Lipids and pigments in deep-sea surface sediments and interfacial particles from the Western Crozet Basin

Marine Chemistry 75 Ž2001. 249–266 www.elsevier.comrlocatermarchem

Lipids and pigments in deep-sea surface sediments and interfacial particles from the Western Crozet Basin Laurence Pinturier-Geiss a,1, Jeanne Laureillard a,) , Catherine Riaux-Gobin b, Joelle ¨ Fillaux a, Alain Saliot a a

Laboratoire de Biogeochimie et Chimie Marines, UMR 7094, UniÕersite´ Pierre et Marie Curie, case courrier 134, ´ Tour 25-24, 4 place Jussieu, 75252 Paris Cedex 05, France b Laboratoire d’Oceanographie Biologique, Laboratoire Arago, UMR CNRS 7621, 66650 Banyuls sur mer, France ´ Accepted 8 March 2001

Abstract Deep-sea sediment samples were collected in the Western Crozet Basin ŽIndian sector of the Southern Ocean. through Permanently Open Ocean Zone ŽPOOZ., Polar Frontal Zone ŽPFZ. and Sub-Antarctic Zone ŽSAZ.. Lipid class and fatty acid compositions were investigated to determine the sources and fate of organic matter in the first centimeter of sediment and, above this layer, in the fluff Žwhen present. and particles in the overlying water. The total lipid content varied from 74 to 1033 mg ly1 in the overlying particles and fluffs, and from 24 to 97 mg gy1 dry mass ŽDM. in surficial sediments. Lipid composition was always dominated by phospholipids in the first centimeter of sediment and often in the overlying particles. The amount of phospholipids Žlabile compounds representative of fresh material. was compared to the amount of chlorophyll a ŽChl a., another compound that is susceptible to rapid degradation. A strong N–S gradient was observed in the distribution of these two compounds, which was attributed to the contrasting hydrodynamic of the study area. The high sedimentation rate in POOZ resulted in better preservation of Chl a in this zone than in other zones of the Crozet Basin ŽPFZ and SAZ.. Phospholipid fatty acids suggested the presence of viable as well as morphologically intact organisms, and these organisms consisted essentially of bacteria with some diatom cysts in the fluff of POOZ. These spores were able to grow in the culture, indicating that they were still viable. Despite the strong hydrodynamic variability, phospholipid fatty acids analysed from the deep-sea surficial sediments were never representative of plankton. This pointed to the extremely labile nature of the phospholipids originally present in planktonic material compared with Chl a, which was always found in overlying particles and surficial sediments. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Lipid classes; Phospholipid fatty acids; Chlorophyll a; Revival tests; Southern Ocean

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Corresponding author. E-mail addresses: LAUR – [email protected] ŽL. Pinturier-Geiss., [email protected] ŽJ. Laureillard., [email protected] ŽC. Riaux-Gobin., [email protected] ŽA. Saliot.. 1 Present address: Department of Business and Development, TotalFinaElf Exploration Norge, P.O. Box 168, 4001 Stavanger, Norway.

1. Introduction Several papers on the Southern Ocean clearly state the oligotrophic nature of the primary production despite the availability of large amounts of nutrients in surface waters ŽJacques and Treguer, ´ 1986; Treguer and Jacques, 1992.. In this typical ´

0304-4203r01r$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 2 0 3 Ž 0 1 . 0 0 0 4 7 - 0

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L. Pinturier-Geiss et al.r Marine Chemistry 75 (2001) 249–266

High Nutrient–Low Chlorophyll environment ŽHNLC. ŽMinas and Minas, 1992., the primary production ranges from 0.10 to 0.30 g C my2 dayy1 , and the mean concentrations of chlorophyll a ŽChl a. vary between 0.12 and 0.40 mg my3 Žreviewed in Knox, 1994.. However, these values hide strong geographic variation and high phytoplankton biomass that has been reported notably in frontal zones Žvon Bodungen et al., 1981; Daphner and Mordasova, 1994; Queguiner et al., 1997; Smetacek et al., 1997.. ´ According to physical and chemical properties of the surface waters ŽTreguer and Van Bennekom, 1991; ´ Park et al., 1993; Belkin and Gordon, 1996., the Southern Ocean is classically divided into five main provinces: Coastal and Continental Shelf Zone ŽCCSZ., Seasonal Ice Zone ŽSIZ., Permanent Open Ocean Zone ŽPOOZ., Polar Frontal Zone ŽPFZ. and Sub-Antarctic Zone ŽSAZ.. These zones have very different productivity regimes ŽJacques and Minas, 1981; Treguer and Van Bennekom, 1991. and these ´ regimes exert a primary control on the flux of organic matter transported to deeper waters, and hence, buried in underlying sediments. As part of the Southern Ocean Joint Global Ocean Flux Study ŽSO-JGOFS. programme, the ANTArctic RESearch ŽANTARES. programme conducts research in the Crozet Basin ŽIndian sector of the Southern Ocean.. One of the aims of this programme is to define the main processes controlling the fluxes of biogenic matter in the water column and at the water–sediment interface. Some labile organic compounds, such as certain lipids and chlor a, are potentially good markers for the presence of living or fresh organic matter. As major constituents of living organic matter, lipids are involved in a variety of cellular functions including membrane structure Žphospholipids: PL, and glycolipids: GL. and energy storage Žtriacylglycerols: TAG, and wax esters: WE.. These natural compounds can provide a record of biological activity in the upper water column and processes occurring during sedimentation. Their analyses as lipid classes enable an evaluation of the origin and fate of organic matter ŽParrish, 1988; Laureillard et al., 1990.. This approach has been used successfully on cultures ŽGoutx et al., 1987; Parrish and Wangersky, 1987., as well as on natural samples of plankton, colloids, settling matter and nearshore sediments

