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Nitrogen Uptake by Phytoplankton in a Shallow Water Tidal Front
Estuarine, Coastal and Shelf Science (2000) 51, 349–357 doi:10.1006/ecss.2000.0678, available online at http://www.idealibrary.com on
Nitrogen Uptake by Phytoplankton in a Shallow Water Tidal Front J.-F. Maguera, S. L’Helguen and P. Le Corre Laboratoire de Chimie Marine, Universite´ de Bretagne Occidentale et U.P.R. 9042 C.N.R.S. Roscoff, Place Nicolas Copernic, Technopoˆle Brest-Iroise, F-29280 Plouzane, France Received 2 February 2000 and accepted in revised form 29 May 2000 Nitrogen uptake by phytoplankton was studied in a shallow water tidal front and its adjacent stratified and well-mixed sectors on the Armorican shelf (north-west Europe) in July 1992. The front was characterized by relatively high phytoplankton biomass (>3·4 g l 1) and high ammonium and nitrate uptake rates (1·05 and 0·63 mmol m 2 h 1 respectively) compared with the stratified (0·71 and 0·21 mmol m 2 h 1) and well-mixed (0·49 and 0·25 mmol m 2 h 1) waters. Ammonium regeneration rates at the front were of the same order as ammonium uptake rates indicating intense recycling of nitrogen by microheterotrophs. The high total nitrogen uptake, in terms of both absolute and chlorophyll-specific rates, in the front suggests that in situ growth, rather than physical processes, is the main cause of phytoplankton abundance in the front. Despite high nitrate uptake rates, the f-ratios (NO3 /(NO3 +NH4+ )) were lower than in the deep water tidal fronts, because of low nitrate concentrations below the thermocline. 2000 Academic Press Keywords: nitrogen uptake; f-ratio; tidal front; continental shelf; north-west Europe
Introduction Tidally-generated thermal fronts separating nutrientdepleted warm stratified waters from nutrient-rich cold well-mixed waters on the continental shelves of the north-western Europe are a regular phenomenon during summer (Pingree & Griffiths, 1978). Two types of fronts, according to the depth of the water column, can be distinguished (Pingree et al., 1978). In the deep-water fronts, the depth of the water column is greater than that of the euphotic zone and the nutrient stock below the thermocline remains high even during summer. In the shallow-water fronts, on the other hand, the euphotic zone extends up to the bottom and the whole water column tends to become nutrient-depleted at this time. Chemical and biological processes in the deepwater fronts have been fairly well studied (Pingree et al., 1975; Holligan, 1979; Holligan et al., 1984; Group Grepma, 1988; Harrison & Wood, 1988). The primary production rates in these fronts, in terms of carbon (Parsons et al., 1983; Videau, 1987) and nitrogen (Horne et al., 1989; Harrison et al., 1990; Le Corre et al., 1993), have been shown to be usually high. Such high production rates have been generally ascribed to increased vertical transfer of nitrate at the front and corresponds, therefore, to a higher fraction a
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of new production (Horne et al., 1989; Morin et al., 1993). In some instances, they are also related to intense nitrogen regeneration within the euphotic zone, leading to an increased proportion of regenerated production (Le Corre et al., 1993). Studies on shallow-water fronts are less numerous (Pingree et al., 1978, 1983; Turley, 1986; Morin et al., 1989; Riegman et al., 1990). Though these studies also have shown increase in phytoplankton biomass in the frontal regions, neither the role of the front in sustaining this, nor the form of nitrogen used by phytoplankton have been elucidated until now. The studies that form the basis of this paper were designed to address these questions and were carried out in the Iroise inner front located on the Armorican continental shelf and its adjacent sectors (Figure 1). This front, separating the stratified coastal waters of the Douarnenez Bay from the well-mixed offshore waters of the Iroise Sea from June to September is a typical example of a shallow-water front (Morin et al., 1991; 1994). Material and methods Five stations, located on a transect perpendicular to the front (Figure 1), were sampled in July 1992 (RV Pluteus, 1–7 July). In the first instance, samples were collected at each station from five depths chosen after 2000 Academic Press
350 J.-F. Maguer et al.
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F 1. Position of the stations in the study area. U.F—Ushant front; I.F—Iroise inner front.
examining the temperature and salinity profiles and used for the measurements of nutrients, chlorophyll a and particulate organic nitrogen (PON). In the second instance, samples were collected from optical depths corresponding to 100, 50, 22·5, 14·5, 8, 3·5 and 1% of the surface incident radiation and used for measurements of nitrogen (nitrate and ammonium) uptake, ammonium regeneration (at station 2 only), nutrients, chlorophyll a and PON. Uptake kinetics of nitrogenous nutrients as a function of substrate concentrations were studied on samples collected from 50% light depth. Concentrations of nitrate were measured in a Technicon Autoanalyzer (Tre´ guer & Le Corre, 1975) and those of ammonium in triplicate by the indophenol blue method (Koroleff, 1970), with analytical precisions respectively of 0·05 and 0·02 mol l 1. Particulate matter for PON measurements was recovered on pre-ignited (450 C, 4 h) GF/F filter pads and analysed in a Perkin Elmer model 240 elemental analyser with a precision of 0·05 mol l 1. Chlorophyll a concentrations were measured in a Turner designs fluorometer at a precision of 0·05 g l 1. Measurements of uptake () of nitrate and ammonium were made using 15N tracer method (Dugdale & Goering, 1967) on seawater samples pre-filtered through 200 m mesh. Ammonium regeneration was measured by the isotope dilution technique (Harrison, 1978). The 15N tracer, as
Na15NO3 or 15NH4Cl (99 atom % for ammonium and 97·4 atom % for nitrate: CEA, France), was added to the samples, as far as possible, at about 10% of the ambient concentrations but maintaining a minimum addition of 0·05 mol l 1 of nitrate and 0·02 mol l 1 of ammonium. When ambient concentrations are close to detection limits, addition of tracer may cause an increase in the nutrient concentrations in the incubation medium and the uptake rates measured under these conditions would be overestimated (Dugdale & Wilkerson, 1986; Harrison et al., 1996). Immediately after addition of tracer, half of the sample was filtered onto pre-ignited GF/F filter pads to get zero-time enrichment 15N of the particulate and dissolved pools. The remaining fraction was incubated in 2·5 l polycarbonate bottles under simulated in situ conditions for 2–3 h around local noon. The incubation bottles were covered with calibrated nickel screens to reduce the incident PAR to a level equivalent to that prevailing at the sampling depth. The ambient temperature was maintained constant with a continuous flow of seawater. On completion of incubation the particulate matter was recovered on pre-ignited Whatman GF/F filter pads. In the case of incubations with ammonium, the filtrate was also recovered, part of it used immediately for ammonium measurements in triplicate, and the rest stored frozen at 20 C for measurement of isotope ratios. The
Nitrogen uptake by phytoplankton in a shallow water tidal front 351 St5
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F 2. Distribution of temperature in the Iroise inner front in July 1992. Isolines in C.
filters were oven-dried (60 C) and stored in clean plastic vials. All filtrations, including those for recovery of particulate matter for chl a and PON measurements, were carried out under a vacuum of about 100 mm Hg. Ammonium from the filtrate was extracted by diffusion in basic pH (Kristiansen & Paasche, 1989). The 15N:14N isotope ratio of particulate matter as well as that of ammonium recovered from the filtrate was determined by emission spectrometry in a GS1 optical spectrometer (SOPRA, France) following the procedures given by Guiraud and Fardeau (1980). Nitrogen uptake rates were calculated with the equations of Dugdale and Wilkerson (1986) which takes into account the initial PON concentrations. Ammonium uptake rates were not corrected for isotopic dilution due to production of 14N (Glibert et al., 1982b). Ammonium regeneration rates were calculated either by the equation of Glibert et al. (1982b) when ammonium concentration did not change measurably during the incubation, or by that of Laws (1984) when they did. Analytical precisions obtained from seven aliquots taken from a single seawater sample and incubated separately were 4 and 6% respectively for nitrate and ammonium uptake and ammonium regeneration at the level of 10 nmol l 1 h 1.
layers from the underlying cold (<15·5 C) waters and a frontal zone (stations 2, 3 and 4) where the thermocline intersects the surface. The stratification indices (SI=t/h, where t is the difference between surface and bottom densities and h is the depth of the water column) for the well-mixed, stratified and frontal zones were respectively 0·0510 3, 1810 3, 3–910 3 units of t m 1.
