Response of Sargasso Sea phytoplankton biomass, growth rates and primary production to seasonally varying physical forcing

Transcription

1 Journal of Plankton Research Vol.20 no.12 pp , 1998 Response of Sargasso Sea phytoplankton biomass, growth rates and primary production to seasonally varying physical forcing Ralf Goericke and Nicholas A.Welschmeyer 1 Marine Life Research Group, Scripps Institution of Oceanography, 9500 Gilman Drive, La Jolla, CA and Woss Landing Marine Laboratories, Moss Landing, CA , USA Abstract. The response of phytoplankton biomass, growth rates and primary production to seasonally varying physical forcing was studied at a station southeast of Bermuda over an 18 month period. Phytoplankton growth rates and primary production were measured using the pigment-labeling method, and phytoplankton biomass was calculated from these measurements. Phytoplankton carbon biomass varied systematically over the year. Highest values were observed during the winter and spring. Seasonal variations of chlorophyll (Chi) a in the surface layer could primarily be attributed to variations in phytoplankton biomass and secondarily to photoacclimation. During the summer period, average values of carbon (C)/Chl ratios (g C g" 1 Chi) ranged from 160 at the surface to 33 at the 1.6% light level, changes attributed to photoacclimation of the phytoplankton, consistent with the observation that phytoplankton biomass did not vary as a function of depth. Phytoplankton growth rates in the surface layer did not vary systematically over the year, ranging from 0.15 to 0.4S day 1, in spite of seasonally varying concentrations of nitrate. Growth rates varied as a function of depth from average values of 0.3 day- 1 in the surface layer to <0.1 day-' at the 1.6% light level. Thus, the primary response of the phytoplankton community to nutrient enrichment during the winter period was an increase in phytoplankton biomass rather than an increase in growth rates. A simple nutrient-phytoplankton-zooplankton model was used to explore this phenomenon. The model demonstrated that the observed response of the phytoplankton to nutrient enrichment is only possible when phytoplankton growth is not severely limited by nutrients. Introduction Early measurements of phytoplankton pigments and 14 C incorporation into paniculate organic matter indicated that phytoplankton biomass and primary production are very low in the subtropical central gyre of the North Atlantic, the Sargasso Sea (Steemann Nielsen, 1954; Menzel and Ryther, 1960, 1961). These observations led to the concept of the subtropical gyre as a severely resourcelimited system, comparable to a terrestrial desert (Ryther, 1963). Based on studies in the late 1960s and early 1970s, Eppley and co-workers (Eppley et al., 1973, 1977; Sharp et al., 1980; Perry and Eppley, 1981) concluded that phytoplankton biomass and primary production were similarly low in the North Pacific Central Gyre (NPCG; at 28 N, 165 W), and phytoplankton growth was thought to be limited by the availability of nitrogen (Eppley etal., 1973; Sharp etal., 1980). However, distributions of oxygen in the water column of the Sargasso Sea and the NPCG suggested that annual rates of new production, sensu Dugdale and Goering (1967), were 2-5 times higher (Shulenberger and Reid, 1981; Jenkins, 1982; Jenkins and Goldman, 1985; Craig and Hayward, 1987; Spitzer and Jenkins, 1989) than rates of new production determined from rates of carbon and inorganic nitrogen uptake (Eppley and Peterson, 1979). These results challenged the concept of the oligotrophic gyre as an oceanic desert. During the 1980s, it was realized that trace metal contamination can inhibit phytoplankton growth and Oxford University Press 2223

2 R.Goericke and N.A.Welschmeyer trace-metal-clean incubation techniques were devised (Fitzwater et al., 1982). Work based on trace-metal-clean incubation methods, at two oligotrophic sites off Bermuda and Hawaii (Karl and Lukas, 1996; Michaels and Knap, 1996), demonstrated conclusively that primary production in the subtropical gyres is indeed higher by a factor of 2-4 than historical data suggested. Rates of phytoplankton growth in the subtropical gyres have been a subject of controversy for the last 30 years as well. Early estimates for the Sargasso Sea and the NPCG ranged from 0.1 to 0.2 day 1 (Riley et al., 1949; Eppley et al., 1973). Other estimates for the Sargasso Sea, based on a variety of methods, ranged from 0.03 to 6 day 1 (summarized in Goldman et al., 1979). More recent estimates of phytoplankton growth rates in the central gyres, mostly based on trace-metalclean techniques, ranged from 0.2 to 1.2 day 1 (Laws et al., 1987; Malone et al., 1993; Jones et al., 1996); data that still do not settle the question of whether phytoplankton growth rates in the central gyres are high or low relative to maximum rates of growth attained under nutrient-replete conditions. To address this question, relative growth rates have to be known, i.e. the ratio of the realized and the maximal growth rate. Estimates of these for the central gyres, based on biochemical indicators, suggested that phytoplankton are growing close to their physiological maximum (Morris etal., 1971; Goldman etal., 1979; Glibert and McCarthy, 1984; Laws et al., 1987,1989). Estimates or proxies of relative growth rates, based on active fluorescence measurements, suggest that phytoplankton growth in the subtropical gyres is nutrient limited (Falkowski etal., 1991; Falkowski and Kolber, 1994). Clearly, the two views of phytoplankton physiological state in the subtropical gyres are still competing: on the one hand, the view of the oceanic desert characterized by low biomass and low relative rates of growth (Ryther, 1963), albeit with rates of productivity higher by a factor of 2-4 than previously assumed, and on the other hand the view of a dynamic community characterized by low biomass, but high rates of growth, that are balanced by high rates of grazing, akin to a spinning wheel (Goldman, 1988, 1993). These contrasting views cannot simply be resolved. Complicating the situation are possible differences between the two sites that denned the paradigm of the subtropical gyres, the Sargasso Sea and the NPCG (Karl and Lukas, 1996; Michaels and Knap, 1996), and possible decadal scale variations in ecosystem structure and functioning at these two sites (Venrick et al., 1987; but see Falkowski and Wilson, 1992). The ideal experimental approach to address this problem are open-ocean enrichment studies (cf. Coale et al., 1996). However, the type of nutrient potentially limiting productivity in the central gyres, inorganic nitrogen or phosphorus, renders this proposition economically not feasible. An alternative are studies of natural enrichments, those due to episodic events (cf. Glover etal., 1988; DiTullio and Laws, 1991) or due to seasonal changes. The Sargasso Sea off Bermuda is a particularly promising site for studies of the effects of seasonally varying physical forcing on phytoplankton physiology. Whereas the summer and fall are characterized by low levels of plant pigments and moderate rates of primary production, convection and wind-induced mixing erode the seasonal thermocline in the winter and inject nutrient-rich waters into the surface layer. As a consequence, 2224

