Physical supply of nitrogen to phytoplankton in the Atlantic Ocean

Authors


Abstract

[1] Mechanisms supplying nitrogen (N) to phytoplankton, and thus constraining the levels of export production, over the oligotrophic subtropical Atlantic are assessed along a meridional transect. Stable nitrogen isotope signals reveal a localized region of N2 fixation over the northern subtropical gyre. Elsewhere, particulate organic nitrogen was isotopically enriched and there was no widespread evidence of a trophic bias. Thus phytoplankton are utilizing an enriched source of N along the transect through much of the oligotrophic Atlantic, which may reflect utilization of nitrate from the deep ocean or, possibly, a supply of dissolved organic nitrogen (DON) from a non-N2 fixing source. While there is a significant supply of DON over the subtropical gyres, reaching 0.15 mol Nm−2 yr−1, less than 10% of the DON is semilabile and thus only implies a relatively small contribution to the nitrogen supply required for export production. Over the central part of the subtropical gyres, the supply of N to phytoplankton is probably from nitrate in the underlying thermocline, possibly from convection and diapycnic transfer, or more likely, from finescale upwelling by mesoscale eddies and frontal circulations. The lateral supply of dissolved organic phosphorus (DOP) appears to be a factor of 2–3 times more important than the lateral supply of semilabile DON, and thus might play a role in contributing to the phosphorus (P) supply for phytoplankton. The lateral supply of DON and DOP might also be important in closing the N and P budgets over the North Atlantic.

1. Introduction

[2] Input of nutrients to the surface, sunlit ocean drives the growth of phytoplankton and maintains export production. This nutrient supply is a particular problem over the extensive subtropical gyres, which are estimated to account for half the global export of organic carbon from the surface to the deep ocean [Emerson et al., 1997]. Wind forcing induces downwelling over the subtropical gyres, leading to nutrient-depleted surface waters. Traditional estimates of nitrogen (N) supply from atmospheric deposition [Knap et al., 1986] and vertical diffusion from the deep ocean [Lewis et al., 1986] are too weak here to explain the diagnosed levels of export production [Jenkins, 1982; Jenkins and Goldman, 1985; Jenkins, 1988].

[3] A range of mechanisms have been invoked to explain how the additional new N is supplied to subtropical gyres (Figure 1a): biological fixation of N2 gas [Michaels et al., 1996; Gruber and Sarmiento, 1997], lateral transport of dissolved organic nutrients [Rintoul and Wunsch, 1991; Williams and Follows, 1998], and time-varying finescale upwelling of nutrients from the deep ocean induced by mesoscale eddies [McGillicuddy and Robinson, 1997; Siegel et al., 1999] and frontal-scale circulations [Mahadevan and Archer, 2000; Levy et al., 2001]. However, there are difficulties with each of these proposed mechanisms. N2 fixation can be inhibited if there are insufficient concentrations of iron and possibly phosphorus (P) in surface waters. The potential of the lateral transfer of dissolved organic nutrients to fuel primary production is dependent on the biological availability of this N pool to phytoplankton. Time-varying upwelling can become unimportant either if there is insufficient time for the phytoplankton to respond to short-lived nutrient inputs or if the nutrient concentrations in the upper thermocline are not maintained.

Figure 1.

A schematic figure depicting (a) the likely nitrogen (N) sources to phytoplankton (P) in the surface ocean from nitrogen fixation, lateral advection of nitrate and dissolved organic nitrogen (DON), vertical transfer of nitrate (NO3) from the deep ocean and ammonium (NH4+) excreted by zooplankton (Z), and (b) the stable nitrogen isotopic values (δ15N) associated with the N source: 1, atmospheric nitrogen (N2) [Minagawa and Wada, 1986]; DON from a N2 fixing source, 2 [Liu et al., 1996] and 3, [Abell et al., 1999], and from non-N2 fixing source, 4 [Benner et al., 1997] and 5 [Knap and Sigman, 2003]; 6, NO3 from the deep ocean [Liu and Kaplan, 1989]; and 7, NH4+ [Checkley and Miller, 1989].

[4] Here we assess the relative importance of these N supply mechanisms for phytoplankton over the Atlantic using data gathered along a meridional transect through the Atlantic, as part of the Atlantic Meridional Transect (AMT) programme. The study focuses on identifying the natural abundance stable nitrogen isotopic composition (δ15N) variations of suspended particulate material and the variations in dissolved organic nutrients along the AMT transect for spring 2000.

1.1. Stable Nitrogen Isotopic Composition of Phytoplankton

[5] Within the surface ocean, phytoplankton preferentially assimilate 14N relative to 15N, as less energy is used in breaking a 14N-X than 15N-X covalent bond. Higher trophic levels become progressively isotopically enriched through fractionation effects associated with metabolism and excretion of N [Rau et al., 1990]. Consequently, export of sinking particulate material (faecal pellets, marine snow) via the biological pump transfers isotopically enriched, particulate organic nitrogen (PON) to deep waters [Checkley and Miller, 1989], which when remineralized below the euphotic zone leads to nitrate that is enriched in 15N [e.g., Liu and Kaplan, 1989; Sigman et al., 1997]. Conversely, the recycled nutrient, ammonia, in surface waters is characterized by isotopically depleted signals [Checkley and Miller, 1989]. The isotopic composition of dissolved organic nitrogen (DON) is presently unclear. Isotopically depleted signals of −2‰ to 1‰ have been measured in the subtropical waters in the North Pacific [Abell et al., 1999], while at BATS, enriched signals of 3‰ to 4‰ were observed [Knapp and Sigman, 2003]. The isotopic composition of high molecular weight DON was further enriched to 6‰ and 7‰ [Benner et al., 1997]. The different isotopic signals for DON might reflect methodological problems, or differences within the DON pools, possibly reflecting the N source, or the degree of degradation, for example, refractory versus semilabile pools [Macko et al., 1987].