Nitrate and ammonium Nitrate and ammonium concentrations in the wellmixed waters (Figure 3(a and b)) were around 1·0 and 0·25 mol l 1, similar to those measured elsewhere in the well-mixed waters of the western English Channel (Wafar et al., 1983). Surface waters of the stratified zone were exhausted of nitrate and ammonium (<0·1 mol l 1). Concentrations of nitrate below the thermocline were low (<1·0 mol l 1) whereas those of ammonium were relatively high (0·6 mol l 1). The nitracline in the frontal zone, like the thermocline, sloped-up towards the surface. Concentrations of nitrate and ammonium in the surface waters of the frontal zone varied from 0·1 to 0·6 mol l 1 and from 0·1 to 0·2 mol l 1 respectively. Below the nitracline, they were relatively low (<1·0 mol l 1 NO3 and <0·3 mol l 1 NH4+ ).
Results Chl a, particulate organic matter (POM) Temperature The vertical distribution of temperature (Figure 2) shows three distinct hydrographic zones: an offshore zone (station 5) where the water column is vertically homogeneous (14·5 C throughout), a coastal zone (station 1) where a shallow thermocline (10–15 m) separates the relatively warm (>17·0 C) surface
Concentrations of chl a were less and homogeneous (1·8 g l 1) in the well-mixed waters, varied from 0·8 to 2·1 g l 1 in the stratified waters (with the higher concentrations located below the thermocline) and were at their maximum (up to 3·4 g l 1) in the frontal zone, located mainly at the level of the thermocline (Figure 4(a)).
352 J.-F. Maguer et al. (a) St5
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St4
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F 3. Distribution of (a) nitrate and (b) ammonium in the Iroise inner front in July 1992. Isolines in mol l 1.
PON concentrations ranged from <2·0 mol l 1 in the well-mixed waters to relatively high values (>3·0 mol l 1) near the front and below the thermocline in the stratified waters (Figure 4(b)). The PON/chl a (Figure 4(c)) and POC/chl a (not shown on the figure) ratios were low (respectively <1·0 mol g 1 and <8·0 mol g 1) in the wellmixed waters and also below the thermocline in the stratified and frontal zones, indicating the importance of phytoplankton as a component of organic matter. Above the thermocline, the ratios were higher and increased rapidly from station 4 (PON/ chl a=1·2 mol g 1; POC/chl a=8·2 mol g 1) to station 1 (PON/chl a=3·2 mol g 1; POC/chl a= 29·0 mol g 1), indicating that the POM was less associated with phytoplankton. The POC/PON ratios also varied similarly, from about 7·0 in the well-mixed waters to >10·0 above the thermocline in the frontal and stratified zones. As the POC/PON ratios of microzooplankton are lower than those of phytoplankton (Goldman et al., 1987; Caron et al., 1988; Stoecker & Capuzzo, 1990), the high POC/PON,
PON/chl a and POC/chl a ratios above the thermocline taken together, therefore, suggests the presence of a large detrital component. Nitrate and ammonium uptake Ammonium uptake varied between 3·2 and 38·1 nmol l 1 h 1 (Figure 5) with higher rates in the frontal (12·5–38·1 nmol l 1 h 1) and stratified (12·2–35·2 nmol l 1 h 1) waters. In these two zones, the high uptake rates were associated with high chl a concentrations. Though generally lower, uptake rates reached up to 23·0 nmol l 1 h 1 at subsurface in the well-mixed waters. Water column-integrated ammonium uptake rates (0·49–1·15 mmol m 2 h 1) were higher in the frontal zone (meanSD= 1·050·12 mmol m 2 h 1) than in the stratified (0·71 mmol m 2 h 1) and the well-mixed (0·49 mmol m 2 h 1) waters (Figure 6). Nitrate uptake rates varied from 2·1 to 26·3 nmol l 1 h 1 (Figure 5). Highest rates were measured in the frontal zone (>26·0 nmol l 1 h 1 at
Nitrogen uptake by phytoplankton in a shallow water tidal front 353 (b)
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F 4. Distribution of (a) chl a (g l 1), (b) PON (mol l 1), (c) PON/chl a (mol N/(g chl a) 1) and (d) POC/PON in the Iroise inner front in July 1992.
Station 5 0
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F 5. Profiles of nitrate (continuous line) and ammonium (broken line) uptake at the 5 stations located on an east-west transect across the front in July 1992. Units in nmol l 1 h 1.
stations 3 and 4), coinciding with the chl a maximum. In the stratified waters, uptake rates were very low (<5·0 nmol l 1 h 1) in the nitrate-depleted surface waters but increased with depth up to the base of the thermocline (12·3 nmol l 1 h 1). In the wellmixed waters also, nitrate uptake was less (<12·2 nmol l 1 h 1) despite the presence of relatively high concentrations of nitrate and decreased from surface with depth. Water column-integrated nitrate uptake rates (Figure 6) were three times higher in the frontal zone (average 0·63 mmol m 2 h 1) than in the stratified (0·25 mmol m 2 h 1) and well-
mixed (0·2 mmol m 2 h 1) waters. The f-ratios (NO3 /(NO3 +NH4+ ) (Eppley & Peterson, 1979) calculated from the integrated values varied from 0·25 to 0·47, with distinctly higher ratios in the frontal zone (Figure 6). The relationship of uptake rates of nitrate and ammonium with the substrate concentrations followed the Mickaelis-Menten kinetics (Figure 7). The max were 18·1 and 30·9 nmol l 1 h 1 respectively for nitrate and ammonium. The Ks values (0·6 and 1·3 mol l 1 respectively) are in the range reported for coastal waters (e.g. Glibert et al., 1982a; Shiomoto
354 J.-F. Maguer et al. Frontal
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F 6. Water column-integrated uptake rates of nitrogen and the f-ratios at the five stations in July 1992. Units in mmol m 2 h 1. Shaded parts: ammonium; open parts: nitrate. Dashed line: f-ratio.
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F 8. Variations of ammonium regeneration (continuous line) and uptake (broken line) rates (nmol l 1 h 1) at a frontal station in July 1992.
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and 43·1 nmol l 1 h 1, increasing with depth to a maximum at the level of the thermocline. Water column-integrated ammonium regeneration rate (1·15 mmol m 2 h 1) was quantitatively equivalent to that of uptake (regeneration/uptake ratio=1·02).
40
Discussion 30
Nitrogen productivity 20 10
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F 7. Variations of uptake rates of nitrate and ammonium (nmol l 1 h 1) as a function of substrate concentrations (mol l 1).
