The lateral flux of biogenic particles from the eastern North American continental margin to the North Atlantic Ocean

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Deep-SeaResearchII, Vol, 41. No. 2/3. pp. 583 601, 1994

Pergamon

Copyright© 1994ElsevierScienceLtd Printed in Great Britain, All rightsreserved I)967~1645/94$7(10+0.00

The lateral flux o f biogenic particles f r o m the eastern North A m e r i c a n continental margin to the N o r t h Atlantic O c e a n

P. G. FALKOWSKI,* P. E. BISCAYE+and C. SANCETTA-~ (Received 10 April 1992; in revised form 18 September 1992; accepted 15 September 1993) A b s t r a c t - - S e d i m e n t trap samples from two field programs on the continental margin of the northeast coast of the United States, which constituted the Shelf Edge Exchange Program (SEEP), were analyzed for phytoplankton taxonomic composition and the fluxes of organic carbon, nitrogen and opaline silica. The traps, with a rotating carousel collection system, were located on taut-wire moorings between 150 and 2700 m below the surface and extended from the 500 m isobath on the upper continental shelf to the 2750 m isobath at the edge of the abyssal plain of the western North Atlantic Ocean. The temporal and spatial distributions of phytoplankton in the azidepoisoned trap samples revealed a general increase of intact cells with depth, which is consistent with lateral transport from the margins to the ocean interior. Taxonomic analysis of the phytoplankton indicated that > 9 0 % of the intact cells (containing identifiable intracellular structures) consisted of diatoms. The distribution of the species further supports the lateral transport origin of the particles, and indicates that the particulate materials are delivered to the ocean interior primarily in pulses of rapidly sinking aggregates. However, quantitative analysis suggests that intact phytoplankton contribute only 0.8 _+ 0.7% (mean and S.D.) and 0.9 _+ 0.7% of the total particulate carbon and nitrogen fluxes, respectively. Using silica-to-carbon ratios to budget the remaining trap organic carbon fluxes, it would appear that between 17 and 100% of the sedimenting particles were originally diatomaceous, but that the organic carbon became solubilized and/or oxidized in the water column during descent. A simple two-dimensional model was dcveloped to quantify the contribution of the flux of particulate organic carbon to the interior of the North Atlantic Ocean. The results suggest that north of Cape Hatteras, the mean lateral flux of particulate organic carbon sinking through the upper 500 m of the water column into the western edge of the basin is 4.8 x 1012 g C y- 1 which is about 6% of the primary production on the shelf. This flux represents the lateral export of carbon from the continental margin to the interior of the North Atlantic Ocean. Based on estimates of vertical export production for the basin of about 4.2 X 10 TM g C y 1, we estimate that the export of carbon from the western margin, north of Cape Hatteras, represents about 1% of the new production of the entire basin. This export is a significant source of energy which fuels the high benthic respiration on the continental slope.

INTRODUCTION

IN the central ocean basins, the rain of particulate organic matter (POM) from the surface is the primary fuel for biological activity in the ocean interior. In most regions of the central ocean, both the standing stock and productivity of phytoplankton are low, limited by the flux of fixed, inorganic nitrogen to the euphotic zone (DUCDALE and GOERINC, 1967; *Oceanographic and Atmospheric Sciences Division, Brookhaven National Laboratory, Upton, NY 11973, U.S.A. t L a m o n t - D o h e r t y Earth Observatory of Columbia University, Palisades, NY 10964, U.S.A. 583

584

P.G. FALKOWSKIet al.

EPPLEY and PETERSON,1979). In order to maintain a steady-state on some finite time and space scale, it is often assumed that the downward flux of particulate organic nitrogen (PON) is balanced by an upward flux of nitrate and, to a lesser extent, the fixation of atmospheric N 2 (EPPLEYand PETERSON,1979). The remineralization of sinking particulate organic matter in the open ocean results in a distribution of particles and particulate fluxes that tend to decrease exponentially from the surface (BETZER et al., 1984; HARRISON, 1992). At the ocean margins, in contrast, physical forcing and cultural eutrophication allow for an increased supply of essential plant nutrients. Consequently, the standing stock of phytoplankton on continental margins is, on average, about an order of magnitude higher than in the central ocean basins (WALSH, 1988). The horizontal gradient in particulate organic materials potentially increases the flux of POM from the margins to the ocean basins. The magnitude and importance of this lateral flux are poorly understood. Here we analyze the spatial distribution of fluxes intercepted by sediment traps deployed across the continental margin of the Mid-Atlantic Bight, and estimate the contribution of the lateral flux of POM from the northeastern margin of North America to the carbon, nitrogen and silicon economies of the North Atlantic Ocean. The sediment trap samples were obtained from two field programs as part of the Shelf Edge Exchange Process (SEEP) studies. The first SEEP deployments took place south of Cape Cod, Massachusetts, between September 1983 and September 1984. The second SEEP deployments were off the coast of Delaware and Maryland (the Delmarva Peninsula) between February 1988 and June 1989 (Fig. 1). The flux of phytoplankton between shelf and slope waters in the SEEP-I area was described by FALKOWSKIet al. (1988). The vertical and lateral total mass fluxes, and fluxes of 21°pb and particulate biogenic constituents to the continental slope and rise and the accumulation of these materials in the sediments were described by BISCAYEet al. (1988) and ANDERSON et al. (1988), respectively. The vertical and lateral total mass and constituent fluxes to the continental slope in the SEEP-II area are analysed by BISCAYEand ANDERSON(1994), and the budget of organic carbon by ANDERSONet al. (1994). Here we describe and analyze the spatial and temporal distributions of the intact phytoplankton species in relation to the total flux of POC, PON and opaline silica. Our goals are: (1) to examine the spatial and temporal distributions of the sedimenting phytoplankton taxa to qualitatively determine the relative importance of lateral and vertical fluxes at the continental margins; (2) to quantify the contribution of phytoplankton to the fluxes of POC, PON and opaline silica; and (3) to estimate the relative importance of the cross-shelf flux of particulate organic material, north of Cape Hatteras, to the carbon, nitrogen and silicon economies of the basin interior, MATERIALS AND METHODS Trap design, d e p l o y m e n t and sample treatment

