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Total and new production in the Gulf of California estimated from ocean color data from the satellite sensor SeaWIFS
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Deep-Sea Research II 51 (2004) 739–752
Total and new production in the Gulf of California estimated from ocean color data from the satellite sensor SeaWIFS ! Alvarez-Borrego* Raquel M. Hidalgo-Gonza! lez, Saul ! de Oceanolog!ıa, CICESE, Km. 107 Carretera Tij-Ens, Ensenada, BC, Mexico Division Received 10 February 2003; accepted 3 May 2004 Available online 3 August 2004
Abstract Integrated total (PTint) and new production (Pnewint) (g C m2 d1) were calculated for the Gulf of California with semi-analytical models from the literature, using chlorophyll a concentrations (Chlsat) and the vertical attenuation coefficients of light (K490) from monthly composites of the satellite sensor SeaWIFS (1997–2002). The phytoplankton biomass vertical distribution associated with Chlsat, and the vertical distribution of the f-ratio (f(z)=Pnew(z)/PT(z)), were deduced from historic oceanographic data. The year was divided into two seasons: cool and warm. Values for PTint had a large seasonal variation (e.g., 1.16–1.91 for the cool season, and 0.39–0.49 for the warm season). Values for Pnewint for the cool season increased from the entrance region to the big islands region and then it remained the same from there to the northern Gulf, with values up to twice as large in the two latter regions (up to 1.33 g C m2 d1) with respect to those of the entrance (up to 0.48). Values of Pnewint for the warm season were less than half those of the cool season (0.25– 0.31). In spite of the limited data, a clear interannual PTint variability is evident for the entrance region, with lowest values for the 1997–1999 ENSO event. This kind of variation was also present for the central Gulf, but the effect was much weaker due to its strong dynamics. r 2004 Elsevier Ltd. All rights reserved.
1. Introduction Oceanic total primary production (PT) has two components: new and regenerated production (PT=Pnew+Pr). New production (Pnew) is the fraction of total primary production that is supported by external or ‘‘new’’ input of nutrients (Dugdale and Goering, 1967). Phytoplankton cells use nutrients recycled within the euphotic zone for *Corresponding author. CICESE, P.O. Box 434844, San Diego, CA 92143–4844, USA. Fax: +1-52-646-175-1545. E-mail address: [email protected] (S. Alvarez-Borrego).
regenerated production (Pr). Eppley and Peterson (1979) assumed that Pnew is quantitatively equivalent to the organic matter that can be exported from the total production in the euphotic zone without the production system running down. These latter authors defined the ratio of Pnew to PT as the f-ratio (f=Pnew/PT) and showed that f was an asymptotic function of the magnitude of total production. The processes of fixation of inorganic carbon in organic matter during photosynthesis, its transformation by trophodynamics, physical mixing, transport and gravitational settling are referred to
0967-0645/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2004.05.006
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collectively as the ‘‘biological pump’’ (Ducklow et al., 2001). The ratio of sinking flux to primary production (e-ratio) and the f-ratio vary as functions of the pathways by which nitrogen flows among different organisms (phytoplankton, large and small grazers and bacteria), but the only way to change the absolute amount of export is to change Pnew, which is usually controlled by physical factors (Frost, 1984). Thus, the description of the temporal and spatial variability of Pnew may give us an idea of the variability of the flux of organic matter out of the surface layer. Measuring PT and Pnew with bottle incubation experiments using compounds labelled with 14C and 15N, respectively, has been the basic methodology to generate direct estimates. But it is very time consuming and yields very limited data with low temporal and spatial coverage. The alternative is to make indirect estimates of PT and Pnew. For example, Dugdale et al. (1989), Sathyendranath et al. (1991), and Alvarez-Salgado et al. (2002) used remotely sensed temperature and color to estimate PT and Pnew. The Gulf of California is a very productive and dynamic sea with strong seasonal and interannual variations (Alvarez-Borrego and Lara-Lara, 1991; Alvarez-Borrego, 2002). However, 14C