Short-term variability of primary production and inorganic nitrogen uptake related to the environmental conditions in a shallow coastal area (Gulf of Trieste, N Adriatic Sea)

Oceanologica Acta 26 (2003) 565–575 www.elsevier.com/locate/oceact

Original article

Short-term variability of primary production and inorganic nitrogen uptake related to the environmental conditions in a shallow coastal area (Gulf of Trieste, N Adriatic Sea) Variabilité à court terme de la production primaire et de l’assimilation d’azote inorganique en liaison avec l’environnement dans une aire côtière de faible profondeur (golfe de Trieste, Adriatique Nord) Carolina Cantoni a,*, Stefano Cozzi a, Irene Pecchiar b, Marina Cabrini b, Patricija Mozeticˇ c, Giulio Catalano a, Serena Fonda Umani b a

CNR—Istituto Sperimentale Talassografico, Viale Gessi 2, 34123 Trieste, Italy Laboratory of Marine Biology, Trieste, Via Piccard 54, 34010 Trieste, Italy c National Institute of Biology, Marine Biology Station, Fornace 41, SI-6330 Piran, Slovenia b

Received 17 December 2002; revised and accepted 31 March 2003

Abstract Primary production (PP) and nitrate (QNO3) and ammonium (QNH4) uptakes were measured together with other environmental parameters from October 1999 to February 2001 in the Gulf of Trieste (N Adriatic Sea). Their trends showed a high variability because of the combined effects of meteorological conditions, water circulation and river discharges. PP ranged from 0.2 to 15.9 µmol C dm–3 d–1, whereas QNO3 varied from 0.8 to 442 nmol N dm–3 d–1, showing a trend similar to that of carbon basically ascribable to the autotrophic activity. QNH4 ranged from 20 to 1308 nmol N dm–3 d–1 and it reached the highest values during the declining phases of phytoplankton blooms, indicating that bacterial community can also be involved in its uptake. Regenerated PP generally prevailed over the new production (depth-integrated f-ratios from 0.05 to 0.50). C/N uptake ratios by planktonic community (annual average of 16 ± 11) showed the repetitive carbon overconsumption (23–33) during periods of high production, and lower values (2–13) during the post-bloom phases and in the months of scarce autotrophic activity. Residence time of freshwater in the area (1 d in November and January, up to 23 d in July) indicated the fast export of low salinity waters in winter and their longer permanence in summer. These values were closer to the ammonium turnover times (1–34 d) than to the nitrate ones (2–831 d). Riverine nitrate load (3–67 t N d–1) generally exceed the biological demand of this nutrient (uptakes from 0.2 to 8 t N d–1), whereas the ammonium load (0.1–3.3 t N d–1) was almost always insufficient (uptakes from 2.6 to 33 t N d–1). These results evidenced the major role of physical transport and recycling processes to regulate, respectively, nitrate and ammonium availability in this shallow ecosystem. © 2003 Éditions scientifiques et médicales Elsevier SAS and Ifremer/CNRS/IRD. All rights reserved. Résumé La production primaire et l’assimilation de nitrates et d’ammonium ont été mesurées en même temps que les facteurs du milieu entre octobre 1999 et février 2001 dans le golfe de Trieste. La variabilité est élevée en raison de l’action combinée des conditions météorologiques, de la circulation et des apports des rivières. La production primaire varie entre 0,2 et 15,9 µmol C dm–3 j–1 alors que l’assimilation de nitrates va de 0,8 à 442 nmol N dm–3 j–1, montrant une tendance identique au carbone lié à la production autotrophe. L’assimilation d’ammonium varie entre 20 et 1308 nmol N dm–3 j–1 et elle atteint ses valeurs maximales durant le déclin de la floraison planctonique, indiquant que la communauté bactérienne est impliquée dans cette assimilation. La production primaire régénérée surpasse la production nouvelle (le facteur f intégré en fonction de la profondeur varie entre 0,05 et 0,5). Les taux C/N d’assimilation de la communauté planctonique (moyenne annuelle de 16 ± 11) soulignent la surconsommation répétitive de carbone (23–33) durant les phases de production actives ; les valeurs minimales * Corresponding author. E-mail address: [email protected] (C. Cantoni). © 2003 Éditions scientifiques et médicales Elsevier SAS and Ifremer/CNRS/IRD. All rights reserved. doi:10.1016/S0399-1784(03)00050-1

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(2–13) caractérisent les phases postérieures à la floraison et les mois de faible activité autotrophe. Le temps de résidence d’eau douce dans la zone (d’un jour en novembre et janvier à 23 jours en juillet) indiquent l’exportation rapide d’eau de basse salinité en hiver et leur permanence en été. Ces valeurs sont plus proches des temps de renouvellement de l’ammonium (1 à 34 jours) que des nitrates (2 à 831 jours). L’apport de nitrates par les fleuves (3–67 t N j–1) surpasse les besoins (0,2 à 8 t N j–) alors que l’apport d’ammonium (0,1–3,3 t N j–1) est presque toujours insuffisant (assimilation de 2,6 à 33 t N j–). Ces résultats mettent en lumière le rôle majeur du transport et du recyclage dans la régulation de la disponibilité en nitrate et ammonium dans des écosystèmes de faible profondeur. © 2003 Éditions scientifiques et médicales Elsevier SAS and Ifremer/CNRS/IRD. All rights reserved. Keywords: Primary production; New production; Nutrients; Turnover time; Riverine inputs Mots clés : Production primaire ; Production nouvelle ; Nutriments ; Temps de renouvellement ; Apports de rivières

