977� 2004 Estuarine Research Federation

Estuaries Vol. 27, No. 6, p. 977–985 December 2004

Ecosystem Metabolism and Carbon Fluxes of a Tidally-

dominated Coastal Lagoon

RUI SANTOS1,*, JOAO SILVA1, ANA ALEXANDRE1, NURIA NAVARRO2, CRISTINA BARRON2, andCARLOS M. DUARTE2

1 Grupo de Ecologia das Plantas Marinhas, Centro de Ciencias do Mar, Universidade do Algarve,Gambelas, 8005-139 Faro, Portugal

2 IMEDEA (CSIC-UiB), Grupo de Oceanografia Interdisciplinar, Instituto Mediterraneo de EstudiosAvanzados, C/Miquel Marques 21, 07190 Esporles (Islas Baleares), Spain

ABSTRACT: The metabolism and carbon flux in the western sector of the highly dynamic coastal lagoon Ria Formosa(south Portugal) were assessed to elucidate the relative importance of the contribution of the main communities, thetreated sewage inputs from the adjacent city of Faro, and the exchange with the adjacent coastal waters to the ecosystemmetabolism. The results depict the Ria Formosa as being a highly productive ecosystem dominated by the seagrass Zosteranoltii. The community dominated by the seagrass Cymodocea nodosa had half of the gross production of Z. noltii, followedby bare sediments and phytoplankton. The net contribution of seagrasses to community metabolism was negligible, asboth Z. noltii and C. nodosa showed a production : respiration ratio close to 1. Benthic microalgae emerge as the mostimportant components of the net metabolism. The western sector of Ria Formosa was in metabolic balance during thesummer when the study was done. Even though the total net ecosystem production was 7.22 Kmol C d�1, the errorassociated with this estimate was 8.38 Kmol C d�1, so ecosystem net production was not significantly different from zero.The Ria Formosa ecosystem is shallow and rapidly flushed by the tides, which force an important exchange of dissolvedorganic carbon (DOC) and particulate organic carbon (POC) with the adjacent coastal waters. The daily net export rateto the adjacent coastal waters, 0.98 Kmol d�1, represented 7.6% of the net ecosystem production, suggesting that thebulk of the net ecosystem production accumulates within the ecosystem. The organic carbon retention in the westernsector of the Ria Formosa is higher than net production, because the allochthonous carbon inputs from urban sewageenter the carbon mass balance with about 40% of the autochthonous processes, at about 1.6 Kmol d�1 of DOC and 2.8Kmol d�1 of POC. The western sector of Ria Formosa has an organic carbon sink of about 46.4 tons per year. Most ofthis is harvested in the form of molluscs (clams, cuttlefish, etc.) and fish (sea bream, sea bass, etc.). The total carbonharvested every year in the form of bivalves is about 40 tons, rendering the Ria Formosa the most productive seafoodarea in Portugal.

IntroductionLittoral ecosystems are interfaces between the

open ocean and land ecosystems, and their metab-olism is connected to the adjacent systems. Thelittoral ecosystems harbor highly productive com-munities, such as seagrass beds, marsh vegetation,and microphytobenthic communities, but theirproduction is also fuelled by allochthonous inputsfrom both the land and sea. Even though partic-ular littoral communities, such as macrophyte-dominated communities, tend to be autotrophic,Smith and Hollibaugh (1993, 1997), Duarte andAgustı (1998), Gattuso et al. (1998), and Hemmin-ga and Duarte (2000) observed that littoral ecosys-tems tend to be heterotrophic leading to the sug-gestion that the excess respiratory processes mustbe fuelled by allochthonous inputs. The extent ofconnectivity with the land and ocean depends on

* Corresponding author: tele: �351 289800973; fax: �351289818353; e-mail: rosantos@ualg.pt

the residence time of the water in the littoral eco-systems, which is dependent on water inputs fromland, the morphological features of the system,and tidal forcing from the sea. The terrestrial andmarine inputs to Tomales Bay, a temperate embay-ment of California, each accounted for about halfof the carbon required to support the heterotro-phic metabolism of the system (Smith and Holli-baugh 1997).

