Artículos

 

Net autotrophy and heterotrophy in the Pontevedra Ria upwelling system (NW Iberian margin)

 

Autotrofia y heterotrofia neta en un sistema costero de afloramiento, la Ría de Pontevedra (noroeste de la plataforma ibérica)

 

Andrew W. Dale and Ricardo Prego*

 

^* Marine Biogeochemistry Research Group Institute of Marine Research (CSIC) 6 Eduardo Cabello, 36208 Vigo, Spain. * E-mail: prego@iim.csic.es

 

Recibido en junio de 2003;
aceptado en abril de 2004.

 

Abstract

A non-stationary state mass balance of the type advocated by the International Geosphere-Biosphere Programme/Land-Ocean Interactions in the Coastal Zone (IGBP/LOICZ) has been used to assess net ecosystem metabolism in the Pontevedra Ria (NW Spain), a large embayment subject to transient upwelling of Eastern North Atlantic Central Water (ENACW) under favourable meteorological conditions. Nitrate (NO₃^-) and phosphate (PO₄^3-) data spanning 12 months were resolved at the oceanic boundary by treating the ria as a single box of constant volume. The nutrient budget was scaled up to an estimate of net community production (NCP) using the compositional relationship of local phytoplankton. The mean annual NCP predicted by the NO₃^-balance was 24.0 mgC m^-2 h^-1, and 35.8 mgC m^-2 h^-1 by the PO₄^3- budget. Nutrient fluxes into the reservoir were strongly driven by the incoming oceanic flow throughout the year, which supplied 88% and 98% of the total NO₃^- and PO₄^3- load, respectively. A high NCP (NO₃^-) of 57.2 mgC m^-2 h^-1 was calculated for the height of the growth season contemporaneous with ENACW intrusion, whereas a slightly higher value of 61.4 mgC m^-2 h^-1 corresponded to PO₄^3-. Nutrient limitation was variable throughout the sampling, switching from PO₄^3- to NO₃^- from winter to spring concurrent with a drop in riverine PO₄^3- input. Scaling the inorganic nutrients to carbon units, the Pontevedra Ria may be considered as net autotrophic, although the NO₃^- budget suggests alternation between autotrophy and heterotrophy over an annual cycle.

Key words: upwelling, nutrient budget, Pontevedra Ria, NW Spain.

 

Resumen

Se aplicó un balance no estacionario, siguiendo el modelo aconsejado por el programa IGBP-LOICZ, para calcular el metabolismo neto del ecosistema en la Ría de Pontevedra, un sistema costero sujeto a eventos de afloramiento de ENACW (Agua Central del Noreste Atlántico) bajo condiciones meteorológicas favorables. Para realizar dicho balance se utilizaron los datos de nitrato y fosfato obtenidos durante un lapso de doce meses en la frontera oceánica de la ría, considerada ésta como un único compartimento de volumen constante. Se estimó la producción neta (NCP, net community production) en base al balance de nutrientes y la composición elemental del fitoplancton local, obteniéndose un valor medio anual de 24.0 mgC m^-2 h^-1 en base al nitrato y de 35.8 mgC m^-2 h^-1 a partir del fosfato. El aporte de nutrientes hacia el compartimento fue muy dependiente del flujo entrante desde el océano a lo largo del año ya que éste contribuye con 88% y 98% del nitrato y fosfato total recibido, respectivamente. El máximo de NCP, 57.2 mgC m^-2 h^-1 en base al nitrato y 61.4 mgC m^-2 h^-1 partiendo del fosfato, se obtuvo durante la época de floraciones coetáneas a la intrusion de ENACW en la ría. La limitación de nutrientes fue variable durante todo el periodo de muestreo, cambiando del fosfato al nitrato desde el invierno hasta la primavera de acuerdo con la baja entrada de fosfato fluvial. Al convertir los nutrientes inorgánicos en unidades de carbono, la ría de Pontevedra puede ser considerada por su balance neto anual como autótrofa, aunque el balance de nitrato sugiere una alternancia entre autotrofía y heterotrofía durante el ciclo anual.

