Variability in lipid flux and composition of particulate matter in the Peru upwelling region

Org. Geochem. Vol. 6. pp. 2113- 215. 1984 Printed in Great Britain. All rights reserved

0146-6380/84 $03.110+1).110 Copyright © 1984 Pergamon Press Ltd

Variability in lipid flux and composition of particulate matter in the Peru upwelling region* STUART G. WAKEHAM,JOHN W . FARRINGTONand ROBERT B. GAGOSIAN Department of Chemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A.

Abstract--Particulate matter samples were collected with free-drifting sediment traps and in situ filtration systems in the Peruvian upwelling area to study the organic geochemistry of particulate organic matter in the water column and its relationship to source organisms and sediments. A variety of lipids--fatty acids. wax esters, steryl esters, triacylglycerols, sterols, fatty alcohols, stanones, unsaturated C37 and C3s methyl ketoncs, and hydrocarbons--were analyzed by capillary gas chromatography and gas chromatography-mass spectrometry. Diel and depth-related variations in lipid composition and flux of an order of magnitude were not uncommon in the sediment trap samples. Two samplings of a single site four days apart produced significantly different results. Flux and composition patterns varied depending on lipid class, collection time and depth, and source. The lipid composition of the suspended particles collected by in situ filtration was quite different from that of sinking particles collected in sediment traps, reflecting complexities in differentiating between source, transport, and transformation processes affecting the two particle size fractions. The data provide estimates of the range of fluctuations in composition of material contributing to the sedimentary record, which integrates over time periods of years to centuries. Key words: lipids, particulate organic matter, sediment traps, in situ pumps, Peru upwelling area, vertical

flux position (Deuser and Ross, 1980; Deuser et al., 1981, 1983; Lee etal., 1983; Honjo etal., 1982). A complex but poorly understood interaction exists between The nature of marine particulate organic matter suspended and sinking particles: for example, biolo(POM) plays a major role in determining the comgical packaging of small particles into fecal pellets, position of sea water and sediments and provides etc. can generate large particles, while disaggreganutrition for mesopelagic, bathypelagic and benthic tion of large particles yields small particles. organisms. Particles in the water column exist in a Few studies have systematically compared comcontinuum of sizes but may be operationally divided positions of suspended and sinking particles at the into two major pools, although no convention exists same sites. Large volume in situ filtrations by Bishop for the size(s) in each category. Small (~< 20 ~m) et al. (1977, 1978, 1980) showed differences in particles have settling velocities of ~< 1 m day -1 inorganic chemistry and vertical flux as a function of (McCave, 1975) and tend to remain in suspension for long periods. These suspended particles constitute ~> particle size. Tanoue and Handa (1980) investigated fatty acids in sediment trap-collected sinking parti95% of the total particle mass in the water column (e.g. McCave, 1975; Bishop et al., 1977) and are cles and suspended particulate matter obtained by filtration of water bottle samples, finding that trap readily sampled by conventional water-bottle techniques and in situ filtering systems. In contrast, large samples contained significantly more unsaturated particles (~> 20 ~m) are relatively rare and poorly fatty acid than did the suspended particulate matter. sampled by water bottles, but dominate the downThis observation was taken to indicate the relative ward flux of particulate matter in the oceans "freshness" of the fast-sinking organic matter com(McCave, 1975; Bishop et al., 1977; Honjo, 1980). pared to "older" suspended particles. Conversely, Large particles, which include zooplankton carcasses amino acid analyses by Lee et al. (1983) suggested in and exuviae, fecal pellets, and aggregates of small situ pump-collected material to be "fresher" than particles, sink at rates of tens to thousands of m d a y corresponding sediment trap material. Significant (Shanks and Trent, 1980; Honjo and Roman, 1978; compositional differences between large and small Small et al., 1979; Bruland and Silver, 1981; Madin, particles have also been reported for steroidal hydro1982; Staresinic et al., 1983). Sediment trap collec- carbons (Wakeham et al., 1984a), sterols (Gagosian tions of large particles have demonstrated a transfer et al., 1983a), carotenoids (Repeta and Gagosian, of significant amounts of labile organic matter from 1983), and hydrocarbons, fatty acids and sterols sites of production in the euphotic and mesopelagic (Saliot et al., 1982, 1983) and are related to differing zones to the deep sea (Tanoue and Handa, 1980; sources and alteration processes. Wakeham et al., 1980, 1984b; Gagosian et al., 1982; As part of a major coordinated effort to investigate Wakeham, 1982; De Baar et al., 1983). Time-series the biogeochemistry of organic matter in the Peru sediment trap experiments in the open ocean have coastal upwelling area, we report here on lipid shown major fluctuations in particle flux and corncomposition of particulate matter collected in two 203 INTRODUCTION

204

SIUARTG. WAKEHAMet al.

sets of free-drifting sediment traps deployed 4 days apart at the same location, and material obtained concurrently by large-volume in situ filtrations. The specific questions addressed are: (1) what is the short-term temporal variation in lipid composition and flux of sinking particles at a single site (i.e. how "patchy" are the particle flux and composition); and (2) how do the compositions of sediment trapcollected and in situ filtration-collected particles compare? EXPERIMENTAL

