Net Ecosystem Metabolism and Nonconservative Fluxesof Organic Matter in a Tropical Mangrove Estuary, PiauíRiver (NE of Brazil)

Marcelo F. L. Souza & Viviane R. Gomes &

Simone S. Freitas & Regina C. B. Andrade &

Bastiaan Knoppers

Received: 30 October 2007 /Revised: 30 July 2008 /Accepted: 30 September 2008 /Published online: 21 October 2008# Coastal and Estuarine Research Federation 2008

Abstract Net ecosystem metabolism (NEM) was measuredin the Piauí River estuary, NE Brazil. A mass balance of C, N,and P was used to infer its sources and sinks. Dissolvedinorganic carbon (DIC) concentrations and fluxes weremeasured over a year along this mangrove dominated estuary.DIC concentrations were high in all estuarine sections,particularly at the fluvial end member at the beginning of therainy season. Carbon dioxide concentrations in the entireestuary were supersaturated throughout the year and highest inthe upper estuarine compartment and freshwater, particularlyat the rainy season, due to washout effects of carbonaceoussoils and different organic anthropogenic effluents. Theestuary served as a source of DIC to the atmosphere with anestimated flux of 13mol CO2 m

−2 year−1. Input from the riverwas 46 mol CO2 m

−2 year−1. The metabolism of the systemwas heterotrophic, but short periods of autotrophy occurredin the lower more marine portions of the estuary. The pelagicsystem was more or less balanced between auto- and

heterotrophy, whereas the benthic and intertidal mangroveregion was heterotrophic. Estimated annual NEM yielded atotal DIC production in the order of 18 mol CO2 m

−2 year−1.The anthropogenic inputs of particulate C, N, and P,dissolved inorganic P (DIP), and DIC were significant. Thefluvial loading of particulate organic carbon and dissolvedinorganic nitrogen (DIN) was largely retained in two flowregulation and hydroelectric reservoirs, promoting a reduc-tion of C:N and C:P particulate ratios in the estuary. The netnonconservative fluxes obtained by a mass balance approachrevealed that the estuary acts as a source of DIP, DIN, andDIC, the latter one being almost equivalent to the losses tothe atmosphere. Mangrove forests and tidal mudflats wereresponsible for most of NEM rates and are the main sites oforganic decomposition to sustain net heterotrophy. The mainsources for this organic matter are the fluvial and anthropo-genic inputs. The mangrove areas are the highest estuarinesources of DIP, DIC, and DIN.

Keywords Autotrophy/heterotrophy .

Carbon dioxide fluxes . Anthropogenic loading .Mass balance

Introduction

Since a long time, mangrove and salt marshes have beenconsidered as relevant sources of organic carbon to coastalwaters (Teal 1962; Odum and Heald 1975). However, theliterature revision showed that though outwelling of organicmatter and nutrients was observed in mangrove ecosystems,they can also act as sinks of organic carbon, including indissolved forms (Lee 1995). This matter is still of interest asno consistent pattern has appeared. Cai et al. (1999) hasfound that salt marshes wetlands are sites of intenseremineralization, which reduce the importance of organic

Estuaries and Coasts (2009) 32:111–122DOI 10.1007/s12237-008-9104-1

M. F. L. Souza :R. C. B. Andrade : B. KnoppersPrograma de Pós-graduação em Geoquímica,Departamento de Geoquímica, Universidade Federal Fluminense,Outeiro de S.J. Batista, s/n,Niterói, Rio de Janeiro 24.007-000, Brazil

V. R. Gomes : S. S. FreitasDepartamento de Engenharia Química,Universidade Federal de Sergipe,Campus Universitário,São Cristóvão, Sergipe 49.100-000, Brazil

Present address:M. F. L. Souza (*)Laboratório de Oceanografia Química, PPGSAT, DCET,Universidade Estadual de Santa Cruz,Rod. Ilhéus/Itabuna Km 16,Ilhéus, Bahia 45.650-000, Brazile-mail: marland@uol.com.br

matter export to the estuary compared with dissolvednutrients. It should be noted that these communities differfrom mangrove by lower aerial biomass storage, with lowerlignin content. Mangroves are also characterized by thepresence of expressive microphytobenthic and macroalgaeassemblages, which include nitrifiers, denitrifiers, and N-fixing organisms. The inputs of particulate organic carbonfrom mangrove litter was recognized as being moreimportant for the maintenance of the microbial food chainand nutrient regeneration in mangrove sediments thanorganic matter outwelling to estuary (Wafar et al. 1997).Dittmar et al. (2001) reported export of dissolved andparticulate organic matter from a North Brazilian mangroveto the Caeté estuary, but the rapid removal from the watercolumn reduced their export to coastal waters. Dissolvednutrients were also exported from this mangrove system(Dittmar and Lara 2001), but these authors considered thatoutwelling should only occur in mangroves of macrotidalregions, with positive sedimentation balances and nitrogenfixation. Furukawa et al. (1997) observed even a slightinwelling of organic carbon from creek to mangrove, in amangrove swamp in Australia.

Estuarine systems tend to exhibit net heterotrophy(Smith and Atkinson 1994; Borges et al. 2006), a kind ofmetabolic balance that requires the predominance oforganic detritus over dissolved nutrient inputs, as it isfound in many mangrove dominated systems (Bouillon etal. 2003; Mukhopadhyay et al. 2006). As a result, not onlythe estuarine waters but also the associated mangrove areas(including aerial biomass) can act as a source of carbondioxide and methane to atmosphere in an annual scale(Mukhopadhyay et al. 2002). The assessment of this trophicstatus of estuaries and their role in the transport of organicmatter and nutrients to coastal waters is a key to understand-ing their importance in a global scale. This knowledge is stillscarce for tropical estuaries of many regions.

This paper addresses the balance between autotrophyand heterotrophy and estimates the importance of fluvial,anthropogenic, and mangrove inputs for the maintenance ofsystem metabolism at the mangrove dominated Piauí Riverestuary, NE Brazil. It also intends to test the hypothesis thatthe fluvial (mainly anthropogenic) organic loading sustainsa net estuarine heterotrophy and that mangrove is the mainsite of recycling, acting as a nutrient exporter.