3 Sargasso Sea phytoplankton primary production and chlorophyll (Chi) a increase, leading at times to pronounced blooms, in particular during the spring when the water column first stratifies (Riley, 1957; Menzel and Ryther, 1961; Michaels and Knap, 1996). Thus, when the phytoplankton community is viewed over longer time scales, two modes may be distinguished in the Sargasso Sea: an oligotrophic mode, the 'typical' condition during the summer and fall; and an enriched mode, the 'typical' winter/spring condition. The oligotrophic mode would be characterized by low levels of phytoplankton biomass and corresponding low rates of primary production. The enriched mode would be characterized by an increase in primary production. This response may be mediated by an increase in either phytoplankton biomass or growth rates, or both. The extent to which an increase in algal biomass per se contributes to elevated primary production during or after enrichment depends on how fast the biomass can accumulate. This end can be met by either a decrease in natural loss processes, e.g. grazing, or an increase in growth rate. We studied the effects of the seasonal enrichment of the mixed layer with nutrients on phytoplankton community structure and physiology off Bermuda. Here we will focus on contrasting phytoplankton dynamics during the summer and winter period in the Sargasso Sea to characterize the physiological response of the phytoplankton community to nutrient enrichment of the euphotic zone during the winter period. Specifically, we intend to test the hypothesis that phytoplankton growth rates increase when the euphotic zone is enriched with nutrients during the winter; a natural consequence of the hypothesis that phytoplankton growth in the Sargasso Sea is nutrient limited during the summer. The focus of this report is the response of phytoplankton biomass and phytoplankton growth rates to nutrient enrichments. The response of phytoplankton community size structure, taxon-specific growth rates and biomass to the two hydrographic seasons at the OFP (Ocean-Flux-Program) Station will be discussed in a separate communication (Goericke, 1998). Method Sample collection The OFP Station, which is located 80 nautical miles southeast of Bermuda (31 50'N, 64 10'W), was visited 12 times over a period of 2 years. Irradiance was measured with a LiCor sensor mounted on the ship. Light attenuation was measured using a Seechi disk. Water samples for pigment analysis and incubations were taken with 301 Niskin bottles off a standard hydrowire. Hydrographic properties were determined for discrete samples only, as described by Altabet (1989). Pigment analysis Total Chi a is defined here as the sum of chlorophyll a (Chi a{) and divinylchlorophyll a (Chi a 2 ), the primary chlorophyll of the marine cyanobacterium Prochlorococcus marinus (Goericke and Repeta, 1992). For fluorometric analysis 2225

4 R.Goericke and N.A.Welschraeyer of total Chi a, 250 or 500 ml of sea water were filtered on 25 mm Whatman GF/F filters and extracted in 10 ml of 90% acetone for 24 h in the dark at -18 C. This extraction procedure is as efficient as grinding and subsequent extraction for 24 h in the dark at -18 C when applied to samples from the Sargasso Sea (data not shown). The acetone extract was analyzed on a Turner 112 fluorometer as described by Holm-Hansen et al. (1965). The fluorometer was calibrated with 90% acetone extracts of diatoms and cyanobacteria whose Chi aj concentrations were determined using the appropriate coefficients or equations of Jeffrey and Humphrey (1975). All total Chi a concentrations reported here are based on fluorometric analysis for the sake of consistency; pigment concentrations measured by HPLC will be reported elsewhere (Goericke, 1998). Values of fluorometrically determined total Chi a (Chiflpiuor)were, on average, 10% higher than total Chi a as measured by HPLC (ChiflHPLc)- Th e equation of a regression of Chi OHPLC ( u g I" 1 ) against Chiflpiuor ( u g I" 1 ) an d tne 95% confidence intervals of the parameter estimates are: Chi a H PLC = -514 (± 19) (± 0.04) Chi afi uor. The presence of chlorophyll b and divinyl-chlorophyll b biases fluorometric measurements of total Chi a and 'pheopigments'. One mol of total Chi b simulates about -0.3 mol of total Chi a and 1.15 mol of 'pheopigment' (Goericke and Repeta, 1993). In the upper 100 m at the OFP Station, concentrations of total Chi b were always low relative to total Chi a, but high relative to concentrations of demetallated Chi a degradation products (Goericke, 1998; and R.Goericke, unpublished data). Thus, 'pheopigment' values are considered heavily biased and will not be reported here. Values of total Chi a at and above the 1.6% light level, as measured with the fluorometric method, are biased due to the presence of total Chi b, on average by -4% with maximum values at 100 m of-14%. Primary production, pigment-labeling experiments Phytoplankton growth rates and primary production were measured on nine occasions using the Chl-labeling method (Redalje and Laws, 1981; Goericke and Welschmeyer, 1993a). As described previously (Goericke and Welschmeyer, 1993b), water was sampled with 30 1, acid-cleaned Niskin bottles that had been modified for trace metal analysis (silicone O-rings, Teflon-covered closure springs). The water was incubated in acid-washed polycarbonate bottles. Light in the bottles was attenuated by neutral-density nickel screens to intensities corresponding to 96, 56, 35, 20, 8 and 1.6% of the surface irradiance (i.e. % 7 O ). The bottles were incubated in a plexiglass incubator cooled with surface sea water aboard the ship under natural sunlight; thus, no modifications were made to the spectral properties of the incident light. The use of white light instead of blue light may have led to an underestimation of growth rates in the 1.6% 7 O incubation bottles compared to rates in situ the 'blue-light effect' (Laws et al., 1989). Samples incubated at higher light intensities are not subject to such a bias. Rates of primary production were determined using 12 h (sunrise to sunset) and 24 h (sunrise to sunrise) incubations in 4 or 8 1 bottles, respectively. Rates of primary production were determined from the amount of 14 C incorporated into POC retained on Whatman GF/F filters. These filters retain >98% 2226

5 Sargasso Sea phytoplankton of all Prochlorococcus sp. (Moore etal., 1995), the smallest photooxytroph known to be present in the Sargasso Sea. The difference between 12 and 24 h rates of primary production was used as an indicator of community dark respiration (Smith etal., 1984). Bottles incubated for 24 h were also sampled for the incorporation of 14 C into Chi ^ and Chi a 2 for the measurement of phytoplankton growth rates using the Chl-labeling method as described previously (Goericke and Welschmeyer, 1993b). The phytoplankton growth rate, u, is defined by: B t = B o exp (u t), where t is time and B t and B o are phytoplankton biomass at times t and f zero. The phytoplankton community growth rate was calculated from the Chi a concentration-weighted average Chi a x and Chi a 2 based growth rates using the formula u = (UQ,] a, Chi a\ + UQ,I ^ ' Chi a 2 )/(Chl a x + Chi a 2 ) (Goericke and Welschmeyer, 1993b). Strictly speaking, the method only measures specific rates of pigment synthesis, which correspond to rates of growth only if growth is balanced (Goericke and Welschmeyer, 1993a). Although the assumption of balanced growth may be justified once rates of pigment synthesis and growth are integrated over the diel light period (Eppley, 1981), we will rely primarily on data either averaged over the seasons or averaged over the mixed layer (cf. Goericke and Welschmeyer, 1993a) to reduce bias, for example, due to photoacclimation during the incubation. In addition, growth rates measured using the Chl-labeling method are subject to some sources of uncertainty, as discussed previously (Goericke and Welschmeyer, 1993a). To summarize, the error associated with determinations of pigment specific activities, and hence growth rate, is expected to be randomly distributed, depending primarily on the precision of liquid scintillation counting and to a lesser degree on measurements of pigment concentration. Values of this error, determined using standard methods of error propagation (Barford, 1967), ranged from ±7% of the growth rate for high- 14 C-activity, high-pigment-concentration samples to ±18% for low- 14 C-activity, low-pigment-concentration samples. To calculate u from measurements of *P and incubation time, we must assume that the value of the turnover rate of the pigment precursor, k P, is known a priori (Goericke and Welschmeyer, 1993a). Erroneous values of k P will bias u. Assuming a growth rate of 0.25 day 1, the bias can be as high as ±40% of the growth rate. The error is a function of the actual growth rate and will increase with decreasing actual growth rates. Phytoplankton carbon biomass (C o ) was calculated from C o = AC(ef' - I)" 1 (Welschmeyer and Lorenzen, 1984), where AC is carbon fixation (ug C I" 1 day 1 ), u is growth rate (day 1 ) and t is incubation time. C o is the expected phytoplankton carbon biomass throughout the incubation period if growth and grazing are balanced in the incubation bottle. It corresponds to the concentration of algal carbon present at the beginning of the incubation if growth and grazing are unbalanced. The small changes in total Chi a in the incubation bottles during 24 h incubations, with average values of -14 and -10% for the upper three light depths for the winter and summer periods, respectively, suggest that growth and grazing were approximately balanced on a time scale of 24 h. The accuracy of C o could be refined if rates of grazing and respiration for the phytoplankton were known accurately (Laws, 1984); however, we do not feel confident to estimate these rates. 2227

