Dissolved dimethylsulphide, dimethylsulphoniopropionate and dimethylsulphoxide in western Mediterranean waters

Deep-Sea Research II, Vol. 44, No. 34, pp. 92’%950. 1991 0 1997 Elsevier Science Ltd All rights reserved. Printed in Great Britain 09674645/97 $17.00 + 0.00

PII: SO9674645(96)0009!%9

Dissolved dimethylsulphide, dimethylsulphoniopropionate and dimethylsulphoxide in western Mediterranean waters RAFEL

SIMb,*_F

JOAN

0.

GRIMALT*

and JOAN

ALBAIGI%*

(Received 16 February 1996; accepted 26 April 1996)

Abstract-Spring-summer concentrations of the three main dissolved dimethyl sulphur species dimethylsuphide dimethylsulphoniopropionate and (DMSSd), (DMS), (DMSPd) dimethylsulphoxide (DMSO), have been determined in western Mediterranean Sea water with some spatial and temporal resolution. Depth profiles showed that the three DMSSd were mostly confined to the euphotic layer. In surface waters, DMSO was generally the dominant DMSSd regardless of the site and the season. Concentration averages resulted in a DMS:DMSP,:DMSO proportion of I: 1: 6 (2.9: 3.0: 16.6 nM). DMSSd concentrations exhibited a great variability, but were higher on the continental shelf than in open seawaters, as were chlorophyll concentrations. Some hot spots with the highest levels were identified off the main continental outflows. None of the DMSSd correlated significantly with chlorophyll. In open seawaters (water column depth > 200 m) DMS increased as chlorophyll declined between April and July. This was attributed to changes in the biological community from spring development to summer decay and ecological succession. The temporal variation of the three DMSS& suggests that they are subject to a tight cycling of production and consumption where the composition of the entire planktonic community, as well as its physiological state, play a significant role. A similar conclusion was achieved from the study of the DMSSd concentrations in a transect between oligotrophic and eutrophic waters in the top NW area. Finally, the western Mediterranean has been assessed as a source of atmospheric sulphur. The moderate DMS emission flux estimates (mean: 5.4 pmol rnp2 day-‘), together with the moderate DMS surface concentrations, were consistent with the low productivity of the Mediterranean Sea. 0 1997 Elsevier Science Ltd.

INTRODUCTION Dimethylsulphide (DMS) is the most abundant volatile sulphur compound in surface seawater, occurring at concentrations high enough to account for the major part of the sulphur flux from the oceans to the atmosphere (Lovelock et al., 1972; Andreae, 1990). Once in the air, DMS undergoes oxidation to yield sub-micron size sulphate and sulphonate particles that contribute to the acidity of aerosols and serve as precursors of tropospheric cloud condensation nuclei (Charlson and Rodhe, 1982; Charlson et al., 1987). Since the suggestion that DMS may play a major role in global climate regulation through affecting the radiative properties of marine clouds and hence the Earth’s albedo (Charlson et al., 1987), many efforts have been devoted to study both the global DMS distribution in surface water and the biogeochemical processes that control its concentration and emission to the atmosphere. Global DMS inventories have been constructed by gathering and modelling the existing

* Department of Environmental Chemistry (CID-CSIC), t E-mail: [email protected]; fax: + 34-3-2045904. 929

Jordi Girona,

18,08034

Barcelona,

Catalonia,

Spain,

930

R. Sim6 et al.

experimental datasets (Bates et al., 1987, 1992; Cooper and Matrai, 1989; Erickson et al., 1990; Andreae, 1990). These datasets have been compiled from a great number of DMS measurements that cover worldwide coastal, shelf and open ocean areas. The ubiquity of DMS in seawater has been evidenced as a consequence of this large measurement effort. However, DMS occurrence is spatially and seasonally variable, especially in temperate and boreal regions, where surface concentrations can vary by as much as two orders of magnitude between summer levels in coastal areas (high) and winter levels in remote areas (low) (Bates et al., 1987; Turner et al., 1988; Leek et al., 1990; Nguyen et al., 1990; Gibson et al., 1990; Berresheim et al., 1991). This large DMS variability introduces uncertainity in the global estimates of the emission fluxes to the atmosphere. Biological activity is responsible for DMS production within the water column, where it is removed by biological consumption and some abiotic loss mechanisms (reviews in Taylor and Kiene, 1989; Wakeham and Dacey, 1989; Andreae, 1990; Kiene, 1993). However, these processes are still far from being fully understood. Dimethylsulphoxide (DMSO) has been identified to be a major pool of dissolved dimethyl sulphur in seawater (Andreae, 1980a; Lee and Wakeham, 1989; Gibson et al., 1990; Ridgeway et al., 1992; Bates et al., 1994). Its implication in the marine cycling of DMS has been anticipated (Wakeham and Dacey, 1989; Taylor and Kiene, 1989; Malin et al., 1992; Kiene, 1993; Liss et al., 1993; Bates et al., 1994; Simb et al., 1995). However, information on DMSO distribution and dynamics so far is too scarce and limited to confirm this implication or to evaluate its possible significance. Temperate coastal seas and near-shore oceanic areas in northern Europe have been revealed to be significant seasonal sources of atmospheric sulphur on a regional scale, affecting the summer sulphur balance over the neighbouring land masses (Fletcher, 1989; Turner et al., 1989; Leek and Rodhe, 1991). The Mediterranean is one of the most characteristic European coastal seas. It is a large semi-enclosed basin where the ratio between shore development and sea surface is high. The impact of continental activities and discharges upon the Mediterranean’s composition and processes has been intensively investigated for several decades and is currently in progress (e.g. this issue). In addition, the year-round oligotrophy and low productivity of open Mediterranean waters, and the formation of a deep chlorophyll maximum during summer stratification, which is of oceanic gyres, give to this sea the comparable to the “typical tropical structure” characteristics of a meso-scale system that allow the study of phenomena of general oceanographic interest (Margalef, 1985; Estrada et al., 1993). Nevertheless, in comparison to north European coastal seas, the Mediterranean has received little attention as regards the distribution and emission of biogenic sulphur. In the present study, we report spring-summer concentrations of DMS, dissolved DMSP, and DMSO in the western Mediterranean, including shelf and open waters. This paper provides one of the first comprehensive descriptions of the joint spatial-temporal occurrence of the dissolved dimethyl sulphur species (DMSSd) in the open sea.

