Molecular characterisation of organic matter in sediments underlying the oxygen minimum zone at the Oman Margin, Arabian Sea

Deep-Sea Research II 47 (2000) 353}375

Molecular characterisation of organic matter in sediments underlying the oxygen minimum zone at the Oman Margin, Arabian Sea Barbara J. Smallwood, George A. Wol!* Environmental Organic Chemistry and Geochemistry Group, Oceanography Laboratories, Department of Earth Sciences, University of Liverpool, Liverpool, L69 3BX, UK Received 20 August 1998; received in revised form 24 January 1999; accepted 1 February 1999

Abstract Lipids in replicate sediment cores collected from a transect through the oxygen minimum zone across the Oman Margin continental slope (&400, 800, 1000 and 1250 m), have been analysed in order to assess the relative contributions of primary and secondary producerderived material to the sediments. The high abundance of compounds that can be ascribed to primary producers, namely diatoms, dino#agellates, coccolithophores, Eustigmatophycae and cyanobacteria, re#ects the high productivity of surface waters, but there is little direct molecular evidence of zooplankton reworking of organic material, except at the deepest water site (&1250 m). There is, however, clear evidence of benthic re-working, probably by detritovore megafauna, at one of the sites near the base of the oxygen minimum zone (&1000 m). The relative abundance of biological markers that can be ascribed to aerobic and anaerobic bacteria in the sediments, namely the hopanoids and branched fatty acids, respectively, mirrors the concentrations of oxygen in overlying water. Considerable intra- and inter-site variability probably results from the spatial and temporal variability in production and from the complexity of sedimentation processes. ( 1999 Elsevier Science Ltd. All rights reserved.

1. Introduction The biogeochemistry of carbon in the Arabian Sea basin is a key area of interest in oceanography (Gaillard, 1997; van Weering et al., 1997; Burkhill et al., 1993; Haq and

* Correspondence author. Fax: 0044-151-794-4099. E-mail address: [email protected] (G.A. Wol!) 0967-0645/00/$ - see front matter ( 1999 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 9 9 ) 0 0 1 1 0 - 1

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Milliman, 1984). At the Oman Margin, upwelling driven by the seasonal southwest monsoon leads to very high productivity; this in turn leads to an intense oxygen minimum zone (OMZ) and to the deposition of organic-rich sediments on the continental slope (Pederson et al., 1992; Paropkari et al., 1992; Paropkari et al., 1993). There are a number of unresolved issues regarding the in#uence of the intense OMZ on the fate of organic carbon. Speci"cally, there is no apparent relationship between the total organic carbon contents of the sediments and bottom-water oxygen concentrations at the margin (Calvert et al., 1992). This has led to the suggestion that oxygen is not the determining factor in the burial of carbon there (Pederson et al., 1992), although this has been disputed (Paropkari et al., 1993). Surprisingly, rates of sulphate reduction in the sediments underlying the OMZ are very low for an upwelling region (Passier et al., 1997), despite the abundance of organic carbon. This may re#ect a lack of metabolizable material, which in turn suggests that the organic matter (OM) arriving at the sediment-water interface is degraded prior to deposition (Pedersen and Shimmield, 1991). Clearly, water column and benthic processes strongly in#uence sedimentary organic matter (OM) composition, and ultimately control its fate. As the sedimentary record may provide the key to understanding carbon cycling in the Arabian Sea, it is imperative to deconvolve pelagic and benthic in#uences on its burial. Lipid biological markers may be helpful in achieving this goal, since they provide information on processes occurring in the sediments (Westerhausen et al., 1993; Santos et al., 1994; Wol! et al., 1995) and in the water column (Wakeham, 1995; Wakeham and Lee, 1989), and on the contributions of allochthonous sources of OM to the sediments (Volkman, 1986; Westerhausen et al., 1993). Although the lipids only account for a small proportion of the total sedimentary OM (Saliot et al., 1982), they are less susceptible to environmental alteration than the other main components of OM, namely the proteins, carbohydrates and pigments (Henrichs, 1992), and they are of great importance to living organisms (e.g. in cell membranes) and essential in the storage and mobilization of energy in reproduction, moulting and metabolism (Brassell and Eglinton, 1986). Whilst very few lipids actually have truly speci"c sources (e.g. Volkman, 1986; Volkman et al., 1993), careful examination of sedimentary lipid distributions, nonetheless, can lead to a delineation of OM sources (e.g. Harvey, 1994), and potentially to their quanti"cation (Prahl et al., 1994). In the present study, the organic component of sur"cial sediment samples underlying the intense OMZ o! the Oman coast has been characterised at the molecular level. We have used the biological marker approach, in order to assess the principal sources of OM to the sediments and the e!ects of benthic reworking on its quality and preservation. Here we concentrate on sources of OM to sur"cial sediments (0}20 mm; mean data for all 0}5, 5}10 and 10}20 mm core sections) and attempt to assess the relative contributions of primary and secondary OM to the sediments. The study was carried out in replicate (]3 samples from separate coring deployments at each site), since it has been established that the concentrations and distributions of biomarkers are extremely patchy in the deep sea (Santos et al., 1994). The e!ects of

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benthic reworking and of diagenetic processes are discussed elsewhere (Smallwood, 1998; Smallwood et al., 1999).