Oceanographic setting

Free-drifting sediment trap (FST) and in situ pump (WHISP--see below) samples were collected during austral fall (February-March), 1978, on R/V KNORR cruise 73, leg 2, in the upwelling area off the coast of Peru at about 15°S. Hydrographic, nutrient and primary productivity data for the cruise have been detailed by Gagosian et al. (1980, 1983a) and are typical of active upwelling. Primary productivities of 3-7 g C m -2 day-t (Staresinic, 1978; Gagosian et al., 1980) due to massive phytoplankton, primarily diatom, blooms lead to particulate organic carbon (POC) concentrations in the euphotic zone of up to about 750 p~g1- l over an order of magnitude greater than in typical open ocean areas. The resulting vertical flux of POC out of the eupohotic zone ( - 530 mg C m -2 day -1) and across 50 m (280 mg C m - : day-J; Staresinic, 1978) often leads to local anoxia in bottom waters of the continental shelf and accumulation of organic rich sediments containing up to 9.5% organic carbon (Henrichs, 1980; Henrichs and Farrington, 1984; Volkman et al., 1983).

contained acyclic, cyclic, and isoprenoid hydrocarbons; fraction IV (50% toluene in hexane) contained wax and steryl esters; fraction VI (5% ethyl acetate in hexane) contained ring saturated 3-ketosteroids, C37 and C3s di- and triunsaturated methyl ketones, and triacylglycerols; fraction VII (10% ethyl acetate in hexane) contained A 4-3-ketosteroids and 4methylsterols; and fraction VIII (20% ethyl acetate in hexane) contained free fatty alcohols and free 4-desmethylsterols. Total fatty acids were determined by saponification of an aliquot of the lipid. Compositional analyses of the fractions were carried out by glass capillary gas chromatography and computerized gas chromatography-mass spectrometry (Wakeham and Frew, 1982; Wakeham, 1982; Gagosian et al., 1982, 1983a,b; De Baar et al., 1983; Wakeham et al., 1983a,b; Volkman et al., 1983). The two in situ pump samples were collected with Woods Hole In Situ Pumps (WHISPs) during the night-time deployments of FSTs 10 and 11 (Cast No. 10; 0045-0323 local time, 8 March 1978; 15°07.4'S, 75°36.7'W). The WHISPs are hydrographic-wire mounted, stream-powered, large-volume filtration systems (Hess, 1984). Samples from 20 and 60 m were collected by pumping 76 and 224 1, respectively, through WHISP-mounted glass fiber filters (Gelman type AlE, 0.3 Ixm nominal pore size). The filters were freeze-dried and analyzed as described for the sediment trap samples. While the WHISPs collect primarily small, suspended particles, inclusion of rarer, large particles cannot be ruled out. In fact, fresh anchovy fecal pellets of up to - 0.5 cm length were collected at 160 m on the WHISP's stainless steel filter support screen without a glass fiber filter, although a factor of ten more water was filtered compared to WHISPs employing filters.

Samples and analysis

FST samples for organic geochemical studies were collected at 20 sites off the coast of Peru (Fig. 1). A description of the FSTs and bulk parameters of particle flux and composition is given by Staresinic (1978). Our report describes lipid composition and flux of two sets of four FSTs deployed at the same location in the intense upwelling, 4 days apart (Table 1). Simultaneous deployments were made at 14 m (the base of the euphotic zone) and about 50 m (below the seasonal thermocline) to examine the change in flux and composition of organic compounds over this depth interval. Diel trap settings were made to assess short-term temporal variations. Sediment trap sample extraction and analysis were described by Wakeham etal. (1983a,b) and Gagosian et al. (1983a,b). Briefly, following FST deployments of 8-12 h without poisons, particulate material was filtered, freeze-dried, and extracted with toluene/ methanol (1 : 1). Lipids were fractionated on silica gel columns according to functionality by elution of fourteen fractions with mixtures of hexane, toluene, ethyl acetate and methanol. Fraction I (hexane)

RESULTS AND DISCUSSION

Floating sediment traps 8-11 and the 20 and 60 m WHISPs were deployed in the interlse upwelling on 7-8 March 1978 (Table 1). FSTs 16-19 represent a resampling of this area on 12-13 March. As the redeployment was 4 days after initial sampling, different upwelling conditions were sampled, as indicated by underway maps of temperature and chlorophyll a (Staresinic, 1978). During the first sampling, upwelled water had been at the surface sufficiently long for phytoplankton to utilize available nutrients to increase their biomass. The second sampling took place at an early stage of development of a subsequent bloom when cold, nutrient-rich water upwelled at the coast. Thus chlorophyll a and primary productivity values were slightly higher during deployment of FSTs 16-19 (Staresinic, 1978; Gagosian et al., 1980). Both sampling periods were characterized by diatom blooms ("brown water", Strickland et al., 1969; Ryther et al., 1971; Gagosian et al., 1983a), and at FSTs 18 and 19 a dense dinoflagellate bloom (Staresinic, 1978).

205

Lipid flux and particulate matter in Peru

I \

, :;~!~il/; !".