ŽParrish et al., 1988; Skerratt et al., 1995; Derieux et al., 1998; Dachs et al., 1999.. Among the lipid classes, particular attention is paid to phospholipids ŽPL., labile compounds that quickly disappear after cell death ŽKing et al., 1977.. These compounds are therefore good markers for the presence of living organisms or ApreservedB membranes in sediments. Additionally, their fatty acid composition can provide information on their origin: bacteria, phytoplankton, and zooplankton. However, no study has addressed the lipid classes of the particulate matter that settles on the deep-sea floor, and our preliminary work on a core collected in PFZ ŽLaureillard et al., 1997. is one of the very few reports on lipid classes of deep-sea sediments. In the open ocean, Chl a is closely related to phytoplankton biomass. This algal pigment can be quickly photo-oxidised in the euphotic zone ŽCarpenter et al., 1986. or further degraded by microorganisms during settling of particles ŽFurlong and Carpenter, 1988. or grazing ŽLeavitt and Carpenter, 1990; Strom et al., 1998.. However, substantial amounts of Chl a and its major degradation products, the phaeopigments, are delivered to the sea floor through sinking of intact cells, faecal pellets or other detrital materials ŽMejanelle et al., 1995., and ´ PhaeorChl a ratio can be used to infer degradation level of material at the water–sediment interface. During plant senescence, considered as an unbalanced turnover in which catabolism processes prevail, the membrane disruption is characterized by a decrease in PL ŽFan et al., 1997. parallel to chlorophyll degradation ŽSpooner et al., 1994b. due to endogenous cell enzymes. Grazing can induce loss of algal membrane integrity that is analogous to that which occurs during senescence, and hence, similar degradation pathways for Chl a ŽSpooner et al., 1994a. and PL. However, relative lability of polar lipids versus that of chlorophyll a has never been addressed simultaneously. This work presents data on the lipid composition of deep-sea surface sediments and interfacial particles in relation to different oceanographic zones crossed in the Indian sector of the Southern Ocean: POOZ south of the Polar Front ŽPF., PFZ between PF and Sub-Antarctic Front ŽSAF., and SAZ between SAF and STF ŽFig. 1.. Lipid distribution and composition are compared to pigment content to

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251

Fig. 1. Sample locations and oceanographic zones. SAZ: Sub-Antarctic Zone; PFZ: Polar Frontal Zone; POOZ: Permanently Open Ocean Zone; STF: Sub-Tropical Front; SAF: Sub-Antarctic Front; PF: Polar Front.

better assess the source of the newly deposited material and its degree of Afreshness.B Pigment content and composition in the sediment surface and in the surface water masses have been previously published by Riaux-Gobin et al. Ž1997.. In this work, we will discuss Chl a and PL degradation processes during vertical particle transport in relation to the primary production of three studied zones. In addition, PL structures in surface-sediment particles were determined in order to assess their origin, and to evaluate

the proportion reaching the seafloor, which originated in the phytodetritus.

2. Methods 2.1. Sampling Sediments were collected along 568E and 728E meridians ŽFig. 1. between 27 March and 18 May

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1993 during the ANTARES I cruise and using the research vessel AMarion DufresneB. Sediments were collected with a multiple tube sediment corer that provided cores with an undisturbed sedimentrwater interface ŽLegeleux et al., 1994.. Two cores were collected at each sampling point, one for lipid analysis, and the other for pigment analysis. Sediment coring locations and corresponding sampling depths are shown in Table 1. On board, the cores were transferred to a room at constant temperature of 4 8C where they were carefully sliced. Lipid analysis was performed on the first centimeter of each core and pigment analysis through the first 0–5 cm of the duplicate core. The samples were stored frozen at y20 Žlipids. and y80 8C Žpigment. until analysis. In the text, stations are referred as x-L or x-P with x corresponding to the number of the station, and L and P indicating that the core was used for lipid or pigment determination at this station. For lipids, a sample of the fluff layer was carefully siphoned off the top of one sub-core ŽSt. 4-L.. This sample was filtered through pre-combusted glass fiber filters ŽWhatman GFrF, 47-mm diameter. and stored frozen at y20 8C for lipid analysis. At other stations, overlying particles and fluffy layers were not clearly separated and were siphoned off together and filtered on pre-combusted glass fiber filters ŽWhatman GFrF, 47-mm diameter.. Again, the filters were stored frozen at y20 8C until analysis. For pigments, the fluff layer was siphoned off and sub-sampled Ža 5-ml sub-sample was filtered onto GFrF Whatman filters and stored frozen at y80 8C for pigment analysis; a 10-ml aliquot was preserved with paraformaldehyde for epifluorescence microscopy study and SEM examination; a 5-ml subsample was isolated for revival tests on-board.. Typical fluffs were collected at stations 3–5 and were described by Riaux-Gobin et al. Ž1997.. At stations 6, 7 and 9, fluffs were reduced to a thin whitish velum devoid of clots ŽRiaux-Gobin et al., 1997. and the first 10–20 cm of overlying water was siphoned off, sub-sampled Ž100–500 ml filtered. and stored as per fluff. 2.2. Analysis 2.2.1. Lipids The analytical procedure used for the lipid extraction is described in detail by Laureillard et al. Ž1997..