2. Materials and methods 2.1. Sampling Undisturbed sediment cores were recovered with a multiple-corer (Barnett et al., 1984) from a transect through and below the OMZ during R.R.S. Discovery cruise 211/94 (Fig. 1) (Gage, 1995). Sediment cores analysed in this study were collected in triplicate from separate multiple-corer deployments at approximate water depths of 400, 800 1000 and 1250 m (Table 1). Cores were either frozen whole immediately and stored (!503C) on board ship before being sliced and lyophilised in the laboratory, or sliced, frozen (!503C) and lyophilised on board ship. All cores were sliced as follows: 0}5, 5}10, 10}20, 20}30, 30}40, 40}50, 50}60, 60}70, 70}90, 90}110, 110}130, 130}150 mm, except for two of the cores from the 800 m site (12713d2 and 12713d3; Table 1), for which sur"cial sections of 10 mm were taken. 2.2. Analytical methodology 2.2.1. Total organic carbon and total nitrogen Total organic carbon and total nitrogen contents of the de-carbonated sediments were determined using a Carlo Erba 1106 CHN Elemental Analyser (Wol! et al., 1995). The TOC (or TN) values were normalised to the original dry sediment (Hedges and Stern, 1984). Reproducibility was determined by replicate analyses (]8) of a homogenised sample; the coe$cients of variation from the mean concentration for both TOC and TN were less than 3%. 2.2.2. Stable isotope analysis of organic carbon Sediments were de-carbonated prior to analysis. HCl (1M, 2 ml) was added dropwise to an aliquot of freeze-dried, unsieved sediment (ca 15 mg) to avoid excess e!ervescence. Once the e!ervescence had ceased, the suspension was sonicated (5 min). The vial was then left at room temperature (30}60 min) for the reaction to progress. HCl (1M, 2 ml) was added again and the vial placed on a mechanical shaker (30 min.). Acid was added continually until no more reaction occurred. The sediment was then washed with milli-Q water (2}3 ml aliquots), centrifuged (3000 rpm; 2 min) and decanted until the supernatant was neutral (pH 7). The sediment was then frozen and lyophilised. Enough de-carbonated sediment (10}20 mg) to produce 1 mg of carbon was then weighed into a clean quartz tube. Pre-cleaned copper (I) oxide (2 g) and silver wire (ca. 5 mm) were placed in the tube, which was degassed with a rotary pump and sealed with an oxy-acetylene torch. The sealed tubes were heated in a furnace (8503C; 2 h) to oxidise the organic carbon to CO . The tubes were cracked 2 under vacuum; the resultant CO was passed through a cryogenic methanol trap 2 (!873C) for puri"cation and collected in evacuated vessels in a liquid N trap 2

Location

19322.02@N, 19322.12@N, 19321.88@N, 19314.13@N, 19314.10@N, 19314.29@N, 19316.77@N, 19316.77@N, 19317.25@N, 19314.38@N, 19314.14@N, 19314.15@N,

Station No.

12695d5 12695d8 12698d3 12713d3 12711d3 12713d2 12718d3 12718d1 12706d1 12723d5 12725d3 12725d5

58315.55@E 58315.46@E 58315.68@E 58322.84@E 58322.86@E 58322.87@E 58329.91@E 58329.91@E 58330.41@E 58331.46@E 58331.30@E 58331.28@E

402 409 422 827 832 833 981 983 1002 1252 1254 1256

Water depth (m)

@

@

@

Cores frozen immediately

54.3 54.1 57.2 41.6 34.4 38.9 14.3* 14.6 14.2* 26.4 28.8 31.0

@ @

@ @

@ @ @ @ @

TOC (mg g~1 sed)

Cores sectioned and lyophilised on ship 6.9 7.1 6.7 4.8 3.7 4.5 1.5* 1.6 1.3* 3.0 3.2 3.6

TN (mg g~1 sed)

7.9 7.7 8.5 8.7 9.2 8.7 9.6* 9.4 10.7* 8.8 8.9 8.6

C/N ratio

!20.7 !20.5 !20.6 !20.6 !20.6 !20.7 !20.7* !20.7 !20.6* !20.5 !20.5 !20.8

d13C

Table 1 Summary of sample locations and water depths. Bulk data for the sur"cial sediments of the Oman Margin. N.B. Sur"cial sediments are the 0}5 mm sections, with the exception of starred cores where 0}10 mm sections were taken (cf. biological marker data, which are averages for 0}5, 5}10 and 10}20 mm sections)