Palabras clave: nutriente, balance, afloramiento, ría, Pontevedra, NO de España.

 

Introduction

Under normal estuarine spatial and temporal constraints, reactive materials such as nutrients behave non-conservatively owing to modifications by biological recycling and chemical transformations acting independently over simple physical advection and mixing. Nutrient mass balances, or box models (Nixon et al., 1995; Kemp et al., 1997), constitute a useful tool to assess the degree of non-conservatism within spatially and temporally defined boundaries. The nutrient budget can give valuable information as to whether the system is a net exporter or importer of nutrients. Smith and Hollibaugh (1997) used the term "trophic status" to describe the balance (net respiration or net synthesis) of organic carbon in an ecosystem, where heterotrophic refers to net organic carbon respiration and autotrophic refers to net organic carbon synthesis. The trophic status can be broadly inferred from inorganic nutrient budgets after the net nutrient flux has been scaled to net organic carbon flux stoichiometric linking according to the chemical composition of photosynthezised organic matter. Clearly, differences may arise depending on which nutrient (either N or P) is taken as the baseline for stoichiometric linking.

Recent projects in the Galician Rias, NW Spain, have focused on the development of nutrient budgets (Prego, 1993a, 1994; Álvarez-Salgado et al., 1996; Rosón et al., 1999). This work focuses on the Pontevedra Ria, one of four large embayments on the western Galician coast known collectively as the Rias Bajas. The Rias Bajas are host to one of the world's largest fisheries of the edible mussel Mytilus edulis, whose production may reach 100,000 t yr^-1 in the Arosa Ria (Tenore et al. , 1982). The most pronounced hydrographical feature of these rias is upwelling (Fraga, 1981) of East North Atlantic Central Water (ENACW, S = 35.67-35.83, θ = 11.8-13.5°C; Fiuza et al., 1998). Upwelling normally occurs from April to October engendered by spatial shifts of the North Atlantic Azores anticyclone and offshore Ekman transport (Wooster et al., 1976; McClain et al., 1986), although under suitable conditions, offshore water masses may intrude into the Pontevedra Ria outside of the upwelling season (Prego et al., 2001). ENACW is rich in remineralized inorganic nutrients and supports the extensive raft-culture of mussels and high primary productivity (Álvarez-Salgado et al., 1996). At other times of the year terrestrial runoff is the dominant nutrient supply. Thus, the rias and adjacent shelf waters can be envisaged as a collage of intricate hydrographic regimes acting to enhance remineralization and primary production both inside the rias and on the continental shelf (Prego, 1993a).

The objective of this paper is to explore the annual net ecosystem metabolism in the Pontevedra Ria by means of a non-stationary state time-series mass balance. Inorganic nutrient fluxes are resolved across the budget front where oceanic- and fluvial-dominated hydrographic regimes meet.

 

Materials and methods

The field campaign took place between October 1997 and October 1998, over 23 transects on board the R/V Mytilus. Water samples for chemical analysis were collected from six stations along the ria axis (fig. 1) using General Oceanic Niskin bottles at standard depths and separated into 50-mL HDPE bottles. CTD data were collected from eleven stations in the ria with a Sea-bird SBE 19. Water samples were generally analyzed for phosphate (PO4^3-) and nitrate (NO3^-) within 24 h, following established autoanalytical colorimetric techniques (Hansen and Grasshoff, 1983). Ten replicate analyses of different aliquots of equal concentrations yielded the following standard deviations: NO₃ ± 0.01 (within the 0-10 µM range) and PO₄^3- 0.03 (0-2 µM).

Frontal budget development

The budget framework closely follows the Land Ocean Interactions in the Coastal Zone (LOICZ) protocol for budget modelling developed by Gordon et al. (1996). The ria is treated as a single partially mixed box (volume 1.47 km³, area 68.6 km²), with boundaries at the limit of tidal influence at the ria head, and at the cross section between Udra Cape and Cabicastro Point at the seaward end (fig. 1).

