Estuarine, Coastal and Shelf Science xxx (2011) 1e10
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Estuarine, Coastal and Shelf Science
journal homepage: www.elsevier.com/locate/ecss
Effects of upwelling, tides and biological processes on the inorganic carbon
system of a coastal lagoon in Baja California
M. Ribas-Ribas a, J.M. Hernández-Ayón b, *, V.F. Camacho-Ibar b, A. Cabello-Pasini b, A. Mejia-Trejo b,
R. Durazo c, S. Galindo-Bect b, A.J. Souza d, J.M. Forja a, A. Siqueiros-Valencia b
a
Departamento de Química-Física, Facultad de Ciencias del Mar y Ambientales, Universidad de Cádiz, Campus Río San Pedro, s/n, Puerto Real, Cádiz 11510, Spain
Instituto de Investigaciones Oceanológicas, Universidad Autónoma de Baja California, km. 103 carretera Tijuana-Ensenada, Ensenada, Baja California 22860, Mexico
Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, km. 103 carretera Tijuana-Ensenada, Ensenada, Baja California 22860, Mexico
d
Proudman Oceanographic Laboratory, Joseph Proudman Building, 6 Brownlow Street, Liverpool L3 5DA, United Kingdom
b
c
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 18 January 2010
Accepted 29 September 2011
Available online xxx
The role of coastal lagoons and estuaries as sources or sinks of inorganic carbon in upwelling areas has
not been fully understood. During the months of MayeJuly, 2005, we studied the dissolved inorganic
carbon system in a coastal lagoon of northwestern Mexico during the strongest period of upwelling
events. Along the bay, different scenarios were observed for the distributions of pH, dissolved inorganic
carbon (DIC) and apparent oxygen utilization (AOU) as a result of different combinations of upwelling
intensity and tidal amplitude. DIC concentrations in the outer part of the bay were controlled by mixing
processes. At the inner part of the bay DIC was as low as 1800 mmol kg1, most likely due to high water
residence times and seagrass CO2 uptake. It is estimated that 85% of San Quintín Bay, at the oceanic end,
acted as a source of CO2 to the atmosphere due to the inflow of CO2-rich upwelled waters from the
neighboring ocean with high positive fluxes higher than 30 mmol C m2 d1. In contrast, there was a net
uptake of CO2 and HCO
3 by the seagrass bed Zostera marina in the inner part of the bay, so the pCO2 in
this zone was below the equilibrium value and slightly negative CO2 fluxes of 6 mmol C m2 d1. Our
positive NEP and DDIC values indicate that Bahía San Quintín was a net autotrophic system during the
upwelling season during 2005.
Ó 2011 Elsevier Ltd. All rights reserved.
Keywords:
Dissolved Inorganic carbon
pCO2
coastal upwelling
seagrass
Baja California
1. Introduction
Coastal waters represent 8% of the global ocean and about 25% of
marine primary production (Walsh, 1989; Wollast, 1991). However,
the role of coastal zones as sinks or sources of CO2 is still not fully
understood (Smith and Hollibaugh, 1997; Borges, 2005; Borges
et al., 2005), resulting in an underestimation of global carbon
budgets (Wollast, 1991). Given the high variability in short temporal
and spatial scales in the coastal oceans (Borges and Frankignoulle,
1999; Borges and Frankignoulle, 2002; Hales et al., 2008; Zhai and
Dai, 2009; de la Paz et al., 2010; Ribas-Ribas et al., 2011) a better
description of the CO2 system in these regions is required. The large
observed ranges in coastal ocean surface pCO2 exceed the dynamic
range observed in the open-ocean, and can occur under spatial
scales as small as a few kilometers and over temporal scales of just
hours (Friederich et al., 2002; Hales et al., 2005).
* Corresponding author.
E-mail address: [email protected] (J.M. Hernández-Ayón).
There is a lack of information on airewater CO2 fluxes in coastal
ecosystems such as lagoons, where the few studies of carbon
cycling have focused solely on the ecosystem metabolism (e.g.,
Carmouze et al., 1998; McGlathery et al., 2001; Hung and Hung,
2003). Moreover, very few studies have addressed CO2 cycling in
lagoons (Hernández-Ayón et al., 2007a; Koné et al., 2009). In the
coastal lagoons located along the northwestern shores of Baja
California, Mexico, the ocean is the most important external source
of nutrients, organic and inorganic carbon (Hernández-Ayón et al.,
2004; Camacho-Ibar et al., 2007; Hernández-Ayón et al., 2007a).
Recurrent upwelling events provide nutrient-rich and high CO2
levels to the coastal zone throughout the year. The semi-diurnal
tides, ranging between 1.0 and 2.4 m, play a key role in these
systems as they force new upwelled water into the embayment.