In the first SEEP deployment, samples were taken in a two-dimensional array of 17 sediment traps as described in BISCAVEet al. (1988). In SEEP-II, 17 traps were deployed in two parallel transects across the shelf-slope front (BlsCAYE and ANDERSON, 1994). All of the phytoplankton species distribution and opal data reported here come from the SEEP-I array. The sediment traps were cylindrical PVC tubes with a 3:1 aspect ratio. An internal,

Lateral particle flux

585

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offset funnel fed collected material successively into 10 sample tubes on a carousel which was rotated every 17.5 days. The sample tubes were deployed filled with filtered seawater whose salinity had been raised to 42%0 with NaC1, and which were poisoned with 10% sodium azide. For phytoplankton analyses, a 5-10 ml aliquot from each sample tube was removed immediately after recovery aboard ship, and further fixed with buffered formalin and kept refrigerated. The remaining principal sample was analyzed for total mass flux, POC and PON as described by BISCAYEet al. (1988).

Phytoplankton analyses Phytoplankton species and abundances were analyzed for each trap sample for the SEEP-I deployment. One ml of preserved subsamples from each trap sample was examined in a Sedgewick-Rafter counting chamber at 200 × magnification with a compound microscope equipped with Hoffman differential contrast optics. Unless specified, only cells with visible intracellular contents were included in the counts; many empty

586

p.G. FALKOWSKIet al.

frustules were present. Cell densities were on the order of 103 m1-1 and, when possible, cells were identified to the species level. Because of mechanical difficulties with the traps during the first (winter) deployment of SEEP-I, a number of traps had incomplete recoveries of the total of 10 samples, whereas the second (summer) deployment was almost totally complete. Consequently, a complete (annual) analysis of phytoplankton from all the moorings was not obtained, and most results presented here are for the summer deployment.

POC and PON analyses POC and PON measurements were made for both SEEP-I and SEEP-II sediment trap samples. POC and PON were analyzed on the principal sample from each trap after removing "swimmers". The problem of swimmers is discussed in BISCAVEet al. (1988); these are zooplankton that, rather than sinking passively into the trap, actively swim in and are killed by the poison in the sample cup. Their contribution to the sample must be subtracted, and can only be done by some physical method prior to sample analysis, which, in SEEP-I, was by sieving at 1 ram. We have since been convinced that this method is not as effective as removing the swimmers manually. Hence, for SEEP-II samples, the swimmers were manually picked out individually from each sample. Thus we note that there may be some indeterminate contribution of swimmer carbon and nitrogen to the numbers to which we compare the carbon and nitrogen coming from the two SEEP-I deployments. This contribution would tend to lead to an overestimate of POC fluxes.

Opal analysis Biogenic opal was analyzed using a colorometric method modified from that of MORTLOCKand FROEHCH(1989), which was developed for analysis of sediment samples, and consists of a single extraction of opal by 2 M Na2CO3. Since the amount of sediment trap material available for analysis is much smaller than is generally available from sediment samples (in our case, 2-3 mg vs the 25-200 suggested by MORTLOCKand FROELICH, 1989), we used a long pathlength cuvette (5 cm) to enhance sensitivity. We assumed a molecular weight of 70 for opal, corresponding to a water content of 14%. RESULTS AND DISCUSSION

Phytoplankton composition in the sediment traps The intact phytoplankton cells preserved in the SEEP-I trap samples consisted almost totally of diatoms. Of the 202 trap samples counted, diatoms accounted for 90% or more of the total phytoplankton in 168 samples. The only dinoflagellate of significance was Exuviella apora, which, when observed, accounted for 9-13% of the total cells. The taxonomic distribution in the traps differed markedly from that found in the water column, where dinoflagellates, such as Gymnodisium pygmaeum and G. simplex, as well as small flagellates, were extremely important. The diversity of diatoms was high; 65 species were observed (Table 1). While some species were observed in many samples, the seven most numerically abundant species consisted of Actinocyclus octonarius, Coscinodiscus excentricus, Nitzchia pungens, Thalassionema nitzschioides, T. punctigera, Rhizosolenia alata

587

Lateral particle flux

Table 1.

