Carbon Dynamics of Florida Bay: Spatiotemporal ... - ACS Publications

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Carbon Dynamics of Florida Bay: Spatiotemporal Patterns and Biological Control Jia-Zhong Zhang* and Charles J. Fischer Ocean Chemistry and Ecosystems Division, Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, Florida 33149, United States S Supporting Information *

ABSTRACT: Carbon dynamics of Florida Bay is manifested by wide ranges of pH (7.65−8.61), dissolved inorganic carbon (DIC, 929−3223 μM) and partial pressure of CO2 (pCO2, 50−1313 μatm) observed over seven years. Despite the seasonal variation, a decline of −0.0066 pH per year was observed as a result of ocean acidification and the spatiotemporal patterns were consistent with known biological processes in the bay. Microbial respiration of organic matter produced high pCO2, resulting in Florida Bay being a CO2 source to the atmosphere during winter and spring. In summer, cyanobacteria blooms developed in the north central bay drew down pCO2, causing bloom waters to become a CO2 sink while the nonbloom waters shrunk but remained a CO2 source. The maxima local CO2 fluxes were 36.4 ± 10.5 and −14.0 ± 5.6 mmol m−2 d−1 for the source and sink region, respectively. Cyanobacteria blooms modulated the interannual variation in bay-wide CO2 net flux, which averaged 7.96 × 109 ± 1.84 × 109 mol yr−1. Extensive cyanobacteria blooms in 2009 resulted in a 50% reduction in the net CO2 flux as compared with 2010 when a minimal cyanobacteria bloom occurred. air−water CO2 fluxes.7−9 Although nutrients are routinely monitored for water quality, there is a severe paucity in DIC data and little is known about the carbon dynamics and ocean acidification in coastal waters.14 To fill the gaps in global carbon budget, many measurements have recently been conducted.15,16 Although estuaries have been generally considered as heterotrophic systems and, thus, a source of CO2 to the atmosphere,7−9,17−19 recent studies have shown that some coastal waters function as sources,20−27 whereas others act as sinks.28−32 More comprehensive studies have revealed that the CO2 sink and source regions change with space and time within a given estuary and the direction and magnitude of CO2 flux were controlled by the location and intensity of phytoplankton photosynthesis relative to that of microbial respiration.33−35 Florida Bay, located at the southern end of the Florida peninsula, U. S. A., is one of the largest coastal lagoons in the world with an area of approximately 2026 km2. The bay stretches between the Everglades wetlands in the north and the Florida Keys to the south (Figure 1). Although its western margin is open to the Gulf of Mexico, water exchange is highly restricted due to extensive shallow mud banks that form the western boundary of the Everglades National Park. Florida Bay

1. INTRODUCTION Atmospheric CO2 level increased from 280 ppm in 1800s to 400 ppm today as a result of fossil fuel combustion and cement production. The oceans have adsorbed approximately 48% of this anthropogenic CO2 emission,1 resulting in a decrease in surface ocean pH.2−4 Continued ocean acidification into the future due to growing atmospheric CO2 level might have profound effects on marine biota, particularly calcifying organisms such as corals.5 However, there is little long-term pH data available to estimate the rate of ocean acidification. Furthermore, spatiotemporal variability needs to be resolved before a long-term trend can be adequately accessed. This is particularly challenging for estuarine and coastal waters, where spatiotemporal variability is much greater than the open ocean.6−9 Estuaries receive massive input of carbon and nutrients from continuous riverine discharge and episodic terrestrial runoff.10−13 The supply of nutrients fuel primary production, which often results in phytoplankton blooms, causing a drawdown of dissolved inorganic carbon (DIC) in surface waters. Terrestrial-derived organic carbon, along with autochthonous production, stimulates intensive microbial respiration. Carbon and nutrient dynamics in estuaries, therefore, are mainly driven by these two opposing processes with varying intensity in space and time. It is the net difference between the primary production and respiration as well as wind speed and water temperature that control the direction and magnitude of This article not subject to U.S. Copyright. Published 2014 by the American Chemical Society

Received: Revised: Accepted: Published: 9161

February 5, 2014 July 3, 2014 July 14, 2014 July 14, 2014 dx.doi.org/10.1021/es500510z | Environ. Sci. Technol. 2014, 48, 9161−9169

Environmental Science & Technology

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Figure 1. Locations of 40 sampling stations in Florida Bay. Seasonal progression of cyanobacteria bloom is indicated by the color contour lines: summer in red and fall in green (after Phlips et al.37).

region.48 Due to limited spatiotemporal coverage in previous studies, the patterns of spatial distribution and seasonal variation have not been established and the processes controlling the spatial distribution of sink and source regions cannot be inferred. More importantly, whether Florida Bay, as a whole, is a source or sink of atmospheric CO2 on seasonal or annual bases remains an open question. The objectives of this study are (1) to establish the seasonal patterns of carbon dynamics and attribute them to the biological processes in the bay; (2) to estimate the ocean acidification trend; and (3) to derive an annual CO2 flux estimate and its interannual variation.