•

, PERU

:!i~::. . ..... o

21 20

15"B0'

e3 • 20

I

I

I

76"00'W

\

I

IN

\\

~,~I

75"30'

75"00'

Fig. 1. Locations of free drifting sediment trap (0) and sediment samples (A) in the Peru upwelling.

l'able 1. Free-drifting sediment trap deployment data R/V KNORR cruise 73. leg 2, February-March, 1978"

Exposure Deployment Water period depth depth (local time) (m) (m)

Mass flux (g m 2 12 h t)

POC flux (rag m 2 12 h t)

Primary Anchovy C : N-;- production fecal (gm flux day i) (% of POC)~:

FST No.

Date

9 8 10 11

7 March 1978 7 March 1978 7-8 March 1978 7-8 March 1978

08.3(I-16.40 08.40-17.22 19.55-(16.50 21.05-07.16

14 52 14 52

400 500 400 400

2.93 2.92 3.34 2.48

164 1411 313 131

7.3 7.3 6.9 9.1

4.48

2.4 1.7 4.7 17.4

16 17 18 19

12 March 1978 12 March 1978 12-13 March 1978 12-13 March 1978

tl8.50-15.55 09.04-16.08 19.30--07.30 19.48-06.47

14 53 14 53

300 300 400 250

4.23 3.12 4.58 2.50

224 209 350 112

5.3 6.7 7.7 4.5

5.24

() 0 0 8.3

*Staresinic (1978). +Mean C : N for all 11-15 m sediment traps (n=8) was 6.4, while for all 5(1 m sediment traps (n=6) the value was 8.3. ~:Staresinic et al. (1983).

F S T samples Bulk particle and P O C fluxes during the two FST deployment periods are similar, but slightly higher values in FSTs 16-19 may reflect the higher primary production rates measured during the second period (Table 1). The shallow night-time FSTs during both periods showed the highest P O C flux. There were significant differences in flux at night between 14 and 52 m, although the d a y t i m e samples were more uniform. The morphology of particulate material collected in the FSTs has been described by Staresinic (19781

and Staresinic et al. (1983). Diatoms, especially Thalassionema nitzchioides and Thalassiosira eccentrica, were abundant in the traps. D i a t o m flux into night traps was an order of magnitude greater than into daytime traps. A major route of sedimentation of intact and partially degraded diatom cells in the Peru upwelling is fast sinking (up to 1000 m day - j ) fecal matter of the southern anchoveta Engraulis ringens. Staresinic et al. (1983) reported that during the 1978 sampling period, up to 17% of the P O C flux into the FSTs could come from anchovy fecal pellets (see Table 1). Major spatial and temporal variations in anchovy fecal pellet i m p o r t a n c e have been

206

STUARTG. WAKEHAMet al.

observed (Staresinic et al., 1983). During a subsequent cruise off Peru in 1981, nearly all of the POC flux was due to anchovy fecal material (Gagosian et al., 1983a). Copepod fecal pellets were also present in the FSTs, and some FSTs, especially at night, contained zooplanton carcasses and molts. Flux data for lipids in FSTs 8-11 and 16-19 are illustrated in Fig. 2. Ratios of lipid flux to POC flux are given in Table 2, and relative abundances of classes and selected "marker" compounds are found in Table 3. Major differences in both flux and concentration patterns are evident, depending on compound class, diurnal vs nocturnal sampling, deployment depth, and the 7-8 March vs 12-13 March collection periods. Interpretations based on the different lipids are not always consistent. F S T s 8-11

Total fatty acid flux (Fig. 2) in the night-time samples (FSTs 10 and 11) was 10-fold greater than in the daytime traps (FSTs 9 and 8). The deep traps had lower fluxes of fatty acids than the shallow traps. The ratio of fatty acid flux to POC flux, however, is different (Table 2). The fatty acid/POC ratio was highest in FST 11, not in FST 10 which had the greatest flux of both fatty acid and POC. Likewise,

"10000

FST 9

although FST 9 has a slightly higher flux of fatty acid and POC than FST 8, their fatty acid/POC ratios were the same. Selected fatty acids (Table 3) illustrate important features of the fatty acid composition of the FSTs and may be compared to surface (0-1 cm) sediment (see Fig. 1 for sediment locations and Volkman et al., 1983) and anchovy fecal pellets. Complete fatty acid compositions in all of the FSTs have been described (Wakeham et al., 1983a,b). Monounsaturated 16 : 1 A 9 is a significant fatty acid of many phytoplankton (Ackman etal., 1964, 1968; Kates and Volcani, 1966; Opute, 1974; Sargent, 1976; Schwarzenbach and Fisher, 1978; Volkman et al., 1981) and 18 : 1A9 is often important in zooplankton (Culkin and Morris, 1969; Morris, 1971; Lee, 1974; Bottino, 1975; Sargeant, 1976; Clarke, 1980). Although the ranges of abundance of these compounds in plankton are considerable, to a first approximation at least, 16 : 1A 9 may be thought to be due primarily to a phytoplanktonic input, while 18 : 1 A 9 indicates zooplankton material. Docosahexaenoic acid ( 2 2 : 6 ) may derive from both phyto- and zooplankton, although because of its lability it may be more important as an indicator of the "freshness" of the POC. Iso- and anteiso-15 : 0 and 18 : 1A~ are often used as indicators of inputs of microbial fatty acids

FST 8

~ooo

L~Fotty Acid IVVox Ester

10

BSteryl Ester ~ Triocylglycerol ~]Sterol

0 10000[

I .b.