List of phytoplankton species found in sediment traps, calculated cell volumes and estimated cell organic carbon content

Species n a m e

A ctinocyclus curvatulus A ctinocyclus octonarius Asterionella glacialis Asterolampra rnarylandica Bacteriastrum biconicum Campylosira cymbelliformis Cerataulina bergoni Ceratium terez Chaetoceros sp. Corethron cryophilum Coscinodiscus centralis Coscinodiscus eccentrica Coscinodiscus oculus iridis Coscinodiscus radiatus Coscinodiscus sp. Coscinodiscus wailesii Cylindrotheca closterium Dactyliosolen antarcticus Detonula pumila Dinophysis acuta Dinophysis ovum Dinophysis sp. Distephanus speculum Ditylum brightwellii Exuviella apora Exuviella compressa Grammatophora angulosa Grammatophora marina Guinardia ftaccida Hemiaulus sinensis Lauderia borealis Lauderia sp. Licomorpha abreviata Navicula distans Navicula sp. Nitzschia bilobata Nitzschia delicatissima Nitzschia paradoxa Nitzschia pungens v. Atlantica Nitzschia seriata Nitzschia sp. Odontella sp. Paralia sulcata Peridinium granii Peridinium rhomboides Phalacroma sp. Phalarchrompulchellum Plagiogramma vanhuerckii Planktoniella sol

Occurrence 1 188 2 l 2 3 1 l 33 13 9 142 5 75 43 34 5 1 139 2 1 1 54 89 12 2 1 1 9 1 9 6 1 57 2 1 6 93 137 4 1 1 3 1 1 1 1 9 1

Volume Carbon cell- J (/~m 3) (pg) 5284 1413 800 15079 2000 2040 17200 10000 10000 20000 32000 7051 28627 3180 5000 16185 12566 18000 3072 29734 29734 30000 942 295524 268 24429 1800 962 7200 8180 9690 4000 4712 15925 2000 10000 240 1020 630 2125 1000 20000 11453 25000 25000 5000 43563 243 45238

251 92 60 556 120 122 615 407 407 689 984 313 904 171 241 587 484 636 167 931 931 937 68 5305 26 802 111 69 318 350 398 203 230 580 120 407 24 72 50 126 71 689 452 816 816 241 1243 24 1279

Continued

P . G . FALKOWSKIet al.

588

Table 1.

Continued

Volume Carbon cell- l Species name Pleurosigma elongatum Pleurosigma normanii Proboscia alata f. Alata Proboscia alata f. Indica Rhizosolenia alata v. Gracillima Rhizosolenia delicatula Rhizosolenia fragilissima Rhizosolenia hebetata Rhizosolenia hebetata f. subspina Rhizosolenia setigera Rhizosolenia stolterfothii Rhizosolenia styliformis Skeletonema costatum Stephanopyxis palmeriana Stephanopyxis sp. Thalassiosira aestivalis Thalassiosira leptopa Thalassionema nitzschioides Thalassiosira nordenskoldii Thalassiosirapunctigera Thalassiothrix delicatula Thalassiothrix frauenfeldii Thalassiothrix longissima Thalassiothrix sp.

Occurrence 1 25 34 23 28

~ m 3)

(pg)

30375 6600 28800 10500 8000

946 297 908 423 344

8

864

64

1 48 73 1 10 19 6 2 4 4 37 145 5 114 12 12 2 1

5500 2400 i0000 4500 12400 96000 360 2620 2620 14431 3180 360 14137 18278 3072 1200 40500 5000

259 138 407 222 480 2262 33 148 148 538 171 33 530 643 167 82 1176 241

and R. hebetata. The distribution of these species is shown in Fig. 2(a) and (b) where the time-series and the spatial relationships of the sediment trap array are represented in both linear and logarithmic representations of cell numbers. Inspection of the temporal distribution of cells reveals that intact phytoplankton arrived at the traps in pulses, or events [Fig. 2(a)]. Simultaneous analysis of moored fluorometer records and currents at the shelf-slope break indicates that the high flux events are due to both local meteorological forcings and remote oceanic forcings (HouGHTON et al., 1988; WIRICK, 1994). The range between the maximum and minimum fluxes for this record is over a factor of 10 between traps. The spatial distributions of the five most abundant intact diatoms found in the traps reveal that the overall abundance of all intact cells was substantially lower in the upper traps compared with the deep traps at all the moorings (Fig. 2). This distribution is inconsistent with a simple vertical source of the cells from the upper ocean, but may be consistent with a lateral input. To investigate this possibility we examined the species composition of the intact cells. A major pulse of intact cells was caught in the traps during the two consecutive sampling periods between Julian days 166 and 201 [14 June and 19 July 1984; Fig. 2(a)]. This pulse was recorded most strongly in near-bottom traps. The pulse was dominated by R. hebetata and Psammodiscus nitidus where up to 2000 cells ml-1 of those two species were observed at mooring 7 in the 2710 m traps, located 50 m above the bottom (mab) in June. Massive

