Net Ecosystem Metabolism and Nonconservative ... - Springer Link

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

Net Ecosystem Metabolism and Nonconservative Fluxes of Organic Matter in a Tropical Mangrove Estuary, Piauí River (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 measured in the Piauí River estuary, NE Brazil. A mass balance of C, N, and P was used to infer its sources and sinks. Dissolved inorganic carbon (DIC) concentrations and fluxes were measured 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 the rainy season. Carbon dioxide concentrations in the entire estuary were supersaturated throughout the year and highest in the upper estuarine compartment and freshwater, particularly at the rainy season, due to washout effects of carbonaceous soils and different organic anthropogenic effluents. The estuary served as a source of DIC to the atmosphere with an estimated flux of 13 mol CO2 m−2 year−1. Input from the river was 46 mol CO2 m−2 year−1. The metabolism of the system was heterotrophic, but short periods of autotrophy occurred in the lower more marine portions of the estuary. The pelagic system was more or less balanced between auto- and M. F. L. Souza : R. C. B. Andrade : B. Knoppers Programa 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. Freitas Departamento 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, Brazil e-mail: [email protected]

heterotrophy, whereas the benthic and intertidal mangrove region was heterotrophic. Estimated annual NEM yielded a total 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. The fluvial loading of particulate organic carbon and dissolved inorganic nitrogen (DIN) was largely retained in two flow regulation and hydroelectric reservoirs, promoting a reduction of C:N and C:P particulate ratios in the estuary. The net nonconservative fluxes obtained by a mass balance approach revealed that the estuary acts as a source of DIP, DIN, and DIC, the latter one being almost equivalent to the losses to the atmosphere. Mangrove forests and tidal mudflats were responsible for most of NEM rates and are the main sites of organic decomposition to sustain net heterotrophy. The main sources for this organic matter are the fluvial and anthropogenic inputs. The mangrove areas are the highest estuarine sources 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 been considered as relevant sources of organic carbon to coastal waters (Teal 1962; Odum and Heald 1975). However, the literature revision showed that though outwelling of organic matter and nutrients was observed in mangrove ecosystems, they can also act as sinks of organic carbon, including in dissolved forms (Lee 1995). This matter is still of interest as no consistent pattern has appeared. Cai et al. (1999) has found that salt marshes wetlands are sites of intense remineralization, which reduce the importance of organic

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matter export to the estuary compared with dissolved nutrients. It should be noted that these communities differ from mangrove by lower aerial biomass storage, with lower lignin content. Mangroves are also characterized by the presence of expressive microphytobenthic and macroalgae assemblages, which include nitrifiers, denitrifiers, and Nfixing organisms. The inputs of particulate organic carbon from mangrove litter was recognized as being more important for the maintenance of the microbial food chain and nutrient regeneration in mangrove sediments than organic matter outwelling to estuary (Wafar et al. 1997). Dittmar et al. (2001) reported export of dissolved and particulate organic matter from a North Brazilian mangrove to the Caeté estuary, but the rapid removal from the water column reduced their export to coastal waters. Dissolved nutrients were also exported from this mangrove system (Dittmar and Lara 2001), but these authors considered that outwelling should only occur in mangroves of macrotidal regions, with positive sedimentation balances and nitrogen fixation. Furukawa et al. (1997) observed even a slight inwelling of organic carbon from creek to mangrove, in a mangrove swamp in Australia. Estuarine systems tend to exhibit net heterotrophy (Smith and Atkinson 1994; Borges et al. 2006), a kind of metabolic balance that requires the predominance of organic detritus over dissolved nutrient inputs, as it is found in many mangrove dominated systems (Bouillon et al. 2003; Mukhopadhyay et al. 2006). As a result, not only the estuarine waters but also the associated mangrove areas (including aerial biomass) can act as a source of carbon dioxide and methane to atmosphere in an annual scale (Mukhopadhyay et al. 2002). The assessment of this trophic status of estuaries and their role in the transport of organic matter and nutrients to coastal waters is a key to understanding their importance in a global scale. This knowledge is still scarce for tropical estuaries of many regions. This paper addresses the balance between autotrophy and heterotrophy and estimates the importance of fluvial, anthropogenic, and mangrove inputs for the maintenance of system metabolism at the mangrove dominated Piauí River estuary, NE Brazil. It also intends to test the hypothesis that the fluvial (mainly anthropogenic) organic loading sustains a net estuarine heterotrophy and that mangrove is the main site of recycling, acting as a nutrient exporter.