1. Introduction Several studies of primary production (PP) have been performed in the northern Adriatic Sea (Zoppini et al., 1995; Degobbis et al., 2000; Socal et al., 2002; Vadrucci et al., 2002; but see Fonda Umani et al., 1992; Harding et al., 1999 for references), although the Gulf of Trieste has received less attention (Faganelli et al., 1982; Olivotti et al., 1986; Fonda Umani, 1991; Malej et al., 1995; Mozeticˇ et al., 1998). On the contrary, studies on the inorganic nitrogen uptake are still lacking for this basin and the few available data (Cozzi et al., 2002) do not permit an extensive evaluation of this process. At the same time, scarce data are available on the comparison between inorganic nitrogen uptake and the carbon-based PP in coastal areas worldwide (Fisher et al., 1982; Carpenter and Dunham, 1985; Dauchez et al., 1991; Tremblay et al., 2000; Diaz et al., 2000). This comparison provides useful information on the state and growth of planktonic communities. Carbon and nitrogen demands are modulated on short temporal scales by phytoplankton depending on the physiological state of the growing cells, on the physical conditions in the marine environment and on the nutrient availability (Harris, 1986). Cells assimilate nitrogen mainly for structural purposes and thus its uptake basically estimates the population growth. On the contrary, carbon and phosphorus are used also in energetic processes (Dugdale and Goering, 1967). Moreover, inorganic nitrogen uptake also allows the distinction between “new” (i.e. based on newly available inorganic nitrogen from outside the euphotic layer; NO3) and “regenerated” (i.e. based on recycled inorganic nitrogen inside the euphotic layer; NH4) PP. This concept is also used to evaluate the net carbon PP exported from the euphotic zone toward the deeper waters, which is believed to be equal, on large spatial and temporal scales, only to new PP (Tremblay et al., 2000; Bury et al., 2001). The present study improves the knowledge of the interactions among production processes, nitrogen cycling and environmental conditions in the Gulf of Trieste. Bloom successions, carbon to nitrogen uptakes and phytoplankton community structures are analyzed with respect to the most important environmental parameters, on the basis of an interdisciplinary approach. Temporal scales with which riverine nutrient loads, circulation and uptakes affect the nutrient balance in the area are also investigated, in order to evaluate

Fig. 1. Sampling stations in the Gulf of Trieste, monitored area (ROI, delimited by the solid line) and position of the mouths of Isonzo and Timavo rivers. Timavo river is a karst stream whose water flows below the ground until the coast.

the effect of the timing of these processes on the ecosystem of the Gulf of Trieste. This study also provides the first data of inorganic nitrogen uptake available in the area. The research activity was carried out under a monitoring project (Interreg II, Italy and Slovenia, 1998–2001) in the Gulf of Trieste (northern Adriatic Sea). 2. Materials and methods 2.1. Study site and sampling strategy The Gulf of Trieste is a shallow coastal area (maximum depth of 25 m), located at the northernmost end of the Adriatic Sea (Fig. 1). Its oceanographic properties are strongly affected by water masses exchange at the open boundary and by variable local meteorological conditions.

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Moreover, the pronounced seasonal cycle in the region determines strong variations of seawater temperature, total irradiance and stratification of the water column during the year (HMSO, 1962; Malacˇicˇ and Petelin, 2001). Isonzo River also exerts an important impact on the dynamics of the Gulf of Trieste, being other rivers only about 10% of the freshwater balance (Olivotti et al., 1986). During winter, its plume generally flows outside the gulf, following a narrow coastal jet along the Italian coast. On the contrary in spring, summer and autumn, freshwater often spreads on large areas, reaching the middle of the gulf (Malacˇicˇ and Petelin, 2001; Malej et al., 1995). Although in a limited way, Timavo River inputs contributes to freshwater balance, being mixed to the Isonzo plume in the northern side of the gulf. Circulation of deeper waters is often cyclonic and it can be opposite to that in the upper layer. Northern Adriatic bottom waters enter in the gulf at the southern side and eventually they flow out, mostly in the shallow northern area, after mixing with the upper waters (Malacˇicˇ and Petelin, 2001). Residual currents in the area are of about 1–3 cm s–1, but total currents higher than 30 cm s–1 can be found in the upper layer, because of the tidal effect and particularly in concomitance to strong Bora wind (ENE) events (Mosetti and Purga, ˇ etina, 1991). 1990; Mosetti and Mosetti, 1990; Rajar and C These physical features affect PP and planktonic community structures, particularly as regards freshwater to advection, which supplies a large quantity of land-born nutrients to this ecosystem (Gilmartin and Relevante, 1983; Malej et al., 1995). Data were collected during 15 cruises, from October 1999 to February 2001, at seven stations (depth from 7 to 23 m), representatives of the northern side of the Gulf of Trieste. The investigated region of interest (ROI; Fig. 1) had a dimension of 11 × 16 km and a total seawater volume of 2.715 km3. Salinity, temperature and underwater PAR (uw-PAR) profiles were acquired using, respectively, the Idronaut 316 and the PNF 300 Biospherical probes. Seawater samples for chemical analysis and incubations were collected using 5 l Niskin bottles at the surface, one or two intermediate depths (about 7 and 15 m) and 1 m above the bottom. Depths were chosen on the basis of CTD and fluorescence profiles, to sample at the chlorophyll maximum and in all water masses detected in the water column. Flow rates (daily average) and nutrient concentrations (monthly sampling) of the Isonzo and Timavo Rivers, and total irradiance at Trieste (monthly average) were kindly provided by Direzione Regionale dell’Ambiente (Friuli Venezia Giulia Region), ARPA (Agenzia Regionale per la Protezione dell’Ambiente) and ACEGAS (Acqua Elettricità Gas e Servizi).