S

FST 17

S

FST 19

~]Fatty Alcohol

~ Stanone C37 and C58 ~Melhyl Kelone J~n-Alkane

~°°° I

ol

Fig. 2. Histograms of lipid flux (p,g m - 2 12 h -1) on a logarithmic scale for FSTs 8-11, 7-8 March 1978and for FSTs 16--19, 12-13 March 1978.

19 0.24 0.02 0.22 4.2 0.63 0.20 0.08 0.15

19 0.58 0.05 1.1 2.4 0.48 0.57 0.37 0.21

8 (52 m) 78 2.7 0.73 1.9 20 0.49 0.76 0.60 0.07

10 (14 m) 110 0.14 0.31 6.4 17 0.69 1.5 0.89 0.19

11 (52 m) 140 0.59 0.13 1.4 11 7.3 2.1 0.01 0.23

16 (14 m) 15 0.07 0.01 1.2 2.7 0.25 1.3 0.02 0.12

17 (53 m)

Lipid flux/POC flux (× 10 3)

41 0.66 0.05 1.5 3.6 4.6 0.7 0.01 0.10

18 (14 m)

FST

17 0.29 0.14 4.1 8.9 0.97 0.89 0.06 0.09

19 (53 m)

*POC values of 95 and 35 /~g I ~ for 20 and 60 m, respectively, extrapolated from data of Gagosian et al. (1983).

Fatty acid/POC Wax ester/POC Steryl ester/POC Triacylglycerol/POC Sterol/POC Fatty alcohol/POC Stanone/POC C37/C3~ methylketone/POC n-Alkane/POC

9 (14 m)

FST

70 0.6 0.1 1.3 9.1 4.6 1.1 0.7

12 1.7 1.0

60 m WHISP

260 0.4 0.2 2.7 40

20 m WHISP

Lipid concentration/POC concentration ( x 10 s)

Table 2. Ratio of lipid flux (txg m -2 12 h 1) to POC flux (Ixg m 2 12 h l) for FSTs 9-11 and 16-19, and the ratio of lipid concentration (txg 1 i) to POC concentration (l~g I ~)* for the WHISP samples

e-,

3'

e-~

t'-

IA'~/total F A (%) 1A'~/total F A (%) 15 : 0/total F A (%) 6/total FA (%) IA'~/18 : 1A jl 0/total F A (%)

6.3 3.5 (I.8 0.35 1.5 1).2

9 (14m)

4.2

21.3

[).78

4.5

2.6

0.82

43.4 6.6

45.0 6.6

0.77

25.8

3.6

61.2 6.4

0.9

0.3

1.4 26.5

0.51 35.3 1.8

2.2

5.3

<1

1.7 4.7

20.3 13.7 0.4 0.77 1.7 0.06

1.5 37.5

11.0 4.8 0.5 0.18 1.3 0.3

8 (52m)

1.9

11.3

5.8

42.7 1[).2

0.3

3.2

0.02 13.8

5.6

0.06 5.5

22.0 26.9 0.2 2.5 4.0 0.02

=

2.0

5.1

4.1

11.1 1.5

0.09

14

0.42 2.6

0.9

0.2 2.6

15.8 4.2 0.4 1.3 2.2 0.8

3.0

2.2

7.0

14.7 5.8

0.09

<1

0.05 24.1

7.4

0.2 13.8

10.8 4.9 0.5 0.07 1.2 0.3

Free-drifting sediment traps Night Day 10 11 16 17 (14m) (52m) (14m) (53m)

2. I

5.0

4.3

39.1 2.6

0.1

9.4

0.44 25.6

3.3

0.8 8.6

111.7 7.9 0.7 11.34 2.7 0.4

18 (14m)

2.9

10.0

6.3

15.6 14.11

1).8

20.0

0.(17 5.0

21

0.8 34.6

6.3 11.7 0.9 0.11 1.5 0.3

19 (53m)

Night

(I.78

3.7

5.5

5.8 30

0.07

10.6

0.15 6.1

1.0

0.2 8.3

16.9 3.9 [I.8 17.5 1.1 0.8

(20m)

0.69

2.0

6.7

44.9 8.2

0.2

12.5

0.50 18.7

1.9

0.5 16.3

20.1 5.8 2.6 14.7 1.0 11.7

(6(Im)

WHISPs

*J. K. Volkman, unpublished results. + N A - - n o t available since analysis not completed. :~C~,/A~C,7 - cholcst-5-en-3/3-yl-hexadecanoate: CI6/A5,22C28 24-methylcholesta-5,22E-dien-313-yl-hexadecanoate. ~A~C_,7 = Cholest-5-en-3[3-ol; 24-Me-A 5,2: = 24-methylcholesta-5,22-dien-3/3-ol- 24-Et-A 5 = 24-ethylcholest-5-en-313-ol. JGagosian et al. (1983b). ' V o l k a n et al. (1983).

