Coupled primary production, benthic foraminiferal assemblage, and sulfur diagenesis in organic-rich sediments of the Benguela upwelling system

Marine Geology 163 Ž2000. 27–40 www.elsevier.nlrlocatermargeo

Coupled primary production, benthic foraminiferal assemblage, and sulfur diagenesis in organic-rich sediments of the Benguela upwelling system Volker Bruchert ¨ b

a,)

, M. Elena Perez ´ b, Carina B. Lange

b

a Max Planck Institute for Marine Microbiology, 28359 Bremen, Germany Geosciences Research DiÕision, Scripps Institution of Oceanography, La Jolla, CA 92093-0244, USA

Received 30 November 1998; accepted 30 July 1999

Abstract Episodically deposited, dark, organic-rich Pleistocene and Late Pliocene sediments from the lower continental slope off southwest Africa reveal complex interactions between changes in primary production, benthic foraminiferal assemblage, and anaerobic microbial processes. The organic-rich layers contain diatom assemblages characteristic of intense seasonal coastal upwelling whereas stratigraphically adjacent sediments reflect pelagic primary production. Coastal upwelling-dominated depositional intervals coincide with periods of enhanced carbon flux to the seafloor. Enhanced organic carbon export during dark layer deposition was accompanied by decreases in the diversity of benthic foraminifera to few opportunistic species adapted to high phytodetritus accumulation rates and low O 2 conditions. In all sediments the sulfur isotopic composition of pyrite indicates redox cycling of sulfide close to the sedimentrwater interface. The sulfur isotopic evidence and the permanent presence of abundant low O 2-adapted benthic foraminifera throughout the organic-rich layers suggest an oxygenated benthic environment. Efficient oxidation of sulfide and removal of sulfide by sulfidization of organic matter inhibited buildup of toxic hydrogen sulfide from bacterial sulfate reduction at the sedimentrwater interface. These data imply that in continental slope sediments underneath productive surface waters benthic dysoxic conditions are maintained by the lateral advection of dissolved oxygen to support a small, but well-adapted benthic community. q 2000 Elsevier Science B.V. All rights reserved. Keywords: Benguela current; diatoms; benthic foraminifera; organic carbon; carbon isotopes; pyrite; sulfur isotopes; benthic oxygenation

1. Introduction Despite the small areal extent of ocean margin upwelling systems, burial of organic matter in these environments accounts for a significant portion of the worldwide burial of organic carbon Že.g., Hen)

Corresponding author. Fax: q49-421-2028690; e-mail: [email protected]

richs and Reeburgh, 1987.. Preservation of organic matter in marine sediments is generally regarded to be controlled by grain size, primary productivity, sediment reworking, sedimentation rates, and the potential for aerobic bacterial degradation Že.g., Muller and Suess, 1979; Bralower and Thierstein, ¨ 1984; Emerson and Hedges, 1988; Pedersen and Calvert, 1990; Canfield, 1993; Arthur et al., 1998; Mayer, 1999.. In sulfidic sediments, the early diage-

0025-3227r00r$ - see front matter q 2000 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 5 - 3 2 2 7 Ž 9 9 . 0 0 0 9 9 - 7

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netic sulfidization of organic matter has been recognized as an additional pathway for the preservation of organic carbon ŽSinninghe Damste´ et al., 1989.. Although all these processes contribute to the preservation of organic matter, their relative importance and their relationship to each other remain uncertain. For an assessment of the intensity of primary production, the relative abundances of diatom species indicative of coastal upwelling are well-suited because diatoms outcompete other primary producers for nu-

trients in young, newly upwelled waters ŽPitcher, 1990.. Less productive pelagic waters, in contrast, are generally dominated by calcareous phytoplankton production ŽPitcher et al., 1991.. The relative proportion of calcareous to coastal upwelling-derived siliceous phytoplankton thus allows a qualitative assessment of the intensity in primary production. Significant progress has been made in the use of abundance and isotopic composition of sedimentary sulfides to reconstruct the intensity of anaerobic

Fig. 1. Location of Site 1084 on the southwest African margin.

