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Seasonality in the fluxes of sugars, amino acids, and amino sugars to the deep ocean: Panama basin
Deep-Sea Research,Vol. 31, No. 9, pp. 1071 to 1083, 1984. Printed in Great Britain.
0198--0149/84$3.00 + 0.00 O 1984 PergamonPress Ltd.
Seasonality in the fluxes of sugars, amino acids, and amino sugars to the deep oeean: Panama Basin VENUOOP^t~N ITTEKKOT,*E~ON T. D~ENS* and SusuMt3 HONJO~ (Received 10 May 1983; in revisedform 24 January 1984; accepted 1 February 1984)
Almtra~---T'nne-seriessediment traps were deployed for an entire year at depths of 890, 2590, and 3560 m at a station in the Panama Basin during 1980. Fluxes of sugars, amino acids, and amino sugars varied seamonallyat each depth. Two peak fluxeswere observed: one in February-March, the other in Juno-July. The peaks were associated with a high productivityperiod by regional upwelling and an unusual coceolithophorid bloom. There were significant differences in the distributions of sugars and amino acids associated with the fluxes. The peak flux of June/July was characterized by high amounts of arabino6e and ribose within the sugar, and high amounts of aspartic acid in the amino acid fractions. The differences were observed at all three depths simultaneously, indicating rapid vertical transport without significant dissolution or decomposition. The observed pattern indicates the utility of specific compounds such as sugars and amino acids as tracers of source materials in the marine environment.
INTRODUCTION
CONSIDERABLE information on the vertical flux of materials to the deep ocean has been obtained from studies with sediment traps (HoN~o, 1980; DEUSER and Ross, 1980; HONDO et al., 1982a) and in situ pumping systems (BIsHoP et aL, 1977). Such studies show that the transport of materials into the deep-ocean environment is rapid and occurs by large particles such as fecal matters fecal pellets, or 'marine snow'. In addition, seasonal fluctuations of material fluxes in phase with primary productivity were also observed (I~USER and Ross, 1980; HONJO, 1982). Better insight into the transport and transformation processes involving the sedimenting material may be gained by characterizing the organic fraction in detail (WAKEHAM et aL, 1980; WEFZZRet al., 1982; LEE et aL, 1983). Such processes control the nature of organic debris arriving at the sea floor and in turn determine the 'utility' of organic matter for benthic communities and the nature and quantity of organic matter ultimately buried in sediments. IT'rEKKOTet al. (1984) reported on the detailed composition of organic matter reaching one deep-sea environment of the Sargasso Sea. It was shown that fluxes of individual classes of compounds such as sugars and amino acids varied in phase with primary productivity. Variations in their distributions appeared to reflect the nature of transport and transformation processes within the overlying water column. We have extended the investigations to include samples collected during sediment trap deployments at various depths in the water column
* Geologisch-Paliontologisches lnstitut and Museum, Universitit Hamburg, Bundesstrass¢ 55, 2000 H a m b u r g 13, Federal Republic o f Germany. t Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A. 1071
1072
V. ITrEKKOT et al.
from yet another deep-sea environment--the Panama Basin. The results are expected to give information on the degradation of organic matter during settling. METHODS
The sediment traps deployed during the experiments were capable of collecting settling particles in six two-month increments totaling a year. The basic configuration of the trap used was the PARFLUX Mark II with a 1.5-m2 opening (Homo et al., 1980). A spring motor drove a rotary sampler and quartz oscillator-based electronics controlled its movement. The timing of the advancing sampler was synchronized among three traps within 10 rain of error over 12 months. Sodium azide tablets were added to the sampler before deployment to stop microbial action during sampling. A mooring array with three such time-series sediment traps was deployed at 890, 2590, and 3560 m below the surface at a station in the Panama Bight (5°22 N, 85°35 W; water depth 3860 m; Fig. I) from 3 December, 1979 to 2 December, 1980. The automated sediment trap worked successfully except for increments at 2590 and 3560m due to mechanical failure. The moored array was recovered on 5 March, 1981. Samples from the experiments will be referred to as time-series samples (TS). For comparison, determinations of sugar and amino acids from samples collected during the PARFLUX experiment at a station in the Panama Basin (5°2 N, 81°53 W) from August 1979 to December 1979 (112 days) with the help of a moored array of sediment traps set at 667, 1268, 2869, 3769, and 3791 m are also presented. For details of the experiment see HONJO et al. (1982a) and HoNJo et aL (1982b). These samples are referred to as depth-series samples (DS). Each trap sample was split into aliquots with an Erez-Honjo splitter (Homo, 1980). Sediments collected in the < 1-mm range were analyzed for sugars, amino acids, and amino sugars. The analytical techniques are described by I~'EKKOT et al. (1984). As only small samples were available the results are based on single analyses. II
I
C
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Fig. 1.
Location of the sediment trap experiment.
Fluxes of sugars, amino acids, and amino sugars in the Panama Basin
10 7 3
RESULTS
T S samples Fluxes of organic carbon were in the range of 5.5 to 17.3, 3.6 to 16.6, and 8.3 to 16.6 mg m -2 d -~ at 890, 2590, and 3560 m, respectively. Two peak fluxes were observed at all depths in February-March and June-July. A similar pattern was also observed for nitrogen. The fluxes varied between 0.67 and 1.74 mg m -2 d -I at 890 m, 0.4 and 2.0 mg m -2 d -~ at 2590 m, and between 0.72 and 1.63 mg m -2 d -~ at 3590 m. Lower fluxes of both carbon and nitrogen were observed in December-January and October-November. Except for the February-March flux of sugars, the fluxes of organic matter were similar to the fluxes of carbon and nitrogen (Fig. 2). The maximum fluxes of sugars were 7.6, 3.6, and 3.6 mg m -2 d -= at 890, 2590, and 3560 m, respectively. For amino acids they were 9.9, 7.2, and 6.6 mg m -2 d -~ at 890, 2590, and 3560 m, respectively. The amino sugar flux to the shallowest trap (890 m) was minimal during February-March. Concentrations of sugars, amino acids, and amino sugars in the particulate matter varied between 4.25 and 10, 6.99 and 33.46, and 0.07 and 5.94 mg g-1 respectively (Tables l and 2). Except for the high concentration (10 mg g-l) of sugars during October-November at 890 m, the higher concentrations were observed during February-March. Although there was an overall decrease in concentration with depth the maxima were evident at all depths.
SUGARS
AMINOACIDS
to
:1
~: i 1
"
2590m
356Om
lg80
,ell
IoIalPiultlulJlaltlsiolul
1980
Fig. 2. Fluxes of sugars and amino acids to three depths at a deep-water station in the Panama Basin during 1980. The fluxes at 2590 m during Ausmt to October (dashed lines) were observed during a previous time-scrics experiment at 2265 m described by HONJOe! al. (1982c). See also Methods.
1074
V. ITTEKKOTet aL
Table 1. Distribution of sugars in mole 96 in samples collected during time-series sediment trap deployments at three depths at a deep-water station in the Panama Basin during 1980
Depth
Month
(m)
1980
Rha
Rib
Man
Ara
Fuc
Gal
Xyl
GIc
Total
890
Feb-Mar Apt-May Jun-Jul Aug-Sep Oct-Nov
8.1 7.3 5.5 6.6 5.9
0.5 1.2 11.6 1.8 1.2
17.1 17.1 20.1 19.4 13.8
6.0 7.4 12.2 11.8 11.9
7.7 9.1 2.0 6.8 9.8
23.5 27.8 18.7 24.6 30.2
10.5 12.9 14.6 11.7 12.4
26.6 17.1 15.3 17.2 14.7
5.28 7.78 5.34 5.82 10.22
2590
Dec-Jan Feb-Mar Apt-May Jun-Jul
7.3 9.4 6.4 6.5
1.3 2.6 2.3 8.1
18.4 17.2 17.9 22.9
10.4 7.0 9.2 13.3
12.6 !2.0 8.8 1.7
24.3 22.8 22.8 19.5
12.5 11.2 13.4 10.5
13.3 17.8 19.2 17.5
6.23 7.95 7.06 4.24
3560
Dec-Jan Feb-Mar Apr-May Jun-Jul
7.7 7.5 8.1 9.4
1.6 1.3 0.9 12.9
17.9 16.5 19.3 17.1
8.6 7.4 8.3 8.7
10.3 10.5 9.0 4.2
25.5 27.5 25.9 19.9
13.6 14.0 12.8 12.3
14.8 15.4 15.7 15.6
5.04 6.12 4.74 4.25
(rag 8 -*)
Rha, rharanos¢; Rib, ribo~; Man, mannose; Ara, arabinose; Fuc, fucose; Gal, galactose; Xyl, xylose; GIc, glucose.
