How does rising atmospheric CO2 affect marine organisms?

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Dimethylsulfide -- Summary
Dimethylsulfide or DMS is an organosulfur compound with the formula (CH3)2S. It is the most abundant biologically-produced sulfur compound to be found in the atmosphere, being emitted to the air primarily by marine phytoplankton. Perhaps its greatest claim to fame is that several years ago Charlson et al. (1987) discussed the plausibility of a multi-stage negative feedback process, whereby warming-induced increases in the emission of DMS from the world's oceans tend to counteract the effects of the initial impetus for warming. The basic tenant of their hypothesis was that the global radiation balance is significantly influenced by the albedo of marine stratus clouds (the greater the cloud albedo, the less the input of solar radiation to the Earth's surface). The albedo of these clouds, in turn, is known to be a function of cloud droplet concentration (the more and smaller the cloud droplets, the greater the cloud albedo and the reflection of solar radiation), which is dependent upon the availability of cloud condensation nuclei on which the droplets form (the more cloud condensation nuclei, the more and smaller the cloud droplets). And in completing the negative feedback loop, Charlson et al. noted that the cloud condensation nuclei concentration often depends upon the flux of biologically-produced DMS from the world's oceans (the higher the sea surface temperature, the greater the sea-to-air flux of DMS).

Since the publication of Charlson et al.'s initial hypothesis, much empirical evidence has been gathered in support of its several tenants. The review of Ayers and Gillett (2000), for example, concluded that "major links in the feedback chain proposed by Charlson et al. (1987) have a sound physical basis," and that there is "compelling observational evidence to suggest that DMS and its atmospheric products participate significantly in processes of climate regulation and reactive atmospheric chemistry in the remote marine boundary layer of the Southern Hemisphere."

In another study, Simo and Pedros-Alio (1999) used satellite imagery and in situ experiments to study the production of DMS by enzymatic cleavage of dimethylsulphoniopropionate in the North Atlantic Ocean about 400 km south of Iceland, finding that the depth of the surface mixing-layer has a substantial influence on DMS yield in the short term, as do seasonal variations in vertical mixing in the longer term, which observations led them to conclude that "climate-controlled mixing controls DMS production over vast regions of the ocean."

Amplifying the significance of this finding, Hopke et al. (1999) analyzed weekly concentrations of 24 different airborne particulates measured at the northernmost manned site in the world - Alert, Northwest Territories, Canada - from 1980 to 1991. One of their more interesting discoveries was the finding that concentrations of biogenic sulfur, including sulfate and methane sulfonate, were low in winter but high in summer, and that the year-to-year variability in the strength of the biogenic sulfur signal was strongly correlated with the mean temperature of the Northern Hemisphere. "This result," according to the authors, "suggests that as the temperature rises, there is increased biogenic production of the reduced sulfur precursor compounds that are oxidized in the atmosphere to sulfate and methane sulfonate and could be evidence of a negative feedback mechanism in the global climate system."

But just how strong is the negative feedback phenomenon proposed by Charlson et al.? Is it powerful enough to counter the threat of greenhouse gas-induced global warming? According to the findings of Sciare et al. (2000), it may well be able to do just that, for in examining ten years of DMS data from Amsterdam Island in the southern Indian Ocean, these researchers found that a sea surface temperature increase of only 1°C was sufficient to increase the atmospheric DMS concentration by as much as 50%. This finding suggests that the degree of warming typically predicted to accompany a doubling of the air's CO2 content would increase the atmosphere's DMS concentration by a factor of three or more, providing what they call a "very important" negative feedback that could potentially offset the original impetus for warming.

More directly supportive of Charlson et al.'s hypothesis was the study of Kouvarakis and Mihalopoulos (2002), who measured seasonal variations of gaseous DMS and its oxidation products -- non-sea-salt sulfate (nss-SO42-) and methanesulfonic acid (MSA) -- at a remote coastal location in the Eastern Mediterranean Sea from May 1997 through October 1999, as well as the diurnal variation of DMS during two intensive measurement campaigns conducted in September 1997. In the seasonal investigation, measured DMS concentrations tracked sea surface temperature (SST) almost perfectly, going from a low of 0.87 nmol m-3 in the winter to a high of 3.74 nmol m-3 in the summer. Such was also the case in the diurnal studies: DMS concentrations were lowest when it was coldest (just before sunrise), rose rapidly as it warmed thereafter to about 1100, after which they dipped slightly and then experienced a further rise to the time of maximum temperature at 2000, whereupon a decline in both temperature and DMS concentration set in that continued until just before sunrise. Consequently, because concentrations of DMS and its oxidation products (MSA and nss-SO42-) rise dramatically in response to both diurnal and seasonal increases in SST, there is every reason to believe that the same negative feedback phenomenon would operate in the case of the long-term warming that could arise from increasing greenhouse gas concentrations, and that it could substantially mute the climatic impacts of those gases.

Also of note in this regard, Baboukas et al. (2002) reported the results of nine years of measurements of methanesulfonate (MS-), an exclusive oxidation product of DMS, in rainwater at Amsterdam Island. Their data, too, revealed "a well distinguished seasonal variation with higher values in summer, in line with the seasonal variation of its gaseous precursor (DMS)," which, in their words, "further confirms the findings of Sciare et al. (2000)." In addition, the MS- anomalies in the rainwater were found to be closely related to SST anomalies; and Baboukas et al. say that this observation provides even more support for "the existence of a positive ocean-atmosphere feedback on the biogenic sulfur cycle above the Austral Ocean," which water body they describe as "one of the most important DMS sources of the world."

