Episodic particle flux in the deep Sargasso Sea

Deep-Sea Research I 45 (1998) 1819—1841

Episodic particle flux in the deep Sargasso Sea: an organic geochemical assessment Maureen H. Conte,* J.C. Weber, Nathan Ralph Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, 360 Woods Hole Road, MS 25, Woods Hole MA 02543, USA Received 10 September 1997; received in revised form 26 January 1998; accepted 24 May 1998

Abstract Since 1978, the Oceanic Flux Program (OFP) time-series sediment trap study has continuously measured particle fluxes in the deep Sargasso Sea (31°50N, 64°10W). One feature of this 19# year record has been the episodic occurrence of large, short-lived flux maxima that are not associated with the annual spring bloom. These maxima generally occur during the Dec.—Jan. period, but not necessarily every year. They have also occurred in other seasons. In January 1996, OFP traps located at 3200 and 3400 m depths intercepted a major flux ‘‘event’’ in which there was an abrupt, threefold increase in mass flux at both depths. Mass flux measured at 3200 m during the event (87 mg m\ d\) was the highest recorded since biweekly resolved sampling was begun in 1989. Organic biomarker analyses of material collected prior to, and during, this high flux event determined that there was an abrupt change in material composition associated with the sudden flux increase. Prior to the event, cholesterol, a single bacteriaderived C hopanone (22,29,30-trisnorhopan-21-one), and saturated and odd/branched fatty  acids predominated: these compounds indicated that the sedimenting material was extensively degraded. During the event, organic material was greatly enriched in C —C phytosterols,   haptophyte algae-derived C —C alkenones, labile polyunsaturated acids, degradation prod  ucts such as steroidal ketones, and also in bacteria-derived compounds such as C —C   hopanoids and b and u!1 hydroxy acids. These compounds indicated the organic fraction contained a large amount of relatively fresh phytoplankton-derived debris and tracers of bacterial biomass and metabolism, which suggested that the sinking material was undergoing active bacterial decomposition. Thus, the flux ‘‘event’’ appears to have resulted from a shortlived bloom in the overlying surface waters which, for reasons not currently apparent, was inefficiently remineralized in the upper ocean and rapidly settled to depth. These findings are the first direct documentation of episodic delivery of labile phytoplankton-derived detritus to the deep ocean in an oligotrophic mid-gyre region. Such transient productivity/flux events may account for a significant fraction of the export flux of biologically available carbon and easily remineralized elements, not only in highly productive areas, but throughout the deep oceans.  1998 Elsevier Science Ltd. All rights reserved.

* Corresponding author. Fax: 001 508 457 2193; e-mail: [email protected]. 0967-0637/98/$—see front matter  1998 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 3 7 ( 9 8 ) 0 0 0 4 6 - 6

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1. Introduction As late as the 1970s, the deep ocean was considered to be a highly stable, quiescent environment. This view began to change when challenged by accumulating evidence of unexpected high species diversity and (apparently) seasonal cycles of reproduction and growth in bathypelagic animals (reviewed in Tyler, 1988; Gage and Tyler, 1991). However, the reasons for this enigmatic evidence of seasonality in the deep and, then presumed, constant environment of the deep ocean were not clearly understood. In 1980 and 1981, Deuser and Ross (1980) and Deuser et al. (1981) reported the existence of seasonal cycles in the flux of organic carbon and other elements at a depth of 3200 m in the Sargasso Sea. They went on to demonstrate that the seasonality in the deep flux was directly linked to the seasonality of primary production in the overlying waters. Since that time, seasonality in particle fluxes in the deep ocean has been found at numerous sites in the Atlantic and Pacific (e.g. Honjo, 1982, 1984; Honjo and Manganini, 1993). In the mid- and high latitude North Atlantic, there is a striking increase in deep particle flux associated with the large spring phytoplankton bloom (Honjo and Manganini, 1993; Newton et al., 1994). A pulse of labile ‘‘phytodetritus’’, sinking through the water column at rates of 100—150 m day\, arrives on the seafloor roughly a month or so after the spring bloom (Billet et al., 1983; Lampitt, 1985; Rice et al., 1986; Thiel et al., 1988/89). Phytodetrital material on the seafloor has also been found across a 10° latitude band in the equatorial Pacific centered at the equator; phytodetrital deposition in this instance was postulated to be associated with convergence due to equatorial upwelling (Smith et al., 1996). The rapid sinking of incompletely remineralized bloom components constitutes an important seasonal food source for benthic macro- and microfauna (Gage and Tyler, 1991; Campos-Creasey et al.,1994) and greatly enhances the flux of labile organic compounds and associated easily remineralized elements to the deep ocean. There is a marked increase in microbial biomass (Thiel et al., 1988/89; Conte et al., 1995) and biological activity (Graf, 1989; Gooday and Turley, 1990; Pfannkuche, 1993; Smith et al., 1994; Smith et al., 1996) as this labile material is remineralized, which enhances sediment mixing and O consumption rates (e.g. Smith and Baldwin, 1984; Smith et al., 1994; Gehlen et al.,  1997). In oligotrophic mid-gyre regions, it is less clear whether seasonal and higher frequency fluctuations observed in particle flux (Honjo and Manganini, 1993; Deuser, 1996) are similarly accompanied by the pronounced fluctuations in the quality of the organic material reaching the seafloor, as observed in more productive regions (e.g. Rice et al., 1994). For example, the sedimentary oxygen consumption rates off the California coast vary in concert with seasonal variations in particle rain rates (Smith, 1992), but sediment oxygen consumption rates at the oligotrophic Bermuda Atlantic Time-Series (BATS) site appear to exhibit little seasonality (Sayles et al., 1994). Resolving this question is important not only for assessment of variability in biological activity in the bathypelagic zone and sediments underlying oligotrophic waters but also for understanding the controls on fluxes and depth scales of remineralization for carbon and associated elements.

