INSIGHT | REVIEW ARTICLES
PUBLISHED ONLINE: 29 AUGUST 2013 | DOI: 10.1038/NGEO1910
Impact of Arctic meltdown on the microbial
cycling of sulphur
M. Levasseur
The Arctic is warming faster than any other region in the world. Among the changes already witnessed, the loss of seasonal
sea ice is by far the most striking. This large-scale shift in sea-ice cover could affect oceanic emissions of dimethylsulphide — a
climate-relevant trace gas generated by ice algae and phytoplankton. During the spring melt period, conditions at the margin of
Arctic sea ice favour the growth of these organisms. As a result, high levels of dimethylsulphide can accumulate at the bottom
of the ice, in leads, and in the water column at the ice edge during the spring melt season. Production of dimethylsulphide
is not limited to the sea-ice edge, however. Significant concentrations have also been detected in the seasonal ice-free zone
in spring and summer. Preliminary observations, together with model results, suggest that the production and emission of
dimethylsulphide will increase in the Arctic as seasonal sea-ice cover recedes. If it escapes to the atmosphere, this newly
generated dimethylsulphide could potentially cool the Arctic climate.
D
imethylsulphide (DMS) is a biogenic gas that represents
the single most important natural source of sulphur to the
atmosphere, accounting for up to 80% of global biogenic
sulphur emissions1. DMS plays several important physiological
and ecological roles in the water column where it is produced, but
it was its climatic role that caught the attention of the scientific
community. Once in the atmosphere, DMS is oxidized to sulphate
aerosol that can cool the climate by scattering solar radiation and
by forming small-radius cloud condensation nuclei that increase
the albedo of low-altitude clouds. The suggestion that oceanic
DMS emissions regulate climate — the so-called CLAW hypothesis (from the name of the four co-authors) — has fuelled hundreds of peer-reviewed papers since its publication in 1987 (ref. 2).
According to this hypothesis, a negative feedback loop operates
between DMS emissions and climate, in which DMS-derived aerosol reduces incoming solar radiation and surface temperatures,
thereby decreasing oceanic production of DMS. However, the
cogency of the proposed feedback loop has recently been called
into question. This revision in our understanding of the climatic
significance of DMS stems from a better appreciation of the diversity of inorganic and organic aerosol sources that can reduce
incoming solar radiation, together with a lack of evidence that
DMS-induced changes in cloud condensation nuclei yield changes
in cloud albedo, and changes in cloud albedo, surface temperature
and/or incident solar radiation feedback on DMS production3.
Indeed, a recent modelling exercise suggests that DMS emissions
induce only a weak increase in the abundance of cloud condensation nuclei over large parts of the world ocean4.
However, DMS emissions could exert a more significant influence on climate in regions where low aerosol concentrations prevail,
such as in the Arctic in summer, according to model simulations4.
This suggestion is reinforced by recent reports linking new particle
formation events in the Arctic atmosphere to DMS emissions5,6. The
impact of oceanic DMS emissions on the Arctic summer climate
may prove increasingly important in the future, owing to continued
reductions in the extent of the summer ice cover, and thus surface
albedo7,8. Indeed, model experiments suggest that the expansion of
the ice-free surface area in the Arctic Ocean could stimulate biological DMS production, partly offsetting the warming caused by the
loss of ice albedo9,10.
The presence of sea ice in the Arctic makes it a spatially complex
physical environment, hosting a diversity of biota that generate and
consume DMS. During spring and summer, microfloral and faunal
assemblages thrive at the bottom of the sea ice, in melt ponds and melt
domes, in mats suspended under the ice, in the water column under
the ice, in leads, at the ice edge and in open water (Figs 1 and 2). Our
knowledge of these environments and their inhabitants is limited11.
However, these environments seem to be characterized by specific
microbial assemblages that generate DMS, and are subject to external
forcings that can either favour or dampen DMS production.
The relative importance of individual algal species, and hence
their capacity to produce DMS, will change as the climate warms.
The microbes associated with sea ice are expected to disappear in
summer as early as 205012. The ice edge and its microbial flora and
fauna will move northward and the seasonal ice-free zone — the
area undergoing ice formation and melt every year — will increase
accordingly. Melt ponds will also increase in number and size, offering a greater surface area for sea–air exchanges of DMS (ref. 13).
The growth in melt ponds, along with more frequent and spatially
extensive leads and less snow cover, is also expected to increase radiation under the ice pack and thereby facilitate the development of
vast under-ice phytoplankton blooms13,14. Eventually, a new ice-free
ocean will take form, with its own DMS dynamics.
Here I review observational and model data on the different
sources of DMS in the Arctic, and assess how the strength of these
sources could change as the climate warms. It should be noted, however, that the flow of DMS data out of the Arctic since the first measurements in the early 1990s15,16 has been irregular, and entire regions
remain unexplored (Fig. 3).
Marine microbial production of dimethylsulphide
Early work on DMS production in the ocean focused on microalgae — the organisms known to be responsible for the production of
its non-gaseous precursor, dimethylsulphoniopropionate (DMSP).
However, it soon became clear that all members of the planktonic
food web, including viruses, bacteria, microalgae and grazers, were
involved in the process (Fig. 4).
Most of our understanding of the functioning of the marine DMS
cycle comes from studies conducted at low and mid-latitudes. In the
open ocean, the DMS cycle starts with the synthesis of DMSP by
Département de biologie (Québec-Océan, ArcticNet and Takuvik), Université Laval, Québec, G1V 0A6, Québec, Canada.
e-mail: [email protected].