37 : 3/37 : 2

Long-chain methyl ketones

A~C27~ 24-Me-~"e2~/total sterols (%) 24-Et-AS~/total sterols (%) Sterols/stanoncs

Steroids"

Wax ester FA/total FA (%) 0.6 34 : 1 wax ester/total 24.8 wax ester (%) Triacylglycerol FA/total 1.0 F A (%) Wax ester/triacylglycerol 1.1 C,,AsC2v$/total steryl 29.7 ester (%) Cl~,lAS"22C2~/total <1 steryl ester (%) Steryl ester FA/total 0.1 F A (%)

Fatty acid esters

16 : 18 : i+a 22 : 18 : 24 :

Fatty acids

FST

Day

3.3

NA

~ 1 0 'j

~18:1 61

NA

NA

NA NA

NA

NA NA

14.2" 3.4* 6.5* NAt 0.5" 1.3

Surface sediment (box core 7)

l a n e 3. Lipids in FSTs, WHISPs, surface sediments, and anchovy fecal pellets from Peru upwelling area

I).7

4.1

6.4

23.0 11.7

NA

NA

NA NA

NA

NA 11.1

13.4 22.7 (I.4 14.3 96 0.5

Anchovy fccal pellets

e~

"4

Lipid flux and particulate matter in Peru (Kaneda, 1967; Johns et al., 1977; Boon et aL, 1978; Perry et al., 1979; Volkman et al., 1980c). Thus relatively high amounts of the branched 15 : 0 acids and a low 18 : 1A9/18 : 1AII ratio tend to indicate some degree of microbial alteration of the organic matter. Tetracosanoic acid (24 : 0) is often attributed to allochthonous (e.g. terrestrial) sources. Surface sediments in the Peru upwelling area contain greater amounts of both microbial and terrestrial markers than FSTs (Table 3; J. K. Volkman et al., unpublished results; cf. Smith et al., 1983a,b). Based on these fatty acids, the sediment traps contain a mixture of phytoplankton and zooplankton fatty acids, in agreement with sample morphology (Staresinic, 1978). The relatively high amounts of 16 : 1A 9, 18 : 1A 9 and 22 : 6, lower levels of branched 15 : 0 acids and a higher 18 : 1A9/18 : 1AII ratio in the night-time FSTs (10 and 11) suggest that organic matter in these samples is less reworked than material in the daytime traps (9 and 8). This assumes, of course, that the fatty acid composition of the source organic material is similar at the start of the two (day and night) sampling periods, and that differences in FST-collected material reflect alterations of the organic matter rather than short-term differences in source. The real situation is probably some combination of these two factors and relative contributions from each cannot be resolved at present. It is also interesting that the greatest relative abundances of 24 : 0, the presumed allochthonous fatty acid, occurs in the daytime traps in which 16 : 1A 9, 18 : I A 9 and 22 : 6 , ' t h e autochthonous components, are lowest. Again, this could represent either varying source functions for these two types of fatty acids, or a relative degradation of the more labile marine-derived and unsaturated components compared to the terrestrial compound. Most often, fatty acids are present, not in the free form, but as esters of fatty alcohols (wax esters), sterols (steryl esters), and glycerol (triacylglycerols). In the FSTs, wax esters, steryl esters and triacylglycerols had flux patterns and abundances relative to POC different from each other, and from their common components, the fatty acids. Wax ester flux was relatively low in FSTs 9, 8 and 11, suggestive of low zooplankton lipid input to these traps, since wax esters are biosynthesized almost exclusively by zooplankton (Kolattukudy, 1976; Sargent, 1976; Sargent et al., 1981; and references therein). FST 10 contained much greater amounts of wax ester as is consistent with migration of zooplankton into surface waters at night to feed on both phytoplankton and zooplankton and preferential collection of zooplankton-derived material (carcasses and fecal pellets) at night compared to daytime (Staresinic, 1978). A clear shift in the wax ester composition of FSTs 8-11 is illustrated by the relatively high abundance of 34 : 1 in the two daytime traps but low levels at night (Table 3). This compound is the predominant wax ester in several samples of copepods and copepod