While the importance of upwelled water as a source of inorganic
carbon to the coast is being studied in coastal zones, few studies
evaluate the fate of this inorganic carbon within the coastal lagoons
(Camacho-Ibar et al., 2007; Hernández-Ayón et al., 2007a).
The objective of this study is to evaluate the role of upwelling
and tides as sources of inorganic carbon to a coastal lagoon, and to
0272-7714/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ecss.2011.09.017
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
2
M. Ribas-Ribas et al. / Estuarine, Coastal and Shelf Science xxx (2011) 1e10
understand the subsequent biogeochemical changes to the inorganic carbon system.
2. Materials and methods
2.1. Study site
San Quintín Bay is a coastal lagoon located in the northwestern
coast of the Peninsula of Baja California, Mexico (30 270 N,
116 000 W, Fig. 1). This embayment covers an area of approximately
42 km2 and has a permanent connection with the open-ocean
through a narrow south-facing mouth. San Quintín Bay is a y-shaped coastal lagoon with an eastern arm known as brazo San Quintín
and a western arm known as Bahía Falsa. Brazo San Quintín covers
an area of 15 km2 while Bahía Falsa covers an area of 9 km2. The
mean depth of San Quintín Bay is approximately 2 m but has
a navigation channel with a maximum depth of 7 m that runs
through both arms. This coastal lagoon is a net evaporative
hypersaline system throughout the year. San Quintín Bay is also
considered a well mixed system as no significant physicochemical
vertical gradients are observed through most of the bay (MillanNuñez et al., 1982). The neighboring ocean, under the influence of
the California Current, is a typical wind-driven coastal upwelling
system. The typical period of upwelling in the region is from April
to August. The seagrass Zostera marina is the dominant macrophyte
covering approximately 40% of San Quintín Bay surface (Ward et al.,
2003), however, dense patches of the macroalga Ulva spp. are
observed near the mouth during the upwelling season (ZertucheGonzález et al., 2009).
In order to assess the spatial variability in the inorganic carbon
system, San Quintín Bay was divided into four sectors: “openocean” (stations 1e3), mouth (stations 4e8), brazo San Quintín
(stations 9e14) and Bahía Falsa (stations 15e20) (Fig. 1).
2.2. Field sampling and analysis
Thermographs (HOBO, Onsetcomputers, USA) were anchored at
the mouth and at the heads of brazo San Quintín and Bahía Falsa
(stations 3, 12 and 18, respectively, Fig. 1) and seawater temperature
was recorded every 10 min from May 27 to July 8, 2005.
The upwelling index for coastal waters off San Quintín Bay was
calculated for the sampling period from QuikSCAT wind data. Tidal
height was obtained based on predictions from the program MAR
V0.7 (http://oceanografia.cicese.mx/predmar/), and water residence time was calculated with a three-box model as described for
San Quintín Bay by Camacho-Ibar et al. (2003).
Water samples were collected at 20 stations in May and July of
2005 (Fig. 1). The salinity of the samples was determined using
a salinometer (AUTOSAL Guildline) while the dissolved inorganic
carbon (DIC) was analyzed using a SOMMA SYSTEM as described by
Johnson et al. (1987). Seawater certified reference materials (CRM)
supplied by A. Dickson from the Scripps Institution of
Fig. 1. San Quintin Bay with its different areas: mouth of the bay, Bahía Falsa (BF) and brazo San Quintín (bSQ). Numbers indicate sampling stations during summer 2005 and
sediments cores in 2008. The thermographs were anchored at stations 3, 12 and 18.
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
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Oceanography were used for calibration every 10 samples. Total
alkalinity (TA) was determined potentiometrically using a 0.1 M
HCl solution dissolved in 0.6 M NaCl. The HCl solution was calibrated against a CRM. After the titration, data were processed as
described by Dickson et al. (2003). The values of TA and DIC were
normalized against salinity, using the salinity average of 33.81
(n ¼ 42) for most samples from the open-ocean stations (St. 1, 2 and
3; Fig. 1). Surface seawater temperature, dissolved oxygen,
chlorophyll-a concentration and pH were monitored using a flowthrough (Data-Flow IV) system throughout the bay. The oxygen
probe of the Data-Flow IV was calibrated on a daily basis, following
the manufacturer’s recommendation for the 100% oxygen saturation point, by exposing the tip of the probe to water-saturated air at
100%. The WETStar fluorometer for chlorophyll-a determinations
with the Data-Flow IV system was calibrated by the manufacturer
(WET Labs Inc., Philomath, OR, USA) prior to the field campaign. The
Scale Factor provided by the manufacturer was used for the
conversion of the fluorescence response into chlorophylla concentration. A previous exercise whereby fluorescence was
measured in situ with the Data-Flow IV, and chlorophyll-a was
determined in discrete samples in the laboratory, showed that in
situ measurements are a good semi-quantitative indicator of
chlorophyll-a concentrations (regression analyses of laboratory
chlorophyll-a against in situ fluorescence showed statistically
significant r2 values ranging from 0.23 to 0.74). The pH scale is the
total hydrogen ion concentration scale. The pH electrode was calibrated against standard seawater buffers at salinity of 35 and
trishydroxymethylaminomethane (Del Valls and Dickson, 1998;
Dickson et al., 2007). The magnitude of the error involved in
using a salinity 35 buffer for most oceanic measurements in the
salinity range 33e37 was less than 0.005 in pH (Dickson et al.,
2007). Partial pressure of seawater CO2 (pCO2) was calculated
using the program CO2sys developed by Lewis and Wallace (1998)
and using the constants proposed by Mehrbach et al. (1973). The
accuracy of the pCO2 values computed from the pHeDIC couple was
less than 10 matm. The accuracy of the AUTOSAL Guildline 8400B
salinometer was better than 0.002. The Apparent Oxygen Utilization (AOU), defined as the deviation of the measured dissolved
oxygen from an O2 concentration in equilibrium with the atmosphere (calculated from the Benson and Krause (1984) solubility
equation) was also calculated.