Material and Methods

Study Area

The Piauí River estuary (Fig. 1) extends over 35 km, withan area of 45 km2. It is a ria-type estuary, with mean depthof 3.8 m, with maximum reaching 25 m near the mouth

(Souza 1999). It is characterized by an ample mesotidalflushing, with maximum tidal range of 2.5 m and theaverage freshwater discharge of about 5 m3 s−1, distributedirregularly through the year. The warm humid/subhumidlittoral receives a pluvial input of 1,400 mm, in contrastwith 750 mm in the Mediterranean dry climate found in theinland areas of the drainage basin. The estuary is wellmixed during most of the year, with a mean salinity of 21.There is a slight stratification in the outer portion during therainy season, when freshwater extends to beyond station 3(Souza 1999). The outer estuary is relatively unpolluted,while upstream of a dam near the city of Estância (Fig. 1),the river receives untreated domestic sewage and industrialeffluents (food processing and textile). Downstream of thisdam, the residues are retained by another dam reservoirduring most of the dry season, when freshwater discharge isreduced to less than 0.5 m3 s−1. This shallow stagnantpolluted water becomes anoxic, and a measurable amountof particulate organic carbon and dissolved inorganicnitrogen (DIN) loading is retained in this reservoir,probably by respiration and denitrification and/or sedimen-tation (Souza 1999). Mangrove logging is also an importantand growing impact.

Sampling Strategy

Free water samples were taken ten times between Januaryand December 1996, at stations located in the inner, mid-,and outer estuary (st. 3, 6, and 7; Fig. 1). These sampleswere collected just before dawn, dusk, and after variabletime intervals between to assess the net ecosystemmetabolism (NEM). Incubations using biological oxygendemand (BOD) bottles were conducted at six times withinthis period to estimate the daily net pelagic metabolism(NPM).

Water sampling was also carried from December 1995 toDecember 1997, comprising eight surveys along the estuaryfrom fresh to marine end members. These samples wereused to construct the mass balance and estimate the netecosystem metabolism by monthly dissolved inorganiccarbon (DIC) changes.

In the estuarine stations, water samples were collected at0.5 and 1.0 m depth above the bottom. Temperature wasmeasured in the field with a Hg thermometer. Subsampleswere reserved to the determination of conductivity with abench digital meter. Aliquots were collected separately insyringes for alkalinity analysis. All samples were stored inpolyethylene flasks previously washed with HCl 1:1,distilled deionized water, and thoroughly rinsed with thesample water. The flasks were kept on ice in the dark forabout 20 min, while transported to the field laboratory(Fig. 1). In the lab, pH was immediately measured(National Bureau of Standards scale) using a digital pH

112 Estuaries and Coasts (2009) 32:111–122

meter with ±0.001 resolution and a combined glasselectrode. The samples were filtered through WhatmannGF/F glass fiber filters of 47 and 25 mm diameter, reservedfor further analysis of particulate material. The filtrate wasfrozen until dissolved inorganic nutrients determination.

Chemical Analysis

Total alkalinity was determined just after pH measurement,by potentiometric titration with a high precision bench pHmeter (Digimed® DM-21, ±0.001 pH resolution), with0.0100 M HCl. The equivalence point was achieved by amodified Gran’s function (Carmouze 1994). The influenceof humic and fulvic acids was minimized carrying theGran’s titration to a pH of about 3.2 (Cai and Wang 1998).Dissolved inorganic carbon content was calculated withtotal alkalinity, pH, and salinity (S). The completeprocedure is detailed by Carmouze (1994). Dissolvedinorganic nutrients (ammonia, nitrite, nitrate, phosphate,

and silicate) were analyzed according to Grasshoff et al.(1983). Particulates were retained on GF/F filters andanalyzed separately for total suspended solids by gravim-etry, particulate organic carbon (POC) by wet chemicaloxidation (Strickland and Parsons 1972), and nitrogen andphosphorus as in Grasshoff et al. (1983).

Net Estuarine Metabolism, Mass Balance,and Stoichiometric Calculations

The net ecosystem metabolism or production (NEM = grossprimary production−respiration) was evaluated using threeapproaches: (a) the free-water method using the daily DICchanges integrated to an annual scale (Hall and Moll 1975),(b) the free-water method using the monthly DIC changesintegrated to an annual scale (Carmouze 1994), and (c)mass balance approach for dissolved inorganic C, N, and Pand stoichiometric linkage (Gordon et al. 1996). Theassessment of net ecosystem metabolism is considered as

Fig. 1 The Piauí River estuaryand the location of samplingstations. Hatched areas representmangrove forests. Station 1sampled in different locationsaccording salinity

Estuaries and Coasts (2009) 32:111–122 113113

the sum of all autotrophic and heterotrophic processesoccurring in the water column and sediment (Nixon andPilson 1984; Carmouze 1994; Smith and Hollibaugh 1997),including the intertidal areas during flooding.

The application of free-water technique to estuarinewaters has been much criticized due to the dynamic natureof water advection and gas diffusion through the atmo-sphere–water interface along the estuarine mixing zone(Hall and Moll 1975; Nixon and Pilson 1984). In thepresent study, we used the variation of carbon dioxideinstead of dissolved oxygen concentration, a gas with anexchange coefficient much lower than dissolved oxygen tomeasure the concentration changes generated by the NEM.

DIC measurements from the 24-h estuarine surveys atstations 3, 6, and 7 were used to calculate NEM. Monthlychanges of average daily DIC concentrations were used tointegrate these rates along the year. The exchange of CO2

with the atmosphere was estimated using calculations basedin Fick’s law and the stagnant layer model (Carmouze 1994).The calculated exchange coefficients ranged from 0.2–0.8 mday−1, according with wind velocity measured with a digitalanemometer near the sampling site. In addition to total NEM,the NPM was also measured during six surveys, throughincubations of estuarine water in 300-ml BOD flasks, at timeintervals of 4 to 6 h, along a diurnal cycle.

The DIC data from 24 h and the eight surveys along theestuary were combined to estimate the monthly changes ofmean DIC concentrations within the three estuarine zones.These results were upscaled to produce an annual NEMrate.

We also used the results of a simple approach to a massbalance of dissolved inorganic nutrients, made followingthe Land–Ocean Interactions in the Coastal Zone (LOICZ)/International Geosphere–Biosphere Programme guidelines(Gordon et al. 1996). A stoichiometric linkage was appliedusing the annual average of the C:N:P composition ofparticulate organic matter. This composition was deter-mined in industrial effluents, river, and estuarine particulatematter. The mangrove stoichiometry used here was found inthe literature (Lanza et al. 1997). Using these calculations,we inferred the rates of biogeochemical processes, as netnonconservative fluxes, nitrogen fixation/denitrification,and primary production/respiration rates (Gordon et al.1996). The detailed procedures and results of the one- andthree-box mass balance used in this paper were described inSouza et al. (2000).

