Artículos

 

Nutrient dynamics in a coastal lagoon (Ria Formosa, Portugal): The importance of lagoon-sea water exchanges on the biological productivity

 

Dinámica de nutrientes en una laguna costera (Ría Formosa, Portugal): La importancia del intercambio de agua laguna-mar en la productividad biológica

 

Manuela Falcão¹ and Carlos Vale^1*

 

¹ IPIMAR - Instituto de Investigação das Pescas e do Mar, Ave. Brasilia 1400, Lisboa, Portugal. *E-mail: cvale@ipimar.pt

 

Recibido en octubre de 2000;
aceptado en septiembre de 2002.

 

Abstract

Silicates, nitrates, phosphates, chlorophyll α and primary productivity were monitored at low and high tide between September 1985 and September 1986, at four stations in Ria Formosa, a meso-tidal coastal lagoon located in the south of Portugal. The water sampling and the in situ observations were done alternatively in neap and spring tide. While silicates at low tide exceeded values at high tide thorughout the year and a weak seasonal trend was discerned, nitrates and phosphates exhibited a clear-cut seasonal variation at high spring tide. Pronounced maxima in the period of low temperatures (early spring), 7 µM of nitrates and 3 µM of phosphates, indicate their import from the adjacent coastal zone. Lower values at low tide and chlorophyll α increases (up to 2 µg g^-1) point to a rapid biological consumption of the imported nutrients. Differences of temperature between coastal waters and those of the lagoon in early spring account for the more efficient consumption by the primary producers of the lagoon. The primary productivity varied from 2 mg C m^-3 h^-1 (winter) to 30 mg C m^-3 h^-1 (summer), reflecting the intensive ¹⁴C incorporation during the warmer period. High rates of nitrates and phosphates consumption could be observed during spring, when their concentrations decreased 50% within a narrow period of 6 hours from high to low tide.

Key words: Coastal lagoon, nutrients, chlorophyll, primary productivity, lagoon-sea exchanges.

 

Resumen

Se monitorearon silicatos, nitratos, fosfatos, clorofila a y productividad primaria en mareas altas y bajas entre septiembre de 1985 y septiembre de 1986, en cuatro estaciones en la Ría Formosa, una laguna costera meso-mareal localizada en el sur de Portugal. Las muestras de agua y las observaciones in situ se realizaron en mareas muertas y vivas, de forma alternada. Mientras que durante la marea baja los silicatos excedieron los valores obtenidos en marea alta durante todo el año, estableciéndose una débil tendencia estacional, los nitratos y fosfatos mostraron una notoria variación estacional durante la pleamar de las mareas vivas. Los máximos pronunciados en el periodo de bajas temperaturas (inicios de primavera), de 7 µM para nitratos y 3 µM para fosfatos, indican su advección desde la zona costera contigua. Los valores menores durante la marea baja y el incremento en la clorofila α (hasta 2 µg g^-1), señalan un rápido consumo biológico de los nutrientes importados. Las diferencias de temperatura entre las aguas costeras, y las de la laguna al inicio de la primavera, promueven un consumo más eficiente entre los productores primarios de la laguna. La productividad primaria varió de 2 mg C m^-3 h^-1 (invierno) a 30 mg C m^-3 h^-1 (verano), reflejando una intensa incorporación de ¹⁴C durante los periodos cálidos. Se pudo observar una elevada tasa de consumo de nitratos y fosfatos durante la primavera, cuando las concentraciones disminuyeron en un 50% dentro de un corto período de 6 horas entre pleamar y bajamar.

Palabras clave: Laguna costera, nutrientes, clorofila, productividad primaria, intercambios laguna-mar.