In order to have a qualitative estimate of the role of sedimentary
particulate inorganic carbon in surface sediments on CO2 fluxes in
the lagoon, this variable was determined in sediment samples
collected from May 20 to 23, 2008 in all the stations (Fig. 1), except
in stations 1 and 2, using a PVC pipe adapted with a check valve. The
first 5 mm were collected and stored in plastic bags at 4 C, then
dried at w40 C. Subsamples without acid treatment were
measured for total carbon, and subsamples acidified with 10% HCl
were measured for organic carbon using an elemental analyzer
LECO CHNS-932. Particulate inorganic carbon in sediments was
then calculated by subtracting organic carbon from total carbon.
2.3. Flux calculations
Airewater fluxes of CO2 were calculated according to:
F ¼ akΔpCO2, where a is the solubility coefficient of CO2 (Weiss,
1974), k is the gas transfer velocity of CO2 and ΔpCO2 is
the airewater gradient of pCO2. The atmospheric pCO2 data used
was 380 matm and was obtained from average of the monthly data
from May, June and July 2005 at Pacific Ocean station (30.0 N;
135.00 W), taken from National Oceanic and Atmospheric
Administration (NOAA/CMDL/CCGG air sampling network) data
available online at http://www.esrl.noaa.gov/gmd/dv/ftpdata.html.
Wind velocity obtained from QuikSCAT was used to determine the
3
magnitude of the airewater CO2 flux. The flux computation was
carried out using daily bins of wind speed (assuming that the all the
sub-regions of the lagoon are uniformly submitted to wind speed
measured anywhere during the survey).
We computed k using the parameterization given by
Wanninkhof and McGillis (1999) using short-term winds:
k ¼ 0:0283u310 ðSc =660Þ1=2
The value “u10” is the wind speed at a height of 10 m and “Sc” is
the Schmidt number calculated according to the relationship
proposed by Wanninkhof (1992).
2.4. Whole system metabolism using the LOICZ budgeting
procedure
Biogeochemical modeling according to Gordon et al. (1996) was
used to estimate non-conservative fluxes of DIC (DDIC), using a 1box and a 4-box model of the Bahía San Quintín system,
following the procedure for nutrient budgets described in
Camacho-Ibar et al. (2003). Net ecosystem production (NEP) was
also computed from the non-conservative fluxes of DIC, however, as
DDIC values are attributed not only to the difference between
production and mineralization of organic matter, but also to net
CO2 exchanges with the atmosphere (DDICg) and precipitation and
dissolution of CaCO3 (DDICc), NEP is estimated as follows:
NEP ¼ DDIC DDICg DDICc
(Gordon et al., 1996). As, to our knowledge, no information on
precipitation and dissolution of CaCO3 is available for San Quintín
bay, this process was assumed negligible (DDICc ¼ 0) in the present
study.
2.5. Statistical analysis
Temporal and spatial differences in hydrological and biogeochemical characteristics were analyzed using one-way analysis of
variance (ANOVA) followed by the Bonferroni post hoc test (Statgraphics Plus 5.1). The threshold value for statistical difference was
taken as p < 0.05.
3. Results
The upwelling index off San Quintín Bay varied between 0 and
200 m3 s1 (100 m)1 during the sampling period (Fig. 2A), with
maximum upwelling index values and minimum temperatures
occurring on May 30e31, June 6, June 10 and June 18 (Fig. 2C, F).
A period of persistent high upwelling index values and low
temperatures, however, was observed from June 18 to July 6. The
minimum upwelling index values were observed between June 12
and 17. The maximum tidal range at San Quintín Bay was approximately 240 cm during the sampling period (Fig. 2B). Maximum
upwelling index values coincided or nearly coincided with spring
tides and with the lowest temperatures (see June 20e27). Sample
collection dates occurred during three spring tides (June 7 and 24,
and July 6) and three neap tides (May 31, June 15 and 31, Fig. 2B).