is a shallow lagoon with an average water depth of 1 m. Dotted mangrove islands and a complex network of shallow carbonate mud banks, many of which emerged at low tide, effectively divide Florida Bay into numerous isolated sub-basins with maximum water depths of 2−3 m. Water exchange is restricted to narrow cuts and overbanks awash at high tide. Seagrass meadows cover much of the bay bottom and provide a habitat for upper trophic level species. In particular, Florida Bay is a nursery ground for many commercial and recreational fisheries including pink shrimp and spiny lobster. The bay experiences a subtropical climate with strong wet−dry seasonality and an annual precipitation of approximately 120 cm, with 70% of the rainfall occurring from June to October. Historically, Florida Bay received its freshwater from sheet flow across the marl prairies of southern Everglades through the Buttonwood embankment into the north central bay and from the numerous creeks fed by Taylor Slough. Since the implementation of extensive water management in the 1950s, the upstream freshwater has been diverted to the coasts of the Atlantic Ocean and the Gulf of Mexico. The southward flow has now been substantially reduced and diverted to the C-111 canal before being discharged into the northeastern bay. In 1987, Florida Bay experienced a mass mortality of seagrass and subsequent cyanobacteria blooms. The cyanobacteria blooms exhibited distinct spatial and temporal features. They developed in the north-central bay in summer and spread southward in fall (Figure 1). Since 1991, areally expansive, persistent, and recurring cyanobacteria blooms have become a regular biological feature, indicating a distinct change in the ecology of the bay.36−39 The decline of the bay’s ecosystem is thought to have been caused by reduced freshwater inflow and increased nutrient loading. Although there are many studies on seagrass, nutrients, and water quality in the bay,40−46 only a couple of studies have focused on CO2. The first reconnaissance survey during 1997− 1998 revealed the variation of carbonate parameters both in space and time within the bay and reflected the heterogeneity and complexity of the bay’s ecosystem.47 Subsequent CO2 flux measurements observed the central bay being a persistent sink

2. MATERIALS AND METHODS 2.1. Sampling and Analysis. Seawater samples were filtered, preserved with chloroform, and stored at 4 °C from 40 stations in Florida Bay (Figure 1) aboard the R/V Virginia Key during the bimonthly survey from 2006 to 2012 (no samples in 2008). Samples were analyzed at our shore-based laboratory for DIC, pH, and nutrients. DIC was measured using a Shimadzu TOC-V total organic carbon analyzer in IC mode. Samples were acidified with HCl to convert DIC to CO2 and the latter was quantified by a nondispersive infrared gas analyzer. The analyzer was calibrated using Dickson’s Certified Reference Material for DIC.49 The method detection limit for DIC is 0.3 μM with a precision of 1%. The pH of sample was measured at 25 °C with an HP-8453 spectrophotometer using m-cresol purple as an indicator.50 The deuterium lamp in the spectrophotometer was turned off during measurements to avoid UV photolysis of both the dye and organic matter in the samples.51 Absorbances were measured at wavelengths of 578 and 434 nm.52 Values for pH were then calculated in total proton scale at 25 °C using indicator pK measured as a function of salinity over the entire estuarine salinity range.51 2.2. Flux Calculation. The pCO2 was calculated using CO2SYS.XLS from DIC, pH, salinity, temperature, and nutrients and the carbonic acid dissociation constants53 as values refitted54 to the total proton scale with a precision of 10 μatm.55,56 The CO2 fluxes across the air−water interface were calculated as 9162

dx.doi.org/10.1021/es500510z | Environ. Sci. Technol. 2014, 48, 9161−9169


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Figure 2. Seasonal changes in spatial distribution of (A) DIC (scale bar: 800−3200 μM, interval 300 μM), (B) pH (7.0−9.0, interval 0.2), and (C) pCO2 (0−1000 μatm, interval 100 μatm) in Florida Bay waters during year 2011.

F = kK 0(pCO2sw − pCO2air ) = kK 0ΔpCO2

function of wind speed using Wanninkhof’s quadratic equation.58 Monthly average wind speed over the past 50 years in the study area varied from 4.11 to 5.45 m s−1. Longterm average wind speed for each month from Florida Climate Center was used in the flux calculation. Bay-wide daily CO2 flux for each survey was intergraded from the 40 stations using a pCO2 contour grid file created with Surfer software. The areas of CO2 sink and source regions and their fluxes were calculated using the grid volume computation function in Surfer. Atmospheric pCO2 values were used to define the surface boundary layer (Z values) between sink and

(1)

where k (cm h−1) is the gas transfer velocity of CO2, and K0 (mol m−3 atm−1) is the solubility coefficient of CO2 at in situ temperature and salinity.57 The pCO2sw and pCO2air are the partial pressure of CO2 (atm) in seawater and air, respectively. A positive value of F indicates a transfer of CO2 from seawater to the atmosphere. The globally averaged marine surface annual mean pCO2 from NOAA Earth System Research Laboratory were used for atmospheric values, increasing from 380.93 to 392.58 ppm in 2006−2012. The k values were computed as a 9163