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decomposition by sulfate-reducing bacteria Že.g., Zaback et al., 1993; Habicht and Canfield, 1997.. By contrast, no reliable geochemical proxy is available to reconstruct the amount of the total oxygen uptake in buried marine sediments required for aerobic respiration and oxidation of dissolved inorganic compounds. For a qualitative assessment of the paleobenthic oxygen demand, benthic foraminifera are well-suited because they are sensitive in abundance and assemblage to organic carbon flux and bottom water oxygen content ŽLoubere, 1991; Mackensen et al., 1993; Bernhard et al., 1997.. The present paper describes a multidisciplinary approach to assess the relative importance of primary production, aerobic and anaerobic benthic processes that produced organic-rich sediments drilled during Leg 175 of the Ocean Drilling Program ŽODP.. ODP Site 1084 is located at 2000 m water depth on the lower continental slope in the Benguela upwelling system of the Northern Cape Basin ŽFig. 1.. At Site 1084 present-day sediment accumulation occurs underneath a filament of cold, nutrient-rich upwelling ŽShanwaters that extends far offshore from Luderitz ¨ non and Nelson, 1996.. Sediments at Site 1084 contain numerous pronounced cyclic color changes from olive, foraminifer-bearing nanofossil clays to dark olive brown, foraminifer- and diatom-bearing organic-rich clays. Individual dark layers are between 30 cm and 4 m thick, and are interpreted as intervals of elevated marine paleoproductivity ŽWefer et al., 1998.. The alternating occurrence of moderately organic carbon-rich and very organic-rich layers in this core make these sediments suitable for a study of the relationships between varying primary productivity and resulting benthic and anaerobic bacterial processes. 2. Materials and methods 2.1. Sampling Sediments were collected from three dark layers in Hole 1084A. Two of these layers were sampled in the Pleistocene section Ž3H and 5H., and one layer was sampled in the Late Pliocene section Ž43X.. One sample each was taken above and below the dark layers, and the remaining samples were collected at equal intervals across the layers.

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2.2. Analytical methods Total carbon and total sulfur were determined with a Carlo Erba CHN Elemental Analyzer NA 1500 by direct combustion of 1–5 mg of ground, freeze-dried sediment. For analysis of organic carbon, another 1–5 mg of ground, freeze-fried sediment were weighed and subsequently treated with 1 N HCl in silver cups for 12 h. The residue was dried at 558C, and analyzed for carbon concentration as above. Carbonate carbon was determined by difference. Analyses were done as duplicates and are reported as averages. For analysis of pyrite and organic sulfur, approximately 2 g of dry, ground, freeze-dried sediment was extracted by ultrasonification three times for 15 min with 15 ml of 2:1 Žvrv. analytical grade dichloromethanermethanol to remove free lipids, elemental sulfur, and free polysulfides ŽBruchert et al., 1995.. This procedure trans¨ forms free polysulfides to elemental sulfur, mostly in the form of cyclooctasulfur. An aliquot was filtered through Whatman GFrC filters and analyzed as S 8 by high-performance liquid chromatography using a Sykam pump ŽS1100., an UV–visible detector ŽSykam S3200. and a Zorbax ODS-column Ž125 = 4 mm, 5 mm; Knauer, Germany.. Methanol Ž100%; LiChrosolv w , Merck. at a flow rate of 1 mlrmin was used as the eluent. Cyclooctasulfur was detected at 265 nm, the detection limit was 1 mM. The dry sediment residue was subsequently extracted with 6 N HCl with 5 ml 10% SnCl 2 under N2 to extract acid-volatile monosulfides ŽAVS.. Evolved H 2 S was trapped in 0.1 N AgNO 3 as Ag 2 S. After AVS extraction, 12 ml of 1 M acidic CrCl 2 solution were added and the slurry was boiled for 1 h to dissolve pyrite. Microscopic observation of the filtered sediment residue showed that over this extraction time complete reduction and dissolution of pyrite had occurred. Evolved H 2 S from chromium reduction was trapped in AgNO 3 as described above, and represents the Cr-reducible sulfur fraction ŽCRS.. Since AVS, elemental sulfur, and free lipid-bound sulfur were extracted before, the CRS fraction contained only pyrite-bound sulfur, and the residual sediment only contained sulfur bound to residual insoluble organic matter. The difference between total sulfur, and the sum of AVS, CRS, and elemental sulfur is interpreted as organic sulfur although