Material and Methods Study Area The Piauí River estuary (Fig. 1) extends over 35 km, with an area of 45 km2. It is a ria-type estuary, with mean depth of 3.8 m, with maximum reaching 25 m near the mouth

Estuaries and Coasts (2009) 32:111–122

(Souza 1999). It is characterized by an ample mesotidal flushing, with maximum tidal range of 2.5 m and the average freshwater discharge of about 5 m3 s−1, distributed irregularly through the year. The warm humid/subhumid littoral receives a pluvial input of 1,400 mm, in contrast with 750 mm in the Mediterranean dry climate found in the inland areas of the drainage basin. The estuary is well mixed during most of the year, with a mean salinity of 21. There is a slight stratification in the outer portion during the rainy 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 industrial effluents (food processing and textile). Downstream of this dam, the residues are retained by another dam reservoir during most of the dry season, when freshwater discharge is reduced to less than 0.5 m3 s−1. This shallow stagnant polluted water becomes anoxic, and a measurable amount of particulate organic carbon and dissolved inorganic nitrogen (DIN) loading is retained in this reservoir, probably by respiration and denitrification and/or sedimentation (Souza 1999). Mangrove logging is also an important and growing impact. Sampling Strategy Free water samples were taken ten times between January and December 1996, at stations located in the inner, mid-, and outer estuary (st. 3, 6, and 7; Fig. 1). These samples were collected just before dawn, dusk, and after variable time intervals between to assess the net ecosystem metabolism (NEM). Incubations using biological oxygen demand (BOD) bottles were conducted at six times within this period to estimate the daily net pelagic metabolism (NPM). Water sampling was also carried from December 1995 to December 1997, comprising eight surveys along the estuary from fresh to marine end members. These samples were used to construct the mass balance and estimate the net ecosystem metabolism by monthly dissolved inorganic carbon (DIC) changes. In the estuarine stations, water samples were collected at 0.5 and 1.0 m depth above the bottom. Temperature was measured in the field with a Hg thermometer. Subsamples were reserved to the determination of conductivity with a bench digital meter. Aliquots were collected separately in syringes for alkalinity analysis. All samples were stored in polyethylene flasks previously washed with HCl 1:1, distilled deionized water, and thoroughly rinsed with the sample water. The flasks were kept on ice in the dark for about 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


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Fig. 1 The Piauí River estuary and the location of sampling stations. Hatched areas represent mangrove forests. Station 1 sampled in different locations according salinity

meter with ±0.001 resolution and a combined glass electrode. The samples were filtered through Whatmann GF/F glass fiber filters of 47 and 25 mm diameter, reserved for further analysis of particulate material. The filtrate was frozen until dissolved inorganic nutrients determination.

and silicate) were analyzed according to Grasshoff et al. (1983). Particulates were retained on GF/F filters and analyzed separately for total suspended solids by gravimetry, particulate organic carbon (POC) by wet chemical oxidation (Strickland and Parsons 1972), and nitrogen and phosphorus as in Grasshoff et al. (1983).

Chemical Analysis Total alkalinity was determined just after pH measurement, by potentiometric titration with a high precision bench pH meter (Digimed® DM-21, ±0.001 pH resolution), with 0.0100 M HCl. The equivalence point was achieved by a modified Gran’s function (Carmouze 1994). The influence of humic and fulvic acids was minimized carrying the Gran’s titration to a pH of about 3.2 (Cai and Wang 1998). Dissolved inorganic carbon content was calculated with total alkalinity, pH, and salinity (S). The complete procedure is detailed by Carmouze (1994). Dissolved inorganic nutrients (ammonia, nitrite, nitrate, phosphate,

Net Estuarine Metabolism, Mass Balance, and Stoichiometric Calculations The net ecosystem metabolism or production (NEM = gross primary production−respiration) was evaluated using three approaches: (a) the free-water method using the daily DIC changes integrated to an annual scale (Hall and Moll 1975), (b) the free-water method using the monthly DIC changes integrated to an annual scale (Carmouze 1994), and (c) mass balance approach for dissolved inorganic C, N, and P and stoichiometric linkage (Gordon et al. 1996). The assessment of net ecosystem metabolism is considered as

