SF6). This volatile compound makes a good oceanographic tracer as it is inert, relatively simple to deploy and can be measured in near-real time using extremely sensitive analytical techniques (Upstill-Goddard et al., 1991). Sulphur hexafluoride has been deployed in previous experiments in lakes (Wanninkhof et al., 1985), rivers (Clark et al., 1994), coastal seas (Watson et al., 1991) and the open ocean (Ledwell et al (1993), Ledwell et al (1998)) in order to determine vertical and horizontal mixing rates. It also has been used successfully as a tracer of waters deliberately enriched with iron in the Pacific (Martin et al., 1994; Coale et al., 1996) and Antarctic Oceans (Boyd et al., 2000) and in passive Lagrangian biogeochemical studies on the Florida Shelf (Wanninkhof et al., 1997) and the North Atlantic (Law et al., 2001). Its usefulness as a tracer of surface water is limited only by loss across the air–sea interface, although a co-release of a suitable second tracer such as 3He (Watson et al., 1991) or non-volatile tracers (Nightingale et al., 2000a) allows this loss to be used to determine air–sea gas exchange rates. Drogue drifting buoys have been used previously in Lagrangian experiments (Savidge et al., 1992), although co-release of SF6 with surface drifters has shown that wind slippage (Nightingale et al., 2000a) and horizontal shear (Stanton et al., 1998) limit confidence in their ability to accurately track surface waters. The great advantage of SF6 as a deliberate tracer is the ability to quantify changes within the patch due to horizontal and vertical mixing rates (Law et al (1998), Law et al (2001)) and gas exchange across the air–sea interface (Nightingale et al., 2000b).

DISCO was a multidisciplinary study involving a wide range of specialist skills. It was carried out by 23 scientists from seven institutions. These were the Plymouth Marine Laboratory (PML), the Dunstaffnage Marine Laboratory (DML), the Scottish Association for Marine Science (SAMS), the Universities of the Highlands and Islands (UHI), the University of East Anglia (UEA), the Marine Biological Association (MBA) and the Defence Evaluation Research Agency (DERA, now QinetiQ).

Section snippets

Methods

The DISCO process study required a patch of water exhibiting elevated DMS dynamics, and so the research was planned around access to a bloom of E. huxleyi. Since studies of E. huxleyi blooms have generally been based on mature blooms characterised by high optical back scatter, we decided that we should work on a pre-bloom population characterised by lower back scatter. Our plan was to locate a well-developed bloom using satellite imaging, and then to work on the edge of the high backscatter

Results and discussion

The full suite of data derived from the DISCO experiment is held at the British Oceanographic Data Centre (BODC) and can be accessed via http://www.bodc.ac.uk. A full report of the DISCO cruise is given in Burkill (2000).

Main discoveries of DISCO

DISCO has revealed new understanding on the dynamics of DMS biogeochemistry and interactions between microbial communities and DMS production. Although these are described fully elsewhere in this Special Issue, a summary of the key findings of the DISCO study are given below:

  • 1.

    Spatial and temporal variability and algal composition of E. huxleyi blooms. The survey of 52,000 km2 of the northern North Sea revealed few E. huxleyi blooms in early June 1999. It seems that these blooms were late in 1999,

Acknowledgements

It is pleasure to acknowledge the tremendous support that allowed DISCO to take place. This included NERC funding of PMLs Core Strategic Research for Dynamics of Marine Ecosystems (DYME), Oceans, Climate and Consequences for the Coastal Zone (OC4Z) and Microbially Driven Biogeochemical Processes (MDB) as well as Postdoctoral and Advanced Research Fellowships to A. Hatton, C. Robinson and M. Zubkov (GT5/97/6/MAS, GT5/96/8/MS and GT5/98/16/MSTB, respectively). Part of the research was supported

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