In general, the sugar spectra are dominated by glucose, galactose, mannose, xylose with arabinose, fucose, and rhamnose contributing significantly (Table 1). In the amino acid fraction (Table 2) aspartic acid and glycine dominate. The non-protein amino acids 13-alanine and y-aminobutyric acid were detected. Ornithine was virtually absent. There are significant differences in the distribution pattern of sugars and amino acids for the two peak fluxes observed in F e b r u a r y - M a r c h and June-July. In contrast to materials arriving at the trap in February-March, the sugar and amino acid spectra of June-July flux were characterized by enrichment of ribose up to 12%, extremely high arabinose :fucose ratios, and the presence of aspartic acid up to 31%. Such characteristics could be discerned at all depths simultaneously. Sugars, amino acids, and amino sugars accounted for 17 to 42% of the organic carbon (Table 5a); 35 to 85% of the nitrogen was accounted for by amino acids and amino sugars. For the peak flux o f June-July the organic carbon accounted for by these compounds was 42, 40, and 27% at 890, 2590, and 3560 m, respectively. The respective contributions of amino acids and amino sugars to organic nitrogen were 79, 85, and 63%. The amino acid:sugar ratios also varied in the range of 1.3 to 5.28. The lower ratios were characteristic of the June-July flux at all depths. DS samples
The fluxes of sugars, amino acids, and amino sugars showed no significant changes with depth (Table 3). Their contribution to organic carbon and nitrogen (Table 5b) was lowest at 1268 m. Higher values were observed at 3769 and 3791 m. The distribution of individual sugars and amino acids indicates the similarity of materials collected, The arabinose: fucose ratios were 0.66, 0.64, 0.63, 0.60, and 0.86 at 667, 1268, 2869, 3769, and 3791 m, respectively. In the amino acid spectra glycine, aspartic acid, glutamic acid, alanine, and
Month 1980
Feb-Mar Apt-May Jun-J~ Aug-Sep Oct-Nov
Dec-Jan Feb-Mar Apt-May Jun-J~
Dec--Jan Feb--Mar Apt-May Jutl-J~
890
2590
3560
33 16 17 17
17 7 15 7
5 16 7 21 18
Cys
157 163 142 256
159 126 118 237
119 139 301 182 148
Asp
59 52 42 44
46 51 47 41
54 53 43 53 57
Thr
73 75 67 73
69 65 57 49
62 66 50 68 72
Ser
183 146 160 126 189 158 197 167
77 95 86 83
140 135 123 136 141
Gly
94 100 91 76
95 108 82 93 104
Glu
90 96 104 88
91 90 87 139
104 94 78 90 91
Ala
52 58 42 44
50 63 57 52
63 58 50 42 52
26 26 20 36
21 39 35 31
39 22 30 26 20
Val Ile
46 54 44 15
42 64 54 47
66 51 49 51 51
Leu
19 26 25 37
30 49 40 34
45 43 35 35 35
Tyr
27 31 25 23
28 42 32 29
38 28 24 28 30
Phe
10 9 9 6
9 4 -
6 7 10 4 4
6 7 5 1
7 5 6 6
4 3 4 3 3
[3-Ala 7-Aba
1 6
3 -
3
Orn
79 75 116 59
94 85 133 76
105 74 60 87 8
Lys
18 16 21 20
16 21 22 21
14 17 18 15 15
His
39 43 38 29
42 47 44 28
41 84 36 65 77
Arg
15.61 18.96 18.33 7.75
17.57 29.70 19.48 8.43
27.93 33.46 6.97 16.85 29.76
2.57 3.54 3.05 0.97
2.62 2.71 0.66 ~07
2.04 5.94 0.32 2.02 4.49
6.06 5.36 6.01 7.94
6.70 10.92 29.50 122.15
13.67 5.63 21.97 8.35 6.61
AAtotal HA total A A : H A (rag g-') (rag g-')
Cys, cysteic acid; Asp, upartic acid; Thr, threonine; Set, serine; GIy, glycine; Ala, alanine; Val, valine; lie, isoleucine; Leu, leucine; Tyt, tyrosine; Phe, phenylalanine; ~-Ala, j~danine; 7-Aba, 7-aminobutyrlc acid; 0rn, ornithine; Lys, lyz~lne; His, histidine; Arg, arginine; AA, amino acid; HA, hexosamines.
(m)
Depth
Table 2. Distribution of amino acids in residues per 1000 in sample# collected during time-series sediment trap deployments at three depths at a deep-water station in the Panama Basin during 1980
v. I'I'rEKKOTel aL
1076
Table 3.
Fluxes o f sugars, amino acids, and amino sugars measured at d~ferent depths during depth-series
sediment trap deployment (see text) at a station in the Panama Basin Depth (m)
Month 1979
Sugars (rag m -~ d -j)
Amino acids (mg m -2 d -I)
Amino sugars (rag m -2 d -j)
667 1268 2869 3769 3791
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
0.644 0.767 0.936 1.011 0.759
3.217 3.618 3.573 3.423 3.196
0.199 0.244 0.205 0.1 ! 7 0.198
Table 4a.
Distribution o f sugars in samples collected during depth-series trap deployments (see text) at a station in the Panama Basin. Abbreviations as in Table 1
Depth (m)
Month 1979
Rha
Rib
Man
Ara
Fuc
Gal
Xyl
GIc
Total (rag g-l)
667 1268 2869 3769 3791 3911"
Aug-Dec Aug-Dec Aug-Dec Aug-Dee Aug-Dec Aug-Dec
7.2 7.6 8.2 9.8 6.4 8.1
2.6 3.0 2.5 1.3 0.4 1.7
17.2 16.6 17.5 17.5 25.2 17.8
6.3 6.1 7.1 7.4 5.7 11.6
9.4 9,5 11.2 11.6 6.7 10.5
25.5 24.7 24.6 24.1 22.2 21.6
8.5 11.I 9.9 10.0 7.7 13.0
23.4 21.4 18.9 18.4 25.7 15.7
6.70 7.68 6.20 5.82 4.37 4.15
* Surface sediment collected at 3911 m.
lysine dominate (Tables 4a and b). The aspartic acid :glycine ratios, indicative of the relative inputs from carbonate and silica producers (see also Ia'rEKKOTet aL, 1984) were 0.84, 0.76, 0.83, 0.73, and 0.78 at 667, 1268, 2869, 3769, and 3791 m, respectively. Amino acids :hexosamine ratios were also uniform throughout the water column except for a high value at 3769 m. The amino acid:sugar ratios decreased from 4.99 at 667 m to 3.41 at 3769 m (Table 5b). DISCUSSION
Sources of organic matter
Previous studies of the DS samples showed that the total flux increased linearly with depth from 105 mg m-2 d -I at 1268 m to 180 mg m -2 d -I at 3769 m (HON,WOet aL, 1982a). Biogenic materials accounted for about 8096 in the shallower traps (667 and 1268 m) and <60% in the deepest traps (3769 and 3791 m). The measured fluxes of sugars, amino acids, and amino sugars are similar to those measured in TS samples during non-productive times of the years. They are higher than those measured at a deep-water station in the Sargasso Sea (IrrEKKOT et al., 1984), in agreement with investigations by HONDOet al. (1982a), who found lower fluxes of organic matter at two deep-water stations in the Atlantic. Sugar and amino acid spectra are similar to those reported in sediment trap materials collected from other environments (LEE et aL, 1983; IrrEKKOT et aL, 1984). A similar distribution was found to b¢ characteristic of organic matter extracted from phytoplankton, marine particulate matter, and sediments (DEGENS and MopPER, 1976; MOLLER and Su~s, 1977; MAITA et aL, 1982). The material represents mainly constituents of phytoplankton cell
2 4 10 13 7 39
667 1268 2869 3769 3791 3911"
122 118 128 121 133 159
Asp
48 50 55 47 54 55
Thr 54 58 53 64 63 66
Ser
* Surface sediment collected at 3911 m.
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
Cys
Depth Month (m) 1979 110 100 107 100 101 102
Glu 145 156 153 166 172 170
Gly 100 97 89 78 89 84
Ala 75 65 72 68 64 48
Val 40 32 37 36 32 32
Ile 61 53 61 55 51 47
Leu 44 44 44 23 21 5
Tyr 38 36 36 35 34 9
Phe 8 10 2 3 15 21
~-Ala
-
-
4 12 7 I0
9 13
84 102 82 98 91 82
y-Aba Orn Lys
17 17 22 25 17 14
48 46 43 59 44 45
His Arg
33.44 36.22 23.66 19.68 18,51 5.50
AAtotal (mgg-')
2.07 2.45 1.36 0.68 1.15 0.41
16.14 14.78 17.37 29.15 16.07 13.54
HA total A A : H A (mgg-')
Table 4b., Distribution o f amtno acids in samples collected during depth.series sediment trap deployments (see text) at a station i~ the Panama Basin. Abbreviations as in Table 2
1078
V. lYrEKXOTet aL
Table 5a. /lmino acids (,4.4), amino sugars (AS), and sugars (S) as percentage of organic carbon and nitrogen in time-series samples (see text). Amino acid :sugar ratios are also git~on
Depth (m)
Month 1980
AA-C
AS-C
S--C
AA-N
AS-N
AA : S*
890
Feb--Mar Apt-May Jun-Jul Aug-Sep Oct-Nov
14.31 20.27 23.87 22.88 22.50
0.78 2.70 0.86 2.14 2.64
2.42 4.39 17.63 7.46 7.26
34.12 59.16 77.60 76.65 70.47
1.36 5.43 1.96 4.25 5.53
5.28 4.30 1.30 2.89 2.91
2590
Dec-Jan Feb--Mar Apt-May Jun-Jul
14.0 16.37 17.38 27.10
1.63 1.12 4.44 O.17
4.77 3.96 5.75 12.69
47.75 42.79 37.78 84.92
3.83 2.15 1.39 0.36
2.82 3.73 2.75 1.98
3560
Dec-Jan Feb-Mar Apr-May Jun-Jul
12.75 14.51 15.40 16.59
1.68 2.11 2.01 1.66
3.98 4.42 3.77 8.83
50.65 41.85 57.53 58.80
4.54 4.28 5.04 4.16
3.09 3.09 3.86 1.82
I
* Calculated from concentrations given in Tables I and 2.