incubations have provided a very limited view of the temporal and spatial variation of the Gulf’s total primary production, and there are no reports on Pnew for the Gulf of California. Satellite ocean-color data give us the opportunity to generate a more complete description of the Gulf’s PT and Pnew variability. Remote sensors provide information on the photosynthetic pigment concentration for the upper 22% of the euphotic zone. To model primary production in the water column from satellite-derived photosynthetic pigments, estimates of the vertical distribution of pigment concentration are required. The assumption of a mixed layer with a homogeneous pigment distribution could lead to inaccurate estimates of integrated primary production (Platt et al., 1991). The deep chlorophyll maximum (DCM) is a consistent feature in the ocean (Dandonneau, 1979; Cullen and Eppley, 1981). Generally, accounting for its presence increases estimates of
integrated production, and since the DCM often appears below the mixed layer, it would seem likely that most of its production is new production (Sathyendranath et al., 1995). A difficulty in estimating oceanic production from surface measurements arises from the regional differences in the vertical distribution of Chl. Following Lewis et al. (1983) and Platt et al. (1988), HidalgoGonza! lez and Alvarez-Borrego (2001) used chlorophyll concentration (Chl(z)) historical data to fit a Gaussian distribution function to represent the pigment vertical profile for different seasons and regions within the Gulf of California. The objective of this work is to quantify the spatial and temporal variation of PT and Pnew for the Gulf of California. To accomplish this, we used SeaWIFS imagery, the Gaussian vertical distribution of Chl(z) as proposed by HidalgoGonza! lez and Alvarez-Borrego (2001) for seasons and regions within the Gulf, and the average photosynthetic parameters proposed by ValdezHolgu!ın et al. (1999) for the whole Gulf. The Gulf of California has clear impacts from interannual events such as El Nin˜o-La Nin˜a cycles (Santamar!ıa-Del-Angel et al., 1994).
2. Study area The Gulf of California is very dynamic because of tidal currents, wind stress, upwelling, and high solar heating. It consists of a series of basins separated by sills. The basins have depths up to >3000 m at the entrance region, and they are very shallow in the northern Gulf (p200 m). Marked seasonal changes of temperature, salinity, currents, and sea level have been reported for the central Gulf of California (Ripa and Marinone, 1989; Soto-Mardones et al., 1999). However, information about the spatial and temporal variability of chemical and biological processes is scarce. Upwelling occurs off the eastern coast with northwesterly winds (‘‘winter’’ conditions from December to May), and off the Baja California coast with southeasterly winds (‘‘summer’’ conditions from July to October), with June and November as transition periods (Alvarez-Borrego and Lara-Lara, 1991). This wind cycle in the Gulf
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of California is called the Mexican monsoon (Douglas et al., 1993). With northwesterly winds upwelling is strong, it has a marked effect on phytoplankton communities (Chls values up to more than 10 mg m3), and due to eddy circulation it increases the phytoplankton biomass across the Gulf (Santamar!ıa-Del-Angel et al., 1994). However, because of strong stratification during summer, upwelling with southeasterly winds has a very weak effect on phytoplankton biomass (Santamar!ıa-Del-Angel et al., 1999). The northern Gulf of California exhibits spectacular tidal phenomena. With a range of >7 m during spring tides in the upper Gulf and >4 m in ! and Angel de la the big islands area (Tiburon Guarda), tidal energy dissipation rates are great. In the upper Gulf tidal energy dissipation rates are as large as >0.5 W m2, and in the big islands area they are >0.3 W m2 (Argote et al., 1995). The lowest surface temperatures of the whole Gulf of California are found here (Soto-Mardones et al., 1999). Tidal mixing over the sill between San Lorenzo and San Esteban islands produces a vigorous stirring of the water column down to >500 m depth (Simpson et al., 1994). Tidal mixing in the big islands area causes a net effect of carrying cold and nutrient-rich waters to the surface throughout the whole year (AlvarezBorrego, 2002). This produces patches of high Chl (up to >2 mg m3) in this area even during summer.