METHODS Sampling

Sampling was carried out during four cruises: aboard the R.V. Hesprides in the Catalan Sea (June l-6 and 22-29,1993), the R.V. Discovery in the NW basin and the shelf of the Gulf of Lions (July 17-August 2, 1993) the R.V. Garcia de1 Cid in the Catalan Sea (April 2628,

Dissolved DMS, DMSPd and DMSO

931

1994) and in the Catalan Sea and NW basin (July 15-21, 1994). Water samples from sea surface and 5-1000 m depths were collected with Niskin bottles attached to a CTD hydrocast system. In April 1994, surface samples were taken from approximately 3 m water depth using the ship’s clean pump supply. Aliquots were taken in sililated, dark glass flasks, with no headspace, and preserved at 4°C. The analyses were performed immediately onwhere aliquots were filtered board, except in the Discovery cruise (samples MAl-MDl), through GF/F, acidified and frozen at -20°C in firmly closed polyethylene flasks until analysis in our laboratory in Barcelona. Tests with both standards and real samples revealed that no DMSPd or DMSO was lost during storage. DMS concentrations in samples MAlMD1 have to be taken as approximate values because they have been corrected for 50% losses which occurred during freezing storage.

Analytical DMS measurements in water were performed following a modified method based on a cryo-trapping gas chromatographic technique described elsewhere (Simo et al., 1993). Subsample volumes of 25 or 50 ml were taken with a Teflon tube attached to a glass syringe. The tube was then replaced with a filter unit holding a 2.4 cm GF/F filter (Whatman, Maidstone, U.K.) connected to a needle. The collected volumes were injected with this filtration unit into the purge device through a Teflon-faced septum by application of a very gentle pressure. The purge device consisted of a sililated glass flask provided with a Teflon-capped side-port and a porous glass frit at the inlet of the sparging gas. Volatile sulphur compounds (VSC) were stripped by water sparging with nitrogen (ultra-high purity) at a flow rate of 150 ml min- ’during 20 min, and cryo-trapped at the temperature of liquid argon. A Nafion dryer (Perma-Pure Inc., Toms River, NJ, U.S.A.) was located between the purge flask and the cryogenic trap to avoid ice blocking in the trap loop. Once sparging was completed, the cryo-trap was connected to the gas chromatograph by means of six port valves. Injection was performed by quickly placing the loop in hot water. Volatiles were still cryo-focused in a second, smaller cryogenic trap before entering the column in order to avoid peak widening. The gas chromatograph was especially designed for the field analysis of VSC (Haunold et al., 1992). It is equipped with a flame photometric detector and a 2 m x l/8” Teflon column filled with Carbopack BHT-100 (Supelco, Bellefonte, PA, U.S.A.). Base line separation of DMS from other VSC (CS2, DMDS, CH$H, COS, H$) was achieved using a temperature program from 50°C to 100°C and a carrier gas flow rate of 20 ml min-‘. Peak areas were recorded with a Hewlett-Packard 3393A integrator. Calibration was performed by injecting known amounts of gaseous DMS released by a permeation tube (VICI Metronics, Santa Clara, CA, U.S.A.) and diluted with a nitrogen flow in a steady-temperature (30 +O.l’C) permeation chamber. Interpolation on linear log(peak area) - log(DMS mass) plots allowed quantification. The detection limit for 50 ml water samples was 0.05 nM. Mean relative standard deviation for real water sample replicates was 6%. Dissolved DMSP (DMSPd) was determined as DMS by the cold alkali treatment method (Dacey and Blough, 1987; Turner et al., 1988). After volatiles were removed from filtered water by sparging, the samples were transferred to sililated dark glass bottles and brought to the brim with milliQ water. Then NaOH was added to set the pH to - 13. The sample was left to react at room temperature for 6 h in order to achieve the full transformation of DMSP into DMS. After neutralising with HCl, the newly formed DMS was stripped from the solution and measured as described above. Bates et al. (1994) mention technical