6 R.Goericke and N.A.Welschmeyer Results Physical environment The annual cycle of sea surface temperature (SST) during the period January 1985-February 1987 displayed a gradual warming from 19 C in the winter to 27 C in the summer and subsequent cooling in the fall (Figure 1A). During the summer, the water column was strongly stratified (Goericke and Welschmeyer, 1993b) and mixed layer depths ranged from 20 to 30 m (Figure IB). Convectionand wind-induced mixing eroded the seasonal thermocline during the latter part of the year when the mixed layer reached depths up to 160 m. However, the water column was stratified temporarily during calm and sunny periods in the winter. The effects of deep mixing during the winter are reflected in nitrate concentrations in the surface layer, which were >0.1 umol N I" 1 in the winter and spring of 1985 and 1987, but <0.1 umol N I" 1 in the winter and spring of 1986 (Figure 2A). Throughout the summer, concentrations of nitrate were at or below the levels of detection in the upper euphotic zone, and the nitracline was located at a depth of m. Total chlorophyll a The 1% light level was located at a depth of m in the winter and spring, and reached depths of ~120 m during the summer (Figure IB). The standing stock of total Chi a was calculated by integration to a depth of 200 m. Values ranged from 22 to 52 mg Chi a rar 2 (Figure 1C). Surprisingly constant values, ranging from 22 to 24 mg Chi a nr 2, were observed in the summer and fall. Seasonal variations in water column structure and total Chi a suggest a division of the year into two periods (Goericke and Welschmeyer, 1993b). The winter period, lasting from early December until early May, was characterized by high concentrations of total Chi a in the mixed layer, a weakly stratified water column, and low SST (19-21 C). The summer period, late May until early December, was characterized by high SST (24~27 C), a stable water column, very low concentrations of total Chi a in the mixed layer (-0.05 ug H; Figure 2B), and a subsurface chlorophyll maximum (SCM) at depths ranging from 100 to 120 m. During the summer period, average mixed layer total Chi a was ug I" 1 (SD = ± jig H, n = 14). In the summer, total Chi a at the SCM ranged from 0.26 to 0.42 ug Chi a I" 1. Since the depth of the SCM was only resolved to within 10 m, it is not possible to determine whether its depth varied between the summers of 1985 and The highest concentration of total Chi a, 0.42 ug I" 1, observed in the SCM at a depth of 100 m in October 1985 (Figure 2B), coincided with the highest observed concentration of nitrate in the SCM (Figure 2A). Primary production We carried out one primary production time course experiment in August 1985 to test for diel patterns of photosynthesis (Figure 3). Rates of carbon assimilation were constant throughout the day until 16:00 h for the 96-20% / light treatments, 2228

7 Sargasso Sea phytoplankton Jan Mar Jun Aug Oct Dec Jan Mar May Jul Sep Nov Feb Fig. 1. Sea surface temperature (A), depth of the mixed layer and the 1% light level (B), and m depth-integrated Chi a (C) plotted against time (1/85-2/87). as indicated by a nearly linear increase in carbon accumulation, but declined during the early afternoon for 8 and 1.6% I o. Carbon fixation throughout the euphotic zone was negligible in the late afternoon (16:00-20:00 h). We did not observe a consistent decrease in 14 C activity at night due to respiration, in contrast to observations derived from comparisons of 12 and 24 h incubations (see below). 2229

8 E A: Nitrate (nm-nl1 ) 1/85 3/85 6/85 8/85 10/85 12/85 1/86 3/86 5/86 7/86 9/86 11/86 2/ ' B: Total Chi a 1/85 3/85 6/85 8/85 10/85 12/85 1/86 3/86 5/86 7/86 9/86 11/86 2/ MO ISO Fig. 2. Time-depth plots of nitrate concentrations (A; based on data from Altabet, 1989) and total Chi a (B) in the upper 220 m at the OFP Station.

9 Sargasso Sea phytoplankton 6:00 9:00 12:00 15:00 18*0 21:00 0:00 3:00 6:00 Local Time (h) Fig. 3. A production time course experiment, August The time course of carbon assimilation (ug C 1~') is plotted against time for all six light depths. The bold line represents the irradiance in units of me nr" 2 s~'. Results of primary production experiments are presented as summer-winter period comparisons by plotting all production data against light depth (% I o plotted on a logarithmic scale; Figure 4). In the surface layer (96-35% 7 O ), total Chi a was almost four times higher during the winter period compared to the summer period; however, values were about equal for the two time periods at the 1.6%. light depth (Figure 4A). Primary production did not vary significantly as a function of light depth in the upper euphotic zone (96-35% 7 0 ); average values ranged from -3 ug C I" 1 day" 1 during the summer period to ~7 ug C I" 1 day" 1 during the winter period (Figure 4B). Primary production declined below the 35% light depth to values <1 ug C I" 1 day 1 at 1.6% 7 0. The productivity index, PI (ug C ug- 1 total Chi a h" 1 ), was significantly higher in the upper euphotic zone during the summer period when compared to the winter period (Figure 4C). The PI declined with depth below the 56% light depth (Figure 4C). Surface layer total Chi a, depth-integrated primary production and the PI varied systematically over the seasons (Figure 5). Rates of carbon fixation (mg C m" 2 day 1 ), calculated by integration to the 0.5% light level, ranged from 156 to 290 mg C nr 2 day 1 during the summer period and from 260 to 370 mg C nr 2 day 1 during the winter period (Figure 5B), except for one low value of 102 mg C nr 2 day 1 in December This day was characterized by a very low irradiance of 7.8 E nr 2 day 1. Average daily productivity during the summer period of 1985 (175 mg C m" 2 day 1 ) was significantly lower (P < 0.025) compared to 1986 (260 mg C nr 2 day 1 ). The PI (Figure 5B) co varied with irradiance; highest values of the PI were observed in June 1985, coinciding with the highest observe J values of surface irradiance, and lowest values were observed during the winter. 2231

10 -t-i f Is) Chlorophyll a [ug-chl a L" ] Primary Production [ ug-c L d ) Productivity Index [ug-c ug-chl a h ] B Summer Period O Winter Period Fig. 4. Results of 12 h primary production experiments plotted against light depth (% surface irradiance) averaged for the summer ( ) and winter (O) period. The width of the horizontal lines indicates the SD of the averages. (A) Total Chi a at the beginning of the incubation. (B) Primary production. (C) Productivity index.