Throughout the study period seawater temperatures were more
than 5 C lower at the mouth of San Quintín Bay than at the heads of
Bahía Falsa and brazo San Quintín (Fig. 2C, F). Temperatures at the
mouth and heads of the bay were lowest during spring tides and
highest during neap tides. Fig. 2DeG shows DIC, AOU, temperature
and pCO2 plotted as daily values from station 1, 20 and 26 from the
mouth, the heads of brazo San Quintín and Bahía Falsa respectively.
When considering temperature as an upwelling indicator for the
open-ocean stations, DIC, AOU and pCO2 display predictable trends.
In the mouth of the bay, low DIC values (<2050 mmol kg1), low
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
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M. Ribas-Ribas et al. / Estuarine, Coastal and Shelf Science xxx (2011) 1e10
Fig. 2. A) Upwelling index evolution (m3 s1 (100 m)1) during the study period; B) Tide (cm) in the coastal area of San Quintin Bay; Time evolution of average daily data of C)
partial pressure of CO2 (matm); D) Dissolved inorganic carbon (mmol kg1); E) Apparent oxygen utilization (mmol kg1); and F) temperature ( C) at the mouth (solid line), Bahía Balsa
(broken line) and brazo San Quintín (dotted line).
AOU values (<30 mmol kg1), and low pCO2 values (<500 matm),
coincide with high temperatures (low upwelling indices) while high
DIC values (>2170 mmol kg1), high AOU values (>90 mmol kg1),
and high pCO2 values (>700 matm), coincide with low temperatures
(intense upwelling). Throughout the study period seawater DIC
concentrations were approximately 150e40 mmol kg1 higher at
the mouth of San Quintín Bay than at the heads of brazo San Quintín
and Bahía Falsa respectively (Fig. 2D), AOU values were approximately 100e50 mmol kg1 higher (Fig. 2E) and pCO2 values were
approximately 400e150 matm higher (Fig. 2G).
Additionally, there were variations in the average water residence times for the mouth of the bay, Bahía Falsa and brazo San
Quintín throughout the study period. The average water residence
time for the mouth was 1 day, 5 days for Bahía Falsa and 16 days for
brazo San Quintín. The average residence time for the whole San
Quintín Bay was w12 days.
Salinity increased from the mouth of the bay toward the heads
of brazo San Quintín and Bahía Falsa (Fig. 3A). While the increase
for salinity in Bahía Falsa was approximately 0.5 (8e12 km), there
was an increase of three units in brazo San Quintín. Dissolved
inorganic carbon showed contrasting patterns between brazo San
Quintín and Bahía Falsa (Fig. 3C). In brazo San Quintín, DIC values
decreased from approximately 2150 mmol kg1 in the open-ocean
to approximately 1900 mmol kg1 at the head. In contrast, DIC
values in Bahía Falsa remained relatively similar to those observed
in the open-ocean (2100 mmol kg1). In addition, DIC normalized by
salinity (NDIC) in brazo San Quintín decreased toward the head,
suggesting for this area an evaporation effect in DIC measurements
(Fig. 3D). However, brazo San Quintín showed a larger decrease in
NDIC than in DIC. Apparent oxygen utilization decreased from
w70 mmol kg1 at the mouth to w55 mmol kg1 at the brazo San
Quintín head, and 30 mmol kg1 at the Bahía Falsa Bahía head
(Fig. 3E). pCO2 decreased from 750 matm at the mouth to 230 matm
at the brazo San Quintín, and w400 matm at the Bahía Falsa head
(Fig. 3F). The average pH value increased from 7.7 at the mouth to
8.2 at the head of brazo San Quintín, and 7.9 at the head of Bahía
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
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Fig. 3. Spatial distribution of A) salinity; B) temperature ( C); C) Dissolved inorganic carbon (mmol kg1); D) Normalized dissolved inorganic carbon (mmol kg1); E) Apparent
oxygen utilization (mmol kg1); F) partial pressure of CO2 (matm); G) pH; and H) Chlorophyll-a (mg m3) along transects from the ocean to the inner parts of brazo San Quintín and
Bahía Falsa.
Falsa (Fig. 3G). Chlorophyll-concentrations decreased from
5.0 mg m3 at the mouth to 2.5 mg m3 at the brazo San Quintín
head and 3.5 mg m3 at the Bahía Falsa head (Fig. 3H).
The plots in Fig. 4 show DIC, AOU, pCO2, pH, chlorophyll-a and TA
plotted against salinity. Dissolved inorganic carbon decreased linearly (r2 ¼ 0.65) as salinity increased in San Quintín Bay (Fig. 4A).