932

R. Simb et al

difficulties in determining DMSP because the partitioning between dissolved and particulate DMSP is very dependent upon filtering pressure. For this reason we applied a very gentle pressure when manually filtering the initial sample. The relative standard deviations obtained with filtration replicates of single samples (< 10%) were the same as those calculated with replicates of standard solutions, confirming a good reproductibility of our DMSPd measurements. Aqueous DMSO was determined by reduction to DMS with borohydride (Andreae, 1980b) in a further step. Once DMSPd was eliminated via DMS formation and stripping, one pellet (45 mg) of NaBHa was added to the neutralised sample in the purge flask and left to react for 6-15 min. During this reaction time the purge device was connected to the cryogenic trap for the pre-concentration of the stripped volatiles. The application of a gentle flow (max. 40 ml min-‘) of the sparging gas during the first minutes after NaBH4 addition allowed the slow dissolution of borohydride and its effective reaction with DMSO. When the reaction was completed, 0.2 ml of HClZ5% were added and sparging proceeded at 150 ml min-’ for 20 additional min. DMS was trapped and measured as described above. A relative standard deviation of < 20% was calculated with replicates of standard solutions. Since DMSP is also decomposed to DMS by borohydride (Andreae, 1980b; Simo et ul., 1996) analysis of DMSO necessarily must be performed after quantitative removal of DMSP. Tests with standards (DMSP HCl: Research Plus, Inc., Bayonne, NJ, U.S.A.; DMSO: Carlo Erba, Milano, Italy) were carried out to ensure the lack of interferences between the two species. No interferences other than DMSP have been observed in the borohydride reduction of DMSO (Andreae, 1980b; Simo, unpublished). Blank controls of milliQ water treated with the reagents used in these procedures were also performed. No DMS peak was observed after alkali treatment. A small DMS signal (equivalent to a concentration lower than 0.3 nM) sometimes appeared after addition of NaBH4 to blanks. However, the data are reported as measured, without blank subtraction for quantification. More analytical details are given elsewhere (Simo et ul., 1996). Chlorophyll a was measured by fluorometry in acetone extracts (Yentsch and Menzel, 1963).

RESULTS Generalpatterns of surface concentrations The location of the sampling sites in the western Mediterranean is indicated in Figs 1 and 2, together with the ranges of surface DMS concentrations. DMS and chlorophyll were analysed in a total of 54 stations: 34 located in the open sea area (water column depth > 200 m) and 20 on the continental shelf. DMSPd and DMSO were determined in a subset of 29 samples, 13 of which were collected in the open sea. A comparative plot with DMS, DMSPd, DMSO and chlorophyll concentrations is shown in Fig. 3. DMS concentrations averaged 2.9 nM and exhibited a great variability between sites (general relative standard deviation: 145%). They were locally highest at near-shore stations where elevated inputs of continental-derived nutrients and organic matter occur, i.e. off the Ebro and Rhone pro-deltas, and close to the city of Barcelona (Figs 1 and 2). These DMS maxima were coincident with local maxima of chlorophyll (Fig. 3). However, in some shelf water samples collected in spring (stations PT3, PTl l-14, Fl, Fig. 3) high chlorophyll levels did not correspond with high DMS yields.

Dissolved

933

DMS, DMSPd and DMSO

42’

??

O-O.1

nM

0 0.5 - 1 nM

??l.S-2nM

?? 2.5

_________~

a LATE

APRIL

1994

- 5 nM

MEDITERRANEm 10 - 20 nM

Wl

Fig. 1. Map showing the sampling sites and ranges of surface water concentrations of DMS (nM) during two of the cruises. Left: R.V. Garcia de/ Cid, 2628 April 1994. Right: R.V. HespCrides, l-6 (filled circles), 22-29 (open circles) June 1993. (A) Transect from station F29 (SE, open) to station F20 (NW, coast); (B) transect from station F54 (SE, Mallorca shelf) to station F43 (NW, Ebro prodelta); (C) transect from station F72 (SE, deep) to station F68 (NW, Barcelona).

934

R. Simb et al. 8’

4’

0’

GULF OF ‘IONS

NW BASIN

I I I

-

-

-

-

I

*O-O.1 ?? 0.5 -

nM

1 nM

@IS-2nM

MID JULY

1994

LATE

JULY

1993

of DMS (nM) Fig. 2. Map showing the sampling sites and ranges of surface water concentrations during two of the cruises. Left: R.V. Garcia de1 Cid, 15-21 July 1994. Right: R.V. Discovery, 17 July2 August 1993; (D) transect from station MA1 (S, deep NW basin) to station MA9 (N, Rhone prodelta).

The mean DMSPd concentration was 3.0 nM, almost equal to that of DMS. This is a distinctive feature of our measurements. Dominances of DMSPd over DMS by factors of 1.8-5 have been reported in other marine regions (Turner et al., 1988; Gibson et al., 1990;

Dissolved

-

DMS

.

935

DMS, DMSPd and DMSO

DMSPd

I

DMSO

_

CHL

in the whole Fig. 3. DMS, DMSPd, DMSO (nM) and chlorophyll a (CHL, ng 1-l) concentrations series of surface seawater samples from the western Mediterranean, April-July. The stations near the Ebro, Rhone and Barcelona outflows are indicated. Stations PT: April 1994, Catalan Sea; stations F: June 1993, Catalan Sea; stations SF and S: July 1994, Catalan Sea and NW basin; stations MA and MD: July 1993, NW basin and Gulf of Lions.

of both compounds (Fig. 3) Malin et al., 1993). Despite these similar means the variability did not show a parallel trend. DMSO concentrations were in most cases higher than those of DMS and DMSPd, reaching levels as high as 62 nM in shelf waters off Barcelona. Overall DMSO concentrations averaged 16.6 nM. DMSO was therefore the most abundant dissolved dimethyl sulphur species (DMSSd) in an average DMS:DMSPd:DMSO proportion of 1: 1:6. There are only few works where the three compounds have been measured (Lee and Wakeham, 1989; Gibson et al., 1990; Ridgeway et al., 1992; Bates et al., 1994). In all of them DMSO dominated over DMS by a factor of 2-5, but DMSPd was sometimes the main species. Despite their common phytoplanktonic origin, DMS and chlorophyll did not correlate significantly (r2 = 0.142, n = 54, not significant). Correlations did not improve to significance even when the samples were distributed by spatial (shelf/open) or temporal (cruises with more than 10 data) criteria. Poor correlations between DMS and phytoplankton biomass indicators (such as chlorophyll a concentration) have generally been obtained in most previous studies (Andreae, 1990) unless large or monospecific algal blooms did occur (e.g. Turner et al., 1988; Malin et al., 1993; Matrai and Keller, 1993). Likewise, neither DMSPd

936

R. Simi, et al

1.