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the sum of all autotrophic and heterotrophic processes occurring in the water column and sediment (Nixon and Pilson 1984; Carmouze 1994; Smith and Hollibaugh 1997), including the intertidal areas during flooding. The application of free-water technique to estuarine waters has been much criticized due to the dynamic nature of water advection and gas diffusion through the atmosphere–water interface along the estuarine mixing zone (Hall and Moll 1975; Nixon and Pilson 1984). In the present study, we used the variation of carbon dioxide instead of dissolved oxygen concentration, a gas with an exchange coefficient much lower than dissolved oxygen to measure the concentration changes generated by the NEM. DIC measurements from the 24-h estuarine surveys at stations 3, 6, and 7 were used to calculate NEM. Monthly changes of average daily DIC concentrations were used to integrate these rates along the year. The exchange of CO2 with the atmosphere was estimated using calculations based in Fick’s law and the stagnant layer model (Carmouze 1994). The calculated exchange coefficients ranged from 0.2–0.8 m day−1, according with wind velocity measured with a digital anemometer near the sampling site. In addition to total NEM, the NPM was also measured during six surveys, through incubations of estuarine water in 300-ml BOD flasks, at time intervals of 4 to 6 h, along a diurnal cycle. The DIC data from 24 h and the eight surveys along the estuary were combined to estimate the monthly changes of mean DIC concentrations within the three estuarine zones. These results were upscaled to produce an annual NEM rate. We also used the results of a simple approach to a mass balance of dissolved inorganic nutrients, made following the Land–Ocean Interactions in the Coastal Zone (LOICZ)/ International Geosphere–Biosphere Programme guidelines (Gordon et al. 1996). A stoichiometric linkage was applied using the annual average of the C:N:P composition of particulate organic matter. This composition was determined in industrial effluents, river, and estuarine particulate matter. The mangrove stoichiometry used here was found in the literature (Lanza et al. 1997). Using these calculations, we inferred the rates of biogeochemical processes, as net nonconservative fluxes, nitrogen fixation/denitrification, and primary production/respiration rates (Gordon et al. 1996). The detailed procedures and results of the one- and three-box mass balance used in this paper were described in Souza et al. (2000). Estimation of the Roles of Sediments and Mangroves The results obtained were used to infer some of the unknown fluxes inside the estuary according to a procedure modified from Cai and Wang (1998). First, we assessed the role of the mangrove in the estuarine balance of CO2,


decomposing the nonconservative fluxes occurring in the estuarine water column (pelagic) and sediment and mangrove surfaces (mangrove). These terms were included in the balance, placed in the proper side of equation according with its sign (inputs/outputs at the left and right side, respectively). The contribution of mangrove (in fact mangrove plus tidal flats and subtidal sediment) to the dissolved nutrient fluxes was estimated according to the following equations: Dissolved inorganic carbon: Mangrove þ VRiver DICRiver þ VX DICX ¼ Pr od:pel:

ð1Þ

þ VR DICR þ DICatm

Vriver ×DICriver VX ×DICX VR ×DICR DICatm Prod.pel.

fluvial inputs mixing with coastal waters residual flux exchange with atmosphere pelagic net production

The same procedure was applied to the DIN and dissolved inorganic phosphorus (DIP). In these cases, the nutrient assimilation by pelagic production was estimated by stoichiometric linkage using the mean C:N and C:P ratio of the system. Dissolved inorganic nitrogen and phosphorus: Mangrove þ VRiver DINRiver ¼ Prod:pel: þ VR DINR þ VX DINX

ð2Þ Mangrove þ VRiver DIPRiver ¼ Prod:pel: þ VR DIPR þ VX DIPX :

ð3Þ Legend as DIC except Prod.pel. calculated as above.

Results and Discussion pH Along the Estuary The autotrophic and heterotrophic processes promote a pH increase/decrease, respectively. Other factors related to estuarine pH are the chemical nature and discharge of freshwater, degree of seawater mixing, the presence of humic compounds, and pollution. In the estuary, marine influence is considerably stronger than fluvial input. A rough estimate of tidal prism using estuarine area (34×1010 m2) and a mean tidal amplitude of 1.2 m is ∼8.2×107 m3 day−1, compared to mean freshwater discharge of only about 6.1×105 day−1. As a consequence, the Piauí River estuarine waters were provided with considerable pH buffering capacity.