Maximum values of DIC (2200 mmol kg1) were found at salinities
lower than 34 while the lowest DIC values were observed in samples
with salinities above 36. The lowest DIC values and highest salinities
corresponded to samples from brazo San Quintín. There was also
a decrease in AOU as salinity increased at San Quintín Bay (Fig. 4B).
Highest AOU values were observed in samples from the mouth of the
bay with salinities below 34. Values of AOU were intermediate at
Bahía Falsa and AOU levels decreased significantly toward the head
of brazo San Quintín. Values of pCO2 decreased from highest values
(<1000 matm) at salinities below 34 to minimum pCO2 values
(<200 matm) with salinities above 37 (Fig. 4C). Values of pH
increased from lowest values (w7.6) at salinities below 34 to
maximum pH values (8.3) with salinities above 37 (Fig. 4D). The
lowest pCO2 and highest pH and salinities corresponded to samples
from brazo San Quintín. Chlorophyll-a had an exponential decrease
as salinity increased at San Quintín Bay (Fig. 4E), although a high
variability of this parameter was observed in open-ocean stations.
Maximum chlorophyll-a levels (10.0 mg m3) were observed when
salinities were below 34 and decreased to approximately
2.5 mg m3 when salinities increased above 35 at brazo San Quintín.
TA was well correlated to salinity (Fig. 4F) for stations from the
mouth of the Bay and Bahía Falsa. This suggests that CaCO3 precipitation/dissolution rates were too low and/or water residence time
too short and/or the water volume too large to significantly affect
surface water TA values around oyster cultures. The same fact was
observed by Gazeau et al. (2005) in Palma Bay. However, in brazo San
Quintín more dispersion was observed.
The relative variation of NTA versus NDIC is an indicator of
dominant biogeochemical processes affecting directly or indirectly
these quantities. Other studies (Borges et al., 2003; Koné and Borges,
2008) have used the slope of this relationship to identify processes:
areobic respiration, sulfate reduction, calcium carbonate dissolution, manganese reduction and iron reduction with theoretical
values of 0.2, 0.99, 2.0, 4.0 and 8.0 respectively. In brazo San
Quintín, NTA and NDIC were well correlated (r2 ¼ 0.83 of the linear
regression) with a slope of 0.36 (Fig. 5). The value of the slope was
lower than sulfate reduction and it was more than five times lower
than CaCO3. This suggests that inorganic carbon uptake and
airewater exchange of CO2 also strongly contributed to the variation
of DIC in the water column. As we will detail later, the uptake of
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
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Fig. 4. Mixing diagrams for A) dissolved inorganic carbon (mmol kg1); B) apparent oxygen utilization (mmol kg1); C) partial pressure of CO2 (matm); D) pH; E) and D) Chlorophylla (mg m3); and F) total alkalinity (mmol kg1) in San Quintin Bay. Black circles represent the mouth of the bay, dark gray squares Bahía Falsa and pale gray triangles brazo San
Quintín. The dotted line in A) represents the conservative mixing line.
HCO
3 by Zostera marina in brazo San Quintín could explain why DIC
and TA decrease simultaneously. However, in our study samples
were collected only during high tides, therefore, the possibility
exists that we have only seen part of the process considering that
this area has a lot of Z. marina and seagrass. Results from a Brazilian
mangrove highlight the effect in the chemical properties during the
ebb and at low tide due to influx of porewater (Ovalle et al., 1990).
On the other hand, the correlation between NTA and NDIC in the
mouth of the bay and Bahía Falsa was relatively low (r2 ¼ 0.40), as in
both areas the relation showed little variability at around
2300 mmol kg1 and 2100 mmol kg1 respectively. The range of
variation was much smaller in these areas because of the short
residence time of the water (Fig. 5). However, a negative slope was
observed (0.19) in the regression line for these areas, indicating
that small DIC changes can be related to processes like aerobic
respiration and airewater exchange of CO2 in the water column.
Airewater CO2 fluxes showed differing values throughout San
Quintín Bay (Fig. 6). Stations located close to the mouth (stations 1e6)
showed the highest positive flux values (w40 mmol C m2 d1). In
Bahía Falsa also positive fluxes were estimated, but the fluxes were
two- to-three-fold lower than at the mouth (w14 mmol C m2 d1).
In contrast, stations at the head of brazo San Quintín (stations 12e14)
had negative flux values (w6 mmol C m2 d1) on this small area.
DDIC values in Bahía San Quintín were negative during
upwelling (Fig. 7) indicating a net consumption of inorganic carbon
within the system. If carbonate precipitation/dissolution related to
calcifying organism activity (e.g., such as cultured oysters in the
western arm of the bay) does not contribute significantly to internal
DIC biogeochemical fluxes, then this DIC decrease results mainly
from carbon uptake by primary producers such as Zostera marina,
Ulva spp., and phytoplankton (Camacho-Ibar et al., 2007), and also
by CO2 degassing. The carbonate content in the sediments, ranging
from 0 to 1.2%, suggests that inorganic carbon precipitation/dissolution may be negligible.