The Lérez River provides the main freshwater input to the ria (mean annual discharge 25.9 m³ s^-1; Ibarra and Prego, 1997), and there is a small discharge from the sewage works, with a mean daily rate of 0.41 m³ s^-1. River flow was recorded daily at a gauging station at the limit of tidal influence. Season-ality in the region can be defined by the river flow, comprising the wet season (November-February), spring (March-May) and the dry season (June-September), with October being a transitional month.

The water balance of the ria of constant volume, V, comprises the river runoff, Qr, sewage inputs, Q_s, and direct precipitation, Q_p, and water losses via evaporation, Q_e (fig. 2). If the sum of these parts (expressed in m³ s^-1) is the net residual flow, Qz, then (assuming negligible groundwater inputs):

If Q_z < 0 then net residual flow out of the ria is implied. Assuming zero salinity for Q_r, Q_p, Q_sand Q_e, the horizontal exchange fluxes for each cruise can be evaluated individually with the following equations (Gordon et al., 1996):

where Q_i and Q_o are the water exchanges (by advection and mixing) in and out of the system, respectively, with average salinities of S_i and S_o (measured at station S on the seaward boundary). In this work, S_o is defined as the average salinity of the ria, dS_o/dT is the change in outgoing salinity between each cruise, and Si on the budget front was calculated using the water density to derive the level of zero velocity (v = 0, fig. 2) separating the two layers.

Inorganic budget and stoichiometric linkage

The net flux, ∑F, of non-conservative material across the budget boundary is quantified as the sum of the products of the individual water fluxes (fig. 2) and the concentration, c, of dissolved material therein:

where the subscripts correspond to those in eq. (1). Similarly, the sum of the net non-conservative biogeochemical processes, which cause deviations in simple constituent mixing, can be represented by B_p and a non-steady state term dN_u/dT:

If no biogeochemical removal or addition of nutrient salts takes place, SF will be purely dependent on physical mixing and transport processes, and therefore be zero. The seasonal and annual results for Bp are shown in table 1.

Net community production (NCP) refers to organic nutrient production and is the difference between gross primary production and respiration. NCP (in mgC_org m^-2 h^-1) can be estimated as B_p, using the C:N:P ratio of 129:17:1 for local phytoplankton (Ríos and Fraga, 1987), assuming that loss of inorganic material is equal to the gain in organic material via photosynthesis. The time-series NCP for the Pontevedra Ria is shown in figure 3.

 

Results and discussion

Seasonal nutrient dynamics and NCP

Wet season

The highest nutrient fluxes from the Lérez River occurred in the wet season, with average flow concentrations of 30 µMNO₃^- and 0.12 µM PO₄^3- (data not shown). The nutrient fluxes were modified from conservative mixing, and table 1 shows that PO4^3- was retained in the ria at a rate of -0.25 mol PO₄^3- s^-1, whereas for NO₃^- there appears to be a net source of 1.74 mol NO₃^- s^-1, possibly from the resuspension and aerobic bacterial decomposition of the bed nutrient stock. These observations for NO3^- further characterize the rapid organic nitrogen recycling relative to consumption during low phytoplankton activity and the dominance of physical over bio-geochemical processes. Similar findings have been reported for the Vigo Ria (Prego, 1994). The average NCP in Pontevedra predicted by PO4^3- from November to February was comparatively low at -20.2 mgC m^-2 h^-1 (table 1); however, some PO₄^3-may be retained in inorganic sorption reactions, thus giving apparent PO₄^3- uptake (Prego, 1993b). Conversely, NO₃^-predicts negative NCP, or net remineralization in the water column, at a rate of 8.3 mgC m^-2 h^-1. Figure 3 shows the evolution of NO3^--NCP and tendency toward heterotrophy. Net heterotrophy in Chesapeake Bay, USA (Smith and Kemp, 1995), was attributed to influxes and remineralization of river-borne allochthonous organic matter (GPP: respiration <1, where GPP is the gross primary production).