Coastal lagoons are productive ecosystems, oftensupporting important fisheries (Valiela 1995).These systems can be important sites of carbonoutwelling to adjacent coastal waters, which hasbeen well documented for tidally dominated sys-tems, such as saltmarshes and mangrove forests(Hemminga et al. 1994; Valiela et al. 2000). Thesemultiple sources (autochthonous and allochtho-nous both land-derived and marine-derived) ren-der evaluation of the carbon flow and the meta-bolic status of coastal ecosystems cumbersome, par-ticularly when intense tidal exchange imposes high

978 R. Santos et al.

Fig. 1. Map of Ria Formosa showing the study area. Blackdots are the locations of the wastewater treatment works.

variability at time scales shorter than those re-quired for community responses.

We evaluated the summer metabolism and dis-solved organic flux of the communities of the west-ern sector of Ria Formosa, a highly-dynamic coastallagoon in southern Portugal, to elucidate their rel-ative contribution to the whole system metabolism.The input of materials from land and the tidal-driven exchange between the western sector of theRia Formosa and the adjacent coastal watersthrough the inlet was evaluated. We then integrat-ed the system metabolism and the exchanges withadjacent systems to assess their relative contribu-tion to the total flux of carbon of western Ria For-mosa.

MethodsSITE DESCRIPTION

Ria Formosa is a mesotidal lagoon, separatedfrom the ocean by a system of five sand barrierislands and six inlets, which extend for about 55km along the south coast of Portugal (Fig. 1). Theaverage water depth is less than 2 m and the tidalheight varies from a maximum of 3.7 m in springtides to a minimum of 0.4 m in neap tides. Thisresults in the flushing of most of the water volumein each tidal cycle (Andrade 1990), thereby im-posing an intense exchange of materials betweenthe Ria and the adjacent coastal waters. Bare sed-iment communities and meadows of the seagrassZostera noltii occupy the lower intertidal flats. Theshallow subtidal, only exposed during low springtides, is dominated by the seagrass Cymodocea no-dosa. Ria Formosa is a highly productive coastal la-goon, supporting an intense mollusc fishery. About95% of the tidal Portuguese clam production is ob-tained in this system (Direccao Regional das Pescase Aquicultura do Sul personal communication).Watershed discharge is sporadic, and dependenton rainfall occurring mainly from October toApril. Salinity values range between 35.5‰ and36.9‰ for all the year, except during short periodsfollowing heavy rainfall when surface water salinitymay be as low as 15‰. Water temperature varies

between 12�C in winter and 27�C in the summer(Falcao 1996).

The western sector of Ria Formosa receives treat-ed sewage inputs from the adjacent city of Faro(population about 70,000) that flow into the mainnavigation channels, representing an importantsource of dissolved inorganic nutrients as well asorganic matter. The Ramalhete channel is themain channel linking the sewage-receiving area tothe western sector of the Ria Formosa (Fig. 1) andconducts most of the water exchange during floodand ebb tides. The exchange of water between thewestern sector of the lagoon and the adjacentcoastal waters occurs through the Barra inlet, avery dynamic sandy site with strong currents.

CARBON INPUTS AND OUTPUTS IN THE WESTERNSECTOR OF RIA FORMOSA

The assessment of carbon pools and exchangesfocused on the Barra inlet and Ramalhete channel.Sewage inputs of organic carbon to the Ramalhetechannel were assessed both at the outlets of theFaro wastewater treatment plant and at the chan-nel, near the edge of the study area (Fig. 1). Watersamples were collected for the measurement of dis-solved and particulate organic carbon (DOC andPOC, respectively), and the carbon inputs were es-timated as the product of the organic carbon con-centrations and the sewage discharge.