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REVIEW ARTICLES | INSIGHT
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
a
b
c
d
e
f
Figure 1 | Examples of the diversity of habitats found in the Arctic. a, Ice edge. b, Lead. c, Melt ponds on first-year ice. d, Ice algae as seen from below the
ice. e, Ship-based sampling of ice algae from the ice pack. f, Ice algae from the bottom of an ice core. Photographs courtesy of Martin Fortier (ArcticNet)
(a–c,e), Christian Fritsen (d) and Virginie Galindo (f).
microalgae. Intracellular concentrations of DMSP can vary by three
orders of magnitude between major microalgal groups; dinoflagellates and prymnesiophytes represent strong producers, and diatoms
weak producers17. The abundance and taxonomic composition of
microalgae therefore directly affects the concentration and distribution of DMSP and DMS in the ocean.
The conversion of DMSP into DMS is mediated by enzymes
that have been found both intracellularly and bound to the outside
of microalgal cells. Direct production of DMS by microalgae has
been documented in the prymnesiophytes Phaeocystis spp., the coccolithophore Emiliania huxleyi and in several dinoflagellates18–20.
Heterotrophic bacteria can also convert DMSP into DMS. During
microalgal blooms, a fraction of the algal intracellular DMSP is
released into the extracellular medium by exudation, or zooplankton grazing and viral attack. This results in the formation of a pool
of dissolved DMSP in the water column. Technically challenging to
quantify 21, this pool is generally small (<2 nmol l–1) and characterized by a rapid turnover time (hours)22. Photoautotrophic cells can
assimilate dissolved DMSP (refs 23,24), but this process is poorly
understood. Rather, the activity of heterotrophic bacteria is thought
to account for the rapid turnover time of the dissolved DMSP
pool25,26.
Our understanding of the role of heterotrophic bacteria in the
DMS cycle has increased rapidly in the past ten years, owing to the
use of radio-labelled DMSP and DMS. It transpires that DMSP is a
widespread substrate among heterotrophic bacteria, providing up to
15% and 100% of their carbon and sulphur demand, respectively 25,27.
A portion of the dissolved DMSP consumed by heterotrophic bacteria is converted to DMS by their own enzymes26,28. The efficiency
with which bacteria convert dissolved DMSP into DMS (the bacterial
DMS yield) varies from 5 to 100%, depending on their nutritional status29 (Box 1). DMS production may also be mediated by free DMSPlyases in the water column26.
Sinks for DMS include bacterial consumption, photolysis
into dimethylsulphoxide (DMSO) and other compounds, and
692
ventilation to the atmosphere. The DMSP–DMS conversion system
has a high buffering capacity (Fig. 4), meaning that only a fraction
of the DMSP is converted to DMS available for sea-to-air exchange.
This means that the full potential for DMS production from DMSP
is far from being achieved. The few studies where most DMSrelated rate processes have been simultaneously measured show that
Sub-ice algal mats
?
Bottom-ice
algae
Ice-edge
phytoplankton
Leads
Melt pond
–1
2.2 nmol l
–1
2,000 nmol l
22 nmol l
–1
Deep chlorophyll
maximum
–1
4.7 nmol l
12 nmol l
?
–1
Under-ice
melt dome
Under-ice phytoplankton bloom
Figure 2 | Diversified biota present in the Arctic in spring and summer.
During spring and summer, microalgae and their associated fauna occupy
the different habitats that the presence of ice offers: they form algal mats
suspended under the ice (sub-ice algal mats; this Review), colonize the
bottom (usually the bottom 5 cm) of the sea ice (bottom-ice algae; ref. 55
and this Review), and grow in leads that form across the ice pack58,91, in melt
ponds forming on the ice (this Review), in the water column under the ice
when snow conditions and the presence of melt ponds and melt domes
allow more light to reach the water column, at the ice edge37,56,58,68, and in
open water where they usually accumulate on or close to the nitracline (a
sharp vertical gradient in nitrate concentrations in the water column) to form
a deep chlorophyll maximum37,68. Values in boxes represent the maximum
concentrations of dimethylsulphide reported in each of these habitats.
Question marks indicate the absence of published measurements.
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INSIGHT | REVIEW ARTICLES
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
49
74
180°
170°
°
160
170°
160
°
150
°
°
150
0°
14
14
0°
Chukchi
Sea
120
°
110°
Laptev
Sea
100°
100°
56
110°
This Review
East Siberian
Sea
Beaufort
Sea
°
120
55
0°
13
13
0°
94
54
Canadian Archipelago
91
16
Kara
Sea
73
48
Fram
Strait
Barents
Sea
60
°
75
°
70°
72
70
°
°
60
37
Greenland
Sea
°
50
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°
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°
Ban
Bay
70°
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°
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°
°
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°
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20°
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10°
20°
10°
0°
Bathymetric and topographic tints
–5,000 –4,000 –3,000 –2,500 –2,000 –1,500 –1,000 –500 –200
–100
–50
–25
–10
0
50
100
200
300
400
500
600
700
800
1,000
(m)
Figure 3 | Map of the Arctic showing the general locations (white boxes) of the studies where marine dimethylsulphoniopropionate and/or
dimethylsulphide measurements have been conducted. Numbers refer to the corresponding references. Background map adapted from ref. 95.
bacterial DMS consumption tends to increase with DMS production, maintaining DMS levels in a relatively narrow range between
0 and 20 nmol l–1 at the surface of the ocean30,31. DMS photolysis, a
secondary photochemical process mediated by chromophoric dissolved organic matter, could be an equally important sink for DMS
close to the surface in shallow mixed layers. Overall, it is estimated
that less than 10% of the DMS produced by plankton finds its way
to the atmosphere32.