Spring

Spring incoming nutrient concentrations from the ocean were lower than in the wet season (data not shown), although higher fluxes occurred with sporadic upwelling events due to organic matter oxidation outside the reservoir (Prego, 1994), as occurs in other upwelling systems (e.g., Friedrich and Codispoti, 1981). The nutrient input was assimilated by the phytoplankton thriving under hydrodynamic control and the ria became a nutrient sink, retaining -0.28 mol PO₄^3- s^-1 and -4.58 mol NO₃^- s^-1 (table 1). Mean values of NCP in spring were -21.9 mgC m^-2 h^-1 based on NO₃^- and -22.7 mgC m^-2 h^-1 based on PO₄^3-. Spring bloom values of -42 mgC m^-2 h^-1 have been reported for the Arosa Ria (Tenore et al., 1982). This spring nutrient sink may be regarded as the synthesis of organic nutrients from the use of offshore or allochthonous NO3^- to the reservoir, analogous to new production (Epply and Peterson, 1979).

Dry season

In September 1998 river runoff fell to 1.4 m³ s^-1 and fluvial NO₃^- and PO₄^3- inputs formed less than 3% and 1% of total ria input, respectively (data not shown). Conversely, offshore NO₃^- and PO₄^3- inputs supplied 97% and >99%, respectively, of the total nutrient input to the ria, at a rate of 15.8 mol NO3^- s^-1 and 1.02 mol PO4^3- s^-1. Increased nutrient removal from spring to the dry season led to net removal rates of -11.98 mol NO₃^- s^-1 and -0.76 mol PO₄^3- s^-1 (table 1), and contributed the major part to the annual nutrient sink of -5.03 mol NO₃^- s^-1 and -0.44 mol PO₄^3- s^-1. These high removal rates may be attributable to increased water column stability between upwelling events (Álvarez-Salgado et al., 1993). High NCP rates of -57.2 mgC m^-2 h¹ (NO₃) and -61.4 mgC m^-2 h^-1 (PO4^3-) were characteristic of the dry season. These values are higher than the mean annual NCP of -24.0 (NO₃^-) or -35.8 (PO₄^3-) mgC m^-2 h^-1, although it must be noted that regenerated production (production from ammonium NH₄+) has not been considered here. The dry-season-derived NCP agrees well with the -30 mgC m^-2 h^-1 (-710 mgC m^-2 d^-1) obtained from direct ¹⁴C incubations in the Vigo Ria by Fraga (1976). The notable increase in productivity resulted from the wind-induced upwelling of nutrient rich ENACW (Álvarez-Salgado et al., 1996). Prego (1993a) calculated -42 mgC m^-2 h^-1 for a dry season NCP in the Vigo Ria using a steady-state box model, although values up to -117 mgC m^-2 h^-1 have been reported (-2800 gC m^-2 d^-1; Fraga, 1976). In the Arosa Ria, Rosón et al. (1999) derived an average dry season NCP of -35 mg C m^-2 h^-1 (-840 mgC m^-2 d^-1), and proposed this result as an accurate value because it was calculated as an integration over all the contrasting hydrodynamic regimes in the ria. Our NCP for the Pontevedra Ria, therefore, agrees well with the neighbouring rias despite the differing approaches to budget modelling. Direct measurements of GPP would be useful for drawing more direct comparisons.

 

Conclusion

The mean annual NCP in the Pontevedra Ria upwelling system is dependent upon the inorganic nutrient chosen for scaling to carbon units, whereby NO3^- predicts an NCP of