Water samples for DOC and POC concentrationestimates were obtained once an hour (DOC) orevery 2 h (POC) along each of four ebb tides andfour flood tides in summer 2002. The organic car-bon exchange with the adjacent coastal waters wasestimated as the product of the water volume ex-changed in each time period and the DOC andPOC concentrations measured during that timeperiod. Total tide fluxes of DOC and POC ex-changed through the Barra inlet were calculatedsumming all the exchanges measured in each tide.The tidal prisms were estimated using the hydro-dynamic model MOHID, developed by the MAR-ETEC Group of Instituto Superior Tecnico (Tech-nical University of Lisbon). This is a primitiveequation model based on the Navier-Stokes equa-tions with Boussinesq and hydrostatic approxima-tions that have been generally applied to simulatecomplex coastal and estuarine flows (Martins et al.2001; Coelho et al. 2002; Santos et al. 2002).

Samples for DOC analysis (10 ml) were filteredthrough precombusted (400�C for 2 h) GF/F fil-ters and collected in acid washed glass ampules.Samples were preserved by adding 100 �l of 2 NHCl before sealing the ampules by flame. TheDOC analysis was performed using Pt-catalyzed,high temperature combustion on a ShimadzuTOC-5000A analyzer. Distilled ultraviolet-radiated

Metabolism of a Coastal Lagoon 979

water from a Millipore Simplicity ultra pure watersystem was used to prepare blanks and the stan-dard curves with potassium biphthalate (range: 0–400 �mol C l�1). The instrument blank was as-sessed using 2 external standards (44–45 and 2�M) provided by Dennis A. Hansell and WenhaoChen (University of Miami). The instrument blankranged between 0 and 5.08 �mol C l�1 and wassubtracted from the measurements.

Water samples for POC analyses (1 l) were im-mediately filtered after sampling through precom-busted 47-mm diam glass-fiber filters (WhatmannGF/F). Filters were dried at 60�C for 3 d and theirweight was determined. Particulate organic matter(POM) was calculated from the weight loss follow-ing combustion at 450�C for 3 h, and converted tocarbon units (Strickland and Parsons 1968). Car-bon comprised 60% of POM at the sewage outletand 20% of POM at the Ramalhete channel. Weassumed the carbon content of POM at the Ra-malhete channel was the same for the POM at theBarra inlet.

COMMUNITY METABOLISM AND DOC FLUXES

The metabolism and net DOC production of thedominant benthic communities and the planktoncommunity in the Ria Formosa were estimated.The benthic communities examined included thesubtidal seagrass C. nodosa, the intertidal seagrassZ. noltii, and intertidal bare sediments. Metabolismand net DOC release were derived from oxygenand DOC evolution in communities enclosed with-in benthic chambers. The duration of the incuba-tion of these intertidal communities was con-strained by the tidal cycle. The communities wereenclosed in dark and clear chambers in July 2002.Each benthic chamber consisted of a PVC cylinder(18 cm diam) inserted in the sediment and a gas-tight (Hansen et al. 2000) polyethylene plastic bagfitted to the PVC cylinder. The water from thechambers was collected through a septum port sit-uated in the bag. Three replicate chambers wereincubated with clear bags and three were incubat-ed in the dark by covering the chambers with thickdark plastic bags. The volume of each chamber wasestimated by injecting 5 ml of a 0.25 M phosphatesolution at the end of the experiment. After mix-ing, 5 ml of water was collected for spectrophoto-metric determination of the phosphate concentra-tion (Hansen and Koroleff 1999). The differencebetween these concentrations and the solution al-low calculation of the volume of each chamber.The volumes varied between 5 and 14 l. The in-cubations allowed estimation of the in situ metab-olism and DOC changes in the benthic commu-nities.

The water from the chambers was sampled after

4 h from the initiation of the incubation. Watersamples from the incubations were withdrawn withacid-washed syringes. Respiration (R) was estimat-ed from the changes in dissolved oxygen (DO)concentration in the dark chambers, and gross pri-mary production (GPP) was calculated as the sumof the hourly R rates and the hourly rates of oxy-gen evolution in the clear bottles. Daily GPP rateswere calculated by multiplying the hourly rates bythe 14.5 h of light per day, and net communityproduction (NCP) was calculated as the differencebetween daily GPP and R. Oxygen units were con-verted to carbon units by assuming an O2 to carbonratio of 1. Water samples collected from the incu-bation were used to measure DOC concentrationsas described above. The net DOC community pro-duction was estimated from the rate of change inDOC between the beginning and end of each ex-periment.