11 Fig. 5. Summary of the production experiments plotted against time. (A) Surface layer total Chi a. (B) Productivity index for 96 and 56% /. (C) Primary production integrated over the water column. (D) Community dark respiration plotted as the percent decrease in l4 C activity in particulate organic matter at night. g 1 I Jun Aug Oct Dec Jan Mar Miy Sap

12 R.Goericke and N.A.Welschmeyer 14 C activity in particulate matter declined at night, most likely due to respiration of recently fixed carbon by phytoplankton and zooplankton. Values integrated over the euphotic zone represented 8-30% of daily rates of primary production (Figure 5D); the average value was 18%. No systematic variations of 14 C loss at night were observed over the seasons. Phytoplankton biomass and growth rates Phytoplankton biomass and growth rates were measured using the Chl-labeling method (Redalje and Laws, 1981; Goericke and Welschmeyer, 1993a). Detailed data for one experiment from August 1985 are shown in Figure 6. Rates of growth ranged from almost 0.45 day 1 in the surface layer to values <0.1 day 1 at 1.6% I o, i.e. slightly above the SCM (Figure 6B). Phytoplankton biomass (C o ; i.e. the organic carbon content of phytoplankton, ug C I" 1 ) was approximately evenly distributed over the upper 100 m of the water column (Figure 6C), it represented ~10% of the particulate organic carbon (Figure 6C). The carbon to total Chi a ratio of the phytoplankton (C/Chl ratio, g C g" 1 total Chi a) was calculated from C o and total Chi a. It decreased from 110 in the surface layer to 25 at 1.6% / o (Figure 6D). Average phytoplankton growth rates for the individual light levels (% / o ) were similar for the summer and winter periods (Figure 7A), ranging from 0.25 to 0.35 day 1 for 96-20% 7 O, declining to values of 0.1 day 1 or less at 1.6% I o. Growth rates of the phytoplankton in the surface layer did not vary systematically over the year, ranging from 0.15 to 0.45 day 1 (Figure 8B). Average values of C o ranged from ~9 ug C I" 1 in the surface layer to ~7 ug C H at 20,8 and 1.6% 7 O (Figure 7B) during the summer period, but were -2.5 times higher in the surface layer during the winter (Figure 7B). C o varied systematically over the seasons in the surface layer; values ranged from 40 ug C I" 1 in the spring to 5 ug C I" 1 during the summer period (Figure 8C). C o was slightly lower S I I 40 Primary Production Gig-C C 1 d" 1 ) Growth Rate (d') Carbon Concentration (jig-c L') POC Carbon to Chi a Ratio Fig. 6. Example of a 24 h Chl-labeling experiment at the OFP Station in the Sargasso Sea (August ). Parameters are plotted against depth. (A) Primary production (ug C I" 1 day-'). (B) Phytoplankton growth rates. (C) Phytoplankton biomass and particulate organic carbon (ug C I" 1 )- Note that values of the phytoplankton biomass are scaled up by a factor of 10. (D) Phytoplankton C/Chl a ratio (fig C ug- 1 Chi a). 2234

13 Sargasso Sea phytoplankton Growth Rate [d' 1 ] Algal Carbon [ iig-c L" 1 ] Carbon to CM a Ratio J SO Summer Period O Winter Period Fig. 7. Results of all chlorophyll-labeling experiments plotted against light depth averaged for the summer ( ) and winter (O) periods. Values are plotted against light depth. The width of the horizontal lines indicates the SD of the averages. (A) Phytoplankton growth rate. (B) Phytoplankton biomass. (C) Phytoplankton C/Chl ratio. in the summer of 1985 compared to the summer of 1986 (P < 0.10). Average C/Chl ratios of the phytoplankton (g C g" 1 Chi a) decreased from values of 180 in the surface layer to values of 33 at 1.6% / o during the summer period (Figure 7C). The analysis of surface layer C/Chl ratios in terms of summer-winter periods is slightly misleading, since these covaried over the year with irradiance (see below). High values (240 g C g" 1 Chi a) were observed in the early summer, declining during the fall, with minima (65 ug C ug" 1 Chi a) observed during the winter (Figure 8D). Discussion Physical environment Off Bermuda, irradiance, air temperature and wind speeds vary over the seasons (Menzel and Ryther, 1960; Jenkins and Goldman, 1985; Spitzer and Jenkins, 1989). Water column structure is driven by this meteorological forcing, which also governs the distribution of nutrients in the water column (e.g. nitrate; Figure 2A). Cold-core rings seldom penetrate to south of Bermuda and were not observed at the OFP Station during our occupations (Altabet, 1989); subtropical fronts are found during the winter primarily south of Bermuda (Weller, 1991). The effects of other types of mesoscale features, however, have been noticed in the BATS time series (Michaels and Knap, 1996). Our observations of water temperature at the OFP Station during the period (Goericke and Welschmeyer, 1993b) are virtually identical to the concurrent observations at Station S (Spitzer and Jenkins, 1989). Convection in the winters of 1985 and 1987 at Station S extended to depths of m (Spitzer and Jenkins, 1989), but was not 2235

14 R.Goericfce and N.A.Welschmeyer Mar Jun Aug Oct Dec Jan Mar May Sap Ju) Aug Oct Dec Jan Mar May Sap Fig. 8. Results of chlorophyll-labeling experiments plotted against time for the surface layer (96-35% / ). (A) Irradiance; the line represents a sinusoidal curve fit to the data. Values for March 1985 and March 1986 (open symbols) were estimated from this curve. (B) Phytoplankton growth rate. (C) Phytoplankton biomass. (D) C/Chl ratio. observed during the winter of Although deep-mixing events were not directly observed by us during the winters of 1985 and 1987, it is likely that deep mixing also occurred at the OFP Station because elevated nitrate concentrations were observed in the mixed layer (Altabet, 1989). Spitzer and Jenkins (1989) concluded that the meteorological and oceanographic conditions off Bermuda during the years were not significantly different from the long-term mean conditions as defined by the time series at Station S (WHOI and 2236