589

Lateral particle flux

Mooring4

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Mooring5

470 m q]

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Mooting 7

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113 153 193 233 273 Julian Day

Fig. 2. Time series of most abundant intact phytoplankton species in the approximate spatial arrangcmcnt of the scdimcnt trap array from SEEP-I. In (a) species arc represented in a lincar scale and the total number of cells is additivc on the abscissa. In (b) each species was transformed to a logarithmic representation for case of inspection. Hence, cell numbers are not additive, and the scale is relative.

590

P.G. FALKOWSK1et al.

Mooring 4

Mooring 5

Mooring6

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113 153 t93 233 273 Julian Day Fig. 2. C o n t i n u e d

Lateral particle flux

591

fluxes of rhizosolenoid diatoms appear to be common in many continental shelf areas (SANCE~A et al., 1991). There is no apparent lag in the major pulse event between depths at moorings 5, 6 and 7, which may be due to the relatively coarse sampling resolution of 17.5 days. The lack of a temporal lag between traps located at 486 and 2710 m depth implies that cells could have sunk 2220 m within 17.5 days, or nominally - 1 2 5 m day - l . While such sinking rates are high, they are not unprecedented for large diatoms (SMAVDA, 1970; SMEXACEK,1978). Based on the Stokes settling velocity equation, the particles would require a mean radius of ca 300 k~m, which is consistent with the observed aggregates of cells found in the trap samples. Closer inspection of the phytoplankton species composition in the trap samples is facilitated in Fig. 2(b), in which the species distributions are presented on a logarithmic scale. The taxonomic distributions reveal that R. hebetata was found in all deep trap samples, but was not found in any traps in the upper 850 m at mooring 7, or in the upper 150 m at moorings 4 and 5. Furthermore, the rank order abundance of species found at 2710 m at mooring 7 closely follows that found below the 450 m depth horizon at moorings 4, 5 and 6, but differs markedly from the species composition found in traps in the upper 500 m at mooring 7. For example, at mooring 7, T. nitzschioides, is the second or third most abundant species found below 500 m, yet is not among the eleven most abundant species in the samples caught in the upper 150 m. Additionally, Skeletonema costatum and Rhizosolinea alata are found in the upper 150 m trap samples, but not at depth. The spatial distribution of particular species, especially R. hebetata, C. excentricus and N. pungens, strongly suggests a lateral, downslope migration of intact phytoplankton from mooring 4 to mooring 7. This is consistent with the downslope and seaward transport of most of the biogenic constituents found in these traps as suggested by BISCAYEet al. (1988). The shelf origin of the biogenic particles is further supported by the occurrence in the deep traps, at all moorings, of diatom taxa characteristic of the inner continental shelf; these include Cocconeis spp., Rhaphoneis spp., Delphineis spp. and Paralia sulcata (data not shown). The three former, and probably the latter as well, are benthic taxa; they occur attached to a substrate, which in the case of Rhaponeis and Delphineis is usually a sand grain (HENDEY,1964; ROUND etal., 1990). As photosynthetic organisms, their depth range is limited by the availability of light, and they are typically found in littoral waters. In the case of P. sutcata, living chains have been reported in the coastal plankton as well, probably as a result of the suspension from strong vertical mixing. In the trap material these taxa almost always were present as individual valves; i.e. the cells are not intact. Even when the frustules are intact (as frequently in the case of P. sutcata, which is a very robust species), intracellular material was not observed. If composition of the diatom assemblage is recalculated using all specimens found, these four taxa alone account for 1015% of the total population of phytoplankton in the trap samples. This represents a minimum value for displaced specimens; single valves of many other taxa are also common, but it is not possible to distinguish those which were very recently disaggregated from vertically settling material, and those which have been resuspended. On the basis of this taxonomic distribution of phytoplankton in the sediment traps, we conclude that at least 15% of the particles found in the deep traps were resuspended from the sediments and transported laterally down the continental slope. This does not include the abundant silt-sized lithic particles, which also could represent redeposited material. We now examine the relative contribution of the phytoplankton flux to the organic carbon, nitrogen, and silica economy of the ocean margins.

592

P.G. FALKOWSKIet

al.

