Oct 14, 1988 - Joseph, 1975; Volkman et al., 1980a) in the region. Haptophytes and ..... For example, in the Drake Passage the fluxes of amino acids, amino.
Org. Geochem. Vol. 14, No. I, pp. 83-96, 1989 Printed in Great Britain. All rights reserved
0146-6380/89 $3.00 + 0.00 Copyright (~' 1989 Pergamon Press plc
Organic geochemistry of particulate matter in the ocean: The role of particles in oceanic sedimentary cycles STUART G. WAKEHAMl and CINDY LEE2 ~Skidaway Institute of Oceanography, P.O. Box 13687, Savannah, GA 31416, U.S.A. 2Marine Sciences Research Center, State University of New York, Stony Brook, NY 11794. U.S.A. (Received 5 April 1988; accepted 14 October 1988)
Abstract--Organic geochemists often use the occurrence of specific organic compounds in marine sediments as biomarkers to relate sedimentary organic matter to biological processes in the overlying water column. However, organic matter undergoes many diagenetic changes during transport through the water column. Only a small fraction of the organic matter produced in surface waters reaches the sea floor to be incorporated into the sediments. This material is subject to considerable transformation by heterotrophic organisms. The initial structures of individual compounds can be altered and the proportion of various compounds and compound classes can change as a result of varying stabilities. We summarize here the results of our studies of the organic geochemistry of suspended and sinking particles collected as part of the PARFLUX and VERTEX programs and present new results for amino acids, fatty acids, sterols and steroidal ketones from the VERTEX project site north of Hawaii. Key words seawater particulate matter, carbon cycle, sinking particles, suspended particles, lipids, fatty acids, sterols, amino acids
INTRODUCTION
The oceanic water column is a transition zone between the sources of organic matter in surface waters and deposition on the sea floor. Particulate organic matter (POM) is produced de novo by marine organisms, primarily in surface waters. In addition, erosion of coastal sediments can resuspend POM along continental margins. Lateral advection of this material can transport it great distances offshore. Particle-associated organic matter in the upper ocean is subject to various in situ transformations. Organic compounds and their alteration products which survive these transformations during their transit to the sea floor may become incorporated into the sedimentary record. Organic geochemical studies have been useful in evaluating the sources of and transformation pathways of organic matter in the water column and sediments since many compounds ("biomarkers") have specific biological sources. Investigations into the biogeochemistry of particulate matter in the oceanic water column are important to organic geochemists interested in deposited sediments for several reasons. The use of biomarkers to determine the source of organic matter and to provide quantitative information about past environments requires knowledge of the relation of the structural features of compounds in ancient sediments to presumed source organisms. The first step is to determine which compounds are contributed to particulate organic matter by marine organisms. Then we must understand the transport and alteration processes in the oceanic water column and at the sediment-water interface. Finally, it is necessary to know what frac-
tions and forms of the organic compounds reaching the sediment-water interface are preserved in the sediments. It is now clear that many transformations of organic matter that occur in the water column are similar to reactions in Recent sediments; thus the water column is a useful environment for studying biogeochemical reactions and mechanisms in general. Oceanic particulate matter plays a crucial role in the global cycling of inorganic and organic compounds. For example, particulate organic matter (POM) affects the precipitation and dissolution of inorganic minerals such as calcite. Inorganic nutrients used by phytoplankton to produce new organic matter in surface waters are regenerated at middepth as POM decomposes. The oxidation of POM also influences the speciation and distribution of trace metals in seawater. POM is intimately involved in the marine carbon cycle (Fig. 1; reviewed by Lee and Wakeham, 1988). The chemical composition and amount of POM in seawater result from a complex set of interactions involving biological production and consumption, and physical processes including aggregation, disaggregation and transport. Primary photosynthetic production by phytoplankton in surface waters is the main source of particulate (and dissolved) organic matter. Most photosyntheticallyproduced carbon enters the marine food web in surface waters through consumption by heterotrophs. A small fraction, usually less than 5-10% of the carbon produced in surface waters, sinks out of the euphotic zone as detritus into the ocean's interior where it is subject to further heterotrophic consumption providing nutrition for meso- and bathypelagic organisms. 83
84
STUARTG. WAKEHAMand CINDYLEE h.)
the nature of organic matter accumulating in marine sediments.
NUTRIENTS,CO2 lPrimary I~roduction (aut°ti°ohy)
death
X
XX~
EXPERIMENTAL
~NNX
Sampling
[~;,HETEROTROPi4S"~::[decomposit o defecation
"PARTICLESi"
ep
/
g g
/
/
" #LARGE PARTICLES sedimentation
se;diment i,fi6C:: v :i : ....... '" . ..... ;,:,,,.', ,, : =, • " ",:?[[ :"/tzbi,'.: 1",:, .... :::1 [ :: diagenesiS ! : ..: preservation
Fig. 1. A conceptual model showing the relationship of particulate matter and water column processes in the oceanic organic carbon cycle.