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(!1783C). Non-condensables (O , N ) were pumped o! before the reaction vessels 2 2 were sealed. The samples were then placed in the mass spectrometer for determination of 44CO , 45CO and 46CO . A graphite standard was run with every batch of 2 2 2 samples; this was prepared as above. Stable isotope values were determined using an automated VG Isogas SIRA 12 triple collecting mass spectrometer. Reproducibility was determined by replicate analyses (]5) of three samples; the coe$cients of variation from the mean for d13C were less than 0.05&. 2.2.3. Total free lipids Extraction. Dry sediment (ca. 500 mg) was extracted in a soxhlet apparatus (24 hr; 100 ml; 9:1 dichloromethane: methanol). A known amount (ca 4 lg) of two internal standards (2,21-dimethyldocosane and 5b(H)-cholanic acid) was added to the sediment and clean anti-bumping granules were added to the solvent, prior to extraction. The extract was evaporated to a small volume under vacuum and transferred to a clean vial (7 ml); it was then evaporated under a steady stream of nitrogen. An aliquot (1/5) of the extract was kept as a reference. Hydrolysis and acidixcation. The extracts were hydrolysed (KOH; 1M; 7 ml; overnight), transferred to a separating funnel (50 ml), diluted with milli-Q water (7 ml) and extracted with hexane (3]15 ml) to obtain the saponi"able neutral fraction. The water-soluble fraction of the extract was then acidi"ed (HCl; 6M; (pH2) and extracted with hexane (3]15 ml) to give the acid fraction. Both fractions were evaporated to dryness, under vacuum. The saponi"able neutral fraction was taken up in a minimum volume of DCM, dried by passing through a short column of anhydrous sodium sulphate (&1 g) into a pre-weighed vial and evaporated under nitrogen as before. Derivatisation. The acidic fraction was methylated (BF /MeOH; 15 ml; darkness; 3 overnight), diluted with Milli-Q water (15 ml) and extracted with hexane (3]15 ml). It was then worked up in the same way as the neutral fractions. Neutral and methylated acidic fractions were derivatised with bis-(trimethylsilyl)-tri#uoroacetamide (BSTFA) (&40 ll; 503C; 30 min) prior to analysis by gas chromatography}mass spectrometry (GC}MS). Gas chromatography}mass spectrometry. GC}MS analyses were performed on the derivatised extracts (acid and neutral fractions analysed separately), using a Hewlett Packard 5890-A gas chromatograph "tted with an on-column injector and a fused silica column (95:5 methyl:phenyl silicone, BPX-5 or equivalent, 0.2 lm "lm thickness; 30 m]0.25 mm i.d.) using helium as the carrier gas (ca 2 ml min~1). A retention gap of deactivated silica (1 m]0.32 mm i.d.) was used at the front of the column. The oven temperature was programmed from 40 to 3203C at 53C min~1 after 1 min at 403C and held at 3203C for 20 min. The column was fed directly into the EI source of a VG TS-250 mass spectrometer. Typical GC}MS operating parameters were as follows: ionisation potential 70 eV; source temperature 2203C; trap current 250 lA. The instrument was operated in full acquisition mode, at a mass resolution of 500 and cycled from 50}700 Daltons every second. Data were collected on a VAX 3500 Workstation, and processed using VG-OPUS software.

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Identixcation and quantixcation. Identi"cation of the lipids was made by comparison of relative retention times, relative retention indices and mass spectra with those in the literature. Individual compounds were quanti"ed by comparison of their peak areas in the total ion current (TIC) chromatogram with those of the internal standards. Relative response factors were assumed to be 1, thus data are only semi-quantitative. Reproducibility was determined by replicate analyses (]4) of an homogenised sample; the coe$cients of variation from the mean concentration for the determined analytes were less than 15%.

3. Results and discussion The bulk characteristics of the sur"cial sediments from the Oman Margin are shown in Table 1. Brie#y, the isotopic composition of carbon (ca !20.5%) and C/N ratios of sedimentary OM (8}10) are consistent with an autochthonous source, although it should be noted that in the `marinea isotopic signature could mask a contribution to the sediments from C-4 land plants, which are also relatively enriched in 13C (!15}!20&; Ostrom and Fry, 1993). The distributions of chemical biological markers in the Oman Margin sediments are extremely complex. Many of the identi"ed compounds are ubiquitous in marine organisms, and it is therefore di$cult to distinguish their precise source(s). Furthermore, the concentrations of individual lipids (relative to dry sediment, TOC and total lipids) show a high degree of spatial variability, both within and between sites. The patchiness might re#ect variability of inputs and/or physical and biological reworking in the sediments. In view of this, a cautious approach has been adopted to assess `sourcesa of the biological markers. Where possible, individual or groups of compounds have been ascribed to speci"c and non-speci"c primary producers, bacteria, other autochthonous OM (phytoplankton or invertebrates, but not speci"cally either) and allochthonous sources. The identities and relative concentrations across the margin are described below: 3.1. Non-specixc markers for primary production Phytol (1) and 6,10,14-trimethylpentadecan-2-one (2) are both non-speci"c indicators of primary production, that are derived from the breakdown of chlorophylls a and b (Ikan et al., 1973; Brooks and Maxwell, 1974; Ragan and Chapman, 1978; Brooks et al., 1978; Sochard et al., 1979; Volkman et al., 1993; Cahoon et al., 1994). However, in the present study, phytol also may have been present as intact chlorophyll a or other esters, since samples were saponi"ed prior to analysis. The ketone, 2, forms by oxidative (Ikan et al., 1973), microbial (Brooks and Maxwell, 1974) or photochemical degradation (Rontani and Aquaviva, 1993; Rontani and Giusti, 1988), which can occur in the water column or, in the "rst two cases, in the sediments. Phytol, either as the free alcohol or as chlorophyll a or other esters, is ubiquitous in the Oman Margin sediments and in some cases is an abundant component, accounting for up to &10% (12725d3, 1250 m) of the total free lipids, as quanti"ed by

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Fig. 1. (a) Location of study area in the Arabian Sea. (b) Three-dimensional bathymetry of the Oman Margin study area and positions of sampling stations, relative to the OMZ.

