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1 January 2008 Dissolved Nutrient Availability during Winter Diatom Bloom in a Turbid and Shallow Estuary (Bahía Blanca, Argentina)
Cecilia A. Popovich, Carla V. Spetter, Jorge E. Marcovecchio, Rubén H. Freije
Author Affiliations +
Abstract

The inner zone of Bahía Blanca Estuary is a shallow, well-mixed, highly turbid, and nutrient-rich temperate ecosystem. The phytoplankton annual cycle is characterized by a recurrent winter/early-spring diatom bloom. From May to August 2002 a research program aimed to describe the potential relations between the dynamics of phytoplankton and nutrients was carried out. Phytoplankton composition, abundance, chlorophyll a (Chl a), and dissolved inorganic nutrients (nitrate, nitrite, ammonium, phosphate, and silicate) were measured. The species involved were classified in blooming (including Thalassiosira spp. and Chaetoceros spp.) and nonblooming species (including other diatoms and dinoflagellates).

The results show: (1) a prebloom period, which includes low biomass values and a strong decrease of NO3; (2) an initial bloom period characterized by high diatom abundance and Chl a, a marked dominance of Thalassiosira curviseriata, and a strong decrease of NH4 ; (3) an intermediate bloom period of high abundance, codominance of blooming species, and a strong decrease of PO43−; and (4) a final bloom period with a decrease in abundance of blooming species and a general nutrient recovery. Thalassiosira curviseriata seems to be a species associated with high nutrient stock and low light intensity. Its growth, mainly concurrent with DIN decrease, was related to new production in this area. The obtained data suggest that low phosphate concentrations, more than DIN and silicates, contributed to the diatom bloom collapse. According to our results, this high production during winter can be explained as a net growth of phytoplankton because of a successful low light- and temperature-acclimated species, possibly favored by low predation and high nutrient availability.

INTRODUCTION

The nutrient stock in aquatic ecosystems significantly decreases when a phytoplankton bloom occurs, being transformed into biomass. In the same way, nutrient availability usually limits species growth at the end of the bloom (Howarth, 1988; Roelke, Eldridge, and Cifuentes, 1999). A general functioning model of a temperate coastal environment usually includes a nutrient cycle, with the highest levels during winter, followed by phytoplankton blooms primarily during spring and summer and secondarily in early autumn (Hallegraeff and Jeffrey, 1993; Smayda, 1980).

The inner zone of Bahía Blanca Estuary is a shallow, well-mixed, highly turbid and temperate ecosystem. Its margins include a large tidal plain, mud-dominated and partially vegetated with halophyte species (i.e., Spartina alterniflora, Sarcocornia perennis). This region is considered to be highly eutrophic because of maximum nutrient concentration reached in autumn (Freije and Marcovecchio, 2004). Its phytoplankton annual cycle is characterized by a winter/early-spring diatom bloom, which includes very recurrent blooming species, with Thalassiosira curviseriata as the dominant one (Popovich, 2004; Popovich and Gayoso, 1999). Historical (1978–1991) biomass values have reached up to 12 ×106 cells L−1, chlorophyll a (Chl a) concentrations up to 54 µg L−1 (Gayoso, 1999), and levels of primary production up to 300 mg m−3 h−1 C within the Bahía Blanca Estuary bloom (Freije and Gayoso, 1988; Freije and Marcovecchio, 2004).

This mentioned diatom bloom seems to be the most important event of the phytoplankton cycle within Bahía Blanca Estuary, not only due to its magnitude but also for its early start time. When a multispecific bloom occurs (as in the Bahía Blanca Estuary case) the comprehension of the existing relations and processes is extremely difficult. The main goal of this study is to settle the relations between nutrient availability and phtyoplankton assemblage development within Bahía Blanca Estuary.

The rates and pathways through which blooms act as agents of geochemical change are highly dependent on the species abundance and composition of the bloom communities (Cloern, 1996). In the present study the bloom was defined as a period where a deviation of a population had occurred, i.e., an increase of abundance or biomass, from its average (Smayda, 1997). The analysis was focused on dominant species, even though nonbloom stages and relations between composition and relative dominance of both blooming and nonblooming species were used.