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frequency and intensity of the bloom was always restricted to the north central bay where cellular biovolumes of the cyanobacteria Synechococcus regularly exceeded 107 μm3 ml−1(Figure 1).37 High concentration of cyanobacteria also appeared during the fall in the south-central region of the bay and coincided with the onset of seasonal cold fronts, when the wind direction shifts from the more common east or southeasterly direction to a north or northwesterly direction.37 A strong northerly or northwesterly wind, brought by a cold front, can drive the bloom-laden water from the north central region to the south central region. This north−south pattern of water circulation is supported by similarities in the patterns of salinity variation observed in these two regions.61 The bay-wide ranges of DIC and pH measured in each survey changed with the seasons. The monthly maxima and minima of DIC observed from 2006 to 2012 are plotted against the month of year in Figure 3A. The top clusters of data are maxima and the bottom minima. Maxima DIC were approximately 3000 μM in spring, decreased to 2500 μM in summer, and then increased to 3000 μM again in December. Monthly minima DIC were approximately 2000 μM in spring, decreased to 1000 μM in May, and then increased to 2000 μM in December. The stations with a monthly maximum DIC always had a minimum pH, ranging from 7.6 to 8.0 (Figure 3B). Likewise, the maxima pH were associated with minima DIC and varied from 8.1 to 8.6. In spring, the maxima pH was 8.2 ± 0.1 and rapidly increased to 8.5 ± 0.1 in May. Maxima pH decreased gradually in fall and winter to 8.3 ± 0.1. The large area of bay waters with elevated pH induced by cyanobacteria blooms can serve as refugia for corals growing in Florida Bay and off the Florida Keys under continued impact of ocean acidification.62 3.2. Estimate Ocean Acidification Trend in Florida Bay. Assuming surface seawater is in equilibrium with increasing atmospheric CO2, the calculated rate of ocean acidification is −0.0017 pH per year.2,4 A plot of all pH data collected in the bay against time showed a statistically significant decreased trend (Supporting Information Figure S1). The estimated rate of −0.0143 pH per year is much higher than those observed in the open ocean2−4 but is only one-third of the rate observed in coastal waters of Tatoosh Island in the eastern Pacific.63 Arguably, the high pHs observed in the sink region were caused by cyanobacteria blooms and this may obscure ocean acidification signals. On the other hand, the CO2 source waters were dominated by respiration processes, which exhibited little seasonal variation. It might be more reliable to estimate the ocean acidification trend in the source waters. Linear least-squares regression analyses of pH in CO2 source waters against time generated a statistically significant (n = 814, p < 0.00005) annual trend of −0.0066 ± 0.0015 pH per year with a 95% confidence interval of −0.0096 and −0.0036 (Figure 4). This rate is three-time higher than that observed in the open ocean.2−4 A 25% decrease in buffer intensity,59 when seawater pH drops from 8.1 to 7.9, contributes in part to the higher rate of acidification observed in these low pH waters.64 Nonetheless, long-term data in different estuaries are needed to verify the higher rate of ocean acidification and to reveal the factors governing the ocean acidification processes in coastal waters. 3.3. Spatial Distribution of pCO2 and Its Seasonal Variation. Spatial distribution of pCO2 and its seasonal variation in 2011 are shown in Figure 2c. In spring, pCO2 values were high for the entire bay, averaging 645 ± 182 μatm.

source region. Calculations produced both positive (source) and negative (sink) areas. The same contour grid file was used for flux calculation in which ΔpCO2 was multiplied by k and K0 such that the vertical axes represent flux per unit area (eq 1). The kK0 values for each survey were used as a vertical Z factor. CO2 fluxes in each region was then intergraded over the area and calculated as “volumes”. A positive volume indicated a CO2 flux from seawater to the air. Annual fluxes were estimated by a summation of monthly fluxes with data gaps interpolated with available data in the same season.

3. RESULTS AND DISCUSSION 3.1. Spatial Distributions of DIC and pH and Their Seasonal Variation. Spatiotemporal patterns of DIC and pH in Florida Bay were similar each year. As an example, spatial distributions of DIC and pH and their seasonal variation in 2011 are shown in Figure 2. The spatial distribution of pH was opposite to that of DIC as a result of carbonate buffering system on seawater pH.59,60 In March, DIC concentrations were high over the entire bay, averaging 2454 ± 243 μM; pH were at annual minima, ranging from 7.69 to 8.10 with an average of 7.93 ± 0.08. The highest DIC and lowest pH were found in the northern coastal stations adjacent to the Everglades wetlands, ranging from 2591 to 2917 μM with an exception of the lowest DIC (1717 μM) and highest pH (8.10) at north-central station 7. In April, bay-wide DIC decreased to 2279 ± 301 μM. This was primarily due to a decrease of DIC at station 7 (1437 μM) and the spreading of low DIC (40) developed in the north central bay coexisted with the lowest DIC observed.42,61 Apparently, precipitation and evaporation processes that cause covariation of salinity and DIC, usually observed in oligotrophic open oceans, were not manifested in Florida Bay because the biological uptake and regeneration of DIC overwhelmed the precipitation and evaporation induced DIC change. Furthermore, these biological processes have no effect on salinity. In fact, the spatiotemporal pattern of carbon parameters resemble known spatial distribution and seasonal succession of cyanobacteria blooms in Florida Bay.36−39 A multiyear comprehensive study conducted by Phlips et al.36,37 documented the development of annual blooms of cyanobacteria in Florida Bay in late spring or early summer. The greatest 9164



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Figure 4. Long-term ocean acidification trend observed from CO2 source waters of Florida Bay. Linear least-squares regression analyses of pH in CO2 source waters against time generated a statistically significant (n = 814, p < 0.00005) annual trend of −0.0066 ± 0.0015 pH per year with a 95% confidence interval of −0.0096 and −0.0036.