[6] The stable nitrogen isotopic composition (δ15N) of phytoplankton (proxy being suspended PON in this study) is primarily determined by two factors: (1) δ15N of the N source (as depicted in Figure 1b) and (2) biological isotopic fractionation during uptake and assimilation of the nutrient source by phytoplankton. If N is in excess, phytoplankton preferentially incorporate the light isotope, 14N, versus 15N, resulting in the isotopic composition of phytoplankton being depleted relative to the N source. In contrast, if N is limiting, the isotopic composition of phytoplankton reflects that of the source due to complete N utilization. Hence the isotopic signature of phytoplankton reflects the relative importance of the different sources of N in oligotrophic environments, since no net isotopic fractionation is expected [Altabet and McCarthy, 1985]. Here we determine the δ15N PON along the Atlantic Meridional Transect.

1.2. Organic Nutrient Approach

[7] DON and dissolved organic phosphorus (DOP) are produced through passive or active exudation by phytoplankton, through N2 fixation, or by bacterial mediated processes and grazing [Bronk, 2002]. A possible mechanism supplying N and P to the subtropical gyres is a lateral influx of DON and DOP from upwelling zones in the tropics and subpolar gyres [Williams and Follows, 1998; Lee and Williams, 2000; Abell et al., 2000]. Here we aim to identify the latitudinal variation in DON and DOP along the AMT transect passing through the Atlantic. The labile and semilabile dissolved organic matter (DOM) pools are reported to be biologically reactive on timescales of hours to days [Bronk et al., 1994; Kiel and Kirchman, 1999] and months to years [Vidal et al., 1999; Carlson, 2002], respectively. Here we include a lower bound estimate of the labile and semilabile components of DON from the latitudinal variation in dissolved free amino acid [DFAA] and total hydrolyzable amino acid [THAA] concentrations.

2. Methodology

2.1. Field Methods

[8] The Atlantic Meridional Transect (AMT10) was surveyed from 35°S, 49°W to 48°N, 20°W (Figure 2) in April and May 2000 by the RRS James Clark Ross. The transect passes across the subtropical gyre in the South Atlantic and along the eastern flank of the subtropical gyre in the North Atlantic (Figure 2, white dashed contours). Suspended particulate matter (SPM) and filtered seawater samples were collected along the transect: SPM was filtered (200–1000 L) from the underway seawater supply (7 m) through precombusted (450°C, >4 hours) 150-mm glass fiber filters (Whatman) using a Sartorius GmBH large volume filtration unit.

Figure 2.

SeaWiFS ocean composite image from January to May 2000 of averaged chlorophyll a concentrations (colored in mg m−3) and vertical wind-driven (Ekman) velocity (m/year) for the same period diagnosed using surface winds from NCEP re-analysis (white contours). Note the extensive area of the subtropical gyres where there is downwelling (dashed contours). The AMT10 Cruise track is included (red line).

[9] In addition, seawater samples (250 mL) were collected for analysis of nitrate plus nitrite (nitrate herein, NO3) and phosphate (PO4−3) and organic nutrients (DON and DOP) from 7 to 10 depths (maximum depth 250 m, one station, 1000 m) at 23 stations using 10-L General Oceanic Niskin bottles mounted on a Sea-Bird electronics 911 plus CTD. Where possible, 2 L of seawater was filtered from discrete depths (7 m and between 35 and 50 m) through precombusted (450°C, >4 hours) 47-mm glass fiber filters (Whatman) for collection of sinking and suspended particulate matter (SSPM).

2.2. Phytoplankton Biomass and Stable Nitrogen Isotopic Analysis

[10] Particulate organic carbon (POC) and PON concentrations were determined using a Carlo Erba (NC 2500) elemental analyzer. Precision was better than 8% (n = 47). Surface (7 m) chlorophyll a concentrations were determined by filtration of seawater (2.1 to 4.2 L) from the nontoxic seawater supply and onboard analysis [Welschmeyer, 1994].

[11] Stable nitrogen isotopic analysis was performed using standard elemental analyzer isotope ratio mass spectrometer (EA-IRMS) techniques [Owens and Rees, 1989]. Subsamples (13-mm diameter discs) were randomly selected from the freeze-dried 150-mm glass fiber filters and homogenized using a mortar and pestle. The δ15N PON was determined using an online system consisting of a Carlo Erba EA coupled to a Finnigan Delta CIRMS. The results are reported in the standard δ notation (‰),

equation image

where Rsample and Rstandard are the 15N/14N ratios in the sample and standard, respectively, the standard being atmospheric nitrogen (N2). Precision was better than ±0.3‰ (n = 51). Where there was insufficient nitrogen for stable isotopic analysis, filters from various depths were combined and homogenized.

2.3. Inorganic and Organic Nutrient Analysis

[12] Concentrations of NO3 and PO4−3 were determined using a Skalar Sanplus segmented flow nutrient autoanalyzer and standard colorimetric techniques [Sanders and Jickells, 2000]. Total dissolved N (TDN) and phosphorus (TDP) concentrations were determined by analysis of NO3 and PO4−3 after ultraviolet oxidation (2 hours) using a Metrohm 705 UV digestion system. Samples were irradiated in 10-mL quartz glass tubes with graphite stoppers at a temperature of 85°C. This method is sufficient to oxidize 60–70% of DON and DOP to NO3 and PO4−3 respectively [Sanders and Jickells, 2000]. DON and DOP concentrations were calculated by ([TDN]-[NO3]) and ([TDP]-[PO4−3]), respectively [Sanders and Jickells, 2000]. Thus our estimates of [DON] and [DOP] and their latitudinal contrasts should be viewed as lower bounds. The detection limits, determined by injection of NO3 and PO4−3 spiked low nutrient seawater, was 0.05 μM for both NO3 and PO4−3. Precision was better than 10% (n = 143).