209

fecal pellets from the Peru upwelling area, but is less abundant in the euphausiid Euphausia mucronata, the dominant macrozooplankter in the sampling area. Among the steryl esters, zooplankton tend to contain mainly cholest-5-en-313-yl esters (Wakeham, 1982), in line with the predominance of free cholest5-en-313-ol in the animals. Phytoplankton, on the other hand, contain lower levels of esters of cholest5-en-313-ol and higher levels of esters typical of phytoplankton sterols (e.g. 24-methylcholesta5,22E-dien-313-ol). Thus, we conclude that FSTs 8-11 are dominated by steryl esters of zooplankton origin (e.g. greater abundance of cholest-5-en-3f3/yl hexadecanoate than 24-methylcholesta-5,22-dien-313-yl hexadecanoate; Table 3). The overall steryl ester flux pattern is generally similar to that of wax esters. Triacylglycerols show a quite different pattern. Like total fatty acids, the triacylglycerol flux at night was greater than in the day; however, unlike fatty acids, the pair of 52 m traps contained more triacylglycerol than the two 14 m traps. The highest triacylglycerol/POC ratio was in FST 11, yet the proportion of fatty acids present in triacylglycerols was greatest in the deeper traps, FSTs 8 and ll (Table 3). Determining the source of triacylglycerols to the FSTs is more difficult than for wax esters and steryl esters, since both phytoplankton and zooplankton biosynthesize triacylglycerols of roughly similar compositions. Free sterols generally showed the same pattern as total fatty acids, a 10-fold flux increase and 5-fold increase in sterol/POC ratio in the night traps. Free fatty alcohols were more uniform. Gagosian et al. (1983a,b) have discussed the sterol composition of these traps in terms of a mixed phytoplankton and zooplankton source (similar to that of fatty acids as discussed above). Cholest-5-en-313-ol and cholesta5,22E-dien-313-ol were the dominant sterols of FSTs 8-11, as would be expected since the sediment trap material contained abundant zooplankton fecal pellets, carcasses, and molts. Lesser amounts of 24m e t h y l c h o l e s t a - 5 , 2 2 E - d i e n - 3 1 3 - o l , and 24methylcholesta-5,24(28)-dien-313-ol, typical of diatoms (Kates et al., 1978; Ballantine et al., 1979; Boutry et al., 1979), were present. An interesting feature of the FST 8-11 sterols is that the relative abundance of 24-methylcholest-5,22E-dien-313-ol was greatest at nighttime traps (FSTs 8 and 11; Table 3), those which also contained the greatest contribution to POC flux from phytodetritus and from anchovy fecal pellets (Table 1 ; Staresinic etal., 1983). The anchovy fecal pellets contained a similar relative abundance of this sterol as the night-time FSTs, but lower amounts of cholest-5-en-313-ol. A sterol generally assigned a terrestrial origin, 24-ethylcholest-5en-313-ol (13-sitosterol), and thus relatively abundant in recent sediments (Huang and Meinschein, 1976; Lee et al., 1980; Gagosian et al., 1983a,b), was less important in FSTs 8-11 than the marine-derived sterols, However, the relative abundance of the

210

STUARTG. WAKEHAMet al.

terrestrial compound is slightly greater in the two deeper sediment traps. Marine organisms are generally not thought to accumulate steroid ketones, and phytoplankton and zooplankton samples from the Peru upwelling area generally contained little, if any, stanone (ring saturated 3-ketosteroids). However, stanones are relatively abundant in the sediment traps (stenone data are not yet available). Major flux trends are not evident for FSTs 8-11, but there is an apparent difference in the sterol/stanone ratio (Table 3). High sterol/stanone ratios in the shallow day and night traps contrast with significantly lower ratios in the deep traps. Stanones in particulate material and recent sediments are believed to arise from microbial transformations of stenols (and/or stanols) (e.g. Gagosian and Smith, 1979; Gagosian et al., 1982; Smith et al., 1982, 1983c). Thus the lower sterol/ stanone ratio in the two deep FSTs might be an indication of microbial degradation of the organic matter. Very long chain di- and triunsaturated C37and C3s methyl ketones were present in FSTs 8-11 (Fig. 2). The flux of methyl ketones was greatest at night (ethyl ketones are also present but have not been quantified), as was their ratio to POC. In FSTs 9, 8 and 10, diunsaturated compounds predominated over their triunsaturated homologs (Table 3). However, the reverse was observed in FST 11. The marine coccolithophore Emiliania huxleyi (as well as perhaps other coccolithophores) biosynthesizes these and other unsaturated long chain compounds (Volkman, 1980a,b), and E. huxleyi is present in patchy distributions in the Peru upwelling area (Ryther et al., 1971). Thus an input of those lipids from E. huxleyi or other coccolithophores is suggested, as was the case for Peru sediments (Volkman et al., 1983). The ratio of triunsaturated to diunsaturated ketones in cultured E. huxleyi is ~ 2-3, similar to that of FST 11 and the surface sediment sample. However, the lower ratios in the other three FSTs suggest either differing source ratios or preferential degradation of the triunsaturated components. FSTs 16-19 Reoccupation of the FST 8-11 sampling site and subsequent collection of a second set of FST samples (FSTs 16-19) further demonstrated the complex nature of the particle flux and composition. The diel and depth trends suggested by FSTs 8-11 and discussed above were not observed during the second sampling (Fig. 2). In part, these differences may reflect the observation of Staresinic (1978) that the second occupation sampled a different stage of upwelling, that is early development of a bloom, rather than a later stage of bloom sampled by FSTs 8-11. A further indication of the differing oceanographic conditions is that the drift trajectories of FSTs 16-19 were southward, whereas FSTs 8-11 drifted northward.