3. Data and methods Platt et al.’s (1991) non-spectral model with inhomogeneous biomass profile was used to estimate total primary production for each depth in case-II waters (Chl>1.5 mg m3) ¼ ½P Chl a PAR P TðzÞ
mðzÞ
ðzÞ
PARðzÞ
ðzÞ
Þ2 0:5 ½ðPmðzÞ Þ2 þ ðPARðzÞ aPAR ðzÞ ðmg C m3 h1 Þ; where PAR is the photosynthetically active radia is the assimilation number (mg C mg tion, Pm 1 1 Chl h ), and aPAR is the initial slope (mg C mg Chl1 h1 (mmol quanta m2 s1)1) of the
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photosynthesis–irradiance relationship (P–E curves). A modification to this model proposed by Giles-Guzma! n and Alvarez-Borrego (2000) was used for case 1 waters (Chlo1.5 mg m3) f Chl a% PTðzÞ ¼ ½PmðzÞ ðzÞ phðz;ChlÞ PARðzÞ max ½ð0:02315P Þ2 þ ðPAR a% mðzÞ
ðzÞ phðz;ChlÞ fmax Þ
2 0:5
:
This modification is a spectral model with inhomogeneous biomass profile and corrects the ) by the in situ spectral distribuinitial slope (aPAR tion of scalar PAR. Instead of aPAR in the Platt et al. (1991) expression, we used 43:2fmax a% phðz;ChlÞ (Giles-Guzma! n and Alvarez-Borrego, 2000). The maximum photosynthetic quantum yield at low irradiance (mol C (mol quanta)1) is fmax. The average specific absorption coefficient of phyto2 1 plankton is a% ph(z,Chl) (m mg Chl ), weighted by the in situ spectral distribution of PAR and calculated following Giles-Guzma! n and AlvarezBorrego (2000). The factor 43.2 converts mol C to mg C, seconds to hours, and mol quanta to mmol quanta. These expressions show that to estimate primary production we need not only the surface Chl value but also the vertical profiles of Chl and PAR. To define the chlorophyll vertical profile, Hidalgo-Gonza! lez and Alvarez-Borrego (2001) proposed to divide the year into two periods. The cool season is the period end of November– end of June, and the rest of the year is considered the warm season. They also proposed dividing the Gulf into four regions for the cool season and into two regions for the warm season (Fig. 1). SeaWIFS monthly composites of Chlsat and K490 with a spatial resolution of B9 km for the period September 1997–September 2002 were used to obtain representative averages for the seasons and regions of the Gulf. The Chlsat and K490 means were obtained from each season composite and for each Gulf region using the program Windows Image Manager (WIM), developed by Kahru, Scripps Institution of Oceanography, La Jolla. As a first approximation, we can represent Chlsat by the Chl(z) average for the first optical depth, weighted by the irradiance attenuated twice (when the light is going down and when it is backscattered up) (Kirk, 1994). For the available Gulf of California in situ Chl data, the Chl(z) weighted
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(a)
(b)
Fig. 1. Regions of the Gulf of California: (a) for the cool season; and (b) for the warm season.
average for the first optical depth is about 10% higher than the surface Chl (Chls), thus Chls =0.9 Chlsat (Hidalgo-Gonza! lez and Alvarez-Borrego (2001). Surface scalar PAR (PARz=0+) was estimated with the Bedford Institute of Oceanography (Halifax, Canada) program available through Internet at http://www.amigo.bio.dfo.ca. This program uses latitude, longitude, year, and Julian day. A representative mean geographic location
was chosen for each region within the Gulf, then PAR was obtained for each Julian day, and an average PAR was calculated for each region and season. Following Morel and Maritorena (2001), this value was multiplied by 0.965 to estimate PAR immediately under the sea surface (PARz=0). The PAR profile (PAR(z)) for case-I waters was calculated following Giles-Guzma! n and AlvarezBorrego (2000), with a variable KPAR (KPAR(z)) calculated with the Chl profile and taking into
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account the variation of the spectral distribution of light with depth. Average Chls was o1.5 mg m3 in all of our cases, but due to the deep Chl maximum in some cases Chl(z) was >1.5 mg m3. In those cases, the PAR profile for the near surface waters (with Chlo1.5 mg m3) was calculated following Giles-Guzma! n and Alvarez-Borrego (2000), and the PAR profile for deeper waters (with Chl>1.5 mg m3) was calculated with the Lambert–Beer law and an average vertical attenuation coefficient, KPAR, deduced from the satellite K490 average value. The regression models proposed by Cervantes-Duarte et al. (2000) (ZPAR1%=A+B/K490) were used to estimate the euphotic zone depth (ZPAR1%) as a function of K490 in each case, and KPAR was estimated (KPAR=4.6/ZPAR1%,). The regression parameters A and B have different values for different regions within the Gulf. Valdez-Holgu!ın et al. (1999) proposed the following working averages for the photosynthetic parameters for the whole Gulf of California and for the cool season (7 one standard error): a surface Pmax = 9.672.4 mg C mg Chl1 h1, with a linear variation between this and 3.770.3 at the middle of the euphotic zone, and then a constant value for deeper waters; a single value of =0.02970.004 mg C mg Chl1 h1 (mmol ainc quanta m2 s1)1 (incubator’s initial slope); and fmax=0.0670.01 mol C (mol quanta)1. And for =3.770.3, with a the warm season: a surface Pmax linear variation between this and 1.570.2 at the middle of the euphotic zone, and another linear variation between the latter and 0.470.1 at the bottom of the euphotic zone; a surface =0.01370.001, with a linear variation between ainc this and 0.001 at the bottom of the euphotic zone; and a single value fmax= 0.01470.002. Taking into consideration the spectral distribution of light in Valdez-Holgu!ın et al.’s (1999) incubator and following Giles-Guzma! n and Alvarez-Borrego ¼ 1:2a : In (2000), for surface waters ainsitu inc case-II waters, aðZÞ tends to maintain the value that corresponds to the spectral distribution of PAR at the surface. This is due to the strong absorption of both red and short-wavelength light because of the abundance of pigments, detritus and color-dissolved organic matter. Thus, we used