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Fig. 1. Biweekly resolved mass fluxes measured at 3200 m depth at the Oceanic Flux Program (OFP) time-series site from 1989 to April 1997. The width of the bar indicates the sampling interval for each collection. Note the occurrence of winter flux maxima in 1991, 1992, and Jan and Dec 1996. Mass flux data through mid 1994 are given in Deuser (1996).

Episodic, high flux ‘‘events’’ are a persistent feature of the 19#yr deep particle flux record of the Oceanic Flux Program (OFP) study site located in the western Sargasso Sea near the BATS site (Deuser, 1996). Short-lived flux maxima, which are better resolved with the biweekly sampling interval, are frequently observed December through January and occasionally in other seasons (Fig. 1). To ascertain the cause of a flux event observed in January 1996, we conducted organic geochemical analyses of the trap material collected prior to and during the event. The results presented here document an abrupt increase in the deep flux of labile phytoplankton-derived material and associated biomarkers of bacterial biomass and metabolism and suggest that this abrupt flux ‘‘event’’ resulted from a transient bloom in the overlying waters that, for reasons not currently apparent, was inefficiently remineralized and rapidly settled to depth. 2. Methods 2.1. Sample collection The Oceanic Flux Program (OFP) time-series sediment trap mooring is located in the western part of the Sargasso Sea gyre near 31°50N, 64°10W, approximately 75 km southeast of Bermuda. The hydrography of the region is characteristic of a large expanse of the North Atlantic gyre (Joyce and Robbins, 1996). There is a 19#year OFP record of particle flux at 3200 m, an 11#year record at 1500 m, and an 8#year record at 500 m. The temporal resolution of the flux samples is bimonthly from 1978 to 1989, and biweekly from 1989 to the present. The surface catchment area of the 3200 m trap is on the order of 4;10 km (Deuser et al., 1990; Siegel and Deuser, 1997). In 1988, the US JGOFS Bermuda Atlantic Time-series Study (BATS) began biweekly to monthly time-series measurements of upper ocean biogeochemical properties in waters overlying the OFP mooring site (Michaels and Knap, 1996).

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The OFP sediment traps are of PARFLUX Mark 7G-13 design, with a sampling aperture of 0.5 m. A honeycomb baffle of 25 mm diameter cells having an aspect ratio of 2.5 is fitted within the trap opening. The trap cups are filled with seawater brine (about 40 ppt), made by freezing Sargasso Sea water collected from a depth of '3000 m. Prior to July 1996, the 500 and 1500 m trap cups were poisoned with HgCl , but the 3200 m trap cups were not poisoned.  Between November 1995 and January 1996, the 1500 m trap was temporarily relocated to 3400 m depth to conduct a method intercomparison experiment. For this experiment, we poisoned the 3400 m trap cups with HgCl while the 3200 m trap cups  remained unpoisoned. Upon recovery, the 3200 m trap material was processed according to standard OFP methods, whereas the 3400 m trap material was processed using a revised protocol designed specifically to maintain sample quality for trace organic and inorganic analyses.

2.2. Analytical methods Upon trap recovery, the samples were stored refrigerated in their polyethylene collection bottles and processed immediately upon return to the lab. Material in the 3200 m trap was size fractionated into '1000 lm, 500—1000 lm, 125—500 lm, 37— 125 lm and (37 lm fractions by passing it through a series of stainless steel sieves; the (37 lm size fraction was recovered after centrifugation. All size fractions were then oven dried at 60°C and weighed for dry weight determinations. Subsamples of dried material in the (37 lm fraction were taken for lipid analyses. These were weighed in NoChromix (Godax Labs) cleaned, combusted (380°C overnight) test tubes, immersed in the extraction solvent (2 : 1 chloroform : methanol), and stored at !30°C until analyzed. Material in the 3400 m trap cups was fractionated into '1000 lm and (1000 lm fractions using a 1.0 mm stainless steel sieve. The (1000 lm fraction was then split into ten aliquots using a McLane sample splitter (McLane Labs) that had been refitted with a Teflon coated tray. The ten aliquots were collected in Nochromix cleaned, combusted glass vials. Three randomly selected aliquots were combined for lipid analyses. These aliquots were filtered onto 47 mm combusted GF/F (Whatman) filters. The filters were placed in Nochromix cleaned, combusted test tubes fitted with Teflon lined caps and then immersed in the extraction solvent (2 : 1 chloroform : methanol) and stored at !30°C until analysis. The remaining seven aliquots were recombined and treated as above for the 3200 m trap samples. The 37—125 lm and (37 lm size fractions in both traps were analyzed for organic carbon and nitrogen and for carbonate. These two size fractions constitute between 68 and 82% of the total mass of the material collected in each cup. They constitute a larger percentage of the total organic material, as the larger size fractions primarily consist of skeletal remains of foraminifera and radiolaria. Organic carbon and nitrogen were analyzed using a Fisons (Carlo Erba) model EA 1108 CNHS machine. The samples were decalcified with high-purity sulfurous acid prior to analysis (Conte and Ralph, in prep.). Carbonate was analyzed using a