In short, the crushed filters and the freeze-dried sediments were ultrasonically extracted twice using a modified one-phase Bligh and Dyer Ž1959. method, employing methylene chloride instead of chloroform. Combined lipid extracts were recovered in the lower methylene chloride layer, dried with magnesium sulphate and then almost completely evaporated at room temperature. Extraction procedure recovery was of 97% Ž n s 2.. A series of blanks was carried through extraction and was analysed, together with the samples, with thin layer chromatography–flame ionization detector analyser ŽTLC–FID Iatroscan w Iatron Laboratories, Japan.. Of the total lipid extract, 75% was analysed by TLC–FID. Four solvent systems were used to separate the total lipid extract into lipid classes according to the polarity of the compounds. The first system, hexanerdiethyl etherrformic acid Ž98:2:0.5., was used to separate hydrocarbons ŽHC., wax esters and steryl esters ŽWE q SE., methyl esters ŽME., short chain ketones ŽscKE. and free fatty acids ŽFFA.. The second system, hexanerdiethyl ether Ž87:13., was used to separate triacylglycerols ŽTAG., steroidal ketones ŽstKE., alcohols ŽALC., sterols ŽST. and diacylglycerols ŽDAG.. The third system, diethyl etherracetone Ž57:43., was used to separate pigments ŽPIG., monoacylglycerols ŽMAG., monogalactosyldiglycerols ŽMGDG. and digalactosyldiglycerols ŽDGDG.. The fourth system, chloroformr methanolrwater Ž57:43:1.4., was used to separate diphosphatidylglycerols ŽDPG., phosphatidylglycerols ŽPG., phosphatidylethanolamines and phosphatidylserines ŽPE q PS. and phosphatidylcholines ŽPC.. Each lipid class was identified from its retention factor and quantified against authentic standards. Mean values and standard deviation Ž n s 3. are reported in Tables 2 and 3. For the purpose of this study, all phosphoglycerides were grouped after quantification into a phospholipid class ŽPL.. Hydrocarbons will be discussed in detail in another paper ŽPinturier-Geiss et al., in preparation.. The same analytical procedure, i.e. the same solvent systems, was used to analyse the blanks in order to check eventual contamination for each lipid class. Moreover, before each analysis, a blank was run to test the purity of the solvents. Polar lipids were separated by eluting the remaining 25% of each extract through a column containing

Zone

Station Žno..

Depth Žm.

Core for lipid analysisa

POOZ POOZ POOZ POOZ PFZ PFZ PFZ PFZ PFZ SAZ SAZ SAZ

2 3 4 5 6 7 8 9 10 13 14 15

1720 3615 4710 4748 4610 4395 4235 4535 4275 4560 4460 4750

– KTB05 KTB07 – KTB13 KTB11 KTB16 KTB19 KTB21 KTB23 KTB26 KTB28

3-L 4-L 6-L 7-L 8-L 9-L 10-L 13-L 14-L 15-L

Latitude ŽS.

Longitude ŽE.

Corresponding core for pigment analysisa

Latitude ŽS.

– X 55801.82 X 51858.53 – X 50800.91 X 48859.59 X 47859.98 X 47800.47 X 45858.16 X 45800.10 X 43858.34 X 43800.73

– X 71848.02 X 61807.84 – X 57859.61 X 57859.16 X 55859.74 X 58800.76 X 55859.08 X 57858.29 X 55858.35 X 58800.50

KTB03 KTB05 KTB06 KTB08 KTB14 KTB12 KTB18 KTB20 KTB22 KTB25 KTB27 KTB29

50841.78 X 55801.82 X 51858.53 X 51859.11 X 50800.24 X 48859.88 X 48800.08 47800.12 X 45859.67 X 45800.84 X 43858.87 X 43800.49

2-P 3-P 4-P 5-P 6-P 7-P 8-P 9-P 10-P 13-P 14-P 15-P

Longitude ŽE. X

X

68825.10 X 71848.02 X 61807.84 X 61807.39 X 57859.52 X 57859.72 X 56800.02 X 58800.39 X 55859.98 X 57858.76 X 55859.69 X 58800.73

Ž – . No data. Station no. and frontal positions cf. Fig. 1. a In the text and tables, the stations are referred as x-L and x-P with x corresponding to the number of the station, L indicating that the core was used for lipid determination, and P indicating that the core was used for pigment determination.

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Table 1 Geographical position and sediment depth of the cores collected for lipid and pigment analysis

253

254

Fluffqoverlying particles Zone Station

POOZ 3-L

POOZ 4-L

PFZ 6-L

PFZ 7-L

PFZ 8-L

PFZ 9-L

PFZ 10-L

SAZ 13-L

SAZ 14-L

SAZ 15-L

Lipid class Žmg ly1 and %. Žmg ly1 .

Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%. Žmg ly1 . Ž%.

HC FFA MAG TAG PL

– – – – –

374"40 132"58 101"38 47"1 378"67

36 13 10 5 37

SLipids

–

1033"203

211"3 50 36"2 8 13"19 3 20"3 5 146"47 34

144"4 58 10"1 4 25"7 10 13"3 5 56"18 22

80"12 26 8"1 3 26"1 8 13"4 4 177"27 58

426"74

247"33

304"46

The numbers after " represent the standard deviation Ž ns 3.. tr s trace, -1%.

52"4 35 21"4 14 0 0 2"2 1 75"12 50 150"23

28"1 26 7"2 6 6"8 5 12"2 11 56"18 51 108"30

102"6 0 18"1 136"8 69"4 325"19

31 0 5 42 21

33"5 4"4 0 39"1 tr 75"10

44 5 0 51 tr

14"2 1"0.1 0 0 59"7 74"9

19 1 0 0 79

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Table 2 Lipid class composition Žmg ly1 and %. in the fluff and overlying particles

0–1 cm of sediments Zone Station

POOZ 3-L

POOZ 4-L

PFZ 6-L

PFZ 7-L

Lipid class Žmg gy1 . Ž%. Žmg gy1 . Ž%. Žmg gy1 . Ž%. Žmg gy1 . Ž%. a

HC FFA TAG ALC ST PL

8"0.1 0.4"0.6 4"1 0 0 15"5

SLipids 25"7 SLipids r TOC Ž%. b

33 2 3.6 0 0 62

6"0.4 tr 0 0 0 18"3

25 tr 0 0 0 75

24"4 nd

5"0.6 7"0.8 0 tr 3"1 16"5

17 23 0 tr 9 51

31"7 0.57

12"0.1 4"0.3 0 0 0 38"8

23 7 0 0 0 70

54"9 0.72

The number after " represents the standard deviation Ž ns 3.. tr s trace, -1%. nd s no data. a Resolved hydrocarbons. b Total organic carbon ŽDe Wit et al., 1997..