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some lipid-bound organic sulfur remains unaccounted for. This fraction, however, rarely comprises more than 5% of the total sedimentary sulfur ŽBruchert et al., 1995.. Triplicate extraction analyses ¨ of 10 selected samples indicated that the measured concentrations of sulfur species agree within 10%. The carbon isotopic composition of organic carbon was determined after treatment of 500 mg of sediment overnight with 2 N HCl. Residue was washed repeatedly with double-deionized water to remove most of the acid. The carbon isotopic composition of the residue was determined by combustion in a Heraeus elemental analyzer interfaced with a Finnigan Mat mass spectrometer. The sulfur isotopic composition of Ag 2 S representing the CRS fraction was also determined by GC-combustion mass spectrometry. Accuracy for d13 C is 0.15‰, and 0.2‰ for d 34 S. Isotopic values for carbon and sulfur are reported in the standard delta notations for

d13 C s

žŽ

13

Cr12 C . sampler Ž 13 Cr12 C . PDB y 1 10 3

žŽ

34

Sr32 S . sampler Ž 34 Sr32 S . CDT y 1 10 3

/

and

d 34 S s

/

The degree of pyritization ŽDOP. was determined by boiling 0.2 g of sediment in 5 ml 12 N HCl for 1 min ŽBerner, 1970.. The leachates were diluted 100fold and analyzed for their iron concentration by atomic absorption spectrometry. DOP is reported as Fe CRSrŽFe HCl q Fe CRS . after correction of Fe HCl for FeAV S which is extracted during the 12-N HCl leach. Fe analyses were done in triplicate and are reported as averages. Relative abundances of diatoms and nanofossils as well as diatom species identification were determined from smear slides. For benthic foraminifera analyses, samples were washed over a 63-mm sieve and dried. Subsequently, the coarse fraction Ž) 150 mm. was sieved and aliquots from this fraction were analyzed. The 150-mm size fraction excludes populations of smaller foraminifera that may form significant populations in oxygen-depleted sediments ŽMoodley et al., 1997.. However, early diagenesis, compaction and burial likely affect small, thinshelled, fragile foraminifera more than larger,

thicker-walled foraminifera. We consider this effect to introduce more bias to interpretations than that introduced by excluding smaller size fractions. The 150-mm size fraction was therefore selected because it represents a compromise between these two obscuring aspects. Identification of the benthic foraminiferal fauna followed taxonomic concepts used in Mackensen et al. Ž1990; 1993. and Schmiedl Ž1995.. The Shannon–Weaver H Ž S . diversity index was used to estimate benthic foraminiferal diversity ŽShannon and Weaver, 1949..

3. Stratigraphy and sedimentation rates In Hole 1084A, the youngest identified stratigraphic datum occurs at 48.65 mbsf. This datum is defined by the calcareous nanoplankton Gephyrocapsa caribbeanica and suggests an age of 0.26 Ma ŽGiraudeau et al., 1998.. However, datum events are only constrained to within 3 m. Furthermore, the shipboard biostratigraphic age model does not reveal short-term changes in sedimentation rates. Here we use a refined age model for 1084A ŽVidal, personal communication. that uses high-resolution Ž4 cm. shipboard measurements of total sediment color reflectance and magnetic susceptibility ŽWefer et al., 1998.. These data reveal a characteristic cyclic pattern that can be used for lateral correlation with ODP Hole 1082A ŽVidal et al., 1998. for which high-resolution oxygen isotope data are available. Comparison of the color reflectance data of Hole 1084A with those of Hole 1082A suggest complete recovery of the uppermost 50 m of stratigraphic section. The age model for site 1084A was constructed by correlating the color reflectance profiles of Holes 1084A and 1082A. This age model was then used to calculate mass accumulation rates ŽMAR; grm2ra. for organic carbon and carbonate carbon using wet bulk densities and porosities determined on board during Leg 175 ŽWefer et al., 1998.. Table 1 lists the oxygen isotope stage age assignments for each dark layer, respective linear sedimentation rates, estimated ages at the top of each dark layer, and the duration of deposition for each dark layer. Recent determination of a high-resolution oxygen isotope profile ŽVidal, personal communication. for the uppermost 50 m for

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Table 1 Age assignments, length of deposition, and sedimentation rates for the three dark layers

Oxygen isotope stage Sedimentation rates Ages at top of dark layer Length of deposition

1084A-3H Ž19.5–21.1 mbsf.