In another study of the phenomenon, Toole and Siegel (2004) note that it has been shown to operate as described above in the 15% of the world's oceans "consisting primarily of high latitude, continental shelf, and equatorial upwelling regions," where DMS may be accurately predicted as a function of the ratio of the amount of surface chlorophyll derived from satellite observations to the depth of the climatological mixed layer, which they refer to as the "bloom-forced regime." For the other 85% of the world's marine waters, they demonstrate that modeled surface DMS concentrations are independent of chlorophyll and are a function of the mixed layer depth alone, which they call the "stress-forced regime." So how does the warming-induced DMS negative feedback cycle operate in these waters?

For oligotrophic regimes, Toole and Siegel found that "DMS biological production rates are negatively or insignificantly correlated with phytoplankton and bacterial indices for abundance and productivity while more than 82% of the variability is explained by UVR(325) [ultraviolet radiation at 325 nm]." This relationship, in their words, is "consistent with recent laboratory results (e.g., Sunda et al., 2002)," who demonstrated that intracellular DMS concentration and its biological precursors (particulate and dissolved dimethylsulfoniopropionate) "dramatically increase under conditions of acute oxidative stress such as exposure to high levels of UVR," which "are a function of mixed layer depth."

These results -- which Toole and Siegel confirmed via an analysis of the Dacey et al. (1998) 1992-1994 organic sulfur time-series that was sampled in concert with the U.S. JGOFS Bermuda Atlantic Time-Series Study (Steinberg et al., 2001) -- suggest, in their words, "the potential of a global change-DMS-climate feedback." Specifically, they say that "UVR doses will increase as a result of observed decreases in stratospheric ozone and the shoaling of ocean mixed layers as a result of global warming (e.g., Boyd and Doney, 2002)," and that "in response, open-ocean phytoplankton communities should increase their DMS production and ventilation to the atmosphere, increasing cloud condensing nuclei, and potentially playing out a coupled global change-DMS-climate feedback."

This second DMS-induced negative-feedback cycle, which operates over 85% of the world's marine waters and complements the first DMS-induced negative-feedback cycle, which operates over the other 15%, is but another manifestation of the incredible capacity of Earth's biosphere to regulate its affairs in such a way as to maintain climatic conditions over the vast majority of the planet's surface within bounds conducive to the continued existence of life, in all its variety and richness. In addition, it has been suggested that a DMS-induced negative climate feedback phenomenon also operates over the terrestrial surface of the globe, where the volatilization of reduced sulfur gases from soils may be just as important as marine DMS emissions in enhancing cloud albedo (Idso, 1990). On the basis of experiments that showed soil DMS emissions to be positively correlated with soil organic matter content, for example, and noting that additions of organic matter to a soil tend to increase the amount of sulfur gases emitted therefrom, Idso (1990) hypothesized that because atmospheric CO2 is an effective aerial fertilizer, augmenting its atmospheric concentration and thereby increasing vegetative inputs of organic matter to Earth's soils should also produce an impetus for cooling, even in the absence of surface warming.

About the same time that Charlson et al. (1987) developed their hypothesis, Martin and Fitzwater (1988) and Martin et al. (1988) developed what has come to be known as the Iron Hypothesis (Martin, 1990), which posits that iron-rich dust swept up from exposed continental shelves during glacial maxima by the greatly enhanced winds of those periods fertilized the world's oceans to the point where their phytoplanktonic productivity rose so high that it drew the air's CO2 concentration down from typical interglacial values (280 ppm) to the much lower values characteristic of glacials (180 ppm). Shortly thereafter, the IronEx studies of Martin et al. (1994) and Coale et al. (1996) confirmed the fundamental premise of this hypothesis: after fertilizing patches of seawater in high-nitrate low-chlorophyll (HNLC) regions of the equatorial Pacific with bio-available iron, they found, in the words of Turner et al. (2004), that this procedure "benefited all the major groups of the algal community, including those which produce significant amounts of intracellular dimethylsulfoniopropionate (DMSPp)," the precursor of DMS, which also saw its concentration rise as a result of the experimental iron treatment (Turner et al., 1996).

In the aftermath of these latter demonstrations, large-scale ocean fertilization with bio-available iron became a doubly-viable potential strategy for the mitigation of global warming. Not only could its natural or anthropogenic implementation result in the removal of CO2 from the atmosphere at an augmented rate in response to heightened phytoplanktonic productivity, it could also lead to the reflection of more incoming solar radiation back to space as a result of greater DMSPp production (and all that follows it) in response to the same basic phenomenon, i.e., enhanced phytoplanktonic productivity. However, the studies supporting the second of the two pathways to augmented planetary cooling had been conducted in the equatorial Pacific; and it was not known if the findings of those studies could be extrapolated to other HNLC ecosystems, such as those of the Southern Ocean. Thus, Turner et al. (2004) conducted two additional iron-release experiments: the Southern Ocean Iron Release Experiment (SOIREE), which took place south of Australia in February of 1999, and EisenEx, which took place south of Africa in November of 2000.

In both of these studies, Turner et al. say "the experimental patches (~50 km²) were created by pumping dissolved iron sulfate into the mixed layer, as the ships sailed on a spiral track out from, and relative to, a buoy." The initial levels of dissolved iron in these patches rapidly decreased, and additional injections were made at their centers during the course of the experiments. As to what occurred thereafter, the scientists report that "in SOIRRE, the major increase in DMS occurred several days after the maximum in DMSPp and by the end of the study DMS levels at 30 m depth were 6.5-fold higher in treated waters than outside," while "in EisenEx, highest observed DMS concentrations [occurred] on days 5 and 12, about 2-fold higher than initial levels." What is more, they say that a series of ocean color images from SeaWiFS revealed a feature with enhanced chlorophyll levels close to the SOIREE site (Boyd et al., 2000), and that "Abraham et al. (2000) argue that this was our patch which had spread to cover 1100 km²."