Particles in seawater are present in a continuum of sizes (McCave, 1975, 1984) and consist of both biotic and abiotic materials. They have diverse sources, including in situ production by marine organisms, precipitation of inorganic materials, resuspension of sedimentary material, and fluvial and aeolian inputs of terrestrial debris. Large rapidly sinking particles (see review by Fowler and Knauer, 1986) in the size range 102-104#m are generally biogenic in origin (planktonic detritus, fecal pellets, eggs, molts and carcasses, and marine snow aggregates) but may contain a significant inorganic component. Large particle classes are generally low in concentration; however, their rapid sinking rates are responsible for most of the vertical flux of material through the water column. At the other end of the size continuum are the far more numerous sub-micron to 100 #m-sized fine suspended particles. Their slow sinking velocities result in long residence times so that suspended particles make a minor contribution to the overall mass flux. In this paper we discuss the biogeochemistry of sinking and suspended particulate organic matter in seawater. Current concepts of the processes which characterize the sources and behavior of marine particulate matter are illustrated using new data from a field experiment in the central North Pacific Ocean (VERTEX IV) and results from previous investigations. Our purpose is to demonstrate the importance of water column processes in determining
VERTEX (Vertical Transport and Exchange) is an interdisciplinary field program designed to characterize the physical, biological and geochemical processes which control the transport and exchange of material in the upper ocean from 0 to 2000 m depth. Sinking and suspended particles discussed below were collected for organic geochemical studies at the VERTEX IV site in the central Pacific gyre 400 km north of Hawaii (28°N, 155°W) during July-August, 1984. The site was extensively surveyed hydrographically during the experiment (Broenkow and Reaves, 1985). Sinking particles were collected in free-floating particle interceptor traps. Samples for lipid analyses were obtained in 0.25 m2-Soutar cones described elsewhere (Martin et al., 1983; Wakeham and Canuel, 1988) and for amino acids in 0.0039m 2 cylinders (Knauer et al., 1979; Lee and Cronin, 1984). Suspended particles for lipid analysis were collected on 293-mm ashed glass-fiber filters (Gelman type A/E) using large volume in situ filtration systems (WHISPs; Wakeham and Canuel, 1988). We will also discuss particle samples from PARFLUX experiments in the equatorial north Atlantic (PARFLUX E) and north central Pacific (PARFLUX P) which were obtained using large moored sediment traps (Honjo, 1980). Some results of lipid and amino acid analyses from these experiments have been described previously (Wakeham et al., 1980; Lee and Cronin, 1982; DeBaar et al., 1983; Wakeham et al., 1984). Samples collected during VERTEX II and III cruises to the eastern tropical North Pacific (Lee and Cronin, 1984; Lee, 1988; Wakeham and Canuel, 1988; Wakeham, 1987) will also be discussed. Analysis
Lipids in sinking and suspended particles from the VERTEX IV site were analysed as described previously (Wakeham and Canuel, 1988). Briefly, the material from sediment traps was lyophilized and extracted with methylene chloride using ultrasonication. Suspended particle samples were Soxhletextracted with toluene:methanol (1: 1). Aliquots of the lipid extracts were separated into major lipid classes by column chromatography on deactivated silica gel. Fractions were analysed by capillary gas chromatography and computerized gas chromatography-mass spectrometry (Wakeham and Canuel, 1988). Wax esters and triacylglycerols were analysed directly (Wakeham and Frew, 1982) while sterols were analysed as trimethylsilyl (TMS) ethers. Aliquots of wax ester and triacylglycerol fractions were transesterified and the fatty acids and fatty alcohols that were released were analysed as methyl esters and acetates, respectively.
85
Particulate matter in the ocean
0
20
40
60
Cumulative Percent 80 100 0 20
PIT
P"/'~lsterols l
40
60
80
100
WHISP
steroidal ketones ~ f a t t y acids l~lwax esters ~triacylglycerols
Fig. 2. Relative abundances of major lipids in VERTEX IV sinking particles (PIT) and suspended particles (WHISP) from the epipelagic and mesopelagic zones. Boldface numbers to the right of the PIT bars are POC flux (mg/m2d); other numbers are lipid flux (#g/m2d). Boldface numbers to the right of WHISP bars are POC concentrations (/~g/1); other numbers are lipid concentrations (ng/l).
Amino acids were determined according to Lee and Cronin (1984). Particle samples were hydrolysed with 6N HC1 for 19h to release amino acids bound as peptides (protein) or adsorbed onto particles. The resulting free amino acids were measured by high-pressure liquid chromatography as o-phthaldialdehyde derivatives. RESULTS AND DISCUSSION Two major questions are addressed in the following sections: (1) what organic material reaches deepsea sediments, and (2) what factors determine the quantity and quality of this organic material? In general, the character of new organic material being delivered to the sediments depends on what is produced in the water column, and what is altered as particles descend to the sea floor. How many and which organic compounds become incorporated into particulate matter depends both on the level of production and on the community structure of organisms producing the POM. Although POM alteration processes in the water column remove some organic compounds by heterotrophic decomposition, other compounds can be introduced at mid-depth, either as alteration products or as compounds synthesized de novo. The residual material which reaches the sediments is thus a combination of compounds produced in surface waters which survive transport and compounds introduced to sinking particles at mid-depth. Production and sources o f particulate organic matter in surface waters
As stated earlier, most particles in the ocean are
produced by plankton in surface waters. There appears to be little relationship between concentrations of smaller suspended particles and primary production at the sea surface (Menzel, 1974), but large particle fluxes are clearly correlated with primary production (Suess, 1980; Lee and Cronin, 1984; Betzer et al., 1984). The organic composition of particles in the upper ocean looks, for the most part, like that of their plankton source (see review by Lee and Wakeham, 1988). Small particles collected by in situ filtration in the epipelagic zone are similar to phytoplankton in composition. The composition of large particles collected in sediment traps at similar depths is dominated by inputs from zooplankton and their fecal pellets. Differences in the composition of large and small particles can be seen clearly in VERTEX IV data in the abundances of lipid classes (Fig. 2) and in the distributions of fatty acids, sterols, and 3-keto-steroids (steroidal ketones) in sediment trap (PIT) and in situ pump (WHISP) samples (Figs 3, 4 and 5). Fatty acids were the most abundant of the several lipid classes measured in VERTEX IV particles collected in the epipelagic zone (Fig. 2). Fatty acids accounted for about 85% of the lipids in suspended particles collected in the euphotic zone (50 m WHISP) but only about 40% in particles sinking out of the euphotic zone (140m PIT) (water column concentrations and vertical fluxes are discussed in a subsequent section). Suspended particles were dominated by 14:0, 16:0 and 22:6co3 fatty acids (Fig. 3); in contrast, 18:lo99 was most abundant in sinking particles. Fatty acids generally are not unambiguous source indicators, but relative abundances of components may be useful in suggesting the relative
86
STUART G.