Phytoplankton Corg, N and opaline silica fluxes Most of the material examined from the trap samples was amorphous, unidentifiable aggregates, with few intact cells. The contribution of intact phytoplankton to the total flux of Corg and N was calculated from knowledge of the abundance of individual species, measurements of cell dimensions, calculations of cell volumes, and the use of STRATHMANN'S(1967) equation relating cell volume to carbon in diatoms (Table 1). We assumed a constant Corg/N ratio of 6/1 by weight, which is based on an average of measured Corg/N ratios for nutrient-replete diatoms in culture (STRICKLAND,1960). The average daily flux of phytoplankton carbon varied by three orders of magnitude, from 4.17 x 10 l m g C m 2 day 1 at mooring 7 at 2710 m between 14 June and 2 July, to 2.82 x 10 -4 mg C m 2 dayat mooring 4 at 150 m in the interval between 27 September and 16 October (Fig. 3). Timeweighted average fluxes for phytoplankton carbon were calculated for depth intervals for the entire summer deployment interval of 175 days (Table 2). These results indicate a general trend of increased flux of phytoplankton carbon with increased depth in the water column. The highest fluxes were found for traps >2000 m deep on the continental rise (moorings 6 and 7). We compared the phytoplankton carbon flux to the measured total particulate organic carbon flux for each of the moorings (Table 2). The results of that analysis reveal that phytoplankton carbon in intact cells accounted for between 0.1 and 2.1% of the total organic carbon flux, averaging 0.8 + 0.7% (mean + S.D.). Similarly, phytoplankton N flux accounted for between 0.2 and 2.2% of the total organic nitrogen flux, averaging 0.9 _+ 0.7%. Clearly, the carbon and nitrogen carried by intact phytoplankton cells was a relatively minor contribution of the total biogenic material flux to the slope. The time-weighted mean flux of opaline silica for the winter and summer SEEP-I deployments, and for the time-weighted average of both deployments (Fig. 4) are qualitatively similar to that of POC (BISCAYE e t al., 1988). That is, there is a general increase in opal flux, POC and cell abundance with depth at a given mooring, and in the mid-water column there is a decrease in all three variables with distance from the shelf. Opal fluxes primarily represent the sedimentation of diatoms (radiolarians were relatively insignificant in these samples). Winter fluxes of opal in the upper 150 m averaged ca 50 mg m -2 day ~, while summer fluxes averaged ca 15 mg m -2 day ~. The seasonal differences in these fluxes are consistent with the changes in phytoplankton community structure, in which diatoms dominate on the shelf in the winter and flagellates are more abundant in the summer (FALKOWSKIe t al., 1983, 1988). These seasonal differences also are seen in the average winter and summer ratios of CorgtO opal [Fig. 5(a) and (b)] in which the relative decrease in opal from the slope seaward is much more apparent in winter than in summer. Opal increases relative to Corg with depth at each mooring, but the high shelf-derived content of opal in winter reduces the vertical gradient in the water column adjacent to the upper slope. The total opaline silica flux is plotted for each trap as a function of time in Fig. 5. These results reveal that the major opaline silica flux "events" are associated with an early December storm (as seen in the other flux constituents reported in BISCAYEet al., 1988), and with the spring bloom in April and May. The intensity of these events decreases offshore and throughout the water column. The June-July intact phytoplankton pulse event seen in near bottom traps (Fig. 2) is not evident at any depth (Fig. 5). This apparent decoupling between the flux of intact diatoms and opaline silica is due to the flux of empty

593

Lateral particle flux

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Mooting 5

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113

Fig. 3.

t53 193 233 273 Julian Day

Time series of the calculated flux of organic carbon in intact p h y t o p l a n k t o n for the sediment traps in SEEP-I.

diatom frustules and suggests that much of the spring diatom bloom is oxidized and/or solubilized in the upper portion of the water column; i.e. the vast majority ( > 9 9 % ) of the diatoms do not reach the traps as intact cells. The average ratio of Corg/Si in living diatoms is 7.7 by atoms (BRzEZINSKI, 1985), which corresponds to a ratio of 1.3 by mass (assuming a molecular weight of 70 g mole -I for

150-170 450-490

150-170 450-490 860-870 1200-1800

150-170 450-490 860-870 1200-1800 >2200

150-170 450-490 860-870 1200-1800 >2200

Mooring 4

Mooring 5

Mooring 6

Mooring 7

Depth (m)

0.033 0.013 0.050 0.044 0.105 0.072

0.020 0.021 0.092 0.102 0.105

0.054 0.074 0.073 0.081

0.036 0.065

12.97 4.69 7.05 2.66 6.26 5.35

16.69 12.36 15.93 10.16 7.27

25.19 29.03 16.91 16.96

13.18 46.74

Total Phytoplankton organic carbon flux carbon flux (mg C m -2 day-l) (rag C m -2 day-l)

0.24 0.23 0.81 1.92 2.08 1.60

0.09 0.18 0.55 1.05 1.48

0.14 0.29 0.45 0.58

0.23 0.15

Percentage phytoplankton carbon

1.24 0.58 0.92 0.43 0.94 0.80

1.65 1.54 2.28 1.49 1.12

3.01 3.79 2.25 2.41

1.73 6.42

Total organic nitrogen flux (Mg N m -2 day -1)