How significant are these findings? They are truly huge; for Turner et al. report that "recent coupled ocean-atmosphere modeling studies show that even a relatively small change in marine DMS emissions may have a significant impact on global temperatures: ± ~1°C for a halving or doubling of DMS emissions, respectively." In addition, they note that "evidence from ice cores suggests that changes in DMS emission at least as large as this have occurred in the past (Legrand et al., 1991) and so it is easily conceivable that significant changes in DMS emissions would occur in future climate scenarios."

Operating in tandem, it is clear that the marine-productivity-mediated increase in reflected solar radiation to space (via the Charlson et al. mechanism) and the more direct marine-productivity-mediated increase in removal rate of CO2 from the atmosphere possess the capacity (whether naturally or anthropogenically implemented in response to an increase in temperature or iron flux to the world's oceans) to substantially counter whatever warming of the planet might possibly occur in response to future anthropogenic CO2 emissions. Hence, there is reason to be guardedly optimistic about the health of the biosphere, based largely on the ability of marine phytoplankton to safeguard their own future by moderating the nature of their physical environment (in this case, ocean surface temperature).

In another study of the Charlson et al. (1987) hypothesis, Broadbent and Jones (2004) explored the possibility that coral reefs may also be major participants in the bio-stabilization of Earth's climate. Working in waters off the coast of Australia, while noting that "Jones et al. (1994) and Broadbent et al. (2002) reported that corals in the Great Barrier Reef (GBR) contain significant amounts of DMSP in their zooxanthellae, suggesting that coral reefs are potentially significant sources of DMS to the water column of reef areas and that coral reefs themselves may be significant sources of atmospheric DMS to the marine boundary layer (Jones and Trevena, 2005)," the two researchers measured concentrations of DMS and DMSP within mucus ropes, coral mucus, surface films and sediment pore waters collected from Kelso Reef, One Tree Reef and Nelly Bay Reef in Australia's GBR.

As a result of their efforts, Broadbent and Jones found that "the concentrations of DMS and DMSP measured in mucus ropes and surface-water samples at One Tree Reef and Kelso Reef are the highest yet reported in the marine environment," exceeding those measured in "highly productive polar waters (Fogelqvist, 1991; Trevena et al., 2000, 2003), and sea ice algal communities (Kirst et al., 1991; Levasseur et al., 1994; Trevena et al., 2003)." More specifically, they report that "concentrations of DMS ranged from 61 to 18,665 nM and for DMSP, from 1,978 to 54,381 nM, representing concentration factors (CF = concentration in the mucus ropes divided by the concentration in seawater from 0.5 m depth) ranging from 59 to 12,342 for DMS and 190 to 6,926 for DMSP." In addition, they say that "concentrations of DMSP in coral mucus were also exceptionally high, with mucus from Acropora formosa containing the highest levels of DMSP." Last of all, they observed that DMS and DMSP concentrations were substantially higher than water-column concentrations in both surface microlayer samples and coral-reef sediment pore waters. Hence, Broadbent and Jones concluded that "the elevated concentrations of DMS and DMSP in mucus ropes, coral mucus, surface films and sediment pore waters strongly suggest that coral reefs in the GBR are significant sources of these two sulphur substances," which in turn suggests that coral reefs may figure prominently in the Charlson et al. phenomenon that helps to keep earth's temperature from rising too high.

In a closely allied study, Jones and Trevena (2005) measured dissolved DMS, DMSP, the water-to-air flux of DMS, and atmospheric DMS concentration during a winter voyage through the northern GBR, Coral Sea, Gulf of Papua (GOP), and Solomon and Bismarck Seas. This work revealed that the "highest levels of most of these constituents occurred in the northern GBR, NW Coral Sea and GOP, with highest levels of atmospheric DMS often occurring in south-easterly to southerly trade winds sampled in the region where the highest biomass of coral reefs occur." They also found that the increase in atmospheric DMS "was mainly a result of a combination of high winds and the extremely low tides in July, when a high biomass of coral reefs in this region was aerially exposed." These findings helped to solidify the link between coral zooxanthellae activity and the atmospheric concentration of DMS, which Broadbent and Jones (2004) called "a negative greenhouse gas," i.e., one whose presence tends to cool the planet. Hence, it broadens the base of the CLAW hypothesis (named for the four scientists of Charlson et al., 1987, who formulated it - Charlson, Lovelock, Andreae and Warren) and makes it ever more likely that that hypothesis represents a viable mechanism for tempering, and possibly even capping, global warming.

In the years that have followed several more studies have continued to further probe the robustness of the CLAW hypothesis. Gunson et al. (2006), for example, performed a number of climate simulations using a coupled ocean-atmosphere general circulation model that included an atmospheric sulfur cycle and a marine ecosystem model. In doing so, they determined, as they describe it, that "the modeled global climate is sensitive to ocean DMS production in the manner hypothesized by CLAW," and that "perturbations to ocean DMS production cause significant impacts on global climate." For a halving of oceanic DMS emissions, for example, they found that the modeled net cloud radiative forcing increased by 3 W/m2 and, through a readjustment of the global radiative energy balance, that the surface air temperature rose by 1.6°C. On the other hand, for a doubling of oceanic DMS emissions, they found that net cloud radiative forcing declined by just under 2 W/m2 and that the surface air temperature decreased by just under 1°C. These are encouraging findings, suggestive of the fact that Earth's climate system is indeed capable of successfully buffering itself against the propensity for warming created by rising atmospheric CO2 concentrations.