15 Sargasso Sea phytoplankton BBSR, 1988). Interannual variability of physical forcing at the site is high, as reflected in the depth of mixing during the spring (Michaels and Knap, 1996). Phytoplankton biomass Cellular concentrations of carbon and Chi a do not covary strictly in phytoplankton (Geider, 1987). Consequently, it is difficult to ascribe observed depth and seasonal variations of total Chi a unambiguously to variations of phytoplankton biomass. We observed a 5-fold change in total Chi a as a function of depth during the summer period (Figure 2B). This change in total Chi a as a function of depth is similar to the ~5-fold difference in cellular Chi a (Chi a^n) typical of nutrient-replete cultures of eukaryotic microalgae grown at light intensities of 6 and 680 ue nr 2 s" 1 (Goericke and Montoya, 1998), light intensities corresponding to those experienced by phytoplankton at the SCM and in the mixed layer, respectively, during the summer. This comparison suggests that phytoplankton biomass during the summer did not change with depth in spite of 5-fold variations of total Chi a; a conclusion confirmed by our measurements of phytoplankton biomass, which did not vary significantly with depth during the summer period (Figure 7B). At the OFP Station, total Chi a varied by more than a factor of five in the surface layer over the year (Figure 5A). The effect of photoacclimation, i.e. the phenotypic acclimation to irradiance, on concentrations of Chi a in the surface layer can be estimated as described above. Median mixed layer irradiance varies due to variations in surface irradiance and mixed layer depth. Irradiance at a depth corresponding to one-half of the mixed layer depth ranged from 140 ue nr 2 s" 1 during January 1986 to 680 ue nr 2 s" 1 during June Chi a^a in nutrient-replete cultures changes on average by a factor of 2.1 in response to such an irradiance change (Goericke and Montoya, 1998). Since a >5-fold change in mixed-layer total Chi a was observed, this suggests that mixed-layer concentrations of total Chi a were primarily affected by seasonally varying phytoplankton biomass and only secondarily by photoacclimation, consistent with the observed seasonal variations of phytoplankton biomass in the surface layer (Figure 8C). Our 5-10 ug C H estimates of phytoplankton biomass in the Sargasso Sea during the summer period are similar to those based on cell counts: Li et al. (1992), using flow cytometry, calculated the biomass of specific groups of microalgae for a station in the northern Sargasso Sea. Biomass distributions of the cyanobacterium Synechococcus and eukaryotic phytoplankton were uniformly high in the upper m of the water column, declining below these depths. The summed biomass of these two groups was ~6.5 ug C I" 1 throughout the upper 90 m. The biomass of the marine prochlorophyte Prochlorococcus was estimated as 2.5 pg C H at the SCM; however, Li et al. (1992) were not able to detect Prochlorococcus in the upper euphotic zone due to limitations of their instrument. Thus, their data suggest ~9 ug C I" 1 phytoplankton biomass in the lower euphotic zone and at least 6.5 ug C I" 1 in the mixed layer; values very similar to our observations at the OFP Station during the summer period. Fuhrman et al. (1989) and Caron (personal communication in Malone et al., 1993) used 2237

16 R.Goeridce and N.A.WeIschineyer epifluorescence microscopy to measure phytoplankton biomass off Bermuda during July 1988 and August 1989, respectively. Values ranged from 3 to 9 ug C I" 1, without clear trends as a function of depth. Although these values are underestimates of true phytoplankton biomass since Prochlorococcus was not enumerated, our observations (Goericke and Welschmeyer, 1993b) suggest that Prochlorococcus could have contributed 10-30% to total phytoplankton pigment biomass at the surface, but up to 65% of the total at the SCM. Estimates of phytoplankton biomass for the NPCG based on cell counts (7-9 ug C H; Beers et al., 1975,1982) and on concentrations of ATP (12 ug C H; Eppley et al., 1973,1977; Sharp et al., 1980) are similar to the recent estimates for the Sargasso Sea. Note, however, that the data of Beers et al. suffer from an unknown bias as photo- and autotrophic 'flagellates and monads' were not differentiated, and as cyanobacteria were not enumerated. Jones et al. (1996) reported a value of 8.2 ug C I" 1 for station ALOHA off Hawaii. These data suggest that phytoplankton carbon biomass in the euphotic zones of the central oligotrophic gyres ranges from 5 to 10 ug C I" 1 when summer conditions prevail. No evidence was seen by us or others that phytoplankton carbon varies as a function of depth by more than a factor of two. These results corroborate the earlier suggestions, summarized in Cullen (1982) and Eppley et al. (1988), that the SCM found throughout the central oligotrophic gyres (Venrick et al, 1973) do not represent phytoplankton biomass maxima. Phytoplankton carbon to Chi a ratios Phytoplankton biomass used to be estimated from 'recommended' C/Chl ratios, which were believed to range from 100 gcgr 1 Chi a at the surface to 25 g C g" 1 Chi a at depth (Strickland and Parsons, 1972). However, it is known from laboratory studies that C/Chl ratios not only vary among groups of microalgae, but also by an order of magnitude as a function of irradiance or nutrient-limited growth rate within any one species (Geider, 1987). Thus, it is not surprising that we observed dramatic variations of phytoplankton C/Chl ratios at the OFP Station. Surface-layer C/Chl ratios varied systematically over the seasons; values ranged from 240 in the early summer, during the period of maximum irradiance, declining to values of 65 in the winter. In the summer, C/Chl ratios decreased with depth to values as low as 25 at the 1.6% light level. We have argued above that systematic variations of the C/Chl ratio over the season are primarily due to photoacclimation since we did not observe systematic variations of growth rates over the seasons. Variations of C/Chl ratios in the surface layer due to a changing phytoplankton community are unlikely since we did not observe dramatic variations in the abundance of taxon-specific pigments (Goericke, 1998), but for variations of Chi a 2, the pigment characteristic of the marine prochlorophyte P.marinus, which contributed 20 and 30% to total chlorophyll biomass in the surface layer during the summer and winter periods, respectively (Goericke and Welschmeyer, 1993b). Our measurements of summer period C/Chl ratios are almost identical to the estimates of Cullen (1982) for oligotrophic central gyres, i.e. values ranging from 2238