Table 5b. /lmino acids (A/l), amino sugars (AS), and sugars (S) as percentage of organic carbon and nitrogen in depth-series samples (see text). Amino acid: sugar ratios are also given
Depth (m)
Month 1979
AA--C
AS-C
S--C
AA-N
AS-N
AA : S*
667 i 268 2869 3769 3791 391 I t
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
16.61 8.81 14.76 21.04 20.96 8.45
0.74 0.44 0.63 0.55 1.0 0.92
2.99 1.69 3.52 5.74 4.58 11.44
45.94 35.20 37.50 62.35 55.84 53.28
1.56 1.28 1.18 1.10 1.85 2.08
4.99 4.71 3.81 3.41 4.23 1.32
* Calculated from concentrations given in Tables 4a and b. t Sediment sample.
walls and biomineralized tissues (DEoENS, 1976). However, there are differences in the proportions o f individual sugars and amino acids within the total fractions, which are related to material flux from the surface layers (see also IHeKKOT et al., 1984). The differences are discussed later. The A A : H A ratios, indicator o f relative inputs from phyto- and zooplankton remains, are high in TS samples collected during F e b r u a r y - M a r c h and June-July. The extremely low ratio observed at 890 m during A p r i l - M a y indicates higher inputs from zooplankton or their remains. Zooplankton remains in various stages of preservation are a significant fraction o f the biogenic flux associated with mesopelagic trap samples ( H o m o e t al., 1982a). Some are living swimmers and not part o f the passive vertical flux, but their contribution can only be estimated (KNAuEIt et al., 1979; H o m o , 1980). However, when the trap samples are poisoned with sodium azide, it is almost impossible to distinguish between poisoned swimmers and passive sinkers. Passive sinking remains of zooplankton appeared to contribute significantly to the flux o f materials to the deep-ocean environment o f the Sargasso Sea in 1981
Fluxesof sugars, aminoacids, and aminosugars in the Panama Basin
1079
(ITI'EKKOT et aL, 1984). Although the possibility of active swimmers contributing to the flux of April-May at 890 m cannot be entirely ruled out, we could not observe additional evidence in the form of a large flux, which might be expected from such a contribution (HONJO, 1982).
Peak fluxes of February-March and June-July Preliminary investigations of the TS samples showed two peaks in mass flux in February-March and June-July (HoNJo, 1982). The flux was minimal during DecemberJanuary and very large during June-July at all depths. The mass flux of February-March was associated with a conspicuous peak in primary productivity caused by regional upwelling (see Fig. 1 in HoNJo, 1982). It included biogenic materials characterized by planktonic foraminiferal tests, opaline shells, and fecal pellets. The large flux of June-July occurred simultaneously at all depths, with the largest in the shallowest trap. The flux at a depth of 890 m during the period was 1.7 g m -2 d -I. Carbonate accounted for 93% of the mass flux at 890 m and for 85 and 62% at 2590 and 3560 m, respectively. Nearly all the carbonate at all depths were associated with a single species of coccofithophorid, Umbelltcosphaera sibogae. The fluxes of various biogenic particles other than U. sibogae such as planktonic foraminifera tests in the June-July flux were relatively small. During other times of the year U. sibogae was only a minor constituent of the living coceolithophorids, and of the flux. The two peak fluxes with entirely different biogenic materials provided an opportunity to compare and contrast the nature of organic matter arriving at the different depths at different times of the year, and to relate it to source materials in surface layers. In addition, as the June-July flux was dominated by a single species, it was also possible to follow the nature of transport and transformation within the water column. In the following we discuss the similarities and differences in the fluxes during February-March and June-July. A mixed input, i.e., both calcareous and siliceous, of materials was reflected in the arabinose:fucose and aspartic acid :glycine ratios. However, these ratios were consistently lower than 1 at all depths indicating a dominant input from siliceous materials (Fig. 3b). We observed a similar distribution in samples collected during continuous sediment trap deployments in the deep Sargasso Sea (ITT~KKOTet al., 1984). In contrast, in June-July the fluxes of aspartic acid and arabinose were significantly higher than those of fucose and glycine, indicating a predominant input from calcareous organisms (Fig. 3b). The arabinose:fucose ratios constituted 6.01, 7.98, and 2.07, and those of aspartic acid :glycine 2.44, 1.88, and 1.53 at 890, 2590, and 3560 m, respectively. Because scanning electron microscopic observations have shown the flux to be caused by a single species of coccolithophorid, it is not surprising that we observed a distribution typical of carbonate-secreting organisms. What is striking, however, from a geochemical point of view, is the fact that the distribution pattern is recorded at all depths simultaneously. The above observation is remarkable especially in the light of recent f'mdings by G^RONER et aL (1983), who found that loss of organic matter can take place due to decomposition, cell lysis, or leaching. Decomposition occurs even in poisoned traps (DI~B^AR et aL, 1983; ITrEKKOT et aL, 1984). During June-July, of the 100% of U. slbogae delivered to 890 m, 41 and 21% arrived at 2590 and 3560 m, respectively. Carbonate dissolution within the sediment trap may have partly contributed to the apparent decrease in flux with depth. However, SEM observations indicate no radical dissolution in the deeper traps. Coccofith-coccosphere flux during February-March did not change with depth except for a slight decrease. The percentage of amino acids in organic carbon associated with the April-May flux decreased slightly with depth (Table 5a). A similar decrease was also observed for the percentage of
1080
V. ITTEKKOTeta/.
(a)
ASPARTIACID C (residues11000]
mBOSE
(b)
ARA:FUC
ASP:GLY
5 o ,
O,
,
,
,
,
,
,
,
,
,
,
,
,
31OO 002Q ~Q ~ l l 2590..3 ma,~i ,osI
~
'
-" 0
°
10 ~l~~i!~i:~ ~'~'~:~ ",, :321]~ ~
2590m
~ t
..I
1980
IsloINI
o IolalFIMtAIMI JIJiA]StOINi 1980
1980
o IoIJ[FIMJAIM JIJIAISl I OINI 1980
Fig. 3. (a) Amounts of ribose (mole %) and aspartic acid (residues/1000) in the total sugar and amino acid fractions,respectively,in organic matter associatedwith material flux to three depths in the Panama Basin. For Augustto Octobervaluessee Fig. 2 caption. (b) Ratios of arabinose:fucosc and aspanic acid:glycine.Detailsas for Fig. 3a. sugars in the organic carbon during June-July, probably due to selective decomposition of amino acids and sugars during settling. As the major cause of the mass flux of June--July was the formation of macroaggregates in the surface layers (sec below), it is also conceivable that their disaggregation within the water column during settling is an additional cause for the observed decrease. However, the distribution of sugars and amino acids associated with the large flux and their simultaneous occurrence at all depths suggest that decomposition within the water column or within the sediment traps had not proceeded to such an extent as to alter the effects of the source materials from the sea surface even at 3560 m. Evidence for the rapid transport of materials into the deeper layers comes from the percentage of ribose in the sugar fraction of materials collected during June-July. Its contribution is consistently higher at all depths (Fig. 3a). Although ribose is suggested to be a minor constituent of coccoliths (Ke.oaprrz and WrrT, 1979), no systematic investigations on the polysaccharide composition of coccolithophorids have been carried out so far. Our data indicate that ribose may be a significant constituent of this group of organisms. Another possibility is that ribose is a constituent of organic matter involved in the formation of macroaggrcgatcs. However, we cannot explain why this particular sugar should play a major role in the formation of macroaggregates. Simulation of floc formation and subsequent sedimentation of clay minerals as macroaggregates (KR^NK and MILLIGAN, 1980) has shown
Fluxesof sugars, aminoacids,and aminosugarsin the PanamaBasin
i081
that the presence of specific organic matter accelerates or retards floc formation and, as a consequence, settling of materials. In addition, organic geochemical investigations of macroaggregates collected from estuaries show carbohydrates to be a major constituent (EIsM^ et ai., 1983). The sediment trap materials collected during June-July consisted of macroaggregates including diversified particles and numerous abiogenic clay particles, all cemented together in an organic matrix. The organic matter appears to be associated with U. sibogae and was not observed during other collecting periods. It appears that the material formed before it entered the azide-poisoned traps and may have been produced by the alga itself. Laboratory experiments with coccolithophorid cultures have shown them to be continuously wrapped in mucus materials and the mass sank rapidly to the bottom of the culture vessel during the stationary growth phase. The production of carbohydrates by algae in increasing amounts during stationary growth phase has been shown to occur in laboratory cultures (MYKLESTAD,1974), in enclosures (BROCKMANNet aL, 1977), and in the natural environment (ITTEKKOTel al., 1982). Production of carbohydrates appears to be related to stress induced by the deficiency of nitrogen nutrients. The ratio of amino acids to sugars is lower in materials collected during June--July (Table 5a). Once such material is formed it can act as a scavenger of materials within the water column and, as a consequence, sink rapidly to the deeper layers. Sedimentation of coccoliths by fecal pellets has been shown to be an important mechanism for their transfer to the deep-sea floor (Homo, 1976; ROrHet al., 1975). However, fecal pellets have not been found in sufficient quantities to explain such a mass mechanism for the June-July flux. It appears that mass transfer has occurred on macroaggregates held together by polysaccharides. Palmeloid stages of coccolithophorids have sinking rates of up to 400 m d-X (Homo, 1982). General discussion
This and other investigations on particle flux to the deep ocean indicate rapid transport mechanisms that are biologically controlled (Homo, 1980; DEtJSEgand Ross, 1980; Homo et al., 19g2a,b; DEUSERet aL, 1983). It has been suggested that large aggregates such as fecal pellets (SCH~DER, 1971; l.zsrrzlN, 1972; Homo, 1976), fecal matter (BISHOP et aL, 1977), and 'marine snow' (ALLDXE~E, 1979; SILVESet aL, 1978) play a significant role in the rapid transfer of materials to the sea floor. I-rrEgKor et al. (1984) presented data that appear to provide biochemical evidence for the role of fecal pellets and passively sinking zooplankton remains. The organic geochemical studies carried out on TS samples also indicate rapid transport of materials. The vehicle of transport here appears to be large aggregates rich in organic matter rich in polysaccharides, which is probably released by the alga itself. Such aggregates seem to be instrumental not only in the vertical transport of biogenic particles from the surface layers, but also in translating horizontally carried particles in midwater into a vertical flux (Homo et aL, 1982c). As such aggregates are probably labile, it would not always be possible to observe them directly in the traps due to disintegration. The nature of organic matter arriving at the deeper traps, even within the fine fractions, during times of high productivity, can only be explained by such rapid transport processes. Such processes as the above will entail shorter residence times for particles within the water column and, as a consequence, less decomposition. Temporal fluctuations observed for sugars and amino acid fluxes and for their distribution patterns show organic matter with high nutritive values for benthic communities arriving at the sea floor at productive times of the year. The occurrence of bottom-dwelling communities below zones of high surface productivity (H~ZEN and HOLLlSTER, 1971) and the seasonality in reproductive patterns of deep-sea
1082
v. lTrEggoret al.