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The freshwater exhibited large temporal changes of pH (Fig. 2a,b). The maximum value was recorded during the peak of dry season (December 1995; Fig. 2a), when fluvial discharge was almost absent. The fluvial pH varied between 7.0 and 7.6 in the other surveys. The estuarine waters also presented a large pH range and the distribution seems to be related with the buffer capacity and long-term mixing. Dissolved Inorganic Carbon DIC concentrations in the Piauí estuary exceeded by far those found in the Georgia estuaries by Cai and Wang (1998), especially in the freshwater end member. These

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

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

concentrations can be due to the contribution of natural and anthropogenic processes, as the dissolution of carbonatic rock (Formation Cotinguiba, Cretaceous) and mainly the discharge of domestic and industrial with a high content of decomposing organic matter for the fluvial concentrations. The latter process is especially apparent during the two surveys in March 1996 (Fig. 3), when a sudden increase of runoff promoted the flushing of the stagnant polluted freshwater to the estuary. In this month, the concentration in freshwater end member reached up to 4,900 μmol l−1, which correspond to a pCO2 of about 10,000 μatm. This value is similar to those found to the humic rivers of Georgia (∼8,100 μatm; Cai and Wang 1998) and almost as high as the observed in the Scheldt river (16,300 μatm; Abril et al. 2000). High pCO2 in freshwater is not a recent finding and is already mentioned in the literature, especially when draining carbonate terrains (Drever 1982). In the estuarine zone, the concentrations were about 2,200± 360 μmol l−1, and events with pCO2 higher than 1,000 μatm were not rare. The inputs of humic and fulvic acids are probably considerable in sight of the great area covered by mangrove. However, the influence of these compounds upon the analytical technique employed for alkalinity analysis and further DIC calculations should only be restricted to the narrow and shallow inner estuarine portion. Otherwise, this influence was minimized by the titration procedure, till pH 3.4. These values are below the observed in heavily polluted estuaries such as the Rhine (3,500– 6,300 μatm; Kempe 1982) and the Scheldt (5,700 μatm; Frankignoulle et al. 1996).

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The importance of the fluvial inputs with high concentrations of DIC was restricted to the beginning of the wet season. During most of the year, the mixing diagram of DIC indicated seawater intrusion to be the main source. The nonlinear DIC × S relationship expresses the nonconservative fluxes within the estuary (net heterotrophy). Saturation and Exchange of CO2 Through Atmosphere/ Water Interface The value and changes of CO2 saturation are useful indicators 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 the sampling station nearest to the sea, in which subsaturation occurred in April, May, June, and November. The innermost station presented extremely high values, with peaks in both dry and wet seasons. This supersaturation at the beginning of the photoperiod indicates that the heterotrophic activity during the night was intense enough to drive pCO2 above atmospheric values. The supersaturation in the dry season can be explained by low water exchange in the upper portion of the estuary. In the absence of a significant freshwater input, the water renewal is forced just by net evaporation and consequent residual flux and also by tidal mixing. Tidal mixing is very ineffective in this narrow and shallow part of the estuary. Thus, it is more likely that the retention and respiration of organic material previously discharged by the river and from the mangrove are responsible for these high CO2 concentrations. Anaerobic metabolism probably is an important component of the respiration processes, especially inside the sediment. Sediments in Piauí River estuary Fig. 4 Degree of saturation in CO2 (%) at three stations along the estuary, measured at dawn. Horizontal line indicates 100% saturation