The highest pCO2 values were found in the eastern and western regions of the bay, ranging from 600 to 1059 μatm. Low pCO2 water was located in the central bay with most stations in a range of 400−600 μatm; only station 7 had a pCO2 value that was significantly lower than the air (285 μatm in March and 264 μatm in April). By the end of May, pCO2 at station 7 decreased to 50 μatm and low pCO2 water spread southward and reached its maximum extent. The area of pCO2 lower than the atmospheric value (a sink region) was 1032 km2, accounting for 51% of the bay area. The bay-wide station average pCO2 was 381 ± 239 μatm, lower than the atmospheric value of 390 μatm. As the season progressed into September, the pCO2 values at station 7 increased to 211 μatm. The minimum pCO2 of 180 μatm occurred at nearby station 6, with a maximum pH of 8.36 and the sink region decreased to 304 km2 (15% of the bay). In October, the pCO2 decreased to 141 and 184 μatm at station 6 and 7, respectively, and the sink area increased slightly to 425 km2 (21% of the bay). In December, the sink area increased to 626 km2 (31% of the bay) and the lowest pCO2 (165 μatm) shifted to station 33 in the central bay. This was consistent with the highest pH of 8.36 observed at the same station. During this study period, pCO2 in bay waters showed similar seasonal dynamics as DIC and pH. The monthly maxima and minima of station pCO2 in 2006 to 2012 are shown in Figure 3C. Maxima pCO2 were approximately 1000 μatm for all seasons. Minima pCO2 were approximately 200 μatm in spring and decreased to below 100 μatm in May, followed by an increase, reaching 200 μatm in fall and winter. Seasonal changes in the areas of the source and sink regions in 2006−2012 are shown in Figure 5a and 5b, respectively. The source and sink area varied over the years but the annual minima in source area always occurred in May, in responding to annual maxima in sink area. 3.4. Monthly Maxima Local Daily CO2 Source and Sink Fluxes and Their Interannual Variation. For each survey, a station with a maximum pCO2 produced the greatest local CO2 source flux to the atmosphere. At the same time, a station with a minimum pCO2 became the greatest local sink for atmospheric CO2 because a minimum pCO2 in each survey was always lower than the respective atmospheric value.

Figure 3. Seasonal changes in the range of (A) DIC concentration, (B) pH, (C) pCO2, and (D) CO2 flux (maxima at top and minima at bottom) in Florida Bay waters over the period of 2006−2012. The red arrows point to the annual DIC, pCO2 minima, and pH maxima recurring in May. The horizontal line in (C) indicates the average atmospheric pCO2 value. 9165



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3.5. Bay-Wide Integrated Daily CO2 Flux and Its Interannual Variation. Bay-wide daily CO2 source fluxes during 2006 to 2012 are plotted against the month of year in Figure 6A. Bay-wide daily CO2 source flux varied from 7.05 ×

Figure 5. Seasonal changes in the areas of CO2 (A) source region and (B) sink region in Florida Bay over the period of 2006−2012.

Therefore, the monthly maxima source and sink fluxes reflect the range of variability in the strength of CO2 source and sink waters as shown in Figure 3D. Maxima local CO2 source flux varied from 15.6 to 65.5 mmol m−2 d−1 with an average of 36.4 ± 10.5 mmol m−2 d−1 over the study period. A minimum local CO2 source flux of 15.6 mmol m−2 d−1 was observed in August 2006, reflecting the lowest monthly maximum station pCO2 of 599 μatm observed over the study period. A maximum local CO2 source flux of 65.5 mmol m−2 d−1 was observed in August 2010, reflecting the highest monthly maximum pCO2 of 1313 μatm observed over the study period at station 4. Maxima local CO2 sink flux varied from −2.9 to −23.3 mmol m−2 d−1 with an average of −14.0 ± 5.6 mmol m−2 d−1 over the study period. The minimum local CO2 sink flux of −2.9 mmol m−2 d−1 was observed in December 2009, reflecting the highest minimum pCO2 of 346 μatm observed for the entire study period at station 26. The maximum local CO2 sink flux of −23.3 mmol m−2 d−1 was observed in May 2011, reflecting the lowest monthly minimum pCO2 of 50 μatm observed for the entire study period at station 7. In contrast to the maxima CO2 source flux, there is a strong seasonal pattern seen in the maxima CO2 sink flux. The maximum local CO2 sink flux always occurred in May every year and decreased gradually in fall. There is considerable interannual variation in the maximum CO2 sink flux. The annual average maximum local CO2 sink flux varied from a low of −11.3 ± 5.1 mmol m−2 d−1 in 2010 to a high of −16.8 ± 7.6 mmol m−2 d−1 in 2007. The ranges of flux variations observed in this study are similar to previous direct measurements using flux chambers in which local daily flux varied from 59.9 to −40.3 mmol m−2 d−1.48

Figure 6. Seasonal changes in daily bay-wide CO2 (A) source flux, (B) sink flux and (C) net flux integrated over the source region, sink region and whole bay, respectively, over the period of 2006−2012.

106 to 6.01 × 107 mol d−1 with an average of 2.73 × 107 ± 1.25 × 107 mol d−1 over the 2006−2012 period. The minimum baywide daily CO2 source flux of 7.05 × 106 mol d−1 was observed in May 2009, reflecting the smallest source area (511 km2) and the largest sink area (1515 km2) observed during the entire study period. The maxima bay-wide daily CO2 source fluxes of 4.50−6.01 × 107 mol d−1 was observed in March and April 2011, reflecting the largest source areas of 1967−2001km2 observed in the entire study period. The annual minima daily CO2 source fluxes occurred in May due to shrinking of the CO2 source region. A substantial interannual variation was observed on top of the seasonal pattern. The annual average bay-wide 9166