benthic organisms (TYLERet al., 1982) probably reflect increased transport of organic matter to the sea floor and its seasonality. Our studies also show that the distribution of sugars and amino acids in materials collected from traps deployed below 3000 m in the deep sea is different from those observed in sediments in both the Atlantic and Pacific oceans. For example, in the Panama Basin, the concentrations of amino acids in the deepest traps is around 18 mg g-i, whereas in sediments it is 5.5 mg g-i. In the Atlantic, there was a significant difference in the proportion of non-protein amino acids in the sediment trap samples and that in sediments (ITTEKKOTet aL, 1984). Such differences were also observed for organic matter content in samples from deep-sea environments (Homo et al., 1982a). It appears that significant biochemical activity takes place in a layer, the "benthic transition layer" of HoNJo et al. (I 982a), between the sediment surface and the deepest traps, which alters the nature of the incoming materials. Because there is a seasonality in the flux of materials, especially in the flux of degradable materials in phase with primary productivity in the surface layers (DEuSER and Ross, 1980; HONJO, 1982), the benthic transition layer of increased biochemical activity should also be expected to be temporal. The difficulty in sampling the layer probably stems from this. A detrital layer with the characteristics of such a zone has been studied during times following the spring bloom in the eastern North Atlantic (BILLETet al., 1983). In conclusion, the patterns of sugars and amino acids in sediment trap samples analyzed so far indicates the nature of the dominant organic input from the surface layers and of the transport and transformation processes. The relative abundances of arabinose and fucose and of aspartic acid and glycine are indicators of the relative inputs from calcareous and siliceous biogenic debris. Ribose appears to be an excellent indicator of rapid transport processes because of its presence at all depths simultaneously in the large flux associated with the coccolithophorid bloom. Acknowledgements--We thank K. W. Doherty and J. F. Connell who were involved in development of the timeseries device for PARFLUX sedimentation trap, G. Schfitze and M. Sternhagen for laboratory a.~'istance, and D. Pieper for secretarial assistance. The r e , arch was supported by the National Science Foundation, Grant OCE 8125429. We are grateful to the two anonymous reviewers for their comments and helpful criticisms of the manuscript. Woods Hole Oceanographic Institution Contribution No. 544 I. REFERENCES A LLDREDGE A. L. (1979) The chemical composition of macroscopic aggregates in two neritic seas, Limnologv and Oceanography, 24, 855-866. BILLET D.S.M., R.S. LAMPITr, A.L. RICE and R.F.C. MANTOURA (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature, London, $02, 520-522. BISHOP J. K. B., J. M. EDMOND, D. R. KeTrE~ M. P. BACON and W. B. SILKER (1977) The chemistry, biology and vertical flux of particulate matter from the upper 400 m of the equatorial Atlantic Ocean. Deep-Sea Research, 24, 5 ! 1-548. BROCKMANN U., K. EBERLEIN,G. HENTZSCHE4H. SCHONF.,D. SIEBERS,K. WANDSCHNEIDERand A. WEBER (1977) Parallel plastic tank experiments with cultures of marine diatoms. Helgol~nder Wissenscha/tliche Meeresuntersuchungen, 30, 201-2 ! 6. DEBAAR H. J., J. W. FARRINOTON and S. G. WAKEHAM(1983) Vertical flux of fatty acids in the North Atlantic Ocean. Journal of Marine Research, 41, 19--4 I. D EGENS E. T. (! 976) Molecular mechanisms on carbonate, phosphate and silica deposition in the living cell. Topics in Current Chemistry, 64, i-112. DEGENS E. T. and K. MOPPER (1976) Factors controlling the distribution and early diagenesis of organic matter in marine sediments. In: Chemical oceanography, Vol. 6, 2nd edition, J. P. RILEY and R. O/ESTER, editors, Academic Press, London, pp. 59--! 13. Dt~US~R W. G. and E. H. Ross (1980) Seasonal change in the flux of organic carbon to the deep Sargasso Sea. Nature, London, 283, 364-365.
Fluxes of sugars, amino acids, and amino sugars in the Panama Basin
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DEUSER W. G., P. G. BREWER,T. D. JICKELLS and R. D. COMMEAU(1983) Biological control of the removal of abiogenic particles from the surface ocean. Science, Wash., 219, 388-391. EISMA D., J. BOON, R. GROENEWEGEN, V. ITTEKKOT, J. KALF and W.G. MOOK (1983) Observations of macroaggrcgates, particle size and organic composition of suspendedmatter in the Ems estuary. Mitleilungen aus dem Geologisch-Palf:ontoiogischen lntituts der Universltflt Hamburg, SCOPF_.JUNEP Sonderband, Pt 2, 54, in press. GARDNER W. D., K. R. HINGA and J. MARRA (1983) Observations on the degradation of biogenic material in the deep ocean with implications on accuracy of sediment trap fluxes. Journal of Marine Research, 41, 195-214. H EEZEN B. C. and C. D. HOLUSTER(i 971 ) Theface of the deep, Oxford University Press, 658 pp. HONJO S. (1976) Coccoliths: production, transportation and sedimentation. Marine Micropaleontology, !, 65-79. HONJO S. (1980) Material fluxes and modes of sedimentation in the mesopelagic and bathypelagic zones. Journal of Marine Research, 38, 53-97. HONJO S. (1982) Seasonality and interaction of biogenic and lithogenic particulate flux at the Panama Basin. Science, Wash., 218, 883-884. HONJO S., J. F. CONNELL and P. L. SACHS(1980) Deep-ocean sediment trap; design and function of PARFLUX Mark [I. Deep-Sea Research, 27, 745-754. HONJO S., S. MANGANIN! and J. COLE (1982a) Sedimentation of biogenic matter in the deep ocean. Deep-Sea Research, 29, 609-625. HONJO S., S. MANGANISI and L. J. POPPE(1982b) Sedimentation of lithogenic particles in the deep ocean. Marine Geology, 50, 199-220. HONJO S., D. SPENCER and J. W. FARRINGTON(1982C) Deep advective transport of litbogenic particles in Panama Basin. Science, Wash., 216, 516-518. ITTEKKOT V., E.T. DEGENS and U. BROCKMANN(1982) Monosaccharide spectra of acid-hydrolyzable carbohydrates in particulate matter during a plankton bloom. Limnology and Oceanography, 27, 71 I-716. ITTEKKOT V., W. G. DEUSER and E. T. DEGENS(1984) Seasonality in the fluxes of sugars, amino acids and amino sugars to the deep ocean: Sargasso Sea. Deep-Sea Research, 31, 1057-1069. KNAUER G. A., J. H. MARTIN and K. W. BRULAND(1979) Fluxes of particulate carbon, nitrogen and phosphorus in the upper water column of the northeast Pacific. Deep-Sea Research, 26, 97-108. KRAMPITZ G. and W. W w r (1979) Biochemical aspects of biomineralization. Topics in Current Chemistry, 78, 57-144. KRANCK K. and T. MiLLIGAN(1980) Macroflocs: production of marine snow in the laboratory. Marine Ecologj, Progress Series, 3, 19-24. LEE C., S.G. WAKEHAM and J. W. FAR~JNGTON (1983) Variations in the composition of particulate organic matter in a time-series sedimeot trap. Marine Chemistry, 13, 181-194. LISITZlN A. P. (1972) Sedimentation in the World Ocean. Special Publications, Society of Economic Paleontologists and Mineralogists, Vol. ! 7, 218 pp. MArrA Y., S. MONTANtand J. ISHII (1982) Early diagenesis of amino acids in Okhotsk Sea sediments. Deep-Sea Research, 29, 485--498. MOLLER P.J. and E. SU~SS (1977) Interaction of organic compounds with calcium carbonate--Ill. Amino acid composition of sorbed layers. Geochimica et Cosmochimica Aeta, 41, 941-949. MYKLESTAD S. (1974) Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture. Journal of Experimental Marine Biology and Ecology, i $, 261-274. ROTH P., M. M. MULUN and W. H. BERGER(1975) Coccolith sedimentation by fecal pellets: laboratory experiments and field observations. Bulletin of the Geological Society of America, 86, 1079-1084. SCHRADER H. J. (1971) Fecal pallets in sedimentation of pelagic diatoms. Science, Wash., 14, 55-57. SILVER M. W,, A. L. SHANKS and J. D. TRENT (1978) Marine snow: microplankton habitat and source of small scale patchiness in pelagic populations. Science, Wash., 201, 37 !-373. TYLER P. A., A. GRANT, S. L. PAIN and J. D. GAGE (1982) IS annual reproduction in deep-sea echinoderms a response to variability in their environment? Nature, London, 300, 747-750. WAKEHAM S. G., J. W. FARRINGTOI~ R. B. GAGOSIAN,C. LEE, H. DEBAAR, G. E. NIGRELLI, B. W. TRIPP, S. O. SMITH and N. M. FREW (1980) Fluxes of organic matter from a rcdimcnt trap experiment in the equatorial Atlantic Ocean. Nature, London, 286, 798-800. WEFER G., EL SUESS, W. BALZER, G. LIEBEZEIT, P.J. MOLLEP,, C. A. UNGERER and W. ZENK (1982) Fluxes of biogenic components from sediment trap deployment in circumpolar waters of the Drake Passage. Nature, London, 299, 145-147.