PFZ 9-L

Žmg gy1 . Ž%.

Žmg gy1 . Ž%. Žmg gy1 . Ž%. Žmg gy1 . Ž%.

Žmg gy1 . Ž%. Žmg gy1 . Ž%.

8"0.1 15"2 5 1 5 64"9

1"0.2 4"0.6 0 tr 0.7"0.1 69"9

1"0.01 2"0.4 0 0 tr 39"2

8 15 5 1 5 66

97"11 0.99

PFZ 10-L

SAZ a 14-L

PFZ 8-L

1 5 0 tr 1 92

75"10 2.02

1"0.2 8"1.2 0 tr 1"0.03 53"8

SAZ 13-L

1 13 0 tr 2 84

64"9 1.61

2"0.02 1"0.4 0 0 0 51.3"6

3 2 0 0 0 94

55"6 1.32

SAZ 15-L

2 5 0 0 tr 92

42"2 1.82

3"0.1 2"0.2 0 tr 0.3"0.1 21"1

11 7 0 tr 1 81

26"2 0.94

0.66

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Table 3 Lipid class composition Žmg gy1 dry mass and %. in the surficial sediments

255

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2 g of silica gel 40 ŽMerck, mesh size 0.063–0.200., activated at 80 8C for 30 min. The first fraction, containing HC, WE, ME and TAG, was eluted with hexanerdiethyl ether Ž93:7, vrv.. The second fraction, containing ALC, ST and DAG, was eluted with diethyl ether Ž5 ml.. The third fraction containing MAG was eluted with diethyl etherracetonerhexane Ž50:40:10, vrv.. The fourth fraction containing FFA was eluted with diethyl etherrm ethylene chlorideracetic acid Ž30:70:1, vrv.. Polar lipids containing phospholipids and glycolipids were recovered with methanolrwater Ž100:5, vrv.. The recovery of the polar lipid fraction was estimated measuring the recovery of cardiolipid ŽDPG. and was of 79%. Polar lipids were converted into fatty acid methyl esters ŽFAME. with 14% BF3 rMeOH in a methanol–toluene mixture Ž2:1. under nitrogen for 1 h at 65 8C. FAME were measured with a HP 5890 gas chromatograph using a nonpolar capillary column ŽHewlett Packard, HP5, 30 m = 0.32 mm i.d... The oven temperature was programmed to rise from 50 to 100 8C at 25 8C miny1 , then to 300 8C at 2 8C miny1 , and finally to remain at 300 8C for 10 min. FAME were also measured with a Varian 3300 gas chromatograph using a polar capillary column ŽSGE, BPX70, 30 m = 0.22 mm i.d... The oven temperature was programmed as follows: initial temperature 90 8C for 3 min, followed by a 25 8C miny1 ramping to 130 8C, a 0.5 8C miny1 ramping to 155 8C, a 1 8C miny1 ramping to 160 8C and finally a 2 8C miny1 ramping to 260 8C where it was held for 10 min. Compounds were identified from co-injection with FAME standards. Quantification was performed using a deuterated C 23 FAME as internal standard. 2.2.2. Pigments and cultures The analytical methods used for pigment analysis and culture experiments are reported in detail by Riaux-Gobin et al. Ž1997.. Chl a Žincluding isomers b and c ., and associated phaeopigments ŽPhaeo a, b, c . were measured on acetone extracts using the spectrofluorimetric technique of Neveux and Lantoine Ž1993.. The analytical precision is - 1% and the standard deviation between duplicates is 5–10%. At each sampling station, cultures in 500 ml Fr2 medium ŽGuillard and Ryther, 1962. were initiated immediately after sampling with 5-ml inoculum of

the fluff Žwhen present. or of water at the sediment interface. Every 5–8 days, these cultures were sampled for Chl a analysis, microscope observation and SEM examination. At the end of the cruise, the cultures were killed and preserved in formalin.

3. Results 3.1. Lipid class and pigment composition The total lipid contents Ž SLipids. were measured in the overlying particles including the fluff layer ŽSt. 4-L., and in the first centimeter of the cores. In the fluff and overlying particles, SLipids ranged from 74 to 1033 mg ly1 ŽFig. 2a and Table 2.. Chl a and phaeopigment concentrations ranged from 0 to 13 mg ly1 and from 0 to 157 mg ly1 , respectively ŽFig. 2a.. In both cases, the maximum values were obtained in POOZ ŽFig. 2a.. SLipids in the fluff decreased quite regularly from south to north with the exception of the sample St. 13-L Ž458S., where a significantly higher lipid concentration was measured Ž325 mg ly1 .. In the first centimeter of the sediment Ž0–1 cm., SLipids ranged from 24 to 97 mg gy1 of dry mass ŽDM; Table 3.. The concentrations were highest in PFZ Ž488S, St. 8-L. whereas Chl a and phaeopigments were maximised in POOZ ŽFig. 2b.. The SLipidsrTOC ratios Ž%. ranged from 0.57 to 2.02. These ratios were highest in PFZ including the Sub-Antarctic Front ŽSAF, St. 13-L.. In the overlying particles and in the 0–1-cm sediment layer, the lipids were mainly composed of phospholipids ŽPL. and hydrocarbons ŽHC. ŽTables 2 and 3.. PL were represented by diphosphatidylglycerols q phosphatidylglycerols ŽDPG q PG. and phosphatidylethanolamines ŽPE.. Hydrocarbons are biogenic in origin and are mainly formed by longchain n-alkanes in the overlying particles with a marked even predominance and by a mixture of short and long-chain n-alkanes in the first centimeter. The results are presented and discussed in detail elsewhere ŽPinturier et al., in preparation.. However, in overlying particles under Sub-Antarctic SAF and Sub-Tropical STF fronts, triacylglycerols ŽTAG. were the most abundant compounds Ž42% and 51% of total lipids, respectively.. Free fatty acids ŽFFA.