et al., 1994; Chang et al., 1995; Kudela & Cochlan, 2000). Ammonium regeneration by microheterotrophs Ammonium regeneration rates by the microheterotrophs near the front (Figure 8) varied between 12·5
Phytoplankton abundance near the tidal fronts is generally high and may attain extreme values of 50–100 g chl a l 1 in some deep-water fronts (Pingree et al., 1979; Holligan, 1979; Holligan et al., 1984). Such a high concentration may be brought about by mechanical concentration of the cells near the fronts or by vertical migration of some species into the euphotic zone (e.g. Eppley et al., 1968; Olson & Backus, 1985; Brunet et al., 1992; Franks, 1992). A high level of primary production, consequent to an enrichment of the surface waters with nutrients, may also bring about this (Parsons et al., 1984; Videau, 1987; Harrison et al., 1990). The phytoplankton biomass observed near the Iroise inner front (Figure 4(a)) are comparable to those measured in other shallowwater fronts (Pingree et al., 1978; Turley, 1986; Riegman et al., 1990) but are lower, on average, than
Nitrogen uptake by phytoplankton in a shallow water tidal front 355
those recorded from deep-water fronts. This also coincides with high nitrogen uptake, in terms of both absolute (Figure 6) and chlorophyll-specific (0·017– 0·020 mmol (mg chl a) 1 h 1 in the front compared 0·013 and 0·010 mmol (mg chl a) 1 h 1 in stratified and well-mixed waters rates, suggesting that in situ growth, rather than physical processes, maintains the high biomass in this shallow-water front. Regenerated production—ammonium uptake Ammonium uptake rates were distinctly higher in the frontal zone than in the adjacent waters (Figure 6), as were in the nearby Ushant tidal front (Le Corre et al., 1993), though no such differences were noted by Horne et al. (1989) in a similar study in the Georges Bank. As the ammonium uptake indices in the frontal region (0·011–0·012 mmol (mg chl a) 1 h 1) are comparable with those in the stratified (0·010 mmol (mg chl a) 1 h 1) and well-mixed (0·008 mmol (mg chl a) 1 h 1) waters, the high ammonium uptake near the front would correspond therefore mainly to an increase in biomass. The low ambient ammonium concentrations (Figure 3(b)) in the frontal region also suggest that regeneration of ammonium should be rapid enough to support the high uptake rates. The closeness between uptake and regeneration profiles (Figure 8) and the near-unity regeneration/ uptake ratio indicate that it is indeed the case and that the microheterotrophs are responsible for most of the ammonium production. The existence of a large particulate detrital pool, as the high ratios of PON/chl a (Figure 4(c)), POC/chl a and POC/PON (Figure 4(d)) indicate, would have been favourable for ammonium regeneration through the microbial chain. A similar importance of microheterotrophs has also been shown in the Ushant tidal front (Holligan et al., 1984; Le Corre et al., 1993), though mesozooplankton have also been known to be an important source of ammonium in some other fronts (Head et al., 1996). New production—nitrate uptake New production rates were also higher in the frontal zone (Figure 6). Unlike the case with ammonium however, the uptake indices in the frontal zone (0·010 mmol (mg chl a) 1 h 1 at station 4) were up to three times higher than in the adjacent waters (0·003 mmol (mg chl a) 1 h 1), indicating that the conditions were more favourable for uptake of nitrate in the frontal zone. This can be traced to a combination of factors. In the well-mixed waters, injection of nitrate by vertical mixing is continuous into the surface waters, raising the ambient nitrate to con-
centrations higher than the Ks. Nevertheless, because of constant mixing, the phytoplankton cells also get transported to different levels of light within the water column. The mean light energy available for photosynthesis thus becomes reduced and the uptake of nitrate, which is strongly dependent on light intensity (MacIsaac & Dugdale, 1972), becomes light-limited (L’Helguen et al., 1996). In the stratified waters, nitrate uptake is substrate-limited, since the stability (SI=1810 3 units of t m 1) restricts vertical transfer of nitrate across the thermocline, leading to concentrations of nitrate (<0·2 mol l 1) much lower than the Ks in the surface waters. The presence of nitrate in the surface waters at concentrations near Ks and the relatively high stability of the water column (SI=3–910 3 units of t m 1) on the other hand, would together account for the higher utilization of nitrate in the frontal zone. Both the new production rates and their proportion in total production in the frontal zone were lower than in several other deep-water fronts (1– 1·5 mmol m 2 h 1; f-ratios 0·6–0·9) (Parsons et al., 1984; Price et al., 1985; Harrison & Wood, 1988; Horne et al., 1989). This is directly related to the abundance of nitrate available for uptake and its supply into the surface waters. Nitrate supply to the tidally-generated thermal fronts results from different physical mechanisms (Loder & Platt, 1985) and intensification of vertical mixing during spring tides is an important one among them (Pingree et al., 1979; Loder & Platt, 1985; Horne et al., 1996). At this time, the cold layer located below the thermocline in the stratified sector gets eroded, leading to vertical transport of nitrate into the frontal zone (Morin et al., 1994). Since nitrate reserves below the thermocline near the deep-water front are usually high—up to 7–8 mol l 1 (Horne et al., 1989; Morin et al., 1993)—vertical mixing can raise nitrate concentrations in the euphotic zone of these fronts to more than 3–4 mol l 1 (Horne et al., 1989; Morin et al., 1993; Townsend & Pettigrew, 1997). In the case of the Iroise inner front, the shallow depths of the stratified sector and the extension of the euphotic zone down to the bottom are conducive to removal of nitrate also below the thermocline, leading thus very low residual (<1·0 mol l 1; Figure 3(a)) nitrate concentrations in summer. Consequently, the enrichment of the front with nitrate becomes only modest and the surface concentrations remain very low (maximum of 0·6 mol l 1). Limitation by substrate availability may also have become accentuated by the presence of ammonium in relatively high proportions (25–36% of nitrate+ammonium) in the front compared with adjacent waters. Ammonium is generally more
356 J.-F. Maguer et al.
preferred by phytoplankton (Dortch, 1990) and at the concentrations it was present in the frontal zone (0·1–0·3 mol l 1) may have inhibited nitrate uptake (Wheeler & Kokkinakis, 1990).
Conclusion The Iroise inner front was characterized by high phytoplankton biomass compared with the adjacent stratified and well-mixed waters. Nitrogen uptake, both in terms of absolute rates and assimilation indices, were high in the frontal zone, suggesting that in situ growth rather than accumulation by physical processes is the cause for this. Uptake rates of both ammonium and nitrate were high, the former sustained by an intense ammonium regeneration by microheterotrophs and the latter, by nitrate supply through vertical mixing. Enrichment of surface waters with nitrate was, however, modest because of the low nitrate concentrations below the thermocline. This fact, along with the ensuing relatively lesser nitrogen production and the f-ratio, differentiates the Iroise inner front from the deep-water tidal fronts. References Brunet, J. M., Brylinski, J. M. & Frontier, S. 1992 Productivity, photosynthetic pigments and hydrology in the coastal front of the Eastern English Channel. Journal of Plankton Research 14, 1541–1552. Caron, D. A., Goldman, J. C. & Dennett, M. R. 1988 Experimental demonstration of the roles of bacteria and bacterivorous protozoa in plankton nutrient cycles. Hydrobiologia 159, 27–40. Chang, F. H., Bradford-Grieve, J. M., Vincent, W. F. & Wood, P. H. 1995 Nitrogen uptake by summer size-fractionated phytoplankton assemblages in the Westland, New Zealand, upwelling system,. New Zealand Journal Marine Freshwater Research 29, 147–161. Dortch, Q. 1990 The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series 61, 183–201. Dugdale, R. C. & Goering, J. J. 1967 Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12, 196–206. Dugdale, R. C. & Wilkerson, F. P. 1986 The use of 15N to measure nitrogen uptake in eutrophic oceans; experimental considerations. Limnology and Oceanography 31, 673–689. Eppley, R. W., Holm Hansen, O. & Strickland, J. D. H. 1968 Some observations on the vertical migration of dinoflagellates. Journal of Phycology 4, 57–64. Eppley, R. W. & Peterson, B. J. 1979 Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 377–680. Franks, P. J. S. 1992 Sink or swim: accumulation of biomass at fronts. Marine Ecology Progress Series 82, 1–12. Glibert, P. M., Goldman, J. C. & Carpenter, E. J. 1982a Seasonal variations in the utilization of ammonium and nitrate by phytoplankton in Vineyard Sound, Massachusetts, USA. Marine Biology 70, 237–249. Glibert, P. M., Lipschultz, F., McCarthy, J. J. & Altabet, M. A. 1982b Isotope dilution models of uptake and ammonium by marine plankton. Limnology and Oceanography 27, 639–650.