have ∼3.5% organic C, compared with ∼0.5% inorganic C (Dr. E.C.G. Couto, unpublished data). This organic content is about twice that found by Smith and Hollibaugh (1997) in Tomales Bay, another shallow estuary in which sulfate reduction is important. The resultant net sulfate reduction may increase total alkalinity, and consequently, the estuarine waters can present a higher retention of DIC, in detriment of CO2 degassing. In the beginning of the wet season, supersaturation increased, presumably due to flushing of material accumulated in the reservoir during the dry season. This input of organic material was characterized by high concentrations of particulate organic (∼2.5 mmol C l−1) and dissolved inorganic (∼4.9 mmol C l−1) carbon. The excess CO2 is caused mainly by mineralization of fluvial material of anthropogenic origin. Most of the remineralization occurs in the upper turbid zones and is related with the sewage and industrial effluents of high organic content. Abril et al. (2002) observed in European estuaries this pattern of heterotrophy in the upper estuary sustained by continental/ anthropogenic sources and a higher contribution of autochthonous POC in the marine regions of the estuaries. The intensity of respiration and CO2 fluxes to the atmosphere were closely related with this allochtonous inputs. Supersaturation at this moment was not only the result of degradation of allochtonous particulate and dissolved organic material but also the advective flux of dissolved inorganic carbon. The transport of DIC by rivers can represent as much as 50% of the estuarine CO2 emission to the atmosphere, while nitrification and heterotrophic activity can account for the other half (Abril et al. 2000). In June, July, and September, under higher freshwater input via the dam, the fluvial input of DIC could even be equivalent to or more important than local heterotrophic


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activity to establish a high supersaturation in the upper estuary. As a consequence, these results indicate the preponderance of heterotrophy not only in the estuarine region but also in the Piauí and Piauitinga freshwater sources and the reservoirs of the system of dams (Souza 1999). Given the daily changes of pCO2, the whole estuary act as a net source of CO2 to the atmosphere (Table 1). The average rates of CO2 loss to the atmosphere found in this study (6–21 mol m−2 year−1) were lower than those observed 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 mol m−2 year−1; Abril et al. 2004). However, Cai and Wang (1998) applied a higher exchange coefficient (KCO2 =3 m day−1) to the whole estuary, whereas in this study, the exchange coefficient was chosen according to the measured wind velocity, resulting in KCO2 between 0.2–0.8 m day−1 (Carmouze 1994). Wind velocities were lower in the estuarine areas with higher supersaturation, due to the presence of a high and dense mangrove forest surrounding the narrow channel. The higher KCO2 was only used in this area in May, when wind direction coincided with the main channel axis. The other authors measured directly the CO2 fluxes with floating chambers, and their results were independent of wind velocity and piston velocity. Net Ecosystem Metabolism We observed a general trend toward net heterotrophy on both monthly (from 24-h measurements; Fig. 5) and annual time scales (monthly free-water measurements; Table 2). Simultaneous decreases (station 3) and increases (station 6) in the degree of heterotrophy followed increases in freshwater runoff between January to March (Fig. 5). This behavior indicates the transport of the organic matter accumulated in the reservoirs during the dry season. Mukhopadhyay et al. (2006) reported the same event at the River Hooghly estuary, India. After this transport, strong CO2 consumption was measured at stations 6 and 7, where net primary production/respiration alternated during the rest of the year. The magnitude of CO2 consumption contrasted 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 Tomales Bay (Smith and Hollibaugh 1997), South San Francisco Bay (Caffrey et al. 1998), and the tropical coastal lagoon of Saquarema (Carmouze 1994), the Piauí River estuary was characterized by spatial patchiness and pulses of net heterotrophy as a response to freshwater discharge, anthropogenic inputs, and the fluxes of organic matter and nutrients. It is important to observe that high net autotrophic rates occurred during periods of CO2 supersaturation (e.g., May). This suggests sharp changes in the prevailing metabolic processes, as observed previously in this (Souza and Couto 1999) and another tropical systems (Carmouze 1994). The assessment of NEM in an annual scale by the integration of monthly changes of average DIC concentrations assumes some stability of the atmospheric exchange and minimizes the effect of short-term changes in metabolism and advective processes. Without a correction for exchange through the atmosphere/water interface, these results were very different from the monthly rates, suggesting an estuary with net primary production (Table 2; NEM= 4.5×10−7 mol year−1). Correcting for atmospheric exchange produced net heterotrophic rates almost equal to CO2 losses to atmosphere (Table 2; NEM=−3.9×10−8 mol year−1). These results were a magnitude order higher than the obtained in the previous mass balance and stoichiometric calculations using the Redfield C:P ratio (Souza et al. 2000; Table 3; −6.9×107 mol year−1). The use of an average C:P ratio 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 total ecosystem metabolic rates (Fig. 6), suggesting that there was equilibrium between autotrophic/heterotrophic processes, in agreement with previous results of Souza and Couto (1999) in November 1994. The event of net autotrophy observed in May 18 seems to be the result of the large fluvial 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 6 3 Overall