(DIN) concentrations were calculated as the sum of NO3 + NO2 + NH4. Phytoplankton cell abundance was estimated in samples of 500 ml, fixed with 20 ml of buffered formalin. Subsamples of 50 ml were taken and analyzed according to Utermöhl (Zingone et al., 1990), using an inverted microscope (320– 400 × magnification). Taxonomic determination of phytoplankton community was carried out using the casual field counting procedure (Zingone et al., 1990). Samples collected for 14C PP were placed in 70 ml polycarbonate bottles and incubated at the underwater irradiance, screening bottles with photographic filters. They were chosen each time among the available ones (100%, 45%, 23%, 10%, 7%, 4%, 1% of surface PAR) to simulate the uw-PAR at the sampling depths. Samples were inoculated with 6 µCi NaH14CO3 sterile solution (Steemann Nielsen, 1952) and placed for 3 h around midday in an on-deck incubator at the seawater temperature. They were then filtered on 0.2 µm polycarbonate Whatman Nuclepore filters and soaked in scintillation vials with a few drops of 5% HCl. 14C activity of each filter was determined by scintillation counting method (Knudson et al., 1989). To calculate the daily PP, the hourly data were integrated on the basis of daylight surface PAR measured in µE m–2 d–1. For a better comparison with nitrogen uptake rates, PP data are presented in molar units (µmol C dm–3 d–1) instead of usual weight units. Inorganic nitrogen uptake rates (nmol N dm–3 d–1) of nitrate (QNO3) and ammonium (QNH4) were determined using, respectively, Na15NO3 and 15NH4Cl labeled reagents, according to Dugdale and Goering (1967) and Owens (1988). These measurements of nitrogen assimilation were obtained after 24 h incubation of 500 ml samples, carried out at the same temperature and PAR used for 14C PP. Samples were filtered on precombusted Whatman GF/F filters, dried at 60 °C and combusted on an Europa ANCA elemental analyzer online with an Europa 20/20 isotope ratio mass spectrometer. Ammonium regeneration experiments were not carried out; therefore QNH4 data could underestimate the “true” values of ammonium uptake being uncorrected for 15 NH4–isotope dilution. Nitrate and ammonium uptakes were also used to calculate the f-ratio (f = QNO3/(QNO3 + QNH4)), which formally represents the importance of “new” PP with respect to the “regenerated” PP (Eppley and Peterson, 1979).

2.2. Nutrients and assimilation of C and N

Evolution of oceanographic properties was analyzed on the basis of data collected in all sampling stations, whereas production processes were determined in three stations located in different sites of the ROI (Fig. 1). However in order to reduce the dataset, temporal variability of this ecosystem is discussed only with respect to the station AA1, which has

Inorganic nutrients (nitrate, NO3; nitrite, NO2; ammonium, NH4; reactive phosphorus, PO4; reactive silicate, SiO2) were analyzed following standard spectrophotometric methods (Grasshoff, 1983). Dissolved inorganic nitrogen

3. Results and discussion 3.1. Short-term variability of production processes in the Gulf of Trieste

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Fig. 2. Temporal patterns at the station AA1 of (a) 14C PP (µmol C dm–3 d– (b) nitrate uptake (QNO3; µmol N dm–3 d–1) and (c) ammonium uptake (QNH4; µmol N dm–3 d–1).

Fig. 4. (a) Temporal patterns of salinity (PSU), (b) nitrate concentration (µmol N dm–3) and (c) ammonium concentration (µmol N dm–3) at the station AA1.

been recognized as the most representative of the whole area. During the period of investigation, we distinguished four situations that are analyzed separately, with comprehensive analysis of physical, chemical and biological processes (Figs. 2–7).

mainly constituted by small phytoflagellates, being the diatom population not yet grown. Inorganic nitrogen uptakes were also low and their values (QNH4 and QNO3 down to 159 and 6 nmol N dm–3 d–1, respectively) showed the prevalence of ammonium assimilation, as confirmed by the integrated f-ratio of 0.03 (Fig. 3). During winter, freshwater inputs rich of nitrate (Fig. 5) are not always available for the phytoplankton community, as the Isonzo River plume is basically restricted to a narrow belt that rapidly flows outside the area in the SW direction, along the Italian Coast (Malacˇicˇ and Petelin, 2001; Malej et al., 1995). This dynamics was confirmed by the presence in the middle of the gulf of the northern Adriatic offshore waters, characterized by high salinity (37.5–38.3), low NO3 concentrations (Fig. 4) and high DIN:PO4 (92) and Si:PO4 (156) ratios (Fig. 6). In January 2001, nitrogen uptake was anticipated with respect to the 2000, although PP was still low (200 mg C m–2 d–1). In this case, environmental conditions in the Gulf of Trieste were more favorable compared to the previous year,