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Platt et al.’s (1991) non-spectral model to estimate primary production for case-II waters, without any correction of aðZÞ for the spectral distribution of light at depth. We used NO3 data from 268 hydrographic stations sampled in oceanographic cruises from 1973 to 1993 to generate average NO3 profiles for each season and region of the Gulf. In all cases NO3 was determined by the spectrophotometric method following Strickland and Parsons (1972). Unfortunately, there are no newer NO3 available data for the Gulf. Harrison et al.’s (1987) expression was used to calculate the f-ratio for each depth (f(z)=fmax[1-exp(-mNO3(z)/fmax)]). Unfortunately, there are no reports on the f(z)–NO3(z) relationship for the Gulf of California. Thus, we chose the parameters m and fmax as reported by Harrison et al. (1987) for oceanographic conditions similar to those found in the Gulf. For the cool season we chose m=0.98 and fmax=0.77, which correspond to the coastal upwelling Peruvian zone, and for the warm season we chose m=12.1 and fmax=0.64, which correspond to the summer oligotrophic intrusion of the Southern California Bight. A sensitivity analysis was performed to assess the effect of uncertainties of variables and parameters on the estimates of average integrated total production for the whole euphotic zone and for the whole day (PTint) (g C m2 d1 or ton C km2 d1). One standard error (s n0.5) was added and subtracted to each input variable and parameter, one at a time, to assess the effect on PTint, and the difference was expressed as percentage. Due to the covariation of the photosynthetic ; a parameters (PmðZÞ PARðZÞ ; and fmax) (i.e., Cote and Platt, 1983; Valdez-Holgu!ın et al., 1999), when adding or subtracting one standard error we did it for all of them at the same time. It was not possible to do a sensitivity analysis with the uncertainties associated with KPAR(z) calculated for case-I waters following Giles-Guzma! n and Alvarez-Borrego (2000) because these latter authors did not provide values for the standard errors associated to their equations. They only mentioned that when comparing 30 PTint values estimated with calculated PAR profiles with the corresponding values estimated with measured profiles, the mean of the
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percent differences was 5.9%. But, as they indicated, PAR profiles that resulted from the model were smooth, whereas those that resulted from measurements in some cases had abrupt changes in the PAR vertical variation rate. Thus, possibly, most of the differences between measured and calculated PAR are due to errors in the measured PAR values. Also, a sensitivity analysis was done to assess the effect of the f-ratio uncertainties on estimates of integrated new production (Pnewint) (g C m2 d1 or ton C km2 d1).
4. Results The high number of pixels allowed for a relatively small standard error for Chls and K490, about 74% in both cases. Average Chls values for the cool season had a clear interannual variation, with lower values in 1997–1998 than during the other winters, in all regions of the Gulf (Table 1). This is the effect of an El Nin˜o event, and it is more evident in region I, the entrance to the Gulf, where it can also be seen in 1998–1999. During the cool seasons of 1997–1998 and 1998–1999 there was a Chls gradient with values increasing from south-to-north. During the other cool seasons (1999–2000, 2000–2001, and 2001–2002) there was no clear south-north gradient. During the warm
season, Chls average values for the whole Gulf were similar to those for the entrance region during the cool season and with an El Nin˜o event. In general, average K490 values were minimal for the southernmost regions (I and 1) and maximal for the big islands region (III). There was a slight tendency for higher K490 average values during the cool season than those for the warm season, but there was no clear interannual variation (Table 1). As expected, average incident PAR(z=0+) had a clear seasonal change and decreased from southto-north, but its interannual variation was not significant (not illustrated). The absolute values of the standard error for NO3 were similar for different depths, regions and seasons (most of them between 0.2 and 0.4 mM), but the relative values changed from B20% at low-NO3 values to B3% at high values (Fig. 2). In general, average surface and near-surface NO3 values increase from the entrance region to the interior of the Gulf, up to the big islands region (III), and then they decrease a little from there to the north (region IV) (Fig. 2). The nutricline is up to 40 m deeper at the entrance to the Gulf (regions I and 1) than in the internal regions, with relatively low-NO3 values from the surface down to 60 m during the cool season. The shallowest nutriclines were those of regions III and IV, with the highest average surface NO3 values in the big islands region (III).