Goldman, J. G., Caron, D. A. & Dennet, M. R. 1987 Nutrient cycling in a microflagellate food chain: IV. Phytoplanktonmicroflagellate interactions. Marine Ecology Progress Series 38, 75–87. Group Grepma 1988 A physical and biological characterization of the Ushant front. Internationale Revue Gesamte Hydrobiologie 73, 511–536. Guiraud, G. & Fardeau, J. C. 1980 De´ termination isotopique par spectrome´ trie optique de compose´ s faiblement enrichis en azote15. Analusis 8, 148–152. Harrison, W. G. 1978 Experimental measurements of nitrogen remineralization in coastal waters. Limnology and Oceanography 23, 684–694. Harrison, W. G., Harris, L. R. & Irwin, B. D. 1996 The kinetics of nitrogen utilization in the oceanic mixed layer: nitrate and ammonium interactions and nanomolar concentrations. Limnology and Oceanography 41, 16–32. Harrison, W. G., Horne, E. P. W., Irwin, B. & Platt, T. 1990 Biological production on Georges Bank: are tidal fronts primary sources of new production in summer? EOS 71, 96. Harrison, W. G. & Wood, L. J. E. 1988 Inorganic nitrogen uptake by marine phytoplankton: evidence of size partitioning. Limnology and Oceanography 33, 468–475. Head, E. J. H., Harrison, W. G., Irwin, B. I., Horne, E. P. W. & Li, W. K. W. 1996 Plankton dynamics and carbon flux in an area of upwelling off the coast of Morocco. Deep-Sea Research I 43, 1713–1738. Holligan, P. M. 1979 Dinoflagellate blooms associated with tidal fronts around the British Isles. In Toxic Dinoflagellate Blooms (Taylor, D. C. & Seliger, H. H., eds). Elsevier, New York, pp. 249–256. Holligan, P. M., leB Williams, P. J., Purdie, D. & Harris, R. P. 1984 Photosynthesis, respiration and nitrogen supply of plankton populations in stratified, frontal and tidally mixed shelf waters. Marine Ecology Progress Series 17, 201–213. Horne, E. P. W., Loder, J. W., Harrison, W. G., Mohn, R., Lewis, M. R., Irwin, B. & Platt, T. 1989 Nitrate supply and demand at the Georges Bank tidal front. Topics in Marine Biology. (Ros, J. D., ed.) Scientia Marina 53, 145–158. Horne, E. P. W., Loder, J. W., Naimie, C. E. & Oakey, N. S. 1996 Turbulence dissipation rates and nitrate supply in the upper water column on Georges Bank. Deep-Sea Research II 43, 1683–1712. Koroleff, F. 1970 Direct determination of ammonia in natural waters as indophenol blue. International Council for the Exploration of the Sea 9, 19–22. Kristiansen, S. & Paasche, E. 1989 An improved method for determining relative 15N abundance in ammonium regeneration studies by direct diffusion. Marine Ecology Progress Series 54, 203–207. Kudela, R. M. & Cochlan, W. P. 2000 Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California. Aquatic Microbial Ecology 21, 31–47. Laws, E. A. 1984 Isotope dilution models and the mystery of vanishing 15N. Limnology and Oceanography 29, 379–386. Le Corre, P., L’Helguen, S. & Wafar, M. 1993 Nitrogen source for uptake by Gyrodinium cf. aureolum in a tidal front. Limnology and Oceanography 38, 446–451. L’Helguen, S., Madec, C. & Le Corre, P. 1996 Nitrogen uptake in permanently well-mixed temperate coastal waters. Estuarine, Coastal and Shelf Science 42, 803–818. Loder, J. W. & Platt, T. 1985 Physical controls on phytoplankton production at tidal fronts. In Proceedings, 19th European Marine Biology symposium (Gibbs, P. E., ed.). Cambridge University Press, Cambridge, U.K., pp. 3–21. MacIsaac, J. J. & Dugdale, D. C. 1972 Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Research 19, 209–232. Morin, P., Birrien, J. L. & Le Corre, P. 1989 The frontal systems in the Iroise Sea: Development of Gyrodinium aureolum Hulburt on
Nitrogen uptake by phytoplankton in a shallow water tidal front 357 the inner front. Topics in Marine Biology (Ros, J. D., ed.) Scientia Marina 53, 215–221. Morin, P., Connan, O. & Le Corre, P. 1994 Fronts thermiques de mare´ e: Cas des fronts de Manche Occidentale et de la mer Celtique. Oceanis 20, 21–43. Morin, P., Le Corre, P., Marty, Y. & L’Helguen, S. 1991 Evolution printanie`re des e´ le´ ments nutritifs et du phytoplancton sur le plateau continental armoricain (Europe du Nord Ouest). Oceanologica Acta 14, 263–279. Morin, P., Wafar, M. V. M. & Le Corre, P. 1993 Estimation of nitrate flux in a tidal front from satellite derived temperature data. Journal of Geophysical Research 98, 4689–4695. Olson, D. B. & Backus, R. H. 1985 The concentrating of organisms at fronts. Journal of Marine Biology Association U.K. 43, 113–137. Parsons, T. R., Dovey, H. M., Cochlan, W. P., Perry, R. I. & Crean, P. B. 1984 Frontal zone analysis at the mouth of a fjord—Jervis Inlet, British Columbia. Sarsia 69, 133–137. Parsons, T. R., Perry, R. I., Nutbrown, E. D., Hsieh, W. & Lalli, C. M. 1983 Frontal zone analysis at the mouth of Saanich Inlet, British Columbia, Canada. Marine Biology 73, 1–5. Pingree, R. D. & Griffiths, D. K. 1978 Tidal fronts on the shelf seas around the British Isles. Journal of Geophysical Research 83, 4615–4622. Pingree, R. D., Holligan, P. M. & Mardell, G. T. 1978 The effects of vertical stability on phytoplankton distribution in the summer on the northwest European shelf. Deep-Sea Research 25, 1011–1028. Pingree, R. D., Holligan, P. M. & Mardell, G. T. 1979 Phytoplankton growth and cyclonic eddies. Nature 5701, 245–247. Pingree, R. D., Mardell, G. T. & Maddock, L. 1983 Marginal front in Lyme Bay. Journal of Marine Biology Association U.K. 63, 9–15. Pingree, R. D., Pugh, P. R., Holligan, P. M. & Forster, G. R. 1975 Summer phytoplankton blooms and red tides along tidal fronts in the approaches to the English Channel. Nature 258, 672–677.
Price, N. M., Cochlan, W. P. & Harrison, P. J. 1985 Time course of uptake of inorganic and organic nitrogen by phytoplankton in the strait of Georgia: Comparison of frontal and stratified communities. Marine Ecology Progress Series 27, 39–53. Riegman, R., Malshaert, H. & Colijn, F. 1990 Primary production of phytoplankton at a frontal zone located at the northern slope of Dogger Bank (North Sea). Marine Biology 105, 329–336. Shiomoto, A., Sasaki, K., Shimoda, T. & Matsumura, S. 1994 Kinetics of nitrate and ammonium uptake by the natural populations of marine phytoplankton in the surface water of the Oyashio region during spring and summer. Journal of Oceanography 50, 515–529. Stoecker, J. K. & Capuzzo, J. M. 1990 Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908. Townsend, D. W. & Pettigrew, N. R. 1997 Nitrogen limitation of secondary production on Georges Bank. Journal of Plankton Research 19, 221–235. Tre´ guer, P. & Le Corre, P. 1975 Manuel d’analyse des sels nutritifs dans l’eau de mer (Utilisation de l’Autoanalyseur II Technicon), seconde e´ dition. Universite´ de Bretagne Occidentale, 110 pp. Turley, C. M. 1986 Urea uptake by phytoplankton at different fronts and associated stratified and mixed waters on the European shelf. British Phycological Journal 21, 225–238. Videau, C. 1987 Primary production and physiological state of phytoplankton at the Ushant tidal front (west coast of Brittany, France). Marine Ecology Progress Series 35, 141–151. Wafar, M. V. M., Le Corre, P. & Birrien, J. L. 1983 Nutrient and primary production in permanently well mixed temperate coastal waters. Estuarine Coastal and Shelf Science 17, 431–446. Wheeler, P. M. & Kokkinakis, S. A. 1990 Ammonium recycling limits nitrate use in the oceanic subarctic Pacific. Limnology and Oceanography 35, 1267–1278.