1),

3.1.1. Early winter (January 2000 and 2001) January 2000 was characterized by rather low values of PP (530 mg C m–2 d– 1; Fig. 2) and by a scarce phytoplankton abundance (160,000 cell dm–3; Fig. 3), as a result of the typical winter conditions characterized by scarce irradiance (>6000 kJ m–2 d–1), low seawater temperature (8 °C) and mixed water column (Fig. 4). Phytoplankton community was

Fig. 3. (a) Abundance of the main classes of phytoplankton (cell dm–3) and (b) f-ratio and molar ratio between carbon and nitrogen uptakes (C/Nup = PP/(QNO3 + QNH4)) at the station AA1, calculated as depthintegrated values.

Fig. 5. Flow rates (daily average, m3 s–1) of the Isonzo and Timavo rivers and dates of the cruises in the ROI.

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Fig. 6. (a) DIN:PO4 ratio and (b) Si:PO4 ratio at the station AA1 (depthintegrated values). Solid line indicates the average (n = 26) of the DIN:PO4 ratios of the Isonzo and Timavo freshwaters.

because of the higher seawater temperature (12 °C) and stronger river loads (up to 1016 m3 s–1). Riverine inputs increased NO3 concentrations in the upper waters (up to 4.2 µmol N dm–3) stimulating its uptake (QNO3 up to 73 nmol N dm–3 d–1, f-ratio of 0.2) by a phytoplankton community mainly constituted by diatoms (Skeletonema costatum and Pseudonitzschia spp.: 570,000 cell dm–3; Fig. 3). 3.1.2. Late winter and early spring (February–April 2000, February 2001) The first event of high PP was observed since February 2000 (Fig. 2), when PP and QNO3 increased in the upper layer, to reach the maximum in March (15 µmol C dm–3 d–1 and 162 nmol N dm–3 d–1). Phytoplankton abundance strongly rose with respect to the previous months (up to 1,500,000 cell dm–3), because of the intense growth of diatoms such as Pseudonitzschia delicatissima, S. costatum and Chaetoceros pseudocurvisetus. This observation confirms the importance of diatoms as organisms responsible for the early spring bloom of the Gulf of Trieste (Malej et al., 1995).

Fig. 7. Monthly averages of (a) air temperature (°C) and total irradiance (kJ m–2 d–1) at Trieste. (b) Temporal pattern of seawater temperature (°C) at the station AA1.

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Carbon and nitrate uptakes (Fig. 2) were well matched on temporal (from February to March) and spatial (higher values in the upper layer) scales. On the contrary, QNH4 showed increasing values (from 46 to 197 nmol dm–3 d–1) largely distributed in most of the water column. This early phytoplankton bloom was triggered by the modification of some environmental conditions that is typically met in the Gulf of Trieste at the end of winter. Even if seawater temperature increased only slightly from February (7 °C) to April (11 °C; Fig. 7), the stratification of the water column was clearly developed by the spreading of low salinity water across the surface (down to 33.8 in April), as a consequence of some intermittent pulses of the Isonzo River (up to 500 m3 s–1; Fig. 5). These pulses also delivered large quantities of nutrients, especially nitrate (6.2 µmol dm–3; Fig. 4), which further increased the DIN:PO4 ratios (136) towards values reflecting the nutrient composition of freshwater (195 ± 55; Fig. 6a). The role of the NO3 inputs to sustain PP was also evidenced by the increment of the f-ratio from 0.03 (January) to 0.23 (February). On the contrary Si:PO4 ratio was strongly reduced, owing to the removal of reactive silicon by diatom population (Fig. 6b). Total irradiance gradually changed during these months, but it reached rather high values only in April, at the end of the period (Fig. 7). In April 2000 diatom bloom ceased and cell abundance fell to 203,000 cell dm–3, as a consequence of strong grazing pressure and silicate shortage (Fonda Umani, 2001). In the deeper waters regeneration of NH4 occurred (1.5 µmol dm– 3), presumably after the sedimentation of phytoplanktonderived material. These new conditions determined the shift of the phytoplankton community composition towards cryptophyceae (Fig. 3), a class that can constitute a significant fraction of nanoplankton in brackish and coastal waters (Butcher, 1967; Harris, 1986). Cryptophytes can become competitive in such conditions because of their capability of vertical migrations that enables the optimal utilization of nutrient and light (Fogg and Thake, 1987). In 2001, dynamics of phytoplankton population did not show the same sharp change as in February 2000, because of the more favorable environmental conditions (i.e. higher seawater temperature, strong river inputs, higher NO3 availability) already found in January. This feature determined more homogeneous trends of carbon and nitrogen uptakes (Fig. 2) and of cell abundance (Fig. 3). On the whole, these observations indicate that riverine loads of nutrients are in late winter an important factor for the rapid trigger of early phytoplankton blooms in the Gulf of Trieste, even when other environmental conditions, such as seawater temperature and total irradiance, are still close to the winter values. 3.1.3. Late spring and summer (May–September 2000) A prolonged and intense PP event during the 2000 was observed in the Gulf of Trieste from June to August. It developed in concomitance to well established summer con-