Table 1 Satellite-derived average values for seasons and regions in the Gulf of California of surface chlorophyll (Chls=0.9 Chlsat mg m3) and light-attenuation coefficient (K490 m1). The standard error (s n0..5) for both variables is B4% in all cases Years
I
II
III
IV
Years
1
2
Chls (mg m )
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.36 0.48 0.92 0.86 0.83
0.48 0.66 0.77 0.98 0.81
0.45 0.69 0.83 0.69 0.79
0.70 0.88 0.89 1.15 0.96
1997 1998 1999 2000 2001 2002
0.30 0.24 0.41 0.55 0.46 0.43
0.42 0.37 0.43 0.45 0.42 0.41
K490 (m1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.06 0.10 0.11 0.10 0.09
0.11 0.13 0.15 0.18 0.16
0.16 0.15 0.20 0.19 0.18
0.13 0.17 0.16 0.17 0.16
1997 1998 1999 2000 2001 2002
0.07 0.06 0.08 0.10 0.08 0.09
0.13 0.12 0.12 0.12 0.15 0.14
3
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Fig. 2. Average NO3 profiles for the seasons and regions in the Gulf of California as shown in Fig. 1. Horizontal bars represent 7 one standard error (s n0.5).
Total production, PT(z), had maxima at shallower depths than those of the Chl(z) maxima (Fig. 3) due to greater PAR(z) near the surface. On the other hand, PT(z) maxima were often in subsurface waters due to the relatively low-surface Chl(z) values. With relatively high surface Chl, maximum PT(z) was at the surface, such as in region IV, where the deep chlorophyll maximum was at B20 m. Pnew maxima had the same depths as those of PT(z) maxima. Production of the deep Chl maximum, both PT and Pnew, was relatively low compared to that of near-surface waters due to low-light levels at the former (Fig. 3). Greatest uncertainties of the estimates for average integrated total production for the whole euphotic zone and for the whole day (PTint) (g C m2 d1 or ton C km2 d1) are due to uncertainties in the photosynthetic parameters. When augmenting or diminishing the photosynthetic parameters by one standard error, PTint changed as much as 17% with low Chls, and as much as 19% with high Chls. This is due to the few degrees of freedom in the P–E parameters. Since we are using single average values for the whole Gulf, these large intervals do not affect the comparisons of PTint between regions, but it does affect the comparisons between seasons and years. When changing Chls by one standard error, PTint changed only p2%, and when changing K490 by one standard error, PTint changed B2.7%. The probability of having all these errors added
together simultaneously is low due to the multiplication rule. Average integrated total production (PTint) shows a regular annual cycle as the dominant feature of these time series while the interannual changes were usually of smaller magnitude (Table 2). During the cool season, the effect of El Nin˜o 1997–1998 can be appreciated throughout the whole Gulf, with lower values of PTint than during the other cool seasons. However, the most intense effect of El Nin˜o, and possibly the only significant one, was recorded for the entrance region. During the warm season there was no clear El Nin˜o effect in any region of the Gulf. Even at the entrance to the Gulf, changes of PTint due to the seasonal cycle were more intense than the interannual changes due to El Nin˜o. At the entrance to the Gulf, during the cool season, El Nin˜o reduced PTint down to B65% with respect to non-El Nin˜o years. During non-El Nin˜o years PTint for the warm season was reduced down to B20% with respect to that for the cool season. On the other hand, there was no south–north PTint significant gradient, for any particular season. The PTint range for the whole Gulf was 1.16–1.91 g C m2 d1 for the cool season, and it was 0.39–0.49 for the warm season. The f-ratio estimates did not change significantly when changing the NO3 profiles by one standard error. Thus, uncertainties in the new production estimates are only those associated to uncertainties of total production.