[13] Dissolved free amino acid concentrations ([DFAA]) were determined using the standard fluorimetric techniques [Parsons et al., 1984]. Total hydrolysable amino acid concentrations ([THAA]) were determined by high-performance liquid chromatography [Cowie and Hedges, 1992], after acid hydrolysis (50% HCl; 90 min).

3. Isotopic Nitrogen Variations Along AMT10

3.1. Hydrographic Context

[14] The transect passed through the extensive downwelling zones of the South Atlantic subtropical gyre and the eastern flanks of the North Atlantic subtropical gyre, extending south of 5°S and north of 20°N, as diagnosed from the Ekman pumping field (Figure 2, solid lines), as well as passing through coastal and equatorial upwelling zones. The gyre-scale variations are also evident in the undulations of the thermocline and nitricline along the transect (Figure 3). Warmer and nitrate-depleted fluid extends below the mixed layer over the southern subtropical gyre (between 35°S and 5°S) and the northern subtropical gyre (15°N to 35°N). The low nitrate concentrations are induced partly through biological consumption and partly by nutrient-rich surface waters along the gyre flanks being subducted into the underlying thermocline. The higher nitrate concentrations north of 40°N are still within the downwelling zone of the subtropical gyre (Figures 2 and 3) and probably result from convection and lateral wind-driven transfer [Williams and Follows, 1998; Williams et al., 2000].

Figure 3.

A meridional section along the AMT10 transect showing (a) temperature (°C) and (b) nitrate (μM) within the upper 250 m. The base of the mixed layer (as defined by Hooker et al. [2000]) is denoted by the dashed line. Note the uplift of the thermocline over the tropics and its depression over the subtropical gyres, which is reflected in an uplift of nitrate-rich waters over the tropics and nitrate-depleted surface waters over the subtropical gyres.

[15] The subtropical surface waters were typically oligotrophic, with concentrations of chlorophyll a < 0.1 mg m−3, PON < 0.26 μM, and NO3 < 0.1 μM, during this April/May transect (Figures 4a and 4b). Along the northern flank of the North Atlantic subtropical gyre (north of 40°N), there were elevated NO3 (>5μM) concentrations, which led to development of a spring bloom (Figure 4a). There were additional chlorophyll a peaks in the tropics and coastal equatorial zone where there is wind-induced upwelling (Figure 2).

Figure 4.

Latitudinal variation (40°S to 60°N) along AMT10 in (a) chlorophyll a (mg m−3) (solid line) and particulate organic nitrogen (PON, μM) (open circles) concentrations; (b) depth-averaged nitrate (NO3) and phosphate (PO4−3) within the mixed layer (μM) (solid circle and open triangle, respectively); (c) stable nitrogen isotopic composition (δ15N, ‰) of PON collected from the nontoxic underway seawater supply at 7 m (solid triangle) and CTD casts between 7 and 55 m (open square). Dashed lines denote five separate regions (from left to right): the south Atlantic subtropical gyre, equatorial and coastal upwelling region, and north Atlantic subtropical gyre separated further into regions of isotopically depleted, enriched, and very depleted regions (see Table 1).

3.2. Isotopic Signals

[16] The isotopic composition of PON was relatively enriched (>3‰) over the transect, apart from localized isotopically depleted signals in the northern subtropical gyre (Figure 4c). First, we discuss the importance of a potential trophic bias, and then, second, the interpretation of the depleted and enriched signals.

3.2.1. Trophic Bias

[17] Zooplankton are typically enriched in 15N by ∼3‰ relative to phytoplankton [Minagawa and Wada, 1984]. Inclusion of particulate material derived from higher trophic levels would add POC and PON but not chlorophyll a to the particulate biomass, and would also lead to enriched δ15N PON. Thus, if this trophic bias is important, a positive relationship between the ratio of POC:chlorophyll a or PON:chlorophyll a and δ15N PON would be expected [Waser et al., 2000].

[18] There was no such relationship observed for PON collected using the underway nontoxic supply (at 7 m; Figures 5a and 5b) and thus we consider that δ15N reflect the original phytoplankton signature. However, PON collected from the CTD, including suspended and sinking particulate material, did show a significant relationship between POC:chlorophyll a or PON:chlorophyll a and δ15N PON (Figures 5c and 5d), presumably reflecting the inclusion of large sinking particles (including zooplankton detritus, faecal pellets, etc.).

Figure 5.

Relationship between δ15N PON (‰) with the ratio of POC:chlorophyll a and PON:chlorophyll a for samples collected from the underway non-toxic seawater supply (Figures 5a and 5b, respectively), and for samples collected from the CTD from 7 m to 55 m (Figures 5c and 5d, respectively). There is no significant correlation between δ15N PON and the ratios for Figures 5a and 5b (any statistical fits, only have a correlation coefficient R2 < 0.02), thus suggesting there is no trophic bias. However, for the nine CTD samples, there does appear to be a statistically significant correlation (above 99%) with isotopically enriched samples correlating with higher ratios; the best fits are δ15N PON = 0.001 POC:chlorophyll a + 1.1582 with R2 = 0.71 and δ15N PON = 0.02 PON:chlorophyll a + 1.20 with R2 = 0.66. Thus the CTD samples including sinking particles probably contain a trophic bias.

[19] Consequently, suspended PON from the underway supply was assumed to reflect the composition of phytoplankton, rather than higher trophic levels. The variations in the isotopic signals are assumed then to reflect changes in the N sources to the phytoplankton and, where there was excess N, the influence of biological isotopic fractionation. In our subsequent analyses, we separately show the PON data from the underway water supply and CTD (in Figures 4 and 5) and base our conclusions on analyses for the underway supply (Table 1).