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Coulometrics model 5011 coulometer equipped with a System 140 module for inorganic carbon determination. The (1000 lm size fraction of the 3400 m trap material and the (37 lm size fraction of the 3200 m trap material were analyzed for lipid biomarkers. Lipids were extracted using a modification of the procedure detailed in Conte et al. (1992). Briefly, an internal standard mixture consisting of C n-alkanol, C n-alkanoic acid, 5a   cholestane and C n-alkane was added to the samples prior to lipid extraction. Lipids  in the trap material were extracted twice in 2 : 1 chloroform : methanol using an ultrasonic unit equipped with a cup horn (&120 W, 2 min). The extracts were combined and washed to remove any salts and non-lipid components using the method of Folch et al. (1957). The lipid extract was concentrated and taken up in chloroform, and residual water was removed by passing the extract through a short bed of combusted, anhydrous Na SO . The extracted sample was transesterified using   5% methanolic HCl (55°C, 12 h) (Christie, 1982). During transesterification, any polar lipids, mono-, di- and tri- acylglycerols, wax esters and sterol esters are converted to their corresponding methyl esters, alcohols and sterols. The transesterified products were extracted into hexane and passed through a short bed of Na SO , and the   hexane was evaporated and replaced by methylene chloride. Just prior to gas chromatography, the sample was trimethylsilylated using BSTFA in pyridine (55°C, 1 h). The transesterified, trimethylsilyl derivatives were chromatographed on a 60 m; 0.32 mm DB5 column (J&W Scientific) and also on a 60 m;0.25 mm CPSil5CB column (Chrompack) (both 0.25 lm film thickness). The gas chromatograph used was a Fisons Series 8000 gas chromatograph and was programmed from 50—150°C at 10°C min\ and from 150—320°C at 4°C min\, with a 30 min. hold at 320°C. H was  used as the carrier gas. Samples were analyzed by GC-MS on a VG-Autospec-Q mass spectrometer using 60 m;0.32 mm (0.25 lm film). DB5 and DB-XLB (J&W Scientific) columns for compound identification. Programming was similar to above except He was used as the carrier gas. All compounds were quantified by GC except the 'C hopanoids, which were quantified by GCMS.  3. Results and discussion 3.1. The 8 year record of biweekly flux at 3200 m depth The biweekly resolved mass flux at 3200 m depth for the period June 1989 to April 1997 is shown in Fig. 1. The timing and duration of the flux maxima show significant interannual variability. A high degree of short-term temporal variability and abrupt changes in flux are also apparent, especially during the winter and early spring. In particular, a mid-winter flux maximum of magnitude comparable to or greater than that of the spring flux maximum is observed in four out of the eight years sampled (1990/1991, 1991/1992, 1995/1996 and 1996/1997). Frequency plots summarizing the seasonal timing of periods of highest mass flux over the 8 yr. period are shown in Fig. 2. Six percent of the samples collected over the 8 yr. period had fluxes over 60 mg m\ d\ (Fig 2A), or greater than twice the average

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Fig. 2. Temporal distribution of high mass fluxes at 3200 m at the OFP site for biweekly resolved samples collected since 1989. (A) Distribution of mass fluxes'60 mg m\ d\, which are greater than twice the overall average 3200 m flux for 1989 to present. (B) Distribution of mass fluxes of 50—60 mg m\ d\.

biweekly resolved flux (30 mg m\ d\). The timing of these exceptionally high fluxes is bimodally distributed, with five of the maxima occurring between Dec. 15 and Jan. 30 and five between Mar. 15 and Apr. 30; only three flux maxima occurred between Jan. 15 and Mar. 30. The magnitudes of the flux maxima for the Dec./Jan. and Mar./Apr. periods were comparable, averaging 72.0 and 74.5 mg m\ d\, respectively. However, the extreme fluxes observed in the winter generally occurred abruptly and were short-lived,

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whereas the extreme fluxes in the spring tended to occur during an extended period of enhanced flux (Fig. 2B, Fig. 1) associated with the annual spring bloom (Michaels and Knap 1996). 3.2. The Jan. 96 flux **event++ In January 1996, the traps located at 3200 and 3400 m intercepted the largest flux ‘‘event’’ measured since biweekly sampling was initiated in 1989. There was an abrupt, nearly threefold increase in mass flux at both depths (Fig 3A). Although there was a marked increase in flux, only small changes were observed in bulk composition. The percentage of organic carbon (% Corg) in the (125 lm size fraction of the collected trap material was about 3.6—4.0% prior to the event and increased slightly to 4.8—5.0% during the event (Fig. 3B). The percentage of carbonate in the (125 lm size fraction showed no apparent change associated with the event (Fig 3C). The high flux event coincided with the method intercalibration exercise (described above) in which the 3400 m trap was poisoned with HgCl and the 3200 m trap  remained unpoisoned. Both fluxes and bulk composition of the 3200 and 3400 m trap material were in close agreement and attest to the excellent trap-related and OFP method reproducibility for mass flux determination and bulk organic carbon and carbonate measurements. The results indicate that the addition of HgCl poison 

Fig. 3. Mass fluxes (A) and percentages of organic carbon (B) and carbonate (C) in the trap material collected at 3200 and 3400 m prior to and during the high flux event in Jan 1996. The 3400 m trap was HgCl poisoned and the 3200 m trap was not poisoned. Note the close agreement between the two trap  depths.