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Fig. 3. Examples of the average chlorophyll, total primary production, and new production profiles for regions I and IV in the Gulf of California.
Average integrated new production for the euphotic zone (Pnewint) (g C m2 d1 or ton C km2 d1) increased from the entrance region
(I) to the big islands region (III) and then it was practically the same in region IV as in region III, during the cool seasons (Table 3), with values up
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Table 2 Satellite-derived integrated total primary production (PTint) per unit area ( g C m2 d1 or ton C km2 d1) and for whole regions in the Gulf of California (ton C d1) I
II
III
IV
Year
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
1.16 1.20 1.85 1.80 1.78
5.8 104 6.0 104 9.3 104 9.0 104 8.9 105
1.52 1.67 1.74 1.91 1.87
9.0 104 9.8 104 10.3 104 11.3 104 11.0 104
1.45 1.60 1.73 1.62 1.66
3.1 104 3.5 104 3.7 104 3.5 104 3.6 104
1.52 1.60 1.60 1.68 1.65
2.6 104 2.7 104 2.7 104 2.8 104 2.8 104
1
2
Year
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
1997 1998 1999 2000 2001 2002
0.42 0.39 0.43 0.49 0.48 0.47
4.6 104 4.3 104 4.7 104 5.3 104 5.2 104 5.1 104
0.43 0.42 0.45 0.44 0.43 0.43
0.93 104 0.91 104 0.97 104 0.95 104 0.93 104 0.93 104
to more than double in regions III and IV (up to 1.33 g C m2 d1) with respect to those of region I (up to 0.48 gC m2 d1). However, there was no clear south–north Pnewint gradient during the warm season. Again, the dominant temporal change was the seasonal cycle. We could not detect any significant effect of the El Nin˜o event on the Pnewint average values for the cool or the warm season. The Pnewint range for the whole Gulf was 0.38–1.33 g C m2 d1 for the cool season, and it was 0.25–0.31 g C m2 d1 for the warm season.
5. Discussion Total and new oceanic production calculated from remotely sensed data on ocean color, which depends on parameterizations developed from ship observations, yield more representative estimates of the large-scale average production than those calculated from ship data alone (Sathyendranath et al., 1991). Morel and Berthon (1989) indicated that it is unreasonable and probably superfluous to envisage the use of a light-production model on a
pixel-by-pixel basis when interpreting satellite imagery. Our objective was to obtain representative average production values for whole seasons and regions within the Gulf of California. Rigorous comparison of the satellite-derived time series of PTint with results from 14C incubations is difficult due to the different time and space characteristics of these measurements (Balch and Byrne, 1994). Nevertheless, it is interesting to compare both kinds of data. Alvarez-Borrego and Lara-Lara (1991) reported 26 14C-derived PTint point values for region II with an average of 1.43 g C m2 d1, compared with our range of 1.52–1.87; they reported 12 values for region III with an average of 2.1 g C m2 d1, compared with our range of 1.45–1.73; and they reported four values for region IV with a mean of 1.1 g C m2 d1 compared with our range of 1.52–1.68. These latter authors only reported five point values for the warm season and for the whole Gulf, which do not allow for comparisons. In spite of great differences in time and space scales, both methods provide average values that are very close, and given the uncertainties of our satellite-derived estimates,
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Table 3 Satellite-derived integrated new primary production (Pnewint) per unit area ( g C m2 d1 or ton C km2 d1) and for whole regions in the Gulf of California (ton C d1) I
II
III
IV
Year
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.38 0.39 0.48 0.46 0.38
2.2 104 2.3 104 2.9 104 2.7 104 2.2 104
0.71 0.75 0.75 0.81 0.79
4.2 104 4.4 104 4.4 104 4.8 104 4.7 104
1.11 1.22 1.33 1.29 1.31
2.4 104 2.6 104 2.9 104 2.8 104 2.8 104
1.16 1.22 1.26 1.29 1.25
1.95 104 2.05 104 2.07 104 2.17 104 2.10 104
1
2
Year
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
1997 1998 1999 2000 2001 2002
0.27 0.25 0.27 0.31 0.29 0.27
3.2 104 2.8 104 3.0 104 3.4 104 3.2 104 3.0 104
0.28 0.28 0.30 0.28 0.27 0.27
0.62 104 0.62 104 0.66 104 0.62 104 0.60 104 0.60 104
these differences are not significant. Kahru and Mitchell (2002) compared their satellite-derived primary productions for the California Current with 14C measurements and reported that the first overestimate the second by about 40%. In our case satellite estimates do not systematically over or underestimate PTint. In spite of possible errors, ocean-color satellite imagery are very consistent; their seasonal cycles and the spatial variation within the Gulf of California behave very much as expected according to physical phenomena such as the movement of water masses and the occurrence of upwelling. Trees et al. (2000) reported that, despite the various sampling periods and numerous geographic locations, there are consistent patterns in the ratios of the log accessory pigments to log total Chl (Chl a, Chl a allomer, Chl a epimer, and chlorophyllide a), and there is a strong log-linear relationship for these ratios. These latter authors indicated that this log-linearity largely explains the success in remotely sensed Chl algorithms, even though phytoplankton populations can vary in their composition and suite of pigments. The large