A possible problem of using O2-based measure-ments to estimate net benthic metabolism is thatthe anaerobic reduction of sulphate may underes-timate respiratory losses and overestimate net pro-duction. This may be the case in the Rıa Formosa.The solution is not simple because CO2-based mea-surements are also confounded by carbonate dis-solution-formation balances that can dominateover metabolic processes when they are in closebalance. The only direct way to consider anaerobicprocesses is to quantify the burial or loss of re-duced products in the ecosystem (e.g., pyrite for-mation), which was not possible in this study.

Subsurface water samples for the measurementof the planktonic metabolism and net DOC pro-duction were collected at Barra inlet and Ramal-hete channel at the end of the flood tide (inflow-ing water) and the end of the ebb tide (outflowingwater). Water samples were siphoned into 125 mlnarrow-mouth Winkler bottles. Five replicates wereused to determine the initial oxygen concentrationand five replicate were used for each incubation inthe dark and light bottles. The light and dark bot-tles were attached to a suspension device and low-ered 0.5 m, where they were allowed to incubatefor 24 h. Community R and NCP rates were cal-culated from changes in DO concentration afterincubation of samples in dark and light bottles, re-spectively, taking into account the hours of lightduring the incubation period. GPP was calculatedas the sum of R and NCP. Bottles for bacterial res-piration (BR) were filled with filtered water (What-mann GF/F, low vacuum pressure) and incubatedas described above in dark bottles. DOC use by theplanktonic community was calculated from chang-es in DOC concentration after in situ incubationof samples in dark Winkler bottles during 24 h.

980 R. Santos et al.

TABLE 1. Community and ecosystem metabolism [average (� SE)] of the western sector of Ria Formosa. GPP � gross primaryproduction, R � community respiration, and NCP � net community production.

CommunitiesAream2

GPPmmol C m�2 h�1

Rmmol C m�2 h�1

Total GPPKmol C d�1

Total RKmol C d�1

NCPKmol C d�1

Plankton

Cymodocea nodosaZostera noltiiSedimentTotal Ecosystem

594,700

21,90056,700

335,700594,700

1.44 � 10�3

(0.10 � 10�3)6.36 (0.68)

12.47 (0.13)2.58 (1.46)

0.60 � 10�3

(0.13 � 10�3)4.35 (0.35)7.57 (1.66)0.73 (0.44)

12.86 � 10�3

(0.89 � 10�3)2.08 (0.22)

10.61 (0.11)12.99 (7.33)25.68 (7.67)

8.56 � 10�3

(1.80 � 10�3)2.28 (0.18)

10.30 (2.25)5.88 (3.52)

18.47 (3.96)

4.30 � 10�3

(1.95 � 10�3)�0.20 (0.32

0.31 (1.69)7.11 (8.71)7.22 (8.38)

Fig. 2. Community respiration rates (R), gross primary production (GPP), net community production (NCP), bacterial respirationrates (BR), contribution of BR to R (%BR), and net dissolved organic carbon (DOC) production at the stations Barra and Ramalhete.H indicates high tide and L indicates low tide.

Five replicates were used to determine the initialand final DOC concentrations as described above.

DO concentration was measured using a spectro-photometric modification of the Winkler titrationmethod (Pai et al. 1993; Roland et al. 1999). Thespectrophotometric determinations were made in1-cm cuvettes at a wavelength of 430 nm on a Beck-man DU 650 spectrophotometer. We related theabsorbance at 430 nm (Abs430) in Winkler-fixedsamples to DO values obtained by titration over alarge range of DO concentrations. The linear mod-el was: DO (mg l�1) � 0.0067 � (Abs430 � 1000)� 0.0217 (R2 � 0.99).