In a contemporaneous study, Wong et al. (2006) recorded DMS concentrations and physical oceanographic data at ocean stations P20 and P26 in the Gulf of Alaska in the Northeast Pacific Ocean. Their analyses of the data showed that as the sea surface temperature of a region rises, "the stratification of the upper water column intensifies and oceanic upwelling weakens," such that "in the nutrient-rich waters of the sub-Arctic Pacific, higher stratification and shallower mixed layer favor the growth of small-sized phytoplankton such as flagellates, dinoflagellates and coccolithophorids." Noting that "most prolific DMSP producers are members of these phytoplankton groups," they say that, "consequently, the local ecosystem is shifted towards one with structure and function adapted to production of DMSP and DMS."

The significance of these observations, in the words of the four researchers, is that "globally, a larger part of the warming oceans may have highly stratified water for a longer part of the year," and they say that "these conditions could enhance the shift in the marine ecosystem described herein, and might induce more rapid turnover of DMSP and higher production of DMS," such that "in a warming global climate, we might anticipate an increasing emission of biogenic DMS from the ocean surface," which, of course, is a phenomenon that would tend to counteract whatever impetus for warming was causing sea surface temperatures to rise, thereby slowing or negating their upward progression.

Also in 2006, Meskhidze and Nenes explored the effects of ocean biological productivity on the microphysical and radiative properties of marine clouds over a large and seasonally-recurring phytoplankton bloom in the Southern Ocean in the vicinity of South Georgia Island, where upwelling nutrient-rich waters, as they describe it, "can support massive phytoplankton blooms, with chlorophyll a concentrations more than an order of magnitude higher than the background," in which endeavor, they used the Sea-viewing Wide Field-of-view Sensor to obtain the needed chlorophyll data and the Moderate Resolution Imaging Spectroradiometer to determine the effective radii of cloud condensation nuclei.

Their efforts paid off handsomely, with the researchers discovering that "cloud droplet number concentration over the bloom was twice what it was away from the bloom, and cloud effective radius was reduced by 30%," such that "the resulting change in the short-wave radiative flux at the top of the atmosphere was -15 watts per square meter, comparable to the aerosol indirect effect over highly polluted regions," and, as might be added, much greater locally than the opposite (positive) radiative forcing calculated to have been produced by the increasing concentrations of all greenhouse gases emitted to the atmosphere since pre-industrial times. And in what amounted to a massive understatement of the major implication of their findings, Meskhidze and Nenes thus concluded that secondary organic aerosol formation in remote marine air may need to be included in global climate models, as it may play, as they described it, "a considerable role in climate transition," which role just happens to be one of powerful negative feedback.

In another impressive experiment that was part of the Third Pelagic Ecosystem CO2 Enrichment Study, Wingenter et al. (2007) investigated the effects of atmospheric CO2 enrichment on marine microorganisms within nine marine mesocosms maintained within 2-m-diameter polyethylene bags submerged to a depth of 10 m in a fjord at the Large-Scale Facilities of the Biological Station of the University of Bergen in Espegrend, Norway. Three of these mesocosms were maintained at ambient levels of CO2 (~375 ppm or base CO2), three were maintained at levels expected to prevail at the end of the current century (760 ppm or 2xCO2), and three were maintained at levels predicted for the middle of the next century (1150 ppm or 3xCO2); and during the 25 days of their experiment, the twelve researchers followed the development and subsequent decline of induced blooms of the coccolithophorid Emiliania huxleyi in the three CO2 environments, carefully measuring several physical, chemical and biological parameters along the way.

When all was said and done, Wingenter et al.'s measurements and analyses indicated that "dimethylsulfide production followed the development and decline of the phytoplankton bloom," and that "maximum DMS concentrations coincided with the peak in chlorophyll-a concentrations in the present day CO2 treatment, but were delayed by 1-3 days relative to chlorophyll-a in the double and triple CO2 treatments." In addition, they found that "DMS was 26% and 18% higher in the 2x and 3xCO2 mesocosms, respectively (days 0-17)." The iodocarbon chloroiodomethane (CH2CII), on the other hand, had its peak concentration about 6-10 days after the chlorophyll-a maximum; but its estimated abundance was 46% higher in the 2xCO2 mesocosms and 131% higher in the 3xCO2 mesocosms.

The international team of scientists concluded from their work that "the differences in DMS and CH2CII concentrations may be viewed as a result of changes to the ecosystems as a whole brought on by the CO2 perturbations." And because emissions of both DMS (Bates et al., 1992) and various iodocarbons (O'Dowd et al., 2002; Jimenez et al., 2003) typically lead to an enhancement of cloud condensation nuclei in the marine atmosphere, the CO2-induced stimulations of the marine emissions of these two substances provide a natural brake on the tendency for global warming to occur as a consequence of any forcing, as they lead to the creation of more-highly-reflective clouds over greater areas of the world's oceans. Consequently, as Wingenter et al. describe it, "these processes may help contribute to the homeostasis of the planet."