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Fig. 2. Concentrations of phytol (1), the branched ketone (2) and PUFA's (3), relative to TOC at all sampling sites.

GCMS (includes free and esteri"ed compounds, as opposed to bound lipids that are not readily saponi"able). Intra-site variability in its concentration relative to TOC is highest at the 400 m site (coe$cent of variation; CV; 109%), but is lower down-slope (CV 41% at 800 m; 18% at 1000 m and 37% at 1250 m). The branched ketone (2) is a minor component in only one sur"cial sediment sample (Fig. 2). Sedimentation of phytoplankton is a primary source of the poly-unsaturated fatty acids (PUFAs; 3) which as trigylyceryl esters can comprise up to 30}40% of cellular fatty acids in algal cultures (Mayzaud et al., 1976; Harvey et al., 1988; Volkman et al., 1989). In the Oman Margin sediments, these compounds represent (3% of the acid fraction and never more than &2% of total lipids within each core and their distributions and concentrations at each site are variable (Fig. 2). 3.2. Class-specixc markers for primary production Mid-chain hydroxy acids (e.g. 4); alkyl diols (e.g. 5); keto-ols (e.g. 6); long-chain alkenones (e.g. 7), long-chain alkenoates (e.g. 8) can be ascribed to microalgal sources, and may be useful as biological markers for speci"c classes of phytoplankton. 3.2.1. Mid-chain diols, hydroxy acids and keto-ols Mid-chain hydroxy acids and alkyl diols have been identi"ed in Eustigmatophyceae (Gelin et al., 1997; Volkman et al., 1992), the genus Nannochloropsis having been suggested as a potential source for these compounds (Gelin et al., 1997). The isomeric compositions of alkyl diols and mid-chain hydroxy acids in the Oman Margin sediments are similar to those reported previously (Volkman et al., 1992; ten Haven et al., 1992; Versteegh et al., 1997), the major diols being 14- and 15hydroxytriacontan-1-ol. These were not quanti"ed individually, as they co-eluted under the GC conditions employed in this study. The major hydroxy acid is a 12hydroxyoctacosanoic acid. There is signi"cant intra-site variability in the relative concentrations of hydroxy acids at 800, 1000 and 1250 m (Fig. 3; CV } 72, 126 and 97%, respectively). The keto-ols are present in a wider carbon number range at 800 and 1250 m (C }C ) than elsewhere (only C in all cores at 400 and 1000 m, except for 28 32 30

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Fig. 3. Concentrations of mid-chain hydroxy acids, alkyl diols and keton-ols, relative to TOC at all sampling sites.

12695d5, where the C }C compounds are present), but the C and C com30 34 30 32 pounds are dominant. There is no statistical di!erence in the relative abundance of these compounds within and below the OMZ. 3.2.2. Long-chain alkenones Long-chain alkenones and alkenoates were originally thought to occur only in certain coccolithophores, speci"cally Emiliania huxleyi (Volkman et al., 1980a; van Vleet and Quinn, 1979), but they also have been identi"ed in a few other classes of microalgae (Marlowe et al., 1983; Volkman et al., 1995). The long-chain alkenones are ubiquitous in sediments across the margin but there are no apparent trends in their relative abundance down-slope. Only n-C and C alkadien-2-ones (Rechka and 37 38 Maxwell, 1988) were identi"ed and these are of relatively equal abundance, with respect to total lipids, in all of the cores (xN "1.4%, n"12). The absence of the tri-unsaturated compounds (i.e. alkenone index, UK "1; Brassell et al., 1986) 37 re#ects the warm sea-surface temperature of the Arabian Sea. Using the growth temperature calibration of Prahl and Wakeham (1987), the data collected in this study correspond to a growth temperature of 293C, which is close to the SST measured in the coastal Arabian Sea (&283C; Ryther and Menzel, 1965). A recent extensive study (Sonzogni et al., 1997) of Indian Ocean sediments noted lower values of UK and 37 SST (0.87 and 25.63C, respectively) at a nearby location (19318.0@N 58326.0@E). This apparent discrepancy probably re#ects errors in our analytical protocol, which was not optimised for the determination of UK . 37 Sediments at this margin contain a very patchy distribution of the long-chain alkenoates, which are present only in four of the 12 cores analysed; they are not detectable at 1000 m. 3.3. Bacterial markers Biological markers deriving from bacterial sources in the Oman Margin sediments include the hopanoids (Ourisson and Albrecht, 1992; Ourisson and Rohmer, 1992;

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Fig. 4. Hopanoic acid concentrations as a percentage of total lipids vs. water depth.