Table 1. Mean δ15N PON and the Estimated Percentage of Nitrate Supporting Primary Production for Selected Latitude Bands in the Atlantic Oceana
Oceanic RegionLatitudeMean δ15N PON ± σ/n1/2nPercent Supply of Nitrate
  • a

    Here σ is the standard deviation, n is the number of observations, and σ/n1/2 is the standard error. The estimates are based on the samples of suspended particulate organic matter taken from the underway supply (with, in brackets, the total values included when samples are taken from the underway seawater supply and CTD). The percentage of nitrate supporting primary production is calculated using a two-end-member isotope model, where there is a depleted source of N (0‰) and an enriched source of N (4.5‰ or 6‰). The selected latitude bands are chosen according to the patterns of the isotopic signals and wind-driven upwelling.

South Atlantic subtropical gyre36°S to 6°S4.88 ± 0.85 (4.09 ± 0.46)3 (8)81 to 108 (68 to 90)
Equatorial and coast upwelling region5°S to 23°N4.80 ± 0.37 (4.75 ± 0.29)8 (16)79 to 106 (80 to 106)
North Atlantic subtropical region24°N to 32°N1.92 ± 0.17 (2.25 ± 0.36)8 (9)32 to 43 (37 to 50)
33°N to 38°N3.16 ± 0.41653 to 70
39°N to 48°N−0.46 ± 0.64 (−0.72 ± 0.52)10 (13)not applicable

3.2.2. Interpretation of Depleted Isotopic Signals

[20] Isotopically depleted PON was observed between 24°N–32°N (1.92 ± 0.17‰; mean ± standard error) and 40°N–48°N (−0.46 ± 0.64‰; underway values shown in Table 1). The northern signal at 40°N–48°N coincided with a bloom and reflects biological fractionation where there is excess nitrate available [Altabet, 1988]. However, relatively depleted isotopic signals (1.92 ± 0.17‰) were also observed in the oligotrophic waters over part of the northern subtropical gyre (24°N–32°N; Figure 4c, Table 1). Here nitrate is also enriched relative to phosphate in the thermocline as revealed by an elevated N:P ratio, and there are elevated concentrations of chemotaxonomic markers indicative of cyanobacteria in the particulate material [Mahaffey et al., 2003]. Collectively, these independent signals imply a dominant role for N2 fixation, rather than production fuelled by NH4+ or DON. In addition, these signals correlate with anomalously high levels of modeled dust deposition, suggesting that the atmospheric forcing may induce N2 fixation by supplying Fe to surface waters [Mahaffey et al., 2003]. Recent geochemical evidence presented by Hansell et al. [2004] suggests that N2 fixation may extend farther west into the subtropical Atlantic, implying that N2 fixation events are not always as localized as the limited latitudinal range implied by our transect data.

3.2.3. Interpretation of Enriched Isotopic Signals

[21] Enriched isotopic signals occurred in the tropical and coastal upwelling zone between 5°S and 20°N (4.80 ± 0.37‰), over the southern subtropical gyre between 35°S and 6°S (4.88 ± 0.85‰) and in the northern subtropical gyre between 33°N and 38°N (3.16 ± 0.41‰; Table 1). The PON samples were collected within the tropical and subtropical euphotic zone, and thus the enriched signals were not due to remineralization of PON, which instead is expected to occur below the euphotic zone within the underlying thermocline.

[22] The relative importance of the N sources to phytoplankton is identified by assuming that the isotopic composition of PON is in equilibrium with N sources and by using a simple two-member mixing model. Here we assume negligible isotopic fractionation in nutrient-depleted surface waters. Conservative choices are made for the enriched isotopic source of 4.5‰ to 6‰, and a depleted isotopic source of 0‰. Accordingly, the enriched isotopic signals over the southern subtropical gyre (35°S–6°S), the tropics (5°S–23°N) and parts of the northern subtropical gyre (33°N–38°N) suggest that an isotopically enriched N supply accounts, respectively, for 81 to 108, 79 to 106, and 53 to 70% of the N utilized by phytoplankton (Table 1). In contrast, the depleted isotopic signal in the northern subtropical gyre (24°N–32°N) suggests that an isotopically enriched source of N only provides up to 32 to 43% of the N supplied to phytoplankton.

[23] From our present knowledge, there are two potential sources of isotopically enriched nitrogen to phytoplankton: nitrate from the deep ocean [Liu et al., 1996; Sigman et al., 1997] and DON from a non-N2 fixation source [Benner et al., 1997; Knapp and Sigman, 2003]. However, DON does not appear to provide a dominant role in N supply here (discussed in section 4).

[24] Nitrate supply over the transect can easily be provided from the deep ocean over the tropics and coastal ocean, where the winds induce persistent upwelling (Figure 2). Explaining a high level of nitrate supply is more problematic over the subtropical gyres where the winds drive downwelling over the basin scale (and the diabatic diffusion is generally viewed as being too weak to sustain export production). There are several possible mechanisms to supply the necessary nitrogen with an enriched isotopic signal, but each has potential difficulties.

[25] A convective supply is only likely to be significant north of 40°N, since elsewhere the diagnosed mixed layer is thin (<80 m) and has low nitrate concentrations (<0.5 μM) (Figure 4b). In addition, convection might be expected to provide different signals in each hemisphere, as the transect samples the southern gyre in autumn (after summer heating) and the northern gyre in late spring (after the end of the winter cooling and maximum convection).

[26] A surface wind-driven transport might be important along the flanks of the subtropical gyre, where nitrogen is horizontally transported from the nutrient-rich subpolar gyre and tropics where there is persistent upwelling [Williams and Follows, 1998]. However, the lateral transfer of nitrate becomes exhausted over a horizontal scale of typically 500 km.