 

Introduction

Tidally dominated coastal lagoons are complex and dynamic ecosystems whose physical, chemical and biological properties show a sharp distributional gradient and short-time to seasonal variability (Nogueira et al., 1997). The nutrient dynamics are driven by the feedback mechanisms between these ecosystems and the coastal waters (Nixon, 1980; Dame et al., 1986; Nixon et al., 1994). Most authors agree that part of the lagoon biomass is exported offshore, the organic matter remineralized in the water column or in the sediments, and inorganic forms of nutrients are imported. Inside the lagoon the biogeochemical processes are extremely complex due to the interactions with the sediments and the benthic-pelagic competition of primary producers (Keizer et al., 1989; Fourqurean et al., 1993). In the case of nitrogen, sediments are a source as well as a major sink in the cycling of this element, regulating its concentration and, thus, the productivity of coastal marine systems (Lohse et al., 1993). In the case of phosphate, the great capacity of sediment and suspended sediments to release and/ or sequester phosphate, maintaining concentrations within a narrow range (Froelich, 1988; Vidal, 1994), may limit the availability of this nutrient for the phytoplankton. In fact, the short-term effects of suspended sediments lead to an effective competition between phytoplankton species and sediment particles for dissolved phosphate (Fourqurean et al., 1993; Vidal, 1994). In the open ocean, the processes involving the biogeochemistry of nitrogen and phosphorus are not so sharp as those occuring in shallow ecosystems (Fourqurean et al., 1993; Nixon et al., 1994). Some estuarine ecologists object to treating the coastal ocean as a source of nutrients for a lagoon or bay because the net long-term flux of nitrogen and phosphorus is virtually always outwards the estuary (Nixon et al., 1994). Thus, for coastal systems with permanent connection to the sea, ocean water may be the major source of inorganic nutrients required to support the productivity of an ecosystem. In this study the spatial, seasonal and tidal variability of nutrients, and the chlorophyll and primary productivity were assesed in a coastal lagoon connected to the sea. Our main concern was to understand the nutrient dynamics including the importance of water exchanges between the lagoon and the adjoining area, and the relationship of nutrient dynamics with the primary biological activity of the ecosystem.

 

Sampling and methods

Surface water was sampled twice a month at low and high tides, from September 1985 to September 1986 at four stations located in the main channels of Ria Formosa (fig. 1). Monthly samples were taken alternatively in neap tide (tidal amplitude ~1 m) and in spring tide (tidal amplitude ~3 m). Under this schedule water was collected throughout the year in four different situations: in neap tide periods (high tide and low tide), when the exchanges between the lagoon and the sea were minimal and, in spring tides (high tide and low tide) when they were maximal. Temperature was measured in situ with a probe. Other physical parameters were measured in the laboratory: salinity with a salinometer Beckman-RS7-C; pH with a Anna Instrument Cole-Parmer Inst. (combined electrode with silver/ silver chloride reference) within 2 hours after sampling; dissolved oxygen by the Winkler method (Grasshoff, 1976). Silicates, nitrates and phosphates were analysed with a Chemlab autoanalyser using the Technicon methodology. For the estimation of the primary productivity, vials were filled up with lagoon water, injected with ¹⁴C and incubated in situ for 4 hours between 10:00 h and 14:00 h, and the carbon assimilation was determined by a scintillation counter LSC NE 6500 (FAO, 1975). Pigments and phaeopigments were determined with a Perkin-Elmer fluorometer according to the methodology described by Strickland and Parsons (1968). The detection limits of the determinations were: 0.1 µM for silicate, 0.05 µM for nitrate and nitrite, 0.1 µM for phosphate, and 0.01 µg L^-1 for pigments and phaeopigments.

 

Results and discussion

Observations of the water quality at low- and high-tide during tidal periods of contrasting amplitudes allow to assess the importance of exchanges between the lagoon and the adjoining area. The conditions at those periods may be particularly different in Ria Formosa, since the water volume exchanged in spring tides may be as much as 70% of the lagoon's total volume (Sprung, 1994). In order to discern better the seasonal variations of the exchanges, the results in neap and spring tides are presented in different plots (figs. 2, 3, 4, 5).