17 Sargasso Sea phytoplankton 150 to 250 g C g" 1 Chi a in the surface layer, decreasing to 25 g C g" 1 Chi a at the SCM. Campbell et al. (1994) and Jones et al. (1996) gave values of 128 and 156 g C g" 1 Chi a, respectively, for the surface mixed layer of station ALOHA off Hawaii, decreasing to values of 40 and 42 g C g" 1 Chi a at the SCM. Such large variations in C/Chl ratios as a function of depth in the ocean have also been observed in nutrient- and light-limited marine microalgae. For example, extreme values of C/Chl ratios for cultures of the diatom Thalassiosira weissflogii ranged from 337 g C gr 1 Chi a for a severely nitrate-limited continuous culture maintained at a dilution rate of 0.15 day 1 to 18 g C gr 1 Chi a for a batch culture maintained at an irradiance of 8 ue nr 2 s -1 (Laws and Bannister, 1980). These data illustrate that the effects of photoacclimation on C/Chl ratios can be similar in natural populations of algae and in cultures. Clearly, variations in C/Chl ratios observed as a function of depth and in the surface layer at the OFP Station over the seasons demonstrate that it is not possible to assume constant ratios for the conversions of Chi a to phytoplankton carbon biomass. Phytoplankton growth rates Phytoplankton growth rates reported here, ranging from 0.2 to 0.4 day 1, are similar to pre-1980 estimates of phytoplankton growth rates for the surface layer of the NPCG, which ranged from 0.1 to 0.3 day 1 (Eppley et al., 1973,1977; Sharp et al., 1980; Perry and Eppley, 1981). However, an analysis of the productivity indices reported by Eppley and co-workers (see below) suggests that these estimates may have been biased; primary production and growth rates may have been 2-4 times higher than reported rates. Phytoplankton growth rates of 0.6 and 1.2 day 1 were reported for the surface layer of the NPCG (Laws et al., 1987; Jones et al., 1996). EJ.Lessard (personal communication) measured growth rates at the BATS station off Bermuda during the summer of 1991 using the dilution method (Landry and Hasset, 1982); her values, ranging from 0.2 to 0.7, with a mean of 0.4 day 1, are slightly higher than those reported here. These rates contrast with high growth rates, calculated from chlorophyll-specific productivity and C/Chl ratios reported by Malone et al. (1993) for the surface layer of the OFP Station for August 1989, which were highly variable, but on average twice as high as those reported by us for corresponding time periods. However, corresponding rates of primary production, adjusted for 16% respiratory loss at night, were lower than those reported in this study. The differences may be due to large interannual variations of phytoplankton growth rates in the Sargasso Sea or due to the larger uncertainties associated with the indirect estimates of phytoplankton growth rate used by Malone et al. (1993). This limited comparison of data from the two central oligotrophic gyres suggests that phytoplankton growth rates in the NPCG, at least during the last 15 years, have been approximately two times higher than rates at the OFP Station. Most of these phytoplankton growth rates for the subtropical gyres are low when compared to the temperature-constrained (26 ) maximum possible growth rate, which is -3 day 1 (Eppley, 1972). However, it is not known whether these rates are low due to inherently low maximum growth rates of subtropical oceanic 2239

18 HGoericke and N.A. Welschmeyer phytoplankton, or due to nutrient or light limitation of growth. The absence of a decrease in growth rates in the surface layer with irradiance (Figure 7A) suggests that phytoplankton growth at the OFP Station was not light limited in the surface layer either during the summer, or during the winter period, although this was most likely the case throughout the year at or below 8% 7 O. Inferring that growth of the phytoplankton community is nutrient limited is difficult. It is easy to demonstrate that growth of some microalgae is nutrient limited by performing nutrient enrichment experiments. Such experiments usually result in blooms of diatoms in the incubation bottles, as shown by Menzel et al. (1963) for the Sargasso Sea. A variety of biochemical indicators have been used to assess the nutritional status of phytoplankton in the subtropical gyres. Results from those experiments suggest that phytoplankton growth is slightly or not at all nutrient limited (Morris et al., 1971; Goldman et al., 1979; Glibert and McCarthy, 1984; Laws et al., 1987,1989). For example, estimates of relative growth rates of phytoplankton in the NPCG, based on rates of 14 C incorporation into protein, ranged from 60 to 100% of maximum rates (Laws et al., 1987,1989). In contrast, activefluorescence-based indicators of physiological state suggest that phytoplankton growth rates are nutrient limited in the subtropical gyres (Falkowski et al., 1991; Falkowski and Kolber, 1994). Thus, our results and those of most other studies imply that phytoplankton in the surface layer of the central gyres are not severely limited by the availability of inorganic nutrients. However, growth rates, -0.4 day 1, are low compared to the corresponding temperature-constrained maximum possible growth rates (Eppley, 1972). Growth rates of microalgae realized under light- and nutrientreplete conditions, i.e. maximum growth rates, are known for only some species isolated from the subtropical open ocean. Values of these rates are 1.8 day 1 (n = 5, where n is the number of species/clones) for diatoms, 1.1 day 1 (n = 7) for prymnesiophytes, 1.4 day 1 («= 4) for Synechococcus spp. (Brand et al., 1986) and 0.6 day 1 (n = 2) for the marine prochlorophyte P.marinus (Moore et al., 1995), i.e. values ranging from 0.6 to 1.4 day 1 once diatoms are excluded, which rarely contribute significantly to phytoplankton biomass in subtropical gyres (Bidigare et al., 1990; Letelier et al., 1993; Goericke, 1998) with the exception of spring blooms (Hulburt et al., 1960). It is possible, however, that these values are not representative for the whole phytoplankton community as the process of isolating algae from the ocean selects for fast-growing clones. Consequently, we should view these values as an upper limit. Still, these values are quite low when compared to the temperature-constrained maximum possible growth rates of ~3 day 1. Interestingly, we also measured low growth rates of day 1 for prymnesiophytes and pelagophytes in the subarctic Pacific (Goericke and Welschmeyer, 1993a) where the SST was 14 C, which corresponds to a temperature-constrained maximum growth rate of 1.45 day 1. In this case, phytoplankton were incubated under conditions which made it likely that growth was maximal, i.e. not limited by light, nitrate, silicate, phosphate or trace metals (Goericke and Welschmeyer, 1993a). Similar laboratory or field observations have been made by others on non-diatom species (summarized by Furnas, 1990), suggesting that it is not only possible, but common, that maximum growth rates are substantially 2240

19 Sargasso Sea phytoplankton less than temperature-constrained maximum possible growth rates (cf. Eppley, 1972). Primary production The studies by Ryther and Menzel in the Sargasso Sea (Menzel and Ryther, 1960, 1961) and Eppley and co-workers in the NPCG (Eppley et al., 1973,1977; Eppley and Sharp, 1975; Sharp et al, 1980) used to define the paradigm of the oligotrophic gyre as an oceanic desert characterized by rates of primary production ranging from ~50 to 150 mg C m~ 2 day 1. Recent measurements, based on tracemetal-free incubation methods, were about two (Michaels and Knap, 1996) to four times (Marra and Heinemann, 1987; Karl and Lukas, 1996) higher than the historical data for the Sargasso Sea and the NPCG. Rates of primary production reported here for the summer period, ranging from 156 to 290 mg C m~ 2 day 1, are similar to those reported by Michaels and Knap (1996). It is likely that depthintegrated rates reported here would have been higher had we carried out incubations in situ (Laws et al., 1990) since rate measurements in the lower euphotic zone may have been biased due to the 'blue-light effect'; however, this does not apply to rates of primary production (or growth) determined for the surface layer. Primary production in the Sargasso Sea during the winter and spring is characterized by large intra- and interannual variations of primary production; the highest values, usually observed during the spring bloom in March and April, ranged from 400 to 800 mg C irr 2 day 1 (Menzel and Ryther, 1960,1961; Michaels and Knap, 1996). We did not observe a spring bloom, highest values of primary production observed by us were 371 mg C m~ 2 day 1 during March A comparison of historical and recent data is possibly confounded by temporal and spatial changes in phytoplankton biomass and primary production in the oligotrophic central gyres (Hayward and McGowan, 1985; Hayward, 1987; Venrick et al., 1987; but Falkowski and Wilson, 1992). The hourly or daily rate of primary production, normalized by concentrations of total Chi a, i.e. the PI, offers a good basis to compare results from the surface layers of different oligotrophic gyres. The PI of nutrient-limited microalgal cultures is relatively constant for varying growth rates and a given irradiance, except for growth at very low relative growth rates (Laws and Wong, 1978; Laws and Bannister, 1980). The PI of phytoplankton in the field that is adversely affected by the incubation method is usually very low; for example, values ranging from 0.01 to 0.2 g C g" 1 Chi h" 1 were reported for the surface layer of the tropical North Atlantic (Gieskes et al., 1979). Productivity indices calculated from recent, trace-metal-clean incubations in the surface layer of oligotrophic gyres during summer conditions are surprisingly constant, ranging from 4 to 10 g C g" 1 Chi h" 1 (Laws et al., 1987; Marra and Heinemann, 1987; Michaels and Knap, 1996). Average values reported by Eppley and co-workers (Sharp et al., 1980) for the NPCG were substantially less; cruise averages were usually <1 g C gr 1 Chi h" 1, except for one cruise with an average of 2.4 gcg" 1 Chi h" 1. Menzel and Ryther (1961) reported that the PI varied inversely with irradiance at Station S over the seasons, as expected from the results of laboratory experiments, with average Pis of -2.5 during the summer and