Given that algae are the sole producers of DMSP, a first-order
relationship between algal biomass and DMS levels is often
observed. However, DMS production also varies with the physiological status of the algae. For instance, nutrient limitations
and high levels of ultraviolet light can stimulate DMS production33. Under high-ultraviolet conditions, DMS concentrations
may increase without marked changes in algal biomass. This
ultraviolet-induced uncoupling between DMS production and
algal biomass is thought to be responsible for the mismatch
between the seasonal peaks in phyto­plankton biomass and DMS
production commonly seen at low latitudes — a phenomenon
termed the ‘DMS summer paradox’34.
The dependency of DMS production on both ecological and
physiological factors translates into two main DMS regimes: a
‘bloom-dominated regime’ where DMS is closely linked to changes
in autotrophic biomass and speciation, and a ‘stress-forced regime’
where DMS production is uncoupled from changes in biomass and
reflects the physiological responses of the algae that produce DMS,
and the bacteria that produce and consume it, to light or nutrient
stress35,36. These two regimes are not totally disconnected from each
other, however; a stress-forced senescent phase can follow a bloomdominated regime37.
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693
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REVIEW ARTICLES | INSIGHT
Air
Lead
Ice
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
Ventilation
DMS
DMS
Ice algae
Water
Algal DMSP-lyases
Algal uptake
DMSPp
(ice algae and
phytoplankton)
Sinking of
cells or
faeces
Exudation
Grazing
Cell lysis
DMSPd
Bacterial
DMS-producing
enzymes
DMS
Free
DMSP-lyases
Bacterial
demethylation/
demethiolation
Photochemical
and biological
oxidation
DMSOd
DMSOp
(ice algae and
phytoplankton)
Reduction
Bacterial
consumption
Figure 4 | Schematic representation of the microbial cycling of dimethylsulphide in the ocean. DMSPp, particulate dimethylsulphoniopropionate;
DMSPd, dissolved DMSP in the water column; DMS, dimethylsulphide in the water column; DMSOp, particulate dimethylsulphoxide; DMSOd, dissolved
DMSO. Black arrows indicate pathways leading to DMS production, and red arrows indicate pathways competing with those leading to DMS production,
highlighting the buffering capacity of the DMS system in the ocean. DMSP and DMSO have been measured in both phytoplankton and ice algae and similar
biological processes affect their cycling. Direct emission of DMS from the bottom ice has never been demonstrated, but could probably take place during
the melting period.
Sea-ice algae
Low to null irradiance in winter keeps autotrophic activity at a
minimum in the Arctic, in spite of increasing evidence of measurable levels of heterotrophic activity over the shelf 38. Autotrophic
production starts in May–June in the bottom 5–10 cm of the sea
ice, when an increase in solar irradiance and a reduction in ice and
snow cover allow the development of microalgae in the skeletal
layer and the brine channels at the bottom of the ice39,40. Within
as little as two weeks, algal biomass in sea-ice brine channels can
reach very high levels in a relatively thin layer, with chlorophyll a
concentrations (a proxy for algal biomass) regularly reaching 200
μg l–1 (and up to 2,000 μg l–1). In comparison, chlorophyll a concentrations in the water column are <1 μg l–1 under the ice, and rarely
exceed 15 μg l–1 in surface water in ice-free conditions. The seasonal
contribution of these ice algal blooms to primary production is still
debated, but could represent 20–50% of net community production in the seasonally ice-free Arctic shelves and up to 90% of net
community production in the Arctic ice pack41,42. At the bottom of
landfast ice, the growth of algal biomass seems to be limited by the
availability of nitrate in the surface waters during the vernal growth
season43, although model results suggest that the rate of ice development could also control algal growth by regulating the exchange of
nutrients between the surface ocean and the bottom ice44. Processes
leading to the senescence of the sea-ice blooms include nutrient
limitation associated with the formation of a meltwater lens adjacent to the bottom of the ice, and ice algal loss due to tidal erosion
and ice and snow melt 40,44. The fate of sea-ice algae during the melt
period seems to vary depending on local hydrodynamical conditions. Following their release from the ice, the algae tend to sink
rapidly to the bottom of the water column45, although a significant
portion of the algal carbon remains afloat, probably due to vertical
mixing and zooplankton grazing 46.
Sea-ice algal blooms at the bottom of the ice are accompanied by
very high concentrations of DMSP and DMS. Early measurements
of particulate DMSP in first-year sea ice, carried out in Resolute
Passage in the Canadian Archipelago, revealed concentrations of up
12,000 nmol l–1 in the bottom 2 cm of the ice16. Subsequent studies confirmed these findings, reporting maximum concentrations
694
of DMSP of 15,000 nmol l–1 at the bottom of the ice in different
regions of the Arctic (Fig. 5)47–49. High concentrations have also
been detected in multiyear ice; during the 1994 Arctic Ocean
Section programme — the first major scientific crossing of the
Arctic Ocean — DMSP concentrations (particulate + dissolved) of
729 nmol l–1 (81 μg l–1 of chlorophyll a) were measured in July at the
North Pole in 200-cm-thick multiyear ice (Fig. 6).