4. Discussion
Upwelling occurs at the coastal shelf adjacent to San Quintín Bay
and tides are responsible for transporting upwelled water into this
coastal lagoon (Zaytsev et al., 2003). Consequently, the penetration
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
M. Ribas-Ribas et al. / Estuarine, Coastal and Shelf Science xxx (2011) 1e10
Fig. 5. Relation between normalized dissolved inorganic carbon and normalized total
alkalinity along the bay. Black circles represent the mouth of the bay, dark gray squares
Bahía Falsa and pale gray triangles brazo San Quintín.
of upwelled water into the arms of San Quintín Bay varied
according to the combination of upwelling intensity and tidal
amplitude. For example, when strong upwelling events coincided
with spring tides from June 19 to 24, cold water with high CO2 and
high pCO2 (Fig. 2) was transported 15 km into brazo San Quintín, as
indicated by the DIC values at brazo San Quintín approaching those
near the mouth (Fig. 2D). On the other hand, when weak upwelling
coincided with neap tides, as was observed from June 16 to 18,
relatively high temperatures were observed at the mouth and the
rest of the bay while DIC depleted waters were observed
throughout the bay because of the longer water residence time
(Fig. 2D).
DIC distributions along the bay depend not only on upwelling
intensity and tidal conditions (residence time) but also on biological processes. Due to its low water residence times (w2 days) the
CO2 system at the mouth of San Quintín Bay is highly dynamic.
Here, the pulses of cold, low pH and rich DIC, high pCO2 water
during upwelling were evident. In addition, the high chlorophylla values indicate that high phytoplankton biomass were common,
developing just off the bay and being pumped into this area
(Camacho-Ibar et al., 2003; Zertuche-González et al., 2009).
DIC and chlorophyll-a values in Bahía Falsa were slightly lower and
Fig. 6. Airewater CO2 fluxes (mmol C m2 d1) along transects from the ocean to the
inner parts of the bay. Dotted line represents the equilibrium.
7
Fig. 7. Non-conservative fluxes of DIC (DDIC) using a 1-box and a 4-box model, and Net
ecosystem production (NEP) computed from fluxes of DIC. DDIC and NEP estimates
with positive values indicate that Bahía San Quintín was a net autotrophic system
during the upwelling season in 2005.
pH was slightly higher than at the mouth because water exchange
with the open-ocean is limited resulting in residence times w5
days (Camacho-Ibar et al., 2003). Brazo San Quintín shows a contrasting scenario, mainly because the longer residence times (w16
days) allow for a larger modification of water mass properties. For
example a decrease of DIC, pCO2 and chlorophyll-a and an increase
of pH was observed in most of the inner section of brazo San
Quintín regardless of the upwelling intensity for both neap and
spring tides. Like DIC, a decrease in inorganic nitrogen concentration from the mouth of the Bay to brazo San Quintín has also been
reported (Camacho-Ibar et al., 2003; Hernández-Ayón et al.,
2007a).
The relationship between DIC and salinity has been used to
identify processes that can affect the inorganic carbon distribution
(Fig. 4A). If a conservative linear relationship is obtained between
DIC and salinity then mixing would be the most important factor
controlling DIC distribution. However, if other processes are
removing or adding carbon, values would fall out of the conservative mixing line. The mixing diagram shows that at salinities >34
there is a negative trend of DIC concentrations, with values below
the conservative mixing line by more than 200e300 mmol kg1 for
brazo San Quintín and Bahía Falsa. This behavior was reported
previously from a preliminary study by Hernández-Ayón et al.
(2007a) and is similar to that reported by Camacho-Ibar et al.
(2003) for nitrate distributions, suggesting that the nonconservative behavior of DIC in San Quintín Bay during the
upwelling season suggests carbon uptake by biological processes,
mostly by macrophytes at the inner arms.
DIC values for Bahía Falsa were below but not as far from the
conservative mixing line as they were for brazo San Quintín
(Fig. 4A). In order to distinguish different processes affecting the
inorganic carbon system such as exchange of CO2 with atmosphere,
dissolution/precipitation of CaCO3 and photosynthesis-respiration,
we compared the relative variation of NTA vs NDIC (Fig. 5). The
analysis shows different trends for the three zones: the oceanic
area showed high NDIC (>2150 mmol kg1) due to upwelling, but
with some lower values w2000 mmol kg1 because of degasification and photosynthesis. In Bahía Falsa, NDIC was lower than at
the mouth, with maximum values of 2100 mmol kg1 and lower
values of 1950 mmol kg1, also attributed to degasification and
uptake of carbon by photosynthesis. As mentioned before, the
residence time for Bahía Falsa is five days, so mixing is an important
process controlling DIC concentrations. However it is important to
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
8
M. Ribas-Ribas et al. / Estuarine, Coastal and Shelf Science xxx (2011) 1e10
note that Bahía Falsa is an area where oyster aquaculture is an
activity covering approximately 30% of the area, thus carbonate
precipitation and dissolution are expected to occur in; because of
its short residence time, however, it is difficult to measure DIC
changes related to any of these processes. On the other hand,
although NTA increased by 30 mmol kg1 in this region, carbonate
dissolution does not explain such increment as a corresponding DIC
increase. An explanation for this NTA increase, could be the
contribution of organic bases from microalgae to the titration
alkalinity in coastal seawaters (Hernández-Ayón et al., 2007b) plus
the alkalinity addition because NO3 uptake 1:1 stoichiometry
between N uptake and alkalinity change (Brewer and Goldman,
1976). The average NO
3 concentration in open-ocean stations (St.