MATERIALS AND METHODS

Study Area

The area of study involves the inner part of the Bahía Blanca Estuary (38°45′–39°40′S, 61°45′–62°30′W.), in Buenos Aires Province, Argentina (Figure 1). The sampling station Puerto Cuatreros, which is considered to be representative of this part of the estuary (Freije and Marcovecchio, 2004), is located within this region. The inner zone has a mean depth of 7 m; the water column is vertically homogeneous and highly turbid as a result of the combined effect of winds and tide currents, which maintain large amounts of suspended matter (Perillo and Piccolo, 1999). Water exchange with-in the estuary is regulated by a semidiurnal tidal wave. The Sauce Chico River discharges in the innermost region of the estuary (Figure 1), with a mean annual runoff of 1.9 m3 s−1, although autumnal rainfalls can increase to flows up to 106 m3 s−1 (Piccolo, Perillo, and Arango, 1990). A branch of this river discharges near the sampling station (Figure 1). In addition, freshwater input from other smaller tributaries into the estuary is intermittent and only significant during periods of high local rainfall.

Sampling

From May 3. until August 26. 2002, on a twice-a-week basis, water samples were collected at Puerto Cuatreros during high tide and daylight hours. Water samples were collected near the surface (approximately 0.50 m depth) with a 2.5-L Van Dorn bottle to analyse nutrients, Chl a, phaeopigments, and phytoplankton. Temperature, conductivity/salinity, pH, turbidity, and dissolved oxygen (DO) were in situ measured using a Horiba U-10 multisensor probe. Photosynthetically active radiation (PAR) in the sampling layer was measured by a submersible Li-Cor 192SB. Data of daily precipitation and historical (10 years) total monthly precipitation at Bahía Blanca City were obtained from the Argentine National Meteorological Service.

Water samples for the study of dissolved inorganic nutrients were filtered through Whatman GF/C and were frozen in plastic bottles until analysed. Nitrate (NO3), nitrite (NO2), ammonium (NH4+), phosphate (PO43−), and silicates were determined following the methods of Treguer and Le Corre (1975), Grasshof, Erhardt, and Kremling, (1983), Richards and Kletsch (1964), Eberlein and Kattner (1987), and Technicon®(1973), respectively. Dissolved inorganic nitrogen concentrations were calculated as the sum of NO3, NO2, and NH4+. A Technicon AA-II Autoanalyzer expanded to five channels was used to perform the nutrient analyses.

Chlorophyll a and phaeopigment concentrations were measured according to the method of the American Public Health Association (APHA), AWWA, WEF (1998).

Samples for quantitative analysis of phytoplankton were preserved with acid Lugol's solution. Abundance of phytoplankton species was determined by enumeration of cells in a Sedgwick-Rafter chamber (McAlice, 1971) using an inverted light microscope (Nikon, Eclipse RE 300). For identification purposes bottle sampling was complemented by surface samples taken with a Nansen 30-µm net, preserved in 4% formaldehyde and examined under a Zeiss Standard R microscope in phase contrast mode. Identified taxa were classified according Gayoso (1999) in blooming and nonblooming species.

Samples were also grouped in bloom and nonbloom samples according to composition, abundance, and dominance degree of the main species for each sampling date (Ignatiades, 1994). Dominance was assessed using a dominance index (DI), that is, percentage of the total standing crop contributed by the two most important species and calculated as

i1551-5036-24-1-95-eq01.gif
where N1 and N2 are the number of individuals of the two most abundant species and N is the total number of individuals. The relative dominances of the first (dominant species) and the second (subordinate species) main species (RD1 and RD2) were calculated as 100(N1/N) and 100(N2/N), respectively.

RESULTS

Environmental Variables

During the considered period subsurface water temperature decreased from 11.9°C to 5.4°C (on July 12), and then increased to 10.7°C (Figure 2a). Salinity did not show significant fluctuations (30.4–32.8 psu), with only one minimum value of 28.1 psu on Aug 23 (Figure 2a). Total daily precipitation was generally scarce and ranged between 0.0 and 39.9 mm (National Meteorological Service). Dissolved oxygen concentration and pH showed values between 6.8 and 10.54 mg L−1 and 8 and 9.55, respectively. In addition, from June 19 to July 19 both percentage of oxygen saturation and pH had values of 93–108% and 8.6–9.55, respectively((Figure 2b).

Turbidity was extremely high and varied between 13 and 147 ntu (nephelometric turbidity units) (Figure 2c). Consequently, light intensity was very low and varied between 14.85 and 128.71 µE m−2 s−1.

