Role of dimethyl sulphide (DMS) in pelagic tritrophic interactions

Lead Research Organisation: University of Essex
Department Name: Biological Sciences

Abstract

The oceans contain only about 1.5% of terrestrial biomass. However, they provide a similar amount of total annual production to that on land and the turnover time for organic matter is 1000-times faster in marine in comparison to terrestrial ecosystems. This highlights that grazing by zooplankton is disproportionally important and competition among grazers is high. It is not surprising that phytoplankton have evolved mechanisms to protect themselves from grazers. These include morphological defences such as grazing-resistant shells, for example in 'armoured' dinoflagellates, and chemical defences such as sophisticated chemical deterrence that influence the selectivity of grazers. Over the years we have accumulated a good understanding of the role of chemical defences in the bitrophic interactions between predators and their prey. However, it is also well known that land plants use another cunning defence strategy that involves the production of volatile signalling compounds (so called infochemicals) that attract the enemy of their predators. This in turn reduces the number of herbivores and releases the plants from excessive grazing pressure. Surprisingly, such infochemical-mediated tritrophic interactions have not been documented for oceanic plankton and our proposed research will rectify this shortcoming. We will focus our activities on one particular marine volatile: dimethyl sulphide (DMS). This compound is probably the best-studied of all marine trace gases, because much interest in DMS research concerns its role in regulating climate. We are starting to appreciate that DMS also has ecological importance and find that many organisms can use plumes of DMS as directional cue for their orientation. For example, some sea birds use DMS to locate areas of high food density. Recently, we also found that zooplankton copepods react to DMS gradients. Copepods are dominant consumers of microzooplankton protists (unicellular ciliates and flagellates) that are important grazers of many small phytoplankton species. In biogeochemical terms ciliates account for, on average, 30 % of the carbon consumed by copepods, representing approximately 5 % of total oceanic primary production and 100 fold the annual fisheries catch (~ 100 Mt yr-1 live weight) in carbon terms. However, these estimates may be considerably higher if other components of the microzooplankton, in particular dinoflagellates, are included. Interestingly, grazing by microzooplankton can result in a dramatic increase of DMS production and this is dependent on the ability of the phytoplankton to make this gas. Hence, phytoplankton may actively influence the 'smelliness' of their predators and this likely makes their enemies more susceptible to copepod attack. It is then not surprising that many of the DMS-producing phytoplankton species are competing successfully and can produce algal blooms that are large enough to be seen from space (for example the coccolithophore Emiliania huxleyi) or can be harmful to other organisms (for example toxic dinoflagellates). Our project will use laboratory experiments where we will quantify grazing of microzooplankton and copepods in relationship to the ability of phytoplankton to make DMS. These data will enable a first assessment of grazing-induced production of DMS in a tritrophic framework. We will also conduct field experiments with freshly collected plankton to verify our laboratory results with data from coccolithophore-dominated waters off Plymouth and in the North-East Atlantic. Our data will inform modelling efforts that aim to predict the effect of differential production of DMS on the susceptibility of microzooplankton to copepod grazing and the fecundity of copepods. This part of our project will be realised through a tied PhD studentship.

Publications

10 25 50
 
Title Michael Steinke 'Research Discoveries' - Essex 
Description Presentation of research and teaching interests 
Type Of Art Film/Video/Animation 
Year Produced 2012 
Impact Increased visibility of funded research 
URL http://vimeo.com/channels/marinebiology/53335556
 
Description Mathematical simulation of the interactions between three trophic levels of plankton: phytoplankton, grazing microzooplankton and predatory mesozooplankton suggest that the inclusion of a grazing-induced dimethyl sulfide (DMS) production term has a stabilizing effect on the system dynamics. This feedback between trophic levels can potentially lead to the formation of a phytoplankton bloom.
Exploitation Route Our findings suggest that marine trace gases may have important biological roles beyond their function as climate-active compounds. The model provides a suitable framework for further study into the possible role of DMS in the ecology of marine food webs beyond its recognised role as a climate-cooling gas.
Sectors Environment

 
Description Data from this project were used to inform the general public on issues relating to the role of gases in mediating climate change.
First Year Of Impact 2010
Sector Environment
Impact Types Cultural

 
Description EnvEast DTP (Volabolome)
Amount £50,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2015 
End 09/2018
 