DMSP is also found dissolved in sea-ice brines. Early attempts to
quantify the size of this dissolved DMSP pool suggested that it could
represent a large reservoir of DMSP (of up to 700 nmol l–1), similar
in magnitude to that of particulate DMSP (ref. 16). Although filtration artefacts may have led to an overestimation of the dissolved
brine pool, recent measurements using contemporary methods of
filtration confirm the presence of this reservoir at the bottom of the
ice (Fig. 5). The processes responsible for the formation, accumulation and turnover of brine dissolved DMSP are unknown. However,
extremely high concentrations (>200 nmol l–1) and turnover times
(>100 nmol l–1 d–1) of DMS have recently been reported in Antarctic
sea-ice brines, indicative of intense microbial cycling of these compounds50. Dissolved DMSP present in the ice could also be released
into the water column during the melt period, and become available to the underlying active, but carbon-limited, heterotrophic
bacterioplankton and converted into DMS (ref. 38).
Given the high concentrations of DMSP observed at the bottom
of sea ice in spring and summer, it comes as little surprise that DMS
is also present at high concentrations. Most sea-ice DMS measurements have been conducted in the Antarctic, where concentrations
have been found to reach 75 nmol l–1 offshore Prydz Bay, 60 nmol l–1
in the area of Adélie Land, 200 nmol l–1 in the Ross Sea and
1,430 nmol l–1 in the Weddell Sea50–53. The few published measurements of DMS in Arctic sea ice also indicate high concentrations,
especially on the shelves. During the 1994 Arctic Ocean Section
programme, DMS concentrations up to 29 nmol l–1 were measured in brines at the bottom of multiyear ice in the Central Arctic
(Fig. 6)54. DMS concentrations ranging from 0.3 to 769 nmol l–1
(with particulate DMSP concentrations of 50–2,150 nmol l–1) were
reported at the bottom of the ice in the Beaufort Sea during the
vernal ice algal bloom55. Finally, high concentrations of DMS (up
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Melt ponds and under-ice blooms
In spring and summer, melting snow and liquid precipitation create
ponds at the surface of the sea ice. These ponds can cover up to 80%
of the sea-ice pack in summer, and are expected to become more
widespread in a warmer climate56,57. During the 1994 Arctic Ocean
Section programme, a survey of 11 melt ponds located between
the Chukchi Sea and the North Pole revealed DMS levels ranging
from less than 0.05 to 2.2 nmol l–1 (Fig. 6)58. Very low levels of DMS
have also been reported in melt ponds in the ice pack north of the
Greenland Sea56. In spite of these first limited indications of rather
low concentrations, melt ponds may represent the sole direct source
of DMS to the air over those parts of the ice pack situated away from
leads and the ice edge. A more thorough survey is needed to assess
their importance as sources of DMS.
Melt ponds and their areal extent are of particular interest owing to their proposed link to the development of under-ice
phytoplankton blooms13. In spring and summer, phytoplankton
blooms may develop under the ice if light conditions are adequate.
The first mention of such under-ice phytoplankton blooms dates
from the 1990s, but it is only recently that the importance of these
blooms has been fully recognized59,60. In 2011, a massive phytoplankton bloom was documented beneath the ~1-m-thick firstyear sea ice on the Chukchi Sea continental shelf 13. This bloom was
apparently favoured by the development of melt ponds above the
ice, which acted as lenses, increasing irradiance under the ice14,61.
The potential for DMS production by these under-ice phytoplankton blooms has yet to be determined. By consuming the inorganic
nutrient pool earlier in the season, under-ice algal blooms could
limit nutrient availability for other phytoplankton blooms located
on the ice edge62. Keeping in mind that water under the ice, and
the blooms it carries, are most likely to come into contact with the
atmosphere through leads or at ice edges, stress-induced DMS production is expected to result when these low-light acclimated cells
suddenly come into contact with full sunlight.
In some areas of the Arctic, centric diatoms of the genus
Melosira (for example, M. arctica) can form large ice-attached
mats at the bottom of the ice (the ‘sub-ice’ environment). Very
high concentrations of chlorophyll a (up to 296 μg l–1) and DMSP
(particulate and dissolved concentrations combined reaching up
to 1,888 nmol l–1) were detected in two such mats during the 1994
Arctic Ocean Section (Fig. 6). Conditions leading to the formation of these mats are not fully understood, rendering it difficult
to predict how projected changes in sea-ice extent and properties
will affect their distribution63. However, the ongoing thinning of
the sea ice and the concomitant increase in melt pond cover in
the eastern-central Arctic Basin has enhanced the development of
M. arctica mats64. The fate of the DMSP packed into these mats,
and whether it is metabolized into DMS and released into the
atmosphere, remains unclear.
Ice-edge blooms
Ice-edge phytoplankton blooms are near ubiquitous around the
Arctic65. The mechanisms responsible for the formation of these
blooms are still being investigated, but the increase in the vertical
stability of the water column associated with sea-ice melt plays a key
role66,67. Sea-ice melt forms a thin (2–10 m) lens of buoyant, relatively
fresh water sitting just under the ice68. This well-illuminated meltwater lens traps ice algae recently released into the water column,
Box 1 | Probing the role of bacteria in DMS production
a
Contribution to the total incorporating
prokaryote cells (% of DAPI Mar + cells)
to 2,000 nmol l–1) have been detected at the bottom of the ice in
the Canadian Archipelago at the end of the ice algal bloom (Fig. 5).
These results confirm the presence of extremely high levels of DMS
in brines at the base of the sea ice on the Arctic shelf in spring and
summer that could readily be released to the atmosphere during the
melt period.