Table

Spatial means and ranges

and chlorophyll and

DMSO

a (CHL,

pg I-‘)

chlorophyll-normalised

western Mediterranean

2.9+4.3*

DMSPd, and

concentrations

surface seawater,

Overall area DMS

of DMS,

concentrations,

April-July

Continental

shelf

DMSO

of DMS.

lnM) DMSPd in

(nmol pg-‘) (1993/1994)

Open sea

n = 54

4.9k6.3 (0.0-19.3) n=20

(0.1-4.3) n=34

DMSPd

3.Ok3.8 (0.06G18.3) n=26

4.1k5.1 (0.07T18.3) n=ll

2.2k2.3 (0.06-6.7) n=15

DMSO

16.6k13.7 (0.07T61.6) n=29

21.4k17.5 (0.07-61.6) n= 13

12.8k7.6 (4.1-30.9) n=l6

CHL

0.21+0.21 (0.02Z1.16)

0.13+0.09 (0.03sO.48)

n=54

0.35kO.27 (0.02%1.16) n=20

18.3+20.5 (0.G72.0)

16.1 k20.9 (0.0-66.5)

19.6+20.1 (1.0-72.0)

n=S4

n=20

n=34

33.5k61.2 (0.2-235.5) n=26

31.9k65.6 (0.2-235.5)

34.6k57.8 (O&187.5) n=15

(0.0-19.3)

DMSjCHL

DMSPd/CHL

DMSOjCHL

136.6& 125.7 (0.3-551.6) n==29

n=ll

126X+ 146.3 (0.3-55 1.6) n=13

1x+1.3

n=34

144.6+

103.1

(9.0-331.3) n=16

nor DMSO correlated significantly with chlorophyll (DMSPd: r2=0.035, n =26, n.s.; DMSO: r2 = 0.000, n = 29, ns.), and none of the three DMSSd correlated with each other.

Spatial distribution

of surface concentrations

The spatial distribution (shelf/open) of concentration averages and ranges is given in Table 1. As a mean, continental shelf waters contained 2.7 times more DMS than open seawaters. This proportion was 1.9 and 1.7 for DMSPd and DMSO, respectively. In the case of chlorophyll, the shelf-to-open ratio was 2.7. Thus, it can be stated, in general terms, that higher levels of DMSSd in the continental shelf area were in correspondence with higher phytoplankton development. A detailed observation of DMS and chlorophyll distributions indicates that this trend is more pronounced in transects from off-shore waters to shelf stations close to important continental outflows. Figure 1 (right) and 2 (right) showed four well-defined transects (A-D) tracked along by the ships, each sampled in a short time. DMS and chlorophyll concentrations along these transects were included in Fig. 3. In all cases,

Dissolved

DMS, DMSPd and DMSO

937

increases of chlorophyll by factors of 2-6 were found from open to continental shelf stations. However, similar increases of DMS were observed only in the transects towards the Ebro (B), Barcelona (C) and Rhone (D) outflows, while in transect A open sea concentrations were in the order of those of shelf waters, or even higher. Normalised concentrations of the DMSSd with respect to chlorophyll have been used to compare distribution patterns of these compounds in different trophic or hydrographic regimes (e.g. Iverson et al., 1989). Also, DMS (or DMSP)/Chl ratios measured in the field have been reported to vary largely depending on the dominant algal species in seawater (Turner et al., 1988) since the ability of synthesising intracellular DMSP is taxon-dependent (Keller et al., 1989). Averages of chlorophyll-normalised concentrations of DMS, DMSPd and DMSO are displayed in Table 1. There were no greatly significant differences between shelf and open waters (a > 0.05), although some of the local maxima of DMSjChl were obtained in shelf stations influenced by continental outflows (individual data not shown). However, as indicated by the standard deviations in Table 1, values of DMSjChl and DMSP&hl exhibited a lot of scatter. Similar dispersions of nearly 100% were obtained by (Iverson et al., 1989) in shelf and oceanic waters of the eastern U.S.A. Therefore, no general trend may be inferred from individual data, and averages must be taken with caution. In open sea (oceanic) waters, Iverson et al. reported DMSjChl and DMSP&hl ratios in the ranges 8-57 and l-200, respectively, i.e. very coincident with those of Table 1. Conversely, in shelf waters they reported ranges of normalised DMS and DMSPd concentrations (1-8 and O-72, respectively) that were lower than those of oceanic stations, whereas we do not (Table 1). The northwest

basin-Rhone

mouth transect

In late July 1993, measurements of DMS& and chlorophyll a were carried out in surface waters of transect D, from the deep NW basin to the vicinity of the Rhone river mouth (Fig. 2, right, and Fig. 4). This transect deserves an individualised analysis, since it contains the largest series of DMSSd measurements. Also, accessory data (pigments, nitrate) obtained by other colleagues in the same waters are available (see discussion section below). Rather constant, low concentrations of DMS and chlorophyll were found in the open seawaters (MAl-MA4: 1 nM, 0.2 pg 1-l) while a sharp increase occurred in the eutrophied shelf (MA6-MA9: 12 nM, 1 pg 1-l) with the maximum level at stations MA7-8, i.e. near, but not nearest, to the river mouth. DMSPd and DMSO exhibited more uniform distributions, with no increases of concentration from the oligotrophic to the eutrophic waters. DMSO was the dominant species at the remote stations, while DMS dominated in the near-shore waters. Temporal variability of surface concentrations basin

in open waters of the Catalan Sea andnorthwest

In order to investigate the spring-to-summer changes of DMSSd concentrations without significant influence of the spatial variations, only open sea data from the Catalan Sea and NW basin are considered. The exclusion of the data obtained in shelf and top NW waters allows one to eliminate the uncertainity introduced by sporadic incursions into near-shore hot spots. In Fig. 5, DMS, DMSPd, DMSO and chlorophyll concentrations are plotted as a function of the sampling date. None of the compound concentrations remained unchanged