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ditions, showing patterns of carbon, nitrate and ammonium uptakes that indicated the presence of a complex sequence of autotrophic and heterotrophic activities. Despite river loads were not extremely high (Fig. 5), the major physical process was the constantly increasing freshwater retention in the area, that reached the maximum level when salinity as low as 36.00 was found at 12 m of depth in July 2000 (Fig. 4). At the same time, the total irradiance (up to 23,190 kJ m–2 d– 1) and the thermal stratification of the water column (25 °C at the surface, 17 °C at the bottom of the station AA1) reached their annual maximum. Carbon uptake was high from May to August (4.6– 15.9 µmol C dm–3 d–1) and it caused the nutrient depletion in the upper low salinity waters (Fig. 4). From June to August, the maximal values of PP showed a progressive shift toward deeper waters, where regenerate nutrients were more abundant (NH4 up to 3.5 µmol N dm–3). Despite these high PP rates, phytoplankton abundance remained rather low during these months (189,000–650,000 cell dm–3) and characterized by the presence of small diatoms, probably controlled by an intense grazing pressure (Fonda Umani, 2001). Compared to the early spring period, DIN:PO4 and Si:PO4 ratios in seawater were strongly reduced from April to June 2000, until values of 21 and 25, respectively (Fig. 6). This indicated that the nutrient availability in the marine environment had changed from that of freshwater, because of the stronger net removals of DIN and reactive silicate compare to reactive phosphorus. On the contrary, their rise in the following months was due to the preponderance of NH4 and SiO2 regeneration in the deeper waters (Fig. 4). Nitrate and ammonium (Fig. 2) were alternatively used for production processes during these months. QNH4 was high in May (519 nmol N dm–3 d–1), during the early phase of the bloom and in concomitance of the increased abundance of chrysophytes (Fig. 3). On the contrary, it decreased in June and August, when QNO3 prevailed (442 nmol N dm–3 d–1, f-ratios = 0.5 in August) and diatoms became again the most important phytoplankton class. In September 2000 very high QNH4 rates were observed, particularly in the deeper waters (1308 nmol N dm–3 d–1), when both PP and QNO3 uptakes had already declined and the phytoplankton abundance was scarce (Fig. 3). These oscillations of PP and of inorganic nitrogen uptakes in summer 2000 were the result of phytoplankton and bacteria activities. From May to August, during the months characterized by high PP, variable carbon uptakes and alternate utilization of NO3 and NH4 seemed mainly driven by the requirements of the phytoplankton assemblage, which easily changes during the bloom evolution and when the community structure is modified. In September, the high QNH4 related to a low PP suggested a particularly important contribution of bacteria to nitrogen uptake during the declining phase of the autotrophic activity. In this hypothesis, the high f-ratio found at the beginning of August would be well representative of the peak of new PP, which was sustained by the riverine inputs of July (Fig. 5). On the contrary, the low

value of the f-ratio found in September (0.15) could not be an appropriate index to describe the phytoplankton activity (see also Section 3.2). 3.1.4. Late autumn (October–November 1999 and 2000) The autumn peak of freshwater discharge usually occurs in the Gulf of Trieste more regularly than the spring one (Mozeticˇ et al., 1998). Flow-rates of Isonzo and Timavo Rivers often reach their yearly maximum in October and November, as was the case of our study (583 m3 s–1 in 1999, 1780 m3 s–1 in 2000; Fig. 5). In these months, very variable production processes characterize this ecosystem, because autumn blooms strongly depend upon the concomitance among riverine nutrient discharges, dynamics of water bodies and favorable environmental conditions. This was the case of October 2000, when PP strongly increased almost in the entire water column (2650 mg C m–2 d–1), determining the development of a diatom-dominated bloom that produced the highest phytoplankton abundance of the whole investigate period (2,000,000 cell dm–3). This event was favored by two river pulses (Fig. 5) that occurred when seawater temperature (19 °C) and irradiance (7800 kJ m–2 d–1) were still rather high. PP was coupled to high QNH4 (up to 425 nmol N dm–3 d–1) in the whole water column and high QNO3 (up to 230 nmol N dm–3 d–1) in the upper layer, but the first prevailed (fratio = 0.16) because of the larger availability of the regenerated nitrogen (Fig. 4). This peak of PP also determined the reduction of DIN:PO4 and Si:PO4 ratios (down to 83 and to 53), as already observed during other strongest blooms. In November 2000, despite of the presence of strong river discharges (salinity down to 30.0, NO3 up to 11.2 µmol N dm–3 at the surface), there was the almost total removal of phytoplankton biomass (abundance down to 35,000 cell dm–3) and the consequent decrease of PP (470 mg C m–2 d–1). Since this reduction was not coupled to high grazing pressure or high sedimentation rates (Fonda Umani, 2001), most of the planktonic biomass could have been transported outside the gulf as a result of the stronger dynamics of water bodies, which took place in the area during this freshet (see also Section 3.3). Production processes in October and November 1999 showed different dynamics with respect to 2000, because of the more restricted river inputs observed during this autumn. Freshwater advection increased the vertical salinity gradient (23.1 at the surface, 37.6 at the bottom), determining the stratification of the water column even in conditions of seawater temperature almost constant from the surface to the bottom (17 °C). Moreover, the nutrient enriched upper waters (NO3 up to 38.3 µmol N dm–3 d–1; Fig. 4) sustained the nitrogen uptakes, determining a rather high phytoplankton abundance (480,000 cell dm–3) that lasted until the end of November 1999. 3.2. Carbon versus nitrogen uptakes Carbon to nitrogen uptake ratio at the station AA1 (C/Nup = PP/(QNO3 + QNH4); Fig. 3b) basically showed the