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60
40
20
0
Gammaproteobacteria
Betaproteobacteria
Roseobacter
Non-Roseobacter
Alphaproteobacteria
40
60
20
Contribution to the prokaryote
community (% of DAPI-stained cells)
0
b
100
% of DMSP converted to DMS
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
80
60
Low sulphur demand
40
20
Moderate sulphur demand
High sulphur demand
0
DMSP concentration (arbitrary units)
Bacteria play a pivotal role in DMS production. They both release
DMS from DMSP and consume DMS. Results from DMSP bacterial consumption experiments conducted with radiolabelled tracer
35
S-DMSP (a) show that clades of heterotrophic bacteria identified
in the Canadian Archipelago consume DMSP (as indicated by per
cent contribution to 35S-DMSP-incorporating cells, y axis) in proportion to their abundance (DAPI, 4’,6-diamidino-2-phenylindole;
Mar, microautoradiography; part a reproduced with permission
from ref. 73). DMSP consumed by bacteria can then be routed
through either one of two competing pathways: (1) the cleavage
pathway (DMSP-lyases and the ‘Ddd’ enzymes (DMSP-dependent
DMS enzymes identified so far: DddY, DddD, DddL, DddP, DddQ,
DddW)) leading to the formation of DMS, and (2) the demethylation/demethiolation pathway leading to the production of methanethiol and other products96.
Experiments conducted in warm and temperate waters with
radio-labelled 35S-DMSP show that bacteria switch from the
demethylation/demethiolation pathway to the production of DMS
when their sulphur demand is satisfied (b; reproduced with permission from ref. 25). Recent studies in Arctic waters indicate that
bacteria use DMSP mostly as a carbon source, resulting in conversion efficiencies of DMSP into DMS (DMS yields) of up to 30%
(refs 73,74). DMS seems to be used as an auxiliary sulphur source
by the same clades that consume DMSP97. The few studies reporting measurements of bacterial DMS production and consumption
often reveal a near-equilibrium between the two rates, which tends
to keep DMS levels within a rather narrow range in nature30,68.
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a
20
c
100
1,000
10,000
Concentration (nmol–l)
10
2
5
0
800
600
400
200
0
d
e
2,000
1,800
1,600
1,400
1,200
1,000
800
300
360
220
180
140
6
5
4
3
2
1
0
100
80
60
40
20
70
75
80
Latitude (°N)
85
90
0
2.0
1.5
1.0
0.5
0
30
20
10
0
10
8
6
4
2
DMS (nmol l–1)
696
4
DMSPt (nmol l–1)
along with marine phytoplankton, which can use the reservoir of
nutrients formed or replenished through upwelling, advection,
tides, eddies and other processes during the dark winter. Blooms
at the ice edge may also be fuelled by wind-generated upwelling of
nutrient-rich deep water 69.
Ice-edge blooms are prolific producers of DMS. In the Arctic,
DMS peaks at ice edges have been reported in spring and summer in the Greenland Sea–Fram Strait area (10 nmol l–1), in the
Fram Strait (18 nmol l–1), in the Barents Sea (22 nmol l–1) and in
the Chukchi Sea (12 nmol l–1)37,56,58,68. The build-up of these DMS
pools in surface water results from several, often ill-defined, abiotic and biotic processes. In most cases however, the observations
point towards the prevalence of a bloom-dominated regime, with
DMS production strongly correlated with algal biomass (for example, refs 58,68). However, in the Barents Sea, high net DMS production has been associated with both a decaying diatom bloom
found close to the ice pack and with a Phaeocystis bloom thriving
further offshore37.
The cycling of sulphur compounds at the ice edge of the Greenland
Sea was studied in some depth in a recent sampling campaign68.
The colonial form of Phaeocystis pouchetii dominated the ice edge,
where DMSP and DMS concentrations reached 164 nmol l–1 and
8 nmol l–1, respectively. DMS concentrations were positively correlated with DMSP, which in turn was correlated with P. pouchetii
biomass, indicative of a bloom-dominated regime. However, high
concentrations of DMS were also detected in blooming stations
influenced by ice melt (~6.4 nmol l–1 d–1), suggesting that the stimulating effect of light stress on DMS production and its inhibitory
effect on bacterial DMS consumption, also measured, contributed
to the high concentrations measured in the shallow upper mixed
layer at the ice edge. This is the best-documented example so far
showing how the bloom-dominated and stress-forced regimes may
15
2.5
DMSPt (nmol l–1)
Figure 5 | Vertical distribution of dimethylsulphide (DMS) in a sea ice
core from the Arctic Canadian shelf and associated concentrations of
particulate and dissolved dimethylsulfoniopropionate (DMSP) at the
bottom of the ice. Concentrations of DMS (circles), total DMSP (square)
and dissolved DMSP (triangle) within ice cores collected in the Resolute
Passage between Cornwallis and Griffith islands, northwest of Resolute
Bay, Nunavut (74° 43’ N, 95° 33’ W), on 4 June 2012. Note log scale for
concentrations of sulphur compounds on x axis. All samples were collected
in ice cores under high snow cover (>20 cm).