Temperature, dissolved oxygen, pH and salinity

Water temperature in the four stations exhibited a seasonal fluctuation with a minimum in winter and a maximum in summer, and differences between low and high tide were minor (fig. 2). However, at spring tides the temperature remained low from February until April, while at neap tides an increase was observed in March. These differences indicate that warming up of coastal waters was delayed with respect to the lagoon water. Concentrations of dissolved oxygen were close to the saturation values and, at neap tides, the seasonal variation was almost reciprocal to that of the mean temperature. The maximum of O₂ was found approximately a month after the minimum mean temperature (fig. 2), which indicates that O₂ concentration in early spring is substantially influenced by photosynthesis. This effect was not observed at spring tides presumably due to the large water volume exchanged with the sea. Differences among the stations were higher at low neap tide reflecting local processes. Values of NBS pH varied from 8.0 to 8.6 at neap tides, and fluctuated around 8.2 (s.d. = 0.13) at spring tides due to mixing with incoming seawater. The higher values obtained at neap tide are probably influenced by photosynthesis. Because freshwater inputs are negligible and runoff episodes were absent during the annual study period (Falcão, 1997), the salinity was relatively constant (36.5) at the four stations during the annual survey. Differences in salinity between low and high tides were minor.

Silicate

Mean concentrations of silicates varied between 0.5 and 7 µM. Although higher values can be discerned at winter neap tides, their main characteristic relies in the fact that concentrations at low tide exceeded those recorded at high tide (fig. 3). The differences were found both at neap and spring tides. Moreover, values measured at high tide were relatively uniform, while differences among stations were found at spring tides. These results indicate that silicates are regenerated in the sediments and diffused out to the water column. With the flood there is a dilution effect and a silicate export to the coastal zone at the tidal rhythm. The importance of the bottom on the distribution of silicate has been observed in previous studies, particularly due to the clam cultures carried out in the extensive inter-tidal flats of the lagoon (Falcão and Vale, 1990, 1998, 2000) and due to molecular diffusion (Ullman and Aller, 1989; Forja et al., 1994).

Nitrate and phosphate

An opposite pattern was found for nitrate and phosphate (fig. 3): both nutrients increased pronouncedly at spring tides with seawater incoming between February and April/May, when the water temperature was lower. At neap tide, values remained low and relatively constant along the annual period. Moreover, in the spring tides of that period, the standard deviation of the mean concentrations was considerably higher than in the rest of the year. This means that nitrate and phosphate concentrations were not uniformly distributed in the lagoon. The parallelism of the two distribution patterns, in addition to the fact that high concentrations were found at stations closer to the lagoon inlet, suggests that nitrates and phosphates are imported from the coastal zone in the period of low water temperature. This import is particularly important in spring tides, but the same trend tenuously observed at neap tides for phosphates indicates that, between February and April/May, consumption by the lagoon's primary producers does not balance the incoming seawater. Elevated concentrations at high tide indicate that nutrients in the coastal zone during winter-spring are higher than those inside the lagoon, probably because the consumption by phytoplankton is more intense inside the lagoon. If we compare the low tide nutrient concentrations obtained at spring and at neap tide, one may infer that the higher values obtained at low spring tide are the remnant from those imported from the sea. This means that nutrients had no time to be completely consumed within the short period of 6 hours. These observations are in accordance with studies developed in other coastal systems that emphasize the importance of the import/export of nutrients for the ecology of the lagoon ecosystems (Nixon et al., 1994). The explanations invoked for the individual increase of nitrate and phosphate in water, such as rapid nitrification (Harrison et al., 1997) and release of phosphate from the sediment when dissolved oxygen decreases (Sundby et al., 1992), can not explain the distribution patterns observed in Ria Formosa. Besides the dilution effect, the decrease of nitrate and phosphate concentrations between high and low tides may also indicate a rapid consumption of the imported nutrients by the lagoon's primary producers.