0.39 0.31 1.01 1.80 2.24 1.81

0.15 0.22 0.64 1.18 1.59

0.19 0.39 0.56 0.68

0.30 0.18

Percentage phytoplankton nitrogen

10.47 8.13 7.59 6.20 6.70 6.73

10.09 8.04 6.98 6.80 6.52

8.38 7.67 7.52 7.03

7.64 7.21

Average total C/N flux ratios (w/w)

Table 2. The time- weighted mean fluxes for the SEEP-I sediment trap deployment off the east coast of the United States in 1984. Total organic carbon and nitrogen fluxes were measured. Phytoplankton carbon and nitrogen fluxes were calculated for intact cells using the estimated carbon content for each species as given in Table 1 and assuming a C/N ratio of 6~1 by weight. The duplicate data for traps >2200 m at mooring 7 are for duplicate sediment traps on the same mooring

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Fig. 5. The series of opal fluxes for each of the moorings in the SEEP-I deployment. Note thc increase in opal fluxes in the near bottom traps. opal). Using this mass ratio, and assuming that the opal flux is due solely to diatoms, we calculated the ratio of Corg/Si for each trap (Fig. 6). The results of this calculation suggest that in the upper 150 m, 100% of the total Corg flux could be attributed to diatom carbon at moorings 6 and 7, but closer to the shelf and deeper in the water column there appeared to be a deficit of Corg relative to opaline silica. We suggest that the decrease in Corg relative to opaline silica closer to the shelf and with depth is a consequence of a relatively rapid rate of solubilization and remineralization of POC compared with opal. We note that the increase in opal relative to Corg with depth in the time-weighted mean fluxes, corresponds with an increase in the absolute flux of opal with depth [Fig. 4(c)]. These results suggest that (a) on the time scales of these measurements (about 6 months) opal is a relatively conservative tracer of biogenic particles, and (b) most of the biogenically derived particulate organic carbon is solubilized or oxidized before it reaches the sea floor. The solubilization and oxidation of Corg appear to be extremely rapid on the upper continental rise. Let us assume that all of the phytoplankton carbon intercepted by the sediment trap at mooring 7 at 2710 m was originally produced on the continental shelf, and that the timeweighted mean flux calculated for this carbon of 0.105 mg Co~g m -2 day -[, represents an

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export of production. We further assume that the trap at 2710 m at mooring 7 represents a slope area 1 m wide extending 1 × 105 m from the shelf-slope break to the continental rise. Thus, the flux of intact cells represents approximately 1.05 × 101 g Corg m-I day-1 along the shelf. The average daily primary production for the continental shelf in the SEEP-I region is ca. 820 mg Co,g m -2 day -1 (FALKOWSKIet aI., 1983, 1988; MALONE et al., 1983). The shelf is about 1.5-fold wider than the trapping area; thus the mean primary production in the region is approximately 1.23 × 105 g Corg m i day i. Hence, the export of intact phytoplankton carbon is approximately 0.009% of the shelf production. Following the same logic, and assuming a C/N ratio of 6 by weight, the export of nitrogen in intact phytoplankton cells is 1.75 mg N m i d a y - l , which represents only 0.001% of the nitrogen required by the primary producers on the shelf to sustain the annual production at a steady-state. These calculations strongly suggest that the export of intact cells from the shelf to the ocean interior appears to be trivial relative to primary production on the shelf and the nitrogen required to sustain that production. The contribution of ocean margin Co,g to the interior of the North Atlantic Ocean A major goal of the SEEP program was to quantify the flux of carbon to the continental slope as a measure of its potential influence on the interior of the central ocean basin. Although the consensus conclusions of most SEEP analyses were that the fraction of primary production that leaves the northeast continental margin in a cross-shelf flux is small relative to shelf production (e.g. FALKOWSKIet al., 1988; KEMP et al., 1994; WmlCK, 1994; ANDERSON et al., 1994), the exported carbon may be a significant fraction of the carbon flux to the interior of the North Atlantic Ocean. Using the sediment trap data from both SEEP-I and -II, we developed a simple two-dimensional box-model to investigate the