0–5.3 5.3–17.3 17.3–35

15.6 11.6 6.4 33.4

28.5 24.9 10.2 21.2

−5.9 −17.6 −21.4 −15.0

−0.9×108 −2.0×108 −1.4×108 −4.3×108

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

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subject to more intense light incidence and high oxygen tension. Inferences on these fluxes in the estuary were made applying the Eqs. 1–3. Resolving the Eq. 1 with the rates obtained in the former sections resulted in: Mangrove þ 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 year1 :

Fig. 5 Rates of net ecosystem metabolism at three stations along the estuary measured by changes of free-water concentration over 24-h periods. Values corrected for the exchange across atmosphere/water interface. Positive and negative values correspond to CO2 production (net heterotrophy) and consume (net autotrophy), respectively

This nutrient supply may be from the degradation of organic particles in suspension or in the sediments at the dam during the dry season. The algebraic sum of positive (net heterotrophy) and negative (net autotrophy) rates is almost zero (Table 3), resulting in only slight net autotrophy 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 a seasonal trend, the overall signal of the pelagic rates was the same of total ecosystem rates. The differences observed may be related to changes in pelagic metabolism such as resource limitation of bacterial communities by organic carbon in the upper estuary and nutrients in the outer estuary (Smith and Kemp 2003) and the seasonal/spatial variation of the picoplankton production/respiration (Smith and Kemp 2001). Estimation of the Role of Sediments and Mangroves The individual contribution of the subtidal, tidal mudflats, and mangrove sediment to net ecosystem metabolism are unknown. Nevertheless, mangrove and tidal mudflats are expected to present higher metabolic rates, since they are

This calculation shows that intertidal sediment in mangroves and mudflats was the site of most heterotrophic activity in the estuary. The change of anoxic to oxic conditions during tidal exposure and the presence of oxic/ anoxic microzones, allowing for the development of heterotrophic processes coupled to denitrification/nitrification, can lead to higher metabolic rates. It is important to note that wherever heterotrophy prevails, a variable fraction of the organic matter respired may be of allochtonous origin (Bouillon et al. 2004, 2007), including from the effluents of Estância City. Atmospheric carbon dioxide assimilated by mangrove trees must also be included in this value. The mangrove contribution calculated only by the difference of NEM and NPM also resulted in net heterotrophy (−4.2× 108 mol Corg year−1). The same procedure was applied to DIN and DIP according to Eqs. 2 and 3, but using the mean C:N and C:P ratio of the system (24:1 and 449:1, respectively), to link the nutrient assimilation by pelagic production. This resulted in: Mangrove þ 4:8 106 ¼ 1:3 106 þ 1:1 106 þ 5:7 106 ¼ þ3:8 106 mol DIN year1

and Mangrove þ 4:5 105 ¼ 6:7 104 þ 3:4 105 þ 1:8 105 ¼ þ 1:6 105 mol DIP year1 :

These results indicate that the mangrove ecosystem is a source of DIP to the estuary equivalent to anthropogenic inputs by the Piauitinga River. This rate was twice to the total 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 DIC concentration 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 6 3 Overall

−0.3 0.1 −1.0 −0.4

5.8 17.2 15.6 12.9

−0.5×107 0.1×107 −4.1×107 −4.5×107

0.9×108 2.0×108 1.0×108 3.9×108

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


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

mol year−1 mmol m−2 year−1

Δ DIP

Δ DIN

Δ DIC

P−RRedfield

P−RPOM

N fixation−denitrification

1.8×105 4.2

2.2×106 50

6.3×108 4.6×103

−69×106 −1.6×103

−289×106 −6.6×103

−2.1×106 −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 balance between nitrogen fixation and denitrification