0198--0149/84$3.00 + 0.00 O 1984 PergamonPress Ltd.
Seasonality in the fluxes of sugars, amino acids, and amino sugars to the deep oeean: Panama Basin VENUOOP^t~N ITTEKKOT,*E~ON T. D~ENS* and SusuMt3 HONJO~ (Received 10 May 1983; in revisedform 24 January 1984; accepted 1 February 1984)
Almtra~---T'nne-seriessediment traps were deployed for an entire year at depths of 890, 2590, and 3560 m at a station in the Panama Basin during 1980. Fluxes of sugars, amino acids, and amino sugars varied seamonallyat each depth. Two peak fluxeswere observed: one in February-March, the other in Juno-July. The peaks were associated with a high productivityperiod by regional upwelling and an unusual coceolithophorid bloom. There were significant differences in the distributions of sugars and amino acids associated with the fluxes. The peak flux of June/July was characterized by high amounts of arabino6e and ribose within the sugar, and high amounts of aspartic acid in the amino acid fractions. The differences were observed at all three depths simultaneously, indicating rapid vertical transport without significant dissolution or decomposition. The observed pattern indicates the utility of specific compounds such as sugars and amino acids as tracers of source materials in the marine environment.
INTRODUCTION
CONSIDERABLE information on the vertical flux of materials to the deep ocean has been obtained from studies with sediment traps (HoN~o, 1980; DEUSER and Ross, 1980; HONDO et al., 1982a) and in situ pumping systems (BIsHoP et aL, 1977). Such studies show that the transport of materials into the deep-ocean environment is rapid and occurs by large particles such as fecal matters fecal pellets, or 'marine snow'. In addition, seasonal fluctuations of material fluxes in phase with primary productivity were also observed (I~USER and Ross, 1980; HONJO, 1982). Better insight into the transport and transformation processes involving the sedimenting material may be gained by characterizing the organic fraction in detail (WAKEHAM et aL, 1980; WEFZZRet al., 1982; LEE et aL, 1983). Such processes control the nature of organic debris arriving at the sea floor and in turn determine the 'utility' of organic matter for benthic communities and the nature and quantity of organic matter ultimately buried in sediments. IT'rEKKOTet al. (1984) reported on the detailed composition of organic matter reaching one deep-sea environment of the Sargasso Sea. It was shown that fluxes of individual classes of compounds such as sugars and amino acids varied in phase with primary productivity. Variations in their distributions appeared to reflect the nature of transport and transformation processes within the overlying water column. We have extended the investigations to include samples collected during sediment trap deployments at various depths in the water column
* Geologisch-Paliontologisches lnstitut and Museum, Universitit Hamburg, Bundesstrass¢ 55, 2000 H a m b u r g 13, Federal Republic o f Germany. t Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A. 1071
1072
V. ITrEKKOT et al.
from yet another deep-sea environment--the Panama Basin. The results are expected to give information on the degradation of organic matter during settling. METHODS
The sediment traps deployed during the experiments were capable of collecting settling particles in six two-month increments totaling a year. The basic configuration of the trap used was the PARFLUX Mark II with a 1.5-m2 opening (Homo et al., 1980). A spring motor drove a rotary sampler and quartz oscillator-based electronics controlled its movement. The timing of the advancing sampler was synchronized among three traps within 10 rain of error over 12 months. Sodium azide tablets were added to the sampler before deployment to stop microbial action during sampling. A mooring array with three such time-series sediment traps was deployed at 890, 2590, and 3560 m below the surface at a station in the Panama Bight (5°22 N, 85°35 W; water depth 3860 m; Fig. I) from 3 December, 1979 to 2 December, 1980. The automated sediment trap worked successfully except for increments at 2590 and 3560m due to mechanical failure. The moored array was recovered on 5 March, 1981. Samples from the experiments will be referred to as time-series samples (TS). For comparison, determinations of sugar and amino acids from samples collected during the PARFLUX experiment at a station in the Panama Basin (5°2 N, 81°53 W) from August 1979 to December 1979 (112 days) with the help of a moored array of sediment traps set at 667, 1268, 2869, 3769, and 3791 m are also presented. For details of the experiment see HONJO et al. (1982a) and HoNJo et aL (1982b). These samples are referred to as depth-series samples (DS). Each trap sample was split into aliquots with an Erez-Honjo splitter (Homo, 1980). Sediments collected in the < 1-mm range were analyzed for sugars, amino acids, and amino sugars. The analytical techniques are described by I~'EKKOT et al. (1984). As only small samples were available the results are based on single analyses. II
I
C
0
$ t Qi:!"
f'~"-..f
a
i:i:!:
/ ~
~:b(}
~iiii~iii::iiiiiiiii-:.iiill
~"
•"
"E.o ....~ ~ I~0o ,,~
C ~ - ~ arn e g i t
R
~i:: o,ill ..::::::::!:!:!: :.,':!:
........ ,,::~i~i~!ii~i!i:~:~:~:ii ::::
===............. =========~=========:i~!!iii ========.... ==================
~
I 80*W
Fig. 1.
Location of the sediment trap experiment.
Fluxes of sugars, amino acids, and amino sugars in the Panama Basin
10 7 3
RESULTS
T S samples Fluxes of organic carbon were in the range of 5.5 to 17.3, 3.6 to 16.6, and 8.3 to 16.6 mg m -2 d -~ at 890, 2590, and 3560 m, respectively. Two peak fluxes were observed at all depths in February-March and June-July. A similar pattern was also observed for nitrogen. The fluxes varied between 0.67 and 1.74 mg m -2 d -I at 890 m, 0.4 and 2.0 mg m -2 d -~ at 2590 m, and between 0.72 and 1.63 mg m -2 d -~ at 3590 m. Lower fluxes of both carbon and nitrogen were observed in December-January and October-November. Except for the February-March flux of sugars, the fluxes of organic matter were similar to the fluxes of carbon and nitrogen (Fig. 2). The maximum fluxes of sugars were 7.6, 3.6, and 3.6 mg m -2 d -= at 890, 2590, and 3560 m, respectively. For amino acids they were 9.9, 7.2, and 6.6 mg m -2 d -~ at 890, 2590, and 3560 m, respectively. The amino sugar flux to the shallowest trap (890 m) was minimal during February-March. Concentrations of sugars, amino acids, and amino sugars in the particulate matter varied between 4.25 and 10, 6.99 and 33.46, and 0.07 and 5.94 mg g-1 respectively (Tables l and 2). Except for the high concentration (10 mg g-l) of sugars during October-November at 890 m, the higher concentrations were observed during February-March. Although there was an overall decrease in concentration with depth the maxima were evident at all depths.
