Environ. Sci. Technol. 2010, 44, 8140–8143
Enhanced Production of Oceanic Dimethylsulfide Resulting from CO2-Induced Grazing Activity in a High CO2 World J A - M Y U N G K I M , † K I T A C K L E E , * ,† EUN JIN YANG,‡ KYOUNGSOON SHIN,§ JAE HOON NOH,| KI-TAE PARK,† BONGGIL HYUN,§ HAE-JIN JEONG,⊥ JU-HYOUNG KIM,# KWANG YOUNG KIM,# MIOK KIM,† HYUN-CHEOL KIM,† PUNG-GUK JANG,§ AND MIN-CHUL JANG§ School of Environmental Science and Engineering, Pohang University of Science and Technology, Pohang, 790-784, Korea, Korea Ocean Research and Development Institute/Korea Polar Research Institute, Songdo Techno Park, Incheon, 406-840, Korea, Korea Ocean Research and Development Institute/South Sea Institute, Jangmok, 656-830, Korea, Korea Ocean Research and Development Institute, Ansan, 425-600, Korea, School of Earth and Environmental Sciences, Seoul National University, Seoul, 151-747, Korea, and Department of Oceanography, Chonnam National University, Gwangju, 500-757, Korea
Received June 15, 2010. Revised manuscript received September 6, 2010. Accepted September 14, 2010.
Oceanic dimethylsulfide (DMS) released to the atmosphere affects the Earth’s radiation budget through the production and growth of cloud condensation nuclei over the oceans. However, it is not yet known whether this negative climate feedback mechanism will intensify or weaken in oceans characterized by high CO2 levels and warm temperatures. To investigate the effects of two emerging environmental threats (ocean acidification and warming) on marine DMS production, we performed a perturbation experiment in a coastal environment. Two sets of CO2 and temperature conditions (a pCO2 of ∼900 ppmv at ambient temperature conditions, and a pCO2 of ∼900 ppmv at a temperature ∼3 °C warmer than ambient) significantly stimulated the grazing rate and the growth rate of heterotrophic dinoflagellates (ubiquitous marine microzooplankton). The increased grazing rate resulted in considerable DMS production. Our results indicate that increased grazing-induced DMS production may occur in high CO2 oceans in the future.
Introduction DMS is a semivolatile organic sulfur compound that represents 95% of the natural marine flux of sulfur gases to the atmosphere (1, 2). Airborne DMS may be oxidized to form * Corresponding author phone: 82-54-279-2285; fax: 82-54-2798299; e-mail:
[email protected]. † Pohang University of Science and Technology. ‡ Korea Polar Research Institute. § South Sea Institute. | Korea Ocean Research and Development Institute. ⊥ Seoul National University. # Chonnam National University. 8140
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non sea-salt sulfate aerosols, which are known to act as cloud condensation nuclei and thereby exert a cooling effect by absorbing or scattering solar radiation (3). Multiple processes interact to regulate DMS production in the ocean. Ubiquitous autotrophic plankton synthesize the DMS precursor dimethylsulfoniopropionate (DMSP) for cellular use, including as an osmolyte (4), a cryoprotectant (5) and an antioxidant (6). DMS is generated by intracellular or extracellular enzymatic cleavage of DMSP by DMSP-lyase, which is synthesized by algae and bacteria, following DMSP secretion from producer cells or release following autolysis or viral attack (7-11). Grazing activity can also result in DMSP conversion to DMS if DMSP and DMSP-lyase are physically mixed following grazing (11, 12). Although numerous studies have shed light on the mechanisms of DMS production (e.g., refs 7-12), knowledge of the possible impact of future oceanic conditions (e.g., high CO2 and warm temperatures) on DMS production is limited. There is an urgent need for manipulative experiments at the community level to gain an integrated understanding of the sensitivity of marine biota to human-induced oceanic changes. The experiments of this nature can be undertaken in large enclosures equipped to control CO2 concentration and temperature. Such experiments allow relatively simple manipulation of experimental conditions, and can be readily repeated and performed with a greater degree of replication than can experiments in the open ocean. Several studies of this type have investigated the effect of ocean acidification (increased CO2 concentration) on DMSP and DMS production (13-15), but studies of the combined effects of acidification and warming have yet to be attempted using a mesocosm, although limited shipboard incubation experiments have been reported (16). The conclusions from such studies have been inconsistent (13-16). In this study we evaluated the community-scale effects of increased CO2 concentration and temperature on marine DMS production in a mesocosm system.