1084A-5H Ž37.2–40.2 mbsf.

1084A-43X Ž385.7–390.6 mbsf.

5A–5C 22.5 " 3.5 cmrka 74–107 ka 7.2 " 1 ka

7.4 16.7 " 0.2 cmrka 224–237 ka 17.9 " 0.2 ka

; 18.7 cmrka 2.33 Ma ; 26 ka

Site 1084A showed good agreement between the two independently derived age models.

4. Results MAR for organic carbon increase in the dark layers 3H and 5H whereas in the dark layer 43X accumulation rates of organic carbon increased only slightly ŽFig. 2A.. Across all layers, MAR for organic carbon and carbonate carbon are inversely proportional. In general, increases in organic carbon accumulation rates correspond to higher relative abundances of diatoms in the dark layers, especially of the genus Chaetoceros Žspores and setae preserved., while lower organic carbon accumulation rates above and below the dark layers proper correspond to higher relative abundances of calcareous nanofossils ŽFig. 2B.. Diatoms attain relative abundances of 20–40% within dark layer 3H, and the assemblage is dominated by Chaetoceros resting spores and T. nitzschioides var. nitzschioides. In contrast, relative abundances of diatoms in dark layer 5H are very low Ž2–5%., and only two moderate Chaetoceros peaks occur ŽFig. 2B.. Nanofossils are generally more abundant in 5H than in 3H ŽFig. 2B.. However, in this layer the major group of organisms responsible for the highest organic carbon accumulation rates at 38.66 and 38.96 mbsf is not known. It is possible that some calcareous nanofossils and diatom shells were dissolved after deposition. An alternative explanation may be that soft-shelled primary producers such as dinoflagellates were the dominant primary producers in these samples. Dark layer 43X is distinct from the other two layers. The dark color can largely be attributed to the disappearance of calcareous fossils rather than to an increase in organic

carbon accumulation rates ŽFig. 2A.. In contrast to the foraminifer- and nanofossil-dominated Pleistocene sediments above and below the dark layers 3H and 5H, diatoms dominate the stratigraphic interval in the Late Pliocene ŽWefer et al., 1998.. Here, the sediments are rich in the antarcticrsubantarctic needle-shaped diatom Thalassiothrix antarctica ŽLange et al., in press.. As was the case for dark layer 3H, Chaetoceros spores are relatively more abundant within the dark layer proper than above or below it ŽFig. 2B.. Abundances of benthic foraminifera vary strongly and are not correlated with organic carbon accumulation rates or relative abundances of Chaetoceros ŽFig. 2B. suggesting that postdepositional dissolution affected overall benthic foraminiferal abundances. However, for the dark layers 3H and 5H it appears that dissolution was not extensive except for two samples because thin-shelled species, such as Chilostomella oÕoidea, Globobulimina spp. and Nonionella spp. are present throughout the layers in variable amounts. The diversity of benthic foraminiferal assemblages within the dark layers is low and increases towards the upper and lower boundaries ŽFig. 2C.. Epifaunal species adapted to high O 2 concentrations such as C. wuellerstorffi are present above and below the dark layers ŽFig. 2B.. The dark layers contain species specifically adapted to low O 2 concentrations and high organic carbon fluxes such as Bulimina, Nonionella, Globobulimina, Chilostomella, and UÕigerina Že.g., Sen Gupta and Machain-Castillo, 1993; Bernhard et al., 1997.. Bernhard et al. Ž1997. have also noted that Chilostomella and Nonionella live in bottom waters of the Santa Barbara Basin where concentrations of O 2 are less than 4.5 mM O 2 . Relative abundances of these species increase in the dark layers ŽFig. 2C., especially of B. exilis which dominates the benthic