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(made necessary here for trace organic analyses) does not significantly alter measurement of mass flux and bulk composition for deployments of short (2 month) duration. 3.3. Lipid biomarker composition of the 3400 m trap material We made detailed analyses of lipid biomarker composition in the samples collected over this time period to ascertain the sources of this material and to provide information on the causative process(es) responsible for this abrupt increase in flux. We present here results for the 3400 m trap, because this material was optimally preserved during collection and subsequently handled specifically for trace organic analysis. The total extractable lipid (TEL) concentration and the major lipid biomarker compounds present in the flux material were similar throughout the sampling period (Table 1). However, the relative concentration of the individual compound classes changed dramatically during the high flux event. GCMS chromatograms of the total extractable lipids (analyzed as their transesterified trimethylsilylated derivatives) in trap material collected prior to, and during, the event are shown in Figs. 4 and 5, respectively. Extractable lipids in the trap material collected during the low flux period prior to the event are dominated by cholesterol, the C hopanone 22,29,30  trisnorhopan-21-one and saturated C14—20 fatty acids (Fig. 4, Table 1). Although some phytoplankton synthesize significant amounts of cholesterol, it is generally absent or a minor sterol component in most species (Volkman, 1986). However, zooplankton and bacteria produce large amounts of cholesterol via the bioconversion of dietary phytosterols (Goad, 1978; Ikewara, 1985), store large quantities in their biomass (Goad, 1978), and excrete large quantities in their feces (Wakeham and Canuel, 1986; Bradshaw, 1990; Bradshaw et al., 1990). Hence, cholesterol is a strong indicator of animal- or fecal-derived organic material. The C hopanone 22,29,30 trisnorhopan 21-one is believed to be a degradation product of the C polyhopanols, which  function as sterol surrogates in bacteria (Ourrison et al., 1987). This compound has previously been reported in sediment trap material (Gagosian et al., 1982; Venkatesan et al., 1987). The C14—20 saturated fatty acids are derived from a variety of sources, but are generally enhanced in bacteria and in fecal and detrital material (e.g. Prahl et al., 1984). In contrast to the simple lipid composition of the material collected prior to the event, extractable lipids in the trap material collected during the event were extremely diverse (Fig. 5, Table 1). A suite of C —C * and * sterols and C 4-methyl    sterols, which are major components of marine phytoplankton taxa (Withers, 1983; Volkman, 1986; Volkman et al., 1990, 1993), were found in 50% higher concentrations in material collected during the flux event, as compared with material collected during the preceeding low flux period before the event. Similarly, long-chain alkenones and alkenoates, synthesized principally by the coccolithophorid Emiliania huxleyi at this site (A. Haidar, unpublished results), were present in 70% higher concentrations in the material collected during the event (Table 1). Concentrations of polyunsaturated fatty acids (PUFAs), which have extremely rapid degradation rates in detrital material (Conte, 1989), were three times higher in material collected during the event. The

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Table 1 Concentrations of lipid biomarkers and diagnostic lipid biomarker ratios in 3400 m OFP sediment trap material collected from Nov 95 to Jan 96. Shorthand notation for lipid classes is given in parentheses; sterol notation is C *W, where x indicates the carbon number, and y indicates the positions of the double bonds. V Concentration increase is ratio of biomarker concentration in material collected in the trap during the high flux event (cup 4) with material collected prior to event (cup 2)

Cup no. Collection date

1 11/16—12/1

Concentration (ng mg\ dry weight): Total extractable lipids (TEL) 1038.4 Total fatty acids (TFA): 327.1 Branched#odd chain acids 9.7 Saturated acids 226.6 Polyunsaturated acids (PUFA) 21.1 Sterols and Stanols (STEROLS): 178.0 Total phytosterols (PHYTO) 79.9 Cholesterol 66.2 Stanols 30.1 Alkenones and Alkenoates (LCK#AA) 19.2 Alkan-1,15-diols and alkan-15-one-1-ols 26.7 Steroidal Ketones (ST KET) 19.1 Hopanoids (HOP) 69.1 C hopanone 69.1  Hydroxy acids (b#u!1) 10.6 1-0-Alkylglycerols 9.1 Biomarker ratios: Branched#odd chain FA (% of TFA) PUFA (% of TFA) 20:5u3/22:6u3 PUFA ratio Phytosterols (% TEL) Phytosterols (% STEROLS) Cholesterol/Phytosterol ratio Stenol/Stanol ratios: C */C *   C */C *   C */C *   C */C *   ST KET/STEROLS ratio Hopanoids (% TEL) 22,29,30 trisnorhopan-21-one (%HOP) HOP/STEROLS ratio HOP(-C27)/STEROLS ratio


2 12/1—12/18

3 12/19—1/5

Concentration 4 increase 1/6—1/23 Cup 4/ Cup 2

1236.3 208.8 15.0 155.8 13.8 483.2 89.9 339.4 52.4

1925.3 190.6 12.2 136.0 19.5 1091.3 116.7 917.2 49.5

1236.8 258.5 23.9 185.7 40.2 296.7 136.1 84.7 61.4

1.0 1.2 1.6 1.2 2.9 0.6 1.5 0.2 1.2

22.2

25.5

36.8

1.7

60.7 33.0 128.4 102.8 5.3 4.5

85.3 45.9 153.4 85.2 8.5 6.4

89.6 82.7 161.1 66.1 8.9 5.8

1.5 2.5 1.3 0.6 1.7 1.3 Ratio increase:

3.0 6.5 0.7 7.7 44.9 0.8

7.2 6.6 0.5 7.3 18.6 3.8

6.4 10.2 0.5 6.1 10.7 7.96

9.2 15.6 0.3 11.0 45.9 0.6

1.3 2.4 — 1.5 2.5 0.2

4.1 5.4 3.4 3.1 0.11 11.1

3.3 10.4 3.2 3.8 0.07 13.2

2.8 46.5 3.8 3.1 0.04 8.2

3.8 4.3 2.0 2.3 0.28 10.7

1.2 0.4 0.6 0.6 4.1 0.8

63.1 1.8 0.7

54.0 1.4 0.6

50.1 1.0 0.5

0.8 0.5 0.7

59.9 1.5 —

Defined as sum of sterols V, VII, XIX, XXXIII, XXXIX and LXV (see Fig 4 caption for compound key).
HOP/STEROLS ratio excluding 22,29,30 trisnorhopan-21-one.