Phytoplankton Abundance, Chl a, and Dominant Species

Both total phytoplankton abundance and Chl a concentrations (Figure 3) showed a winter diatom bloom (June to August) in the inner zone of Bahía Blanca Estuary; the phytoplankton community was dominated by an assemblage of blooming species (Thalassiosira spp. and Chaetoceros spp.) together with nonblooming species (other diatoms and dinoflagellates) (Table 1).

From June 19. to July 1. Thalassiosira curviseriata was the dominant species (Table 2). During this period Chl a concentrations reached two peaks, 44 µg L−1and 30.4 µg L−1 (Figure 3a), in correspondence with maximum in diatom numbers (4 × 106 cells L−1 on June 19 and 3.5 × 106 cells L−1 on June 28) (Figure 3b). During this period dinoflagellate abundance was low (10 × 103 cells L−1) (Figure 3b).

The samples associated with these data had high values of DI (73.39–96.2 %) (Table 2). Of blooming species, 90%, including Thalassiosira spp. and Chaetoceros spp., were recorded during this period, but T. curviseriata was always the dominant one (relative dominance RD1 > 64.5%) (Table 2). In each sample the total cell abundance surpassed 1 × 106 cells L−1, and 64.5–81.89% of this increase was due to T. curviseriata, 6.75–31.7% to the subordinate one (T. hibernalis or T. eccentrica) (Table 2), and the rest to all the other species in the assemblage (Figure 4). Thalassiosira curviseriata was the only blooming species that occurred during May (in the prebloom period), appearing in all the analysed samples, and also increasing its abundance.

On July 4 the composition of dominant species changed and until July 19 the phytoplankton community was codominated by several blooming species, mainly by Chaetoceros spp and bigger species of Thalassiosira (Table 2). The maximum Chl a value was 23.9 µg L−1, while the diatom abundance reached 5 × 106 cells L−1 (July 12) (Figures 3a, 3b). Moreover, dinoflagellate abundance increased up to 80 × 103 cells L−1 (Figure 3b).

This period has been characterized by the occurrence of smaller DI values (36–48%) and smaller and homogeneous values of relative dominance (RD < 31.51%) in comparison with first period (June 19 to July 1) (Table 2). The total cell abundance has surpassed 1 × 106 cells L−1 in each sample; however, 19.6–31.5% of this increase was due to the first dominant species (Chaetoceros spp., T. curviseriata or T. hibernalis), 16.4–19.59% to the subordinate one (Chaetoceros spp., T. eccentrica, or T. curviseriata), and the rest to all the other species in the assemblage (Figure 4). Among the nonblooming species Guinardia delicatula was the most outstanding, reaching values of 4.7 × 105 cells L−1 while the dinoflagellate Scripsiella trochoidea rapidly increased up to values close to 80 × 103 cells L−1.

A different dominance pattern was observed from July 30 to August 12. The occurrence of a dominant blooming species was always linked to a nonblooming one (like Cyclotella meneghiniana or Leptocylindrus minimus) (Table 2). The biomass decreased down to minimum values of 9.7 µg L−1 Chl a and 3.3 × 105 cells L−1 (Figures 3a, 3b) and only 45% of blooming species appeared. The dinoflagellate S. trochoidea remained present in the samples up to August 2, when it was replaced by an unidentified dinoflagellate (length 27 µm) that reached up to 90 × 103 cells L−1 (Figure 3b). The contribution of both the blooming species and the nonblooming species to the total phytoplankton abundance ranged between 40% and 50% (Figure 4). Finally, August 12 was the last day of bloom, taking in consideration that from August 16 both dominant species were nonblooming ones (G. delicatula, L. minimus, and Cerataulina pelagica) (Table 2).