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257

Fig. 2. Plots of the concentration of SLipids, chlorophyll a ŽChl a., phaeopigments ŽPhaeo. and PhaeorChl a ratio as a function of latitude in the overlying particles and in the fluff Ža. and in surface sediments Žb.. Data for pigments are from Riaux-Gobin et al. Ž1997..

and monoacylglycerols ŽMAG. were the other two principal classes detected in the samples. 3.2. Fatty acid methyl ester (FAME) composition The polar lipid fraction separated by column chromatography may contain phospholipids and glycolipids. However, glycolipids were not detected by Iatroscan analysis, which suggests that polar lipids were largely phospholipids. Phospholipid ester-lin-

ked fatty acids were analysed in four sediment samples collected from the different oceanic regimes: St. 4-L in POOZ, St. 8-L in PFZ, St. 13-L and St. 15-L in SAZ, from SAF and STF, respectively. FAME composition is given in Table 4. Monounsaturated and saturated fatty acids represented the major fraction of fatty acids in all the sediments analysed. They were dominated by 16:0, 16:1v7, 18:1v7 and 18:1v9c. PUFA were not abundant and did not exceed 3% of total fatty acids ŽSt. 8-L.. Branched

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258

Table 4 Fatty acid composition Ž%. of phospholipids in surface sediments of four stations ŽSt. 4-L, St. 8-L, St. 13-L, St. 15-L. Fatty acids Ž%.

St. 4-L

St. 8-La

St. 13-L

St. 15-L

i-14 a-14 14:0 i-15 a-15 15:0 15:1 i-16 16:0 16:1v13 16:1v10 16:1v7 16:1v5 i-17 a-17 17:0 17:1 c-17:0 18:0 18:1v10 18:1v9 cis 18:1v7 18:1v5 18:2v6 cis 18:3v3 18:4v3 19:0 c-19:0 20:0 20:1v9 20:2 21:0 20:4v6 20:5v3 22:0 22:1v11 22:1v9 23:0 24:0 22:6v3 25:0 26:0 27:0 28:0 30:0 SSaturated Ž%. SMUFA Ž%. SPUFA Ž%. SBranchedq cyclic Ž%.

0.3 0.5 4.6 3.0 4.7 1.6 0.5 0.9 17.9 1.4 5.0 13.2 4.9 0.5 0.4 1.1 1.1 0.8 6.3 – 5.7 7.3 0.9 0.5 – – 0.6 0.5 0.7 0.5 – 0.4 0.2 0.3 3.6 – – 0.8 4.4 0.4 0.7 1.7 0.3 0.9 0.8 47 41 1 12

0.3 – 1.9 1.4 2.5 1.3 – 0.7 22.0 – 6.0 8.9 2.2 0.6 0.5 1.2 1.0 0.7 9.0 2.2 5.1 7.4 0.0 1.2 0.5 0.3 0.6 0.7 1.0 0.4 – 0.5 0.3 0.4 1.9 0.6 0.3 3.0 4.4 – 2.6 2.6 0.7 2.1 0.9 56 34 3 7

– – 3.7 2.6 4.9 1.3 – 1.1 9.5 6.7 3.9 14.5 4.0 – – 0.8 0.9 1.3 4.6 – 6.8 12.7 1.5 – – – 0.2 0.6 0.6 0.6 0.2 0.4 0.4 tr 2.5 – – 0.7 4.0 0.7 0.3 4.2 0.9 2.1 0.9 37 51 1 11

– – 2.6 3.0 5.3 1.2 – 1.3 12.6 1.2 3.5 13.3 4.1 0.9 0.5 0.7 1.0 1.1 3.6 – 6.1 11.2 1.4 – – – 0.3 0.7 0.7 0.5 0.1 0.2 0.3 tr 2.2 – – 0.6 5.7 0.8 0.9 6.5 2.3 2.7 0.8 44 42 1 13

Table 4 Ž continued . Fatty acids Ž%.

St. 4-L

St. 8-La

St. 13-L

St. 15-L

SC 16 r SC 18 16:1v7r16:0 SBacterial markers Ž%. b

2.1 0.7 33

1.6 0.4 33

1.6 1.5 39

1.6 1.1 46

MUFA s monounsaturated fatty acids. PUFA s polyunsaturated fatty acids. i-s iso; a-s anteiso; c-scyclopropyl. tr s trace, - 0.1%. a Laureillard et al. Ž1997.. b SBranchedqcyclicq18:1v7qLCFA Žlong chain saturated fatty acids, )C 20 ..

and cyclic compounds ranged from 7% to 13% of total fatty acids.