WAKEHAM
and
CINDY
LEE
VERTEXIV 18
.=
0
,
2
4
"~
7, ,
.... 6 8
0
2
4
T
10 12 14 16 18 20 22 24 26
~25
WHISP
PIT 140m
~32
0
,7~','
6
2
~a33
6
8
8
10 12 14 16 18 20 22 24 26
25
10 12 14 16 18 20 22 24 26
0
2
~20
4 8
4
1500ml
10 12 14 16 18 20 22 24 26
D ) ) m ) D m SAT
MONO- DI-
T~ll-TETRA- )ENTA HEXA -
Fig. 3. Fatty acid distributions in VERTEX 1V PIT and WHISP samples. Bars refer to Table 1. importances of phytoplankton vs zooplankton inputs. For example, typical phytoplankton fatty acids are 14:0, 16:0, 16:1co7, 22:5 and 22:6 while zooplankton fatty acids often include 16:0, 18:1~9, 18:0, 20:5 and 22:6 (Sargent, 1976). Mixed algal populations are to be expected at the VERTEX IV site, as oligotrophic waters of the central Pacific contain a variety of algal groups including predominantly small flagellates (e.g. prymnesiophytes and prasinophytes) and cyanobacteria (blue-green algae; cyanophytes) (M. W. Silver, personal communication). Characteristic fatty acids in prymnesiophytes are 18 : 4e93, 18 : 5~o3, 20: 5~ 3 and
22:6~6 (Chuecas and Riley, 1969; Sargent et al., 1985; Volkman et al., 1981), while cyanobacteria generally biosynthesize varying amounts of 16:0, 16:1~7, 18:1~9, 18:2o96 and 18:3~o3 (Piorreck et al., 1984; Piorreck and Pohl, 1984). Generally low levels of 16:le)7 and 20:5~3 in the suspended particles are consistent with low abundances of diatoms (bacillariophytes; Orcutt and Patterson, 1975; Joseph, 1975; Volkman et al., 1980a) in the region. Haptophytes and chlorophytes, characterized by abundant polyunsaturated C18 fatty acids (Volkman et al., 1981), also do not appear to be major contributors to the suspended particle pool. Dinoflagellates
VERTEX
IV
~-22
tI O,,1
0
2
4
6
8
10 12 14 16 18 20 22
0
2
,4
WHISP 50m~
r ,i
ir o!l
6
10 12 14 16 18 20 22
,"l m ~43
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,.
i
c,~, 0
1500m t
,m 2
4
, ,~,,,,~,,~,~,, 8
,7,'i" m 10 12 14 16 18 20 22
A5.22 A22
12-
f °c
/$5
2
4
6
8
10 12 14 16 18 20 22
A 0 A5,24¢28) A24(28)
Fig. 4. Sterol distributions from VERTEX IV PIT and WHISP samples. For compound identifications, refer to Table 2.
Particulate matter in the ocean VERTEX
87
IV
PIT
27E
-
, . , . 7. " .
o 0
2
WHISP
1~.52
4
6
m ,.,",.7.'I"~T'T 8
o
10 12 14 16 18 20 22 24
I
, , , , , . B. 0 2 4 6
u
. . . . . . . . . B 8 10 112:14 16 18 20 212 24
(1.
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q139
m22
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1-135
1500m
":Jlil l ,n I':JI/i,IH," f 0
2
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o,,!,,,,, ,,m,,,n,
10 12 14 16 18 20 22 24
A 22
A4'22
0
A4
5mr
2
5~A'
4
6
8
10 12 14 16 18 20 22 24
A4,24(2a)
Fig. 5. Steroidal ketone distributions in VERTEX IV PIT and WHISP samples. For compound identifications, refer to Table 3.
might be a source of some o f the 22: 6 (Nichols e t a l . , 1984), but data on sterols (discussed below) indicate relatively minor inputs from dinoflagellates. Oleic acid (18 : 1~o9) is typically not a major fatty acid in phytoplankton, and its dominance in the sediment trap material may thus be attributed to a zooplankton source (Sargent, 1976). The depletion of short-chain (e.g. C~4 and C~6) and polyunsaturated acids in Table 1. Fatty acid assignments for Figs 3, 9 and 10 Bar No. Fatty acid assignment 1 14:0a 2 iso - 15:0 3 a n t e b o -- 15:0 4 15:0 5 16:0 6 16:1 7 16:2 8 16:3 9 16:4 10 18:0 11 18:1~9~ 12 18:1~7 13 18:2 14 18:3 15 18:4 16 18:5 17 20:0 18 20:1 19 20:2 20 20:4 21 20:5 22 22:0 23 22:1 24 22:5 25 22:6 26 24:0 27 24:1 "Number of carbon atoms:number of double bonds. ~l'he ~o-notation denotes the position of the double bond relative to the terminal methyl group.