number of pixels within each of our Gulf of California regions allowed for relatively small Chl and K490 standard errors. The vertical distribution of model-derived primary production is also very consistent and behaves as expected from 14C experiments. The largest contribution to production is from the surface and near-surface waters (i.e., the upper 15 m), with a relatively small contribution from the deep Chl maximum (Fig. 3). This agrees with ! et al., 2000). reports in the literature (i.e. Maran˜on For the purpose of defining regions to apply primary production models to satellite color data, the larger the regions the better. For example, for the purpose of modeling production, ValdezHolgu!ın et al. (1999) proposed means of photosynthetic parameters (from P–E curves) for the whole Gulf of California as a single region. Sathyendranath et al. (1995) indicated that most boundaries between biogeochemical regions prove to have some significance for the depth of the chlorophyll maximum. That is the case for our Gulf of California regions. The Gulf of California has a spectrum of physical dynamics that affect the
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vertical distribution of phytoplankton biomass in different ways, so that it has to be divided into relatively small geographic regions. The underlying assumption of a Gaussian distribution function is that for a given region of the ocean, in a given season, the typical shape of the chlorophyll profile is stable. Gaussian biomass profiles derived for different regions of the Gulf, and with the same Chl surface value, produce different integrated production values (HidalgoGonza! lez and Alvarez-Borrego, 2001). The effect of nutrient concentrations is not explicit in our primary production models because it is implicit in Chl. Nutrients control phytoplankton biomass but have a very weak effect on photosynthetic parameters (Cullen et al., 1992). Nutrient concentrations have an explicit effect on the estimates of Pnew(z) through the f-ratio values. However, since there are no data to document the effect of El Nin˜o–La Nin˜a cycles on the nutrients of the Gulf of California, it is not possible to describe the temporal change of NO3, and our fratio values used to calculate Pnew(z) are constant with time. The strong warm season depletion of primary production in the Gulf is due to the invasion of the equatorial surface water (ESW). This warm surface water, up to >30 C, causes a very strong water-column stratification, greatly decreasing the effect of summer upwelling on the phytoplankton biomass (Santamar!ıa-Del-Angel et al., 1999) and on primary production. The energy required to move a parcel of water from 100 m to the surface during summer is 5–15 times that for winter (Corte! s-Lara et al., 1999). Our results suggest that the summer intrusion of the ESW into the Gulf of California produces every year an effect on primary production stronger than that of an El Nin˜o event with winter conditions. Watts et al. (1999) measured Pnew for the northwestern Indian Ocean using 15N stableisotope, tracer techniques, and found that both the integrated f-ratio (Pnewint/PTint) and Pnewint were larger during the monsoon, with ranges of 0.10–0.96, and 0.04–3.66 g C m2 d1, respectively, and lower during the intermonsoon, with ranges of 0.07–0.52, and 0.05–0.65 g C m2 d1, respectively. This was due to upwelling and greater wind-
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induced vertical mixing during the monsoon. Their average integrated f-ratio and Pnewint for the monsoon, and for the whole northwestern Indian Ocean, were 0.60 and 1.55 g C m2 d1, respectively. These averages are close to those for the cool season of the northern Gulf of California regions. Liu et al. (2002) used a monsoon-forced model to describe the temporal and spatial variability of chlorophyll and primary production in the South China Sea (SCS), and found good agreement with data derived from SeaWIFS. In the SCS there are also two peaks of primary production, with the strongest during the winter monsoon, a weaker peak during the summer monsoon, and low production during the two inter-monsoon periods. Highest winter monsoon PTint values reported for the SCS by Liu et al. (2002) were between similar and 80% of the PTint warm season values for the entrance to the Gulf of California (region 1), and they were only B16% of the Gulf’s cool season values for non-El Nin˜o years. Based on a 6-year time series of sediment trap samples, Thunell (1998a) documented