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increase in PUFAs indicates that the material collected during the high flux event was composed of much higher amounts of labile, easily degradable material than material collected beforehand. Alkan-1,15-diols and alkan-15-one-1-ol concentrations also increased significantly during the event (Fig. 5, Table 1). These compounds, of presumed phytoplanktonic origin, have previously been reported in marine and coastal sediments (reviewed in Versteegh et al., 1997), but their sources are not well established. Originally, they were attributed to cyanobacterial input (Morris and Brassell, 1988), but subsequent studies (de Leuuw et al., 1992) have questioned this assignment. Recently, Volkman et al. (1992) and Gelin et al. (1997) have identified these compounds in Nannochloropsis species of the algal class Eustigmatophyceae (Chromophyta), suggesting that they have a eucaryotic algal rather than cyanobacterial source. However, differences in the chain length and isomeric distribution of these compounds between Nannochloropsis cultures and sediment samples indicates additional species synthesize these compounds in oceanic waters. We also identified 12-OH(u17)-C acid, a mid-chain hydroxy fatty acid, and a  30 : 1 alkenol in the high flux trap material (Fig. 5). The mid-chain hydroxy fatty acids are believed to be related to the alkyl diols and keto-ols (reviewed in Versteegh et al., 1997). While other mid-chain hydroxy fatty acids occur in Nannochloropsis, the 12-OH(u17)-C fatty acid has previously been reported in only a limited number of  high organic sediments (ibid). Its presence in the trap samples at this oligotrophic site confirms a water column source and indicates a more widespread distribution of this compound in the ocean. The 30 : 1 alkenol is also synthesized by Nannochloropsis (Volkman et al., 1992), and hence it may possibly have a source related to the alkadiols, keto-ols and mid-chain hydroxy acids in our samples. In addition to lipid biomarkers of phytoplanktonic origin, concentrations of biomarkers of presumed microbial origin also increased significantly during the event (Table 1). Concentrations of hopanoic acids, alcohols and ketones were significantly higher in material collected during the event. The hopanoid compounds are believed 䉳 Fig. 4. GCMS chromatograms of total extractable lipids in trap material at collected 3400 m in Cup 2 (12/2—12/18/95), prior to the high flux event (cf. Fig. 3). The column used was a 60 m;0.32 mm (0.25 lm film) DB-XLB column. (A) Total ion current (TIC). (B) TIC of sterol elution region. (C) m/z 191 fragment, a diagnostic fragment of hopanoids and some triterpenoids. Compound key (also for Fig. 5): Sterols- I: 24-nor-cholesta-5,22E-dien-3b-ol; II: 24-nor-cholesta-22E-en-3b-ol; V: 27-nor-24-methylcholesta-5,22Edien3b-ol; VII: cholesta-5,22E-dien-3b-ol; VIII: 5a-cholest-22E-en-3b-ol; IX: cholest-5-en-3b-ol (cholesterol); X: 5a-cholestan-3b-ol (cholestanol); XIX: 24-methylcholesta-5,22E-dien-3b-ol; XX: 24-methyl-5acholest-22E-en-3b-ol; XXXIII: 24-ethylcholesta-5,22E-dien-3b-ol; XXXIV: 24-ethyl-5a-cholest-22E-en-3bol; XXXVIII: 24-ethyl-cholest-5-en-3b-ol; XXXIX: 24-ethyl-5a-cholestan-3b-ol; LX: C 4-methyl stanol;  LXV: 4a, 23, 24-trimethyl-5a-cholest-22-en-3b-ol (dinosterol). Hopanoids-HI: 22,29,30 trisnor-hopan-21C C one; H4 and H5: unidentified triterpenoids: H6: C triterpanol ; H7: C triterpenol ; H8: C hopanone;    H9: C/D ring methylated hopanoid C ; H10: C b, b homohopanoic acid; H11; C b, b homohopan-31-ol;   H12: C b,b bishomohopanoic acid; H13: C b,b-bishomophopan-32-ol; H14: C b,b trishomohopanoic    acid. Other compounds: A: 1,12(u17) C28 :0 diol; B: C30:1 alkenol; C: cholest-4-en-3-one; D: 1,14(u17)C30:1 diol; E: C30:0 alkan-1,15-diol; F: C30: 0 alkan-15-one-1-ol; G: unidentified compound; I.S. C n-alkane  (internal standard) C denotes tentative compound assignment.

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to be aerobic degradation products of the C polyhopanols of bacteria (Ourisson et  al., 1987). Interestingly, while the concentrations of the hopanoic acids and alcohols increased in the high flux trap material, the concentration of the C hopanone  22,29,30 trisnorhopan-21-one decreased, suggesting that the higher chain length acids and alcohols are intermediaries and that the C hopanone is the end product of  polyhopanoid degradation. Branched and odd chained C12—18 saturated and hydroxy (b and u!1) fatty acids and 1-O-alkylglycerols also increased by 30—70%. The (C branched and odd  chain fatty acids and b-hydroxy fatty acids are major bacterial components (Gillian and Johns, 1986) and have been extensively utilized as bacterial indicators (e.g. Boon et al., 1977; Cardoso and Eglinton, 1983; Matsumoto and Nagashima, 1984; Fukushima et al., 1992). Although the u!1 acids have been widely reported in sediments, a direct biological source has been documented only for the C !C   compounds, which were found in a methanogen (Skerratt et al., 1992). It has also been suggested that they are derived from seagrasses (Shaw and Johns, 1985) or bryophytes (Caldicott and Eglinton, 1976) or from hydroxylation of alkanes and fatty acids by aerobic bacteria (de Leeuw et al., 1995). The 1-O-alkylglycerols were first identified in methanolysis products of the glycolipid and phospholipid fractions of thermophilic microbial mats and presumably occurred originally as the alkylacylglycerol moiety of polar lipids of methanogenic and sulfate-reducing bacteria (Zeng, 1988). 1-O-alkylglycerols are also found in suspended particles (M.H. Conte, unpublished data), sediment trap material (Wakeham 1982) and in surface sediments (Madureira, 1994), suggesting an additional aerobic bacterial source. While they have not been reported in any studies of microalgae, given the limited data available, a eucaryotic source is also a possibility. Concentrations of sterol degradation products also increased sharply in material collected during the event (Table 1). In particular, the steroidal ketone concentration was 2.5 times higher than in material collected beforehand. Steroidal ketones are believed to be intermediates in the microbial transformation of sterols to stanols (Bjo¨rkhem and Gustafsson, 1971; Eyssen et al., 1973; Gagosian et al., 1980; Mermoud et al., 1984). The ratio of steroidal ketones to the primary sterols was four times higher during the event, consistent with the formation of steroidal ketones early in the oxic degradation pathway. Stanols are also produced during microbial degradation of sterols (Bjo¨rkhem and Gustafsson, 1971; Gaskell and Eglinton, 1975; Mermoud et al., 1984), although a small fraction are synthesized directly by some algae (Nishimura and Koyama, 1977; Volkman, 1986). Fluxes of phytoplankton- and microbially-derived compounds increased by a factor of 3—8 during the event (Table 2). Polyunsaturated fatty acids and steroidal ketones 䉳 Fig. 5. GCMS chromatograms of total extractable lipids in trap material collected at 3400 m in Cup 4 (1/6-1/23/96), during the high flux event (cf. Fig. 3). (A) Total ion current (TIC). (B) TIC of sterol elution region. (C) m/z 191 fgragment, a diagnostic fragment of hopanoids and some triterpenoids. For compound key see Fig. 4. The asterisk in the sterol elution region shows the 12-OH(u17)-C hydroxy fatty acid (here  detected as a shoulder on the DB-LXB column used for these GC-MS runs).