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importance of the carbon flux at the margin to the overall carbon economy of the ocean interior. Let us assume that POM can enter the interior of the central ocean via either the vertical flux from above, or laterally from the margin. Let us take an imaginary plane across the 490 m depth horizon extending from the continental shelf seaward into the Atlantic Ocean. All biogenic particles produced in the euphotic zone, whether originating from the continental shelf or from the overlying waters in the central basin, are either remineralized in the upper 490 m, solubilized to form DOC, or are caught in the sediment traps. A section of the mean annual sediment flux from the margin to the ocean interior in the upper at 400-490 m, composited from all SEEP-I and -II sediment trap data, can be adequately described by an exponential function of the form Y = a + b e ( x / , , ) , where Y is the flux of POC and x is the distance from the coast (Fig. 7). In this analysis we assume that a mooring at 31°50'N, 64°10'W, located 1700 km from the coast in >4000 m of water in the Sargasso Sea (DEUSER et a l . , 1990) is sufficiently far removed from the margin such that continental sources of carbon to the vertical POC flux are insignificant. Annual sedimentation at this site averages c a 2 mg Co~g m -2 day ~ at 3200 m, and is slightly lower (for reasons not understood) at 500 m (W. Deuser, personal communication). The area under the curve represented in Fig. 7 represents the daily mean flux of Corg at 490 m depth per meter of coastline for a section extending 1700 km seaward from the shelfslope break into the North Atlantic Ocean. Let us assume that the vertical flux is uniform throughout this section and supports the mid-ocean flux of 2 mg Corg m 2 day-X. Subtracting this mid-ocean "baseline" flux from the curve, and integrating the remaining area yields 5.3 x 103 g Corg m -1 day -~. This is the lateral flux of POC which sediments through 490 m, The calculated value is probably generous, as it is likely that the baseline of 2 mg Corg m -2 day -1 is low for the margins, where higher primary productivity probably supports a higher vertical flux. Let us assume that the lateral Corg flux calculated is representative of the entire continental margin from Cape Hatteras to Labrador, 2.5 x 106 m in length. The resulting

Lateral particle flux

599

flux is 4.8 × 10 ~2g Corgy-1 entering the ocean interior from this margin area. The estimate of new production for the North Atlantic Ocean, based on oxygen budgets from the JGOFS program (BENDER et al., 1992) and analyses of the seasonal patterns of surface chlorophyll (CAMPBELLand AARUP, 1992) suggests that the vertical flux of POC out of the upper mixed layer in the northern portion of the basin averages about 21 g Corg m -2 y-1. We take the area of this portion to be about 20 × 10 6 km 2. Based on these data, the annual mean vertical flux of POC out of the euphotic zone in the North Atlantic Ocean is about 4.2 × 10 ~4 gC y - t . Thus, our analysis suggests that the northeast shelf of the North American continent contributes about 1% of the carbon to the ocean interior. Primary production on the northeast shelf averages about 300 g Cormm-2 y l (MALONE e t a l , 1983; CAMPaELLand O REILLY, 1989), which is about 7.5 × 10 ~3 g CorgY -l for the shelf, or about 2% of the total primary production in the N,:~r~h Atlantic Ocean. Based on the estimates of the lateral flux of POC from SEEP-I and -~1 sediment traps presented here, we calculate that the export of POC is approxim~tely 6.4% of the annual primary production on the shelf. This loss is relatively small and implies that the primary production on the shelf does not require a high import of nitrate from the ocean (WALSH, 1991), but rather nitrogen cycling and nitrification on the continental shelf must be much more important than hitherto thought. Alternative, independent estimates of shelf export, based on shelf carbon budgets (FALKOWSKIet al., 1988), carbon budgets for the upper slope depocenter (ANDERSONet al., 1992), oxygen budgets (KEMP et al., 1992; FALKOWSKIet al., 1988) and estimates of the cross shelf flux of chlorophyll (WIRIC~:, 1992), yield values between 0.75 and 3.8 × 1012 g Co~g y-~. This range of values for the lateral export of POC from the northeast shelf is remarkably constrained, given the uncertainties in each of the approaches taken. While our calculations suggest that the fraction of total shelf production which is exported off the shelf is relatively small, in large measure because virtually all of the shelf production is oxidized on the shelf (FALKOWSK!et al., 1983, 1988; KEMPet al., 1992; ROWE et al., 1986), the exported carbon is a significant source of energy to the western margin of the North Atlantic basin. The oxidation of this carbon on the continental slope (JAHNKE and JACKSON, 1992; ROWEet at., 1993) represents an important conduit for carbon from the ocean margins to the deep sea. Understanding the factors which regulate this conduit is crucial to elucidating the roles of continental margins in the global carbon cycle. CONCLUSIONS Analysis of the taxonomic composition of phytoplankton in the sediment trap samples from the first SEEP field program revealed that almost all of the sedimenting cells which remained intact were diatoms. The temporal and spatial distribution of species suggests that a significant fraction of the biogenic particle flux to depth at the western edge of the North Atlantic Ocean is supported by shelf derived production. The evidence for a lateral flux of materials from the shelf to the central ocean basin is further supported by the quantitative distribution of biogenic constituents, including POC, PON and opaline silica, which increase with depth. The temporal distribution of materials indicates that the materials are injected into the central basin in pulses, which appear to have rapid sedimentation rates. The ratio of Corg to opaline silica in the trap materials is similar to that of diatoms in culture, and suggests that a large fraction of the amorphous detrital material in the preserved trap samples was originally diatomaceous. When a composite of the SEEP

600

P . G . FALKOWSKIet al.