Experimental Section The experiment was conducted in the coastal waters of Korea (34.6°N and 128.5°E) over 20 days from 21 November 2008 to 11 December 2008. Natural phytoplankton blooms are known to frequently occur at the experimental site throughout the year. The experiment involved mesocosm enclosures of approximately 2400 L, which were used, in triplicate, to simulate three sets of environmental conditions: an ambient control (∼400 ppmv CO2/ambient temperature), an acidification treatment (∼900 ppmv CO2/ambient temperature), and a greenhouse treatment (∼900 ppmv CO2/∼3 °C warmer than ambient temperature) (Supporting Information (SI) Figure S1). As only nine enclosures were available we were unable to allocate enclosures to test the effect of temperature alone. However, we evaluated the combined effects of temperature and elevated CO2 (the greenhouse treatment), which are likely to reflect future ocean conditions. The simulated CO2 (∼900 ppmv) and temperature (∼3 °C warmer than ambient temperature) values were chosen to approximate conditions in the year 2100, based on model projections of the A2 Scenario of the Intergovernmental Panel on Climate Change (IPCC) Special Report on Emissions Scenarios (17). The mesocosm facility and its operation are briefly described in the SI. Thorough descriptions can be found elsewhere (18). To initiate the development of a phytoplankton bloom, equal quantities of nutrients were added to each mesocosm on day 0, yielding initial nutrient 10.1021/es102028k
2010 American Chemical Society
Published on Web 09/30/2010
FIGURE 1. Dimethylsulfide (DMS) concentration change during the study period. The green, blue, and red symbols and lines represent the control, acidification and greenhouse conditions, respectively. The shading represents the standard deviations (1σ) from the mean for the replicate mesocosms.
FIGURE 2. The grazing rate (largely due to microzooplankton) in the control (green), acidification (blue), and greenhouse (red) mesocosms during the study period. Error bars represents the standard deviations from the mean for the replicate mesocosms.
concentrations of ∼41 µmol kg-1 nitrate (N), ∼2.5 µmol kg-1 phosphate (P), and ∼40 µmol kg-1 silicate (Si). All enclosures were sampled daily at a depth of ∼1 m after the sample particulates and solutes inside the enclosures were homogeneously mixed (SI Figure S2). The small variation ( 0.8) (Figures 1 and 3). Because the intracellular level of DMSP varies considerably among autotrophic plankton species, the prey composition may be intimately linked to DMS production (20). In all mesocosms, the microzooplankton (20-100 µm) fed largely on diatoms including Skeletonema costatum, Chaetoceros spp., and Eucampia zodiacus (Figure 4). Among these major prey species, only S. costatum, which has a DMSP cell quota of ∼0.5 pg cell-1 (20, 25), showed a significant positive growth response to increased pCO2 (Figure 4b and SI Table S1) (ANOVA, p < 0.05). Microzooplankton also fed on other VOL. 44, NO. 21, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY
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FIGURE 5. Abundance of prey autotrophic plankton classes during the study period: (a) Autotrophic nanoflagellates, (b) Autotrophic picoplanktons, and (c) Autotrophic dinoflagellates.
FIGURE 4. Abundance of prey diatom during the study period: (a) Total diatoms, (b) Skeletonema costatum, (c) Chaetoceros spp., and (d) Eucampia zodiacus. autotrophic plankton groups (i.e., autotrophic picoplankton, nanoflagellates and dinoflagellates), but in our experiment only autotrophic nanoflagellates (which are known to be significant DMSP producers) showed increased growth in response to elevated pCO2 (Figure 5a), in contrast to the other potential prey groups (Figure 5b, c). An additional line of evidence is derived from data on the DMSP concentrations. During the bloom period the contribution of particulate DMSP (DMSPP) to total biomass (expressed as particulate organic carbon; POC) in the acidification and greenhouse mesocosms was substantially greater than in the control mesocosms (SI Figure S4). The higher values of DMSPP/POC, in combination with the higher grazing rates, indicate that the microzooplankton in the acidification and greenhouse mesocosms probably fed on more DMSP-containing prey than in the control mesocosms. This resulted in greater DMS production in the acidification and greenhouse mesocosms than in the control mesocosms. The key factors likely to influence DMS production in the oceans (the growth rate of DMSP-containing phytoplankton 8142
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and the grazing rate of microzooplankton) responded positively to high CO2 concentrations simulating acidification and greenhouse conditions. This increased DMS production in high CO2 conditions is in marked contrast to the results of a recent mesocosm-based study (13), in which a reduction in DMS production was found under high CO2 conditions. Based on existing information it is not possible to explain this apparent discrepancy. We speculate that a difference in grazing activity between the two studies may be a factor, but this possibility cannot be investigated because the role of grazers in DMS production was not investigated in the other study (13). Our results are in broad agreement with those obtained in another mesocosm study (14, 15), where DMS production in high CO2 conditions was increased by bacterial and viral production. However, in this report the increases in DMS production under high CO2 conditions were statistically marginal (14, 15). Our finding that increased CO2 had discernible effects on growth, grazing rates or subsequent DMS production contrasts with previous studies (16, 26, 27) in which increased temperature (∼4 °C higher than ambient temperature) has been reported to be a dominant factor. This apparent discrepancy may be explained by species-specific responses to increased temperature and CO2 concentration (28). Additional experiments are needed to resolve the discrepancy. 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. If so, DMS production in the ocean may act to counter the effects of global warming in the future. To confirm our results, additional experiments in a range of oceanic regions and during different seasons are needed.
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Acknowledgments This work was supported by Midcareer Researcher Program (Nos. 2005-0051075, 2009-0084756) funded by the Korea National Research Foundation of Ministry of Education, Science and Technology.
Supporting Information Available
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A full description of the materials and methods. This material is available free of charge via the Internet at http:// pubs.acs.org/. (18)
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