1e3) was 12.1 mM and the uptake of NO
3 in Bahía Falsa was about
9 mM. So, this value could be part of the 30 mmol kg1 increase
observed in Bahía Falsa.
In the inner part of brazo San Quintín, NDIC decreased by
550 mmol kg1 relative to the mouth whereas NTA decreased by
250 mmol kg1. This type of trend is often attributed to carbonate
precipitation (Zeebe and Wolf-Gladrow, 2001); however, our
results indicate no evidence of carbonate-rich sediments or
calcareous macroalgae in the area. We suggest this decreases are
due to biological carbon uptake processes. Brazo San Quintín is an
area with high residence time where not only the highest DIC
depletion was observed but also AOU concentrations with negative
values and pH measurements greater than 8.0 (Fig. 4B, D). These
observations indicate that in this area of San Quintín Bay the effects
of photosynthesis on DIC dynamics are stronger. As chlorophylla concentration was approximately 2.0 mg m3 in this zone
(Fig. 4E), we assume that phytoplankton was not responsible for
this pattern. In contrast, dense seagrass meadows of Zostera marina
are present in brazo San Quintín (Ward et al., 2004), being the most
important primary producer in this area. Some studies indicate that
under CO2 limitation conditions, Z. marina is a macrophyte able to
uptake bicarbonate by the enzyme carbonic anhydrase and by the
proton pump mechanism (Beer and Rehnberg, 1997; Delille et al.,
2000; Hemminga and Duarte, 2000). Carr and Axelsson (2008)
found that major portion of ATP spent by Z. marina for the gener
ation of acid zones involves HCO
3 utilization. The uptake of HCO3
by Z. marina in brazo San Quintín could explain why DIC and TA
decrease simultaneously since bicarbonate is a major component of
both parameters of the CO2 system. Another explanation could be
the coralline epiphyte algae covering Z. marina (Saunders et al.,
2003; Johnson et al., 2005). These epiphytes calcify leading to
strong fluxes of DIC and TA. The growth of epiphyte flora and faune
of Posidonia oceanica has been reported by Barrón et al. (2006).
These two processes have also been proposed by Delille et al.
(2000) to explain removal of CO2
3 and/or HCO3 in Macrocystis
kelp beds.
The role of the bay as a source or sink of carbon during the
upwelling season is spatially and temporally variable. In the mouth,
near the source of upwelled water, the bay is expected to be
a source of CO2 because water transported from depths of 75 m to
100 m is rich in DIC and pCO2 (Lara-Espinoza, 2007). High pCO2
values induce positive fluxes from the ocean to the atmosphere for
this area during the upwelling season and throughout most of the
bay during spring tides. During this study, positive fluxes of CO2
were found in more than 85% of the bay (Fig. 6).
The most notable characteristic of the upwelling system in the
mouth of San Quintin is that average sea surface pCO2 was about
twice the atmospheric value at the time of the observations
(380 matm) and an average flux value of 50 mmol C m2 d1. We
compare the airewater CO2 fluxes and pCO2 values at stations 1e3
with data in other coastal upwelling systems. The Peruvian
upwelling system was found to be a source of CO2 to the
atmosphere during all seasons (Friederich et al., 2008). They found
pCO2 data in the continental shelf ranged from w150 ppm to
w1500 ppm. The spatially normalized annual flux estimate obtained in this study was 5.7 mol m2 y1 (15.6 mmol m2 d1). This
value is lower than our calculated flux but it should be taken into
account that our study took place during strong upwelling season.