SUGARS
AMINOACIDS
to
:1
~: i 1
"
2590m
356Om
lg80
,ell
IoIalPiultlulJlaltlsiolul
1980
Fig. 2. Fluxes of sugars and amino acids to three depths at a deep-water station in the Panama Basin during 1980. The fluxes at 2590 m during Ausmt to October (dashed lines) were observed during a previous time-scrics experiment at 2265 m described by HONJOe! al. (1982c). See also Methods.
1074
V. ITTEKKOTet aL
Table 1. Distribution of sugars in mole 96 in samples collected during time-series sediment trap deployments at three depths at a deep-water station in the Panama Basin during 1980
Depth
Month
(m)
1980
Rha
Rib
Man
Ara
Fuc
Gal
Xyl
GIc
Total
890
Feb-Mar Apt-May Jun-Jul Aug-Sep Oct-Nov
8.1 7.3 5.5 6.6 5.9
0.5 1.2 11.6 1.8 1.2
17.1 17.1 20.1 19.4 13.8
6.0 7.4 12.2 11.8 11.9
7.7 9.1 2.0 6.8 9.8
23.5 27.8 18.7 24.6 30.2
10.5 12.9 14.6 11.7 12.4
26.6 17.1 15.3 17.2 14.7
5.28 7.78 5.34 5.82 10.22
2590
Dec-Jan Feb-Mar Apt-May Jun-Jul
7.3 9.4 6.4 6.5
1.3 2.6 2.3 8.1
18.4 17.2 17.9 22.9
10.4 7.0 9.2 13.3
12.6 !2.0 8.8 1.7
24.3 22.8 22.8 19.5
12.5 11.2 13.4 10.5
13.3 17.8 19.2 17.5
6.23 7.95 7.06 4.24
3560
Dec-Jan Feb-Mar Apr-May Jun-Jul
7.7 7.5 8.1 9.4
1.6 1.3 0.9 12.9
17.9 16.5 19.3 17.1
8.6 7.4 8.3 8.7
10.3 10.5 9.0 4.2
25.5 27.5 25.9 19.9
13.6 14.0 12.8 12.3
14.8 15.4 15.7 15.6
5.04 6.12 4.74 4.25
(rag 8 -*)
Rha, rharanos¢; Rib, ribo~; Man, mannose; Ara, arabinose; Fuc, fucose; Gal, galactose; Xyl, xylose; GIc, glucose.
In general, the sugar spectra are dominated by glucose, galactose, mannose, xylose with arabinose, fucose, and rhamnose contributing significantly (Table 1). In the amino acid fraction (Table 2) aspartic acid and glycine dominate. The non-protein amino acids 13-alanine and y-aminobutyric acid were detected. Ornithine was virtually absent. There are significant differences in the distribution pattern of sugars and amino acids for the two peak fluxes observed in F e b r u a r y - M a r c h and June-July. In contrast to materials arriving at the trap in February-March, the sugar and amino acid spectra of June-July flux were characterized by enrichment of ribose up to 12%, extremely high arabinose :fucose ratios, and the presence of aspartic acid up to 31%. Such characteristics could be discerned at all depths simultaneously. Sugars, amino acids, and amino sugars accounted for 17 to 42% of the organic carbon (Table 5a); 35 to 85% of the nitrogen was accounted for by amino acids and amino sugars. For the peak flux o f June-July the organic carbon accounted for by these compounds was 42, 40, and 27% at 890, 2590, and 3560 m, respectively. The respective contributions of amino acids and amino sugars to organic nitrogen were 79, 85, and 63%. The amino acid:sugar ratios also varied in the range of 1.3 to 5.28. The lower ratios were characteristic of the June-July flux at all depths. DS samples
The fluxes of sugars, amino acids, and amino sugars showed no significant changes with depth (Table 3). Their contribution to organic carbon and nitrogen (Table 5b) was lowest at 1268 m. Higher values were observed at 3769 and 3791 m. The distribution of individual sugars and amino acids indicates the similarity of materials collected, The arabinose: fucose ratios were 0.66, 0.64, 0.63, 0.60, and 0.86 at 667, 1268, 2869, 3769, and 3791 m, respectively. In the amino acid spectra glycine, aspartic acid, glutamic acid, alanine, and
Month 1980
Feb-Mar Apt-May Jun-J~ Aug-Sep Oct-Nov
Dec-Jan Feb-Mar Apt-May Jun-J~
Dec--Jan Feb--Mar Apt-May Jutl-J~
890
2590
3560
33 16 17 17
17 7 15 7
5 16 7 21 18
Cys
157 163 142 256
159 126 118 237
119 139 301 182 148
Asp
59 52 42 44
46 51 47 41
54 53 43 53 57
Thr
73 75 67 73
69 65 57 49
62 66 50 68 72
Ser
183 146 160 126 189 158 197 167
77 95 86 83
140 135 123 136 141
Gly
94 100 91 76
95 108 82 93 104
Glu
90 96 104 88
91 90 87 139
104 94 78 90 91
Ala
52 58 42 44
50 63 57 52
63 58 50 42 52
26 26 20 36
21 39 35 31
39 22 30 26 20
Val Ile
46 54 44 15
42 64 54 47
66 51 49 51 51
Leu
19 26 25 37
30 49 40 34
45 43 35 35 35
Tyr
27 31 25 23
28 42 32 29
38 28 24 28 30
Phe
10 9 9 6
9 4 -
6 7 10 4 4
6 7 5 1
7 5 6 6
4 3 4 3 3
[3-Ala 7-Aba
1 6
3 -
3
Orn
79 75 116 59
94 85 133 76
105 74 60 87 8
Lys
18 16 21 20
16 21 22 21
14 17 18 15 15
His
39 43 38 29
42 47 44 28
41 84 36 65 77
Arg
15.61 18.96 18.33 7.75
17.57 29.70 19.48 8.43
27.93 33.46 6.97 16.85 29.76
2.57 3.54 3.05 0.97
2.62 2.71 0.66 ~07
2.04 5.94 0.32 2.02 4.49
6.06 5.36 6.01 7.94
6.70 10.92 29.50 122.15
13.67 5.63 21.97 8.35 6.61
AAtotal HA total A A : H A (rag g-') (rag g-')
Cys, cysteic acid; Asp, upartic acid; Thr, threonine; Set, serine; GIy, glycine; Ala, alanine; Val, valine; lie, isoleucine; Leu, leucine; Tyt, tyrosine; Phe, phenylalanine; ~-Ala, j~danine; 7-Aba, 7-aminobutyrlc acid; 0rn, ornithine; Lys, lyz~lne; His, histidine; Arg, arginine; AA, amino acid; HA, hexosamines.
(m)
Depth
Table 2. Distribution of amino acids in residues per 1000 in sample# collected during time-series sediment trap deployments at three depths at a deep-water station in the Panama Basin during 1980
v. I'I'rEKKOTel aL
1076
Table 3.
Fluxes o f sugars, amino acids, and amino sugars measured at d~ferent depths during depth-series
sediment trap deployment (see text) at a station in the Panama Basin Depth (m)
Month 1979
Sugars (rag m -~ d -j)
Amino acids (mg m -2 d -I)
Amino sugars (rag m -2 d -j)
667 1268 2869 3769 3791
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
0.644 0.767 0.936 1.011 0.759
3.217 3.618 3.573 3.423 3.196
0.199 0.244 0.205 0.1 ! 7 0.198
Table 4a.
Distribution o f sugars in samples collected during depth-series trap deployments (see text) at a station in the Panama Basin. Abbreviations as in Table 1
Depth (m)
Month 1979
Rha
Rib
Man
Ara
Fuc
Gal
Xyl
GIc
Total (rag g-l)
667 1268 2869 3769 3791 3911"
Aug-Dec Aug-Dec Aug-Dec Aug-Dee Aug-Dec Aug-Dec
7.2 7.6 8.2 9.8 6.4 8.1
2.6 3.0 2.5 1.3 0.4 1.7
17.2 16.6 17.5 17.5 25.2 17.8
6.3 6.1 7.1 7.4 5.7 11.6
9.4 9,5 11.2 11.6 6.7 10.5
25.5 24.7 24.6 24.1 22.2 21.6
8.5 11.I 9.9 10.0 7.7 13.0
23.4 21.4 18.9 18.4 25.7 15.7
6.70 7.68 6.20 5.82 4.37 4.15
* Surface sediment collected at 3911 m.
lysine dominate (Tables 4a and b). The aspartic acid :glycine ratios, indicative of the relative inputs from carbonate and silica producers (see also Ia'rEKKOTet aL, 1984) were 0.84, 0.76, 0.83, 0.73, and 0.78 at 667, 1268, 2869, 3769, and 3791 m, respectively. Amino acids :hexosamine ratios were also uniform throughout the water column except for a high value at 3769 m. The amino acid:sugar ratios decreased from 4.99 at 667 m to 3.41 at 3769 m (Table 5b). DISCUSSION
Sources of organic matter
Previous studies of the DS samples showed that the total flux increased linearly with depth from 105 mg m-2 d -I at 1268 m to 180 mg m -2 d -I at 3769 m (HON,WOet aL, 1982a). Biogenic materials accounted for about 8096 in the shallower traps (667 and 1268 m) and <60% in the deepest traps (3769 and 3791 m). The measured fluxes of sugars, amino acids, and amino sugars are similar to those measured in TS samples during non-productive times of the years. They are higher than those measured at a deep-water station in the Sargasso Sea (IrrEKKOT et al., 1984), in agreement with investigations by HONDOet al. (1982a), who found lower fluxes of organic matter at two deep-water stations in the Atlantic. Sugar and amino acid spectra are similar to those reported in sediment trap materials collected from other environments (LEE et aL, 1983; IrrEKKOT et aL, 1984). A similar distribution was found to b¢ characteristic of organic matter extracted from phytoplankton, marine particulate matter, and sediments (DEGENS and MopPER, 1976; MOLLER and Su~s, 1977; MAITA et aL, 1982). The material represents mainly constituents of phytoplankton cell
2 4 10 13 7 39
667 1268 2869 3769 3791 3911"
122 118 128 121 133 159
Asp
48 50 55 47 54 55
Thr 54 58 53 64 63 66
Ser
* Surface sediment collected at 3911 m.