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Fig. 2. ŽA. MAR of CaCO 3 and organic carbon in the dark layers 3H, 5H, and 43X. ŽB. Relative abundances of diatoms, nanofossils, Chaetoceros spp., and total number of benthic foraminifera per gram sediment. ŽC. Relative abundances of benthic foraminifera indicative of low O 2 conditions and high phytodetritus accumulation rates Ž Bulimina exilis and Epistominella smithi ., benthic foraminifera indicative of high O 2 conditions Ž Cibicidoides wuellerstorfi and Gyroidina soldanii . and benthic diversity index.

foraminiferal assemblage in the three dark layers with B. aculeata as the second most important constituent in dark layers 3H and 5H. Noteworthy is the

occurrence and abundance of E. smithi at the bottom of dark layer 3H. E. smithi is also well-adapted to oxygen-poor waters, as has been observed in the

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Fig. 3. ŽA. Concentrations of organic carbon, CRS representing pyrite-sulfur, and concentration of organic sulfur. ŽB. Stable sulfur isotopic composition of pyrite and stable carbon isotopic composition of organic carbon. ŽC. Total sulfur and organic sulfur expressed as percentage of total amount of sulfide produced by bacterial sulfate reduction. The total amount of reduced sulfate was calculated using depth-integrated 35-sulfate reduction rates from a nearby site by Ferdelman et al. Ž1999..

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California borderland basins ŽSen Gupta and Machain-Castillo, 1993.. In all sediments organic carbon ŽC org . and organic sulfur contents covary closely whereas concentrations of pyrite are relatively invariable when compared to organic carbon ŽFig. 3A.. d13 C values of organic carbon suggest that marine organic matter was the dominant source of organic carbon inside and outside the dark layers ŽFig. 3B.. Organic sulfur represents the dominant sedimentary sulfur species in these sediments. These results suggest that reactive organic matter could successfully compete with iron for dissolved sulfide. Such conditions are generally met when the formation of pyrite is limited by available reactive iron ŽMossmann et al., 1991.. Values of the DOP are generally less than 0.5 ŽTable 2.. These results are in agreement with findings by Morse and Emeis Ž1990. and would suggest that the formation of pyrite was not limited by reactive iron. Nevertheless, although our results indicate an excess of residual reactive iron, we suggest that the iron extracted by our method was not available for the formation of iron sulfides. A significant part of the extracted iron probably resides in robust iron minerals that could not be reduced over the time scales of sediment burial considered here. In all samples, the isotopic composition of pyrite is strongly depleted in 34 S, and is relatively invariable by comparison with the observed variation of pyrite in other sedimentary

Table 2 DOP values in the three dark layers starting at the top of each dark layer ŽDOPs Fe CR S rŽFe HCl qFe CRS . ŽBerner, 1970.. 1084A-3H

1084A-5H

1084A-43X

0.53 0.50 0.40 0.49 0.38 0.41 0.47 0.44 0.40 0.44 0.54

0.30 0.27 0.37 0.30 0.35 0.39 0.32 0.37 0.45 0.76 0.47

0.30 0.14 0.30 0.40 0.55 0.43 0.34 0.37 0.52 0.45 0.30 0.20 0.26 0.18

sequences of organic-rich sediments ŽFig. 3C. ŽZaback and Pratt, 1992; Bruchert et al., 1995.. ¨

5. Discussion 5.1. EÕidence for increased primary production The composition of the dark layers reflects an intimate link between organic carbon accumulation rates and the intensity of coastal upwelling. We believe that the abrupt shift from nanofossil-rich sediments below the dark layers to Chaetoceros-rich sediments within the dark layers reflects a sudden change in paleocirculation patterns. At present, young upwelled waters along the coast of west Africa are characterized by the dominance of chain-forming and colonial diatoms such as Chaetoceros Žsubgenus Hyalochaetae. and Thalassionema ŽProbyn, 1992; Treppke et al., 1996.. Spores of the genus Chaetoceros form a major component of the phytoplankton settling from the upper mixed layer, and have been shown to be effective in seeding newly upwelled waters ŽPitcher, 1990.. We consider them here as a proxy of cold upwelled waters transported to site 1084 by the Benguela Coastal Current. Sediments underlying the dark layers represent more pelagic environments of mature stratified upwelled waters whereas the dark layers proper represent environments with intense seasonal upwelling. Site 1084 is located in close vicinity to the Luderitz upwelling ¨ cell, within reach of the upwelling in the frontal zone between the Benguela Coastal Current and the Benguela Oceanic Current. Sediments deposited in this setting record the relative strength and areal extent of the coastal and pelagic primary production signals. The dark layers 3H and 5H were deposited in interglacial time periods, but not during full interglacials ŽVidal, personal communication.. Several characteristics of sediment accumulation during these time periods could have contributed to an enhancement of organic carbon accumulation rates. Ž1. Increase in the strength of trade winds could have enhanced wind-driven coastal upwelling ŽSchneider et al., 1997.. Ž2. A slight drop in sea level compared to full interglacials would have caused a seaward shift of coastal upwelling ŽSummerhayes et al., 1995..