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showed the largest, approximately 7-fold, increase in flux. The only biomarkers whose flux did not increase significantly during the event were the C hopanone  22,29,30 trisnorhopan-21-one and cholesterol, which were already enriched in the samples collected prior to the event. Fluxes of the phytoplankton-derived compounds (sterols, alkenones/alkenoates and alkan-1,15-diols and alkan-15-one-1-ols) and, to a lesser extent, hopanoic acids and alcohols and the steroidal ketones increased gradually in the month prior to the major flux event (Table 2) and suggested that upper ocean productivity was increasing before the flux event. The magnitude and timing of the flux increases of the phytoplankton-derived biomarker classes were similar and suggested that they had a similar production history in the overlying water column. In contrast, fluxes of microbial fatty acids, saturated fatty acids and polyunsaturated fatty acids were largely constant during this period, and increased only during the flux event itself. 3.4. Estimation of the timing of the bloom event in the overlying surface waters The unsaturation ratio of the C alkenones (º)Y ) in the trap material records the   Integrated Production Temperature (IPT, Conte et al., 1992) of these compounds by

Table 2 Fluxes of lipid biomarker classes in 3400 m OFP sediment trap, Nov 95—Jan 96. Shorthand notation for lipid classes is given in parentheses. Flux increase is the ratio of flux measured during the high flux event (cup 4) with the flux measured prior to event (cup 2)

Cup no. Collection date

1 11/16—12/1

Flux (kg m\ day\): Total extractable lipids (TEL) 17.5 Total fatty acids (TFA): 5.5 Branched#odd chain FA 0.2 Saturated FA 3.8 Polyunsaturated FA (PUFA) 0.4 Sterols and Stanols (STEROLS): 3.0 Total phytosterols (PHYTO) 1.3 Cholesterol 1.1 Stanols 0.5 Alkenones and Alkenoates (LCK#AA) 0.3 Alkan-1,15-diols and alkan-15-one-1-ols 0.4 Steroidal Ketones (SK) 0.3 Hopanoids (HOP) 1.2 22,29,30 trisnorhopan-21-one 1.2 Hydroxy acids (b#u!1) 0.2 1-0-Alkylglycerols 0.1 includes minor steroidal ketone coelutant.

Flux increase Cup 4/ Cup 2

2 12/1—12/18

3 12/19—1/5

4 1/6—1/23

36.8 6.2 0.4 4.6 0.4 14.4 2.7 10.1 1.6

53.9 5.3 0.3 3.8 0.5 30.5 3.3 25.7 1.4

95.7 20.0 1.8 14.4 3.1 23.0 10.5 6.6 4.8

2.6 3.2 4.1 3.1 7.6 1.6 3.9 0.6 3.0

0.7

0.7

2.8

4.3

1.8 1.0 3.8 3.1 0.2 0.2

2.4 1.3 4.3 2.4 0.3 0.2

6.9 6.4 12.5 5.1 0.8 0.7

3.8 6.5 3.3 1.7 3.8 3.5

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alkenone synthesizers in the overlying surface waters. The IPT is the temporally and depth integrated average of the water temperature of alkenone and alkenoate synthesis, as modified slightly by variations in the extent of degradation associated with changes in water column residence time during different seasons (Conte et al., 1992). IPT is related to sea surface temperature (SST) but is not a direct estimate of SST. In the Bermuda region, the majority of the alkenone/alkenoate production takes place in the surface mixed layer rather than in the thermocline (Conte and Weber, submitted), so the IPT is closely related to the average integrated sea surface temperature of alkenone/alkenoate production. We estimated the IPT of alkenone production using a nonlinear temperature calibration derived from analyses of suspended particles in the surface waters at the OFP site (Conte and Weber, submitted): º)Y "!2.264#0.225¹!0.004¹ (r"0.97, n"36).  This calibration was constructed from surface particulate material samples collected bimonthly over a two year period (July 95—Dec 97). During this period, the water temperature ranged from 19—28°C. We compared the temporal trend in IPT estimates in the traps with the average temporal trend in surface water temperatures over the collection period to infer the production history of the alkenones and the timing of the synthesis of the material collected during the high flux event (Table 3). The IPT estimates in the traps agree well with biweekly averaged temperatures in the mixed layer in November through January but show interesting differences related to the production history of the alkenones in the sinking particles. The IPT estimate for the trap sample collected from 11/16—12/1 (Cup 1) is *2°C colder than the average 0—50 m water temperature in the