Brassell et al., 1983) and branched acids (iso and anteiso) (Volkman et al., 1980b; Perry et al., 1979). Hopanoids have been identi"ed in a wide variety of aerobic bacteria, including many strains of eubacteria (gram positive and gram negative) and cyanobacteria, but are absent in obligate anaerobes (Ourisson and Rohmer, 1992). Their presence in the Oman Margin sediments therefore re#ects an `aerobica microbial contribution to the OM. Conversely, iso- and anteiso-branched acids are generally ascribed to anaerobic bacteria (e.g. Parkes and Taylor, 1983; Parkes, 1987). 17b(H),21b(H)-Bishomohopanoic acid (9) and 17b(H),21b(H)-bishomohopanol (10) are the most abundant solvent extractable hopanoids in the Oman Margin sediments. There are smaller contributions from 17b(H),21b(H)-homohopanol, 17b(H),21b(H)trishomohopanol, 17b(H),21b(H)-hopane and diploptene (11). Diploptene is probably derived directly from cyanobacteria (Ourisson et al., 1987), whilst the other compounds may derive from the degradation of bacteriohopanepolyols under aerobic conditions (i.e. in the water column or soon after sedimentation. Bacteriohopanetetrol and related conjugates have been identi"ed in high concentrations in the Oman Margin sediments collected as part of this study; 18.5 lg g~1 dry sed., 256 lg g~1 TOC; Innes, 1998). The presence of minor amounts of the C hopanol may re#ect in 33 situ anaerobic degradation of the precursor(s) in the sediments, or possibly in anaerobic micro-environments in particles during transport to the sediments. The relative concentrations of hopanoic acids, with respect to total lipids, increase signi"cantly downslope (p(0.05; Fig. 4), reaching a maximum of &4% at 1250 m. (The relative concentrations of the hopanoids, i.e. including hopanoic acids, hopanols and hopenes, are depressed at the 1000 m site, possibly as a result of benthic activity; Smallwood et al., 1999; otherwise concentrations increase downslope). This strongly suggests that bacterial inputs from aerobic processes within the water column and possibly in sur"cial sediments are most signi"cant at the deepest water site which is consistent with the observation that these sediments underlie more oxygenated waters than those between 400 and 1000 m (Gage, 1995). Anteiso- and iso-alkanoic acids are ubiquitous across the margin, but unlike the hopanoic acids, show no down-slope trend. The anteiso-pentadecanoic acid is the most abundant acid and the anteiso isomer (C and C ) is consistently dominant. 15 17 The distributions of branched acids in the Oman Margin sediments are consistent

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with those of anaerobic microbial communities (Gillan and Johns, 1986; Perry et al., 1979), but it is not clear whether they derive from benthic or water-column communities. 3.4. Non-diagnostic autochthonous biological markers The non-diagnostic biological markers, including the fatty acids and sterols, are the most abundant and have the most complex distributions within these sediments. 3.4.1. Fatty acids The Oman Margin cores all show an even/odd carbon number predominance of n-alkanoic acids and a bimodal distribution with maxima at C and between 16 C and C (Fig. 5a). Core 12695d8 is distinct in that concentrations of all fatty 22 26 acids are very low and are dominated by C and relatively greater amounts of 16 saturated C (Fig. 5b); the monounsaturated compounds C and C are 14 16>1 18>1 depleted and the PUFAs (Fig. 2) are also absent, suggesting that the OM of this core is more degraded than in other margin samples. It is not possible to determine the precise sources for the fatty acids at the Oman Margin due their ubiquitous occurrence in eukaryotes and eubacteria, but they

Fig. 5. Fatty acid distributions at the Oman Margin. (a) 12695d5, 402 m, a `typicala distribution. (b) 12695d8, 409 m. Key: C }C monounsaturated fatty acid. C }C n-alkanoic acid. C }C iso 14>1 14 16 16 15* 15 fatty acid. C }C anteiso fatty acid. 15! 15

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appear to be typical of a mixed source from phytoplankton (dino#aggelates, prymnesiophytes, cyanobacteria and diatoms; Claustre et al., 1988}1989) and bacterially derived OM, with some contributions from zooplankton (Wakeham, 1995; Wakeham and Lee, 1989; Saliot et al., 1982). 3.4.2. Hydroxy acids a- and u-Hydroxy acids are present in the Oman Margin sediments, generally in low abundance, with high variability in their concentrations. The u-hydroxy acids are most abundant at the 400 m (12695d8; up to 5.2% of the total lipids; 0.41 mg g~1 TOC) and 800 m sites (12711d3; up to 4.7% of the total lipids; 0.24 mg g~1 TOC), where the distribution is dominated by the C acid. At the other sites, the distribu22 tions of the u-hydroxy acids are more wide ranging, but they are less signi"cant components accounting for (1% of the total lipids. a-Hydroxy acids are abundant only within core 12698d3 (2.9% of total lipids; 0.16 mg g~1 TOC), and have a wide carbon number range (C }C ) with a unimodal 16 28 distribution. The distributions of the hydroxy acids do not re#ect those of the alkanoic acids, so it is unlikely that the hydroxy acids are products of their degradation (Cranwell, 1982). Hence, their most likely source is directly from a mixed phytoplankton, bacteria and cyanobacteria (Matsumoto et al., 1987). 3.4.3. Isoprenoids Squalene is present in all sediments analysed at the Oman Margin. This compound is an important biosynthetic intermediate in a wide range of organisms, being the precursor to triterpenoids such as the steroids and hopanoids. In the absence of compound-speci"c isotopic data, it is impossible to specify a direct source, although it should be noted that its highest concentrations (relative to the total lipids; x"3.2%, n"3) are in the sediments from the 1000 m site, and that this may be related to the high abundance of benthic megafauna there (Smallwood et al., 1999). A series of compounds with mass spectra similar to squalene, but which are not the widely reported highly branched isoprenoids (Rowland and Robson, 1990) were tentatively identi"ed as C ,C ,C and C isoprenoid hydrocarbons (where x"0, 25>x 30>x 31>0 35>y 2}5, y is unknown). These are minor components of the sediments (x"1.7% of total lipids, n"10) and have patchy and variable distributions. Their origin is unknown. 3.4.4. Sterols With the exception of the 1000 m site, the sterols are the most abundant compound class in the lipids of the Oman Margin sediments. They have a high structural diversity, 21 di!erent sterols having been identi"ed (Fig. 8a}c). The source speci"city of individual sterols is questionable, even 4,23,24-trimethylcholest-22-en-3-ol (dinosterol; 12), which was thought to originate exclusively from dino#aggelates, has now been identi"ed in other algae, including diatoms (Volkman et al., 1993) and prymnesiophytes (Conte et al., 1994). Hence, interpretation of sterol assemblages in sediments is still complex and tentative; sterol distributions are not necessarily diagnostic for particular sedimentary environments (Volkman, 1986). Furthermore, some sterols