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
Cys
Depth Month (m) 1979 110 100 107 100 101 102
Glu 145 156 153 166 172 170
Gly 100 97 89 78 89 84
Ala 75 65 72 68 64 48
Val 40 32 37 36 32 32
Ile 61 53 61 55 51 47
Leu 44 44 44 23 21 5
Tyr 38 36 36 35 34 9
Phe 8 10 2 3 15 21
~-Ala
-
-
4 12 7 I0
9 13
84 102 82 98 91 82
y-Aba Orn Lys
17 17 22 25 17 14
48 46 43 59 44 45
His Arg
33.44 36.22 23.66 19.68 18,51 5.50
AAtotal (mgg-')
2.07 2.45 1.36 0.68 1.15 0.41
16.14 14.78 17.37 29.15 16.07 13.54
HA total A A : H A (mgg-')
Table 4b., Distribution o f amtno acids in samples collected during depth.series sediment trap deployments (see text) at a station i~ the Panama Basin. Abbreviations as in Table 2
1078
V. lYrEKXOTet aL
Table 5a. /lmino acids (,4.4), amino sugars (AS), and sugars (S) as percentage of organic carbon and nitrogen in time-series samples (see text). Amino acid :sugar ratios are also git~on
Depth (m)
Month 1980
AA-C
AS-C
S--C
AA-N
AS-N
AA : S*
890
Feb--Mar Apt-May Jun-Jul Aug-Sep Oct-Nov
14.31 20.27 23.87 22.88 22.50
0.78 2.70 0.86 2.14 2.64
2.42 4.39 17.63 7.46 7.26
34.12 59.16 77.60 76.65 70.47
1.36 5.43 1.96 4.25 5.53
5.28 4.30 1.30 2.89 2.91
2590
Dec-Jan Feb--Mar Apt-May Jun-Jul
14.0 16.37 17.38 27.10
1.63 1.12 4.44 O.17
4.77 3.96 5.75 12.69
47.75 42.79 37.78 84.92
3.83 2.15 1.39 0.36
2.82 3.73 2.75 1.98
3560
Dec-Jan Feb-Mar Apr-May Jun-Jul
12.75 14.51 15.40 16.59
1.68 2.11 2.01 1.66
3.98 4.42 3.77 8.83
50.65 41.85 57.53 58.80
4.54 4.28 5.04 4.16
3.09 3.09 3.86 1.82
I
* Calculated from concentrations given in Tables I and 2.
Table 5b. /lmino acids (A/l), amino sugars (AS), and sugars (S) as percentage of organic carbon and nitrogen in depth-series samples (see text). Amino acid: sugar ratios are also given
Depth (m)
Month 1979
AA--C
AS-C
S--C
AA-N
AS-N
AA : S*
667 i 268 2869 3769 3791 391 I t
Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec Aug-Dec
16.61 8.81 14.76 21.04 20.96 8.45
0.74 0.44 0.63 0.55 1.0 0.92
2.99 1.69 3.52 5.74 4.58 11.44
45.94 35.20 37.50 62.35 55.84 53.28
1.56 1.28 1.18 1.10 1.85 2.08
4.99 4.71 3.81 3.41 4.23 1.32
* Calculated from concentrations given in Tables 4a and b. t Sediment sample.
walls and biomineralized tissues (DEoENS, 1976). However, there are differences in the proportions o f individual sugars and amino acids within the total fractions, which are related to material flux from the surface layers (see also IHeKKOT et al., 1984). The differences are discussed later. The A A : H A ratios, indicator o f relative inputs from phyto- and zooplankton remains, are high in TS samples collected during F e b r u a r y - M a r c h and June-July. The extremely low ratio observed at 890 m during A p r i l - M a y indicates higher inputs from zooplankton or their remains. Zooplankton remains in various stages of preservation are a significant fraction o f the biogenic flux associated with mesopelagic trap samples ( H o m o e t al., 1982a). Some are living swimmers and not part o f the passive vertical flux, but their contribution can only be estimated (KNAuEIt et al., 1979; H o m o , 1980). However, when the trap samples are poisoned with sodium azide, it is almost impossible to distinguish between poisoned swimmers and passive sinkers. Passive sinking remains of zooplankton appeared to contribute significantly to the flux o f materials to the deep-ocean environment o f the Sargasso Sea in 1981
Fluxesof sugars, aminoacids, and aminosugars in the Panama Basin
1079
(ITI'EKKOT et aL, 1984). Although the possibility of active swimmers contributing to the flux of April-May at 890 m cannot be entirely ruled out, we could not observe additional evidence in the form of a large flux, which might be expected from such a contribution (HONJO, 1982).
Peak fluxes of February-March and June-July Preliminary investigations of the TS samples showed two peaks in mass flux in February-March and June-July (HoNJo, 1982). The flux was minimal during DecemberJanuary and very large during June-July at all depths. The mass flux of February-March was associated with a conspicuous peak in primary productivity caused by regional upwelling (see Fig. 1 in HoNJo, 1982). It included biogenic materials characterized by planktonic foraminiferal tests, opaline shells, and fecal pellets. The large flux of June-July occurred simultaneously at all depths, with the largest in the shallowest trap. The flux at a depth of 890 m during the period was 1.7 g m -2 d -I. Carbonate accounted for 93% of the mass flux at 890 m and for 85 and 62% at 2590 and 3560 m, respectively. Nearly all the carbonate at all depths were associated with a single species of coccofithophorid, Umbelltcosphaera sibogae. The fluxes of various biogenic particles other than U. sibogae such as planktonic foraminifera tests in the June-July flux were relatively small. During other times of the year U. sibogae was only a minor constituent of the living coceolithophorids, and of the flux. The two peak fluxes with entirely different biogenic materials provided an opportunity to compare and contrast the nature of organic matter arriving at the different depths at different times of the year, and to relate it to source materials in surface layers. In addition, as the June-July flux was dominated by a single species, it was also possible to follow the nature of transport and transformation within the water column. In the following we discuss the similarities and differences in the fluxes during February-March and June-July. A mixed input, i.e., both calcareous and siliceous, of materials was reflected in the arabinose:fucose and aspartic acid :glycine ratios. However, these ratios were consistently lower than 1 at all depths indicating a dominant input from siliceous materials (Fig. 3b). We observed a similar distribution in samples collected during continuous sediment trap deployments in the deep Sargasso Sea (ITT~KKOTet al., 1984). In contrast, in June-July the fluxes of aspartic acid and arabinose were significantly higher than those of fucose and glycine, indicating a predominant input from calcareous organisms (Fig. 3b). The arabinose:fucose ratios constituted 6.01, 7.98, and 2.07, and those of aspartic acid :glycine 2.44, 1.88, and 1.53 at 890, 2590, and 3560 m, respectively. Because scanning electron microscopic observations have shown the flux to be caused by a single species of coccolithophorid, it is not surprising that we observed a distribution typical of carbonate-secreting organisms. What is striking, however, from a geochemical point of view, is the fact that the distribution pattern is recorded at all depths simultaneously. The above observation is remarkable especially in the light of recent f'mdings by G^RONER et aL (1983), who found that loss of organic matter can take place due to decomposition, cell lysis, or leaching. Decomposition occurs even in poisoned traps (DI~B^AR et aL, 1983; ITrEKKOT et aL, 1984). During June-July, of the 100% of U. slbogae delivered to 890 m, 41 and 21% arrived at 2590 and 3560 m, respectively. Carbonate dissolution within the sediment trap may have partly contributed to the apparent decrease in flux with depth. However, SEM observations indicate no radical dissolution in the deeper traps. Coccofith-coccosphere flux during February-March did not change with depth except for a slight decrease. The percentage of amino acids in organic carbon associated with the April-May flux decreased slightly with depth (Table 5a). A similar decrease was also observed for the percentage of