Nitrogen Uptake by Phytoplankton in a Shallow Water Tidal Front J.-F. Maguera, S. L’Helguen and P. Le Corre Laboratoire de Chimie Marine, Universite´ de Bretagne Occidentale et U.P.R. 9042 C.N.R.S. Roscoff, Place Nicolas Copernic, Technopoˆle Brest-Iroise, F-29280 Plouzane, France Received 2 February 2000 and accepted in revised form 29 May 2000 Nitrogen uptake by phytoplankton was studied in a shallow water tidal front and its adjacent stratified and well-mixed sectors on the Armorican shelf (north-west Europe) in July 1992. The front was characterized by relatively high phytoplankton biomass (>3·4 g l 1) and high ammonium and nitrate uptake rates (1·05 and 0·63 mmol m 2 h 1 respectively) compared with the stratified (0·71 and 0·21 mmol m 2 h 1) and well-mixed (0·49 and 0·25 mmol m 2 h 1) waters. Ammonium regeneration rates at the front were of the same order as ammonium uptake rates indicating intense recycling of nitrogen by microheterotrophs. The high total nitrogen uptake, in terms of both absolute and chlorophyll-specific rates, in the front suggests that in situ growth, rather than physical processes, is the main cause of phytoplankton abundance in the front. Despite high nitrate uptake rates, the f-ratios (NO3 /(NO3 +NH4+ )) were lower than in the deep water tidal fronts, because of low nitrate concentrations below the thermocline. 2000 Academic Press Keywords: nitrogen uptake; f-ratio; tidal front; continental shelf; north-west Europe
Introduction Tidally-generated thermal fronts separating nutrientdepleted warm stratified waters from nutrient-rich cold well-mixed waters on the continental shelves of the north-western Europe are a regular phenomenon during summer (Pingree & Griffiths, 1978). Two types of fronts, according to the depth of the water column, can be distinguished (Pingree et al., 1978). In the deep-water fronts, the depth of the water column is greater than that of the euphotic zone and the nutrient stock below the thermocline remains high even during summer. In the shallow-water fronts, on the other hand, the euphotic zone extends up to the bottom and the whole water column tends to become nutrient-depleted at this time. Chemical and biological processes in the deepwater fronts have been fairly well studied (Pingree et al., 1975; Holligan, 1979; Holligan et al., 1984; Group Grepma, 1988; Harrison & Wood, 1988). The primary production rates in these fronts, in terms of carbon (Parsons et al., 1983; Videau, 1987) and nitrogen (Horne et al., 1989; Harrison et al., 1990; Le Corre et al., 1993), have been shown to be usually high. Such high production rates have been generally ascribed to increased vertical transfer of nitrate at the front and corresponds, therefore, to a higher fraction a
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of new production (Horne et al., 1989; Morin et al., 1993). In some instances, they are also related to intense nitrogen regeneration within the euphotic zone, leading to an increased proportion of regenerated production (Le Corre et al., 1993). Studies on shallow-water fronts are less numerous (Pingree et al., 1978, 1983; Turley, 1986; Morin et al., 1989; Riegman et al., 1990). Though these studies also have shown increase in phytoplankton biomass in the frontal regions, neither the role of the front in sustaining this, nor the form of nitrogen used by phytoplankton have been elucidated until now. The studies that form the basis of this paper were designed to address these questions and were carried out in the Iroise inner front located on the Armorican continental shelf and its adjacent sectors (Figure 1). This front, separating the stratified coastal waters of the Douarnenez Bay from the well-mixed offshore waters of the Iroise Sea from June to September is a typical example of a shallow-water front (Morin et al., 1991; 1994). Material and methods Five stations, located on a transect perpendicular to the front (Figure 1), were sampled in July 1992 (RV Pluteus, 1–7 July). In the first instance, samples were collected at each station from five depths chosen after 2000 Academic Press
350 J.-F. Maguer et al.
48°40 N
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F 1. Position of the stations in the study area. U.F—Ushant front; I.F—Iroise inner front.
examining the temperature and salinity profiles and used for the measurements of nutrients, chlorophyll a and particulate organic nitrogen (PON). In the second instance, samples were collected from optical depths corresponding to 100, 50, 22·5, 14·5, 8, 3·5 and 1% of the surface incident radiation and used for measurements of nitrogen (nitrate and ammonium) uptake, ammonium regeneration (at station 2 only), nutrients, chlorophyll a and PON. Uptake kinetics of nitrogenous nutrients as a function of substrate concentrations were studied on samples collected from 50% light depth. Concentrations of nitrate were measured in a Technicon Autoanalyzer (Tre´ guer & Le Corre, 1975) and those of ammonium in triplicate by the indophenol blue method (Koroleff, 1970), with analytical precisions respectively of 0·05 and 0·02 mol l 1. Particulate matter for PON measurements was recovered on pre-ignited (450 C, 4 h) GF/F filter pads and analysed in a Perkin Elmer model 240 elemental analyser with a precision of 0·05 mol l 1. Chlorophyll a concentrations were measured in a Turner designs fluorometer at a precision of 0·05 g l 1. Measurements of uptake () of nitrate and ammonium were made using 15N tracer method (Dugdale & Goering, 1967) on seawater samples pre-filtered through 200 m mesh. Ammonium regeneration was measured by the isotope dilution technique (Harrison, 1978). The 15N tracer, as
Na15NO3 or 15NH4Cl (99 atom % for ammonium and 97·4 atom % for nitrate: CEA, France), was added to the samples, as far as possible, at about 10% of the ambient concentrations but maintaining a minimum addition of 0·05 mol l 1 of nitrate and 0·02 mol l 1 of ammonium. When ambient concentrations are close to detection limits, addition of tracer may cause an increase in the nutrient concentrations in the incubation medium and the uptake rates measured under these conditions would be overestimated (Dugdale & Wilkerson, 1986; Harrison et al., 1996). Immediately after addition of tracer, half of the sample was filtered onto pre-ignited GF/F filter pads to get zero-time enrichment 15N of the particulate and dissolved pools. The remaining fraction was incubated in 2·5 l polycarbonate bottles under simulated in situ conditions for 2–3 h around local noon. The incubation bottles were covered with calibrated nickel screens to reduce the incident PAR to a level equivalent to that prevailing at the sampling depth. The ambient temperature was maintained constant with a continuous flow of seawater. On completion of incubation the particulate matter was recovered on pre-ignited Whatman GF/F filter pads. In the case of incubations with ammonium, the filtrate was also recovered, part of it used immediately for ammonium measurements in triplicate, and the rest stored frozen at 20 C for measurement of isotope ratios. The
Nitrogen uptake by phytoplankton in a shallow water tidal front 351 St5
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F 2. Distribution of temperature in the Iroise inner front in July 1992. Isolines in C.
filters were oven-dried (60 C) and stored in clean plastic vials. All filtrations, including those for recovery of particulate matter for chl a and PON measurements, were carried out under a vacuum of about 100 mm Hg. Ammonium from the filtrate was extracted by diffusion in basic pH (Kristiansen & Paasche, 1989). The 15N:14N isotope ratio of particulate matter as well as that of ammonium recovered from the filtrate was determined by emission spectrometry in a GS1 optical spectrometer (SOPRA, France) following the procedures given by Guiraud and Fardeau (1980). Nitrogen uptake rates were calculated with the equations of Dugdale and Wilkerson (1986) which takes into account the initial PON concentrations. Ammonium uptake rates were not corrected for isotopic dilution due to production of 14N (Glibert et al., 1982b). Ammonium regeneration rates were calculated either by the equation of Glibert et al. (1982b) when ammonium concentration did not change measurably during the incubation, or by that of Laws (1984) when they did. Analytical precisions obtained from seven aliquots taken from a single seawater sample and incubated separately were 4 and 6% respectively for nitrate and ammonium uptake and ammonium regeneration at the level of 10 nmol l 1 h 1.
layers from the underlying cold (<15·5 C) waters and a frontal zone (stations 2, 3 and 4) where the thermocline intersects the surface. The stratification indices (SI=t/h, where t is the difference between surface and bottom densities and h is the depth of the water column) for the well-mixed, stratified and frontal zones were respectively 0·0510 3, 1810 3, 3–910 3 units of t m 1.