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Ž3. This drop in sea level may have also exposed the coastal diatomaceous belt to the wave base resulting in redeposition of near-shore material on the continental slope ŽSummerhayes et al., 1995.. Of the three scenarios, the third is considered of minor importance. No benthic foraminifera and diatoms indicative of near-shore shallow water environments were observed. The latter had the same abundances inside as outside the dark layers. High abundances of Chaetoceros spores have been interpreted as reflecting lateral advection from shelf sediments at DSDP Site 532 on the Walvis Ridge rather than the occurrence of upwelling per se ŽSancetta et al., 1992.. However, the good preservation of setae and delicate surface ornaments of the spores in our material do not support that possibility. Scenarios Ž1. and Ž2. are difficult to differentiate. A slight drop in sea level would have pushed winddriven coastal upwelling near Luderitz further off¨ shore making it likely that the coastal upwelling signal over Site 1084 became stronger. However, the different primary producer assemblages in dark layers 3H and 5H suggest different spatial arrangements of young and mature upwelled waters for these time periods. Alternatively, they may also indicate differences in the strength of coastal upwelling and the influence of the offshore filament from the Luderitz ¨ upwelling cell. In dark layer 3H, the year-round biogenic accumulation was dominated by diatoms which tend to flourish in young upwelled waters. By contrast, in dark layer 5H slight variations in the position of young vs. mature upwelled waters may have resulted in the alternating presence of coccoliths and Chaetoceros spp. Also, non-siliceous, noncalcareous phytoplankton Že.g., flagellates, dinoflagellates. may have dominated the export production in this dark layer for which we do not have a preserved record ŽFig. 2A and B.. In all dark layers, however, overall primary production increased. 5.2. Benthic foraminifera species as benthic oxygen indicators For the following discussion we follow the terminology for benthic oxygenation discussed in Fenchel and Finlay Ž1995.. We use the term anoxic to indicate environments that have dissolved oxygen con-

35

centrations less than 4.5 mM O 2 , dysoxic when concentrations of dissolved oxygen are between 4.5 and 23 mM, and oxic when oxygen concentrations exceed 23 mM. Suboxic conditions describe sediments that have O 2 concentrations less than 4.5 mM, but that are not chemically reducing. Field and experimental studies have demonstrated survival of benthic foraminifera in environments with O 2 concentrations less than 4.5 mM and under sulfidic conditions for up to 30 days ŽBernhard, 1993; Bernhard and Alve, 1996; Moodley et al., 1997.. However, survival of foraminifera in anoxic or even sulfidic sediments over geologic time periods is unlikely. Benthic foraminifera that are adapted to very low O 2 concentrations likely have a high affinity for O 2 and will thus contribute to maintaining very low O 2 concentrations that are below the detection limit for presently available analytical systems for oxygen determination ŽKuhl ¨ and Revsbech, in press.. Furthermore, ODP Site 1084 is located at 2000 m water depth. At these depths, seasonal bottom water ventilation is unlikely ŽReimers et al., 1990.. Such shortterm ventilation events occur in shallower, partially enclosed basins with seasonal anoxic conditions such as the Santa Barbara Basin, CA, and permit the survival of low O 2-adapted species ŽBernhard and Reimers, 1991.. For the sediments investigated here, the continuous presence of foraminifera suggests that oxidants were present at and just below the sedimentrwater interface and that near-zero sulfide concentrations were maintained. We cannot exclude short-term anoxic events or even the occasional buildup of sulfidic benthic conditions for these sediments, but given the length of deposition of the dark layers, suboxic conditions probably existed at the sedimentrwater interface for most of the time. Thus, despite a substantial increase in organic carbon accumulation rates in the dark layers 3H and 5H, oxidants in the form of free oxygen, nitrate, or oxidized manganese and iron must have always been present in the uppermost sediment layer. Unfortunately, benthic foraminiferal assemblages cannot provide a more detailed assessment of the depth of oxygen penetration because of their vertical motility and specific vital adaptations to changing oxygen concentration and food supply ŽRathburn and Corliss, 1994; Alve and Bernhard, 1995; Schmiedl et al., 1997; Moodley et al., 1998.. In recent near-surface sediments off