Nutrient Availability

The highest nutrient concentrations determined during the prebloom period (May) have been considered as the available nutrient stock (Figure 5). Thus, the maximum concentrations that were observed were NO3 (10.8 µM), NO2 (1.6 µM), NH4+ (102.82 µM), PO43− (1.6 µM), and silicates (121.28 µM). Nitrite and nitrate showed an abrupt fall in coincidence with the first biomass peak (June 19) (Figure 5a). NO2 decreased down to values of 0.24 µM and NO3 down to nondetectable values (n.d. µM) (Figure 5a); after this, a NO3 partial recovery (3.08 µM) was observed. NH4+ was the dominant form of DIN and its concentration quickly decreased to 14.28 µM just before the occurrence of the second biomass peak (June 28), after which the concentration remained stable and close to 15 µM (Figure 5b). This ammonium decreasing process occurred 6 weeks after the starting point of the decrease of nitrate and nitrite. PO43− concentration rapidly decreased to 0.95 µM (Figure 5c) at the first biomass peak, and then progressively increased (1.36 µM). The silicate concentrations showed a steady decrease to 85.95 µM (Figure 5c).

Following this trend, the DIN/PO43− ratio (Figure 5d) increased from 60 (before bloom) to 100, concurring with the first biomass peak and showing a strong use of P with respect to N. However, among N sources, it must be mentioned that while a strong NO3 and NO2 decrease occurred, both the high NH4+ concentration and the PO43− concentration decrease contributed to the DIN/PO43− increase. Thus, these high N/P values, as when they were related to those of Redfield (1958), together with PO43− concentrations close to 1 µM, should not be interpreted as evidence of P limitation. Before the second biomass peak, the strong NH4+ decrease, the low NO3 and NO2 values, and the partial PO43− recovery contributed to the sharp decrease of the DIN/PO43− ratio down to 14.3 (Figure 5d).

From July 4 to July 19 and in correspondence with peaks of codominant blooming species, all of the analysed nutrients reached their minimum values (Figures 5a–d); however, ammonium concentrations were never less than 14.6 µM. The DIN/PO43− atio increase (13 to 77) (Figure 5d), concurring with the abundance of peaks of codominant blooming species, indicated high P consumption. Finally, August 12 was the starting point of all the nutrient recovery within the system (Figure 5).

DISCUSSION

High levels of phytoplankton biomass were associated with depletion of NO3 (nondetectable values), minimum values of PO43− (around 0.2 µM), and silicates (around 35 µM); oxygen saturation percentage (up to 108%); and increase of pH (up to 9.5) during the sampling period. These variations have been observed in many other temperate bays and estuaries during bloom periods (Cabeçadas, Nogueira, and Brogueira, 1999; Cloern, 1996 and cites therein; Townsend and Thomas, 2002), and have been associated with phytoplankton productivity. Cloern (1996) has pointed out that these large fluctuations in the water indicate a net autotrophic ecosystem. The increase of biomass (Chl a up 44.3 µg L−1), which characterized the beginning of the bloom within the inner zone of Bahía Blanca Estuary, was almost (64.5–81.89%) because of T. curivseriata growth, while the subsequent increases of abundance were the result of a community 50% codominated by different blooming species.

The highest nutrient concentrations at the sampling site were observed in autumn (prebloom period), in accord with the general pattern of nutrients within the inner zone of Bahía Blanca Estuary (Freije and Marcovecchio, 2004). These values were relatively higher than those reported for Río de la Plata Estuary, which is the Argentina's largest one and which is strongly dominated by riverine input (Calliari, Gómez, and Gómez, 2005). In the case of NH4+, our values were even similar to the highly eutrophic Colne Estuary (at the seaward end), which is influenced by anthropogenic inputs (Kocum, Underwood, and Nedwell, 2002). Bahía Blanca Estuary shows low influence of riverine input; however, Sauce Chico River discharge at the inner area of this estuary, with high load of DIN, has been shown to be an important source of dissolved nutrients to this system, mainly during autumn (prebloom period) and spring (postbloom period) when its flow increases because of high precipitation within the region (Piccolo, Perillo, and Arango, 1990) (Figure 6). In particular, inflow from Sauce Chico River supplied up to 220.5 µM of nitrate and 118.6 µM of ammonium (R.H. Freije, personal communication). These high concentrations of N may be partially explained by considering that the studied catchments cross over a region with intense farming and cattle-raising activities. In addition, the occurrence of both the nutrient regeneration process within the water–sediment interface as well as the zooplankton activity increase during the postbloom period within these shallow waters must be considered (Barría de Cao, Beight, and Piccolo, 2005; Hoffmeyer, Frost, and Castro, 2000), together with other sources (e.g., adjacent salt marshes, anthropogenic inputs) that may contribute to nutrient increase during spring and summer. Thus, the river runoff appears to be a potential important source of N for new production (sensu, Dugdale and Goering, 1967) in the inner zone of Bahía Blanca Estuary.