Nitrate and ammonium Nitrate and ammonium concentrations in the wellmixed waters (Figure 3(a and b)) were around 1·0 and 0·25 mol l 1, similar to those measured elsewhere in the well-mixed waters of the western English Channel (Wafar et al., 1983). Surface waters of the stratified zone were exhausted of nitrate and ammonium (<0·1 mol l 1). Concentrations of nitrate below the thermocline were low (<1·0 mol l 1) whereas those of ammonium were relatively high (0·6 mol l 1). The nitracline in the frontal zone, like the thermocline, sloped-up towards the surface. Concentrations of nitrate and ammonium in the surface waters of the frontal zone varied from 0·1 to 0·6 mol l 1 and from 0·1 to 0·2 mol l 1 respectively. Below the nitracline, they were relatively low (<1·0 mol l 1 NO3 and <0·3 mol l 1 NH4+ ).
Results Chl a, particulate organic matter (POM) Temperature The vertical distribution of temperature (Figure 2) shows three distinct hydrographic zones: an offshore zone (station 5) where the water column is vertically homogeneous (14·5 C throughout), a coastal zone (station 1) where a shallow thermocline (10–15 m) separates the relatively warm (>17·0 C) surface
Concentrations of chl a were less and homogeneous (1·8 g l 1) in the well-mixed waters, varied from 0·8 to 2·1 g l 1 in the stratified waters (with the higher concentrations located below the thermocline) and were at their maximum (up to 3·4 g l 1) in the frontal zone, located mainly at the level of the thermocline (Figure 4(a)).
352 J.-F. Maguer et al. (a) St5
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F 3. Distribution of (a) nitrate and (b) ammonium in the Iroise inner front in July 1992. Isolines in mol l 1.
PON concentrations ranged from <2·0 mol l 1 in the well-mixed waters to relatively high values (>3·0 mol l 1) near the front and below the thermocline in the stratified waters (Figure 4(b)). The PON/chl a (Figure 4(c)) and POC/chl a (not shown on the figure) ratios were low (respectively <1·0 mol g 1 and <8·0 mol g 1) in the wellmixed waters and also below the thermocline in the stratified and frontal zones, indicating the importance of phytoplankton as a component of organic matter. Above the thermocline, the ratios were higher and increased rapidly from station 4 (PON/ chl a=1·2 mol g 1; POC/chl a=8·2 mol g 1) to station 1 (PON/chl a=3·2 mol g 1; POC/chl a= 29·0 mol g 1), indicating that the POM was less associated with phytoplankton. The POC/PON ratios also varied similarly, from about 7·0 in the well-mixed waters to >10·0 above the thermocline in the frontal and stratified zones. As the POC/PON ratios of microzooplankton are lower than those of phytoplankton (Goldman et al., 1987; Caron et al., 1988; Stoecker & Capuzzo, 1990), the high POC/PON,
PON/chl a and POC/chl a ratios above the thermocline taken together, therefore, suggests the presence of a large detrital component. Nitrate and ammonium uptake Ammonium uptake varied between 3·2 and 38·1 nmol l 1 h 1 (Figure 5) with higher rates in the frontal (12·5–38·1 nmol l 1 h 1) and stratified (12·2–35·2 nmol l 1 h 1) waters. In these two zones, the high uptake rates were associated with high chl a concentrations. Though generally lower, uptake rates reached up to 23·0 nmol l 1 h 1 at subsurface in the well-mixed waters. Water column-integrated ammonium uptake rates (0·49–1·15 mmol m 2 h 1) were higher in the frontal zone (meanSD= 1·050·12 mmol m 2 h 1) than in the stratified (0·71 mmol m 2 h 1) and the well-mixed (0·49 mmol m 2 h 1) waters (Figure 6). Nitrate uptake rates varied from 2·1 to 26·3 nmol l 1 h 1 (Figure 5). Highest rates were measured in the frontal zone (>26·0 nmol l 1 h 1 at
Nitrogen uptake by phytoplankton in a shallow water tidal front 353 (b)
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F 4. Distribution of (a) chl a (g l 1), (b) PON (mol l 1), (c) PON/chl a (mol N/(g chl a) 1) and (d) POC/PON in the Iroise inner front in July 1992.
Station 5 0
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F 5. Profiles of nitrate (continuous line) and ammonium (broken line) uptake at the 5 stations located on an east-west transect across the front in July 1992. Units in nmol l 1 h 1.
stations 3 and 4), coinciding with the chl a maximum. In the stratified waters, uptake rates were very low (<5·0 nmol l 1 h 1) in the nitrate-depleted surface waters but increased with depth up to the base of the thermocline (12·3 nmol l 1 h 1). In the wellmixed waters also, nitrate uptake was less (<12·2 nmol l 1 h 1) despite the presence of relatively high concentrations of nitrate and decreased from surface with depth. Water column-integrated nitrate uptake rates (Figure 6) were three times higher in the frontal zone (average 0·63 mmol m 2 h 1) than in the stratified (0·25 mmol m 2 h 1) and well-
mixed (0·2 mmol m 2 h 1) waters. The f-ratios (NO3 /(NO3 +NH4+ ) (Eppley & Peterson, 1979) calculated from the integrated values varied from 0·25 to 0·47, with distinctly higher ratios in the frontal zone (Figure 6). The relationship of uptake rates of nitrate and ammonium with the substrate concentrations followed the Mickaelis-Menten kinetics (Figure 7). The max were 18·1 and 30·9 nmol l 1 h 1 respectively for nitrate and ammonium. The Ks values (0·6 and 1·3 mol l 1 respectively) are in the range reported for coastal waters (e.g. Glibert et al., 1982a; Shiomoto
354 J.-F. Maguer et al. Frontal
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F 6. Water column-integrated uptake rates of nitrogen and the f-ratios at the five stations in July 1992. Units in mmol m 2 h 1. Shaded parts: ammonium; open parts: nitrate. Dashed line: f-ratio.
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F 8. Variations of ammonium regeneration (continuous line) and uptake (broken line) rates (nmol l 1 h 1) at a frontal station in July 1992.
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and 43·1 nmol l 1 h 1, increasing with depth to a maximum at the level of the thermocline. Water column-integrated ammonium regeneration rate (1·15 mmol m 2 h 1) was quantitatively equivalent to that of uptake (regeneration/uptake ratio=1·02).
40
Discussion 30
Nitrogen productivity 20 10
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F 7. Variations of uptake rates of nitrate and ammonium (nmol l 1 h 1) as a function of substrate concentrations (mol l 1).