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daily CO2 source flux varied from a low of 1.99 × 107 ± 1.03 × 107 mol d−1 in 2009 to a high of 3.44 × 107 ± 1.34 × 107 mol d−1 in 2010. Bay-wide daily CO2 sink fluxes in 2006 to 2012 are shown in Figure 6B. Because of the seasonal occurrence of cyanobacteria bloom and the subsequent die off in the bay, bay-wide daily CO2 sink flux varied over 3 orders of magnitude, ranging from −2.86 × 104 to −1.83 × 107 mol d−1 with an average of −3.10 × 106 ± 4.20 × 106 mol d−1 over the entire study period. The minimum bay-wide daily CO2 sink flux of −2.86 × 104 mol d−1 was observed in October 2010, reflecting the smallest sink area (56 km2) and the largest source area (1970 km2) observed in the entire study period. The maximum bay-wide daily CO2 sink flux of −1.83 × 107 mol d−1 was observed in May 2009, reflecting the largest sink area of 1515 km2 observed during the entire study period. The annual maxima daily CO2 sink fluxes occurred in May due to the expansion of the CO2 sink region induced by the cyanobacteria blooms. In addition to the seasonal pattern, there was also a substantial interannual variation. The annual average bay-wide daily CO2 sink flux varied from a low of −1.29 × 106 ± 1.59 × 106 mol d−1 in 2012 to a high of −5.60 × 106 ± 8.59 × 106 mol d−1 in 2009. The bay-wide daily CO2 net fluxes were obtained by adding the negative regional sink flux to the positive regional source flux for each survey. The bay-wide daily CO2 net fluxes observed during 2006 to 2012 are shown in Figure 6C. Baywide daily CO2 net flux varied from −1.12 × 107 mol d−1 to 5.99 × 107 mol d−1 with an average of 2.42 x107 ± 1.56 × 107 mol d−1 over the 2006−2012 period. The minimum bay-wide daily CO2 net flux of −1.12 × 107 mol d−1 was observed in May 2009, reflecting the largest sink area of 1515 km2 observed in the entire study period. Only in this survey, Florida Bay, as a whole, behaved as a sink for atmospheric CO2. The maximum bay-wide daily CO2 net flux of 5.99 × 107 mol d−1 was observed in April 2011, reflecting the second smallest sink area (59.6 km2) and the second largest source area (1967 km2) observed during the entire study period. The annual minima daily CO2 net fluxes occurred in May due to the cyanobacteria bloom. In addition to this seasonal pattern, there was considerable interannual variation. The annual average bay-wide daily CO2 net flux varied from 1.43 × 107 ± 1.85 × 107 mol d−1 in 2009 to 3.31 × 107 ± 1.49 × 107 mol d−1 in 2010. 3.6. Bay-Wide Integrated Annual CO2 Flux and Its Interannual Variation. Bay-wide daily CO2 net fluxes were multiplied by the number of days in a month to obtain baywide monthly CO2 fluxes. Because the samples were collected from bimonthly survey cruises, the missing data on monthly source and sink fluxes were interpolated separately from available source and sink data in the same season. Summation of the 12 monthly data provided a first order estimate of baywide annual CO2 fluxes. The bay-wide annual CO2 fluxes to the atmosphere are 7.93, 6.60, 5.32, 10.53, 9.09, and 8.29 × 109 mol C yr−1 for 2006, 2007, 2009, 2010, 2011, and 2012, respectively (Supporting Information Figure S2). The average annual flux was 7.96 × 109 ± 1.84 × 109 mol C yr−1 (3.93 ± 0.91 mol C m−2 yr−1) over the 2006−2012 period. The minimum annual flux observed in 2009 corresponds to a year in which a widespread cyanobacteria bloom occurred in the central bay. The maximum extent of the cyanobacteria bloom observed in 2009 resulted in a 50% reduction in net CO2 flux to the atmosphere as compared with that of year 2010, in which a minimal cyanobacteria bloom occurred. The annual fluxes observed in Florida Bay are similar to those observed in Tendo

Lagoon in the Ivory Coast of West Africa34 and estuaries of Cocheco, Bellamy, and Oyster rivers in New England, U. S. A. with limited freshwater flow.65 It is worth noting that these flux estimates are subjected to many sources of error. The samples were collected during the daytime, and diurnal variation in pCO2 due to photosynthesis is likely to cause an overestimate of sink flux.66,67 A previous study indicated the diurnal variation in Florida Bay was most likely influenced by precipitation and dissolution of calcium carbonate.68 Comprehensive studies are needed to quantify the spatial variation of diurnal signals in the bay, particularly measurements in the north central region during peak cyanobacteria blooms. Because of the high variability in biogeochemical processes observed in the bay, sufficient sampling coverage in both spatial and temporal scales are essential to accurately estimating the annual CO2 flux in Florida Bay. The 40 sampling stations used in this study seem to adequately cover the spatial variability of carbon parameters in Florida Bay. However, deficiency in temporal coverage in this study is likely the greatest error in the annual carbon budget estimates. Fortunately, sampling was conducted during the peak cyanobacteria bloom each May, except for 2008. In future studies, a monthly sampling program conducted over multiple years, and perhaps biweekly sampling during the bloom period would improve significantly on the estimates of annual carbon budget for Florida Bay.

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ASSOCIATED CONTENT

* Supporting Information S

A plot of all pH data against time in Florida Bay (Figure S1) and a plot of interannual variation of bay-wide CO2 flux to the atmosphere (Figure S2). This material is available free of charge via the Internet at http://pubs.acs.org/.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Phone: (305) 361 4512. Fax: (305) 361 4447. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors thank Lindsey Visser, Chris Kelble, Grant Rawson, and Jeff Judas for assistance with sample collection during the field survey in Florida Bay. This study was supported by NOAA/OAR base funds. The scientific results and conclusions, as well as any views or opinions expressed herein, are those of the authors and do not necessarily reflect the views of NOAA or the Department of Commerce.