-24.0 mgC m^-2 h^-1 and PO4^3- predicts -35.8 mgC m^-2 h^-1. An

average estuarine NCP value of 22 mgC m^-2 h^-1 (190 gC m^-2 yr^-1) has been given by Boynton et al. (1982). Our results suggest an imbalance of internal fluxes and nutrient limitation; however, we have only focussed our discussion on NO3^- and PO4^3-, and quantification of NH4^- and NO2^- would clearly be desirable. Furthermore, NO3^- and PO4^3- NCP predictions are affected by denitrification and phosphorus regeneration. Short-term upwelling enrichment events influence the trophicity of the Pontevedra Ria. The ria acts as a biogeochemical reactor, processing organic matter from inorganic starting material supported by large regular injections of inorganic nutrients to the ria during upwelling. The organic material is then exported, remineralized and re-introduced into the ria. When upwelling occurs in the wet season, large amounts of the bed nutrient stock are washed out of the system. From an inorganic nutrient standpoint, the Pontevedra Ria is net autotrophic; however, there is an alternation between heterotrophy and autotrophy in the wet season for both NO3^- and PO4^3-. This finding lends no support to earlier reports of a general tendency towards net heterotrophy in marine systems (Smith et al., 1991) and, therefore, the Pontevedra Ria may be considered to be naturally eutrophic.

 

Acknowledgements

We would like to thank Captain Jorge Alonso and the crew of the R/V Mytilus and all those who participated in the sampling campaign and nutrient analyses. The Centro Meteorológico Territorial de Galicia supplied precipitation and evaporation data and Aquagest cooperated in the Gaugin station measurements. This work was supported by CICYT under the project "Hydrodynamics and biogeochemical cycle of silicon in the Pontevedra Ria" (ref. MAR96-1782). This article is a contribution to the Spanish LOICZ programme.

 

References

Álvarez-Salgado, X.A., Rosón, G., Pérez, F.F. and Pazos, Y. (1993). Hydrographic variability off the Rías Baixas (NW Spain) during the upwelling season. J. Geophys. Res., 98: 14447-14455.         [ Links ]

Álvarez-Salgado, X.A., Rosón, G., Pérez, F.F., Figueiras, F.G. and Pazos, Y. (1996). Nitrogen cycling in an estuarine upwelling system, the Ria de Arousa (NW Spain). I. Short-time-scale patterns of hydrodynamic and biogeochemical circulation. Mar. Ecol. Prog. Ser., 135: 259-273.         [ Links ]

Boynton, W.R., Kemp, W.M. and Keefe, C.W. (1982). A comparative analysis of nutrients and other factors influencing estuarine phytoplankton production. In: V.S. Kennedy (ed.), Estuarine Comparisons. Academic Press, San Diego, pp. 69-90.         [ Links ]

Epply, R.W. and Peterson, B.J. (1979). Particulate organic matter flux and planktonic and new production in the deep ocean. Nature, 282: 677-680.         [ Links ]

Fiuza, A.F.G., Hamann, M., Ambar, I., Diaz del Rio, G., Gonzalez, N., and Cabanas, J.M. (1998). Water masses and their circulation off western Iberia during May 1993. Deep-Sea Res., 45: 1127-1160.         [ Links ]

Fraga, F. (1976). Fotosíntesis en la Ría de Vigo. Invest. Pesq., 40: 151-167.         [ Links ]

Fraga, F. (1981). Upwelling off the Galician coast, northwest Spain. In: F.A. Richards (ed.), Coastal Upwelling Series. Vol. 1. American Geophysical Union, Washington DC, pp. 176-182.         [ Links ]

Friederich, G.E. and Codispoti, L.A. (1981). The effect of mixing and regeneration on the nutrient content of upwelling waters of Peru. In: F.A. Richards (ed.), Coastal Upwelling Series. Vol. 1. American Geophysical Union, Washington DC, pp. 221-227.         [ Links ]

Gordon, D.C. Jr., Boudreau, P.R., Mann, K.H., Ong, J.E., Silvert, W.L., Smith, S.V., Wattayakorn, G., Wulff, F. and Yanagi, T. (1996). LOICZ (Land-Ocean Interactions in the Coastal Zone): Biogeochemical Modelling Guidelines. LOICZ Rep. Stud., 5: 1-96.         [ Links ]

Hansen, H.P. and Grasshoff, K. (1983). Automated chemical analysis. In: K. Grasshoff, M. Ehrhardt and K. Kremling (eds.), Methods of Seawater Analysis. 2nd ed. Verlag Chemie, Weinheim, pp. 368-376.         [ Links ]