4. Discussion 4.1. Polar lipid and chlorophyll lability The biochemical composition of material sedimenting in the ocean is dependent on its source and various biogeochemical processes operating in the water column. In the water column, the degradation of chlorophyll is mainly controlled by oxygen concentration ŽLeavitt, 1988; Nelson, 1993., light exposure ŽCarpenter et al., 1986; Leavitt and Carpenter, 1990; Nelson, 1993., bacterial activity ŽAfi et al., 1996. and grazing ŽStrom et al., 1998.. The presence of oxygen and light enhances degradation rate of pigments, which shows apparent first-order kinetics with respect to light exposure ŽNelson, 1993.. Chlorophylls can also be degraded in the dark by grazing and with high efficiency rates Ž) 70%, Strom et al., 1998.. Another important factor influencing the rate of pigment degradation is the type of material in which the pigments occur. Nelson Ž1993. reported that when exposed to light, pigments in killed diatom cells degraded twice as fast as those contained in faecal pellets. However, as previously noted by Roy and Poulet Ž1990., no degradation was observed in the dark when the pigments were located in faecal pellets. When delivered to the sea floor, Chl a and phaeopigments are further degraded through

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multiple pathways under both oxic and anoxic conditions ŽSun et al., 1993a,b. and following first-order kinetics ŽSun et al., 1991.. In oxic sediments, bound Chl a is initially released into a free pool and subsequently degraded with rate constants ranging from 0.01 to 0.1 dayy1 ŽSun et al., 1993b.. In comparison to pigment degradation, rather few studies have been conducted on the degradation rate of polar lipids. Harvey et al. Ž1986. investigated the bacterial degradation of two different membrane lipids, ether and ester lipids, in coastal marine sediments under aerobic and anaerobic conditions; 69% of the phospholipids were degraded in 4 days under aerobic conditions, with 52% of the phospholipids being hydrolysed in the first 12 h. White et al. Ž1979. reported a similar rate in sediments with 50% of 32 P incorporated into lipids released within 2 days. In summary, pigments and PL can be extensively degraded in the water column and in sediments but degradation of both lipid types has never been simultaneously evaluated in deep-sea sediments.

C 22 . have been recently linked to bacteria ŽLaureillard et al., 1997.. We observed LCFA up to C 32 in sediments at St. 8 and established that they were derived from sedimentary bacteria ŽLaureillard et al., 1997.. These compounds occurred in the phospholipid fraction extracted from successive sediment layers Ž0–15-cm depth.. No living meiofauna could be present in the deepest layers where ETS activities were low or not detectable ŽDe Wit et al., 1997.. A relative increase of LCFA ŽC 24 –C 27 . within the phospholipid ester-linked fatty acids has been also observed during in situ experimental degradation of faecal pellets in deep waters and was suspected to be associated with the growth of barophilic bacteria ŽMejanelle, 1995.. LCFA from the phospholipid ´ fraction were found as markers of enteric bacteria in faecal material from copepods and euphausiids ŽLaureillard et al., in preparation.. The absence of higher plants in the study area and rapid dilution along long-range transport of any eventual vascular imprint allows a more accurate attribution of these biomarkers ŽMatsumoto, 1989; Simoneit et al., 1991..

4.2. Phospholipid ester-linked fatty acids

4.3. Lipid and pigment distribution in relation to primary productiÕity regime and Õertical export characteristics

Fatty acids associated with PL will provide indications of the source of fresh organic matter because some FA are specific to plankton or bacteria. The acids 14:0, 16:0, 16:1v7, 20:5v3 are, for example, typical major lipids in diatoms. Characteristic features of diatoms also include low proportions of C 18 acids resulting in high S C 1 6 rS C 1 8 and 16:1v7rSC 16 ratios that are usually higher than 1 ŽViso and Marty, 1993.. Branched chain fatty acids Ž iso and anteiso C 15 , iso and anteiso C 17 ., odd chain monoenoic acids Ž15:1, 17:1., and cyclopropane fatty acids Ž =C 17 and =C 19 . are commonly used as indicators of bacterial input to sediments ŽPerry et al., 1979; Volkman et al., 1980, 1988; Smith et al., 1986.. Numerous publications have also associated bacterial inputs with vaccenic acid Ž18:1v7. in sediments Že.g., Gillan and Hogg, 1984; Guckert et al., 1985; Parkes, 1987; Smith et al., 1986; Mancuso et al., 1990. or in suspended particles ŽSaliot et al., 1997.. Other organisms, such as diatoms, contain this fatty acid, but at a very low concentration ŽNichols et al., 1986; Dunstan et al., 1994.. Long-chain saturated fatty acids ŽLCFA)

Lipid and pigment composition fluctuated considerably with latitude, suggesting that the material deposited at the water–sediment interface had different origins or was subject to different biochemical processes occurring in both water column and underlying sediments. While pigments are synthesized by algae, the zone, where surficial sediments, overlying and fluff particles showed higher Chl a abundance, did not coincide with the zones of higher primary productivity. This reveals that the coupling between organic matter synthesized in the euphotic zone and the sediment burial differs from one zone to another. Particular characteristics of vertical fluxes and relative lability of Chl a and phospholipids may explain the discrepancy between primary productivity and sedimentary record. 4.3.1. POOZ (558S to 528S) The Permanently Open Ocean Zone ŽPOOZ. corresponds to the northern part of the Antarctic Zone