[27] Over the center of the subtropical gyres, the nitrate might be supplied to phytoplankton through finescale, transient upwelling from the deep ocean. A time-varying circulation leads to a time-averaged supply of nitrate through an asymmetrical response of the ecosystem: phytoplankton growth occurs when the nitricline is uplifted into the euphotic zone, while there is no growth when it is depressed into the dark interior [Falkowski et al., 1991; McGillicuddy and Robinson, 1997]. This mechanism is excited through the passage of mesoscale eddies [McGillicuddy and Robinson, 1997; McGillicuddy et al., 1998] and the development of submesoscale frontal circulations [Mahadevan and Archer, 2000; Levy et al., 2001].

[28] An upper bound for the eddy supply of nutrients has been estimated to reach from 0.19 to 0.24 mol N m−2 yr−1 for the Sargasso Sea [McGillicuddy et al., 1998; Siegel et al., 1999] with typically four events required per year to close the N budget at BATS. However, the time required for phytoplankton to remove nutrients (days) is less than that of the supply mechanisms (weeks), thus making it difficult to monitor such events. In contrast to previous studies relying on snapshots of hydrographic or remotely sensed data, our view is based upon longer-term isotopic signals of phytoplankton, which have a residence time lasting tens of days [Waser et al., 2000]. If the eddy and frontal mechanisms provide the dominant supply of deep nitrate, then in turn this transfer raises the question of how the underlying nutrient concentrations in the thermocline are sustained; see discussion by Williams and Follows [2003].

4. Organic Nutrient Variations Along AMT10

4.1. Inorganic and Organic N and P Distributions

[29] DON and DOP dominated (>60%) the total dissolved nitrogen (TDN) and phosphorus (TDP) pools in near-surface waters (<80 m), as revealed by a deep cast (1000 m: at 13.51°S, 32.33°W) shown in Figure 6. [DON], calculated from ([TDN]-[NO3]), were relatively high in the surface waters (<180 m mean ± 1 standard error, 5.58 ± 0.96 μM, n = 4) and decreased with depth (>500 m; 2.15 ± 0.3 μM, n = 2) (Figure 6a). In contrast, [DOP], calculated from ([TDP-PO43−]) were relatively high in surface waters (<180 m; 0.43 ± 0.15 μM, n = 4), but negligible at depth (>500 m; < 0.02 ± 0.001 μM) (Figure 6b).

Figure 6.

Depth variation of (a) total dissolved nitrogen (TDN) (open circle: μM) and nitrate (solid circle) and (b) total dissolved phosphorus (TDP) (open triangle) and phosphate (solid triangle) in the South Atlantic at 13.51°S, 32.33°W over 1000 m. Error bars are ±1 standard error. Note that there is a difference between TDN and nitrate in the deep waters indicating background DON, whereas this difference does not occur for TDP and DOP.

[30] Relatively high concentrations of TDN and TDP, depth-averaged over the mixed layer, were observed at the southern and northern flanks of the southern subtropical gyre (>4.79 ± 0.30 μM and >0.20 ± 0.02 μM, respectively), and at the southern and northern flanks of the northern subtropical gyre (>5.62 ± 0.35 μM and >0.08 ± 0.01 μM, respectively; Figure 7). Both [TDN] and [TDP] decreased into the centers of the southern (3.40 ± 0.21 μM and 0.07 ± 0.01 μM, respectively) and northern subtropical gyres (4.71 ± 0.29 μM and 0.11 ± 0.01 μM, respectively) along the AMT transect.

Figure 7.

Latitudinal variation (40°S to 60°N) of (a) total dissolved nitrogen (open circles) and nitrate (NO3; solid circles) and (b) total dissolved phosphorus (open triangle) and phosphate (PO43−; solid triangle) concentrations (μM) along the AMT10 transect. Data are averaged above the mixed layer depth. Error bars represent 1 standard error.

[31] Overall, there was more latitudinal variation in DOP than DON over the AMT transect (Figure 8a). DON (55 to 100%) and DOP (67 to 100%) dominated the TDN and TDP pools, respectively, over most of the AMT10 transect (Figure 8b); NO3 and PO43− instead dominated north of 40°N (Figures 7 and 8b).

Figure 8.

Latitudinal variation (40°S to 60°N) of (a) dissolved organic nitrogen (DON; solid circles) and dissolved organic phosphorus (DOP; open triangles) concentrations (μM), (b) percentage (%) contributions of DON to TDN (solid circles) and DOP to TDP (open triangles) averaged over the mixed layer, and (c) DON to DOP ratio along the AMT10 transect (with the dashed line indicating the Redfield ratio). Error bars represent 1 standard error.

[32] DON:DOP ratios ranged from 13 to 73 along the AMT transect, being highest in the eastern flanks of the northern subtropical gyre and lowest in the southern subtropical gyre (Figure 8c). The ratios were particularly high (>70) between 10°N and 25°N suggesting that there was a local source of N, but not P. There are two possible mechanisms that might provide this signal. First, an additional supply of N might be achieved by nitrogen fixation. Second, advection and subduction of the more refractory DON should increase the DON concentrations in the thermocline, while the DOP is utilized and recycled in the surface layer (see section 4.3).

4.2. Bioavailability of DON

[33] In order to provide some indication of how bioavailable the DON is along the AMT10 transect, the dissolved free amino acids [DFAA] and total hydrolyzable amino acids [THAA] concentrations were determined (Figure 9a). [DFAA] ranged from 7.3 × 10−3 ± 1.4 × 10−3 to 53.7 × 10−3 ± 1.6 × 10−3 μM N, being slightly elevated in the equatorial and coastal upwelling region off West Africa, but relatively low (<0.1 μM) over the remainder of the AMT10 transect (Figure 9a). [THAA] ranged from 0.4 ± 0.1 μM N to 1.4 ± 0.1 μM N; relatively high [THAA] were observed over the subpolar region during AMT10 (>1.2 μM) (Figure 9a).