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Namibia, high organic carbon concentrations can be found in the diatomaceous belt on the shelf where sulfidic bottom waters develop episodically ŽBremner, 1983.. For the lower continental slope sediments studied here it appears that the depth of oxygen penetration and the width of the suboxic zone became narrower but did not disappear even though organic carbon accumulation rates increased substantially. Apparently, the lateral supply of oxygen-rich bottom waters was sufficient to compensate for the increased benthic oxygen demand. 5.3. EÕidence from sedimentary sulfides for sulfur cycling For an interpretation of sedimentary sulfur contents it is important to consider not only the processes associated with bacterial sulfate reduction, but also those associated with sulfide oxidation ŽJørgensen, 1977.. Some of the highest rates of sulfate reduction have been measured in sediments where there is no free dissolved sulfide, a negligible depth gradient in sulfate, and where the amount of sedimentary sulfide is very small compared to the sulfate reduction rates ŽFerdelman et al., 1997.. In recent continental slope sediments from the Namibian continental margin, sulfide oxidation accounts for 20– 96% of the total oxygen consumption ŽFerdelman et al., 1999.. Conversely, increases in total sulfur contents do not require high rates of bacterial sulfate reduction. Instead, they reflect a greater efficiency of sulfide retention, which may or may not accompany a greater intensity of bacterial sulfate reduction. On the basis of total sulfur concentrations alone, these two processes cannot be separated. The efficiency of sulfide retention increases either in the absence of oxidants for sulfide oxidation, especially of dissolved oxygen, or if additional sulfide can be precipitated. In the dark layers we infer that the total amount of aerobically and anaerobically oxidized organic matter increased but that the amount of preserved organic carbon also increased. The close correspondence between organic sulfur and organic carbon contents suggest a link between organic carbon burial and the diagenetic sulfidization of organic matter ŽSinninghe Damste´ et al., 1989; Eglinton et al., 1994.. Dissolved sulfide and polysulfide produced

during bacterial sulfate reduction and subsequent partial oxidation of sulfide have been shown to react with organic matter to form secondary organosulfur compounds ŽKohnen et al., 1991; Schouten et al., 1994.. These sulfidized organic molecules appear to be less degradable than their unsulfidized counterparts ŽKohnen et al., 1991.. Diagenetic sulfidization of organic matter is now recognized as a major pathway leading to preservation of organic matter in anoxic marine sediments ŽTegelaar et al., 1989.. In the dark layers, a significant proportion of dissolved sulfide or partially oxidized intermediates such as polysulfides became bound to reactive organic matter. Excess sulfide that diffused upwards was oxidized below the sedimentrwater interface by reaction with dissolved oxygen, iron and manganese oxides, or nitrate. The net result was a narrower oxic zone at the sedimentrwater interface. A corollary of the above model is the implication that removal of sulfide through sulfidization of organic matter prevented the complete consumption of available oxidants by upward diffusing sulfide. To quantify the effect of sulfidization we determined the burial efficiency of sulfur, which is defined as the ratio between the accumulation rate of sedimentary sulfur and the total amount of reduced sulfate. Sulfate reduction rates were measured with the 35-sulfate radiotracer method in the uppermost 20 cm at a nearby site by Ferdelman et al. Ž1999.. Accumulation rates of sulfur were determined in analogy to the rates for organic carbon and carbonate. The results of these calculations indicate that the burial efficiency of total sulfur varied only between 3 and 13% ŽFig. 3C.. Thus, while organic sulfur formation increased the burial efficiency of organic carbon, the burial efficiency of sulfur only increased by about 10%. Even in the most organic carbon-rich sediments, over 87% of the dissolved sulfide were oxidized. d 34 S values of pyrite support the above interpretation. Except for one sample, the isotopic difference between pyrite and seawater sulfate for these sediments is always larger than 53‰. The isotopic fractionation between sulfate and sulfide achieved by bacterial sulfate reducers is to an extent rate-dependent, and greater at slow rates of sulfate reduction, but it has never been observed to be greater than 42‰ ŽHabicht and Canfield, 1997.. Greater isotopic differences between pyrite and sulfate can only result