Ibarra, E. y Prego, R. (1997). La Ría de Pontevedra: Revisión de su conocimiento. Monogr. Quím. Oceanogr., 1: 55-87.         [ Links ]

Kemp, W.M., Smith, E.M., Marvin-DiPasquale, M. and Boynton, W.R. (1997). Organic carbon metabolism and net ecosystem metabolism in Chesapeake Bay. Mar. Ecol. Prog. Ser., 150: 229-248.         [ Links ]

McClain, C.R., Chao, S.Y., Atkinson, L.P., Blanton, J.O. and Castillejo, F. (1986). Wind-driven upwelling in the vicinity of Cape Finisterre, Spain. J. Geophys. Res., 91: 8470-8486.         [ Links ]

Nixon, S.W., Granger, S. and Nowicki, B. (1995). An assessment of the annual mass balance of carbon, nitrogen and phosphorus in Narragansett Bay. Biogeochemistry, 31: 15-61.         [ Links ]

Prego, R. (1993a). General aspects of carbon biogeochemistry in the ria of Vigo, northwestern Spain. Geochim. Cosmochim. Acta, 57: 2041-2052.         [ Links ]

Prego, R. (1993b). Biogeochemical pathways of phosphate in a Galician Ria (North-western Iberian Peninsula). Estuar. Coast. Shelf Sci., 37: 437-151.         [ Links ]

Prego, R. (1994). Nitrogen interchanges generated by biogeochemical processes in a Galician ria. Mar. Chem., 45: 167-176.         [ Links ]

Prego, R., Dale, A.W. deCastro, M., Gómez-Gesteira, M., Taboada, J.J., Montero, P., Villareal, M.R. and Pérez-Villar, V. (2001). Hydrography of the Pontevedra Ria: Intra-annual spatial and temporal variability in a Galician coastal upwelling system (NW Spain). J. Geophys. Res., 106: 19845-19858.         [ Links ]

Ríos, A.F. y Fraga, F. (1987). Composición química elemental del plancton marino. Invest. Pesq., 51: 619-632.         [ Links ]

Rosón, G., Álvarez-Salgado, X.A. and Pérez, F.F. (1999). Carbon cycling in a large coastal embayment affected by wind-driven upwelling: Short-time-scale variability and spatial differences. Mar. Ecol. Prog. Ser., 176: 215-230.         [ Links ]

Smith, E.M. and Kemp, W.M. (1995). Seasonal and regional variations in plankton community production and respiration for Chesapeake Bay. Mar. Ecol. Prog. Ser., 116: 217-231.         [ Links ]

Smith, S.V. and Hollibaugh, J.T. (1997). Annual cycle and intertidal variability of ecosystem metabolism in a temperate climate environment. Ecol. Monogr., 67: 509-533.         [ Links ]

Smith, S.V., Hollibaugh, J.T., Dollar, S.J. and Vink, S. (1991). Tomales Bay metabolism: C-N-P stoichiometry and ecosystem heterotrophy at the land-sea interface. Estuar. Coast. Shelf Sci., 33: 223-257.         [ Links ]

Tenore, K.L., Boyer, L.F., Cal, R.M., Corral, J., García-Fernández, C., González, N., González-Gurriaran, E., Hanson, R.B., Iglesias, J., Krom, M., López-Jamar, E., McLain, J., Pamatmat, M.M., Pérez, A., Rhoads, D.C., de Santiago, G., Tietjen, J., Westrich, J. and Windom, H.L. (1982). Coastal upwelling in the Rias Bajas, NW Spain: Contrasting the benthic regimes of the rias de Arosa and Muros. J. Mar. Res., 40: 701-772.         [ Links ]

Wooster, W.S., Bakun, A. and McClain, D.R. (1976). The seasonal upwelling cycle along the eastern boundary of the North Atlantic. J. Mar. Res., 34: 131-141.         [ Links ]