In a similar experiment, Vogt et al. (2008) analyzed the effects of atmospheric CO2 enrichment on various marine microorganisms and DMS production under the same three CO2 concentrations as those employed by Wingenter et al. (2007) -- 375, 760 and 1150 ppm -- for a period of 24 days. In doing so, they found there were no significant phytoplankton species shifts among treatments, and that "ecosystem composition, bacterial and phytoplankton abundances and productivity, grazing rates and total grazer abundance and reproduction were not significantly affected by CO2-induced effects," citing in support of this statement the work of Riebesell et al. (2007), Riebesell et al. (2008), Egge et al. (2007), Paulino et al. (2007), Larsen et al. (2007), Suffrian et al. (2008) and Carotenuto et al. (2007). In addition, they state that "while DMS stayed elevated in the treatments with elevated CO2, we observed a steep decline in DMS concentration in the treatment with low CO2," i.e., the ambient CO2 treatment.

With respect to their many findings, the eight researchers say their observations suggest that "the system under study was surprisingly resilient to abrupt and large pH changes," which is just the opposite of what the world's climate alarmists characteristically predict about CO2-induced "ocean acidification." And that may be why Vogt et al. described the marine ecosystem they studied as "surprisingly resilient" to such change: it may have been a little unexpected.

Working in the coastal waters of Korea from 21 November to 11 December 2008, Kim et al. (2010) also conducted a CO2 enrichment experiment, utilizing 2400-liter mesocosm enclosures to simulate, in triplicate, three sets of environmental conditions -- an ambient control (~400 ppm CO2 and ambient temperature), an acidification treatment (~900 ppm CO2 and ambient temperature), and a greenhouse treatment (~900 ppm CO2 and ~3°C warmer-than-ambient temperature) -- and within these mesocosms they initiated phytoplankton blooms by adding equal quantities of nutrients to each mesocosm on day 0, while for 20 days thereafter they measured numerous pertinent parameters within each mesocosm.

Their results indicated that "the total accumulated DMS concentrations (integrated over the experimental period) in the acidification and greenhouse mesocosms were approximately 80% and 60% higher than the values measured in the control mesocosms, respectively." And they attributed these results to the fact that, in their experiment, (1) "autotrophic nanoflagellates (which are known to be significant DMSP producers) showed increased growth in response to elevated CO2," and that (2) "grazing rates [of microzooplankton] were significantly higher in the treatment mesocosms than in the control mesocosms." Because of these findings, in the concluding paragraph of their paper Kim et al. write that "in the context of global environmental change, the key implication of our results is that DMS production resulting from CO2-induced grazing activity may increase under future high CO2 conditions," and, therefore, they conclude that "DMS production in the ocean may act to counter the effects of global warming in the future."

In another study, Watanabe et al. (2007) utilized sea surface DMS data and other hydrographic parameters measured in the North Pacific Ocean between latitudes 25 and 55°N to develop and validate an empirical equation for sea surface DMS concentration that uses sea surface temperature, sea surface nitrate concentration and latitude as input data. Then, by applying the algorithm they developed to hydrographic time series datasets pertaining to the western North Pacific that span the period 1971 to 2000, the seven researchers found that the annual flux of DMS from sea to air in that region increased by 1.9-4.8 µmol m-2 year-1, which increase, in their words, "was equal to the annual rate of increase of about 1% of the climatological annual averaged flux of DMS in the western North Pacific in the last three decades." And these observations also suggest that the negative climate feedback phenomenon driven by increasing oceanic DMS concentrations is "alive and well."

Working with climate and DMS production data from the region of the Barents Sea (70-80°N, 30-35°E), which were obtained over the period 1998 to 2002, Qu and Gabric (2010) employed a genetic algorithm to calibrate chlorophyll-a measurements (obtained from SeaWiFS satellite data) for use in a regional DMS production model. Then, using GCM temperature outputs for the periods of 1960-1970 (pre-industry CO2 level) and 2078-2086 (triple the pre-industry CO2 level), they calculated the warming-induced enhancement of the DMS flux from the Barents Sea region.

The two researchers report that "significantly decreasing ice coverage, increasing sea surface temperature and decreasing mixed-layer depth could lead to annual DMS flux increases of more than 100% by the time of equivalent CO2 tripling (the year 2080)." In commenting on these findings, Qu and Gabric state that "such a large change would have a great impact on the Arctic energy budget and may offset the effects of anthropogenic warming that are amplified at polar latitudes." What is more, they say that "many of these physical changes will also promote similar perturbations for other biogenic species (Leck et al., 2004), some of which are now thought to be equally influential to the aerosol climate of the Arctic Ocean."

One year later, working with Phaeocystis antarctica -- a polar prymnesiophyte or haptophyte (marine microalga or phytoplankton) -- Orellana et al. (2011) measured the concentrations of DMS and DMSP in whole cells and isolated secretory vesicles of the species, as well as in samples of broken cells, because, as they elucidate, "in addition to autolysis (Hill et al., 1998), viral lysis (Malin et al., 1998), and zooplankton grazing (Dacey and Wakeham, 1986; Wolfe and Steinke, 1996), it is believed that DMSP passively diffuses into seawater," while noting that "understanding the regulation of this mechanism is necessary in order to obtain a correct partitioning of the cellular and extracellular DMSP and DMS pools in seawater and allow predictions of global budgets." In doing so, the four U.S. researchers successfully demonstrated that "DMSP and DMS were stored in the secretory vesicles of Phaeocystis antarctica," where "they were trapped within a polyanionic gel matrix, which prevented an accurate measurement of their concentration in the absence of a chelating agent." And as a result of this finding, they concluded that "the pool of total DMSP in the presence of Phaeocystis may be underestimated by as much as half."