938

R. Sim6 et al.

1.2

I

100

150 KM

-DMS

250

200

300

OFF-SHORE

___ CHL

A DMSPd

I

DMSO

a (CHL, pg l- ‘) concentrations in surface Fig. 4. DMS, DMSPd, DMSO (nM) and chlorophyll waters, plotted vs the distance off-shore along transect A between a central station in the NW basin (40”58N 6”2E) and the Rhone River mouth.

along time. As a mean, DMS levels increased from April to July, as their scatter decreased. Conversely, the highest DMSPd concentrations were measured in April and July, while in June they were very low. DMSO followed the opposite pattern, exhibiting concentrations in June that were, in most cases, higher than those of April and July. On the other hand, mean chlorophyll levels declined continuously from April to July, as did their scatter. This trend was expected, because maximal phytoplankton biomass in the area generally occurs during springtime and tends to diminish with time (Estrada et al., 1985). As a consequence of these individual variations, the speciation of dissolved dimethyl sulphur also changed with time. While in April and July DMSO represented two-thirds and half of the total DMSSd pool, in June it accounted for 90%. Depth profiles Depth profiles of DMS, DMSPd, DMSO, chlorophyll and temperature at four summer stations in the Catalan Sea (late June 1993) and the NW basin (July 1994) are shown in Fig. 6. The vertical profiles of temperature showed in all cases a pronounced thermal gradient (thermocline) of ca 8°C. Well developed deep chlorophyll maxima (DCM) occurred near the bottom of the thermocline (50-70 m depth). The DCM is a prominent feature of the oligotrophic northwestern Mediterranean during a large part of the year (Estrada et al., 1993).

Dissolved

939

DMS, DMSPd and DMSO

__

5

0.6

m

4

. *

0 .

. .

0

8’

. 0.4

.

.

r^ 3”.

.= .

i2

-

DMS

. . 00

1

0 0

,“O

0

.

0

T

0.6

2.5 I

0.4

I I

3 ‘M

0.2

L

0 I

e ---

0

APRIL

0

MAY

JUNE

JULY

Fig. 5. DMS (top), DMSPd (middle), DMSO (bottom) surface seawater concentrations (nM) in open sea waters of the Catalan Sea (western Mediterranean), as a function of the sampling dates. For comparison, every plot displays also the chlorophyll a concentrations (CHL, pg l- ‘).

R. Simb et al.

940

0

ST. F135

1’)

(w 1

o+

2

4

1 i I

z

10

20

30

L-J

DMS

25.’

50

>

i/// DMSO

,

I

/

x

15

DMSP,

CHL loo

100 g P

(nW

0

2

?

11

I5

I

ST. F212

Oi

I

50

0

12

8

,,A--_--_’ DMS

L__L

25

0

(Pg I’)

WC

Ii 125

125

150

175

T

200

~-r-

10

30

ST. Sl

(Kg I’) 02

0

0

c

b

a

~1

20 (-0

04

0

(K2 1‘)

(nM) 2

00

4

03

ST. S2 06

(nM)

0

4

8

12

12

25

25

50

15

g s

8

DMSP,

100 1

125

125

1

I ,

150 1

175 1

i T

d

200 i

10

20

30

(‘0

Fig. 6. Depth profiles of DMS, DMSPd, DMSO, chlorophyll (CHL) and temperature (r) at four open sea stations in the western Mediterranean. (a) F135,41”7N 2”23E, 23/6/93, 11:OO h; (b) F272, 40”39N 2”46E, 24/6/93, 11:OO h; (c) Sl, 42”ON 5”43E, 17/7/94,6:00 h; (d) S2,42”1N 4”47E, 16/7/94, 5:30 h.

Dissolved

941

DMS, DMSPd and DMSO

In agreement with what has been previously reported in the open oceans (e.g. Andreae, 1990) and the western Mediterranean (Nguyen et al., 1978; Belviso et al., 1993; Simo et al., 1995) DMS and DMSPd were mostly restricted to the euphotic layer, with maximal concentrations occurring between the sea surface and the base of the thermocline. DMSO also was mostly confined to the upper part of the water column, decreasing below the euphotic zone. DMS generally presented highest concentrations at or near the surface, and a sharp decrease at the depth and above the DCM. Only in one case (station S2, Fig. 6d) a small secondary maximum was observed in coincidence with the DCM. The vertical profiles of DMSO essentially followed those of DMS, although at concentrations 2-10 times higher. In two stations (F135 and F272, Figs 6a and b) DMSPd exhibited a distribution that was very different from those of DMS and DMSO. It paralleled the chlorophyll profile, with a deep maximum just below the thermocline. Conversely, at station S2 (Fig. 6d) DMSPd concentration was maximal at 25 m depth and decreased through the DCM. The differences in the vertical profiles observed between the DMSSd and chlorophyll, and between the diverse DMSSd, are not unexpected. Although in the oligotrophic northwestern Mediterranean waters a large part of the summer primary production is associated with the DCM (Lefevre et al., 1995), the chlorophyll maximum does not always reflect a maximum of density of cells, nor a maximum of primary production (Estrada et al., 1985). On the other hand, the instantaneous concentration of each DMSSd is the net result of a tight cycling of production and consumption processes whose nature and rates may vary down the stratified water column (Wakeham et al., 1987; Kiene, 1992; Simo et al., 1995).