1080
V. ITTEKKOTeta/.
(a)
ASPARTIACID C (residues11000]
mBOSE
(b)
ARA:FUC
ASP:GLY
5 o ,
O,
,
,
,
,
,
,
,
,
,
,
,
,
31OO 002Q ~Q ~ l l 2590..3 ma,~i ,osI
~
'
-" 0
°
10 ~l~~i!~i:~ ~'~'~:~ ",, :321]~ ~
2590m
~ t
..I
1980
IsloINI
o IolalFIMtAIMI JIJiA]StOINi 1980
1980
o IoIJ[FIMJAIM JIJIAISl I OINI 1980
Fig. 3. (a) Amounts of ribose (mole %) and aspartic acid (residues/1000) in the total sugar and amino acid fractions,respectively,in organic matter associatedwith material flux to three depths in the Panama Basin. For Augustto Octobervaluessee Fig. 2 caption. (b) Ratios of arabinose:fucosc and aspanic acid:glycine.Detailsas for Fig. 3a. sugars in the organic carbon during June-July, probably due to selective decomposition of amino acids and sugars during settling. As the major cause of the mass flux of June--July was the formation of macroaggregates in the surface layers (sec below), it is also conceivable that their disaggregation within the water column during settling is an additional cause for the observed decrease. However, the distribution of sugars and amino acids associated with the large flux and their simultaneous occurrence at all depths suggest that decomposition within the water column or within the sediment traps had not proceeded to such an extent as to alter the effects of the source materials from the sea surface even at 3560 m. Evidence for the rapid transport of materials into the deeper layers comes from the percentage of ribose in the sugar fraction of materials collected during June-July. Its contribution is consistently higher at all depths (Fig. 3a). Although ribose is suggested to be a minor constituent of coccoliths (Ke.oaprrz and WrrT, 1979), no systematic investigations on the polysaccharide composition of coccolithophorids have been carried out so far. Our data indicate that ribose may be a significant constituent of this group of organisms. Another possibility is that ribose is a constituent of organic matter involved in the formation of macroaggrcgatcs. However, we cannot explain why this particular sugar should play a major role in the formation of macroaggregates. Simulation of floc formation and subsequent sedimentation of clay minerals as macroaggregates (KR^NK and MILLIGAN, 1980) has shown
Fluxesof sugars, aminoacids,and aminosugarsin the PanamaBasin
i081
that the presence of specific organic matter accelerates or retards floc formation and, as a consequence, settling of materials. In addition, organic geochemical investigations of macroaggregates collected from estuaries show carbohydrates to be a major constituent (EIsM^ et ai., 1983). The sediment trap materials collected during June-July consisted of macroaggregates including diversified particles and numerous abiogenic clay particles, all cemented together in an organic matrix. The organic matter appears to be associated with U. sibogae and was not observed during other collecting periods. It appears that the material formed before it entered the azide-poisoned traps and may have been produced by the alga itself. Laboratory experiments with coccolithophorid cultures have shown them to be continuously wrapped in mucus materials and the mass sank rapidly to the bottom of the culture vessel during the stationary growth phase. The production of carbohydrates by algae in increasing amounts during stationary growth phase has been shown to occur in laboratory cultures (MYKLESTAD,1974), in enclosures (BROCKMANNet aL, 1977), and in the natural environment (ITTEKKOTel al., 1982). Production of carbohydrates appears to be related to stress induced by the deficiency of nitrogen nutrients. The ratio of amino acids to sugars is lower in materials collected during June--July (Table 5a). Once such material is formed it can act as a scavenger of materials within the water column and, as a consequence, sink rapidly to the deeper layers. Sedimentation of coccoliths by fecal pellets has been shown to be an important mechanism for their transfer to the deep-sea floor (Homo, 1976; ROrHet al., 1975). However, fecal pellets have not been found in sufficient quantities to explain such a mass mechanism for the June-July flux. It appears that mass transfer has occurred on macroaggregates held together by polysaccharides. Palmeloid stages of coccolithophorids have sinking rates of up to 400 m d-X (Homo, 1982). General discussion
This and other investigations on particle flux to the deep ocean indicate rapid transport mechanisms that are biologically controlled (Homo, 1980; DEtJSEgand Ross, 1980; Homo et al., 19g2a,b; DEUSERet aL, 1983). It has been suggested that large aggregates such as fecal pellets (SCH~DER, 1971; l.zsrrzlN, 1972; Homo, 1976), fecal matter (BISHOP et aL, 1977), and 'marine snow' (ALLDXE~E, 1979; SILVESet aL, 1978) play a significant role in the rapid transfer of materials to the sea floor. I-rrEgKor et al. (1984) presented data that appear to provide biochemical evidence for the role of fecal pellets and passively sinking zooplankton remains. The organic geochemical studies carried out on TS samples also indicate rapid transport of materials. The vehicle of transport here appears to be large aggregates rich in organic matter rich in polysaccharides, which is probably released by the alga itself. Such aggregates seem to be instrumental not only in the vertical transport of biogenic particles from the surface layers, but also in translating horizontally carried particles in midwater into a vertical flux (Homo et aL, 1982c). As such aggregates are probably labile, it would not always be possible to observe them directly in the traps due to disintegration. The nature of organic matter arriving at the deeper traps, even within the fine fractions, during times of high productivity, can only be explained by such rapid transport processes. Such processes as the above will entail shorter residence times for particles within the water column and, as a consequence, less decomposition. Temporal fluctuations observed for sugars and amino acid fluxes and for their distribution patterns show organic matter with high nutritive values for benthic communities arriving at the sea floor at productive times of the year. The occurrence of bottom-dwelling communities below zones of high surface productivity (H~ZEN and HOLLlSTER, 1971) and the seasonality in reproductive patterns of deep-sea
1082
v. lTrEggoret al.
benthic organisms (TYLERet al., 1982) probably reflect increased transport of organic matter to the sea floor and its seasonality. Our studies also show that the distribution of sugars and amino acids in materials collected from traps deployed below 3000 m in the deep sea is different from those observed in sediments in both the Atlantic and Pacific oceans. For example, in the Panama Basin, the concentrations of amino acids in the deepest traps is around 18 mg g-i, whereas in sediments it is 5.5 mg g-i. In the Atlantic, there was a significant difference in the proportion of non-protein amino acids in the sediment trap samples and that in sediments (ITTEKKOTet aL, 1984). Such differences were also observed for organic matter content in samples from deep-sea environments (Homo et al., 1982a). It appears that significant biochemical activity takes place in a layer, the "benthic transition layer" of HoNJo et al. (I 982a), between the sediment surface and the deepest traps, which alters the nature of the incoming materials. Because there is a seasonality in the flux of materials, especially in the flux of degradable materials in phase with primary productivity in the surface layers (DEuSER and Ross, 1980; HONJO, 1982), the benthic transition layer of increased biochemical activity should also be expected to be temporal. The difficulty in sampling the layer probably stems from this. A detrital layer with the characteristics of such a zone has been studied during times following the spring bloom in the eastern North Atlantic (BILLETet al., 1983). In conclusion, the patterns of sugars and amino acids in sediment trap samples analyzed so far indicates the nature of the dominant organic input from the surface layers and of the transport and transformation processes. The relative abundances of arabinose and fucose and of aspartic acid and glycine are indicators of the relative inputs from calcareous and siliceous biogenic debris. Ribose appears to be an excellent indicator of rapid transport processes because of its presence at all depths simultaneously in the large flux associated with the coccolithophorid bloom. Acknowledgements--We thank K. W. Doherty and J. F. Connell who were involved in development of the timeseries device for PARFLUX sedimentation trap, G. Schfitze and M. Sternhagen for laboratory a.~'istance, and D. Pieper for secretarial assistance. The r e , arch was supported by the National Science Foundation, Grant OCE 8125429. We are grateful to the two anonymous reviewers for their comments and helpful criticisms of the manuscript. Woods Hole Oceanographic Institution Contribution No. 544 I. REFERENCES A LLDREDGE A. L. (1979) The chemical composition of macroscopic aggregates in two neritic seas, Limnologv and Oceanography, 24, 855-866. BILLET D.S.M., R.S. LAMPITr, A.L. RICE and R.F.C. MANTOURA (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature, London, $02, 520-522. BISHOP J. K. B., J. M. EDMOND, D. R. KeTrE~ M. P. BACON and W. B. SILKER (1977) The chemistry, biology and vertical flux of particulate matter from the upper 400 m of the equatorial Atlantic Ocean. Deep-Sea Research, 24, 5 ! 1-548. BROCKMANN U., K. EBERLEIN,G. HENTZSCHE4H. SCHONF.,D. SIEBERS,K. WANDSCHNEIDERand A. WEBER (1977) Parallel plastic tank experiments with cultures of marine diatoms. Helgol~nder Wissenscha/tliche Meeresuntersuchungen, 30, 201-2 ! 6. DEBAAR H. J., J. W. FARRINOTON and S. G. WAKEHAM(1983) Vertical flux of fatty acids in the North Atlantic Ocean. Journal of Marine Research, 41, 19--4 I. D EGENS E. T. (! 976) Molecular mechanisms on carbonate, phosphate and silica deposition in the living cell. Topics in Current Chemistry, 64, i-112. DEGENS E. T. and K. MOPPER (1976) Factors controlling the distribution and early diagenesis of organic matter in marine sediments. In: Chemical oceanography, Vol. 6, 2nd edition, J. P. RILEY and R. O/ESTER, editors, Academic Press, London, pp. 59--! 13. Dt~US~R W. G. and E. H. Ross (1980) Seasonal change in the flux of organic carbon to the deep Sargasso Sea. Nature, London, 283, 364-365.
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