Noting that "models for the distribution of marine DMS have lately been increasing in number and complexity, such that a regional portrait of their evolving climate response is constructible," Cameron-Smith et al. (2011) employed the most recent version of the Community Climate System Model (CCSM), described by Collins et al. (2006), to produce the first marine sulfur simulations performed with what they refer to as "the most sophisticated ocean sulfur cycle model yet reported."

In one of their simulations, the atmospheric CO2 concentration was held steady at 355 ppm, while in another it was set at 970 ppm, in order to simulate the climate near the end of the 21st century, as projected by the IPCC (2001) SRES A1F1 emissions scenario. And this latter CO2 concentration and its modeled climatic consequences resulted in the simulation of "rings of high DMS near Antarctica due to the inclusion of a Phaeocystis parameterization," for this unicellular, photosynthetic, eukaryotic alga generates, in the words of the five U.S. scientists, "several times the typical DMSP level (dimethyl sulfoniopropionate, a major DMS precursor) and favors cold water habitat (Matrai and Vernet, 1997)."

Consequently, in the face of the modeled global warming produced by the specified increase in the atmosphere's CO2 concentration, there is a migration of Phaeocystis species towards the cooler waters of higher latitudes; and under these conditions the model employed by Cameron-Smith et al. simulated increases in the "zonal averaged DMS flux to the atmosphere of over 150% in the Southern Ocean," which they say was "due to concurrent sea ice changes and ocean ecosystem composition shifts caused by changes in temperature, mixing, nutrient, and light regimes." And based on other modeling exercises they conducted, they say that the shift in the location of maximum DMS emissions towards colder regions "is usually reinforced with even more sophisticated models."

As for the ultimate climatic implications of the southward shift of the band of significantly-enhanced maximum DMS emissions in the Southern Hemisphere, Cameron-Smith and colleagues say that "in global estimates involving constant upward or downward DMS flux changes, average planetary surface temperatures separate by three or more degrees Celsius," citing the work of Charlson et al. (1987) and Gunson et al. (2006). Thus, it can finally be appreciated that this strong biological response to a CO2-induced impetus for warming, can result in a greatly-strengthened negative regional feedback -- via enhanced regional cloud development -- that results in more incoming solar radiation being reflected back to space with enhanced regional cooling. And the resulting DMS-enhanced "thermal insulating" of Antarctica from the rest of the world by this mechanism could very well significantly reduce the propensity for that continent's ice sheets to lose mass and contribute to sea level rise, even in a world that is experiencing a net warming.

In conclusion, it is unfortunate that in light of the overwhelming empirical evidence for both land- and ocean-based DMS-driven negative feedbacks to global warming, the effects of these processes are only now beginning to be incorporated into today's state-of-the-art climate models. And when such effects are properly considered, it may be that these biologically-driven phenomena may prove to totally compensate for the warming influence of all greenhouse gas emissions experienced to date, as well as all those that are anticipated to occur in the future.

References
Abraham, E.R., Law, C.S., Boyd, P.W., Lavender, S.J., Maldonado, M.T. and Bowie, A.R. 2000. Importance of stirring in the development of an iron-fertilized phytoplankton bloom. Nature 407: 727-730.

Ayers, G.P. and Gillett, R.W. 2000. DMS and its oxidation products in the remote marine atmosphere: implications for climate and atmospheric chemistry. Journal of Sea Research 43: 275-286.

Baboukas, E., Sciare, J. and Mihalopoulos, N. 2002. Interannual variability of methanesulfonate in rainwater at Amsterdam Island (Southern Indian Ocean). Atmospheric Environment 36: 5131-5139.

Bates, T.S., Lamb, B.K., Guenther, A., Dignon, J. and Stoiber, R.E. 1992. Sulfur emissions to the atmosphere from natural sources. Journal of Atmospheric Chemistry 14: 315-337.

Boyd, P.W. and Doney, S.C. 2002. Modeling regional responses by marine pelagic ecosystems to global climate change. Geophysical Research Letters 29: 10.1029/2001GL014130.

Boyd, P.W., Watson, A.J., Law, C.S., Abraham, E.R., Trull, T., Murdoch, R., Bakker, D.C.E., Bowie, A.R., Buesseler, K.O., Chang, H., Charette, M., Croot, P., Downing, K., Frew, R., Gall, M., Hadfield, M., Hall, J., Harvey, M., Jameson, G., LaRoche, J., Liddicoat, M., Ling, R., Maldonado, M.T., McKay, R.M., Nodder, S., Pickmere, S., Pridmore, R., Rintoul, S., Safi, K., Sutton, P., Strzepek, R., Tanneberger, K., Turner, S., Waite, A. and Zeldis, J. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407: 695-702.

Broadbent, A.D., Jones, G.B. and Jones, R.J. 2002. DMSP in corals and benthic algae from the Great Barrier Reef. Estuarine, Coastal and Shelf Science 55: 547-555.

Cameron-Smith, P., Elliott, S., Maltrud, M., Erickson, D. and Wingenter, O. 2011. Changes in dimethyl sulfide oceanic distribution due to climate change. Geophysical Research Letters 38: 10.1029/2011GL047069.

Carotenuto, Y., Putzeys, S., Simonelli, P., Paulino, A., Meyerhofer, M., Suffrian, K., Antia, A. and Nejstgaard, J.C. 2007. Copepod feeding and reproduction in relation to phytoplankton development during the PeECE III mesocosm experiment. Biogeosciences Discussions 4: 3913-3936.

Charlson, R.J., Lovelock, J.E., Andrea, M.O. and Warren, S.G. 1987. Oceanic phytoplankton, atmospheric sulfur, cloud albedo and climate. Nature 326: 655-661.