to the estuary. This rate was slightly higher than the one obtained in the mass balance. Though the first mass balance exercise resulted in low rates of net nitrogen fixation (Souza 1999), more accurate calculations reveal a slight net denitrifying system (Souza et al. 2000; Table 4). This demonstrates that in this system, the model exhibits a strong sensitivity to both N:P stoichiometry and DIN concentrations. This result does not mean that we should disregard the potential importance of nitrogen fixation as a source of nitrogen potentially exported. Blooms of N2-fixing organisms such as Lyngbya cf. confervoides and Enteromorpha spp. were observed during this and previous studies (Souza and Couto 1999). Remineralization of this autochtonous and allochtonous organic nitrogen produces the inorganic nitrogen export. Several works have already described the role of mangroves in the export of dissolved nutrients, either in inorganic or organic forms (Wong 1984). Boto and Robertson (1990) reported that nitrogen fixation in sediment, algal mats, aerial roots, and trunks of a mangrove in Australia was almost equal the export of dissolved inorganic nitrogen. Woitchik et al. (1997) also found that nitrogen fixation in an African coastal lagoon represents a significant (13–21%), but not the primary source of nitrogen to the mangrove sediment (the litter fall). Nitrogen

fixation and a positive sediment balance were considered essential conditions to nutrient outwelling from tropical mangroves (Dittmar and Lara 2001). It is important to observe that the LOICZ guidelines recommend the use of the dissolved organic fractions of N and P as well as DIN and DIP. The budgets using only the inorganic forms (as the results presented in this study) can result in unaccounted nutrient inputs due to the remineralization of more labile organic compounds, especially in the presence of high N fixation rates and inputs of untreated waste loads. Sources and Sinks of Organic Carbon in the Estuary To compare the magnitude of fluvial (9.2×108 mol POC year−1) and anthropogenic (4.7×108 mol POC year−1) inputs of organic carbon and decomposition of organic carbon in the mangroves, we scaled up the DIP production in the mangrove by the average C:P ratio of mangrove (∼1,000:1; Lanza et al. 1997). This produced an estimate of the total mass of respired organic carbon of about −1.6× 108 mol year−1. This rate is certainly underestimated, since DIP is also removed in the mangrove by biotic and abiotic processes. However, this rate just exceeds an estimate of mangrove contribution with POC, made according to Wafar et al. (1997) and the mangrove area of Piauí River (7.2 km2; 1.1×108 mol POC year−1). Estimated in the same way, the fluxes of DOC from litterfall are about twice this value. Two other approaches to estimating the organic matter decomposition in the mangrove were the use of Eq. 1 or simply subtraction of the NPM from NEM. Both procedures resulted in higher rates than the former one (−6.5 and Table 4 Rates of net pelagic metabolism at three stations along the estuary obtained by integration of the incubation results over the year

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

Station

NPM (mol m−2 year−1)

Total NPM (mol year−1)

7 6 3 Overall

−0.7 −2.3 2.2 −0.3

−0.1×108 −0.3×108 0.1×108 −0.3×108

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

120


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

108 mol year−1 mol m2 year−1 (estuary) mol m2 year−1 (mangrove)

Fluvial inputs

P−Rmangrove

Litter fluxes

POC

POC + DOC

POC

DOC

−4.2 or –6.5 −13 or −20 58

1.1 3.2 44

2.2 6.6 92

9.2 27 128

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

−4.2×108 mol C year−1, respectively). The first value exceeded the other estimates of NEM, while the latter values correspond to about 95% of NEM. These estimates suggest that mangrove production cannot sustain the net heterotrophy observed at the mangrove and estuary (Table 5). This sounds as an obvious assertion when the main source of phosphorus is considered, but carbon in mangrove trees can be mainly fixed directly from atmosphere (outside the system boundaries). Accordingly, it is important to consider anthropogenic contributions through the dam, either directly as dissolved organic carbon (unpublished data) or as particulate organic matter of low C:N ratio and less refractory. One of the effects of the construction of dams is the increase of organic matter decomposition rates (producing some dissolved species) and assimilation of the resulting dissolved inorganic nutrients as more labile particulate matter in the reservoirs (Hopkinson and Vallino 1995). A reduction of the C:N and C:P ratio was observed in samplings in River Piauitinga and its reservoirs (Souza 1999). Even in the absence 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 N enrichment and bacterial growth. Tam (1998) observed experimentally that wastewater inputs promote bacterial growth and activity. The former author suggested that the coupling of high bacterial biomass and productivity rates with low densities of macroinfaunal organisms, as observed in Piauí River, implies that bacterial production and remineralization can be a sink for carbon in tropical mangrove estuaries. There was a tendency to consider dissolved organic fraction as the primary form in which carbon fixed in the mangrove is exported (Twilley 1985; Bano et al. 1997). Dissolved organic carbon is considered less refractory to decomposition and more readily used by heterotrophic bacteria than organic particles. It was reported that this fraction could sustain much of the heterotrophy occurring in mangroves (Bano et al. 1997). However, Dittmar et al. (2001) observed that dissolved organic carbon behaved conservatively along a Brazilian mangrove estuary, suggesting a refractory chemical nature.