DISCUSSION The Mediterranean

vs other temperate

seas as a DMS-producing

system

The data presented here represent the first study of the distribution of DMS (and DMSPd) in a wide area of the Mediterranean Sea. Previous determinations of dimethylated sulphur in this region were mostly restricted to limited areas in the Ligurian Sea (Nguyen et al., 1978; Belviso et al., 1993; Boniforti et al., 1993). Moreover, the present dataset provides one of the first joint measurements of the three DMSSd (DMS, DMSPd and DMSO) in open seawaters, including both spatial and temporal variability. Previous studies on DMSS were either confined to only one site or based on one single sampling cruise (Lee and Wakeham, 1989; Gibson et al., 1990; Ridgeway et al., 1992; Bates et al., 1994). Table 2 compares the mean DMS concentrations determined so far in the Mediterranean Sea with those measured in other temperate marine regions. Our mean DMS concentration in the overall northwestern Mediterranean area (2.9 nM) does not differ greatly from spring levels measured in the Ligurian Sea (0.2-9 nM, 4.6 nM). Conversely, it stands well below the summer concentration observed on the British shelf (7.0 nM), which exhibits a closer similarity to our mean DMS concentration in shelf waters (water column depth (200 m: 4.9 nM, Table 1). However, it is far below the DMS yields in a eutrophic, coastal site in the Ligurian Sea (16.2 nM). In Mediterranean open sea waters (water column depth > 200 m: 1.8 nM, Table l), the average of DMS measurements falls slightly beneath the summer mean concentrations reported for the temperate North Pacific (2.2 nM) and the temperate North Atlantic (2.5 nM). It resembles closely the average reported for subtropical oligotrophic waters

942

R. Simo et al Table 2.

DMS concentrations (nM) reported in the Mediterranean Sea and other temperate marine regions

Region and season

Concentration, mean or range

Temperate

N Atlantic

Temperate

N Pacific

summer

Btirgermeister

et al. (1990)

Bates et al. (1987) 2.2 0.7

winter Subtropical World’s

2.5

Reference

oligotrophic

temperate

Shelf around summer winter

Sea

Ligurian spring

Sea

Andreae

2.1

and Barnard

Andreae

Britain

Mediterranean July January Ligurian spring

seas

1.8

Turner

(1984)

(1990)

et al. (1988)

7.0 0.1 latitudes

Erickson

et al. (1990)

Nguyen

et al. (1978)

3.6 0.9

0.2-9 Belviso ef al. (1993) 4.6

Ligurian, coastal spring-summer

16.2

Boniforti

Western Mediterranean spring-summer shelf open sea

2.9 4.9 1.8

et al. (1993)

This work

(1.8 nM) and the annual average for the world’s temperate seas (2.1 nM). These moderate DMS concentrations in the open sea area are consistent with the oligotrophic nature of the Mediterranean waters, where productivity is low all year round (Estrada et al., 1985).

Biological

control of surface DMS

and DMSP,

variability

Since the origin and, partially, the fate of DMS in seawater are biological, the factors that control the distribution and variation of DMS are expected to be those that influence the composition and activity of the biological community. The main source of aqueous DMS is the enzymatic cleavage of DMSP, which is mostly released from the algal cell to seawater during phytoplankton senescence and grazing by zooplankton (Dacey and Wakeham, 1986; Nguyen et al., 1988; Turner et al., 1988; Leek et al., 1990). The intracellular DMSP content in algae, and hence their ability for producing DMS, varies largely with species, some groups

Dissolved DMS, DMSPd and DMSO

943

being more prolific producers than others (Keller et al., 1989; Liss et al., 1993). Particularly, both culture and field studies have revealed that, among ecologically important groups of phytoplankters, dinoflagellates and prymnesiophytes (including coccolithophorids) are the most significant DMS producers (Holligan et al., 1987; Turner et al., 1988; Keller et al., 1989; Malin et al., 1993; Liss et al., 1993). This taxon-dependence has been invoked as the main reason for the poor DMS vs chlorophyll correlations usually obtained, and for the variability of DMS (and DMSP)/Chl ratios among different hydrographic and trophic regimes. Iverson et al. (1989) attributed the increase of chlorophyll-normalised DMS and DMSPd concentrations from shelf to oceanic stations to the increasing contribution of coccolithophores with respect to diatoms. Accordingly, the similarity observed between our mean DMSS&hl ratios (Table 1) points to an analogous ability in producing or excreting dissolved dimethyl sulphur between the plankton communities of shelf and open seawaters. In addition to phytoplankton, bacterioplankton is also involved in DMS production. The implication of heterotrophic bacteria in the decomposition of DMSP into DMS and acrylate has been demonstrated (Kiene, 1990, 1992). In a previous study (Simb et al., 1995) we have reported a close correlation between DMS formation from DMSP and bacterial heterotrophic production along a stratified water column in the western Mediterranean. The composition of the entire planktonic community and the physiological state of its components both have therefore a determinant influence on DMS production in surface seawater. The increase of mean DMS concentrations between April and July, observed in the open Catalan Sea (Fig. 5) is in rather good agreement with seasonal variations occurring in other temperate regions, where spring-to-summer increases by factors of 2-3 have been reported (Bates et al., 1987; Turner et al., 1988; Nguyen et al., 1990; Leek et al., 1990). During spring, Mediterranean phytoplankton biomass usually achieves its largest development. The algal community is dominated by diatoms, which tend to be substituted by dinoflagellates, more adapted to the incipient water stratification (Estrada et al., 1985). Primary production exceeds heterotrophic activity. All these characteristics are consistent with the concurrence in April of some high chlorophyll and DMSPd levels with low DMS concentrations (Fig. 5). Diatoms are bad DMSP producers, but in sufficient numbers and with a high grazing pressure they may account for considerable yields of DMSPd in the surrounding water (Keller et al., 1989). Growing populations of dinoflagellates also contribute to DMSP production. Thus, DMSP formation and excretion probably exceed DMSPd decomposition by bacteria, so that DMSPd can accumulate. In late spring-early summer, the decay of the spring algal development causes a decline in chlorophyll concentration. Dinoflagellates have substituted diatoms, while coccolithophorids sometimes occupy an intermediate position between both (Estrada et af., 1985). The dominance of DMS over DMSPd in June, and the fact that DMS increases despite the decrease of chlorophyll (Fig. 5), may be indications of this ecological succession and of a late stage in the decay of the spring algal development. In this respect, lags between chlorophyll and DMS peak concentrations observed in in situ seawater (Leek et al., 1990) and laboratory studies (Nguyen et al., 1988) indicated that maximal DMS production takes place during the declining phase of algal blooms. Furthermore, Kiene and Service (1991) have suggested that DMSPd breakdown is faster than DMS losses. Thus, high DMS concentrations may occur when chlorophyll and/or DMSPd are depleted at the late decomposition of a bloom. Microscopical examination of samples from June 1993 revealed heterogeneous phytoplanktonic communities of moderate density, with a predominance of