sinking, compared to suspended, particles might reflect modification of algal fatty acids by heterotrophs prior to the particles sinking into the trap. Heterotrophic modification of the organic composition of particulate matter will be discussed in greater detail in the next section. Sterols were relatively insignificant components of the lipid mixtures in suspended particles (2-5% of total) in the epipelagic zone but were slightly more important in sinking particles (8%) at t 4 0 m . The most abundant sterol in suspended particles from the epipelagic zone, 24-methylcholesta-5,22E-dien-3fl-ol (bar 7 in Fig. 4), is frequently used as a biomarker for diatom lipids because it represents over 90% of the sterols in most species of diatoms [see review of algal sterols by Volkman (1986) and references cited Table 2. Sterol assignments for Figs 4, 9 and 10 Bar No. Sterol assignment 1 24-norcholesta-5,22E-dien-3,8-ol 2 27-nor-24-methylcholesta-5,22E-dien-3fl-ol 3 cholesta-5,22E-dien-3fl-ol 4 5,,-cholest-22E-en-3fl-ol cholest-5-en-3fl-ol 5 6 5,,-cholestan-3#-ol 7 24-methylcholesta-5,22E-dien-3fl-ol 8 24-methyl-5a-cholest-22E-en-3/~-ol 9 24-methylcholesta-5,24(28)-dien-3fl-ol 10 24-methylcholest-24(28)-en-3fl-ol 11 24-methylcholest-5-en-3#-ol 12 24-methyl-5:t-cholestan-3/i'-ol 23,24-dimethylcholesta-5,22E-dien-3#-ol 13 14 23,24-dimethyl-5a-cholest-22E..en-3fl-ol 24-ethylcholesta-5,22E-dien-3,6'-ol 15 16 24-ethyl-5ct-cholest-22E-en-3#-ol 17 C29-dienol 18 23,24-dimethylcholest-5-en-3fl-ol 19 24-ethylcholest-5-en-3/3-ol 20 24-ethyl-5ct-cholestan-3fl-ol 21 24-ethylcholesta-5,24(28)-dien-3/~'-ol 4~t,23,24-trimethylcholest-22E-en-3/~-ol 22
88
STUART G. WAKEHAM and CINDY LEE Table 3. Steroidal ketone assignments for Figs 5, 9 and 10
Bar No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Steroidal ketone assignment 27-nor-24-methyl-5~t-cholest-22-en-3-one 27-nor-24-methylcholesta-4,22,-dien-3-one 5fl -cholesta-4,22-dien-3-one cholest-22-en°3-one cholest-4-en-3-one 5fl-cholestan-3-one 5~-cholest-22-en-3-one 5ct-cholestan-3-one + 24-methyl-5]J-cholest-22-en-3-one 24-methylcholesta-4,22-dien-3-one 24-methyl-5fl -cholest-22-en-3-one 24-methyl-5ct-cholest-22-en-3-one 24-met hylcholest -4-en- 3-one 24-met hylcholesta-4,24(28 )-dien-3-one 24-met hyl-5fl -cholestan-3-one 24-methyl-5~t-cholestan-3-one 24-ethylcholesta-4,22-dien-3-one 24-ethylcholest-4-en-3-one 23,24-dimethyl-5~t-cholest-22-en-3-one 23, 24-dimethyl-5/%cholestan-3-one 24-ethylcholest -22-en-3-one 24-ethyl-5fl-cholestan-3-one 4, 24-dimethyl-5:t -cholestan-3-one 24-et hyl- 5:t-cholestan-3-one 4,23,24-trimethyl-5~ -cholest-22-en-3-one
therein]. However, diatoms are probably not major components of the algal community at the VERTEX IV site (M. W. Silver, personal communication), so a significant diatom source of this sterol is unlikely. On the other hand, 24-methylcholesta-5,22E-dien-3fl-ol is common (over 80% of total sterol component) in many species of prymnesiophytes (Volkman et al., 1981; Marlowe et al., 1984) and in a cyanobacterium (Teshima and Kanazawa, 1972), the types of organisms present at this VERTEX site. Other abundant C28 phytosterols in the VERTEX IV suspended particles are 24-methylcholesta-5,24(28)-dien-3fl-ol (9) and 24-ethylcholesta-5,22E-dien-3fl-ol (15). Both a r e present in some species of diatoms, prymnesiophytes and chrysophytes but are too widely distributed among phytoplankton classes to be useful source indicators (Volkman, 1986). Cholest-5-en-3flol (_5)in seawater particulate matter has been thought to originate mainly from zooplankton (Gagosian et al., 1982, 1983; Wakeham and Canuel, 1988) because it is a dominant component of marine invertebrates (Goad, 1978). Although zooplankton are probably more important quantitatively, algal sources of cholest-5-en-3fl-ol have also been recognized (Volkman, 1986). The case for 24-ethylcholest-5-en-3fl-ol (19) as an indicator of terrigenous material has also become weaker in recent years, since this compound has been reported in a variety of marine algae (Volkman, 1986; Nichols et al., 1987) and in seawater particles and sediments (Matsumoto et al., 1982; Volkman, 1986) collected in areas of the ocean remote from continental inputs. Thus, a predominantly algal source for the 24-ethylcholest-5-en-3fl-ol in the central Pacific VERTEX suspended particles is suggested; however, since the stereochemistry of this compound has not been determined, its source remains uncertain. Only minor inputs of particulate
sterols by dinoflagellates are indicated by small amounts of 23,24-dimethylcholesta-5,22E-dien-3fl-ol (13) and 4~t,23,24-trimethylcholest-22E-en-3fl-ol (22). The main feature of sterols in sinking particles in the epipelagic zone is the elevated abundance of cholesta-5,22-dien-3fl-ol (3) and cholest-5-en-3fl-ol (_5), most likely of zooplankton origin. This inference is supported by a marked depletion of the phytosterois in sinking compared to suspended particles. The dominance of zooplankton sterols in the sediment trap material could be due to inclusion in the passively sinking particle pool of zooplankton carcasses and moults, or to inclusion of live organisms ("swimmers") in the sample. Fecal pellets are also important components of sediment trap material. Fecal pellets produced by herbivores tend to be depleted in phytosterols and enriched in animal sterols due to metabolic processes taking place in the animals' gut, as will be discussed later. The 3-keto-steroids (steroidal ketones) are minor intermediates in sterol biosynthesis by marine organisms (Goad, 1978) and were present in suspended and sinking particles where they represented only 0.5% of the total lipid. The ketones were dominated by A4- and A4.:2-stenones in the 140 m sediment trap sample, but the 50m WHISP sample was considerably more complex in composition and contained a wide range of both stenones and nuclear-unsaturated stanones. Compared to sterols, literature reports of steroid ketones in marine organisms are limited. A4-Stenones have been reported in dinoflagellates (Withers et al., 1978; Kokke et al., 1982) and red algae (Kanazawa and Yoshioka, 1971), and stenones and stanones have been found in several marine animals (Popovet al., 1976; Edmonds et al., 1977; Delseth el al., 1978; Wakeham and Canuel, 1986). Other important lipids biosynthesized by marine organisms include long-chain alkyl esters (wax esters) and triacylglycerols, both involved in energy storage and mobilization. The synthesis of wax esters tends to be limited to zooplankton, especially calanoid copepods. These copepods inhabit oceanic areas characterized by spotty food supply, and wax ester distributions are therefore highly dependent on species, ecological niche, nutritional status, and life stage (Sargent et al., 1981). Triacylglycerols, on the other hand, are the major energy reserve lipid in phytoplankton and those zooplankton which do not store large amounts of wax ester. Wax esters in VERTEX IV sinking particles attest to the contribution of zooplankton lipids, while the very low levels of wax esters in the suspended particles show that few wax ester-synthesizing zooplankton were sampled by the in situ titration procedure (Fig. 2). Triacylglycerols are not as source-specific as wax esters, but analysis of fatty acids released by hydrolysis of the triacylglycerols (data not shown) suggest a relatively greater input of phytoplankton triacylglycerols in the suspended particles and more zooplankton-derived material in the sinking particles.