Collins, W.D., Bitz, C.M., Blackmon, M.L., Bonan, G.B., Bretherton, C.S., Carton, J.A., Chang, P., Doney, S.C., Hack, J.J., Henderson, T.B., Kiehl, J.T., Large, W.G., McKenna, D.S., Santer, B.D. and Smith, R.D. 2006. The Community Climate System Model Version 3 (CCSM3). Journal of Climate 19: 2122-2143.

Dacey, J.W.H., Howse, F.A., Michaels, A.F. and Wakeham, S.G. 1998. Temporal variability of dimethylsulfide and dimethylsulfoniopropionate in the Sagasso Sea. Deep Sea Research 45: 2085-2104.

Dacey, J.W.H. and Wakeham, S.G. 1986. Oceanic dimethylsulfide: production during zooplankton grazing. Science 233: 1314-1316.

Egge, J., Thingstad, F., Engel, A., Bellerby, R.G.J. and Riebesell, U. 2007. Primary production at elevated nutrient and pCO2 levels. Biogeosciences Discussions 4: 4385-4410.

Fogelqvist, E. 1991. Dimethylsulphide (DMS) in the Weddell Sea surface and bottom water. Marine Chemistry 35: 169-177.

Gunson, J.R., Spall, S.A., Anderson, T.R., Jones, A., Totterdell, I.J. and Woodage, M.J. 2006. Climate sensitivity to ocean dimethylsulphide emissions. Geophysical Research Letters 33: 10.1029/2005GL024982.

Hill, R.W., White, B.A., Cottrell, M.T. and Dacey, J.W.H. 1998. Virus-mediated total release of dimethylsulfoniopropionate from marine phytoplankton: a potential climate process. Aquatic and Microbial Ecology 14: 1-6.

Hopke, P.K., Xie, Y. and Paatero, P. 1999. Mixed multiway analysis of airborne particle composition data. Journal of Chemometrics 13: 343-352.

Idso, S.B. 1990. A role for soil microbes in moderating the carbon dioxide greenhouse effect? Soil Science 149: 179-180.

Jimenez, J.L., Bahreini, R., Cocker III, D.R., Zhuang, H., Varutbangkul, V., Flagan, R.C., Seinfeld, J.H., O'Dowd, C.D. and Hoffmann, T. 2003. New particle formation from photooxidation of diiodomethane (CH2I2). Journal of Geophysical Research 108: 10.1029/2002JD002452.

Jones, G.B. and Trevena, A.J. 2005. The influence of coral reefs on atmospheric dimethylsulphide over the Great Barrier Reef, Coral Sea, Gulf of Papua and Solomon and Bismarck Seas. Marine and Freshwater Research 56: 85-93.

Kim, J.-M., Lee, K., Yang, E.J., Shin, K., Noh, J.H., Park, K.-T., Hyun, B., Jeong, H.-J., Kim, J.-H., Kim, K.Y., Kim, M., Kim, H.-C., Jang, P.-G. and Jang, M.-C. 2010. Enhanced production of oceanic dimethylsulfide resulting from CO2-induced grazing activity in a high CO2 world. Environmental Science & Technology: 10.1021/es102028k.

Kirst, G.O., Thiel, C., Wolff, H., Nothnagel, J., Wanzek, M. and Ulmke, R. 1991. DMSP in ice algae and its possible role. Marine Chemistry 35: 381-388.

Kouvarakis, G. and Mihalopoulos, N. 2002. Seasonal variation of dimethylsulfide in the gas phase and of methanesulfonate and non-sea-salt sulfate in the aerosols phase in the Eastern Mediterranean atmosphere. Atmospheric Environment 36: 929-938.

Larsen, J.B., Larsen, A., Thyrhaug, R., Bratbak, G. and Sandaa R.-A. 2007. Marine viral populations detected during a nutrient induced phytoplankton bloom at elevated pCO2 levels. Biogeosciences Discussions 4: 3961-3985.

Leck, C., Tjernstrom, M., Matrai, P., Swietlicki, E. and Bigg, E.K. 2004. Can marine micro-organisms influence melting of the Arctic pack ice? EOS, Transactions, American Geophysical Union 85: 25-36.

Legrand, M., Feniet-Saigne, C., Sattzman, E.S., Germain, C., Barkov, N.I. and Petrov, V.N. 1991. Ice-core record of oceanic emissions of dimethylsulfide during the last climate cycle. Nature 350: 144-146.

Levasseur, M., Gosselin, M. and Michaud, S. 1994. A new source of dimethylsulphide (DMS) for the Arctic atmosphere: ice diatoms. Marine Biology 121: 381-387.

Malin, G., Wilson, W.H., Bratbak, G., Liss, P.S. and Mann, N.H. 1998. Elevated production of dimethylsulfide resulting from viral infection of cultures of Phaeocystis pouchetii. Limnology and Oceanography 43: 1389-1393.

Martin, J.H. 1990. Glacial-interglacial CO2 change: The iron hypothesis. Paleoceanography 5: 1-13.

Martin, J.H. and Fitzwater, S.E. 1988. Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331: 341-343.

Martin, J.H., Gordon, M. and Fitzwater, S. 1988. Oceanic iron distributions in relation to phytoplanktonic productivity. EOS: Transactions of the American Geophysical Union 69: 1045.

Matrai, P. and Vernet, M. 1997. Dynamics of the vernal bloom in the marginal ice zone of the Barents Sea: Dimethyl sulfide and dimethylsulfoniopropionate budgets. Journal of Geophysical Research 102: 22,965-22,979.