90
75
60
45
30
15
0
Chlorophyll a (μg l–1)
10
0
Chlorophyll a (μg l–1)
1
6
20
DMS (nmol l–1)
120
25
DMSPt (nmol l–1)
100
8
Chlorophyll a (μg l–1)
80
180
140
DMS (nmol l–1)
60
220
Chlorophyll a (μg l–1)
b
360
DMSPt (nmol l–1)
Depth (cm)
40
110
100
90
80
70
60
50
40
340
300
Ice coverage (%)
Ice thickness (cm)
0
0
Figure 6 | Latitudinal variations in sea-ice conditions, dimethylsulphide
(DMS) and related variables during the 1994 Arctic Ocean Section
expedition from 26 July to 26 August 1994 on board the USCGC
Polar Sea. a, Sea-ice cover (white symbols) and thickness (black
symbols). b–e, Concentrations of chlorophyll a (black symbols), total
dimethylsulphoniopropionate (DMSPt; particulate + dissolved) (grey
symbols) and DMS (white symbols) in melt ponds (b), in the bottom
2–4 cm of the sea ice (c), in mats of Melosira arctica suspended under the
sea ice (d) and in the first metre of the water column under the ice (e). The
general location of the transect is shown in Fig. 4 (ref. 54).
combine, leading to high net production of DMS at the ice edge.
The authors concluded that any change in environmental conditions
that modifies the strength, duration and extent of the Phaeocystis
bloom at the ice edge would have a strong effect on sulphur biogeochemistry in the region, and on the role of the Arctic as an atmospheric DMS source.
Sea-ice algae released into the water column during the melt
period can substantially add to the DMSP and DMS peaks found
at the ice edge around the Arctic, according to a model simulation
of coupled nutrient–sulphur cycling in the Pan-Arctic70. In another
model study, a large release of ice algae was suggested to explain the
high DMS values observed in the marginal ice zone in the southern part of the Barents Sea10. However, field observations to support
this contribution are lacking, and the validation of the ecological
components of Arctic Ocean physical models is still in its infancy 71.
Nevertheless, these results confirm the common presence of high
DMS concentrations and production at ice edges around the Arctic,
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© 2013 Macmillan Publishers Limited. All rights reserved
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
probably resulting from the prevailing high rates of primary production, the common occurrence of high DMSP algal producers, the
potential release of ice algae and ice DMSP into the water column, as
well as the influence of ultraviolet-light on plankton DMS production and bacterial DMS consumption.
Expansion of the seasonal ice-free zone
INSIGHT | REVIEW ARTICLES
Box 2 | Seeking an atmospheric DMS signal
Measurements of the concentrations of methanesulphonic
acid — a specific photooxidation product of DMS in the atmosphere and found in ice cores collected in continental glaciers —
have been used to capture temporal changes in DMS emissions in
polar regions over interannual, decadal and glacial–interglacial
time periods. In the Arctic, the relationship between total sea-ice
extent north of 70° N and atmospheric methanesulphonic acid
concentrations was recently examined at three coastal locations:
Alert, Nunavut, period 1980–2009; Barrow, Alaska, period 1997–
2008; and Ny-Ålesund, Svalbard, period 1991–2004 (ref. 98). An
increase in late spring atmospheric methanesulphonic acid concentrations was apparent at all three sites from the year 2000,
coincident with the northward migration of the seasonal ice-free
zone. High methanesulphonic acid concentrations measured in
a Svalbard ice core were also found to be associated with warm
sea surface temperature and reduced sea-ice extent between 1920
and 1996 (ref. 99). It is of interest to note that variations in the
winter maximum sea-ice extent also appear to influence DMS
production. Indeed, the higher methanesulphonic acid concentrations measured before 1920 in the Svalbard ice core can be
explained by an increase in meltwater production from the more
extensive winter sea-ice cover at that time100. In contrast with the
observations from these coastal stations, no systematic year-toyear change was observed in summer aerosol concentrations in
the central Arctic between 1991 and 2008 (ref. 101).
Signs of a relationship between sea-ice extent and DMS production in the seasonal ice-free zone can be seen on the glacial–
interglacial time scale in the Arctic. Indeed, the analysis of ice
cores from the Greenland glaciers reveals higher atmospheric
methanesulphonic acid concentrations during warmer climates,
characterized by minimal sea-ice cover 102.
Although evidence for an increase in the concentration of
atmospheric DMS in the central (as opposed to the coastal)
Arctic during the past two decades is equivocal, the atmospheric
measurements of methanesulphonic acid and aerosols from the
coastal regions tend to support the observations and models suggesting that a reduction in seasonal ice cover will result in higher
DMS emissions. However, many other factors may explain these
relationships, including changes in air mass circulation and
atmospheric chemistry. It should be noted that the use of methanesulphonic acid as a proxy for changes in DMS ocean emissions and sea-ice extent is debated103.
The seasonal ice-free zone increases as the summer sea-ice
minimum recedes. Determining the biogeochemical characteristics
of this new ice-free ocean is probably the most challenging question
that polar researchers have to address.
Observations from both the Atlantic and Pacific sectors of the
Arctic suggest that DMS production could remain high throughout the entire seasonal ice-free zone from May to August. In the
Fram Strait, for instance, the potential for high DMS production
was reported for the whole seasonal ice-free zone during an expedition in 199156. In this case, DMS and chlorophyll a levels were not
correlated over the large areas and different seasons covered, suggesting that physiological and ecological interactions controlled the
cycling of sulphur. In the Barents Sea, high primary productivity
and DMSP concentrations were reported throughout the seasonal
ice-free zone in spring and summer in 1993, 1998, 1999 and 200172.
In the Northern Baffin Bay–Canadian Archipelago region, DMS
levels also remain relatively high (4–7 nmol l–1) between May and
September, before decreasing to below 0.8 nmol l–1 in October, and
to 0.3 nmol l–1 in November in the Beaufort Sea47,73,74. In support
of these oceanographic measurements, high levels of DMS have
been detected in the atmosphere over Svalbard during the summer months; weekly variations in atmospheric DMS concentrations
were highly correlated with variability in chlorophyll a concentrations in surrounding waters75.