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overconsumption of carbon with respect to nitrogen (annual average of 16 ± 11), as carbon assimilation often exceeded the nitrogen one when compared to the phytoplankton composition of the Redfield model (C/N from 6.4 to 8.7; Takahashi et al., 1985). On the contrary, particularly low C/Nup values were found in October 1999 and September 2000 (down to 2). Despite unbalanced uptakes have already been observed in oceanic and coastal areas, the ultimate reason of their oscillation has not been still clearly identified among the several hypothesis concerning the interactions between plankton physiology and environmental conditions (Harris, 1986; Sambrotto et al., 1993; Tremblay et al., 2000; Bury et al., 2001; Diaz et al., 2000). Our data showed the repetitive occurrence of particularly high C/Nup values during the blooms of February (33), June (24), July (22) and October 2000 (23). During the two first cases production processes were characterized by higher f-ratios (0.23 and 0.40), indicating the increased role of new production to sustain the autotrophic activity in the early spring and summer. High peak of PP and relative high C/Nup ratio of October 2000 were mainly coupled to the regenerated production (f-ratio = 0.16). On the contrary, C/Nup ratio decreased during the late bloom phase in April–May (7–9) and September 2000 (2), as well as during the months characterized by lower productivity (2–13 in October–November 1999, 6 in January 2001). November 2000 was the main exception to this pattern: PP was low but still characterized by high carbon overconsumption (C/Nup = 37) and low f-ratio (0.05) as during the bloom of the previous month. However, the strong alteration of general conditions observed in this case in the area (see Section 3.1.4) could have probably affected the carbon and nitrogen requirements of the planktonic community. Several reasons can be invoked to explain this temporal pattern of C/Nup ratio. The shorter time of incubation of 14C PP (3 h) compared to nitrogen uptakes (24 h) makes PP an estimate of gross carbon production (i.e. without significant 14 C respiration and other losses; Harris, 1986) and QNO3 + QNH4 an estimate of net nitrogen uptake (i.e. not including the loss from PO15N to DO15N after uptake; Slawyk et al., 1998). Moreover, carbon and nitrogen demands by phytoplankton are often uncoupled on short temporal scale, because of the physiological adaptation of cells to the variable physical conditions and nutrient availability in the marine environment (Harris, 1986). High carbon to nitrogen uptakes by planktonic communities have been also inferred during spring blooms in coastal areas, on the basis of a general analysis of the available data of dissolved organic matter worldwide (Williams, 1995). This study indicates that PP accumulates on seasonal scale (i.e. in the mid- to late-summer) a post-bloom DOM richer in carbon than in nitrogen. This observation was also confirmed by DOM data collected in the Gulf of Trieste, although on a shorter than seasonal scale. The highest DOC/DON ratios were found during the months (April, August and November)

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that followed the strongest PP events of the 2000 (Fonda Umani, 2001). Other two aspects of the inorganic nitrogen uptake have also to be taken into consideration when the temporal trend of the C/Nup ratio is analyzed. On one side, uptakes of nitrite (Collos, 1998) and urea (Wafar et al., 1995), which are not usually measured, should be evaluated to obtain the total nitrogen demand of the planktonic community. On the other side, inorganic nitrogen uptakes by phytoplankton can also be overestimated because of the NH4 assimilation by bacteria (Hoch and Kirchman, 1995), when they are partially retained in the particulate matter during sample filtration on the Whatman GF/F filters (Lee et al., 1995). In this case, even higher C/Nup ratios should be attributed to phytoplankton production if ammonium uptake is not entirely ascribable to the autotrophic activity. On the whole, our data suggests that carbon overconsumption by phytoplankton could be the most important reason that increases C/Nup ratios during the events of high PP, whereas they do not exclude that NH4 uptake by bacteria can decrease the C/Nup ratios during the phases of scarcer autotrophic activity. 3.3. Temporal scales of production processes and physical transport in the Gulf of Trieste In order to evaluate the effect of the timing of riverine inputs, water circulation and biological uptakes on the nutrient balance in the Gulf of Trieste, we also estimated the temporal scales with which these processes act in the ROI (Rodhe, 1992). On the contrary to the previous temporal description, this analysis was performed using the whole dataset. Residence time of freshwater in the ROI (sFW) was calculated as ratio between the total freshwater content in this seawater volume and the sum of freshwater loads of Isonzo and Timavo Rivers. Total freshwater content was firstly calculated in each sample of the seven sampling stations, on the basis of a linear dilution between “pure” freshwater (salinity equal to 0.0) and “pure” seawater (average of the deeper/offshore waters: 37.3 in summer to 38.3 in winter) and it was successively 3D-integrated in the entire volume of the ROI. This integration was performed as 2-D interpolation (using a standard Kriging method; Cressie, 1990) along the transect from the Isonzo River mouth to the middle of the gulf (Fig. 1), which accounts most of the variability of parameters in the area. The result was successively 3-D linearly extended in the SW–NE direction using the other sampling station data. We obtained values of sFW ranging from 1 d, in November and January, to 23 d in July 2000 (annual average of 6 ± 5 d), which indicate the fast physical transport of the upper low salinity waters in winter and the slow transport in summer. Since the Isonzo plume substantially influence this area, sFW is basically a parameter indicative of the strong or weak dynamics of water bodies in the ROI.