The areal (m�2) rates of metabolism and netDOC production estimated were converted to totalcarbon production or consumption across thewestern sector of the Ria Formosa as the productof the areal rates and the estimated area coveredby the different communities (Table 1), whichwere delineated from aerial-photograph mosaicsfrom 1998. These images were digitized and geo-

referenced. Photo-interpretation and manual fac-torization of the vegetation types was performed.Each area corresponding to a particular vegetationclass was drawn in an AutoCAD Map layer so thateach class could be easily identified and isolated.A series of biological and topographical field sur-veys were done to ground-truth the vegetation clas-ses and the position coordinates. The correctedmapping of the vegetation types of the western sec-tor of Ria Formosa was produced and the areascovered by them were calculated. The area and vol-ume covered by plankton was estimated consider-ing the mean inundated area in the Ria Formosaand a mean depth of 1 m.

Results

ECOSYSTEM METABOLISM

The highest plankton community R rates werefound at the Ramalhete channel at high tide (Fig.2). Respiration increased significantly from 5.47

Metabolism of a Coastal Lagoon 981

Fig. 3. Respiration (R) versus gross primary production(GPP) of benthic and planktonic communities.

TABLE 2. Dissolved organic carbon fluxes [average (� SE)] of Ria Formosa communities. DOC light � dissolved organic carbonuse during light hours, DOC dark � dissolved organic carbon use during night hours, and Total DOC � daily net DOC production.

CommunitiesAream2

DOC Lightmmol C m�2 h�1

DOC Darkmmol C m�2 h�1

Total DOCKmol C d�1

PlanktonCymodocea nodosaZostera noltiiSediment

594,70021,90056,700

335,700

0�0.23 (0.32)

0.30 (0.67)�1.00 (0.55)

�0.56 � 10�3 (0.36 � 10�3)�0.03 (0.21)�1.85 (0.92)�0.31 (0.47)

�3.19 � 10�3 (1.93 � 10�3)�0.08 (0.15)�0.69 (1.04)�5.97 (4.19)

�mol C m�2 d�1 at low tide to 44.38 �mol C m�2

d�1 at high tide at Ramalhete channel; there wasno significant difference (p 0.05) at Barra inlet.The tidal pattern of BR was the opposite of totalplankton respiration, as it was lower at high tideand increased significantly (p 0.05) at low tide.The contribution of BR to total plankton respira-tion was higher at low tide than at high tide bothat Ramalhete channel and Barra inlet. At Ramal-hete channel, BR accounted for 79.2% of planktonR at low tide and at high tide it accounted only for4.6%. At Barra inlet, the tidal variation in the con-tribution of BR to community respiration was low-er, ranging from 66.6% at low tide to 61.8% at hightide. BR accounted for 53.1% of plankton com-munity respiration rates. GPP and NCP increasedfrom low tide to high tide both in Ramalhete chan-nel and Barra inlet. The plankton community wasalways autotrophic with positive NCP (i.e., GPP R) in both stations at both tide levels.

Both GPP and R of benthic communities in RiaFormosa exceeded those of the plankton commu-nity. GPP ranged from 1.44 � 10�3 mmol C m�2

h�1 for plankton to 12.47 mmol C m�2 h�1 for Z.noltii; R ranged from 0.60 � 10�3 mmol C m�2 h�1

for plankton to 7.57 mmol C m�2 h�1 for Z. noltii(Table 1). Both GPP and R were two-fold higherin Z. noltii than in C. nodosa. The community ofbare sediments showed the lowest GPP and R ofbenthic communities. Due to the large area occu-pied by bare sediments, these communities showedthe largest contribution to the net carbon produc-tion in the western sector of Ria Formosa (7.11Kmol C d�1). This contribution was not signifi-cantly different from zero because of the large er-ror associated with this estimate (8.38 Kmol C d�1).The seagrass communities were found to be inmetabolic balance, with their net carbon produc-tion not being significantly different from 0. Thenet carbon production of the plankton communi-ties were the only estimates significantly differentfrom zero and were autotrophic.