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(e.g. 24-ethylcholest-5-en-3-ol; 13) may derive from terrestrial sources (Nishimura, 1978). Eight of the 12 cores (not including 12695d8, 409 m and those at the 1000 m site) have remarkably similar sterol distributions (e.g. Fig. 6a), although the relative abundance of individual sterols, with respect to total lipids, does vary. The distributions of the sterols are consistent with a mixed phytoplankton and invertebrate origin.

Fig. 6. Distributions of sterols at the Oman Margin: (a) Mean relative abundances of sterols from eight sediment cores (see text). Error bars represent $one standard deviation from the mean. (b) 12695d8, 409 m. (c) 12706d1, 1002 m. Key: (a) 27-norcholesta-5,22-dien-3b-olH, (b) 27-norcholest-22E-en-3b-ol, (c) cholesta-5,22-dien-3b-olH, (d) 22E-cholesten-3b-ol, (e) 5-cholesten-3b-ol, (f) cholestan-3b-ol, (g) 24methylcholesta-5,22E-dien-3b-ol, (h) 24-methylcholest-22E-enol, (i) 7-cholesten-3b-ol, (j) 24-methylcholest-5-en-3b-ol (13) (k) 24-methylcholestan-3b-ol, (l) 4a-methylcholestan-3b-ol, (m) 24-ethylcholesta5,22E-dien-3b-ol, (n) 24-ethylcholesta-5,7-dien-3b-ol, (o) 24-ethylcholest-22E-en-3b-ol, (p) 24-ethylcholest-5-en-3b-ol, (q) 24-ethylcholestan-3b-ol, (r) 4a,23,24-trimethylcholst-22E-en-3b-ol (12), (s) 24propylcholesta-5,22E-dien-3b-ol, (t) 24-ethylcholest-7-en-3b-ol, (u) 24-propylcholest-5-en-3b-ol. H22E and Z isomers included together.

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For example, 24-methylcholesta-5,22-dien-3-ol is a common sterol in diatoms (Volkman, 1986) and prymnesiophytes (Goad, 1983; Volkman et al., 1981), dinosterol in dino#agellates and some other phytoplankton (see above), whilst cholest-5-en-3-ol and its dehydro counterparts cholesta-5,22(E)-dien-3-ol and cholesta-5,22(Z)-dien-3ol could be derived from zooplankton and/or benthic invertebrates (Goad, 1978 and references therein). The sterol distribution within core 12695d8 (Fig. 6b) is distinct from the other cores at 400 m, having a lower diversity of sterols (15) and a greater abundance of the *5 and fully saturated (*0) compounds. The latter are often presumed to be derived from the former via reduction in anoxic environments (e.g. Wakeham and Beier, 1991). Taken with the distribution of fatty acids and PUFAs (discussed above) it seems clear that the OM of this core is more degraded than that of any other site. The core almost certainly sampled a `relica sediment surface that has been exposed by sediment movement, for example via slumping. Its presumed greater age and, therefore, longer exposure to microbial activity probably accounts for its unique sterol composition. The sterols of the 1000 m site have a remarkable distribution (e.g. 12706d1; Fig. 6c), compared to other cores on the margin, since they are dominated by cholest5-enol, cholesta-5,22(Z)-dien-3-ol and cholesta-5,22(E)-dien-3-ol, common sterols of invertebrates (Goad, 1978) and 24-ethylcholest-5-enol with only minor contributions from other phytosterols (e.g. dinosterol). This signature has been ascribed to benthic activity and modi"cation of the sediments by the large population of mobile invertebrate megafauna that characterise that site (Encephaloides sp., a spider crab and the brittle star, Ophiolimna antarctica; Smallwood et al., 1999). 3.4.5. Glyceryl ethers Glyceryl ethers (e.g. 14) are present in very low relative abundance (;1% of total lipids) and are only detectable at the 400 and 800 m sites. Their precise source is again, impossible to ascribe de"nitely, since they derive from a wide variety of sources, having been identi"ed in bacterial membranes (Wakeham, 1982) benthic invertebrates (Santos, 1994) and other marine animals (Koizumi et al., 1990; Isay et al., 1976; Hallgreen and Larsson, 1962). We speculate that the benthic macrofauna is the most likely source of glyceryl ethers at the 800 m site, since this has one of the highest abundances of macrofauna at the margin (Gage, 1995), including large densities of polycheates (2112 m~2; Levin and Edesa, 1997). 3.5. Allochthonous biological markers A number of biological markers that could be ascribed to terrigenous OM (TOM, Hedges et al., 1997) have been identi"ed in the Oman Margin sediments, namely the long-chain waxy n-alkanes, n-alkanols and n-alkanoic acids (Santos et al., 1994; Westerhausen et al., 1993; Eglinton and Hamilton, 1967). 3.5.1. n-Alkanes Contributions of n-alkanes to the sediments at this margin are very minor and their absolute quantities and distributions are highly variable. For example, the carbon