The flux of many lipids (fatty acids, sterols, fatty alcohols, wax esters, and stanones) in FSTs 16-19 paralleled trends for total particulate matter and POC, which were greatest in the two shallow day and night samples (FSTs 16 and 18). For these lipids, FSTs 16--19 show an increased flux at night (FSTs 18 and 19). Fatty alcohols were present in the two 14 m traps at levels comparable to the sterols, while in the night traps fatty alcohols were considerably less abundant, as they were in all FSTs 8-11. On the other hand, the long chain C37 and C3s ketones were 1-2 orders of magnitude less abundant in FSTs 16-19. Several features of specific compound distributions deserve mention, as they differ from results found from FSTs 8-11. Based on the abundances of 16 : 1A9 and 18 : 1 Ay, it is tempting to suggest that FSTs 16-18 contained more phytoplankton-derived material than FST 19, while FST 19 contained more zooplankton lipid. The generally lower levels of cholest-5-en-313-ol support this, but the low abundance of 24methylcholesta-5,22E-dien-313-ol in FSTs 16-18 complicates this interpretation. In terms of the triacylglycerol-fatty acid portion of the total fatty acid pool, FSTs 16-19 show a pattern similar to that of FSTs 8-11, with the 52 m samples containing a higher percentage than the 14 m samples. FST 19 contains an unusually high portion of the total fatty acid esterified in triacylglycerols (21% of total fatty acids). FSTs 16 and 19 contained higher amounts of 24-methylcholesta-5,22-dien-313-yl hexadecanoate relative to cholest-5-en-313-yl hexadecanoate, but FSTs 17 and 18 had more of the zooplankton steryl ester than the phytoplankton-derived ester. For sterols, the deep night sample again had the highest relative abundance of 24-methylcholesta5,22E-dien-313-ol (as did FST 11). Both deep trap samples contained elevated abundances of 24ethylcholest-5-en-313-ol. Sterol/stanone ratios did not show the depth variation apparent in FSTs 8-11, implying that, except perhaps for FST 19, alteration of sterols may have been extensive, certainly to a greater degree than in the 14 m traps during the first sampling (FSTs 9 and 10). The relatively low flux of the C37 and C3s methyl ketones in FSTs 16--19 is further evidence of the patchiness of biological source marker inputs to sinking particles. Although the primary productivity in the water column was actually somewhat higher during the second sampling (Table 1), the second set of sediment traps collected less of the long chain ketones, perhaps due to differences in phytoplankton species composition not reflected by bulk primary productivity measurements. On the other hand, the triunsaturated/diunsaturated ketone ratio in FSTs 16-19 is more similar to a likely source organism, E. huxleyi. Thus, although the absolute flux of long chain ketones seems to be low, suggesting a lower input function, the triunsaturated/diunsaturated compound ratio implies that the particulate matter is relatively fresh. This is somewhat contradictory to the interpretation of the sterol/stanone ratios.

Lipid flux and particulate matter in Peru

WHISP samples Lipid concentrations in the two nocturnal WHISP samples are illustrated in Fig. 3. Ratios of lipid classes in the particles to POC are estimated (assuming WHISP POC concentrations to be similar to those measured in water bottle casts at about the same time; Gagosian et al., 1980) in Table 2. WHISP data should be compared to data for FSTs 10 and 11 which were collecting sinking particles at the same location and time as the WHISPs were sampling suspended particles. Concentration (~g 1-~ of seawater, Fig. 3) differences between the 20 and 60 m WHISPs were generally greater than flux differences between the two FSTs. For example, fatty acids and sterols were an order of magnitude less concentrated in the 60 m WHISP sample compared to the 20 m material, but only a factor of 2-3 decrease in flux was observed for FST 10 at 14 m vs FST 11 and 52 m. The relative abundance of stanones was greater in the WHISPs than the FSTs, but less for wax esters and triacylglycerols. The ratios of the lipids to POC are also significantly different than ratios for the FSTs, and the differences are not always comparable. Thus, the 20 m WHISP sample contained more fatty acid relative to POC than the 14 m FST, but the 60 m WHISP sample was depleted in fatty acid compared to the 52 m FST. On the other hand, both WHISP samples are enriched in sterol relative to the corresponding FSTs, although the difference between WHISPs is greater than for FSTs. The opposite trend was observed for triacylglycerols. Specific marker lipids provide additional evidence of important compositional differences between WHISP and FST samples. The WHISPs contained 16 : 1A9 at the high end of the range of relative abundances for this component in the FSTs, but 18 : 1A9 at the low end of its range. This might suggest a significant input of phytoplankton fatty acids and a less important input of zooplanktonderived material to the WHISPs. Such an interpreta-

r~l

WHISP 4O- H F~ 20rn

tion would be consistent with the WHISPs sampling primarily small, suspended or slowly sinking particles, such as phytoplankton cells, but being less efficient at collecting large, fast sinking particles (e.g. fecal pellets, zooplankton carcasses and molts) or live, swimming zooplankton. However, the picture based on the sterols is less clear. Cholest-5-en-3f3-ol is the major sterol in the 60 m WHISP but 24methylcholesta-5,22E-dien-3[3-ol dominates the 20 m WHISP sample. The WHISP samples contained considerably higher levels of 22 : 6 than FSTs. While 22 : 6 cannot be specifically diagnostic of phytoplankton vs zooplankton sources, the abundance of this labile, polyunsaturated fatty acid might attest to the relative "freshness" of the particulate material sampled by the in situ pumping system. On the other hand, potential indicators of microbial alteration of the organic matter (iso- and anteiso-15 : 0 and the 18: lAg/ 18 : 1M l ratio) are intermediate between FST and surface sediment values. Low ratios of sterol/stanone and 37 : 3/37 : 2 methyl ketones are supportive of some unknown degree of degradation of the organic matter collected.