The GPP of Ria Formosa communities were sig-nificantly correlated with their R rate (p 0.001),with this relationship closely following the 1:1 line,indicative of a general metabolic balance in thecommunities investigated (Fig. 3). The produc-tion : respiration (P : R) ratio of the plankton com-munities was 1.50, which has an excess productionrelative to demand of 50% of the GPP.

The Ria Formosa communities showed a net up-take of DOC under both dark and light except forZ. noltii, which showed a net release of 0.30 mmolC m�2 h�1 in the light (Table 2). There was anuptake of DOC by plankton at all stations, exceptat Barra inlet at low tide, when DOC released 7.50�mol C m�2 d�1 (Fig. 2). On a daily basis, all com-munities were net sinks of DOC, suggesting thatthis DOC must come from external inputs.

CARBON FLUXES

The average � SE organic matter concentrationsin the summer of the sewage inputs to Ria Formosawere 1,127 � 105.3 �M DOC and 5,058 � 492.3POC, which diluted to 108 � 4.92 �M DOC and177 � 8.0 �M POC at the Ramalhete channel.There were no significant differences betweenhigh tide and low tide concentrations of both DOCand POC at Ramalhete channel. The associated or-ganic carbon inputs to Ria Formosa from Faro sew-

982 R. Santos et al.

Fig. 4. Tidal export and import of a) dissolved organic car-bon (DOC) and b) particulate organic matter (POC) throughthe Barra inlet.

ages were calculated as 15.8 Kmol d�1 of DOC and70.8 Kmol d�1 of POC, representing a total organiccarbon input of 86.6 Kmol d�1. About 10% of al-lochtnous DOC and 4% of allochtnous POCreached the western basin with the remaining flow-ing through the eastern sector, as derived frommass balance analysis, representing an input ofland-derived carbon of 4.4 Kmol d�1 to the westernbasin of Ria Formosa.

The DOC concentration was lower at Barra inlet(Bhigh � 108.46 � 0.46 �M and Blow � 84.64 � 4.78�M) than at Ramalhete channel (Rhigh � 150.04 �13.81 �M and Rlow � 137.75 � 4.55 �M), consis-tent with the increase expected from sewage inputsand the decline along the ecosystem expectedfrom the net DOC use of the communities. Thehigher DOC concentrations at high tide comparedto low tide derived from the hydrodynamic regimeof this area, where the sewage inputs are divertedto the eastern sector during ebb tide and to thestudy site during flood tide. The average tidal ex-port of DOC through the Barra inlet during ebbtides was 0.70 � 0.21 Kmol and the import duringflood tides was 0.37 � 0.18 Kmol (Fig. 4). The av-erage tidal export of POC was 0.54 � 0.21 Kmoland the import was 0.38 � 0.19 Kmol. There wasa net export of 0.33 Kmol of DOC and 0.16 Kmolof POC per tidal cycle, or twice these amounts perday.

DiscussionThe results presented here depict the Ria For-

mosa as a highly dynamic ecosystem, containinghighly productive communities. The Z. noltii com-munity, a small species that develops extensivemeadows sustaining a rather low biomass (229.42� 19.20 to 543.50 � 17.84 g DW m�2, Cabaco un-published data) half of the general average for sea-grasses (Duarte and Chiscano 1999), is able to sus-tain a sizeable GPP (within the average value re-ported for seagrass communities, Hemminga andDuarte 2000). The net contribution of seagrassesto community metabolism is negligible, as both C.nodosa and Z. noltii showed a P : R ratio close to 1and have a coverage area 10 times below that ofplankton and bare sediments. Benthic microalgaeemerge as the most important component of themetabolism in the Ria Formosa, being responsiblefor most of the net production in the ecosystem.At the same time, all of the communities in thesystem were net sinks of DOC, ranging from mar-ginal sinks (plankton and seagrass communities)to substantial sinks in the case of bare sedimentcommunities.