Most of the features characterizing the distribution of DMS in
the Arctic seasonal ice-free zone have been captured in a numerical model76. High monthly concentrations of DMS in the seasonal
ice-free zone were predicted in July (~5.0 nmol l–1) and August
(~3.0 nmol l–1), and lower levels in September (~1.0 nmol l–1) and
October (~0.5 nmol l–1). Mean sea-ice cover and surface nitrate concentrations were found to be important predictors of surface seawater DMS concentrations. Altogether, observation and model results
suggest that DMS concentrations may remain relatively high (above
4 nmol l–1) for almost five months of the year in the seasonal ice-free
zone around the Arctic.
Current DMS models consistently project an increase in DMS
emissions with an increase in the extent of the seasonal ice-free
zone70,76,77. For example, annual DMS fluxes are projected to increase
by more than 100% in the Barents Sea region at 70–80° N in a scenario in which carbon dioxide levels are tripled by the year 2080, due
to a significant reduction in ice cover, combined with a rise in sea
surface temperatures and a decrease in mixed layer depth10. A noteworthy consideration, however, is that this model does not take into
account changes in DMSP and DMS production that might result
from increased ice melt. Increased concentrations of DMS late in the
summer could prove particularly important from a climate perspective, as this is the time of the year when DMS emissions are believed
to be more effective at generating cloud condensation nuclei, and
thereby increasing cloud albedo and cooling the climate5,78. As such,
increased DMS emissions in late summer and early autumn could
speed up the formation of sea ice in the autumn.
It is clear that high DMS concentrations in the Arctic Ocean
are not restricted to the ice edges, but extend over most of the
seasonal ice-free zone in spring and summer. But whether model
projections of increased DMS production in the future hold will
depend on whether similar conditions prevail in the progressively
expanding seasonal ice-free zone. A partial answer can be found in
a comparison of years characterized by the high and low residual
end-of-summer ice-pack surface. In the Beaufort Sea, the northward migration of the ice edge between 1994 (high residual ice
pack) and 2008 (low residual ice pack) resulted in a shift in the composition of the phytoplankton assemblage in the seasonal ice-free
zone, with lower phytoplankton biomass and production during
the low ice year 79. The reduction in productivity was attributed to a
reduction in nutrient supplies, in turn attributed to a freshening of
surface waters due to increased ice melt and river discharge. These
findings are consistent with the observed decrease in the mean cell
size of phytoplankton in the same region, also attributed to a reduction in nutrient supplies80. In the Fram Strait, the low seasonal ice
cover of 2007 resulted in a seasonal ice-free zone entirely dominated
by P. pouchetii, a prolific DMSP and DMS producer, whereas previous studies conducted in high ice conditions reported the presence
of diatoms at the ice edge and P. pouchetii further offshore68.
As the seasonal ice-free zone grows in size, climate-induced
changes in ocean circulation may also bring new species to the Arctic
deep basin. Indeed, blooms of the Atlantic coccolithophore E. huxleyi,
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697
© 2013 Macmillan Publishers Limited. All rights reserved
REVIEW ARTICLES | INSIGHT
a strong DMS producer, were spotted in the Northern Barents Sea in
August 2003, and there are signs of a northward migration of E. huxleyi in the Pacific sector of the Arctic81–83. These few studies show that
the speciation characteristics of an expanding seasonal ice-free zone
could differ from those observed at present, with a tendency towards
the establishment of strong DMS producers in both the Atlantic and
Pacific sectors of the Arctic. Whether the observed shift in species
composition compensates for the reduction in biomass reported by
other studies remains to be seen, and will depend on the main drivers
of DMS emissions as sea ice retreats.
Removing the lid
The Arctic is changing at an alarming rate. As a result of its remoteness, key information necessary to understand sulphur cycling
in the region, and how it might change in a high carbon dioxide
world, is still lacking. Although DMS measurements are limited,
some general patterns are emerging. Observations and model
results consistently show high DMS concentrations at ice edges, due
to both ice algae and marine phytoplankton. High concentrations
are also apparent over large parts of the seasonal ice-free zone in
spring and summer, a conclusion supported by ice-core measurements of methanesulphonic acid, a proxy for DMS in the atmosphere (Box 2). Whether this band of high DMS concentrations is
a common feature around the Arctic ice pack, as recently reported
for phytoplankton biomass65, remains to be seen. Given that a very
small portion of the Arctic shelves has been surveyed so far, with little data for the Kara, Laptev and East Siberian seas, and the potential
heterogeneity in sea-ice dynamics, river runoff, wind regimes and
plankton taxonomy, large-scale extrapolation of current observations would be risky.
Independent oceanic and atmospheric observations, together
with model results, suggest that the production and emission of
DMS will increase in the Arctic as seasonal sea-ice cover recedes.
This conclusion makes sense, given that the sea-ice pack limits DMS
ventilation for most of the year and that DMS concentrations under
the ice in spring and summer are generally well above those in the
atmosphere. In these circumstances, removing the sea ice ‘lid’ will
almost certainly generate a new ocean–atmosphere DMS flux. The
intensity of this new ocean–atmosphere flux is more difficult to predict, however, as it will depend on the biogeochemical characteristics of this new open ocean. Preliminary results suggest that in the
central Arctic, the retreat of the ice cover will give way to a highly
stratified, nutrient-poor ocean characterized by relatively low levels of phytoplankton biomass and an algal community dominated
by small cells. Under this scenario, DMS production will depend
on the taxonomic composition of the plankton community, that is,
the abundance of strong DMSP producers with DMSP-lyase activity, the composition of bacterial assemblages, and the physiological
response of the main DMS producers to stresses such as high levels
of ultraviolet light and nutrient limitation. Deep chlorophyll maxima — a common feature of the present-day Arctic open waters that
has been associated with high DMS concentrations — are expected
to form and persist in this stratified ocean37,68,84. As deep chlorophyll
maxima are actually relatively shallow (10–40 m) in the Arctic,
DMS that accumulates in these layers could escape to the atmosphere during storms, as reported at lower latitudes85.