Table 3 U)Y , alkenone and alkyl alkenoate flux (LCK#AA) and Integrated Production Temperature (IPT)  recorded by C alkenones in the trap material. The IPT was estimated using a nonlinear temperature  calibration algorithm (º)Y "!2.264#0.225¹!0.004¹, n"36, r"0.97) derived from surface water  particulates collected at the OFP/BATS site (Conte and Weber, submitted). The estimated IPT of new input into the trap cup was calculated as described in the text. The 0—50 m water temperature at the OFP/BATS site for November through January biweekly averaged time periods was calculated from CTD profile data collected by the BATS program in 1989—1995 (US JGOFS-BATS database). The average date the water temperature profiles were collected is shown for reference Trap cup Date

1 2 Nov 16—Dec 1 Dec 2—18

3 Dec 19—Jan 5

4 Jan 6—23

U)Y  LCK#AA flux (lg m\ d\)

0.773 0.3

0.804 0.7

0.807 0.7

0.787 2.8

IPT in trap (°C) Estimated IPT of new input BATS 0—50 m T (°C) BATS avg sample date

21.8 21.8 23.5 Nov 22

22.5 23.4 22.5 Dec 8

22.6 23.4 21.5 Dec 21

22.1 21.9 21.0 Jan 13

See text.

Nov 1—15

23.8 Nov 11

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preceding months, so the alkenones in the trap could not have originated directly from settling of these compounds out of the surface water. One possible scenario to explain the low IPT in Cup 1 is that the alkenone production was in the thermocline. However, vertical profiles of alkenone concentration do not support this explanation. The alkenone concentrations in the surface 0—20 m in September and November 1995 were 3—5;higher than concentrations at 80—100 m, and, furthermore, water temperatures at the chlorophyll maximum in November (about 80 m) were '23.0°C, over 1°C higher than the IPT in Cup 1 (Conte and Weber, submitted). Alternatively, a major fraction of the alkenones in Cup 1 may have been derived from particle scavenging of alkenones present in suspended particulate debris in the water column. Scavenging of suspended deep water particles at the site is suggested by the results of Bacon et al. (1985), who documented seasonal cycles in the fluxes of Th and Pa, radionuclides whose production is predominately in the water column rather than surface waters. In support, suspended particles in the water column in the eastern North Atlantic during low flux periods in the summer do not reflect the higher summer SST but rather have an IPT close to the average annual production temperature (Conte et al., 1992). We currently do not have a firm estimate of the average annual production temperature of alkenones at this site, but the 21.8°C IPT of Cup 1 is consistent with water temperatures at the time of the spring bloom in this region. The IPT estimates for material collected over the period 12/1/95 to 1/5/96 (Cups 2 and 3) are similar (22.5—22.6°C) and increase by approximately 0.7°C from the IPT of material collected in Cup 1 (Table 3). The increase in IPT in the trap material, coupled with an increase in the flux of alkenones#alkenoates in Cups 2 and 3 suggests a contribution of alkenones from recent surface water production. Assuming Cup 1 represents a constant ‘‘background’’ flux of alkenones, the IPT of the additional alkenone flux is 23.4°C, consistent with surface water temperatures in late November (Table 3). This, and the doubling of phytoplankton derived compound fluxes in Cups 2 and 3, suggests a significant increase in surface water productivity in late November/early December 1995. The IPT in trap material collected during the flux event decreased by 0.5°C from the material collected preceding the event. The relatively cold IPT of 22.1°C agrees well with December water temperatures and indicates that the bulk of this material was derived from recent alkenone production. Using a rough assumption that this additional production was added to a constant flux of sinking material having an IPT of 22.6°C, the IPT of the high flux material is estimated as 21.9°C, consistent with water temperatures in mid December. This suggests that the maximal production of the alkenone synthesizers, and by inference maximal production of other phytoplankton, occurred around the middle of December approximately 3—5 weeks prior to interception of the sinking material at 3400 m. This estimate for the timing of alkenone synthesis implies average sinking rates of 100—150 m d\, consistent with other estimates of particle settling rates (e.g. Lampitt, 1985; Deuser, 1986; Rice et al., 1986) An alternative explanation for the trends in the estimated IPT in the trap material is that the source region of the trap material drastically changed, and that the bloom material originated from a region further north of the site with much colder water