Biological markers and short-term sediment trap experiments The biomarker approach is based on relating organic compounds in environmental samples to their biological sources. To do so requires an understanding of the oceanic processes which produce, transport and transform these compounds in the water column. Because sediments integrate processes over time scales of years to centuries, temporal fluctuations in organic matter input tend to be smoothed out by processes occurring at the sediment water interface or by the lack of our sampling and analytical capabilities to work with samples representing millimeters of deposition. Time-series sediment trap experiments over periods of weeks to months have shown that particle flux and composi-

WHISP 60m

"I.00.1 0.04

o.oo

i~

211

~

[~Total __.FattyAcid I wax Ester E~Steryl Ester ~]Triocylglycerol ~]Sterol

~FoAtyclohol ~C37 and C38 '_BMethylKetone n-AIkone

Fig. 3. Histogramsoflipidconcentrations(ixgl-l)onalogarithmicscalefor2Oand6OmWHISPsamples, 8 March 1978.

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STUARTG. WAKEHAMet al.

tion do vary over the sampling periods in response to pulses in primary productivity (Deuser and Ross, 1980; Deuser et al., 1981, 1983) or current changes (Honjo et al., 1982; Lee et al., 1983). However, the results discussed here and previously for short-term FSTs in the Peru upwelling (Wakeham et al., 1983a; Gagosian et al., 1983a,b) show that order of magnitude variations in flux and composition of particulate organic matter are common. Furthermore, the biogeochemical information obtained by examination of different lipid types often is complicated by the myriad biosynthetic, transformation and transport processes. Thus, although there are qualitative relationships between biomarkers in potential source organisms and Recent sediments off Peru (e.g. Smith et al., 1983a,b,c; Volkman et al., 1983; Gagosian et al., 1983a,b), elucidation of the quantitative relationship between biomarkers and organic matter production and what is recorded by biomarkers in sediments needs further investigation. We present two examples as illustrations of progress in this area of research. (1) T e t r a c o s a n o i c acid ( 2 4 : 0 ) and 24ethylcholest-5-en-3[3-ol ([3-sitosterol) are often designated as potential indicators of terrestrial source inputs to sediments. However, a poor correlation between these compounds exists in the Peru FSTs (Table 2 and Fig. 4). Two explanations could account for this problem. First, these compounds may not be equally distributed in various species of terrestrial plants, so that in fact their source functions are different. Alternatively, they may be distributed differently within the same plants, for example the fatty acid in surface cuticle wax but the sterol in membranes. This could also lead to differing source inputs, since surface wax and membrane components may not be mobilized equally. Or there may be preferential degradation (or protection against degradation) depending on the physical state of the compounds and/or the mechanism by which they are transported to and through the oceans. (2) Anchovy fecal pellets are an important mechanism for rapid vertical transport of phytoplankton-derived organic matter to the Peru sediments (Staresinic, 1978; Staresinic et al., 1983; Gagosian et al., 1983a,b). Is there a correlation between the flux of certain phytoplankton marker compounds and that of anchovy fecal material? No obvious relationship was observed between the flux of 16 : 1A~ or 22 : 6 and anchovy fecal pellet flux. However, Fig. 5 shows that, in fact there is a general relationship between the flux of the C37 and C3~ unsaturated methyl ketones and anchovy fecal pellet flux. The scatter in the data is considerable, but can be explained in terms of patchy distribution of both the source phytoplankton (perhaps E. huxleyi) and feeding anchovy schools. These examples illustrate the need for a more precise understanding of the distribution of potential biomarkers between organisms as well as within the

2.0

/6

5

/gl2

o

17o 0

20 , 19ll 0.5

I

t.0

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izg 24- E thylcholes l-5- en-31~-olillm9POC Fig. 4. Tetracosanoic acid flux/POC flux vs 24-ethylcholest5-en-313-ol flux/POC flux for Peru upwelling FSTs.

organisms themselves. Furthermore, we have alluded here and elsewhere (e.g. Wakeham et al., 1983a; Volkman et al., 1983; Gagosian et al., 1983a,b) to the question of the physical form in which organic compounds are transported to and in the oceans and its relationship to whether the compounds are degraded or preserved. These issues must be addressed in order that a realistic application of the biomarker concept to aquatic ecosystems and sediments be achieved. CONCLUSIONS

(1) Significant variations in flux and lipid composition of large particles collected in sediment traps occur over periods of hours and days. Diel and depth-related fluctuations of an order of magnitude are not uncommon and patterns vary depending on lipid type and source. (2) Suspended particulate matter collected by in situ large-volume filtration systems had a lipid composition very different from that of the large particles, probably reflecting differences in source, transport and transformation processes affecting each size fraction. (3) Patchiness in flux and composition of lipids in particulate matter places limits on the use of biological markers as quantitative indicators of organic matter sources in the water column and sediments. Acknowledgements--We thank Dr N. Staresinic for help in

collecting the free-drifting sediment trap samples, and

Lipid flux and particulate matter in Peru

213

200

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13

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9

t9 '

4 7

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Fig. 5. C~7 and C~s methyl ketone flux vs anchovy fecal pellet POC flux for all Peru FSTs.

G. Nigrelli, J. Livramento, E. A. Canuel and N. Frew for analytical assistance. This research was supported by Office of Naval Research Contracts N00014-79-C-0071 and N00014-82-C-0071 and National Science Foundation Grants OCE-77-26084, OCE-80-18436 and OCE-82-14695. This is Contribution No. 5610 of the Woods Hole Oceanographic Institution. REFERENCES

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