Although current DMS models tend to agree in their forecasts
of increasing future production, the representation of the microbial
processes in these models remains simplistic. Furthermore, they
overlook the individual or synergistic effects that stressors could
have on DMS production. Ocean acidification figures prominently
among the stressors that might affect DMS production in Arctic
waters, as this ongoing process is exacerbated in the fresh, cold,
carbon-dioxide-rich waters of the Arctic, and has been linked to a
potential reduction in DMS production86. The effects that enhanced
698
NATURE GEOSCIENCE DOI: 10.1038/NGEO1910
wind turbulence — in the absence of the sea-ice lid — will have
on DMS emissions are also unclear. However, increased turbulence
could both deepen the upper mixed layer where phytoplankton
assemblages reside, and increase wind-driven sea spray and DMS
ventilation. Finally, DMS flux from the vestigial summer ice pack is
also expected to grow in a warmer climate, owing to improved connectivity between inter-brines channels, and the expansion of melt
ponds and leads.
It is in the relatively pristine atmosphere of polar regions that
oceanic DMS emissions are expected to contribute the most to new
particle formation events in the atmosphere, and so influence climate. It is also in polar regions that the most diverse biota producing
dimethylsulphide are encountered. Understanding how global warming and the ongoing reduction of seasonal sea-ice cover will affect
the strength of these different sources is challenging. Ascertaining
the future of DMS emissions in the Arctic will require more comprehensive sampling of the different regions of the Arctic, and a better
understanding of the key processes governing DMS production in
and around the sea ice, and of the sensitivity of these processes to
projected changes in the Arctic environment.
Methods
Arctic ice-core measurements of DMS and DMSP in Fig. 5. Ice-core sections
for the analysis of DMS samples were collected using gas-tight syringes87. The ice
was allowed to slowly thaw (temperature inside the syringes never exceeded 5 °C)
before it was transferred into a purge and trap system for sparging and extraction
with ultra-high purity He. Gaseous DMS was trapped into inlet liner cartridges
filled with polymer TENAX TA 60/80 mesh88, stored at –80 °C and subsequently
analysed by gas chromatography 89. For DMSP samples, two ice-core sections (bottom 3 cm) were extracted, pooled in a dark isothermal container and melted in
0.2-μm-filtered sea water to minimize osmotic stress of the microbial community 90.
DMSP samples included total and dissolved DMSP; dissolved DMSP was sampled
following the small-volume gravity drip filtration technique21. DMSP samples were
preserved with sulphuric acid and later analysed by gas chromatography following
purging and cryotrapping 89.
Sea-ice conditions, DMS and related variables across the Arctic Ocean in Fig. 6.
Details on the 1994 Arctic Ocean Section expedition are in ref. 58. At every ice station, ice cores were taken with a SIPRE ice corer (7.5 or 10.5 cm internal diameter).
The bottom 2–4 cm of ice was cut and melted in surface seawater filtered through
0.2 μm polycarbonate membranes to minimize osmotic stress90. Chlorophyll a and
DMSP concentrations determined in the ice were corrected for the dilution effect
of added sea water. Samples from the sub-ice (M. arctica mats) were collected by
scuba divers, using a 2.2 l syringe sampler; the samples were free of ice. Melt ponds
were sampled when present with a clean bucket. Water column samples were collected with a rosette equipped with 10 l Niskin bottles. Gaseous DMS was trapped
into inlet liner cartridges filled with TENAX88 and analysed onboard by gas chromatography 89. DMSP samples were preserved and later analysed by gas chromatography following purging and cryotrapping 89.
Received 22 January 2013; accepted 8 July 2013;
published online 29 August 2013
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Acknowledgements
I thank M. Lizotte (Québec-Océan, Université Laval, Québec, Canada), M. Gosselin
(Institut des sciences de la mer de Rimouski, Université du Québec à Rimouski, Québec,
Canada), M. Scarratt and S. Michaud (Maurice Lamontagne Institute, Department
of Fisheries and Ocean Canada, Mont-Joli, Quebec, Canada), J. Abbatt (University of
Toronto, Toronto, Ontario, Canada) and R. Leaitch (Environment Canada, Downsview,
Ontario, Canada) for providing comments on early versions of this manuscript. I thank
M. Gosselin (Institut des sciences de la mer de Rimouski, Université du Québec à
Rimouski, Québec, Canada), N. Simard and S. Michaud (Institut Maurice-Lamontagne,
Mont-Joli, Québec, Canada), S. Sharma (Environment Canada, Downsview, Ontario,
Canada), L. Barrie (Department of Geological Sciences, Stockholm University,
Stockholm, Sweden) and T.S. Bates (School of Oceanography, University of Washington,
Seattle, Washington, USA) for releasing unpublished data from the 1994 Arctic Ocean
Section programme (Fig. 6), and M. Gourdal for releasing data from the Arctic-Ice
Covered Ecosystem project (Fig. 5).
Additional information
Reprints and permissions information is available online at www.nature.com/reprints.
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Competing financial interests
The author declares no competing financial interests.
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