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temperatures. Deep traps collect material originating from hundreds of square kilometers of surface ocean; the dimensions and ‘‘center’’ of this statistical catchment area depend upon the ocean current regime and particle sinking speeds (Siegel and Deuser, 1997). Satellite images of the region indicate temperature gradients with latitude and associated with eddy features (N. Nelson, unpublished data). While the source area of the particles that we collected in these trap samples over this period cannot be quantitatively evaluated with the information at hand, the consistency of the IPT trends, along with other biomarker evidence for increasing phytoplankton production in the overlying waters before the flux event, provides no need to invoke an abruptly altered catchment area of the trap to explain the high flux event. 3.5. Implications for processes controlling export fluxes in the Sargasso Sea The lipid biomarker composition of the material collected in the 3400 m trap shows a strong enrichment of labile-phytoplankton derived compounds during the high flux event in January 1996 and points to a short-lived phytoplankton bloom/export event in the overlying surface waters as the cause of this abrupt increase in flux. Using alkenone-based estimates of the surface water temperature, we estimate that this bloom occurred around mid December. Although we have not conducted detailed biomarker analyses of trap material collected during the other extreme flux maxima, which occurred in 1990/1991, 1991/1992 and 1996/1997, it is likely that they too are the result of short-lived mid-winter blooms. The mid—winter flux maxima, recorded in 1990/1991, 1991/1992, and 1996/1997 indicate a 4—6 week duration of enhanced deep particle flux during these events, significantly shorter than deep flux maxima associated with the spring ‘‘bloom’’ period (Fig. 1). The upper ocean conditions that prevailed in December 1995 and promoted this transient productivity event and greatly enhanced export flux are not known, since no upper ocean measurements were made during this period. Clearly, the conditions that promote these episodic flux events do not occur every year. The wintertime high flux events occur during a period of rapid mixed layer deepening in this region, and it may be that alternating periods of water column stabilization and destabilization are instrumental in promoting conditions that favor transient productivity events and enhanced export flux. During periods of inclement weather, there is a rapid deepening of the mixed layer, driven by a negative heat flux and wind mixing. This will bring nutrients up into the photic zone and will stimulate production if adequate light is available (e.g. Marra et al., 1990; Malone et al., 1993; Waters et al., 1994). These periods of mixed layer deepening are generally followed by a period of favorable weather. During these stable periods, the water column is weakly stabilized by a positive heat flux, and a second shallow mixed layer is often seen superimposed upon the deepening seasonal mixed layer (BATS results and unpublished data). These short-lived periods of water column stability following nutrient input from mixed layer deepening generate ideal conditions for rapid phytoplankton growth in the '20°C waters of the Bermuda region. If a bloom does develop during these quiescent periods, a subsequent episode of inclement weather will erode the weakly stratified surface layer and promote renewed downmixing. This rapid mixing

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of phytoplankton biomass to depth will effectively bypass surface water remineralization processes and enhance the efficiency of material export from the euphotic zone. Hence, because of downmixing, the increase in export flux can proportionately be much greater than the increase in surface water production. This hypothesized scenario has previously been suggested by observations in Gulf Stream warm-core rings (Smith and Baker, 1985; Bishop et al., 1986). There, alternating periods of stabilization and destabilization of the mixed layer, generally lasting only a few days each, resulted in enhanced phytoplankton production that was subsequently downmixed to depths of 400 m. The downmixed phytoplankton material, estimated to account for 67% of the primary production, was initially intact (Conte, 1989). It was subsequently consumed by zooplankton grazers, resulting in a marked increase in fecal material production at depth (Bishop et al., 1986). In contrast to the ‘‘freshness’’ of the material collected during the high flux event, the sinking material collected beforehand was extensively degraded. Only low concentrations of bacteria-derived compounds were present on this material, suggesting that microbial biomass and, by inference, activity was low. The enriched concentration of cholesterol and saturated fatty acids, coupled with the extremely low polyunsaturated fatty acid abundance, suggests a predominant contribution of animal-derived detritus and fecal material (Prahl et al., 1984; Wakeham and Canuel, 1986; Bradshaw, 1990; Bradshaw et al., 1990). This is consistent with the view that during low flux periods, much of the sinking material is produced in situ by zooplankton activities at depth rather than having a direct surface source. The alkenone IPT in Cup 1 (Table 3) also indicates that a fraction of the sinking particles collected during low flux periods is derived from repackaging of deep suspended particles. The degraded composition of sinking material prior to the high flux event is typical of many of the deep trap samples that we have analyzed (unpublished data) and indicates that sinking particles during much of the year at this location are of low food quality. In contrast, the marked increase in bacteria-derived compounds during the high flux event, and also in degradation products of primary production, suggest that the settling bloom-derived material was a site of intense microbial activity. This close association of bacteria-derived compounds with labile organic material has been previously observed in suspended particulate material (Conte 1989) and also in surface sediments following a pulse of bloom material (Conte et al., 1995). No doubt, the arrival of this labile material on the seafloor must have stimulated biological activity there (cf. Gooday, 1988; Thiel et al., 1988/89; Graf, 1989; Pfannkuche, 1993; Smith et al., 1994, 1996). However, the period of accelerated remineralization following this pulse was likely to have been short-lived, as the benthic response to pulses of ‘‘phytodetritus’’ is rapid (e.g. Thiel et al., 1988/89; Graf, 1989; Smith et al., 1994; Gehlen et al., 1997). This may explain why previous benthic lander deployments at this site (Sayles et al., 1994) did not detect any marked variations in benthic oxygen utilization. In summary, our results provide direct evidence for the rapid delivery of extremely labile, biologically available material to the deep ocean in an oligotrophic region. It appears that this short-lived pulse resulted from a transient productivity event in the overlying waters, which was inefficiently remineralized in surface waters and rapidly

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settled to depth. We do not yet know the overall contribution of such episodic flux events to the deep water flux of labile organic material and associated elements, but the number of occurrences of extreme short-lived flux maxima in the OFP record suggests that they are not infrequent. If these events are meteorologically forced, as hypothesized above, then it is likely that global climate variations — especially those that affect wintertime weather patterns, such as the North Atlantic Oscillation (Joyce and Robbins, 1996; Talley, 1996) — will prove to have a major impact on export flux to the deep ocean.

Acknowledgements We thank the crew of the R/V ¼eatherbird II, D. Simoneau, R. Tavares and L. Christman for their invaluable assistance with the OFP mooring and sample collection. We also thank L. Christman and A. Cohen for assistance with laboratory analyses. The National Science Foundation grant OCE-9312826 supported the OFP timeseries sediment trap mooring studies. Acknowledgement is also made to the donors of The Petroleum Research Fund, adminstered by the American Chemical Society, and to the donors of the J. Lamar Worzel and Penzance Funds for their support of organic geochemical studies of the OFP trap material. The Bermuda-Atlantic Time-Series (BATS) data were collected with funding from the National Science Foundation to the Bermuda Biological Station for Research, Inc. We acknowledge the individual scientists, technicians and ship crew who have assisted in the BATS program.

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