Figure 9.

Latitudinal variation in surface (7 m) concentrations (μM) of (a) dissolved free amino acids (DFAA; solid square) and total hydrolyzable amino acids (THAA; open triangle) and (b) the contribution (%) of DFAA to DON (solid square) and THAA to DON (open triangle).

[34] DFAA represented only 0.2 to 0.6% of the total DON pool, while THAA represented 3.6 to 9.9% of the total DON pool (Figure 9b). If DFAA is assumed to represent the labile fraction of the DON pool, then the labile DON only accounted for <0.6% of the DON pool. Likewise, if THAA is assumed to represent the semilabile pool, then the semilabile DON only accounts for less than 10% of the total DON.

[35] Previous studies have also shown that deep water DOM is of limited bioavailability and reactivity, and thus represents the refractory organic nutrient pool [Barber, 1968]. Measurements from a deep station in the Atlantic (13.51°S, 32.33°W; Figures 6a and 6b) reveal refractory DON and DOP pools (defined instead by deep ocean concentrations), accounting for 2.1 μM (38%) and <0.02 μM (<13%) of the surface DON and DOP pools, respectively. Any changes in the relatively small labile (<0.6%) and semilabile (<10%) DON pools are likely to be masked by the magnitude of the refractory pool. In contrast, the variations in [DOP] may be more likely to reflect variations in biologically available DOP, the refractory DOP pool being considerably smaller than that of DON.

4.3. Control of DON and DOP Distributions

[36] There are contrasting distributions of DON and DOP over the subtropical gyres: DON appears relatively uniform, while DOP has a minimum in the central part of the subtropical gyres along the AMT10 cruise track. These different distributions might reflect either differences in the biological or physical control of DON and DOP.

4.3.1. Biological Control

[37] DON consists of a variety of molecules from simple amino acids, neutral and amino sugars to complex humic and uncharacterized protein molecules [McCarthy et al., 1997; Benner, 2002] and peptidoglycan [Tanoue, 1995]. In contrast, DOP is made up of nucleic acids, ATP, cyclic AMP, lipids, vitamins, and phosphate polymers [Karl and Bjorkman, 2002]. Differential compartmentalization of N and P in these diverse and complex molecules leads to the uncoupling of the biological production, recycling, and remineralization of N and P [Vidal et al., 1999; Loh and Bauer, 2000; Karl et al., 2002]. In addition, differences in their reactivity are due to the greater molecular complexity of the DON pool [Antia et al., 1991; McCarthy et al., 1997] compared to the DOP pool [Karl and Yanagi, 1997; Suzumura et al., 1998; Kolowith et al., 2001] and heterotrophic activity in the euphotic zone.

[38] N2-fixing organisms are a significant source of DON, but are P limited [Karl et al., 2002], thus leading to elevated surface DON, but possibly utilizing surface DOP (Figure 10a). N2 fixation, along with differential recycling of DON and DOP, will amplify the DON pool in the surface ocean, but may only drive exchange of P between inorganic and organic pools in the Atlantic.

Figure 10.

A schematic figure depicting (a) nutrient pathways involving the biological transfer of DON and DOP between N2 fixing organisms and phytoplankton, where DON is exuded, whereas DOP is both exuded and utilized, and (b) the physical transfer of DON and DOP through vertical and horizontal transport. Whereas DON is remineralized in the surface and deep ocean, DOP is only remineralized in surface ocean, leading to negligible DOP in the deep ocean.

4.3.2. Physical Control

[39] Physical transfer of nutrients from the deep to surface ocean will lead to contrasting signals emerging for surface [DON] and [DOP], since there is significant refractory DON pool and negligible DOP in the deep ocean. Hence, over the subtropical gyres, upwelling (either locally from eddies or indirectly from upwelling at the equator and subpolar gyre and subsequent horizontal transfer) would transfer the refractory DON to the surface ocean without any accompanying increase in DOP (Figure 10b).

4.4. Wind-Driven Transfer of DON and DOP

[40] The lateral wind-driven transfer of DON and DOP can be directly estimated from AMT10 data. While this wind-driven transfer only provides part of the advective transfer, climatological diagnostics suggest that this transfer is important along the gyre flanks [Williams and Follows, 1998]. The nutrient supply to the surface layer from the surface wind-induced Ekman transfer along the track is given by

equation image

where h is thickness of surface Ekman layer, N is an arbitrary nutrient concentration, u and v are the eastward and northward Ekman velocities, w is the implied Ekman upwelling velocity, and Nh is the nutrient concentration at the base of the surface layer. The lateral Ekman nutrient flux is given by the product of the volume flux (hu, hv) and the nutrient concentration, N,

equation image

where τx and τy are the eastward and northward wind stresses, ρ is the density, and f is the Coriolis parameter. The Ekman flux along the AMT section is evaluated using monthly NCEP winds for April and May 2000, and the stress, τ = ρacdUaUa∣, is evaluated using a drag coefficient cd based on wind speed and air-sea temperature contrasts [Hellerman and Rosenstein, 1983]; ρa is the air density and Ua is the wind speed at 10 m.

[41] As our focus is on the gyre-scale transfer of N and P, the subsequent diagnostics concentrate on the meridional flux and supply; including the zonal component only alters the details of our results. The pattern of wind forcing over April and May leads to a convergence in the Ekman horizontal volume flux over both the northern and southern subtropical gyres, leading to an Ekman pumping of 30 m yr−1 over the southern gyre, but only 7 m yr−1 over the northern gyre (Table 2). This weak signal over the northern gyre is due to the AMT10 transect being along the eastward side of the basin (Figure 2, contours).