Particulate matter in the ocean Table 4. Amino acid fluxes at VERTEX IV. The inner trap compartment collected both detrital material and some active swimmers. The outer compartment collected only swimmers
Depth (m) 50 150 300 500 700 900 1000 1100 1550
Flux ( # g a a - C m 2d ~) ....... Inner Outer 11.1 12.1 14.3 13.3 12.2 7.3 10.4 1.9 8.0
15.7 12.2 8.2 4.7 9.9 4.8 9.7 3.5 3.2
Proteins and carbohydrates account for a large part of the organic carbon in particles. These compounds are largely structural components in marine organisms and do not vary as greatly in composition between organisms as do some lipids. Nevertheless, insight into the origin of particles may be derived from subtle differences in composition. For example, inputs from algal producers of siliceous vs. carbonate skeletons can be distinguished by relative abundances of amino acids and sugars. Thus aspartic acid'glycine and arabinose:fucose ratios indicate the dominant input of siliceous organisms to large particles in the Sargasso Sea and Panama Basin (Ittekkot et al., 1984a,b). Ittekkot and coworkers also used the fact that zooplankton are greatly enriched in hexosamines compared with amino acids to indicate relative inputs from phytoplankton and zooplankton using amino acid:hexosamine ratios. The influence of bacteria on organic matter composition is indicated by certain non-protein amino acids present in particles. The presence of muramic acid, a component of bacterial cell membranes, in particulate material indicates bacterial colonization (Lee et aL, 1983; Ittekkot et al., 1984a). On the other hand, bacterial degradation is indicated by increased abundances of ornithine, a decomposition product of the protein amino acid arginine (Lee and Cronin, 1984). Fluxes of hydrolyzed amino acids at the VERTEX IV site are shown in Table 4. The constancy of amino acid fluxes over 1550m (inner section) suggests that there is little decomposition with depth compared to other more productive sites where amino acid fluxes have been measured (Lee and Cronin, 1984). Amino acids were collected in sediment traps containing specially designed swimmer collectors (modified after the design of Coale and Bruland, unpublished). These traps had an inner container which collected vertically sinking material. An outer section collected only material which could actively "swim" toward the side of the trap cylinder and die when it contacted the formalin solution lower in the trap. Separation of swimmers and sinking particles was not perfect; the inner trap contained
89
both swimmers and detrital material, while the outer trap collected active swimmers almost exclusively. Fluxes calculated from material in the inner section changed little with depth. These fluxes generally compare well with previous deep-water sediment trap measurements (using Honjo traps) from the North Pacific (Ittekkot et al., 1984b). Fluxes calculated from material collected in the outer section were considerably higher in the two near-surface traps, as would be expected if active swimmers are collected. These results show that even at 1500 m, swimmers can lead to significant overestimates of fluxes in poisoned traps. Duplicate traps at each depth showed that replication was poorer in the outer portion of the trap containing swimmers than in the inner portion (data not shown). Other specific organic compounds which we did not measure in the VERTEX IV samples could provide additional information about the sources of organic matter. For example, carotenoids are photosynthetic accessory pigments to chlorophylls in all phytoplankton and might help to distinguish different algal sources. Repeta and Gagosian (1984) found fucoxanthin to be the dominant carotenoid in suspended particles in the Peru upwelling area. The abundance of this carotenoid was attributed to diatoms, the dominant phytoplankton in the water column. Little of the dinoflagellate marker, peridinin, was present, and dinoflagellate abundances were in fact low. Large particles collected in sediment traps, on the other hand, contained more fucoxanthinol than the smaller suspended particles, and a zooplankton source was suggested for this compound.
Alteration of particulate organic matter composition in surface waters by zooplankton and fish Most of the particulate organic material biosynthesized by phytoplankton in surface waters is recycled in the upper ocean, much of it being consumed by zooplankton and fish. Zooplankton grazing on phytoplankton incorporate about 45% of the phytoplankton carbon into growth and egest 3-4% in the form of fecal pellets; the remainder is respired or released as DOC (Copping and Lorenzen, 1980). Ingestion of living and detrital particles by animals can lead to the production of new particles in the form of fecal matter which may have a very different composition than the animal's original particulate diet (Corner et al., 1986). Alterations in composition of organic matter occur via enzymatic reactions during assimilation or by transformation by microflora in the gut. These alterations may continue after defecation of the fecal pellet if enzymes and microorganisms remain active in the fecal pellet after it has been released from the organism. Fecal matter comprises a significant portion of the particulate material which sinks through the water column and thus is an important vehicle for transporting organic compounds to the sediments.