Estimation of the Roles of Sediments and Mangroves

The results obtained were used to infer some of theunknown fluxes inside the estuary according to a proceduremodified from Cai and Wang (1998). First, we assessed therole of the mangrove in the estuarine balance of CO2,

decomposing the nonconservative fluxes occurring in theestuarine water column (pelagic) and sediment and man-grove surfaces (mangrove). These terms were included inthe balance, placed in the proper side of equation accordingwith its sign (inputs/outputs at the left and right side,respectively). The contribution of mangrove (in factmangrove plus tidal flats and subtidal sediment) to thedissolved nutrient fluxes was estimated according to thefollowing equations:

Dissolved inorganic carbon:

Mangroveþ VRiverDICRiver þ VXDICX ¼ Pr od:pel:

þ VRDICR þ DICatm

ð1Þ

Vriver×DICriver fluvial inputsVX×DICX mixing with coastal watersVR×DICR residual fluxDICatm exchange with atmosphereProd.pel. pelagic net production

The same procedure was applied to the DIN anddissolved inorganic phosphorus (DIP). In these cases, thenutrient assimilation by pelagic production was estimatedby stoichiometric linkage using the mean C:N and C:P ratioof the system.

Dissolved inorganic nitrogen and phosphorus:

Mangroveþ VRiverDINRiver ¼ Prod:pel: þ VRDINR þ VXDINX

ð2Þ

Mangroveþ VRiverDIPRiver¼ Prod:pel: þ VRDIPR þ VXDIPX:

ð3ÞLegend as DIC except Prod.pel. calculated as above.

Results and Discussion

pH Along the Estuary

The autotrophic and heterotrophic processes promote a pHincrease/decrease, respectively. Other factors related toestuarine pH are the chemical nature and discharge offreshwater, degree of seawater mixing, the presence ofhumic compounds, and pollution.

In the estuary, marine influence is considerably strongerthan fluvial input. A rough estimate of tidal prism usingestuarine area (34×1010 m2) and a mean tidal amplitude of1.2 m is ∼8.2×107 m3 day−1, compared to mean freshwaterdischarge of only about 6.1×105 day−1. As a consequence,the Piauí River estuarine waters were provided withconsiderable pH buffering capacity.

114 Estuaries and Coasts (2009) 32:111–122

The freshwater exhibited large temporal changes of pH(Fig. 2a,b). The maximum value was recorded during thepeak of dry season (December 1995; Fig. 2a), when fluvialdischarge was almost absent. The fluvial pH varied between7.0 and 7.6 in the other surveys. The estuarine waters alsopresented a large pH range and the distribution seems to berelated with the buffer capacity and long-term mixing.

Dissolved Inorganic Carbon

DIC concentrations in the Piauí estuary exceeded by farthose found in the Georgia estuaries by Cai and Wang(1998), especially in the freshwater end member. These

concentrations can be due to the contribution of natural andanthropogenic processes, as the dissolution of carbonaticrock (Formation Cotinguiba, Cretaceous) and mainly thedischarge of domestic and industrial with a high content ofdecomposing organic matter for the fluvial concentrations.The latter process is especially apparent during the twosurveys in March 1996 (Fig. 3), when a sudden increase ofrunoff promoted the flushing of the stagnant pollutedfreshwater to the estuary. In this month, the concentrationin freshwater end member reached up to 4,900 μmol l−1,which correspond to a pCO2 of about 10,000 μatm. Thisvalue is similar to those found to the humic rivers ofGeorgia (∼8,100 μatm; Cai and Wang 1998) and almost ashigh as the observed in the Scheldt river (16,300 μatm;Abril et al. 2000). High pCO2 in freshwater is not a recentfinding and is already mentioned in the literature, especiallywhen draining carbonate terrains (Drever 1982). In theestuarine zone, the concentrations were about 2,200±360 μmol l−1, and events with pCO2 higher than 1,000 μatmwere not rare. The inputs of humic and fulvic acids areprobably considerable in sight of the great area covered bymangrove. However, the influence of these compoundsupon the analytical technique employed for alkalinityanalysis and further DIC calculations should only berestricted to the narrow and shallow inner estuarine portion.Otherwise, this influence was minimized by the titrationprocedure, till pH 3.4. These values are below the observedin heavily polluted estuaries such as the Rhine (3,500–6,300 μatm; Kempe 1982) and the Scheldt (5,700 μatm;Frankignoulle et al. 1996).

Fig. 2 Mixing diagrams of pH showing the four different patterns ofdistribution along the salinity gradient. Filled circle=19 Dec 95,unfilled square=2 Mar 96, filled triangle=20 Apr 96, unfilled circle=18 Sep 96

Fig. 3 Mixing diagram of the dissolved inorganic carbon concen-trations. a End of the dry season (2 March 1996) and at the beginningof the rainy season (16 March 1996); b wet season. Filled square=19Dec 95, filled triangle=2 Mar 96, filled circle=16 Mar 96, unfilledtriangle=20 Apr 96, unfilled circle=18 May 96; plus symbol=18 Jun96; ex symbol=18 Sep 96; unfilled square=22 Nov 96

Estuaries and Coasts (2009) 32:111–122 115115

The importance of the fluvial inputs with high concen-trations of DIC was restricted to the beginning of the wetseason. During most of the year, the mixing diagram ofDIC indicated seawater intrusion to be the main source. Thenonlinear DIC × S relationship expresses the nonconserva-tive fluxes within the estuary (net heterotrophy).

Saturation and Exchange of CO2 Through Atmosphere/Water Interface

The value and changes of CO2 saturation are usefulindicators of the metabolic process in an aquatic ecosystem(Carmouze 1994). Figure 4 presents the percent of CO2

saturation at the beginning of the photoperiod (∼6:00 A.M.).The estuary tended to be supersaturated, except at thesampling station nearest to the sea, in which subsaturationoccurred in April, May, June, and November. The inner-most station presented extremely high values, with peaks inboth dry and wet seasons. This supersaturation at thebeginning of the photoperiod indicates that the heterotro-phic activity during the night was intense enough to drivepCO2 above atmospheric values.

The supersaturation in the dry season can be explainedby low water exchange in the upper portion of the estuary.In the absence of a significant freshwater input, the waterrenewal is forced just by net evaporation and consequentresidual flux and also by tidal mixing. Tidal mixing is veryineffective in this narrow and shallow part of the estuary.Thus, it is more likely that the retention and respiration oforganic material previously discharged by the river andfrom the mangrove are responsible for these high CO2

concentrations. Anaerobic metabolism probably is animportant component of the respiration processes, especial-ly inside the sediment. Sediments in Piauí River estuary

have ∼3.5% organic C, compared with ∼0.5% inorganic C(Dr. E.C.G. Couto, unpublished data). This organic contentis about twice that found by Smith and Hollibaugh (1997)in Tomales Bay, another shallow estuary in which sulfatereduction is important. The resultant net sulfate reductionmay increase total alkalinity, and consequently, the estua-rine waters can present a higher retention of DIC, indetriment of CO2 degassing.