Table 2. Meridional Ekman Volume and Nutrient Fluxes at the Gyre Boundaries and Implied Ekman Pumping and Supply of Nutrients for the Subtropical Gyres Passing Along the AMT10 Transecta
Meridional FluxesSouthern Subtropical Gyre BoundariesNorthern Subtropical Gyre Boundaries
  • a

    Ekman pumping and supply of nutrients are evaluated from the convergence of the meridional fluxes at the gyre boundaries. Note that the estimates for the northern gyre are much smaller than that of the southern gyre, which is due to the transect running close to the eastern boundary of the northern gyre where the Ekman pumping is weak (see Figure 2).

 35°S6°S10°N39°N
Volume, m2 s−1−0.02−3.130.93−0.21
Nitrate, mmol N m−1 s−1−0.008−0.550.19−0.32
DON, mmol N m−1 s−1−0.13−16.5.4−0.87
Phosphate, mmol P m−1 s−1−0.001−0.180−0.014
DOP, mmol P m−1 s−1−0.005−0.360.074−0.019
 
Supply of Volume and NutrientsSouthern Subtropical Gyre (35°S to 6°S)Northern Subtropical Gyre (10°N to 39°N)
Ekman pumping, m yr−130.36.8
Nitrate, mol N m−2 yr−10.0050.005
DON, mol N m−2 yr−10.150.047
Phosphate, mmol P m−2 yr−11.70.14
DOP, mmol P m−2 yr−13.40.92

4.4.1. Lateral Flux and Supply of Nitrogen Along AMT10

[42] Estimates of the horizontal Ekman flux of N along the AMT10 transect (Figure 11a, solid line) reveal the expected gyre-scale pattern [Williams and Follows, 2003]. There is a southward flux of NO3 from the tropics into the southern subtropical gyre (−0.56 mmol N m−1 s−1 at 6°S), a northward flux from the tropics (0.19 mmol N m−1 s−1 at 10°N), and a southward flux from the northern flank (−0.32 mmol N m−1 s−1 at 39°N) into the northern subtropical gyre. The convergences of the Ekman nitrate flux lead to an average nitrate supply of 0.005 mol N m−2 yr−1 over both the southern and northern subtropical gyres (Table 2). This estimate of the Ekman supply of nitrate is smaller than the climatological estimate of typically 0.03 mol N m−2 yr−1 [Williams and Follows, 1998], which reflects the weak horizontal gradients in surface nitrate observed along the late spring transect.

Figure 11.

Meridional Ekman flux of (a) nitrate (solid squares) and DON (open diamonds) (mmol N m−1 s−1) and (b) phosphate (solid squares) and DOP (open diamonds) (mmol P m−1 s−1) between 35°S and 50°N along the AMT10 transect; positive denotes a northward flux. In all cases, the direction of the fluxes leads to a supply of nutrients over the southern subtropical gyre and northern subtropical gyre. Note that the scale of the DON flux is shown a factor of 10 larger than that of nitrate, reflecting how only 10% of the DON flux is probably semilabile.

[43] There is a generally similar pattern for the Ekman flux of DON, but at least an order of magnitude larger than for nitrate; the DON flux reaches −16 mmol N m−1 s−1 at 6°S and 5.4 mmol N m−1 s−1 at 10°N. Consequently, the convergence of the Ekman DON flux reaches 0.15 and 0.06 mol N m−2 yr−1 over the southern and northern subtropical gyres, respectively (Table 2).

[44] While this DON supply is an order of magnitude larger than the corresponding nitrate fluxes, they may not be that significant in sustaining biological production, due to much of the DON being refractory. From the preceding arguments that an upper limit for the semilabile content of DON is 10%, then the supply of DON is only likely to sustain levels of export production reaching 0.015 and 0.006 mol N m−2 yt−1 over the southern and northern subtropical gyres, respectively. The remaining supply of DON from the horizontal convergence in the Ekman layer will, in a steady state, lead to a vertical pumping of DON into the thermocline achieved through the w term in equation (1). This subduction of DON should then contribute to the relatively high DON:DOP ratio within the thermocline (Figure 8c).

4.4.2. Lateral Flux and Supply of Phosphorus Along AMT10

[45] A broadly similar pattern emerges for phosphorus with the Ekman flux of DOP dominating over that of phosphate (Figure 11b). From the tropics, there is a southward flux for both DOP and phosphate into the southern gyre (−0.63 and −0.05 mmol P m−1 s−1 at 10°S, respectively) and a northward flux of DOP into the northern gyre (0.07 mmol P m−1 s−1) and no detectable phosphate flux at 10°N. For the northern gyre, there is only a weak southward influx of −0.019 and −0.014 mmol P m−1 s−1 for DOP and phosphate at 39°N. Thus the phosphorus supply from DOP is greater than that of phosphate by a factor of 2 for the southern gyre and a factor of 6 for the northern gyre (Table 2).

[46] If the DOP supply is converted assuming a Redfield ratio into an equivalent N supply and the DON is only assumed 10% semilabile, then the DOP supplies are factors of 3 and 2 larger than that from DON over the southern and northern subtropical gyres, respectively. Thus the lateral DOP supply is probably more important in sustaining export production than the DON supply.