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Table 1 Estimate in the ROI of nitrate and ammonium standing stocks (t N), nitrate and ammonium uptakes (t N d–1), primary production (t C d–1), Isonzo and Timavo rivers load of nitrate and ammonium (t N d–1), residence time of freshwater (d) and turnover times of nitrate and ammonium (d) Cruise

ROI

Rivers

October 1999 November 1999 January 2000 Feburary 2000 March 2000 April 2000 May 2000 June 2000 July 2000 August 2000 September 2000 October 2000 November 2000 January 2001 February 2001

NO3 (t N) 129 31 38 97 24 126 57 23 17 22 35 26 131 104 47

NH4 (t N) 30 21 15 12 12 26 43 25 31 50 81 41 76 13 16

QNO3 (t N d–1) 0.3 0.3 0.7 2.0 1.2 0.8 1.3 4.4 7.1 8.0 4.0 3.8 0.2 1.0 1.2

QNH4 (t N d–1) 5.6 3.3 4.0 2.6 6.2 4.4 13.5 17.8 15.6 20.2 32.9 30.5 2.2 4.2 6.6

PP (t C d–1) 43 88 153 143 177 89 368 216 309 322 173 417 65 28 84

NO3 (t N d–1) 47 13 4 3 11 18 12 10 6 13 6 15 67

Average (SD)

61 (44)

33 (22)

2.4 (2.5)

11 (10)

178 (123)

17 (18)

Despite of the scarcity of data available in literature, these results can be compared with the measurements of current velocity in the Gulf of Trieste. The physical transport of water bodies on daily scale is mainly affected by the total (tidal + residual) current and/or by strong currents due to particular meteorological events (as strong as 30 cm s–1; ˇ etina, 1991). On the Mosetti and Purga, 1990; Rajar and C contrary, only the residual current (1–3 cm s–1) determines the water transport on weekly scale. Considering these values and the size of the ROI, sFW from 1 to 21 d have to be supposed. Turnover times of NO3 (sNO3) and NH4 (sNH4) were calculated as ratio between the standing stocks of nitrate and ammonium (expressed in tons) and the biological sinks of these nutrients (QNO3 and QNH4; expressed in tons per day): both these quantities were estimated by 3D-interpolation in the volume of the ROI of all available data (seven sampling stations for nutrients and three stations for nitrogen uptakes). Integrated PP in the area (tons per day) was calculated as the integrated nitrogen uptakes. Finally, total nitrate and ammonium loads of the Isonzo and Timavo Rivers were also estimated using flow rates and concentrations of nutrients in freshwater. Table 1 and Figs. 8 and 9 summarize the results of this calculation. PP values in Table 1 (from 28 to 417 t C d–1) correspond to an average productivity in the area of 2.7 ± 1.8 mg C m–3 h–1. This value is higher of the previous estimates reported by Gilmartin and Revelante (1983) (1.7 ± 1.2 mg C m–3 h–1) and Malej et al. (1995) (1.8 ± 1.7 mg C m–3 h–1), both referring to sampling stations in the Gulf of Trieste less influenced by river discharges as compared to our area of study. However, the western coastal waters of the northern Adriatic Sea (up to 68 ± 49 mg C m–3 h–1 at 1.5 NM off the coast; Zoppini et al.,

NH4 (t N d–1) 3.3 0.7 0.2 0.1 0.6 0.7 0.5 0.3 0.3 0.8 0.2 0.7 2.2

Residence time sFW (d) 2 1 4 13 3 7 8 10 23 4 9 3 1 1 6

Turnover times sNO3 (d) 370 99 54 49 21 152 43 5 2 3 9 7 831 100 40

sNH4 (d) 5 6 4 4 2 6 3 1 2 2 2 1 34 3 2

0.8 (0.9)

6.3 (5.8)

119 (218)

5.4 (8.1)

1995) and the Po River plume region (14 ± 18 mg C m–3 h–1; Gilmartin and Revelante, 1983) are on the contrary more productive than the entire Gulf of Trieste. Fig. 8 shows that sNH4 (1–34 d) is often shorter than sFW (1–23 d). This means that the biological uptake can potentially remove the almost whole standing stock of NH4 before this nutrient is exported outside the gulf. sNH4 exceeds sFW only in few cases (October–November 1999, November 2000, January 2001), indicating that the ecosystem does not efficiently utilize this inorganic nitrogen source only in winter, when QNH4 is scarce and the physical transport is fast. Ammonium behavior will be therefore strongly affected by production processes and its availability in the marine environments will mainly depend on nitrogen recycling rather than on circulation. NO3 behavior is markedly different from that of NH4. sNO3 is greater than sFW up to two orders of magnitude during most of the time (from 21 to 831 d in winter, spring and autumn), with the only exception of June–October 2000

Fig. 8. Comparison between the residence time of freshwater (sFW, d) and the turnover times of nitrate (sNO3, d) and ammonium (sNH4, d) in the ROI.