et al., 1994; Chang et al., 1995; Kudela & Cochlan, 2000). Ammonium regeneration by microheterotrophs Ammonium regeneration rates by the microheterotrophs near the front (Figure 8) varied between 12·5
Phytoplankton abundance near the tidal fronts is generally high and may attain extreme values of 50–100 g chl a l 1 in some deep-water fronts (Pingree et al., 1979; Holligan, 1979; Holligan et al., 1984). Such a high concentration may be brought about by mechanical concentration of the cells near the fronts or by vertical migration of some species into the euphotic zone (e.g. Eppley et al., 1968; Olson & Backus, 1985; Brunet et al., 1992; Franks, 1992). A high level of primary production, consequent to an enrichment of the surface waters with nutrients, may also bring about this (Parsons et al., 1984; Videau, 1987; Harrison et al., 1990). The phytoplankton biomass observed near the Iroise inner front (Figure 4(a)) are comparable to those measured in other shallowwater fronts (Pingree et al., 1978; Turley, 1986; Riegman et al., 1990) but are lower, on average, than
Nitrogen uptake by phytoplankton in a shallow water tidal front 355
those recorded from deep-water fronts. This also coincides with high nitrogen uptake, in terms of both absolute (Figure 6) and chlorophyll-specific (0·017– 0·020 mmol (mg chl a) 1 h 1 in the front compared 0·013 and 0·010 mmol (mg chl a) 1 h 1 in stratified and well-mixed waters rates, suggesting that in situ growth, rather than physical processes, maintains the high biomass in this shallow-water front. Regenerated production—ammonium uptake Ammonium uptake rates were distinctly higher in the frontal zone than in the adjacent waters (Figure 6), as were in the nearby Ushant tidal front (Le Corre et al., 1993), though no such differences were noted by Horne et al. (1989) in a similar study in the Georges Bank. As the ammonium uptake indices in the frontal region (0·011–0·012 mmol (mg chl a) 1 h 1) are comparable with those in the stratified (0·010 mmol (mg chl a) 1 h 1) and well-mixed (0·008 mmol (mg chl a) 1 h 1) waters, the high ammonium uptake near the front would correspond therefore mainly to an increase in biomass. The low ambient ammonium concentrations (Figure 3(b)) in the frontal region also suggest that regeneration of ammonium should be rapid enough to support the high uptake rates. The closeness between uptake and regeneration profiles (Figure 8) and the near-unity regeneration/ uptake ratio indicate that it is indeed the case and that the microheterotrophs are responsible for most of the ammonium production. The existence of a large particulate detrital pool, as the high ratios of PON/chl a (Figure 4(c)), POC/chl a and POC/PON (Figure 4(d)) indicate, would have been favourable for ammonium regeneration through the microbial chain. A similar importance of microheterotrophs has also been shown in the Ushant tidal front (Holligan et al., 1984; Le Corre et al., 1993), though mesozooplankton have also been known to be an important source of ammonium in some other fronts (Head et al., 1996). New production—nitrate uptake New production rates were also higher in the frontal zone (Figure 6). Unlike the case with ammonium however, the uptake indices in the frontal zone (0·010 mmol (mg chl a) 1 h 1 at station 4) were up to three times higher than in the adjacent waters (0·003 mmol (mg chl a) 1 h 1), indicating that the conditions were more favourable for uptake of nitrate in the frontal zone. This can be traced to a combination of factors. In the well-mixed waters, injection of nitrate by vertical mixing is continuous into the surface waters, raising the ambient nitrate to con-
centrations higher than the Ks. Nevertheless, because of constant mixing, the phytoplankton cells also get transported to different levels of light within the water column. The mean light energy available for photosynthesis thus becomes reduced and the uptake of nitrate, which is strongly dependent on light intensity (MacIsaac & Dugdale, 1972), becomes light-limited (L’Helguen et al., 1996). In the stratified waters, nitrate uptake is substrate-limited, since the stability (SI=1810 3 units of t m 1) restricts vertical transfer of nitrate across the thermocline, leading to concentrations of nitrate (<0·2 mol l 1) much lower than the Ks in the surface waters. The presence of nitrate in the surface waters at concentrations near Ks and the relatively high stability of the water column (SI=3–910 3 units of t m 1) on the other hand, would together account for the higher utilization of nitrate in the frontal zone. Both the new production rates and their proportion in total production in the frontal zone were lower than in several other deep-water fronts (1– 1·5 mmol m 2 h 1; f-ratios 0·6–0·9) (Parsons et al., 1984; Price et al., 1985; Harrison & Wood, 1988; Horne et al., 1989). This is directly related to the abundance of nitrate available for uptake and its supply into the surface waters. Nitrate supply to the tidally-generated thermal fronts results from different physical mechanisms (Loder & Platt, 1985) and intensification of vertical mixing during spring tides is an important one among them (Pingree et al., 1979; Loder & Platt, 1985; Horne et al., 1996). At this time, the cold layer located below the thermocline in the stratified sector gets eroded, leading to vertical transport of nitrate into the frontal zone (Morin et al., 1994). Since nitrate reserves below the thermocline near the deep-water front are usually high—up to 7–8 mol l 1 (Horne et al., 1989; Morin et al., 1993)—vertical mixing can raise nitrate concentrations in the euphotic zone of these fronts to more than 3–4 mol l 1 (Horne et al., 1989; Morin et al., 1993; Townsend & Pettigrew, 1997). In the case of the Iroise inner front, the shallow depths of the stratified sector and the extension of the euphotic zone down to the bottom are conducive to removal of nitrate also below the thermocline, leading thus very low residual (<1·0 mol l 1; Figure 3(a)) nitrate concentrations in summer. Consequently, the enrichment of the front with nitrate becomes only modest and the surface concentrations remain very low (maximum of 0·6 mol l 1). Limitation by substrate availability may also have become accentuated by the presence of ammonium in relatively high proportions (25–36% of nitrate+ammonium) in the front compared with adjacent waters. Ammonium is generally more
356 J.-F. Maguer et al.
preferred by phytoplankton (Dortch, 1990) and at the concentrations it was present in the frontal zone (0·1–0·3 mol l 1) may have inhibited nitrate uptake (Wheeler & Kokkinakis, 1990).
Conclusion The Iroise inner front was characterized by high phytoplankton biomass compared with the adjacent stratified and well-mixed waters. Nitrogen uptake, both in terms of absolute rates and assimilation indices, were high in the frontal zone, suggesting that in situ growth rather than accumulation by physical processes is the cause for this. Uptake rates of both ammonium and nitrate were high, the former sustained by an intense ammonium regeneration by microheterotrophs and the latter, by nitrate supply through vertical mixing. Enrichment of surface waters with nitrate was, however, modest because of the low nitrate concentrations below the thermocline. This fact, along with the ensuing relatively lesser nitrogen production and the f-ratio, differentiates the Iroise inner front from the deep-water tidal fronts. References Brunet, J. M., Brylinski, J. M. & Frontier, S. 1992 Productivity, photosynthetic pigments and hydrology in the coastal front of the Eastern English Channel. Journal of Plankton Research 14, 1541–1552. Caron, D. A., Goldman, J. C. & Dennett, M. R. 1988 Experimental demonstration of the roles of bacteria and bacterivorous protozoa in plankton nutrient cycles. Hydrobiologia 159, 27–40. Chang, F. H., Bradford-Grieve, J. M., Vincent, W. F. & Wood, P. H. 1995 Nitrogen uptake by summer size-fractionated phytoplankton assemblages in the Westland, New Zealand, upwelling system,. New Zealand Journal Marine Freshwater Research 29, 147–161. Dortch, Q. 1990 The interaction between ammonium and nitrate uptake in phytoplankton. Marine Ecology Progress Series 61, 183–201. Dugdale, R. C. & Goering, J. J. 1967 Uptake of new and regenerated forms of nitrogen in primary productivity. Limnology and Oceanography 12, 196–206. Dugdale, R. C. & Wilkerson, F. P. 1986 The use of 15N to measure nitrogen uptake in eutrophic oceans; experimental considerations. Limnology and Oceanography 31, 673–689. Eppley, R. W., Holm Hansen, O. & Strickland, J. D. H. 1968 Some observations on the vertical migration of dinoflagellates. Journal of Phycology 4, 57–64. Eppley, R. W. & Peterson, B. J. 1979 Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282, 377–680. Franks, P. J. S. 1992 Sink or swim: accumulation of biomass at fronts. Marine Ecology Progress Series 82, 1–12. Glibert, P. M., Goldman, J. C. & Carpenter, E. J. 1982a Seasonal variations in the utilization of ammonium and nitrate by phytoplankton in Vineyard Sound, Massachusetts, USA. Marine Biology 70, 237–249. Glibert, P. M., Lipschultz, F., McCarthy, J. J. & Altabet, M. A. 1982b Isotope dilution models of uptake and ammonium by marine plankton. Limnology and Oceanography 27, 639–650.