In the beginning of the wet season, supersaturationincreased, presumably due to flushing of material accumu-lated in the reservoir during the dry season. This input oforganic material was characterized by high concentrationsof particulate organic (∼2.5 mmol C l−1) and dissolvedinorganic (∼4.9 mmol C l−1) carbon. The excess CO2 iscaused mainly by mineralization of fluvial material ofanthropogenic origin. Most of the remineralization occursin the upper turbid zones and is related with the sewage andindustrial effluents of high organic content. Abril et al.(2002) observed in European estuaries this pattern ofheterotrophy in the upper estuary sustained by continental/anthropogenic sources and a higher contribution of autoch-thonous POC in the marine regions of the estuaries. Theintensity of respiration and CO2 fluxes to the atmospherewere closely related with this allochtonous inputs. Super-saturation at this moment was not only the result ofdegradation of allochtonous particulate and dissolvedorganic material but also the advective flux of dissolvedinorganic carbon. The transport of DIC by rivers canrepresent as much as 50% of the estuarine CO2 emission tothe atmosphere, while nitrification and heterotrophic activ-ity can account for the other half (Abril et al. 2000). InJune, July, and September, under higher freshwater inputvia the dam, the fluvial input of DIC could even beequivalent to or more important than local heterotrophic

Fig. 4 Degree of saturation inCO2 (%) at three stations alongthe estuary, measured at dawn.Horizontal line indicates 100%saturation

116 Estuaries and Coasts (2009) 32:111–122

activity to establish a high supersaturation in the upperestuary. As a consequence, these results indicate thepreponderance of heterotrophy not only in the estuarineregion but also in the Piauí and Piauitinga freshwatersources and the reservoirs of the system of dams (Souza1999).

Given the daily changes of pCO2, the whole estuary actas a net source of CO2 to the atmosphere (Table 1). Theaverage rates of CO2 loss to the atmosphere found in thisstudy (6–21 mol m−2 year−1) were lower than thoseobserved for the Satilla River (15–200 mol m−2 year−1;Cai and Wang 1998), Scheldt (∼440 mol m−2 year−1;Frankignoulle et al. 1996) and Loire estuaries (∼100 molm−2 year−1; Abril et al. 2004). However, Cai and Wang(1998) applied a higher exchange coefficient (KCO2=3 mday−1) to the whole estuary, whereas in this study, theexchange coefficient was chosen according to the measuredwind velocity, resulting in KCO2 between 0.2–0.8 m day−1

(Carmouze 1994). Wind velocities were lower in theestuarine areas with higher supersaturation, due to thepresence of a high and dense mangrove forest surroundingthe narrow channel. The higher KCO2 was only used in thisarea in May, when wind direction coincided with the mainchannel axis. The other authors measured directly the CO2

fluxes with floating chambers, and their results wereindependent of wind velocity and piston velocity.

Net Ecosystem Metabolism

We observed a general trend toward net heterotrophy onboth monthly (from 24-h measurements; Fig. 5) and annualtime scales (monthly free-water measurements; Table 2).Simultaneous decreases (station 3) and increases (station 6)in the degree of heterotrophy followed increases infreshwater runoff between January to March (Fig. 5). Thisbehavior indicates the transport of the organic matteraccumulated in the reservoirs during the dry season.Mukhopadhyay et al. (2006) reported the same event atthe River Hooghly estuary, India. After this transport,strong CO2 consumption was measured at stations 6 and 7,where net primary production/respiration alternated duringthe rest of the year. The magnitude of CO2 consumptioncontrasted with that reported by Souza and Couto (1999) in

a preliminary sampling at the same stations in this estuary(−0.7 to +0.6 mmol CO2 m−2 day−1, November 1994).Compared to the seasonal changes between autotrophy/heterotrophy observed in temperate embayments as Tom-ales Bay (Smith and Hollibaugh 1997), South SanFrancisco Bay (Caffrey et al. 1998), and the tropical coastallagoon of Saquarema (Carmouze 1994), the Piauí Riverestuary was characterized by spatial patchiness and pulsesof net heterotrophy as a response to freshwater discharge,anthropogenic inputs, and the fluxes of organic matter andnutrients. It is important to observe that high net autotro-phic rates occurred during periods of CO2 supersaturation(e.g., May). This suggests sharp changes in the prevailingmetabolic processes, as observed previously in this (Souzaand Couto 1999) and another tropical systems (Carmouze1994).

The assessment of NEM in an annual scale by theintegration of monthly changes of average DIC concen-trations assumes some stability of the atmospheric exchangeand minimizes the effect of short-term changes in metabo-lism and advective processes. Without a correction forexchange through the atmosphere/water interface, theseresults were very different from the monthly rates, suggest-ing an estuary with net primary production (Table 2; NEM=4.5×10−7 mol year−1). Correcting for atmospheric exchangeproduced net heterotrophic rates almost equal to CO2 lossesto atmosphere (Table 2; NEM=−3.9×10−8 mol year−1).These results were a magnitude order higher than theobtained in the previous mass balance and stoichiometriccalculations using the Redfield C:P ratio (Souza et al. 2000;Table 3; −6.9×107 mol year−1). The use of an average C:Pratio of particulate suspended matter give a value closer(−2.9×108 mol C year−1) to the NEM estimate.

Net Pelagic Metabolism

The net pelagic metabolism was not as high as totalecosystem metabolic rates (Fig. 6), suggesting that therewas equilibrium between autotrophic/heterotrophic process-es, in agreement with previous results of Souza and Couto(1999) in November 1994. The event of net autotrophyobserved in May 18 seems to be the result of the largefluvial inputs in the beginning of the rainy season (March).

Table 1 Rates of CO2 exchange across the atmosphere/water interface

Station Distance from the mouth (km) Section area (km2) Mean S Mean CO2 flux (mol m−2 year−1) Total CO2 flux (mol year−1)

7 0–5.3 15.6 28.5 −5.9 −0.9×108

6 5.3–17.3 11.6 24.9 −17.6 −2.0×108

3 17.3–35 6.4 10.2 −21.4 −1.4×108

Overall 33.4 21.2 −15.0 −4.3×108

Positive and negative values correspond to dissolution and loss to atmosphere, respectively

Estuaries and Coasts (2009) 32:111–122 117117

This nutrient supply may be from the degradation oforganic particles in suspension or in the sediments at thedam during the dry season. The algebraic sum of positive(net heterotrophy) and negative (net autotrophy) rates isalmost zero (Table 3), resulting in only slight netautotrophy in an annual scale (−0.3×108 mol CO2 year

−1).Although the small number of measurements in the

pelagic ecosystem does not permit an assessment of aseasonal trend, the overall signal of the pelagic rates wasthe same of total ecosystem rates. The differences observedmay be related to changes in pelagic metabolism such asresource limitation of bacterial communities by organiccarbon in the upper estuary and nutrients in the outerestuary (Smith and Kemp 2003) and the seasonal/spatialvariation of the picoplankton production/respiration (Smithand Kemp 2001).