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if a significant portion of dissolved sulfide is recycled into the sulfate pool by oxidation andror disproportionation ŽCanfield et al., 1998.. Thus, the isotopic values of pyrite restrict its formation to the uppermost centimeters, because only here oxygen and other oxidants such as manganese and iron oxyhydroxides or nitrate could have been available for sulfide oxidation ŽThamdrup et al., 1994.. Secondary pyrite formation deeper in the sediments appears to have been minor. The effective recycling of sulfide in the uppermost centimeters prevents a more quantitative assessment of the rates of bacterial sulfate reduction from the isotopic composition of pyrite. In these sediments, the rate dependence of the isotopic fractionation during bacterial sulfate reduction is overprinted by isotope effects during sulfide recycling.

6. Conclusions The present study reveals coupling between surface water productivity, benthic foraminiferal assemblages, and benthic microbial processes. Increased upwelling intensity caused a shift in the primary producer community from calcareous nanoplankton to diatoms and a shift of the benthic foraminiferal assemblage to few species adapted to low O 2 conditions and abundant phytodetritus. Previous interpretations have linked the accumulation of organic-rich sediments in upwelling regimes to the gradual development of sulfidic, benthic anoxia which were inferred to have enhanced the preservation of organic matter ŽSummerhayes, 1983; Bailey, 1991.. Furthermore, very low d34 S values of pyrite were used to support the presence of sulfidic bottom waters Že.g., Beier and Hayes, 1989.. In these lower continental slope sediments off Namibia, the continuous presence of benthic foraminifera support an interpretation of permanent, but very low benthic oxygenation despite very low sulfur isotopic values. Sulfidization of organic matter operated as a negative feedback mechanism buffering rates of bacterial sulfate reduction and increasing the overall preservation of organic carbon. Although organic sulfur formation increased the burial efficiency of organic carbon, it did not substantially increase the burial efficiency of

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sulfur. Oxygen transport into sediments was sufficient at all times to prevent complete oxygen consumption at the sedimentrwater interface by sulfide oxidation. These data have implications for the calculation of particulate organic carbon rain rates from benthic oxygen fluxes ŽGlud et al., 1994; Jahnke, 1996. because they suggest that organic carbon accumulation rates can become decoupled from the benthic oxygen flux. Our results suggest a very efficient microbial and chemical buffering system in the uppermost centimeters of continental slope sediments underneath productive surface waters. Ultimately, higher organic carbon accumulation rates will probably lead to sulfidic benthic environments, yet for sediments with organic carbon and sulfur distributions comparable to those analyzed here, sulfide-free, suboxic environments are sustained that are host to well-adapted benthic communities.

Acknowledgements We would like to thank the editor Michael Arthur and the reviewers Kay Christian Emeis and Joan Bernhard for providing constructive suggestions to this manuscript. Laurence Vidal shared information about the oxygen isotope stratigraphy at ODP Site 1082 and 1084 and helped with correlating Hole 1084A and Hole 1082A. We would also like to acknowledge Mattias Gehre for the sulfur isotope analysis of pyrite, and Monika Segl for the carbon isotope analysis of organic carbon. Tim Ferdelman and Tony Rathburn provided thoughtful comments on an earlier draft. This research was supported by JOI USSSP grants to V.B., M.E.P., and C.B.L., research funds from the Max Planck Society to V.B., and the Basque Country Government to M.E.P.

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