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preference index (CPI; +(odd n-alkanes C }C )/+(even n-alkanes C }C ); 23 31 22 30 Poynter and Eglinton, 1990) ranges from 0.18 to 2.01 within the three replicate cores analysed from 400 m water depth. The n-alkanes of the sur"cial sediments with the highest CPI might be ascribed to a higher plant source, but their distribution is unusual, being dominated by n-C , with a virtual absence of the higher homologues. 29 The n-alkanes within this core are very minor components (7 lg g~1 TOC) and are minor relative to other compound classes. Their unusual distribution may therefore, be caused by uncertainty in their quanti"cation. The cores with the most obvious higher plant input within the margin are from 400 (12695d8) and 1250 m (12725d5) water depth and both show a unimodal distribution (not shown) with relatively low CPI's of 1.22 and 1.46, respectively, maximizing at C . Similar distributions of 31 C }C n-alkanes have been attributed to the bacterial community of Thioploca in 20 35 shelf and slope sediments underlying the coastal upwelling o! Peru (Volkman et al., 1981; Telkova et al., 1976). Thioploca also was identi"ed in sediments underlying the OMZ at the Oman Margin (Gage, 1995). We suggest that it may contribute n-alkanes to the sediments, overprinting an allochtonous signature, thus leading to the depressed CPI values. 3.5.2. n-Alkanols Absolute concentrations of n-alkanols are variable, tending to decrease across the margin, but their distributions are similar at all the sites (not shown), generally ranging from C to C with a strong even/odd carbon number predominance and 14 32 a maximum at C or C . The distributions are unimodal, with the exception of the 22 24 cores 12698d3 (422 m) and 12695d8 (409 m), which have no modality. Whilst n-alkanols with chain lengths greater than C may derive from TOM, they 21 also can be ascribed to algal, faunal or bacterial sources (Sargent et al., 1981; Sargent et al., 1977; Lee and Loeblich, 1971). The Oman Margin distributions are not typical of higher plants, where the mean carbon numbers are normally higher (Westerhausen et al., 1993) and their source(s) in these sediments cannot be de"nitely ascribed. The dominance of the C homologue suggest a primarily marine origin, although there 22 may well be a subordinate higher plant-derived signal. 3.5.3. Fatty Acids High-molecular-weight fatty acids may be derived from allochthonous OM (Poynter and Eglinton, 1990). In the Oman Margin samples, they are subordinate to the low-molecular-weight compounds in every core (e.g. Fig. 5a and b), with the exception of one core from the 1250 m site (12723d5; 1252 m), where the distribution is dominated by high-molecular-weight fatty acids (not shown). The total input of allochthonous fatty acids to the sediments is also minor. 3.6. Origin of OM in the Oman Margin Sediments Primary productivity in the northwest Arabian Sea is the highest in the world oceans, with a maximum rate of up to 6 g C m~2 d~1 (Owens et al., 1993) during the SW monsoon. At its peak, the majority of phytoplankton production ('90%) within

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the upwelling area o! Oman is associated with cells greater than 5 lm, and includes coccolithophores, diatoms and dino#aggelates (Owens et al., 1993). During the intermonsoon and less intense winter monsoon (NE monsoon), the water column dynamics lead to more oligotrophic conditions (Burkhill et al., 1993). Productivity is still intense, but with the decrease in nutrient concentrations the signi"cance of picoplankton increases within the sur"cial waters (Passow et al., 1993). Spatial and temporal variability of primary productivity is considerable (Jochem et al., 1993), but decreases eastwards from the centre of intense upwelling, towards the oligotrophic central gyre, where it is less than 0.3 g C m~2 d~1 (Owens et al., 1993). The biological markers (non-speci"c and speci"c) ascribed to primary production in sediments at this margin contribute signi"cantly to the OM within the sediments at three sites (400, 800 and 1250 m; up to 27% of total lipids within these cores; Fig. 7), but have extremely variable distributions. Only phytol shows a signi"cant relationship with water depth, increasing in relative abundance vs. the total lipids (p(0.05) away from the shelf break (Fig. 8). At "rst sight, this appears paradoxical, in that primary production decreases away from the shelf break. However, phytol is labile (Bradshaw and Eglinton, 1993) and intense biological activity either in the water column or in sur"cial sediments would be expected to lead to its degradation. Hence, the increase in its relative concentration downslope most likely re#ects a decrease in the extent of water column re-working, and presumably in the residence time of sinking particles in the water column, with increasing distance from the shelf-break. Other markers for primary production, such as the PUFAs (3) (Bradshaw and Eglinton, 1993) and the C (2) branched ketone are extremely labile (Volkman et al., 18 1981; Brooks et al., 1978), and a relatively more rapid rate of degradation for them (vs. phytol) could explain their more variable and patchy distribution in the sediments.