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REFERENCES

(1) Sabine, C. L.; Feely, R. A.; Gruber, N.; Key, R. M.; Lee, K.; Bullister, J. L.; Wanninkhof, R.; Wong, C. S.; Wallace, D. W. R.; Tilbrook, B.; Millero, F. J.; Peng, T. H.; Kozyr, A.; Ono, T.; Rios, A. F. The oceanic sink for anthropogenic CO2. Science 2004, 305, 367−371. (2) Dore, J. E.; Lukas, R.; Sadler, D. W.; Church, M. J.; Karl, D. M. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 12235− 12240. (3) González-Dávila, M.; Santana-Casiano, J. M.; Rueda, M. J.; Llinás, O. The water column distribution of carbonate system variables at the ESTOC site from 1995 to 2004. Biogeosciences 2010, 7, 3067−3081. 9167



Article

(4) Byrne, R. H.; Mecking, S.; Feely, R. A.; Liu, X. Direct observations of basin-wide acidification of the North Pacific Ocean. Geophys. Res. Lett. 2010, 37, L02601 DOI: 10.1029/2009GL040999. (5) Doney, S. C.; Fabry, V. J.; Feely, R. A.; Kleypas, J. A. Ocean acidification:the other CO2 problem. Annu. Rev. Mar. Sci. 2009, 1, 169−192. (6) Wollast, R. Evaluation and comparison of the global carbon cycle in the coastal zone and in the open ocean. In The Global Coastal Ocean; Robinson, A. R., Brink, K. H., Eds.; John Wiley & Sons: 1998; pp 213−252. (7) Chen, C.-T. A.; Huang, T.-H.; Chen, Y.-C.; Bai, Y.; He, X.; Kang, Y. Air−sea exchanges of CO2 in the world’s coastal seas. Biogeoscience 2013, 10, 6509−6544. (8) Borges, A. V.; Schiettecatte, L.-S.; Abril, G.; Delille, B.; Gazeau, F. Carbon dioxide in European coastal waters. Estuarine, Coastal Shelf Sci. 2006, 70, 375−387. (9) Borges, A. V.; Abril, G. Carbon Dioxide and Methane Dynamics in Estuaries. In Treatise on Estuarine and Coastal Science, Vol. 5: Biogeochemistry; Wolanski, E., McLusky, D., Eds.; Academic Press: Waltham, 2011; pp 119−161. (10) Meybeck, M. Carbon, nitrogen and phosphorus transport by world rivers. Am. J. Sci. 1982, 282, 401−450. (11) Guo, L.; Zhang, J.-Z.; Guéguen, C. Speciation and fluxes of nutrients (N, P, Si) from the upper Yukon River. Global Biogeochem. Cycles 2004, 18, GB1038 DOI: 10.1029/2003GB002152. (12) Zhang, J.-Z.; Kelble, C. R.; Fischer, C. J.; Moore, L. Hurricane Katrina induced nutrient runoff from an agricultural area to coastal waters in Biscayne Bay, Florida. Estuarine, Coastal Shelf Sci. 2009, 84, 209−218, DOI: 10.1016/j.ecss.2009.06.026. (13) Liu, K. K., Atkinson, L.; Quiñones, R.; Talaue-McManus, L., Eds. Carbon and Nutrient Fluxes in Continental Margins: A Global Synthesis; Springer-Verlag: Berlin Heidelberg, 2010. (14) Borges, A. V. Do we have enough pieces of the jigsaw to integrate CO2 fluxes in the coastal ocean? Estuaries 2005, 28 (1), 3− 27, DOI: 10.1007/ BF02732750. (15) Laruelle, G. G.; Dürr, H. H.; Slomp, C. P.; Borges, A. V. Evaluation of sinks and sources of CO2 in the global coastal ocean using a spatially-explicit typology of estuaries and continental shelves. Geophys. Res. Lett. 2010, 37, L15607. (16) Laruelle, G. G.; Dürr, H. H.; Laurwald, R.; Hartmann, J.; Slomp, C. P.; Goossens, N.; Regnier, P. A. G. Global multi-scale segmentation of continental and coastal waters from the watersheds to the continental margins. Hydrol. Earth Syst. Sci. 2013, 17, 2029−2051. (17) Smith, S. V.; Hollibaugh, J. T. Coastal metabolism and the oceanic organic carbon balance. Rev. Geophys. 1993, 31 (1), 75−89, DOI: 10.1029/92RG02584. (18) Gattuso, J. P.; Frankignoulle, M.; Wollast, R. Carbon and carbonate metabolism in coastal aquatic ecosystems. Annu. Rev. Ecol. Syst. 1998, 29, 405−434. (19) Cai, W.-J. Estuarine and coastal ocean carbon paradox; CO2 sinks or sites of terrestrial carbon incineration? Annu. Rev. Mar. Sci. 2011, 3, 123−145. (20) Frankignoulle, M.; Abril, G.; Borges, A.; Bourge, I.; Canon, C.; Delille, B.; Libert, E.; Théate, J.-M. Carbon dioxide emission from European estuaries. Science 1998, 282, 434−436. (21) Raymond, P. A.; Bauer, J. E.; Cole, J. J. Atmospheric CO2 evasion, dissolved inorganic carbon production, and net heterotrophy in the York River estuary. Limnol. Oceanogr. 2000, 45 (8), 1707−1717, DOI: 10.4319/lo.2000.45.8.1707. (22) Jiang, L.-Q.; Cai, W.-J.; Wang, Y. A comparative study of carbon dioxide degassing in river- and marine-dominated estuaries. Limnol. Oceanogr. 2008, 53 (6), 2603−2615, DOI: 10.4319/lo.2008.53.6.2603. (23) Borges, A. V.; Djenidi, S.; Lacroix, G.; Theate, J.; Delille, B.; Frankignoulle, M. Atmospheric CO2 flux from mangrove surrounding waters. Geophys. Res. Lett. 2003, 30, 1558 DOI: 10.1029/ 2003GL017143. (24) Cai, W.-J. Riverine inorganic carbon flux and rate of biological uptake in the Mississippi River plume. Geophys. Res. Lett. 30(2), 1032; doi:10.1029/2002GL016312.