Meskhidze, N. and Nenes, A. 2006. Phytoplankton and cloudiness in the Southern Ocean. Science 314: 1419-1423.

O'Dowd, C.D., Jimenez, J.L., Bahreini, R., Flagan, R.C., Seinfeld, J.H., Hameri, K., Pirjola, L., Kulmala, M., Jennings, S.G. and Hoffmann, T. 2002. Marine aerosol formation from biogenic iodine emissions. Nature 417: 632-636.

Orellana, M.V., Matrai, P.A., Janer, M. and Rauschenberg, C.D. 2011. Dimethylsulfoniopropionate storage in Phaeocystis (Prymnesiophyceae) secretory vesicles. Journal of Phycology 47: 112-117.

Paulino, A.I., Egge, J.K. and Larsen, A. 2007. Effects of increased atmospheric CO2 on small and intermediate sized osmotrophs during a nutrient induced phytoplankton bloom. Biogeosciences Discussions 4: 4173-4195.

Qu, B. and Gabric, A.J. 2010. Using genetic algorithms to calibrate a dimethylsulfide production model in the Arctic Ocean. Chinese Journal of Oceanology and Limnology 28: 573-582.

Riebesell, U., Bellerby, R.G.J., Grossart, H.-P. and Thingstad, F. 2008. Mesocosm CO2 perturbation studies: from organism to community level. Biogeosciences Discussions 5: 641-659.

Riebesell, U., Schulz, K., Bellerby, R., Botros, M., Fritsche, P., Meyerhofer, M., Neill, C., Nondal, G., Oschlies, A., Wohlers, J. and Zollner, E. 2007. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450: 10.1038/nature06267.

Sciare, J., Mihalopoulos, N. and Dentener, F.J. 2000. Interannual variability of atmospheric dimethylsulfide in the southern Indian Ocean. Journal of Geophysical Research 105: 26,369-26,377.

Simo, R. and Pedros-Alio, C. 1999. Role of vertical mixing in controlling the oceanic production of dimethyl sulphide. Nature 402: 396-399.

Steinberg, D.K., Carlson, C.A., Bates, N.R., Johnson, R.J., Michaels, A.F. and Knap, A.H. 2001. Overview of the US JGOFS Bermuda Atlantic Time-series Study (BATS): a decade-scale look at ocean biology and biogeochemistry. Deep Sea Research Part II: Topical Studies in Oceanography 48: 1405-1447.

Suffrian, K., Simonelli, P., Nejstgaard, J.C., Putzeys, S., Carotenuto, Y. and Antia, A.N. 2008. Microzooplankton grazing and phytoplankton growth in marine mesocosms with increased CO2 levels. Biogeosciences Discussions 5: 411-433.

Sunda, W., Kieber, D.J., Kiene, R.P. and Huntsman, S. 2002. An antioxidant function for DMSP and DMS in marine algae. Nature 418: 317-320.

Toole, D.A. and Siegel, D.A. 2004. Light-driven cycling of dimethylsulfide (DMS) in the Sargasso Sea: Closing the loop. Geophysical Research Letters 31: 10.1029/2004GL019581.

Trevena, A.J., Jones, G.B., Wright, S.W. and Van den Enden, R.L. 2000. Profiles of DMSP, algal pigments, nutrients and salinity in pack ice from eastern Antarctica. Journal of Sea Research 43: 265-273.

Trevena, A.J., Jones, G.B., Wright, S.W. and Van den Enden, R.L. 2003. Profiles of dimethylsulphoniopropionate (DMSP), algal pigments, nutrients, and salinity in the fast ice of Prydz Bay, Antarctica. Journal of Geophysical Research 108: 3145-3156.

Turner, S.M., Harvey, M.J., Law, C.S., Nightingale, P.D. and Liss, P.S. 2004. Iron-induced changes in oceanic sulfur biogeochemistry. Geophysical Research Letters 31: 10.1029/2004GL020296.

Turner, S.M., Nightingale, P.D., Spokes, L.J., Liddicoat, M.I. and Liss, P.S. 1996. Increased dimethyl sulphide concentrations in sea water from in situ iron enrichment. Nature 383: 513-517.

Vogt, M., Steinke, M., Turner, S., Paulino, A., Meyerhofer, M., Riebesell, U., LeQuere, C. and Liss, P. 2008. Dynamics of dimethylsulphoniopropionate and dimethylsulphide under different CO2 concentrations during a mesocosm experiment. Biogeosciences 5: 407-419.

Watanabe, Y.W., Yoshinari, H., Sakamoto, A., Nakano, Y., Kasamatsu, N., Midorikawa, T. and Ono, T. 2007. Reconstruction of sea surface dimethylsulfide in the North Pacific during 1970s to 2000s. Marine Chemistry 103: 347-358.

Wingenter, O.W., Haase, K.B., Zeigler, M., Blake, D.R., Rowland, F.S., Sive, B.C., Paulino, A., Thyrhaug, R., Larsen A., Schulz, K., Meyerhofer, M. and Riebesell, U. 2007. Unexpected consequences of increasing CO2 and ocean acidity on marine production of DMS and CH2CII: Potential climate impacts. Geophysical Research Letters 34: 10.1029/2006GL028139.

Wolfe, G.V. and Steinke, M. 1996. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnology and Oceanography 41: 1151-1160.

Wong, C.-S., Wong, S.-K. E., Pena, A. and Levasseur, M. 2006. Climatic effect on DMS producers in the NE sub-Arctic Pacific: ENSO on the upper ocean. Tellus 58B: 319-326.

Last updated 23 May 2012