Description EnvEast DTP (isoprene)
Amount £50,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 10/2014 
End 09/2017
 
Description N/A
Amount £8,454 (GBP)
Organisation BAE Systems 
Department BAE Systems Submarine Solutions
Sector Private
Country United Kingdom
Start 08/2015 
End 10/2015
 
Title Protocols for the quantification of dimethyl sulfide (DMS) and other volatile organic compounds in aquatic environments 
Description Aquatic environments produce a range of volatile organic compounds (VOCs) that can transfer into the atmosphere and affect climate. Much of our understanding on the biogeochemistry of volatiles in seawater stems from research on the biogenic trace gas dimethyl sulfide (DMS). Here, we describe four protocols for the quantification of DMS and other VOCs in aqueous samples that utilise direct injection or cryogenic enrichment techniques before separation and quantification using gas chromatography with flame photometric detection (GC-FPD). With few adjustments, the protocols can be customised to quantify a range of other gases including hydrocarbons such as isoprene and ethene, or halocarbons such as methyl chloride or bromoform. The limit of quantification for DMS is 1.5 pmol and the protocols range in sensitivities for DMS from 0.2 to 20 µM (direct injection of 200 µL headspace), 50 to 250 nM (headspace purging of 1.92 mL gaseous phase), 0.5 to 350 nM (in-vial purging of 3 mL aqueous phase), and the sub-nanomolar range for in-tube purging of sample volumes up to 200 mL. Two additional adaptations of the protocol include quantification of the biological DMS-precursor dimethylsulfoniopropionate (DMSP) and the DMS-oxidation product dimethyl sulfoxide (DMSO). 
Type Of Material Technology assay or reagent 
Year Produced 2016 
Provided To Others? Yes  
Impact Harmonised quantification of aquatic trace gases. 
 
Description DMS-grazer interactions 
Organisation Interuniversity Institute for Marine Science at Eilat
Country Israel 
Sector Academic/University 
PI Contribution Access to analytical equipment. Quantification of DMSP in provided samples.
Collaborator Contribution Provision of sample material from the Red Sea and a CO2 vent site in the Mediterranean.
Impact Two collaborative publications.
Start Year 2012
 
Description Freshwater Trace Gases 
Organisation UK Centre for Ecology & Hydrology
Country United Kingdom 
Sector Public 
PI Contribution Collaborative sampling of lakes in the Lake District and quantification of isoprene and DMS.
Collaborator Contribution Purchase of thermal desoprtion tubes, access to research vessel and sampling
Impact Collaborative drafting of research proposal
Start Year 2017
 
Description Grazing-induced production of DMS can stabilize food-web dynamics and promote the formation of phytoplankton blooms in a multitrophic plankton model 
Organisation University of Leicester
Country United Kingdom 
Sector Academic/University 
PI Contribution New collaborations with Andrew Morozov (Uni Leicester) and Jon Pitchford (Uni York) resulted in this publication
Start Year 2012
 
Description Microbial DMS cycling 
Organisation Friedrich Schiller University Jena (FSU)
Country Germany 
Sector Academic/University 
PI Contribution Hosting PhD student. Collaborative experiments using our analytical equipment.
Collaborator Contribution Providing skills in compound synthesis and access PhD student.
Impact Manuscript in preparation
Start Year 2013
 
Description Signalling in microbial biofilms 
Organisation BAE Systems
Department BAE Systems Submarine Solutions
Country United Kingdom 
Sector Private 
PI Contribution Literature Review: Role of biogenic volatile organic compounds (BVOCs) in the chemical communication of marine biofilms
Collaborator Contribution Financial Support
Impact Literature Review
Start Year 2015
 
Description How algae make the climate 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact Presentations sparked questions and discussion.

Local pupils showed interest in studying for a BSc degree at the University of Essex.
Year(s) Of Engagement Activity 2014
 
Description SET for Britain 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? Yes
Geographic Reach National
Primary Audience Policymakers/politicians
Results and Impact As part of the SET for Britain initiative, research officer Dr Mark Breckels and PhD student Nicola Lewis presented their science to a range of politicians and a panel of expert judges at the House of Commons, March 2012.
Year(s) Of Engagement Activity 2012
 
Description Visit Days 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Schools
Results and Impact A seminar and workshop on 'The Smell of the Sea'
Year(s) Of Engagement Activity 2013,2014,2015,2016