The consideration of the statistical significanceof total system production and R estimates showsthe western sector of Ria Formosa to be in meta-

bolic balance during the summer season. The onlynet producer was the plankton, but its contributionwas very low when compared with benthic com-munities. The high errors associated with the ben-thic NCP estimates do not allow us to conclude ifthe system is autotrophic or in metabolic balance.A possible factor driving to metabolic balance isthe underestimation of benthic remineralizationby the use of O2-based methods. This underesti-mation is at most 25% in benthic systems (Heip etal. 1995). The reason why the effect is low evenunder high sulfate reduction rates is that most ofthe sulfate reduced in shallow coastal sediments isreoxidized again and captured in O2-based mea-surements. In a detailed budget of sulfur in coastalsediments, Jorgesen (1977) showed that out of 6.2g S m�2 yr�1 undergoing sulfate reduction, only12% (0.7 g S m�2 yr�1) was buried. Kemp et al.(1997) estimated that half of the sediment oxygenconsumption rate in Chesapeake Bay was due tosulfide reoxidation. This underestimation is prob-ably not relevant in the western sector of Ria For-mosa as recent CO2-based summer measurements

Metabolism of a Coastal Lagoon 983

of Z. noltii community R (Silva et al. In press)showed values of 1.3–9.5 mmol C m�2 h�1, whichare in the order of the values estimated here (Ta-ble 1). CO2-based net carbon production estimatesof Z. noltii community (�0.24 Kmol C d�1) suggesta low heterotrophy during summer. In an annualbasis, the metabolism of the system may tend to beautotrophic, as the production of some of the keycomponents of the community is lowest in thesummer, when this study was conducted and whenrespiratory losses are also likely to be highest.

The metabolic balance reported for the westernsector of Ria Formosa differs from estuaries, whichare generally heterotrophic, and from macrophyte-based systems (Gattuso et al. 1998), which are gen-erally autotrophic. These authors estimated an av-erage net ecosystem production for macrophyte-based systems about 6-fold higher than that re-ported for Ria Formosa. The low net ecosystemproduction may be accounted for by a high R ratecompared to macrophyte-based systems, which isassociated with the high abundance of fauna com-ponents, particularly molluscs and crustaceans,and the use of the important organic matter inputsfrom the sewage of the city of Faro, which delivershigh quantities of POC and DOC to the system.The DOC inputs support a fraction of the systemrespiration, as the ecosystem consumed DOC at arate of 6.74 Kmol d�1, removing all of the inputsfrom land. In the DOC mass balance there is asource of DOC missing as the consumption plusthe net export through the Barra inlet, 7.4 Kmold�1, is much higher than the land inputs, 1.6 Kmold�1. Even if all sewage POM was decomposed toDOC within the system, the total land inputs to thestudy area would be 4.4 Kmol d�1, instead of 1.6Kmol d�1, still much less than the consumptionplus the net export through the Barra inlet, 7.4Kmol d�1.

The Ria Formosa filter feeders rely mostly on thePOC derived from the primary producers thanfrom the POC delivered from land. The assessmentof carbon, nitrogen, and sulphur flow to bivalvesusing stable isotopes have shown the dominant bi-valve species to selectively feed on POM, mostly onthe fraction derived from phytoplankton, benthicmicroalgae, and green algae of the order Ulvales,Z. noltii, and Spartina maritima (Machas et al. 2003).The carbon stable isotope signal of POM derivedfrom land is highly depleted in relation to POMderived from the Ria Formosa, particularly in thewinter. This signal is not reflected in the filter feed-ers.

The Ria Formosa ecosystem is rapidly flushed bythe tides, resulting in a short residence time (An-drade 1990) and forcing an important exchangewith the adjacent coastal waters. We measured a

net export of both DOC and POC; about 40% ofthe organic carbon exiting the Ria Formosa duringthe ebb tide was not compensated by the organiccarbon entering the lagoon during flood tides.The daily net export rate (0.98 Kmol d�1), repre-sents 22% of the allochthonous carbon inputsfrom land estimated at about 4.4 Kmol d�1, sug-gesting that the bulk of this input, about 3.4 Kmold�1, accumulates within the ecosystem.