The decrease in concentration of maximum dissolved nutrient stock started close to a month before the bloom regardless of corresponding sources. A lag in response of phytoplankton blooms to nutrient availability has been associated with mechanism of uptake by phytoplankton (Gentilhomme and Lizon, 1998). Our results show that mainly the use of nitrate, even at high NH4+ concentrations (around 100 µM), agrees with T. curviseriata growth. When NO3 decreased close to 1.6 µM (but not depleted from the water column), NH4+ appeared to be the main source of N that supported the second abundance peak of this species. These maximum population points were strongly linked with highest Chl a concentrations, suggesting that DIN—unlike P and Si—was responsible for the highest primary production in this area. Nevertheless, and bearing in mind the observed trends of the N sources, this type of use could occur gradually, alternating the utilization of NO3 to NH4+ Our observation must be correlated with many studies about uptake of NO3 by phytoplankton, especially from coastal and estuarine environments, at high NH4+ levels (Comin and Valiela, 1993; Kudela and Dugdale, 2000). Even this mechanism up to the present has not been fully understood; both cultivated and natural phytoplankton communities have evidenced an optimum nitrate uptake under low light conditions (Leonardos and Geider, 2004; Martinez, 1991; Needoba and Harrison, 2004). Thalassiosira curviseriata, isolated from this environment, showed high α values (slope of light-limited growth) and maximum growth rate at low light intensities (saturation intensity 70–80 µE m−2 s−1) (Popovich and Gayoso, 1999). So, the potential ability of T. curviseriata to play a significant role as a colonist species (equivalent to C-strategies of Reynolds and Smayda, 1998) in environments with high nutrient stock (especially DIN availability) and low irradiance must be fully assessed in future studies, mainly in experimental ones.

The increase in abundance of populations that codominated the phytoplankton assemblage during the intermediate period of the bloom agree with lower Chl a concentrations as well as with a lower stock of available nutrients. NH4+ was the main source of N, showing stable values (around 15 µM) up to the end of the bloom, irrespective of phytoplankton abundance increase. During this dry winter period, both the relatively constant values of NH4+and undetectable values of nitrate suggest alternative sources of N relative to riverine input ones. Zooplankton grazing as studied during winter bloom in this environment showed a coupling of aloricate ciliates (microzooplankton) and diatom populations, particularly on the phytoplankton cells <25 µm (Pettigrosso, Barria de Cao, and Popovich, 1997). Ciliates with T. curviseriata (valve diameter 6–21.5 µm) in their food vacuoles have frequently been observed (Pettigrosso, 2003). Bacterially mediated degradation of organic matter from sediments and regeneration through grazing and excretion by microheterotrophs (“regenerated nitrogen”) were recognized as an important source of NH4+ to sustain algal growth in shallow coastal environments when tributary inputs were low (Bode et al., 2005; Shostell and Bukaveckas, 2004). In our environment, the occurrence of a trophic coupling between diatom bloom and aloricate ciliate could play a double role: on the one hand, they could represent a potential source of NH4+ to “regenerated production” (sensu, Dugdale and Goering, 1967). On the other hand, they could favor the growth of blooming species of larger size (Thalassiosira pacifica, T. rotula, T. angustelineata, etc.) and Chaetoceros spp., as those found in advanced stages of bloom. The Chaetoceros dominance within other environments has been explained, considering that it is not an optimal food source for many ciliates (Haigh et al., 1992). Moreover, during the intermediate period the increase of DIN/PO43− values (20 to 80), in correspondence with peaks of abundance of codominant blooming species, suggests that mainly phosphate (more than N) was removed from water by the growing phytoplankton, reaching values around 0.2 µM. After this, the biomass decreased, and bloom finished in early August. Dortch and Whitledge (1992) indicated limitation of P if N/P > 30 and PO43− < 0.2 µ M. So, P appeared to be the main potential limiting nutrient for this blooming diatom community. This effect was clearer than that of silicate (>35 µM) and DIN (around 15 µM of NH4+). Phosphate limitation had already been reported in many coastal and estuarine systems (Benitez-Nelson, 2000; Fisher et al., 1999; Flynn, 2002) and its largest effect was linked to limitation of winter and spring production (Conley, 2000 and references therein). Additionally, diatoms are poor competitors for phosphate compared with other groups (flagellates), although silicate is in excess (Egge, 1998). Dinoflagellate abundance increase at a later stage of bloom in Bahía Blanca Estuary may be indicating some competitive strategies of this phytoplankton community. Additionally, the significant increase of the autochthonous copepod Acartia tonsa (omnivorous) and Eurytemora americana (herbivorous) in August and September occurring within Bahía Blanca Estuary (Hoffmeyer, Frost, and Castro, 2000) could help to explain the mentioned diatom bloom collapse.