R. Simi, et al

944

dinoflagellates, and abundant small flagellates (including Phaeocystis sp. and Chrysochromulina sp.) and heterotrophic dinoflagellates (R. Margalef, personal communication, 1994). Furthermore, significant numbers of coccolithophorids formed sporadic blooms, as in shelf waters in front of the Ebro outflow. As indicated above, most of these phytoplankters are good DMS producers upon cell weakening or lysis. Accordingly, most observed individuals were in an unhealthy or decomposition state, and respiration most likely exceeded primary production (R. Margalef, personal communication, 1994). In mid-July, the opposite trend between DMS and chlorophyll was confirmed (Fig. 5) so the ratio DMSjChl reached the maximal value. At the same time, DMSPd returned to nearly spring levels. This is probably because the decay of spring populations had already finished, and new, less abundant populations, adapted to oligotrophic conditions, had developed. In this sense, depth-integrated bacterial heterotrophic production (measured as tritiated leucine incorporation) in samples SF and S (July) was less than half in samples F (June; C. Pedros-Alio, personal communication, 1994) showing that decomposition activity was lower. These growing populations would have a high ability for producing DMSP-DMS.

The role of DMSO

in the DMSSd

cycling

Once produced in seawater, DMS is subject to a variety of sinks besides air-sea exchange. These include microbial consumption (Kiene and Bates, 1990) photo-oxidation (Brimblecombe and Shooter, 1986) and adsorption onto sedimenting particles (Shooter and Brimblecombe, 1989). Recently, it has been recognised that an active biological cycling dominates the marine DMS turnover far over abiotic losses (Kiene and Bates, 1990; Leek et al., 1990; Kiene, 1992; Bates et al., 1994; Simb et al., 1995). DMSO seems to be a significant product of DMS photo-oxidation in seawater (Brimblecombe and Shooter, 1986; Kieber et al., 1996) and one of the metabolites of DMS microbial oxidation. It has been suggested that, in the marine upper layers, DMS oxidation via monooxygenase activation in aerobic bacteria should lead to the formation of DMSO (Taylor and Kiene, 1989). This bacterial DMS-to-DMSO conversion has been confirmed with culture experiments (Zhang et al., 1991; Juliette et al., 1993) but there is still no reliable field evidence that this process actually takes place in the sea. The dynamics of DMSO in Mediterranean surface seawaters reinforces the suggestion that this species is somehow involved in the biological cycling of methylated sulphur. The difference between the temporal variations of DMSO and DMSPd concentrations (Fig. 5) suggests that these compounds do not follow the same production pathway. Most elevated DMSO yields were found in June, in coincidence with the decay of the phytoplanktonic community, when bacterial heterotrophic activity was highest. Conversely, in July, when there was less heterotrophic activity, DMSO concentrations were significantly lower. Lower levels also were found in April, when most algal populations were likely in a growing state. These results point to maximal DMSO production during algal decomposition. However, such a suggestion needs to be confirmed, since it is based on large scale concentration dynamics and no measurements of process rates are so far available. In this respect, it has to be mentioned that photo-oxidation may have also contributed significantly to DMSO formation since high daytime insolation occurred during all the cruises, but simple photochemical processes can hardly account for DMSO concentration changes between June and July. The possibility that DMSO could be reduced to DMS by pelagic seawater bacteria, as

Dissolved DMS, DMSPd and DMSO

945

observed in laboratory cultures (Zinder and Brock, 1978; Suylen et al., 1986; Taylor and Kiene, 1989; Zhang et al., 1991), adds supplementary interest to the study of this compound. In view of the high concentrations measured in Mediterranean waters (Table l), DMSO represents a major DMSSd pool that can be used for the agents that control DMS concentration.