Estimation of the Role of Sediments and Mangroves

The individual contribution of the subtidal, tidal mudflats, andmangrove sediment to net ecosystem metabolism are un-known. Nevertheless, mangrove and tidal mudflats areexpected to present higher metabolic rates, since they are

subject to more intense light incidence and high oxygentension. Inferences on these fluxes in the estuary were madeapplying the Eqs. 1–3.

Resolving the Eq. 1 with the rates obtained in the formersections resulted in:

Mangroveþ 1:5 � 109 þ 2:1 � 108

¼ 0:3 � 108 þ 1:9 � 109 þ 4:3 � 108

¼ þ 6:5 � 108 mol DIC year�1:

This calculation shows that intertidal sediment inmangroves and mudflats was the site of most heterotrophicactivity in the estuary. The change of anoxic to oxicconditions during tidal exposure and the presence of oxic/anoxic microzones, allowing for the development ofheterotrophic processes coupled to denitrification/nitrifica-tion, can lead to higher metabolic rates. It is important tonote that wherever heterotrophy prevails, a variable fractionof the organic matter respired may be of allochtonous origin(Bouillon et al. 2004, 2007), including from the effluents ofEstância City. Atmospheric carbon dioxide assimilated bymangrove trees must also be included in this value. Themangrove contribution calculated only by the difference ofNEM and NPM also resulted in net heterotrophy (−4.2×108 mol Corg year

−1).The same procedure was applied to DIN andDIP according

to Eqs. 2 and 3, but using the mean C:N and C:P ratio of thesystem (24:1 and 449:1, respectively), to link the nutrientassimilation by pelagic production. This resulted in:

Mangroveþ 4:8 � 106 ¼ 1:3� 106 þ 1:1 � 106 þ 5:7 � 106

¼ þ3:8 � 106 mol DIN year�1

and

Mangroveþ 4:5 � 105 ¼ 6:7 � 104 þ 3:4 � 105 þ 1:8 � 105

¼þ 1:6� 105 mol DIP year�1:

These results indicate that the mangrove ecosystem is asource of DIP to the estuary equivalent to anthropogenicinputs by the Piauitinga River. This rate was twice to thetotal nonconservative flux obtained in the mass balance.The mangroves are also the more important source of DIN

Table 2 Rates of net ecosystem metabolism at three stations and along the entire estuary (total NEM) obtained by integration of DICconcentration over the year

Station NEM (mol m−2 year−1) NEMcorrected (mol m−2 year−1) Total NEM (mol year−1) Total NEMcorrected (mol year−1)

7 −0.3 5.8 −0.5×107 0.9×108

6 0.1 17.2 0.1×107 2.0×108

3 −1.0 15.6 −4.1×107 1.0×108

Overall −0.4 12.9 −4.5×107 3.9×108

Were presented the values with and without the correction for the exchange across the atmosphere/water interface. Positive and negative valuescorrespond to CO2 production (net heterotrophy) and consumption (net autotrophy), respectively

Fig. 5 Rates of net ecosystem metabolism at three stations alongthe estuary measured by changes of free-water concentration over24-h periods. Values corrected for the exchange across atmosphere/waterinterface. Positive and negative values correspond to CO2 production (netheterotrophy) and consume (net autotrophy), respectively

118 Estuaries and Coasts (2009) 32:111–122

to the estuary. This rate was slightly higher than the oneobtained in the mass balance. Though the first mass balanceexercise resulted in low rates of net nitrogen fixation(Souza 1999), more accurate calculations reveal a slight netdenitrifying system (Souza et al. 2000; Table 4). Thisdemonstrates that in this system, the model exhibits a strongsensitivity to both N:P stoichiometry and DIN concentra-tions. This result does not mean that we should disregard thepotential importance of nitrogen fixation as a source ofnitrogen potentially exported. Blooms of N2-fixing organ-isms such as Lyngbya cf. confervoides and Enteromorphaspp. were observed during this and previous studies (Souzaand Couto 1999). Remineralization of this autochtonous andallochtonous organic nitrogen produces the inorganic nitro-gen export.

Several works have already described the role ofmangroves in the export of dissolved nutrients, either ininorganic or organic forms (Wong 1984). Boto andRobertson (1990) reported that nitrogen fixation in sedi-ment, algal mats, aerial roots, and trunks of a mangrove inAustralia was almost equal the export of dissolvedinorganic nitrogen. Woitchik et al. (1997) also found thatnitrogen fixation in an African coastal lagoon represents asignificant (13–21%), but not the primary source ofnitrogen to the mangrove sediment (the litter fall). Nitrogen

fixation and a positive sediment balance were consideredessential conditions to nutrient outwelling from tropicalmangroves (Dittmar and Lara 2001).

It is important to observe that the LOICZ guidelinesrecommend the use of the dissolved organic fractions of Nand P as well as DIN and DIP. The budgets using only theinorganic forms (as the results presented in this study) canresult in unaccounted nutrient inputs due to the remineral-ization of more labile organic compounds, especially in thepresence of high N fixation rates and inputs of untreatedwaste loads.

Sources and Sinks of Organic Carbon in the Estuary

To compare the magnitude of fluvial (9.2×108 mol POCyear−1) and anthropogenic (4.7×108 mol POC year−1)inputs of organic carbon and decomposition of organiccarbon in the mangroves, we scaled up the DIP productionin the mangrove by the average C:P ratio of mangrove(∼1,000:1; Lanza et al. 1997). This produced an estimate ofthe total mass of respired organic carbon of about −1.6×108 mol year−1. This rate is certainly underestimated, sinceDIP is also removed in the mangrove by biotic and abioticprocesses. However, this rate just exceeds an estimate ofmangrove contribution with POC, made according to Wafaret al. (1997) and the mangrove area of Piauí River (7.2 km2;1.1×108 mol POC year−1). Estimated in the same way, thefluxes of DOC from litterfall are about twice this value.Two other approaches to estimating the organic matterdecomposition in the mangrove were the use of Eq. 1 orsimply subtraction of the NPM from NEM. Both proce-dures resulted in higher rates than the former one (−6.5 and

Fig. 6 Rates of net pelagic metabolism obtained by the change ofDIC concentration in water incubations over 24-h periods. Positiveand negative values correspond to CO2 production (net heterotrophy)and consume (net autotrophy), respectively

Table 3 Summary of the mass balance calculations, including advective fluxes used in equations and nonconservative fluxes (Souza et al. 2000)

Δ DIP Δ DIN Δ DIC P−RRedfield P−RPOM N fixation−denitrification

mol year−1 1.8×105 2.2×106 6.3×108 −69×106 −289×106 −2.1×106

mmol m−2 year−1 4.2 50 4.6×103 −1.6×103 −6.6×103 −48

Δ DIP, DIN, and DIC are net nonconservative fluxes of inorganic remineralization products; P−RRedfield and RPOM are the net primary production/respiration rates calculated according to Redfield and average particulate organic matter C:P ratio; N fixation−denitrification is the balancebetween nitrogen fixation and denitrification

Table 4 Rates of net pelagic metabolism at three stations along theestuary obtained by integration of the incubation results over the year

Station NPM (mol m−2 year−1) Total NPM (mol year−1)

7 −0.7 −0.1×108

6 −2.3 −0.3×108

3 2.2 0.1×108

Overall −0.3 −0.3×108

Positive and negative values correspond to CO2 production (netheterotrophy) and consumption (net autotrophy), respectively

Estuaries and Coasts (2009) 32:111–122 119119

−4.2×108 mol C year−1, respectively). The first valueexceeded the other estimates of NEM, while the lattervalues correspond to about 95% of NEM.