trap samples is used to develop a two-dimensional box model, the resulting analysis suggests that export of POC to the slope is 6.4% of the total shelf primary production. Although this flux appears to be small, its contribution to the carbon economy of the North Atlantic ocean is locally significant at the margin. We recognize that the calculations described are extrapolations from a relatively small area of the continental shelf to a large region, and therefore may not accurately represent the export of carbon from the entire shelf. We did not include the contribution of materials which exit at Cape Hatteras, nor did we account for materials which may exit via the numerous canyons along the shelf-slope break (GARDENER, 1989). Nonetheless, our estimates are remarkably comparable with those presented by others using entirely different approaches. Aeknowledgements--This research was supported by the U.S. D e p a r t m e n t of Energy, Office of Health and Environmental Research under Contract No. DE-AC02-76CH00016 to P. G. Falkowski and DE-FG0287ER60555 to P. E. Biscaye. We thank Kevin W y m a n , Sabina Lowe and Dorota Kolber for technical assistance and Robert Anderson, Rick Jahnke, Douglas Wallace, Creighton Wirick and an a n o n y m o u s reviewer for comments. This is L D E O Contribution N u m b e r 5231.

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FALKOWSKIP. G., J. VIDAL,T. S. HOPKINS,G. T. ROWE,T. E. WHITLEDGEand W. G. HARRISON(1983) Summer nutrient dynamics in the Middle Atlantic Bight: primary productivity and the utilization of phytoplankton carbon. Journal of Plankton Research, 5,515-537. GARDNERW. D. (1989) Baltimore Canyon as a modern conduit of sediment to the deep sea. Deep-Sea Research. 36, 323-358. HARRISONW. G. (1992) Regeneration of nutrients. In: Primary productivity and biogeochemical cycles in the sea, P. G. FALKOWSKIand A. WOODHEAD,editors, Plenum Press, New York, pp. 385-407. HENDEYN. I. (1964) An introductory account of the smaller algae of British coastal waters, Part V, Bacillariophyceae (diatoms). Fishery Investigations Series IV. Ministry of Agriculture, Fisheries and Food. H.M. Stationary Office, London, 317 pp. (45 pl). HOUGHTON R. W., F. AIKMANIII and H. W. Ou (1988) Shelf-slope frontal structure and cross-shelf exchange at the New England shelf-break. Continental Shelf Research, 8,687-710. JAHNKE R. and G. A. JACKSON(1992) The spatial sea floor oxygen consumption in the Atlantic and Pacific Oceans. In: Deep-sea food chains and the global carbon cycle, G. T. ROWE and V. PARIENTE, editors, Kluwer, Amsterdam, pp. 295-307. KEMP P. F., P. G. FAt.KOWSKI,C. FLAGG,W. PHOEL, S. SMITH,D. W. R. WALLACEand C. D. W[RICK(1994) Modeling oxygen and carbon flux during stratified spring and summer conditions on the continental shelf. Deep-Sea Research H, 41,629-655. MALONE T. F., Y. S. HOPKINS, P. G. FALKOWSKIand T. E. WHITLEOGE (1983) Production and transport of phytoplankton binmass over the continental shelf for the New York Bight. Continental Shelf Research, 1, 305-337. MORTLOCK R. D. and P. N. FROELICH(1989) A simple method for the rapid determination of biogenic opal in pelagic marine sediments. Deep-Sea Research, 36, 1415-1426. ROUND F. E., R. M. CRAWFOROand D. G. MANN(1990) The diatoms, Cambridge University Press, Cambridge, 747 pp. ROWE G. T. et al. (1986) Do continental shelves export organic matter? Nature, 325,559-561. ROWE G. T., P. KEMP,S. TRUMBOREand P. E. BISCAVE(1994) Carbon budget for the mid-slope depocenter of the Middle Atlantic Bight: a test of the shelf export hypothesis. Deep-Sea Research 11, 41,657~68. SANCETrA C., T. VILLAREALand P. G. FALKOWSKI(1991) Massive fluxes of rhizosolcnoid diatoms: A common occurrence? Lirnnology and Oceanography, 36, 1452-1457. SMAVDAT. J. (1970) The suspension and sinking of phytoplankton in the sea. Oceanography and Marine Biology Annual Review. 8,353-414. SMETACEKV. S., K. VON BOCKEL,B. ZEITSEHELand W. ZENK(1978) Sedimentation of particulate matter during a phytoplankton spring bloom in relation to the hydrographical regime. Marine Biology, 47, 211-226. STRATHMANNR. R. (1967) Estimating the organic carbon content of phytoplankton from cell volume or plasma volume. Limnology and Oceanography, 12,411-418. STRICKLANI)J. D. H. (196(/) Measuring the production of marine phytoplankton. Fisheries Research Board of Canada Bulletin, 122, 172 pp. WaLsrI J. J. (1988) On the nature of continental shelves, Academic Press, San Diego, 520 pp. WALSn J. J. (1991) Importance of continental margins in the marine biogeochemical cycling of carbon and nitrogen. Nature, 350, 53-55. WIRICK C. D. (1994) Exchange of phytoplankton across the continental shelf-slope boundary of the Middle Atlantic Bight during the 1988 spring bloom. Deep-Sea Research li, 41,391-410.