Chlorophyll α

The time-course evolution of chlorophyll α was in line with the nitrate, phosphate and O₂ variations. Chlorophyll α was low in winter and increased in early spring, defining a maximum from February to April (fig. 4). In this period the variability among stations was higher indicating a less uniform pigment distribution inside the lagoon. Many authors refer that the increase of pigments confirms the rapid biological assimilation of nitrates and phosphates by phytoplankton (Jordan et al., 1991). In fact, during early spring, the consumption of nitrates and phosphates observed from high tide to low tide correspond to the higher increase of chlorophyll a. This shows the importance of the nutrients imported from the coastal zone in this period for the production of phytoplankton inside the lagoon. The higher values of chlorophyll obtained at high tide in February and March, evidence an import of phytoplakton in this period while, after March, values at low tide surpass them. This means that the production of phytoplankton starts earlier in oceanic water than in the lagoon water but, after March, the lagoon exports phytoplankton.

Primary productivity

The seasonal variation of primary productivity measured during neap and spring tides is characterised by lower values in winter, a gradual increase in early spring, and high values in spring/summer (fig. 5). The period of higher primary production does not coincide with that of chlorophyll a, the higher carbon fixation occurring later. The carbon fixation rate was highest during summer, when nitrogen compounds were less abundant in the water (Falcão and Vale, 1998). This suggests that any nitrogen entering the system is being rapidly removed and/or that most of the carbon fixation is being supported by nitrogen that has been somehow rapidly remineralized within the system (Nixon, 1980). A significant contribution of ammonium may come from the intertidal sediments when they are flooded by the tide (Falcão and Vale, 1995). The lower values of primary productivity in this lagoon (2-9 mg C m^-3 h^-1 in winter/autumn) are similar to those obtained in coastal waters, while higher values (20-30 mg C m^-3 h^-1 in spring/summer) are comparable to those of the most productive estuarine flats (Falcão, 1997). The photosynthetic efficiency, defined as the ratio between primary productivity and chlorophyll a, reaches the minimum during the winter period and follows a progressive increase from spring to summer (fig. 5) meaning that the maximum yield for the carbon fixation rate occurs during the summer.

 

Conclusions

This study reports nitrate and phosphate imports from the adjoining coastal area to the lagoon during the spring, and a permanent export of silicates out of it. These findings agree with others on the base of the nutrient concentrations obtained inside the lagoon and in the adjoining coastal area (Falcão, 1997). The nutrient exchanges calculated revealed an import of nitrates and phosphates during spring (~60%) and an export of silicates over the year. At spring tide, the fast consumption (from high tide to low tide) of the imported nitrates and phosphates may correspond to 50% of their total amount. Over there, the lowest levels of nitrates and phosphates observed when seawater incoming is negligible (neap tide) reinforce that the lagoon water is poor in nutrients because these are rapidly consumed. Part of the nutrients are consumed by the phytoplankton whose concentration increases during spring and, another part of them is presumably consumed by the micro-phytobenthos in the top-layer sediment as demonstrated by Sundbãck and Granéli (1988). Nutrients available for phy-toplankton and phytobenthos consumption are not only those imported from coastal waters but also those released from the bottom. The influence of the bottom in the regeneration of nutrients that enrich the water column should not be negligible mainly concerning ammonium, phosphate and silicate (Lerat et al., 1990; Kristensen, 1993; Hopkinson, 1987; Forja et al., 1994). Studies developed in this lagoon demonstrated that inter-tidal areas are apparently capable of supplying most of the daily N and P requirements of phytoplankton in the overlying water (Falcão and Vale, 1998). Other authors demonstrate that rates of net nitrogen mineralization were relatively low during most of the year with a particularly active period from June to August, possibly due to an effect of the temperature on soil microbial activity (Cartaxana et al., 1999). However, the enrichment of the water column in nitrogen and phosphorus during summer was not observed in this work suggesting its immediate consumption. The sharp increase of primary productivity obtained during the summer might be translated into high rates of nutrient production and consumption. On the base of these findings and according to the classification of trophic degrees in marine systems (Wetzel, 1983), Ria Formosa may be considered oligomesotrophic in winter/autumn and hipertrophic in spring/summer. Our results confirm that nutrients imported from the coastal waters as well as those produced inside the lagoon, are enough to maintain an autotrophically dominated system in spite of inexpressive fresh water inputs.

 

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