90
STUART G. WAKEHAMand CINDY LEE
Several studies have documented the changes in organic composition of particulate material during metabolism by zooplankton. Compositional changes can be due to metabolic transformations where dietary compounds are biochemically converted to new compounds not initially present in the diet. Changes can also occur because of the different relative reactivities of compounds; the more labile compounds are selectively removed in favor of less reactive molecules (modification or "editing"). An example of editing due to different compound reactivities was described by Tanoue et al. (1982) who fed Dunaliella tertiolecta to the euphausiid Euphausia superba and reported preferential depletion of algal amino acids and fatty acids compared to sugars during metabolism and fecal pellet production. Editing of compound classes may not affect the composition of compounds within a class,, however. Zooplankton and their fecal pellets are not very different from source plants in terms of individual sugar and amino acid compositions. For example, the amino acid composition of fecal pellets produced by Calanus was not very different from the algal diet consumed by this copepod (Cowey and Corner, 1966). Other classes of compounds show substantially more editing and transformation during metabolism. Material defecated by herbivores contains a mix of extensively modified algal lipids and lipids endogenous to the zooplankton. Short-chain and polyunsaturated fatty acids and C28-sterols often found in dietary phytoplankton, e.g. 24-methylcholesta-5,22Edien-3/~-ol and 24-methylcholesta-5,24(28)-dien-3/~ol, are efficiently metabolized by zooplankton. Thus fecal pellets are depleted in these compounds and enriched in zooplankton-derived compounds, such as cholesterol and wax esters (Prahl et al., 1984b; Harvey et al., 1987). Dietary fatty acids appear to be more readily assimilated than dietary sterols (Wakeham and Canuel, 1986; Harvey et al., 1987). Certain compounds appear to be relatively stable or recalcitrant to metabolic alteration, due to either relatively long carbon backbones, unusual patterns of unsaturation, or unique stereochemistry (Alexander, 1975). Volkman et al. (1980b) suggested that unsaturated C37- and C3s-methyl and ethyl ketones may be enriched in fecal matter relative to the algal source. The degree of unsaturation of these compounds in particles changes little with transport down the water column (Prahl and Wakeham, 1987). Harvey et al. (1987) found that 4-methylsterols were relatively resistant to metabolism. Wakeham and Canuel (1986) found that, when the pelagic crab Pleuroncodes planipes fed on zooplankton, preferential metabolism of fatty acids, the dominant lipid in zooplankton, resulted in the egestion of fecal pellets in which the more resistant sterols were the dominant lipid. Modifications of organic compounds continue throughout the food web and can depend on feeding mechanism. For example, Neal et al. (1986) compared the lipid composition of fecal pellets produced
by barnacle nauplii feeding on unicellular algae (herbivory) with fecal pellets from adult copepods feeding on the barnacle nauplii fecal pellets (coprophagy). Pellets produced during coprophagy and herbivory had minimal differences in fatty acid composition. However, a much wider range of plant sterols were present in fecal pellets produced by coprophagy compared with direct herbivory. Prahl et al. (1985) found similar alteration of dietary compounds further up the food web in a study of carnivorous fish feeding on copepods. Enzymatic reactions by enteric microflora in zooplankton and fish can introduce transformation products of dietary compounds into gut contents which eventually are egested. The conversion of algal chlorophyll to phaeophorbide by herbivorous zooplankton is a well known example (Shuman and Lorenzen, 1977). Hydrolysis of the algal carotenoids fucoxanthin and peridinin to fucoxanthinol and peridininol in the guts of herbivores may lead to production of fecal pellets enriched in the alcohols (Repeta and Gagosian, 1984). Wakeham and Canuel (1986) detected steroidal hydrocarbons and ketones in feces of the crab P. planipes when these compounds were not evident in the crab's diet; they proposed that these steroids were transformation products produced by the enteric bacteria of the crab. Prahl et al. (1984a) documented the production of dihydrophytol by the copepod Calanus helgolandicus fed on a unialgal diet deficient in this saturated alcohol and suggested that algal phytol might be reduced enzymatically by the animal or by gut microflora. Transport and alteration o f particulate organic matter throughout the water column
Particles which escape consumption by heterotrophs in surface waters can settle into the deep ocean and may eventually reach the sea floor. Vertical fluxes of sinking POM and concentrations of suspended POM both decrease markedly in the upper 200~00 m of the water column. This is consistent with the view that most degradation of organic matter occurs before particles exit the euphotic zone. Only 1-10% of the organic carbon produced in surface waters sinks below 500 m (Bishop et al., 1978; Martin et al., 1987). At the VERTEX IV site, where the upper 1500 m of the water column was sampled, vertical fluxes of POC and lipids decreased sharply by 500m and then remained relatively constant to 1500 m (Fig. 6). Concentrations of suspended POC and most lipids decreased more rapidly in surface waters, but reached constant values by 250 m. In the VERTEX IV samples and at other sites, vertical fluxes remain relatively constant at depths below about 1000 m (presumably the same holds for suspended particulate lipids but comparable data are lacking). In the deep ocean, fluxes of organic matter generally appear to be relatively invariant regardless of trends in the upper water column (Fig. 7). Amino acid fluxes decreased with depth when "swimmers"
Particulate matter in the ocean
rng/m2d 0 20 40 O- . L J__J.~
pg/m2d 150 300 I I I I
-#
VERTEX IV PITS pg/m2d pg/m2d pg/m2d 5 10 O 800 1600 0 500 1000 I I i I ~ I I I I
pg/m2d 600 1200 r I I I
J
500Q.
91
i
a lOOO. I 15oo
pg/I 30 60 0
ng/I 30 60
VERTEX ng/I 3
IV WHISPS ng/I 1200 2400
ng/I 20
ng/I 200 400
6
40
• , •500¢..