[47] In summary, the horizontal supply of dissolved organic nitrogen is at least an order of magnitude larger than that of nitrate along the AMT transect for April and May 2000. The horizontal supply of DOP is at least twice that of phosphate. Thus the cycling and transport of dissolved organic nutrients appears to be more important than the corresponding transport of dissolved inorganic nutrients. However, assuming the geochemical estimates of export production in the Sargasso Sea is representative [Jenkins, 1982; Jenkins and Goldman, 1985; Jenkins, 1988], then the N and P supply need to reach typically 0.5 mol N m−2 yr−1 and 36 mmol P m−2 yr−1 (assuming a P requirement in Redfield ratio). In comparison, the DOP lateral supply is an order of magnitude smaller, 3.4 mmol P m−2 yr−1 over the southern subtropical gyre; our estimate for the northern gyre is almost certainly an underestimate due to the transect path. However, given the difficulty in supply P from the atmosphere, the lateral supply of DOP probably plays a role, but needs to be augmented by other processes. The answer to this problem of how to supply P to phytoplankton might again lie with a supply of deep phosphate, concomitant with the supply of deep nitrate (as suggested by the isotopic analysis in section 3.2).

4.4.3. Closing the N and P Budgets Over the North Atlantic

[48] Inverse studies for N and P over the basin scale have so far only focused on the transport of nitrate and phosphate given the lack of data for DON and DOP. For the North Atlantic, inverse studies suggest that there is a loss of inorganic nutrients over the subtropical gyre [Rintoul and Wunsch, 1991; Ganachaud and Wunsch, 2002]. For example, Rintoul and Wunsch [1991] diagnosed a southward nitrate flux of −8 ± 39 kmol N s−1 across the basin at 24°N and a northward flux of 119 ± 35 kmol N s−1 at 36°N. This mismatch led Rintoul and Wunsch to propose that the N budget was closed through an influx of DON; an alternative option is nitrogen fixation, but that still leaves an implied mismatch for the P budget. If our diagnostics along the AMT transect are representative of the whole basin, then our northward surface DON flux of 5 mmol N m−1 s−1 along the transect at 10°N corresponds to a northward DON flux of 20 kmol N s−1 at 10°N across the whole basin (assuming a basin width of 4000 km). This estimate of the DON flux and its corresponding semilabile component (10% of the total flux) are comparable to the southward nitrate flux of −8 ± 39 kmol N s−1 diagnosed at 24°N. While there are many uncertainties in this extrapolation, such as not knowing the variation with longitude and the return DON flux at depth, the estimate suggests that the DON transport can play an important role in closing the N budget over the North Atlantic. This issue will only be fully resolved, though, by repeating the hydrographic sections and inverse calculations including both DON and DOP measurements.

5. Conclusions

[49] The growth of phytoplankton and maintenance of export production requires a nutrient supply in surface waters to offset the loss from biological fallout. A variety of new mechanisms have been proposed over downwelling subtropical gyres to augment traditional estimates of nutrient supply and explain how export production is sustained: nitrogen fixation, transport of dissolved organic nutrients, and transient upwelling. In order to reveal where each of these mechanisms are significant, we have collected and analyzed data along a meridional transect through the Atlantic. Our focus has been to identify characteristic signals by examining the stable isotopic N signals of phytoplankton and assessing the changes in DON and DOP along the transect. Our study is, though, unable to provide estimates of the rate of nutrient supply and is based only on a single survey, which passes along the eastern side of the northern subtropical gyre and passes across the southern subtropical gyre. In addition, the survey ideally needs to be repeated for different seasons and years given the strong seasonal and interannual variability in biological cycling.

[50] For our transect over the oligotrophic Atlantic, nitrogen fixation appears only to be significant over a restricted latitudinal range over the northern subtropical gyre [Mahaffey et al., 2003], coincident with where there are high levels of atmospheric dust input. Elsewhere, there are relatively enriched isotopic N signals suggesting N is supplied from deep nitrate or, possibly, utilized from DON. The supply of deep nitrate to phytoplankton is easily achieved over upwelling zones or at high latitudes where convection is active. There can be a lateral transfer of nitrate achieved by the wind or eddy transfer over the flanks of the subtropical gyre [Williams and Follows, 1998], and convection can provide an important transfer at the end of winter [Williams et al., 2000]. However, over the central part of the subtropical gyres between April and May, the most plausible mechanism supplying deep nitrate is by finescale, time-varying circulations associated with mesoscale eddies or fronts. Consequently, the isotopic signals suggest that phytoplankton are able to respond to these transient, episodic injections of nutrients with the deep nitrate supply providing the dominant contribution (over 80% for the southern subtropical gyre, Table 1).

[51] Alternatively, the lateral supply of DON to the center of the subtropical gyre might provide the necessary N to sustain export production. However, most of the DON appears to be refractory, as suggested by high concentrations of DON at depth, as well as low concentrations of DFAA and THAA. Thus the lateral supply of DON probably only plays a minor role in sustaining levels of export production. However, the lateral supply of DON and DOP might play a more important role in offsetting the loss of nitrate and phosphate implied from inverse studies over the North Atlantic subtropical gyre [Rintoul and Wunsch, 1991; Ganachaud and Wunsch, 2002]. Any lateral supply of DON and DOP probably originates from the tropics, rather than from the subtropical/subpolar boundary.

[52] The DOP distribution differs from that of DON, with no significant DOP in the deep waters and more marked minima in the center of the subtropical gyres and higher concentrations on the gyre flanks. These contrasting distributions probably reflect differences in how the biological and physical processes operate for N and P. Given the difficulty in providing P from the atmosphere, the dominant mechanism supplying P to phytoplankton probably again involves a vertical supply of deep phosphate, which is augmented by the lateral transfer of DOP.

Acknowledgments

[53] We acknowledge the AMT programme supported by the UK NERC Consortium grant (NER/O/S/2001/01245) and NERC studentship (GT04/1999/MS/0134). We thank the officers and crew of RRS James Clark Ross and are grateful for assistance from V. Roussenov, R. Sanders, M. Follows, C. Wilson, T. O'Higgins, A. Poulton, V. Hill, and S. Groom.

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