20 R.Goericke and N.A.Welschmeyer during the winter. We too observed that the PI varied systematically over the seasons; however, our values were higher by roughly a factor of two, ranging from 2 to 7 g C g" 1 Chi h" 1. The average value for the summer period was five, slightly lower than results from the BATS program, which reported values ranging from two to 10 (Michaels and Knap, 1996). However, the BATS program observed significant interannual variations in the PI. The PI for the summer period of was significantly higher (8.9 g C gr 1 Chi tr 1 ) than the corresponding value for , i.e. 6.1 g C g" 1 Chi h" 1. This comparison of productivity indices suggests that the historical data sets underestimated primary production in the surface layers of the oligotrophic central gyres by a factor of 2-4 (cf. Michaels and Knap 1996). Phytoplankton response to seasonal changes The potentially most important factors affecting phytoplankton at the OFP Station are seasonally varying irradiance and fiuxes of nutrients into the euphotic zone. We expected that seasonally varying irradiance would affect C/Chl ratios due to photoacclimation of the phytoplankton, whereas seasonally varying nutrient fluxes would affect phytoplankton growth rates and phytoplankton biomass. Surface layer phytoplankton biomass and total Chi a were significantly correlated at the OFP Station [r = 0.74, P(r = 0) < 0.05; Figure 9A], demonstrating that seasonally varying total Chi a was at least partially driven by changing phytoplankton biomass. However, it is possible to attribute a significant fraction of the unexplained variance between phytoplankton biomass and total Chi a to photoacclimation since C/Chl ratios and irradiance were significantly correlated as well (/ = 0.65, P < 0.05; Figure 9B). Whereas our calculations (see above) suggest that the observed variations of irradiance should only result in a 2-fold change in cellular Chi a or C/Chl ratios in the mixed layer over the seasons, we observed an almost 4-fold range of values (Figure 8D). The larger than expected range of C/Chl ratios was most likely a consequence of varying phytoplankton growth rates, an effect well documented for nutrient-limited continuous cultures (Laws and Wong, 1978; Laws and Bannister, 1980). For example, the highest surface layer growth rate observed during the summer period coincided with the lowest summer period C/Chl ratio (August 1985; arrow in Figure 9B). However, it is not possible to analyze the relationship between growth rates and C/Chl ratios formally because the two parameters are not statistically independent as measured by us. The seasonal cycle of phytoplankton biomass in the surface layer was characterized by low concentrations in the summer (4-8 ug C I" 1 ) and a build-up of biomass in the winter; maximum values of phytoplankton biomass were observed in the spring (20-40 ug C I" 1 ). It is likely that we underestimated variations in phytoplankton biomass over the year because we did not observe a typical diatom-dominated spring bloom which can occur when nutrient-rich surface water stratifies thermally in the spring. These blooms are characterized by concentrations of Chi a > 0.5 ug I" 1 (Menzel and Ryther, 1960). The seasonal cycle of phytoplankton biomass described by us is consistent with the interpretation of 2242

21 Sargasso Sea phytoplankton T, 40- Chlorophyll a (ng L ) <s O O o o o o o o o Irradiance (Einst m' 2 d -1 ) Fig. 9. Surface layer phytoplankton biomass plotted against total Chi a (A). Surface layer C/Chl ratio plotted against irradiance (irradiance for March 1985 and March 1986 taken from Figure 8A) (B). The value for August 1985 is indicated by an arrow in (B). the seasonal cycle of Chi a at Station S by Menzel and Ryther (1960), who suggested that changing concentrations of Chi a represent actual changes in phytoplankton biomass. In contrast to phytoplankton biomass, phytoplankton growth rates (cf. Figure 7A) did not respond to the enrichment of the system with nutrients during the winter period (Figure 10). This result suggests that phytoplankton growth was not severely nutrient limited, consistent with the results of others based on studies of biochemical indicators (see above). Our conclusion would be invalid if algal growth were light limited in the surface layer during the winter period; however, this is quite unlikely (see above). The metabolism of the phytoplankton, and to some extent zooplankton, as reflected in relative 14 C PO c losses at night (Smith et al., 1984), did not vary systematically over the year either (Figure 5D), consistent with our observations for phytoplankton growth rates. Clearly, the differences between the summer and winter period noted by us do not warrant the postulation of two different physiological states of the phytoplankton. The phytoplankton grew year round at rates substantially less than maximum possible temperature-constrained rates, inconsistent with the view that the subtropical planktonic community is a rapidly spinning wheel (cf. Goldman, 1988). Nonetheless, the ecosystem as a whole still displayed two distinct modes: the oligotrophic mode during the summer period and the enriched mode during the winter period. This change in ecosystem state is most likely brought about by the increased flux of nutrients into the euphotic zone. The mechanisms that lead to this response are not obvious; however, significantly larger phytoplankton growth rates did not mediate this response. A necessary condition for an increase in phytoplankton biomass, but not growth rates, in response to higher fluxes of nutrients into the euphotic zone, might be that phytoplankton growth is not severely limited by nutrients such that changing nutrient concentrations lead only to small increases in growth rates. Other interactions, e.g. the poise between phytoplankton growth and zooplankton grazing, may mediate the response of the system to nutrient enrichment. To / B 2243

22 R.Goericke and N.A.WeIschmeyer o - 20 Log (Nitrate Concentration [umol-n L" 1 ]) ' / / Depth (m) " orv\ - \ / \ \ II Fig. 10. Average log (nitrate) plotted against depth for the winter ( ) and summer (O) periods. answer these questions, we studied the response of a simple nutrient-phytoplankton-zooplankton model to varying rates of nutrient input into the system (Figure 11). We found parameter combinations that resulted in a steady state of the system over a broad range of nutrient supply rates. The steady states were characterized by a strong increase in phytoplankton biomass in response to increased rates of nutrient supply in the absence of a strong response of phytoplankton growth rates. Phytoplankton growth rates did not respond strongly because the system found a steady state where phytoplankton growth was not severely limited by nutrient concentrations, i.e. u > 0.5 u max. Zooplankton biomass also increased significantly as a function of nutrient supply rates to the system; however, this increase was not as pronounced as the increase in phytoplankton biomass. At steady state, zooplankton grazing rates were prey saturated when rates of nutrient supply were high. It would be naive to take the results from this simple model at face value, or interpret the response of the model in detail, as the structure of the model does not reflect the structure of the respective ecosystem realistically. However, this model demonstrates that our observations are consistent with our current understanding of ecosystem function. In our case, the observations were (i) larger fluxes of nutrients into the euphotic zone during the winter, (ii) a positive response of phytoplankton biomass, but (iii) no significant response of phytoplankton growth rates. The model demonstrated that these observations describe a possible response of the system to nutrient enrichment. The important aspect of this conclusion is that such a response is only possible if phytoplankton growth rates 2244