Both nutrients and phytoplankton biomass data recorded along a longitudinal transect within Bahía Blanca Estuary showed a negative gradient toward the outer zone of the estuary (Popovich, 1997), indicating that the inner estuary performs as the original area of the bloom as well as a source of inorganic nutrients. Under this context, our results suggested that the successful development of an autochthonous diatom community within the inner zone of the Bahía Blanca Estuary during winter may represent an important mechanism of eutrophication regulation within coastal waters. In the inner Bahía Blanca Estuary the tidal velocity is 0.69–0.77 m s−1 (Pérez and Perillo, 1998) and the water residence time is near 28 days (G.M.E. Perillo, personal communication), conditions under which a strong utilization of nutrients in the inner zone might be expected. In estuaries, the dynamics of nutrients and hence primary productivity are strongly dependent upon their external supply and regeneration. Our results indicate that during the early stage of winter bloom, the dominance of T. curviseriata (“new production”) will be favored by autumnal nutrient freshwater input, in combination with other environmental factors (i.e., low light intensities, shallow mixing, low predation, and low temperatures). During later stage ones, in situ nutrient regeneration will sustain the production of other blooming species (“regenerated production”), in comparison to tributary loadings. From these considerations emerge the hypothesis that in this extremely turbid environment, different mechanisms of nutrient production (inputs, regenerations) could act in the inception, magnitude, and duration of winter diatom bloom. The solutions to this hypothesis emphasize our need for a better understanding of mechanisms of nutrient cycling estuaries (reservoir and turnover). As a first step, studies conducted to investigate the nutrient dynamics for different compartments within the system (surface estuarine water, porewater, and sediments) will be published.

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Appendices

Figure 1.

Map of the Bahía Blanca Estuary, indicating the localization of Puerto Cuatreros (sampling station) in the inner zone of the estuary.

i1551-5036-24-1-95-f01.gif

Figure 2.

Temperature and salinity (a), dissolved oxygen percentage and pH (b), and turbidity (c) at Puerto Cuatreros during the sampling period (May–August 2002).

i1551-5036-24-1-95-f02.gif

Figure 3.

Variation of chlorophyll a concentration (a) and diatom and dinoflagellate abundances (b) at Puerto Cuatreros over time.

i1551-5036-24-1-95-f03.gif

Figure 4.

Abundance of Thalassiosira spp. (a), Chaetoceros spp. (b), and nonblooming species (c) in the sampling station over time. Denomination of taxa as in Table 1.

i1551-5036-24-1-95-f04.gif

Figure 5.

Dissolved nutrients concentrations: nitrite and nitrate (a), ammonium (b), phosphate, and silicates (c), and DIN, DIP concentrations and DIN/PO43− ratio (d) at Puerto Cuatreros during the sampling period (May–August 2002).

i1551-5036-24-1-95-f05.gif

Figure 6.

Variation of historical monthly precipitation at the Bahía Blanca City (Argentine National Meteorological Service)

i1551-5036-24-1-95-f06.gif

Table 1.

Assemblage of blooming species and nonblooming species and their maximal abundance observed during the sampling period (May–August 2002).

i1551-5036-24-1-95-t01.gif

Table 2.

Dominant species composition, relative dominance (RD1 and RD2), and dominance index (DI) during the sampling period.

i1551-5036-24-1-95-t02.gif
Cecilia A. Popovich, Carla V. Spetter, Jorge E. Marcovecchio, and Rubén H. Freije "Dissolved Nutrient Availability during Winter Diatom Bloom in a Turbid and Shallow Estuary (Bahía Blanca, Argentina)," Journal of Coastal Research 2008(241), 95-102, (1 January 2008). https://doi.org/10.2112/06-0656.1
Received: 22 February 2006; Accepted: 1 July 2006; Published: 1 January 2008
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