Fig. 7. Summary of sources of sur"cial sediments to sediments at the Oman Margin. Pies areas are proportional to the total lipids concentrations as determined by GCMS.

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Fig. 8. Phytol concentrations as a percentage of total lipids vs. water depth.

Zooplankton grazing is an important limitation on primary production in the upwelling zone. For example, the copepod Calanoides carinatus is the dominant grazer o! the Somalian coast, where heavy grazing by metazooplankton accounts for up to 50% of primary production (Passow et al., 1993). Surprisingly, the biological markers do not re#ect the intense zooplankton grazing, at least in the sediments underlying the OMZ. There may be a number of explanations for this. Biological markers are rarely source speci"c, as discussed above, and the mixing of the zooplankton and algal signatures precludes quanti"cation of the e!ects of zooplankton feeding. Furthermore, the algal signal could also be so strong that it e!ectively swamps any input from zooplankton. However, the most likely explanation for the limited zooplankton signature is that the sediments re#ect the intense biological activity in the water column. Drogue sediment traps deployed at the Oman Margin during the spring inter-monsoon period (Passow et al., 1993), showed that only a minor part of trap material was from faeces; the largest fraction was from highly fragmented and degraded material. OM within the upper water column is thought to be e$ciently recycled and modi"ed by a complex food web (Passow et al., 1993) before being lost to the sediments. At the deepest site the relatively higher concentration of phytol may be an indication of decreasing water-column reworking of large particles, with increasing distance o!shore. The Arabian Sea supports a substantial bacterial community in the water column, which can remineralize a large fraction of primary productivity, even during the SW monsoon (Azam et al., 1994). Approximately 50% of primary production is thought to be forced through a microbial loop via dissolved organic matter (DOM) where the OM can be e$ciently remineralised by bacteria (Azam et al., 1994). Hence, it is not surprising that the bacterial biomarkers are re#ected in the sediments (Fig. 7). On the other hand, benthic bacteria are not well quanti"ed, although they undoubtedly contribute signi"cantly to the benthic biomass. There is no correlation between the branched acid and hopanoid concentrations, which con"rms that they arise from di!erent bacterial communities, i.e. anaerobic vs. aerobic, or benthic vs. pelagic, or are subject to di!ering rates of degradation, or that their relative concentrations in some way re#ect the intensity of the OMZ, or a combination of all of the above. If the branched acids are primarily derived from anaerobes and the hopanoids from

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aerobes, then the contrasting distributions may simply re#ect the intensity of the OMZ downslope, with increasing oxygen concentration with distance from the shelf break being re#ected by an increase in hopanoid abundance. In the absence of `end-membera data for TOM, it is di$cult to quantify allochthonous OM inputs to the Oman Margin sediments (cf. Prahl et al., 1994). However, the most striking conclusion, is that the allochthonous OM inputs are extremely patchy and show no relationship with distance from land. Presumably, TOM at the Oman Margin is mainly derived from aeolian dust transported to the Arabian Sea via the monsoonal winds and transferred to the water column by wet deposition (Ittekot et al., 1992). The patchiness of the sedimentary signal of allochthonous OM may re#ect, in part, the variability in strength of the aeolian signal and `swampinga by the sedimentation of autochthonous OM, which may itself be spatially variable. The patchiness also may arise from the highly complex water column dynamics, which certainly appear to a!ect the autochthonous OM.

4. Conclusions The data presented in this paper arise from one of the "rst detailed molecular investigations of replicate sur"cial sediments from the Oman margin. The principal objective was to elucidate the major sources of OM to the sediments, which are summarised in Fig. 7. The main characteristics of the sediments within and just below the OMZ are summarised below: (1) The major portion of OM to the sediments is from an autochthonous origin. (2) A minor, variable and patchy, allochthonous signal, presumably derived from aeolian transport, is identi"able within the sediments but does not show correlation with distance from land. (3) High abundances of productivity indicators re#ect the level of primary production within overlying waters. The composition of biological markers is consistent with inputs from diatoms, dino#agellates, coccolithophores, Eustigmatophycae and cyanobacteria. Their relative concentrations within and between sites are highly variable and probably re#ect the spatial and temporal variability of primary productivity and the complexity of processes controlling sedimentation from the sur"cial waters. (4) The lipid biomarkers do not provide evidence of intense reworking by zooplankton within the euphotic zone; this may re#ect the rapid disaggregation of large faecal particles in the water column. (5) The distribution of sterols at the 1000 m site is signi"cantly di!erent to any other site, having a high proportion of invertebrate markers, whilst their concentrations are much lower. This probably arises from benthic reworking by the abundant megafauna at that site. (6) The bacterial signal allows a tentative distinction between a pelagic (aerobic?) and benthic (anaerobic?) signal, the former increasing in relative importance with increasing water depth. The observed trend mirrors the intensity of the OMZ at the margin.

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Acknowledgements We are grateful to the crew and master of RRS Discovery for their assistance at sea and to Ms. Jane Barnard, Mrs. Doris Angus and Dr. Anu Thompson for help in the laboratory. The work was supported by NERC small grant GR9/1545&A'; BS thanks NERC for a Studentship.

Appendix Structures

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