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between the Polar Front ŽPF. and the northernmost extent of the sea ice. This area is usually described as a well-mixed water mass, rich in nutrients but with a low primary production in comparison with PFZ ŽPondaven et al., 2000. and SAZ ŽJacques and Minas, 1981.. Surprisingly, SLipids and Chl a concentration measured in the fluffs and in the overlying particles of POOZ were the highest of the three studied areas ŽFig 2a.. These high concentrations, together with low PhaeorChl a ratio, imply a relatively recent origin. These observations are confirmed by the results of the cultures initiated from the fluff or from the water–sediment interface for St. 2. These revival tests were positive for all the samples of POOZ, St. 2-P, St. 3-P, and St. 4-P, and to a lesser extent for St. 5-P ŽFig. 3., indicating that some microphytes were still living when sampled. This might also explain the presence of TAG that have been proved to be rapidly hydrolysed at the death of the cells ŽAfi et al., 1996; Van Wambeke et al., in press.. Corroborating the characteristics of freshness of the sedimentary organic matter of POOZ, high concentrations of PL were detected in the fluff and overlying particles: 378 and 146 mg ly1 ŽFig. 4.. The cultures of diatoms and the scanning electron microscopy examination of the fluffs have indicated that small encysted diatoms were still living and consequently that the chloroplasts were not degraded ŽRiaux-Gobin et al., 1997.. Thus, high concentrations of chlorophyll and PL in the fluff and overlying particles in POOZ ŽFig. 4. are in good agreement with the revival tests of dormant cells. Modification in the ratio between the cellular components may appear in these peculiar stages since both their morphology and physiology are altered. The encysted cells correspond to a dormant stage of the cell, which may explain the relatively low proportion of PL ŽTable 2a.. Indeed, the majority of photosynthetic carbon is fixed in the polar lipids during the exponential growth phase of the cell ŽSargent et al., 1985.. If we consider that these dormant stages have reduced metabolic activity, they might likewise have low PL content. Very few studies have been devoted to lipid composition of resting cysts and those that exist mainly focus on the molecular composition of cysts, in particular, on the highly resistant bio-macromolecular material contained in the cell wall of dinocysts ŽKokinos et al., 1998..

Fig. 3. Culture of microphytes initiated from the water collected at the water–sediment interface. The Y-axis represents the chlorophyll a content Žln ŽChl a..; the X-axis represents the incubation times. The arrow denotes the beginning of the experiment.

Complementary studies should be undertaken to develop a general understanding of the lipid composition of these specific cell stages. The sediments of POOZ, in comparison with the other zones, showed relatively high levels of Chl a as opposed to their low PL and total lipid contents ŽFig. 2b.. The high chlorophyll content relative to PL content in sediments of POOZ ŽFig. 4. might be favoured by higher biosynthesis of chlorophyll due to low light conditions characteristic of these latitudes, and a shorter residence time of the particles in the water column. The sediments of POOZ are characterised by a high sedimentation rate of 10 cm

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Fig. 4. Plots of polar lipids ŽPL. and chlorophyll a ŽChl a. content as a function of latitude in overlying particles, in fluff and in sediments. Data for pigments are from Riaux-Gobin et al. Ž1997..

kyeary1 ŽRabouille et al., 1997., resulting mainly from the production of highly silicified diatoms, which generates relatively heavy and fast-sinking particles ŽQueguiner et al., 1997.. The production of ´ highly silicified diatoms is particular to these HNLC waters, in which Fe depletion induces a higher Si uptake per diatom cell ŽHutchins and Bruland, 1998.. Measurements of biogenic silica export fluxes recorded by sediment traps deployed in the Indian sector of POOZ at 528S have provided direct evidence for the occurrence of mass sedimentation events of diatom during the austral summer ŽPondaven et al., 2000.. Fluxes recorded by traps were among the highest values ever recorded for biogenic silica export fluxes ŽPondaven et al., 2000.. The low grazing pressure by euphausiids and the weak advective currents ŽPark and Gamberoni, 1997. also con´ tribute to the high sedimentation rate measured in POOZ. Thus, the more abundant pigment in fluff particles and the surficial sediments may be partly the results of a more efficient vertical transport in

this zone, which allows chlorophyll to escape from photochemical degredation. However, high concentrations of chlorophyll were not associated with similar high PL contents in surficial sediments of POOZ, as opposed in the fluff and overlying particles ŽFig. 4., suggesting that living encysted cells were essentially encountered in the fluff. This assumption was supported by the PL fatty acid composition ŽSt. 4-L., which was not similar to that usually found in diatoms ŽClaustre et al., 1989; Viso and Marty, 1993.. Coccoliths in a good state of preservation have also been observed in the upper layer of POOZ sediments ŽRiaux-Gobin et al., 1995.. However, 18:1v9 and mainly 14:0 that are very abundant in these species ŽConte et al., 1994. were not observed in significant amounts in our samples. Consequently, even if the mineral structure of these small coccoliths is well-preserved, their characteristic PL appear to have been removed. Contribution of bacteria is suggested by the presence of bacterial markers Ž33%. in the polar lipid fraction.

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4.3.2. PFZ (508S to 468S) The Polar Frontal Zone ŽPFZ. is bordered to the south by the Polar Front and to the North by the Sub-Antarctic Front. This zone has been defined as productive even though few data describing levels of primary production are available for the Crozet Basin ŽJacques and Minas, 1981; Treguer and Van Ben´ nekom, 1991.. SLipidsrTOC ratios in the upper sediments of PFZ were the highest of the three study areas ŽTable 3., and correspond with high surface primary production Ž285 to 401 mg C my2 dayy1, Jacques and Minas, 1981.. The highest concentration of PL was observed in the center of PFZ ŽSt. 8-L. gradually decreasing toward the northern and southern stations ŽFig. 4.. The fatty acid composition of PL, with a low level of PUFA and a relatively high level of SC 18 , differs from that usually present in diatoms ŽViso and Marty, 1993.. Together with low Chl a content, this might indicate a minor contribution of intact phytoplanktonic cells and reflect relatively high degradation efficiency in the water column and at the water–sediment interface. The absence of revivable cells ŽSt. 8-P, Fig. 3. during the diatom culture tests and the high content of FFA Žup to 15 mg gy1 for St. 8-L. also pointed to the presence of degraded organic matter in these sediments. Two major processes can explain these lipid characteristics: a high residence time of the particles in the water column andror a high grazing pressure. The sediments of PFZ are mainly comprised of small diatom assemblages ŽPichon et al., 1998. and the sedimentation rate in this zone is particularly low Ž1 cm yeary1 ; Rabouille et al., 1997., despite high primary production in the water surface layers. The long residence time of particles in the water column particularly seems to affect chlorophyll content more than PL content ŽFig. 4.. However, the fatty acid composition of PL have a signature more bacterial than phytoplanktonic ŽTable 4.. Additionally, indications of grazing are evident at station 8-L where the occurrence of TAG suggests the presence of detritus deriving from meioendofauna ŽLaureillard et al., 1997.. TAG are the main storage lipids in several meiofaunal populations, amphipods ŽHill et al., 1992., polychaetes ŽLuis and Passos, 1995. and in benthic organisms living in cold waters ŽParrish et al., 1996. where low and seasonal supplies of food may induce a higher lipid storage. TAG are very