These estimates suggest that mangrove productioncannot sustain the net heterotrophy observed at themangrove and estuary (Table 5). This sounds as an obviousassertion when the main source of phosphorus is consid-ered, but carbon in mangrove trees can be mainly fixeddirectly from atmosphere (outside the system boundaries).Accordingly, it is important to consider anthropogeniccontributions through the dam, either directly as dissolvedorganic carbon (unpublished data) or as particulate organicmatter of low C:N ratio and less refractory. One of theeffects of the construction of dams is the increase of organicmatter decomposition rates (producing some dissolvedspecies) and assimilation of the resulting dissolved inor-ganic nutrients as more labile particulate matter in thereservoirs (Hopkinson and Vallino 1995). A reduction ofthe C:N and C:P ratio was observed in samplings in RiverPiauitinga and its reservoirs (Souza 1999). Even in theabsence of the results of DOC fraction in the fluvial inputs,they may be enhancing the mangrove bacterial processes.Alongi (1988) reported a high correlation between C and Nenrichment and bacterial growth. Tam (1998) observedexperimentally that wastewater inputs promote bacterialgrowth and activity. The former author suggested that thecoupling of high bacterial biomass and productivity rateswith low densities of macroinfaunal organisms, as observedin Piauí River, implies that bacterial production andremineralization can be a sink for carbon in tropicalmangrove estuaries.

There was a tendency to consider dissolved organicfraction as the primary form in which carbon fixed in themangrove is exported (Twilley 1985; Bano et al. 1997).Dissolved organic carbon is considered less refractory todecomposition and more readily used by heterotrophicbacteria than organic particles. It was reported that thisfraction could sustain much of the heterotrophy occurringin mangroves (Bano et al. 1997). However, Dittmar et al.(2001) observed that dissolved organic carbon behavedconservatively along a Brazilian mangrove estuary, sug-gesting a refractory chemical nature.

Despite the biological availability of dissolved inorganiccarbon, there are also some clues that a significant parcel ofthe bacterial production in tropical mangroves is originatingfrom bacteria attached to particulate organic matter (Bano etal. 1997). Crump et al. (1998) reported that particle-attached bacteria were responsible for as much as 90% ofbacterial production and can dominate particulate organicmaterial degradation and transfer to detrital food web in atemperate turbid estuary (Columbia River). A further studyrevealed that most of the bacterial activity in this estuaryoccurs in small slowly settling particles (Crump and Baross2000). Particle-attached microbial activity (reduced C:Nratio) may be the main pathway of organic carbon transferto higher trophic levels. In fact, Anesio et al. (2003)showed that respiration of bacteria attached to particle isnot only significant but that the coupling with free bacteriaby assimilation of dissolved products of its enzyme activityis important to organic matter remineralization.

The coupling between water column and mangrovesediment can also be greatly enhanced by the presence ofbenthic filter feeding organisms. In the mangrove of PiauíRiver estuary, there are extensive banks of Mytellaguyanensis and Mytella charruana, which were collectedand commercialized (E.C. Couto, personal communica-tion). The intensive extraction of these bivalves and ofUcides cordatus (true mangrove crab) may constitute asomewhat important and unmeasured loss of carbon.

Implications for Management

The domestic and industrial effluents of Estância undoubtedlyshould receive treatment, and the presence of the damschanges the nature and the effects of these inputs to theestuary. The organic load is modified to a less refractory formand the organic particles are enriched during their permanencein the reservoirs, being more suitable to degradation byparticle-attached bacteria. These changes support the estuarinetrend toward heterotrophy, and probably the estuary function-ing would be very different if these pollutants were flowingcontinuously. The decommissioning of the hydroelectricreservoir should be considered, since it only serves to a textileindustry and generate less than 1 kWh.

Table 5 Comparison between fluvial and mangrove inputs and estimates of net decomposition rates

Fluvial inputs P−Rmangrove Litter fluxes

POC POC + DOC POC DOC

108 mol year−1 9.2 −4.2 or –6.5 1.1 2.2mol m2 year−1 (estuary) 27 −13 or −20 3.2 6.6mol m2 year−1 (mangrove) 128 58 44 92

Litter fluxes estimated from Wafar et al. (1997) average results and mangrove area. P−Rmangrove calculated according NEM−NPM and Eq. 1,respectively

120 Estuaries and Coasts (2009) 32:111–122

Conclusions

This mesotidal estuary presented a net heterotrophicmetabolism in an annual scale, acting as a source of DINand DIP to coastal waters, while most of the produced DICwas lost to atmosphere (13 mol CO2 m

−2 year−1). The watercolumn was almost balanced between auto- and heterotro-phy and the mangrove forests and tidal mudflats wereresponsible for most of the NEM. The autochtonousproduction and mangrove litter cannot sustain the estuarineand mangrove heterotrophy and the anthropogenic inputscontribute with more than 50% of fluvial inputs ofparticulate organic matter.

The results suggest that fluvial and anthropogenicorganic matter is the main source for the sustenance ofmangrove ecosystem metabolism and the enhancement ofbenthic microbial processes. This organic matter, ratherthan mangrove autochthonous production, is responsible forthe net heterotrophy and export of dissolved inorganicnutrients. Thus, terrestrial and anthropogenic organiccarbon may be supporting a greater part of secondaryproduction than considered up till now.