23 Sargasso Sea phytoplankton A growth P f \ Nutri- 1 ents input T ( Phyto- ^ -*H plankton J. s. growth z \ recyc toss 1 z Zoo- ^ plankton J B: The model's response to varying "input" input N P Z growthp Fig. 11. The response of a simple nutrient (N, mass voh), phytoplankton (P, mass vol-'), zooplankton (Z, mass vol"') model (A) to varying inputs of nutrients (input; mass vol" 1 time" 1 ) was studied. The following assumptions were made. Phytoplankton growth is nutrient limited: growth p (time" 1 ) = Mmax-p ' Nl{k n + N). Growth of zooplankton is a function of phytoplankton density: growth z (time"') = u max. z Pl(kp + P)- Zooplankton losses are a simple function of their density: lossj (time" 1 ) = loss max Zl(k z + Z). The recycling of nutrients within the system (recyc; mass vol"' time" 1 ) was assumed to be a constant fraction (r eff, recycling efficiency) of the zooplankton loss: recyc = lossj Z-sed = r cll lossj Z. The loss of mass from the system via sedimentation (sed, mass voh time-') is denned above implicitly. The differential equations representing the model were solved numerically (Euler's algorithm). The independence of results from initial values and numerical stability of the implementation were established for the parameters used for this simulation: u max. p = 0.60, k n = 0.05, u max _ z = 1.30, k p = 0.30, loss max = 1.50, k z = 0.25, r cft = We varied the input of nutrients into the system from 0.05 to 0.5 to study the sensitivity of model ecosystem structure to this parameter (B). Phytoplankton growth rates were relatively insensitive, increasing by -20% in response to a 10-fold change in 'input'. However, phytoplankton biomass increased almost 10-fold. Growth rates and nutrient concentrations actually decreased for the highest values of input. Even though this model phenomenon is interesting, we will not discuss it further since it may be a particular feature of such a simple model. are higher than -0.5 u max throughout the year. This conclusion is consistent with other evidence discussed above that also suggested that phytoplankton growth in the subtropical gyres is not severely nutrient limited with relative growth rates possibly higher than 0.5 u max. These results also demonstrate that the analogy between chemostats and the subtropical gyres might be misleading. Biomass and growth rates in chemostats are a direct function of nutrient concentrations and dilution rates, i.e. 'input'. In the open ocean, however, this tight coupling no longer holds because the removal of phytoplankton biomass, i.e. grazing, is now uncoupled from the rate at which nutrients are supplied to the system. Our observations and analysis only pertain to populations and systems that have attained steady state. The transient response of a phytoplankton community to nutrient enrichment is quite likely characterized by a significant increase in growth rates due to the higher concentrations of nutrients and the often observed shifts in the composition of the community from slow-growing flagellates to fastgrowing diatoms and possibly cyanobacteria (Glover et al, 1988; DiTullio et al., 1991; Malone et al., 1993). We found that the structure of the phytoplankton community and the growth rates of most dominant groups of microalgae were not greatly affected by the seasonally varying fluxes of nutrients into the euphotic zone (Goericke and Welschmeyer, 1993b; Goericke, 1999), consistent with our conclusions above, particularly our expectation that such systems are resilient to environmental perturbations. Thus, our conclusions are not inconsistent with 2245

24 R.Goericke and N.A.Welschmeyer observations of enhanced growth rates in response to transient nutrient enrichments. To summarize, the response of phytoplankton to seasonally varying fluxes of nutrients into the euphotic zone is quite likely not only a function of the physiology of the individual taxa, but also a result of the interactions between different trophic levels in the ecosystem. The characteristics of the interactions between trophic levels that are responsible for the observed response are not known at the present time. Our simple model portrays one possible scenario. Systems that respond to nutrient enrichment as our model system and likely the Sargasso Sea off Bermuda are quite resilient to environmental perturbations. Acknowledgements We thank Peter Brewer, Mike Bacon and Mark Altabet for inviting R.G. on their cruises to the Sargasso Sea, Amy Michelson and Keith Anderton for help at sea, Mark Altabet for samples and the Bermuda Biological Station for Research for logistic support. Penny Chisholm, Jim McCarthy, Colleen Cavenough and John Cullen commented on earlier versions of the manuscript. This research was supported by NSF grant OCE and ONR grant N K-0155 to N.A.W. References Altabet,M.A. (1989) A time-series study of the vertical structure of nitrogen and particle dynamics in the Sargasso Sea. Limnol. Oceanogr., 34, Barford,N.C. (1967) Experimental Measurements: Precision, Error and Truth. Addison Wesley Pub. Comp., Reading, MA, 143pp. BeersJ.R., Reid,F.M.M. and Steward.G.L. (1975) Microplankton of the North Pacific central gyre. Population structure and abundance, June Int. Rev. Ges. HydrobioL, 6, BeersJ.R., Reid,F.M.M. and Steward.G.L. (1982) Seasonal abundance of the microplankton populations in the North Pacific central gyre. Deep-Sea Res., 29, Bidigare,R.B., MarraJ., Dickey.T.D., Iturriaga,R., Baker,K.S., Smith,R.C. and Pak,H. (1990) Evidence for phytoplankton succession and chromatic adaptation in the Sargasso Sea during spring Mar. Ecol. Prog. Sen, 60, Brand,L.E., Sunda.W.G. and Guillard,R.R.L. (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. /. Exp. Mar. BioL Ecol, 96, CampbellJL, NollaJi.A. and VaulotJ}. (1994) The importance of Prochlorococcus to community structure in the central North Pacific Ocean. LimnoL Oceanogr., 39, Coale.K.H. et al. (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature, 383, Craigji. and Hayward.T. (1987) Oxygen supersaturation in the ocean: biological versus physical contributions. Science, 235, CullenJJ. (1982) The deep chlorophyll maximum: comparing vertical profiles of chlorophyll a. Can. J. Fish. Aquat. Sci., 39, DiTullio.G.R. and LawsJE. A. (1991) Impact of an atmospheric-oceanic disturbance on phytoplankton community dynamics in the North Pacific Central Gyre. Deep-Sea Res., 38, Dugdale,R.C. and GoeringJ-J. (1967) Uptake of new and recycled forms of nitrogen in primary productivity. LimnoL Oceanogr., 12, Eppley,R.W. (1972) Temperature and phytoplankton growth in the sea. Fish. Bull, 70, Eppley,R-W. (1981) Relations between nutrient assimilation and growth in phytoplankton with a brief review of estimates of growth rates in the ocean. Can. Bull Fish. Aquat. Set, 210, Eppley,R.W. and Peterson3-J- (1979) Particulate organic matter flux and planktonic new production in the deep ocean. Nature, 282,

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