\
O.
tmlOOO [
1
1500-
POC
Sterots
Fatty acids
Steroidal ketones
Triacylglycerols
Wax esters
Fig. 6. Vertical depth profiles for particulate organic carbon (POC) and lipids associated with sinking particles (PIT) and suspended particles (WHISP) at VERTEX IV.
were included but were relatively constant to 700 m when they were not (Table 4). Swimmers may have also influenced flux calculations for POC and lipids in this and other studies. As material sinks out of the euphotic zone, degradation continues to alter the composition of particles as they are transported through the ocean's interior towards the sea floor. Alteration rates in the deep sea are probably slower than in surface waters because of lowered ambient temperatures and heterotrophic activity, but can result in major changes in the composition of particles with depth. For example, in the Drake Passage the fluxes of amino acids, amino sugars and carbohydrates decreased with depth over 2500m (Wefer et al., 1982). A relatively greater
0 0
PARFLUX mg/m2d pg/m2d IJg/rn2d 10 0 100 200 0 20 400 5 I i I t i I i
1000"~2000-
~
decrease in flux of amino acids with depth relative to carbohydrates, was attributed to preferential degradation of proteinaceous material. Amino sugars were relatively stable with depth; it was suggested that the source of these sugars might be poorly degradable chitinaceous material. At the VERTEX IV site, changes in relative amounts of various compound classes with depth were also apparent. Fatty acids became a relatively less abundant portion of the lipids while sterols became more abundant (Fig. 2) with depth; indeed, sterols dominated the 1500 m trap material whereas fatty acids dominated at 140m. Fatty acids in the 1500m sinking (PIT) and suspended (WHISP) particles reflected a loss of polyunsaturated corn-
3000-
E pg/m2d pg/m2d 200 400 0 1 2 0 i I i I
/
/
~\\\\\\\\\\\\\\-~ ;teroidal ketones
,%.\\\\\\\\\\\\\~, Fatty acids
pg/m2d 5 10
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POC
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Fig. 7. Vertical profiles of organic components at PARFLUX E (data from Wakeham et al., 1980).
STUART G. WAKEHAM and CINDY LEE
92
Cumulative Percent 20
40
60
80
100
ketones may also be involved. An increase in the flux of amino acids at 1000 m at VERTEX IV (Table 4) was present in both the swimmer and non-swimmer fractions, suggesting that living organisms can influence flux calculations at great depths. Organic material reaching the sediment-water interface
qD t~
~ 1 sterols R=mwax esters BBIsteroidal ketones I ~ triacylglycerols m fatty acids
Fig. 8. Relative abundances of lipids in PARFLUX E sediment trap samples (from Wakeham et al., 1980). Boldface numbers to the right of the bars are POC flux (mg/m2d); the other set of numbers is lipid flux (~g/m2d).
ponents and increased abundances of 18:0 and 18:1 compared to the 140 m PIT and 50m WHISP samples. Preferential loss of C2s-phytosterols resulted in particles at 1500 m which were enriched in cholest-5-en-3fl-ol and 24-ethylcholest-5-en-3fl-ol. Even though the bulk of particulate organic compounds originate at the surface and decomposition processes remove these compounds with depth, increased vertical fluxes and suspended concentrations of some compounds can occur at mid-depth. For example, flux maxima of sterols and triacylglycerols occurred at 989 m at the P A R F L U X E site (Fig. 7) (Wakeham et al., 1980). These maxima were attributed to inputs to this trap of organic compounds biosynthesized by zooplankton species living at depth. The distributions of compounds are also consistent with inputs of material biosynthesized by mid-water organisms. Similar maxima at mid-depth have been observed in the Pacific for fatty acids and wax esters at 1500 m at VERTEX I and at 2700 m at the P A R F L U X P site (Wakeham et al., 1984). Steadily increasing concentrations of wax esters associated with suspended particles at VERTEX IV (Fig. 6) likewise suggest inclusion of wax estercontaining zooplankton-derived particulate material in the in situ filtration samples at depth (also observed at VERTEX II and III; Wakeham and Canuel, 1988). Steroid ketones consistently increase in abundance relative to other lipids as depth increases (Fig. 2 for VERTEX IV and Fig. 8 for P A R F L U X E). This increased abundance might be due to preferential preservation of these compounds compared to other lipids. However, the increase in vertical flux of the steroid ketones between 500 and 1500 m at VERTEX IV (0.9 and 2.2#g/m:d, respectively) and possibly between 3755 m and 5068 m at P A R F L U X E (3.6 vs 4.0/t g/m2d) suggests that in situ production of steroid
Hedges et al. (1988) recently calculated relative reactivities of various organic compounds as they passed to the sediments from the shallow (.~ 110 m) water column of Dabob Bay, Washington. They found that the organic materials produced in the overlying waters exhibited a wide range of reactivities toward respirative degradation at the sediment-water interface. Some compounds, such as the vanillyl and cinnamyl structural units derived from vascular plant debris, exhibited essentially no degradation. On the other hand, syringyl phenols, also derived from vascular plants, were measurably degraded (30-40%). Approximately 70% of the neutral sugars and total organic nitrogen was lost at the water-sediment interface. Previously reported losses of planktonderived lipids ( ~ 9 0 % ; Prahl et al., 1980) and plant pigments ( ~ 9 9 % ; Furlong and Carpenter, 1988) at this site were even greater. Although differences in relative rates of degradation of organic compounds in the sediment have long been inferred, the studies by the previous authors demonstrate the relative reactivity relationships for a large variety of compounds and tie in these reactivities to degradation at or near the sediment-water interface. In the deep ocean, only a few percent or less of all the organic matter biosynthesized in the euphotic zone reaches the sea floor, and little of this organic material can be recognized structurally as compounds originally produced in surface waters. Gagosian et al. (1982) estimated that at the P A R F L U X E site, 0.2-0.7% of the total sterols produced in the euphotic zone survived transport to 5068 m. An even smaller percentage of the fatty acid production reach bottom waters. Only about 0.01-0.2% of surface-produced fatty acids reached traps at 5068 m in the Atlantic ( P A R F L U X E) and 5582m in the Pacific (PARFLUX P) (Wakeham et al., 1984). Based on sediment trap and surface core data, Lee and Cronin (1982) found that less than 10% of the surface-produced amino acids reached the bottom at a more shallow site in the Peru upwelling zone. Particles which do reach deep-sea sediments are probably similar in composition to the material collected in near-bottom sediment traps. Fatty acid, sterol, and steroidal ketone distributions in material from the 5068 m PARF L U X E sediment trap (deployed about 200 m above the bottom) and the VERTEX III trap are shown in Figs 9 and l0 respectively. Differences between this material and samples from closer to the surface (389 m) illustrate the result of alteration processes in the water column.