Acknowledgments We thank Dr. J. P. H. Alves for the laboratorysupport in the Departamento de Química/UFSE. We acknowledge Dr.E. C. G. Couto (Departamento de Ciências Biológicas/UESC) for theparticipation in field trips and for the important comments aboutbiological features; Dr. S.V. Smith (CICESE) made several importantcontributions to the water and nutrient budgets that resulted in the dataexposed in Table 3; people of the LOICZ IPO and the InstitutoArgentino de Oceanografia, particularly Dr. Chris Crossland and Dr.Gerardo Perillo, for the opportunity to discuss these data and budgetsduring the South America Biogeochemical Budgeting Workshop heldin Bahia Blanca, Argentina, in 1999. Dr. A. Raw (UESC) providedvaluable critical and language review. Dr. C. A. Simenstad (Universityof Washington) reviewed a former version of the manuscript, resultingin several improvements. A. M. Fernandes, M. V. Carvalho, P. S.Lima, C. Assis, D. Assis, and E. Santos helped with field andlaboratory assistance. Several field surveys were done in vessel ofBrazilian Navy, for what we specially thank the Port Authority Cap.R. V. Dutra and Corporal F. Souza at CPSE. CNPq provided supportfor the work described in this paper in the form of a DCR researchgrant proc. no. 300.738/1995-1 (first author) and PQ grant proc. no.300.772/2004-1 (last author).

References

Abril, G., H. Etcheber, A.V. Borges, and M. Frankignoulle. 2000.Excess atmospheric carbon dioxide transported by rivers into theScheldt estuary. Earth and Planetary Sciences 330: 761–768.

Abril, G., M. Nogueira, H. Etcheber, G. Cabeçadas, E. Lemaire, andM.J. Brogueira. 2002. Behaviour of organic carbon in ninecontrasting European estuaries. Estuarine, Coastal and ShelfScience 54: 241–262. doi:10.1006/ecss.2001.0844.

Abril, G., M.-V. Commarieu, D. Maro, M. Fontagne, F. Guérin, andH. Etcheber. 2004. A massive dissolved inorganic carbon releaseat spring tide in a highly turbid estuary. Geophysical ResearchLetters 31: L09316. doi:10.1029/2004GL019714.

Alongi, D.M. 1988. Bacterial productivity and microbial biomass intropical mangrove sediments. Microbial Ecology 15: 59–79.doi:10.1007/BF02012952.

Anesio, A.M., P.C. Abreu, and B.A. Biddanda. 2003. The role of freeand attached microorganisms in the decomposition of estuarinemacrophyte detritus. Estuarine, Coastal and Shelf Science 56:197–201. doi:10.1016/S0272-7714(02)00152-X.

Bano, N., M. Nisa, N. Khan, M. Saleem, P.J. Harrison, S.I. Ahmed,and F. Azam. 1997. Significance of bacteria in the flux of organicmatter in the tidal creeks of the mangrove ecosystem of the IndusRiver delta, Pakistan. Marine Ecology Progress Series 157: 1–12.doi:10.3354/meps157001.

Borges, A.V., L.-S. Schiettecatte, G. Abril, B. Delille, and F. Gazeau.2006. Carbon dioxide in European coastal waters. Estuarine, Coast-al and Shelf Science 70: 375–387. doi:10.1016/j.ecss.2006. 05.046.

Boto, K.G., and A.I. Robertson. 1990. The relationship betweennitrogen fixation and tidal exports of nitrogen in a tropicalmangrove system. Estuarine, Coastal and Shelf Science 31: 531–540. doi:10.1016/0272–7714(90)90011-F.

Bouillon, S., M. Frankignoulle, F. Dehairs, B. Velimirov, A. Eiler, G.Abril, H. Etcheber, and A.V. Borges. 2003. Inorganic and organiccarbon biogeochemistry in the Gautami Godavari estuary(Andhra Pradesh, India) during pre-monsoon: The local impactof extensive mangrove forests. Global Geochemical Cycles 17(4): 1114. doi:10.1029/2002GB002026.

Bouillon, S., T. Moens, and F. Dehairs. 2004. Carbon sourcessupporting benthic mineralization in mangrove and adjacentseagrass sediments (Gazi Bay, Kenya). Biogeosciences 1: 71–78.

Bouillon, S., J.J. Middleburg, F. Dehairs, A.V. Borges, G. Abril, M.R.Flindt, S. Ulomi, and E. Kristensen. 2007. Importance ofintertidal sediment processes and porewater exchange on thewater column biogeochemistry in a pristine mangrove creek (RasDege, Tanzania). Biogeosciences 4: 311–322.

Caffrey, J.M., J.E. Cloern, and C. Grenz. 1998. Changes in productionand respiration during a spring phytoplankton bloom in SanFrancisco Bay, California, USA: implications for net ecosystemmetabolism. Marine Ecology Progress Series 172: 1–12.doi:10.3354/meps172001.

Cai, W.J., and Y. Wang. 1998. The chemistry, fluxes, and sources ofcarbon dioxide in the estuarine waters of the Satilla and AltamahaRivers, Georgia. Limnology and Oceanography 43(4): 657–668.

Cai, W.J., L.R. Pomeroy, M.A. Moran, and Y. Wang. 1999. Oxygenand carbon dioxide mass balance for the estuarine–intertidalmarsh complex of five rivers in the southeastern U.S. Limnologyand Oceanography 44(3): 639–649.

Carmouze, J.P. 1994. O metabolismo dos ecossistemas aquáticos. InFundamentos teóricos, métodos de estudo e análises químicas,ed. Edgard Blücher, 254. São Paulo: Fundação de Amparo àPesquisa do Estado de São Paulo.

Crump, B.C., and J.A. Baross. 2000. Characterization of the bacterially-active particle fraction in the Columbia River estuary. MarineEcology Progress Series 206: 13–22. doi:10.3354/meps206013.

Crump, B.C., J.A. Baross, and C.A. Simenstad. 1998. Dominance ofparticle-attached bacteria in the Columbia River estuary, USA.Aquatic Microbial Ecology 14(1): 7–18. doi:10.3354/ame014007.

Dittmar, T., and R.J. Lara. 2001. Driving forces behind nutrient and organicmatter dynamics in a mangrove tidal creek in North Brazil. Estuarine,Coastal and Shelf Science 52: 249–259. doi:10.1006/ecss.2000.0743.

Dittmar, T., R.J. Lara, and G. Kattner. 2001. River or mangrove? Tracingmajor organic matter sources in tropical Brazilian coastal waters.Marine Chemistry 73: 253–271. doi:10.1016/S0304-4203(00)00110-9.

Drever, J.I. 1982. The geochemistry of natural waters. Surface andgroundwater environments. Upper Sadle River, New Jersey:Prentice-Hall.

Estuaries and Coasts (2009) 32:111–122 121121

Frankignoulle, M., I. Bourge, and R. Wollast. 1996. Atmospheric CO2

fluxes in a highly polluted estuary (the Scheldt). Limnology andOceanography 41: 365–369.

Furukawa, K., E. Wolanski, and H. Mueller. 1997. Currents andsediment transport in mangrove forests. Estuarine, Coastal andShelf Science 44: 301–310. doi:10.1006/ecss.1996.0120.