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NH4 load (from 0.1 to 3.3 t N d–1) almost always does not equilibrate the biological uptake (from 2.6 to 33 t N d–1). This indicates that regeneration is the most important processes to regulate NH4 availability and that other nitrogen reservoirs (i.e. particulate and dissolved organic matter) have to act in the marine environment as sources of nitrogen to equilibrate ammonium uptake. 4. Conclusions

Fig. 9. (a) Nitrate and (b) ammonium balances in the ROI: comparison among standing stocks (t N), inorganic nitrogen uptakes (t N d–1) and total river loads (t N d–1).

(2–9 d). This indicates that, although NO3 sustains the early phytoplankton bloom in late winter (see the decrement of sNO3 in March 2000), its standing stock is almost always largely exceeding the NO3 demand of production processes. In such conditions, the pattern of NO3 in the Gulf of Trieste will depend mainly on the spreading of the Isonzo River plume. Large fractions of nitrate will be exported outside of the ROI, because of the circulation of water bodies in the area and the shortage of NO3 in this ecosystem will be improbable. Only in summer 2000, the particularly long permanence in the area of low salinity waters (sFW = 23 d in July) and the high nitrate uptake (7.1 t N d–1) almost induced the depletion of the NO3 standing stock. The balance of inorganic nitrogen forms (Fig. 9a,b) shows the reciprocal importance of riverine loads and biological uptakes to regulate the availability of NO3 and NH4 in the Gulf of Trieste. Isonzo and Timavo rivers discharged from 3 to 67 t of nitrate and from 0.1 to 3.3 t of ammonium per day. Daily river input of NH4 represents up to 10% of the whole standing stock of this nutrient in the sea: this supply is not always negligible and NH4 should not simply be considered only as nitrogen “regenerated” in the marine environment. On the contrary, even if NO3 river load is abundant (up to 61% per day), nitrate regeneration in the marine environment is a flux still not quantified. This makes uncertain to consider NO3 only as a land-born nutrient. Production processes remove on the average 4% of the NO3 standing stock (Fig. 9a) and 34% of the NH4 standing stock (Fig. 9b) per day. Riverine load of nitrate (from 3 to 67 t N d–1) generally exceed the biological demand (uptake from 0.2 to 8 t N d–1) and thus a large fraction of this nutrient does not enter in the food web of Gulf of Trieste. Only in the presence of anomalous conditions, as previously underlined for July–September 2000, the NO3 uptake approximates its external input and standing stock, causing the ecosystem almost to reach nitrate deficiency. On the contrary, riverine

Production processes in the Gulf of Trieste are strongly variable, because of the effect of river inputs, local meteorological conditions and circulation. The rise of total irradiance and seawater temperature determines favorable environmental conditions for autotrophic communities on seasonal scale, but their persistency also depends upon the aperiodic riverine-nutrient and freshwater discharges. On the contrary, strong freshets in autumn and early winter do not always increase PP, because of the rapid transport of the nutrient-rich low salinity waters outside the gulf. After river inputs, nutrient recycling becomes the most important process to sustain the productivity of this ecosystem, as confirmed by the prevalence of ammonium uptake. Its particularly high values observed during the post-bloom phases could be partially attributed to bacteria uptake. This observation suggests that f-ratio is not always an appropriate index to distinguish the importance of “new” versus “regenerated” PP. Even if diatoms largely dominate planktonic community, the combined effect of grazing pressure and silicate shortage temporary determines the prevalence of other classes, such as cryptophytes. There is a growing evidence of the variability of carbon to nitrogen consumption by planktonic communities and of its departure from the Redfield value. Our data basically show higher carbon overconsumption during the high PP events and more balanced ratios during the periods of scarce autotrophic activity. The timing of river loads and circulation also affect production processes in Gulf of Trieste. Our analysis indicates that nitrate demand for PP is scarce compare to NO3 standing stock and to the river load, so that the deficiency of this nutrient is expected only in conditions of really scarce circulation. In the other cases, nitrate is mostly exported outside the gulf, before to be efficiently introduced in the food web. On the contrary, riverine load does not balance the high NH4 uptake. This means that it has to be balanced in this shallow ecosystem by nitrogen recycling, making the behavior of ammonium mostly determined by biological processes rather than by the physical transport. Acknowledgements The study was funded by the European Community and the Friuli Venezia Region Interreg II Project. We are grateful to Dr. Massimo Celio and Dr. Cinzia Comici for the CTD

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data and for the activity on the field, to Dr. Claus Falconi and Dr. Sergio Predonzani for the nutrient analyses. We also thank Direzione Regionale dell’Ambiente (Friuli Venezia Giulia Region), ARPA (Agenzia Regionale per la Protezione dell’Ambiente) and ACEGAS (Acqua Elettricità Gas e Servizi) for the data of total irradiance, flow rates and nutrient concentrations of the Isonzo and Timavo Rivers.

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