The NW transect The results shown in Fig. 4, corresponding to the transect between open oligotrophic and shelf waters eutrophied by the Rhone River, are illustrative of some of the phenomena that determine the distribution of DMSSd in seawater. The analyses of photosynthetic pigments of chemotaxonomic specificity, performed at the same stations (Barlow et al., 1995 and personal communication, 1995), provided very useful information on the distribution of phytoplankters along the transect. Thus, in surface waters of remote stations (MAl-6) prymnesiophytes were the most abundant algae followed by cyanobacteria. Diatoms, chrysophytes and dinoflagellates represented minor contributions. Closer to the Rhone mouth in the eutrophied area (stations MA7-9), the relative content of diatoms increased more markedly than the other algal groups. This diatom dominance is a usual feature in et al., 1990; Cruzado and Velasquez, waters influenced by the Rhone plume (Mantoura 199 1). As stated above, diatoms are not good DMSP producers, but their high numbers may have contributed to DMS formation at stations MA7-8. The high DMS content at these stations is also consistent with the increase of prymnesiophytes and dinoflagellates. Even the decomposition of the organic matter carried by the river plume may have contributed, but the decrease in DMS concentration at the most inshore station MA9, and the lack of other volatile reduced sulphur compounds at detectable levels, make this possibility hard to believe. Thus, it seems that the nutrient-rich river plume stimulates DMS production in the area of its influence, not by transporting decomposition processes within the freshwater plume but by fertilising primary production in the surrounding saline waters. A significant correlation between DMS and chlorophyll was obtained within the transect However, their transect distributions showed some (r2 = 0.495, n = 9, c1= 0.025). discrepancies, since DMS increased further offshore (MA5-6) than chlorophyll (MA7). Also the accessory pigments increased at MA7. This spatial decoupling between algal biomass and DMS may be related to nitrogen availability. DMSP is the sulphur analog of glycine betaine, and both seem to be involved in osmoregulation in the algal cell. The suggestion that DMSP synthesis is preferred under conditions where nitrogen is in short supply (Turner et al., 1988) has been reinforced by field and laboratory measurements where DMS or DMSP increased when aqueous nitrate was depleted (Nguyen et al., 1988; Leek et al., 1990, Grone and Kirst, 1992). In the MA transect, nitrate concentrations were more than 30 times higher at stations MA7-9 than at open sea stations (MAl-5) (Cruzado, 1995) so the steep nitrate gradient occurring in the intermediate waters (MA&7) might cause a nitrogen stress to the algal community which resulted in the highest DMS vs chlorophyll content observed at station MA6 (Fig. 6). Sea-to-air

DMSfZuxes

Using some of the surface DMS concentrations presented here, we have made an estimate of the spring-summer emission flux of DMS from the Catalan Sea to the atmosphere. A

946

R. Sim6 et al. Table 3. DMS emission&xes to the atmosphere (pm01 m-’ day-‘) reported for the western Mediterranean and other temperate marine regions Region and season

Pacific Ocean, summer winter

Flux mean or range

20”-

Bates ef al. (1987, 1992)

50”N 5.OG5.1 2.1-2.2

North Atlantic summer-fall North Atlantic, summer

et al. (199 1)

Berresheim 5.0~10.0 North

Sea

Turner

et al. (1989)

Nguyen

et al. (1990)

32

South Indic summer winter

3.0 1.3

World’s

temperate

World’s

shelf and coastal

seas

3.3-9.9

Andreae

( 1990)

5.6-l 1.2

Andreae

(I 990)

Baltic Sea summer

4.1

North Sea summer

10.9

Mediterranean July January

References

Leek and Rodhe (1991)

Leek and Rodhe (1991)

Erickson

latitudes

Western Mediterranean spring-summer shelf open sea

et al. (1990)

5 2 This work 5.4 10.3 2.7

detailed description of the flux calculations and results will be presented elsewhere (Simo et al., 1997). Briefly, the equation F= K,AC (Liss and Merlivat, 1986) was used, where K, is the transfer velocity of DMS in the water phase, and AC is the difference between the air and water concentrations of DMS, assumed to be equal to the aqueous concentration, C,, since atmospheric concentrations were very low (average: 1.1 + 1.2 nmol mp3; Simo et al., 1997) and were negligible relative to water levels. Transfer velocities were calculated as a function of water temperature and wind speed (Liss and Merlivat, 1986). Only the surface seawater DMS measurements for which wind speed values were available were used, i.e. most of the April 94 cruise data, all of the early June 93 cruise data and all of July 94 cruise data. The arithmetic mean of the individual fluxes was 5.4 pmol m-* day-‘. Partial means were 2.7~molm~*day-’ and 10.3 pmol me2 day-’ for the open and the shelf areas, respectively. Table 3 compares these fluxes with some calculated for other marine regions.

Dissolved

DMS, DMSP,, and DMSO

947

The overall mean was in good agreement with that observed in the Baltic Sea and that predicted by a model for Mediterranean latitudes, but it was clearly lower than the summer fluxes in the North Sea. The flux from continental shelf waters was rather coincident with that of the North Sea, and fell at the upper end of the range proposed for world’s coastal and shelf areas. Finally, the open sea flux fell near the lower end of the range proposed for temperate seas, and well below the summer emissions estimated for the open oceans. These moderate air-sea fluxes are consistent with the above-mentioned moderate seawater concentrations, and are to be attributed to the low productivity of the Mediterranean sea. Acknowledgements-We thank the scientists and crews aboard the R.V. Hespt%des, Garcia de1 Cid and Discovery, as well as their chief scientists, Miquel Alcaraz, Jaume Rucabado and Jordi Font, and Fauzi Mantoura, respectively. Field assistance by Jordi Dachs is acknowledged. Thanks are also due to Marta Estrada, Celia Marrase and Magda Vila for providing chlorophyll data, to Ramon Margalef for kindly sharing with us his microscopic observations of phytoplankton, and to Ray Barlow for the accessory pigment distributions. Carlos Pedros-Alio provided stimulating discussions in two of the cruises. This work was supported by the C.E.C. Projects EROS-2000 and MAS2-CT934063 and by the Spanish Ministry for Education and Science (Project PB934)190002-01).

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