Particulate matter in the ocean PARFLUX
93
E
D27
-1 o
!
_=°
,?,
,
~ 2 4 6 ~ 10 l~ 14 ~6 18 ~0 22 24 ~6
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16
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212
118
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!i
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,
! ......
o ~ 4 ~, J ,o ,2 ,i ,o ,' 20 2'~ ~',, STEROIDALKETONES
SAT MONO DI- TRPTETRA-PENTA-HEXA-
Fig. 9. Fatty acid, sterol and steroidal ketone distributions in the shallowest (389 m) and deepest (5068 m) sediment traps at the 5200 m deep PARFLUX E site. [Fatty acid data from DeBaar et al. (1983); sterol and steroid ketone data from Gagosian et al. (1982)].
face ocean sources of particles are difficult to average out in sediment trap samples covering less than at least a year time period, while the sediments integrate on scales of years to centuries. Yet another difficulty in comparing compositions of sinking particles and sediments is the presence of a loosely-packed, easily resuspended "floc" at the sediment-water interface. This material is often lost except during careful boxcoring. This floc can have a chemical composition different from the underlying sediment. The sterol composition, for example, suggests that the material at the sediment-water interface is fresher than that in
It is difficult to compare the composition of particles sinking to the ocean floor with particles which are presently accumulating in open ocean sediments. This is because there has been poor coordination of organic geochemical studies of particulate matter with analyses of the underlying sediment. For example, sediment samples are not available for organic analysis at the P A R F L U X E and P sites where sediment traps were deployed near the bottom. Where sediments are available (e.g. the 3500 m deep VERTEX II/III site), the deepest sediment trap was 2000 m above the bottom. Seasonal variations in sur-
V E R T E X III
80
I~ 32
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ACIDS
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; ~ ~ ; ; ,;,i,~, S T E ~
1
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201, 3 FLOC ii,I ..hn, l
-- '? ~ ,'o• ,'2'? ,'4~? ,'6' ,'8' 2'o 2'2
10
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rn
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.
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.
.
.
.
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"1 ' ' ' =Y ' 8. 10 . 12 . .14 .16 . 18 20 22 24
i q
~
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,
0 2 4 6 8 10 12 14 16 18 20 22 24 STEROIDALKETONES
Fig. 10. Fatty acid, sterol and steroidal ketone data from the 1500m sediment trap and bottom sediment floc (3500 m water depth) at VERTEX IlI.
94
STUARTG. WAKEHAMand CINDY LEE
deeper sediments, possibly because it has been less reworked by benthic organisms (Lee et al., 1979). Analyses of hydrocarbons in the floc layer also support this interpretation (Burns, 1986). The floc is probably a transition zone between water column particulate matter and sub-bottom sediments, but organic geochemical processes occurring in the floc have not been extensively studied. Keeping in mind the large depth difference between the bottom (3500 m) and the 1500 m trap at VERTEX III, we can compare the composition of particles and floc there. Fatty acid, sterol, and steroidal ketone distributions at the VERTEX III site are shown in Fig. 10. The relatively high abundances of 16:1 and 18:1 in the trap sample contrast with the depletion of these compounds in the floc and the enrichment of saturated (14:0, 16:0, 18:0, 20:0 and 22:0) components. In the sterols, the marked predominance of cholest-5-en-3fl-ol in the trap material contrasts with the lesser abundance of cholesl-5-en-3fl-ol and increased abundances of 24methylcholesta-5,22E-dien-3fl-ol, 24-methylcholesta5,24(28)-dien-3fl-ol and 24-ethylcholesta-5-en-3fl-ol. Steroidal ketones in the trap sample are dominated by cholest-4-en-3-one, but in the sediment floc by 24-methyl-5a-cholesta-22-en-3-one.These differences in composition could be due to a combination of (1) continued alteration of particulate organic matter as it sinks between 1500 m and the 3500m bottom, (2) diagenesis and alteration of material within the sediment floc, and (3) the very different time scales involved in the two sample types. Since the data discussed in this paper cover a variety of oceanic regimes and a very limited and diverse sample set, detailed comparisons of particle and sediment data are unwarranted at this point. Nevertheless, it is clear that significant differences exist between the composition of organic material biosynthesized in the upper ocean which is the ultimate source of organic matter in the sediments, and the composition of the sediment itself. CONCLUSIONS The transport and alteration processes acting on particulate organic matter sinking through the oceanic water column are complex. The preceding discussion has demonstrated that material which reaches the seafloor and enters into the sediment record is significantly different in composition from material produced in surface waters. The utility of biomarkers as indicators of the source of organic matter and biogeochemical alteration processes depends on understanding the qualitative and quantitative relationships between the amount and composition of organic compounds in surface waters and in sediments. The qualitative aspects of this problem are relatively straightforward, since the presence of the same compounds in both surface water particulate material and sediments implies a logical
source-sink connection, especially if unique biological sources can be identified. On the other hand, a quantitative use of biomarkers is much less well defined. As we have shown, there are substantial and often selective losses of organic compounds during sedimentation. The nature of the water column, for example, its depth, productivity, and redox condition, also has a major influence on the fate of organic material during vertical transit and hence on the composition of material deposited at the sedimentwater interface. More research on rates and mechanisms of transformation reactions is needed to develop biomarkers as quantitative tools in organic geochemistry. thank our co-participants in the VERTEX program for assistance in sampling during the 1984 cruise. We also thank E. Canuel, C. Cronin and N. Zhu for assistance in chemical analyses of the VERTEX IV samples. This research was supported by Office of Naval Research Contracts N00014-85-C-0071 and N00014-87-C-0071 and VERTEX travel grant OCE 80-03200 from the National Science Foundation. Acknowledgements--We
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