Gordon, D.C. Jr., P.R. Boudreau, K.H. Mann, J.-E. Ong, W.L. Silvert,S.V. Smith, G. Wattayakorn, F. Wulff, and T. Yanagi. 1996.LOICZ Biogeochemical Modelling Guidelines. LOICZ Reports &Studies No. 5., 2nd Edition. Texel, The Netherlands: LOICZ IPO,vi + 96 pp.

Grasshoff, K., M. Ehrardt, and K. Kremling. 1983. Methods ofseawater analysis. Weinhein: Verlag Chemie, 419 pp.

Hall, C.A.S., and R. Moll. 1975. Methods of assessing aquaticprimary productivity. In Primary productivity of the Biophere,eds. H. Lieth, , and R. H. Whittaker, 19–53. Berlin: Springer.

Hopkinson, C.S., and J.J. Vallino. 1995. The relationship amongman’s activities in watersheds and estuaries: a model of runoffeffects on patterns of estuarine community metabolism. Estuaries18(4): 598–621. doi:10.2307/1352380.

Kempe, S. 1982. Long term records of CO2 pressure fluctuations infresh waters. In Transport of carbon and minerals in majorrivers. Part 1, ed. E.T. Degens, 91–332. Hamburg: UniversitatHamburg.

Lanza, G., F.J. Flores-Verdugo, and F. Wulff. 1997. Teacapan-AguaBrava-Marismas Nacionales, Sinaloa and Nayarit. In Comparisonof carbon, nitrogen and phosphorus fluxes in Mexican coastallagoons. LOICZ Reports & Studies No. 10, eds. S.V. Smith, S.Ibarra-Orlando, P.R. Boudreau and V. Camacho-Ibar, 38–42.Texel, The Netherlands: LOICZ IPO, ii + 84 pp.

Lee, S.Y. 1995. Mangrove outwelling: a review. In Asia-PacificSymposium on mangrove ecosystems. Hydrobiologia 295, eds. Y.S. Wong and N.F.Y. Tam, 203–212. The Netherlands: Springer.

Mukhopadhyay, S.K., H. Biswas, T.K. De, B.K. Sen, S. Sen, and T.K.Jana. 2002. Impact of Sundarban mangrove biosphere on thecarbon dioxide and methane mixing ratios at the NE Coast ofBay of Bengal, India. Atmospheric Environment 36: 629–638.doi:10.1016/S1352-2310(01)00521-0.

Mukhopadhyay, S.K., H. Biswas, T.K. Dea, and T.K. Jana. 2006. Fluxesof nutrients from the tropical River Hooghly at the land–oceanboundary of Sundarbans, NECoast of Bay of Bengal, India. Journalof Marine Systems 62: 9–21. doi:10.1016/j.jmarsys.2006.03.004.

Nixon, S.W., and M.E.Q. Pilson. 1984. Estuarine total systemmetabolism and organic exchange calculated from nutrient ratios:an example from Narragansett Bay. In The estuary as a filter, ed.V. S. Kennedy, , 261–290. Orlando: Academic.

Odum, E.P., and E.J. Heald. 1975. The detritus bases food web of anestuarine mangrove community. In Estuarine research, ed. L. E.Cronin, , 265–286. New York: Academic.

Smith, S.V., and M.J. Atkinson. 1994. Mass balance of nutrient fluxesin coastal lagoons. In: Coastal lagoon processes, ed. B. Kjerfve,133–155. Amsterdam: Elsevier.

Smith, S.V., and J.T. Hollibaugh. 1997. Annual cycle and interannualvariability of ecosystem metabolism in a temperate climateembayment. Ecological Monographs 67(4): 509–533.

Smith, E.M., and W.M. Kemp. 2001. Size structure and theproduction/respiration balance in a coastal plankton community.Limnology and Oceanography 46(3): 473–485.

Smith, E.M., and W.M. Kemp. 2003. Planktonic and bacterialrespiration along an estuarine gradient: responses to carbon andnutrient enrichment. Aquatic Microbial Ecology 30(3): 251–261.doi:10.3354/ame030251.

Souza, M.F.L. 1999. Metabolismo e balanço de massa do estuário doRio Piauí, Sergipe. Ph.D. thesis, Universidade Federal Flumi-nense, Niterói, Brazil.

Souza, M.F.L., and E.C.G. Couto. 1999. Short-term changes andlongitudinal distribution of carbon metabolism in the Piauí Riverestuary (Sergipe, Brazil). Revista Brasileira de Biologia 59(2):24–27. doi:10.1590/S0034-71081999000200003.

Souza, M.F.L., V.R. Gomes, S.S. Freitas, R.C.B. Andrade, B.A.Knoppers, and S.V. Smith. 2000. Piaui River Estuary, SergipeState. In Estuarine systems of the South American region: carbon,nitrogen and phosphorus fluxes. LOICZ Reports & Studies No. 15,eds. S.V. Smith, V. Dupra, J.I. Marshall Crossland, and C.J.Crossland, 10–17. Texel, The Netherlands: LOICZ, ii + 87 p.

Strickland, J.D.H., and T.R. Parsons. 1972. A practical handbook ofseawater analysis. Bulletin of Fisheries Research Board Canadian167. The Quarterly Review of Biology 44(3): 327.

Tam, N.F.Y. 1998. Effects of wastewater discharge on microbialpopulations and enzyme activities in mangrove soils. EnvironmentalPollution 102(2-3): 233–242. doi:10.1016/S0269-7491(98)00084-0.

Teal, J.M. 1962. Energy flow in a salt marsh ecosystem of Georgia.Ecology 43: 614–624. doi:10.2307/1933451.

Twilley, R.R. 1985. The exchange of organic carbon in a basinmangrove forests in a southwest Florida estuary. Estuarine,Coastal and Shelf Science 20: 543–557. doi:10.1016/0272-7714(85)90106-4.

Wafar, S., A.G. Untawale, and M. Wafar. 1997. Litter fall and energyflux in a mangrove ecosystem. Estuarine, Coastal and ShelfScience 44: 111–124. doi:10.1006/ecss.1996.0152.

Woitchik, A.F., B. Ohowa, J.M. Kazungu, R.G. Rao, L. Goyens, andF. Dehairs. 1997. Nitrogen enrichment during decomposition ofmangrove leaf litter in an east African coastal lagoon (Kenya):relative importance of biological nitrogen fixation. Biogeochem-istry 39: 15–35. doi:10.1023/A:1005850032254.

Wong, C.H. 1984. Mangrove aquatic nutrients. In Proceedings of theWorkshop on Productivity of the Mangrove Ecosystem: Manage-ment Implications, eds. J.-E. Ong and W.-K. Gong, 60–67.

122 Estuaries and Coasts (2009) 32:111–122