Goldman, J. G., Caron, D. A. & Dennet, M. R. 1987 Nutrient cycling in a microflagellate food chain: IV. Phytoplanktonmicroflagellate interactions. Marine Ecology Progress Series 38, 75–87. Group Grepma 1988 A physical and biological characterization of the Ushant front. Internationale Revue Gesamte Hydrobiologie 73, 511–536. Guiraud, G. & Fardeau, J. C. 1980 De´ termination isotopique par spectrome´ trie optique de compose´ s faiblement enrichis en azote15. Analusis 8, 148–152. Harrison, W. G. 1978 Experimental measurements of nitrogen remineralization in coastal waters. Limnology and Oceanography 23, 684–694. Harrison, W. G., Harris, L. R. & Irwin, B. D. 1996 The kinetics of nitrogen utilization in the oceanic mixed layer: nitrate and ammonium interactions and nanomolar concentrations. Limnology and Oceanography 41, 16–32. Harrison, W. G., Horne, E. P. W., Irwin, B. & Platt, T. 1990 Biological production on Georges Bank: are tidal fronts primary sources of new production in summer? EOS 71, 96. Harrison, W. G. & Wood, L. J. E. 1988 Inorganic nitrogen uptake by marine phytoplankton: evidence of size partitioning. Limnology and Oceanography 33, 468–475. Head, E. J. H., Harrison, W. G., Irwin, B. I., Horne, E. P. W. & Li, W. K. W. 1996 Plankton dynamics and carbon flux in an area of upwelling off the coast of Morocco. Deep-Sea Research I 43, 1713–1738. Holligan, P. M. 1979 Dinoflagellate blooms associated with tidal fronts around the British Isles. In Toxic Dinoflagellate Blooms (Taylor, D. C. & Seliger, H. H., eds). Elsevier, New York, pp. 249–256. Holligan, P. M., leB Williams, P. J., Purdie, D. & Harris, R. P. 1984 Photosynthesis, respiration and nitrogen supply of plankton populations in stratified, frontal and tidally mixed shelf waters. Marine Ecology Progress Series 17, 201–213. Horne, E. P. W., Loder, J. W., Harrison, W. G., Mohn, R., Lewis, M. R., Irwin, B. & Platt, T. 1989 Nitrate supply and demand at the Georges Bank tidal front. Topics in Marine Biology. (Ros, J. D., ed.) Scientia Marina 53, 145–158. Horne, E. P. W., Loder, J. W., Naimie, C. E. & Oakey, N. S. 1996 Turbulence dissipation rates and nitrate supply in the upper water column on Georges Bank. Deep-Sea Research II 43, 1683–1712. Koroleff, F. 1970 Direct determination of ammonia in natural waters as indophenol blue. International Council for the Exploration of the Sea 9, 19–22. Kristiansen, S. & Paasche, E. 1989 An improved method for determining relative 15N abundance in ammonium regeneration studies by direct diffusion. Marine Ecology Progress Series 54, 203–207. Kudela, R. M. & Cochlan, W. P. 2000 Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California. Aquatic Microbial Ecology 21, 31–47. Laws, E. A. 1984 Isotope dilution models and the mystery of vanishing 15N. Limnology and Oceanography 29, 379–386. Le Corre, P., L’Helguen, S. & Wafar, M. 1993 Nitrogen source for uptake by Gyrodinium cf. aureolum in a tidal front. Limnology and Oceanography 38, 446–451. L’Helguen, S., Madec, C. & Le Corre, P. 1996 Nitrogen uptake in permanently well-mixed temperate coastal waters. Estuarine, Coastal and Shelf Science 42, 803–818. Loder, J. W. & Platt, T. 1985 Physical controls on phytoplankton production at tidal fronts. In Proceedings, 19th European Marine Biology symposium (Gibbs, P. E., ed.). Cambridge University Press, Cambridge, U.K., pp. 3–21. MacIsaac, J. J. & Dugdale, D. C. 1972 Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Research 19, 209–232. Morin, P., Birrien, J. L. & Le Corre, P. 1989 The frontal systems in the Iroise Sea: Development of Gyrodinium aureolum Hulburt on
Nitrogen uptake by phytoplankton in a shallow water tidal front 357 the inner front. Topics in Marine Biology (Ros, J. D., ed.) Scientia Marina 53, 215–221. Morin, P., Connan, O. & Le Corre, P. 1994 Fronts thermiques de mare´ e: Cas des fronts de Manche Occidentale et de la mer Celtique. Oceanis 20, 21–43. Morin, P., Le Corre, P., Marty, Y. & L’Helguen, S. 1991 Evolution printanie`re des e´ le´ ments nutritifs et du phytoplancton sur le plateau continental armoricain (Europe du Nord Ouest). Oceanologica Acta 14, 263–279. Morin, P., Wafar, M. V. M. & Le Corre, P. 1993 Estimation of nitrate flux in a tidal front from satellite derived temperature data. Journal of Geophysical Research 98, 4689–4695. Olson, D. B. & Backus, R. H. 1985 The concentrating of organisms at fronts. Journal of Marine Biology Association U.K. 43, 113–137. Parsons, T. R., Dovey, H. M., Cochlan, W. P., Perry, R. I. & Crean, P. B. 1984 Frontal zone analysis at the mouth of a fjord—Jervis Inlet, British Columbia. Sarsia 69, 133–137. Parsons, T. R., Perry, R. I., Nutbrown, E. D., Hsieh, W. & Lalli, C. M. 1983 Frontal zone analysis at the mouth of Saanich Inlet, British Columbia, Canada. Marine Biology 73, 1–5. Pingree, R. D. & Griffiths, D. K. 1978 Tidal fronts on the shelf seas around the British Isles. Journal of Geophysical Research 83, 4615–4622. Pingree, R. D., Holligan, P. M. & Mardell, G. T. 1978 The effects of vertical stability on phytoplankton distribution in the summer on the northwest European shelf. Deep-Sea Research 25, 1011–1028. Pingree, R. D., Holligan, P. M. & Mardell, G. T. 1979 Phytoplankton growth and cyclonic eddies. Nature 5701, 245–247. Pingree, R. D., Mardell, G. T. & Maddock, L. 1983 Marginal front in Lyme Bay. Journal of Marine Biology Association U.K. 63, 9–15. Pingree, R. D., Pugh, P. R., Holligan, P. M. & Forster, G. R. 1975 Summer phytoplankton blooms and red tides along tidal fronts in the approaches to the English Channel. Nature 258, 672–677.
Price, N. M., Cochlan, W. P. & Harrison, P. J. 1985 Time course of uptake of inorganic and organic nitrogen by phytoplankton in the strait of Georgia: Comparison of frontal and stratified communities. Marine Ecology Progress Series 27, 39–53. Riegman, R., Malshaert, H. & Colijn, F. 1990 Primary production of phytoplankton at a frontal zone located at the northern slope of Dogger Bank (North Sea). Marine Biology 105, 329–336. Shiomoto, A., Sasaki, K., Shimoda, T. & Matsumura, S. 1994 Kinetics of nitrate and ammonium uptake by the natural populations of marine phytoplankton in the surface water of the Oyashio region during spring and summer. Journal of Oceanography 50, 515–529. Stoecker, J. K. & Capuzzo, J. M. 1990 Predation on protozoa: its importance to zooplankton. Journal of Plankton Research 12, 891–908. Townsend, D. W. & Pettigrew, N. R. 1997 Nitrogen limitation of secondary production on Georges Bank. Journal of Plankton Research 19, 221–235. Tre´ guer, P. & Le Corre, P. 1975 Manuel d’analyse des sels nutritifs dans l’eau de mer (Utilisation de l’Autoanalyseur II Technicon), seconde e´ dition. Universite´ de Bretagne Occidentale, 110 pp. Turley, C. M. 1986 Urea uptake by phytoplankton at different fronts and associated stratified and mixed waters on the European shelf. British Phycological Journal 21, 225–238. Videau, C. 1987 Primary production and physiological state of phytoplankton at the Ushant tidal front (west coast of Brittany, France). Marine Ecology Progress Series 35, 141–151. Wafar, M. V. M., Le Corre, P. & Birrien, J. L. 1983 Nutrient and primary production in permanently well mixed temperate coastal waters. Estuarine Coastal and Shelf Science 17, 431–446. Wheeler, P. M. & Kokkinakis, S. A. 1990 Ammonium recycling limits nitrate use in the oceanic subarctic Pacific. Limnology and Oceanography 35, 1267–1278.