labile compounds preferentially degraded when compared to other lipid classes ŽAfi et al., 1996; Striby, 2000; Van Wambeke et al., in press.. Consequently, the presence of TAG in deep-sea sediments is usually considered as an indicator of benthic endofauna. In sediments collected under the southern extension of PFZ ŽSt. 6-P and St. 7-P., PhaeorChl a ratios were particularly high Ž43 and 42, respectively. and are close to the value measured in a faecal cast collected at station 5 ŽPhaeorChl a s 34, RiauxGobin et al., 1997.. Therefore, faecal pellets probably contribute significantly to sediments at St. 6 and St. 7. In this area, sedimentary organic matter appeared more detrital than in POOZ. 4.3.3. SAZ (458S to 438S) The Sub-Antarctic Zone ŽSAZ. is formed by the confluence of two fronts: Sub-Antarctic Front ŽSAF. and Sub-Tropical Front ŽSTF.. The waters are highly turbulent ŽPark and Gamberoni, 1997., and relatively ´ high primary production Ž72–134 mg C my2 dayy1, Jacques and Minas, 1981. has been measured in the surface waters during the austral summer. SLipids and the SLipidsrTOC ratio are high under SAF front and decreased toward the north and were lowest in the area influenced by the tropical waters ŽSTF.. Chl a was always measurable even in the northern sediments but remained very low especially in the overlying particles ŽFig. 2a.. The very turbulent regime of SAZ ŽPark et al., 1993; Park and Gamberoni, 1997. can increase the residence time of ´ particles in suspension in the euphotic layers where the degradation of Chl a is particularly efficient ŽNelson, 1993; Strom et al., 1998.. The presence of TAG in overlying particles may also indicate some reworking of the detritus by the benthic fauna. Fatty acid composition of PL measured under the fronts ŽSAF s St. 13 and STF s St. 15. was closer to a typical diatom imprint than in POOZ and in PFZ ŽTable 4.. The relative abundance of 16:1v7 Ž14.5% and 13.3%. and the 16:1v7r16:0 ratios of 1.5 and 1.1 ŽSt. 13-L and St. 15-L, respectively. were low but remained in the range of values found in diatom cultures ŽVolkman et al., 1989; Viso and Marty, 1993; Dunstan et al., 1994.. However, SC 16 rSC 18 Ž1.6. was much lower than the ratios reported for these cultures. In addition, the proportion of bacterial markers was greatest Ž39% and 46%. in areas with

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especially high proportion of 18:1v7 Ž12.7% and 11.2%., suggesting a dominance of bacteria over other living fractions of organic matter ŽPL.. Bacteria are important catalytic agents during early diagenesis and can form a substantial volume of the total organic content until the labile substrate is depleted ŽHarvey and Macko, 1997.. It is noteworthy that bacterial contribution to sedimentary lipids is higher in the northern sediments where the organic content is lower, than in the southern sediments where the organic content is higher ŽTable 4.. This suggests that degradation of organic matter associated with sedimenting particles is less efficient in the waters of SAZ than in the waters of POOZ and PFZ and that living organic matter represented by PL are mainly due to the presence of bacteria.

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a is better preserved than the polar lipids in this environment. Acknowledgements We thank Paul Treguer, co-ordinator of ´ ANTARES programme ŽJGOFS-France., for his constant support, Jean Franc¸ois Gaillard, Chief Scientist of the ANTARES I cruise, for his help in sampling operations, Young Hyang Park for his invaluable comments on frontal structures of the study area, and Jean Claude Relexans and Henri Etcheber for organic carbon data. We also wish to thank the crew of R.V. Marion Dufresne for their help during the cruise and Institut Franc¸ais pour la Recherche et la Technologie Polaires ŽIFRTP. for logistic and financial support.

5. Conclusions References The lipid and Chl a content of overlying particles and surface sediments was analysed in order to estimate the source of the organic matter and its degree of preservation in the Western Crozet Basin. A North–South gradient was observed in the distribution of Chl a and lipids and this corresponded to different hydrological conditions. Despite great water depths, high lipid contents together with high Chl a concentrations were measured in the fluff of POOZ. These high values were associated with a growth of encysted cells inoculated from the fluff, which demonstrated that these vegetative stages were still living. This is consistent with a rapid sedimentation rate in this area. In the sediments, the dominant signature of polar lipids was derived from bacteria. The phospholipid fatty acids were not representative of the surface microphytoplankton even in POOZ, where diatom cysts were still living in the fluff and where vertical transfer of particles appeared to occur faster than in other zones. Neither a high sedimentation rate ŽPOOZ. nor a high primary production ŽPFZ. resulted in a record of PL of diatoms in these deep Antarctic sediments, which demonstrates that PL from surface plankton had been hydrolysed before deposition to the sediment. This decoupling between Chl a and PL signature in sediments reveals that Chl

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