(25) Ito, R. G.; Schneider, B.; Thomas, H. Distribution of surface fCO2 and air−sea fluxes in the Southwestern subtropical Atlantic and adjacent continental shelf. J. Marine Systems 2005, 56, 227−242. (26) Zhai, W. D.; Dai, M. H.; Cai, W.-J.; Wang, Y. C.; Wang, Z. H. High partial pressure of CO2 and its maintaining mechanism in a subtropical estuary: the Pearl River estuary, China. Mar. Chem. 2005, 93, 21−32. (27) Muduli, P. R.; Kanuri, V. V.; Robin, R. S.; Kumar, B. C.; Patra, S.; Raman, A. V.; Rao, N. G.; Subramanian, B. R. Spatio-temporal variation of CO2 emission from Chilika Lake, a tropical coastal lagoon, on the east coast of India. Estuarine, Coastal Shelf Sci. 2012, 113, 305− 313. (28) Maher, D. T.; Eyre, B. D. Carbon budgets for three autotrophic Australian estuaries: Implications for global estimates of the coastal airwater CO2 flux. Global Biogeochem. Cycles 2012, 26, GB1032 DOI: 10.1029/2011GB004075. (29) Frankignoulle, M.; Borges, A. V. Direct and indirect pCO2 measurements in a wide range of pCO2 and salinity values (The Scheldt estuary). Aquat. Geochem. 2001, 7, 267−273. (30) Chen, C. T. A.; Borges, A. V. Reconciling opposing views on carbon cycling in the coastal ocean: Continental shelves as sinks and near-shore ecosystems as sources of atmospheric CO2. Deep Sea Res., Pt. II 2009, 56, 578−590. (31) Borges, A. V.; Delille, B.; Frankignoulle, M. Budgeting sinks and sources of CO2 in the coastal ocean: Diversity of ecosystems counts. Geophys. Res. Lett. 2005, 32, L14601 DOI: 10.1029/2005GL023053. (32) Wanninkhof, R.; Hitchcock, G.; Wiseman, B.; Vargo, G.; Ortner, P. B.; Asher, W.; Ho, D. T.; Schlosser, P.; Dickson, M.-L.; Masserini, R.; Fanning, K.; Zhang, J.-Z. Gas exchange, dispersion, and biological productivity on the west Florida Shelf: Results from a Lagrangian tracer study. Geophys. Res. Lett. 1997, 24, 1767−1770. (33) Ortega, T.; Ponce, R.; Forja, J.; Gómez-Parra, A. Fluxes of dissolved inorganic carbon in three estuarine systems of the Cantabrian Sea (north of Spain). J. Mar. Systems 2005, 53, 125−142. (34) Koné, Y. J. M.; Abril, G.; Kouadio, K. N.; Delille, B.; Borges, A. V. Seasonal variability of carbon dioxide in the rivers and lagoons of Ivory Coast (West Africa). Estuaries Coasts 2009, 32, 246−260. (35) Chen, C. T. A.; Huang, T. H.; Fu, Y. H.; Bai, Y.; He, X. Strong sources of CO2 in upper estuaries become sinks of CO2 in large river plumes. Curr. Opin. Environ. Sustain. 2012, 4, 179−185. (36) Phlips, E. J.; Badylak, S. Spatial variability in phytoplankton standing crop and composition in a shallow inner-shelf lagoon, Florida Bay, Florida. Bull. Mar. Sci. 1996, 58, 203−216. (37) Phlips, E. J.; Badylak, S.; Lynch, T. C. Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon. Limnol. Oceanogr. 1999, 44, 1166− 1175. (38) Brand, L. E.; Pablo, J.; Compton, A.; Hammerschlag, N.; Mash, D. C. Cyanobacterial blooms and the occurrence of the neurotoxin, beta-N-methylamino-L-alamine (BMAA), in South Florida aquatic food webs. Harmful Algae 2010, 9, 620−635. (39) Goleski, J. A.; Koch, F.; Marcoval, M. A.; Wall, C. C.; Jochem, F. J.; Peterson, B. J.; Gobler, C. J. The role of zooplankton grazing and nutrient loading in the occurrence of harmful cyanobacterial blooms in Florida Bay, USA. Estuaries Coasts 2010, 33 (5), 1202−1215. (40) Boyer, J. N.; Fourqurean, J. W.; Jones, R. D. Seasonal and longterm trends in the water quality of Florida Bay (1989−1997). Estuaries 1999, 22, 417−430. (41) Koch, M. S.; Erskine, J. M. Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: interactions with light, salinity and temperature. J. Exp. Mar. Biol. Ecol. 2001, 266, 81−95. (42) Zhang, J.-Z.; Fischer, C. J.; Ortner, P. B. Potential availability of sedimentary phosphorus to sediment resuspension in Florida Bay. Global Biogeochem. Cycles 2004, 18, GB4008 DOI: 10.1029/ 2004GB002255. (43) Zhang, J.-Z.; Huang, X.-L. Relative importance of solid −phase phosphorus and iron in sorption behavior of sediments. Environ. Sci. Technol. 2007, 41 (8), 2789−2795, DOI: 10.1021/es061836q. 9168