If we averaged maximal value (that usually correspond with high
upwelling index) reported by them (53.3 mmol m2 d1) a better
agreement is found with our data. When an annual study was done,
smaller or even opposite fluxes would be expected. The central
California upwelling system act as a sink of CO2 (0.3
to 0.7 mol m2 y1) during El Niño period but as a source of CO2
during La Niña period (1.5e2.2 mol m2 y1), thus, strong interannual variability should be expected in upwelling regions
(Friederich et al., 2002). In contrast, the pCO2 values over the
continental shelf off the Galician coast range between 265 and
415 matm during upwelling season and thus continental shelf areas
is net sink of CO2 during the upwelling season in the range of 2.3
(0.6) to 4.7 (1.0) mmol C m2 d1 (Borges and Frankignoulle,
2002). González-Dávila et al. (2009) concluded that coastal
upwelling regions may act as sinks of CO2, due to carbon
consumption by photosynthesis, counteracting the physical
processes. However, they found latitude difference, with the
northern zone characterized by seasonal upwelling acted as a slight
source of CO2 with a value ranged from 0.4 to 0.3 mol m2 y1
(w0.9 mmol C m2 d1). This annual value is one order of magnitude lower than our value for the mouth stations.
Although the strongest positive fluxes were registered in the
mouth during the strongest upwelling events, high positive values
were also observed in the inner bay as waters oversaturated with
CO2 were transported by the tidal motion. The only exception was
at the inner of brazo San Quintín which showed slightly negative
CO2 fluxes due to DIC removal by seagrasses. It has been reported
that areas with dense seagrass beds have a strong effect on the
aquatic biogeochemistry, including intense O2 production and CO2
uptake thus being net sinks of CO2 (Gazeau et al., 2005; Barrón
et al., 2006; Bouillon et al., 2007). The average estimation for CO2
fluxes for the entire bay was þ8.4 mmol C m2 d1, a value that fits
within the results reported by Chen and Borges (2009) for other
coastal lagoons but it is lower than other near-shore coastal
ecosystems such as macrotidal estuaries (118 mmol C m2 d1),
mangrove surrounding waters (51 mmol C m2 d1), and salt marsh
surrounding waters (64 mmol C m2 d1) compiled by Borges
(2005). This value is also lower than the average values of
44 mmol C m2 d1 reported in lagoons of Ivory Coast (Koné et al.,
2009), which are influenced by river discharge. These authors
pointed out that some lagoons are connected to the sea by much
deeper channels and therefore had wave and tidal action from the
ocean. This fact implies finally than those lagoons were more
oversaturated than the ocean restricted lagoons. With the results of
this study, it is concluded that San Quintín Bay acts as a source of
CO2 during upwelling events. Unfortunately, we only did a couple of
transects during non-upwelling season (September 2004),
however the average for CO2 fluxes for the entire bay using this data
was þ0.64 mmol C m2 d1. Based on this information, the bay acts
also as a source of CO2 to the atmosphere when non-upwelling
season.
Our NEP estimates (Fig. 7) and DDIC with positive values
indicate that Bahía San Quintín was a net autotrophic system
during the upwelling season from 2005. Based on mid to late
summer observations, it was previously reported that San Quintín
Bay is a net heterotrophic system, due to imports of labile
phytoplanktonic carbon generated in the adjacent ocean during
upwelling (Camacho-Ibar et al., 2003). Based on observations of
nutrient dynamics during the upwelling seasons of 2004 and 2005
Please cite this article in press as: Ribas-Ribas, M., et al., Effects of upwelling, tides and biological processes on the inorganic carbon system of
a coastal lagoon in Baja California, Estuarine, Coastal and Shelf Science (2011), doi:10.1016/j.ecss.2011.09.017
M. Ribas-Ribas et al. / Estuarine, Coastal and Shelf Science xxx (2011) 1e10
(Camacho-Ibar et al., in preparation) we suggest that this apparent
contradiction can be explained based on a dependence of NEP in
San Quintín Bay on upwelling conditions, including intensity and
persistence. In 2005, upwelling was not only intense but highly
persistent (Fig. 2), supplying large amounts of dissolved inorganic
nutrients to a N-limited community of primary producers, and
relatively low amounts of phytoplankton from the adjacent ocean
to fuel ecosystem respiration. In order to have significant phytoplankton blooms in shelf waters of this upwelling region,
upwelling events have to alternate with relaxation periods of at
least 4e5 days to allow for phytoplankton biomass build up
(Wilkerson et al., 2006). This is evidenced by the near to zero
value of NEP during June 17 (i.e., the system in the way of
switching from net autotrophic to net heterotrophic), which
coincided with the only significant relaxation period during our
study. The overall trend of increasing NEP toward the beginning of
July reflects the overall trend of upwelling intensification during
our sampling campaign.
Acknowledgments
This work was financed by the Secretaria de Educación PúblicaConsejo Nacional de Ciencia y Tecnología 2002 40144 (México) and
a FPU grant to MRR (AP2005-4791) of the Ministerio de Educación
(Spain). El Aula Universitaria Iberoamericana at Universidad de
Cádiz provided traveling financial support to MRR. Thanks to Xosé
Álvarez-Salgado for his constructive comments, to Lorena PoncelaRodríguez for her help in the graphics edition and Eduardo Ortiz for
carbon analysis. The comments from one anonymous reviewer
improved the Manuscript, thanks very much.
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