Despite the biological availability of dissolved inorganic carbon, there are also some clues that a significant parcel of the bacterial production in tropical mangroves is originating from bacteria attached to particulate organic matter (Bano et al. 1997). Crump et al. (1998) reported that particleattached bacteria were responsible for as much as 90% of bacterial production and can dominate particulate organic material degradation and transfer to detrital food web in a temperate turbid estuary (Columbia River). A further study revealed that most of the bacterial activity in this estuary occurs in small slowly settling particles (Crump and Baross 2000). Particle-attached microbial activity (reduced C:N ratio) may be the main pathway of organic carbon transfer to higher trophic levels. In fact, Anesio et al. (2003) showed that respiration of bacteria attached to particle is not only significant but that the coupling with free bacteria by assimilation of dissolved products of its enzyme activity is important to organic matter remineralization. The coupling between water column and mangrove sediment can also be greatly enhanced by the presence of benthic filter feeding organisms. In the mangrove of Piauí River estuary, there are extensive banks of Mytella guyanensis and Mytella charruana, which were collected and commercialized (E.C. Couto, personal communication). The intensive extraction of these bivalves and of Ucides cordatus (true mangrove crab) may constitute a somewhat important and unmeasured loss of carbon. Implications for Management The domestic and industrial effluents of Estância undoubtedly should receive treatment, and the presence of the dams changes the nature and the effects of these inputs to the estuary. The organic load is modified to a less refractory form and the organic particles are enriched during their permanence in the reservoirs, being more suitable to degradation by particle-attached bacteria. These changes support the estuarine trend toward heterotrophy, and probably the estuary functioning would be very different if these pollutants were flowing continuously. The decommissioning of the hydroelectric reservoir should be considered, since it only serves to a textile industry and generate less than 1 kWh.


Conclusions This mesotidal estuary presented a net heterotrophic metabolism in an annual scale, acting as a source of DIN and DIP to coastal waters, while most of the produced DIC was lost to atmosphere (13 mol CO2 m−2 year−1). The water column was almost balanced between auto- and heterotrophy and the mangrove forests and tidal mudflats were responsible for most of the NEM. The autochtonous production and mangrove litter cannot sustain the estuarine and mangrove heterotrophy and the anthropogenic inputs contribute with more than 50% of fluvial inputs of particulate organic matter. The results suggest that fluvial and anthropogenic organic matter is the main source for the sustenance of mangrove ecosystem metabolism and the enhancement of benthic microbial processes. This organic matter, rather than mangrove autochthonous production, is responsible for the net heterotrophy and export of dissolved inorganic nutrients. Thus, terrestrial and anthropogenic organic carbon may be supporting a greater part of secondary production than considered up till now. Acknowledgments We thank Dr. J. P. H. Alves for the laboratory support in the Departamento de Química/UFSE. We acknowledge Dr. E. C. G. Couto (Departamento de Ciências Biológicas/UESC) for the participation in field trips and for the important comments about biological features; Dr. S.V. Smith (CICESE) made several important contributions to the water and nutrient budgets that resulted in the data exposed in Table 3; people of the LOICZ IPO and the Instituto Argentino de Oceanografia, particularly Dr. Chris Crossland and Dr. Gerardo Perillo, for the opportunity to discuss these data and budgets during the South America Biogeochemical Budgeting Workshop held in Bahia Blanca, Argentina, in 1999. Dr. A. Raw (UESC) provided valuable critical and language review. Dr. C. A. Simenstad (University of Washington) reviewed a former version of the manuscript, resulting in several improvements. A. M. Fernandes, M. V. Carvalho, P. S. Lima, C. Assis, D. Assis, and E. Santos helped with field and laboratory assistance. Several field surveys were done in vessel of Brazilian Navy, for what we specially thank the Port Authority Cap. R. V. Dutra and Corporal F. Souza at CPSE. CNPq provided support for the work described in this paper in the form of a DCR research grant proc. no. 300.738/1995-1 (first author) and PQ grant proc. no. 300.772/2004-1 (last author).

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