Article

(44) Huang, X.-L.; Zhang, J.-Z. Spatial variation in sediment-water exchange of phosphorus in Florida Bay: AMP as a model organic compound. Environ. Sci. Technol. 2010, 44, 7790−7795, DOI: 10.1021/es100057r. (45) Zhang, J.-Z.; Huang, X.-L. Effect of temperature and salinity on phosphate sorption on marine sediments. Environ. Sci. Technol. 2011, 45, 6831−6837, DOI: 10.1021/es200867p. (46) Huang, X.-L.; Zhang, J.-Z. Phosphorus sorption on marine carbonate sediment: Phosphonate as model organic compounds. Chemosphere 2011, 85 (8), 1227−1232, DOI: 10.1016/j.chemosphere.2011.07.016. (47) Millero, F. J.; Hiscock, W. T.; Huang, F.; Roche, M.; Zhang, J.-Z. Seasonal variation of the carbonate system in Florida Bay. Bull. Mar. Sci. 2001, 68, 101−123. (48) Dufore, C. M. Spatial and temporal variations in the air−sea carbon dioxide fluxes of Florida Bay. M.Sc. Thesis, University of South Florida, Tampa, FL, 2012. (49) Guide to best practices for ocean CO2 measurements, PICES Special Publication 3; Dickson, A. G., Sabine, C. L., Christian, J. R., Eds.; Oak Ridge National Laboratory: Oak Ridge, TN, 2007. (50) Millero, F. J.; Zhang, J.-Z.; Fiol, S.; Sotolongo, S.; Roy, R. N.; Lee, K.; Mane, S. The use of buffers to measure the pH of seawater. Mar. Chem. 1993, 44, 143−152. (51) Mosley, L. M.; Husheer, S. L. G.; Hunter, K. A. Spectrophotometric pH measurement in estuaries using thymol blue and m-cresol purple. Mar. Chem. 2004, 91, 175−186. (52) Clayton, T. D.; Byrne, R. H. Spectrophotometric seawater pH measurements: total hydrogen ion concentration scale calibration of m-cresol purple and at-sea results. Deep-Sea Res. 1993, 40, 2115−2129. (53) Mehrbach, C.; Culberson, C. H.; Hawley, J. E.; Pytkowicz, R. M. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol.Oceanogr. 1973, 18, 897− 907. (54) Dickson, A. G.; Millero, F. J. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. DeepSea Res. 1987, 34, 1733−1743. (55) Pierrot, D.; Lewis, E.; Wallace, D. W. R. MS Excel Program Developed for CO2 System Calculations, ORNL/CDIAC-105a; Oak Ridge National Laboratory, Carbon dioxide Information Analysis Center, U.S. Department of Energy: Oak Ridge, TN, 2006. (56) Lewis, E.; Wallace, D. W. R. Program Developed for CO2 System Calculations, ORNL/CDIAC-105; Oak Ridge National Laboratory, Carbon Dioxide Information Analysis Center, U.S. Department of Energy: Oak Ridge, TN. (21pp), 1998. (57) Weiss, R. F. Carbon dioxide in water and seawater: the solubility of a non-ideal gas. Mar. Chem. 1974, 2, 203−215. (58) Wanninkhof, R. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res. 1992, 97 (C5), 7373−7382, DOI: 10.1029/92JC00188. (59) Zhang, J.-Z. The use of pH and buffer intensity to quantify the carbon cycle in the ocean. Mar. Chem. 2000, 70, 121−131. (60) Soetaert, K.; Hofmann, A. F.; Middelburg, J. J.; Meysman, F. J. R.; Greenwood, J. The effect of biogeochemical processes on pH. Mar. Chem. 2007, 105, 30−51. (61) Kelble, C. R.; Johns, E. M.; Nuttle, W. K.; Lee, T. N.; Smith, R. H.; Ortner, P. B. Salinity patterns of Florida Bay. Estuarine, Coastal Shelf Sci. 2007, 71, 318−334. (62) Manzello, D. P.; Enochs, I. C.; Melo, N.; Gledhill, D. K.; Johns, E. M. Ocean acidification refugia of the Florida Reef track. PLoS One 2012, 7 (7), e41715,10 DOI: 10.1371/journal.pone.0041715. (63) Wootton, J. T.; Pfister, C. A.; Forester, J. D. Dynamic patterns and ecoclogical impacts of declining ocean pH in a high-resolution multi-year dataset. Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 18848− 18853. (64) Cai, W.-J.; Hu, X.; Huang, W.-J.; Murrell, M. C.; Lehrter, J. C.; Lohrenz, S. E.; Chou, W.-C.; Zhai, W.; Hollibaugh, J. T.; Wang, Y.; Zhao, P.; Guo, X.; Gundersen, K.; Dai, M.; Gong, G.-C. Acidification of subsurface coastal waters enhanced by eutrophication. Nat. Geosci. 2011, 4, 766−770.

(65) Hunt, C. W.; Salisbury, J. E.; Vandemark, D.; McGillis, W. Contrasting carbon dioxide inputs and exchange in three adjacent New England estuaries. Estuaries Coasts 2011, 34, 68−77. (66) Dai, M.; Lu, Z.; Zhai, W.; Chen, B.; Cao, Z.; Zhou, K.; Cai, W.J.; Chen, C-T. A. Diurnal variations of surface seawater pCO2 in contrasting coastal environments. Limnol. Oceanogr. 2009, 54 (3), 735−745. (67) Zhang, J.-Z.; Wanninkhof, R. H.; Lee, K. Enhanced new production observed from the diurnal cycle of nitrate in an oligotrophic anticyclonic eddy. Geophys. Res. Lett. 2001, 28 (8), 1579−1582. (68) Yates, K. K.; Dufore, C.; Smiley, N.; Jackson, C.; Halley, R. B. Diurnal variation of oxygen and carbonate system parameters in Tampa Bay and Florida Bay. Mar. Chem. 2007, 104, 110−124.

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NOTE ADDED AFTER ASAP PUBLICATION This paper was originally published ASAP on July 29, 2014, with an incorrect version of Figure 2. The correct version was reposted on July 31, 2014.

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