These results depict the Ria Formosa as beingnot only a highly productive ecosystem, but alsoone with prominent links to adjacent ecosystems,which enter the carbon mass balance with a com-parable weight as that of the autochthonous pro-cesses. An overall depiction of the summer carbonbalance of the Ria Formosa requires explicit con-sideration of inputs and outputs with adjacent eco-systems (land and coastal ocean) as well as the au-tochthonous processes. A parsimonic representa-tion of the resulting mass balance can be summa-rized by the equation:

GPP � I � R � E � S

where I is the import of organic carbon, E repre-sents the export, and S represents the storage inthe system. The results presented, which containestimates for all terms except S, allow estimationof S in the western sector of the Ria Formosa as:

S � GPP � I � R � E�1� 25.7 � 4.4 � 18.5 � 1.0 � 10.6 Kmol C d

equivalent to a yearly organic carbon sink of 46.4tons. As stated before care must be taken in con-sidering this value as the errors associated with itare very high. A fraction of the stored carbon isremoved in the form of molluscs (clams, cuttlefish,etc.) and fish (sea bream, sea bass, etc.), which ren-ders the Ria Formosa the most productive seafoodarea in Portugal. Our results suggest that this sum-mer production is supported by urban sewages asthe natural communities within the Ria Formosaare probably in metabolic balance.

The Ria Formosa lagoon produces each yearmore than 10,000 tons of shellfish (Direccao Re-gional das Pescas e Aquicultura do Sul personalcommunication). The intertidal study area is about10% of the total intertidal lagoon; the shellfish har-vest of the western sector of the Ria Formosa canbe estimated as more than 1,000 tons per year. Theshellfish flesh dry weight is about 10% of freshweight (Silva unpublished data), with a carboncontent of about 40%. The total carbon harvestedevery year in the western sector of the Ria Formosais 40 tons, suggesting that almost all of the carbonstored is probably harvested in the form of sea-food.

984 R. Santos et al.

The results demonstrate the importance of ex-changes with adjacent ecosystem in increasing thenet carbon accumulation in the western sector ofthe Ria Formosa. The allochthonous surplus ren-ders this ecosystem an important source of har-vestable biomass to society. The carbon mass bal-ance represents a short-term balance that may notbe representative of annual conditions. Allo-chthonous inputs remained relatively comparablealong the seasons (Machas unpublished data), butboth the plankton and the Z. noltii communitiesare most productive during winter when respira-tion rates decline by as much as 10 fold. The esti-mate of storage derived in this study may somewhatunderestimate the long-term values.

Estuaries and coastal lagoons, such as Ria For-mosa, are highly productive ecosystems and majorsites for seafood production, and yet many are het-erotrophic ecosystems (Gattuso et al. 1998; Hop-kinson and Smith 2004). Hopkinson and Smith(2004) report estuaries with GPP 400 mmol Cm�2 d�1 tend to be heterotrophic, while those 500 mmol C m�2 d�1 tend to be autotrophic. Thewestern sector of Ria Formosa is in metabolic bal-ance with an average GPP of about 260 mmol Cm�2 d�1. This difference may be attributed to thehigh flushing rate of the western sector of Ria For-mosa, rendering the truly estuarine area restrictedto the small area directly affected by sewage. Thecomprehensive depiction of the carbon fluxes inthis study, where four out of the five terms of thebudget were directly determined, allowed the bud-getary exercise to be conducted, revealing the RiaFormosa to be an important sink of organic matterfrom land and supporting an important extractionof biomass for human use.

ACKNOWLEDGMENTS

This work was part of project EUROTROPH (EVK3-CT-2000-00040) funded by the European Commission and the SpanishPlan of I�D (REN2001-4977-E), and a CSIC-ICCTI bilateral co-operation program. We thank A. Cunha, L. Mata, and R. Del-gado for assistance in the field and N. Castillo, R. Santiago, andM. Calleja for assistance with DOC measurements. C. Barronwas funded by a fellowship and scholarship from the govern-ment of the Balearic Islands.

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Received, January 27, 2004Revised, July 6, 2004

Accepted, August 3, 2004