the seasonal and interannual changes in particles fluxes in Guaymas basin, at the northern part of region II. Sedimentation in this region of the Gulf of California is dominated by two seasonally varying components: biogenic silica during the late fallspring (cool season) and lithogenic material during the summer (warm season), this forms laminated diatomaceous sediments, and a couplet of laminae constitute a varve deposited in a year (Calvert, 1966). These varves in the central Gulf of California are formed where the basin slopes intersect the oxygen minimum in the water column. The seasonal variability in sediment fluxes described by Thunell (1998a) is a direct response to the reversing monsoon climate in the Gulf. The Gulf’s strong seasonal variability of Pnewint, with values up to more than double for the cool season with respect to those of the warm season, is in accordance with the seasonal variability of particle fluxes reported by Thunell (1998a). Thunell (1998b) reported that for the Santa Barbara basin, a coastal upwelling zone off southern California, export ratios are inversely related to total primary production, and this is due to increased advective
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transport during the highly productive upwelling season. This is not the case for the Gulf of California because it is a semienclosed sea with eddy circulation across the whole Gulf. It is not possible to describe interannual changes properly with only 5 years of data in our time series. However, it is interesting to notice that in the Gulf of California there was practically no interannual variation of PTint and Pnewint from warm to warm season in the period 1997–2002, but the physical forcing of large temporal and spatial scales affected the Gulf’s production during the cool seasons. There was a clear El Nin˜o effect on Chls and primary production mainly at the entrance to the Gulf but also evident throughout the whole Gulf during the 1997–1998 cool season. This effect was also present during 1998–1999 but only for the entrance region. At the entrance region, primary production decreased down to B65% during 1997–1998 with respect to their values in the cool seasons of 2000–2001 and 2001– 2002. Santamar!ıa-Del-Angel et al. (1994) described a similar El Nin˜o effect on Chlsat during the winters of 1982–1983 and 1983–1984 using ocean color data from the Coastal Zone Color Scanner. These latter authors reported a dramatic suppression of Chlsat at the entrance to the Gulf during El Nin˜o 1982–1983, with values down to B20% of those for non-El Nin˜o years, but with a relatively small impact in the big islands and northern regions. This was very consistent with Mee et al.’s (1985) Chl (1979–1983) time series obtained for a location at the mouth of the Gulf 30 km from the eastern coast, which showed that Chl values for winter dropped from B10 mg m3 during non-El Nin˜o years to o2 mg m3 in 1983. Santamar!ıaDel-Angel et al. (1994) concluded that the sequence of El Nin˜o and non-El Nin˜o events do not affect the phytoplankton assemblages in all regions of the Gulf of California in the same manner. Our results confirm this conclusion. In some areas of the Gulf, such as the big islands region and the northern Gulf, local physical phenomena causes strong turbulence as described above, reducing the effect of El Nin˜o. Based on his particle flux data, Thunell (1998b) indicated that production in the Santa Barbara basin is reduced during ENSO events. Thunell
(1998a) also observed interannual differences in the magnitude of sediment fluxes in Guaymas basin (region II), indicating that they appear to be related to El Nin˜o events, and he speculated that there might be higher primary production during non-El Nin˜o years. Our limited data show that for region II there was a PTint reduction of up to 15% during the 1997–1998 El Nin˜o, and although these reductions are not very dramatic and may not be significant, they are in agreement with Thunell’s (1998a) findings. The largest interannual change of our time series is for region I, with a PTint reduction of up to 35% during an El Nin˜o year, but no sediment flux has been reported for this region of the Gulf.
Acknowledgements We thank Dr. Trevor Platt and Dr. Charles C. Trees for their constructive comments and criticisms to an earlier version of this manuscript. We are very grateful to the National Council of Science and Technology of Mexico (CONACYT) for supporting the project J002/750/00C-834/00. J. M. Dominguez and F. Ponce did the artwork.
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Hidalgo-Gonz!alez, R.M., Alvarez-Borrego, S., 2001. Chlorophyll profiles and the water column structure in the Gulf of California. Oceanologica Acta 24, 19–28. Kahru, M., Mitchell, B.G., 2002. Influence of the El Nin˜o–La Nin˜a cycle on satellite-derived primary production in the California Current. Geophysical Research Letters 29, 2045–2050. Kirk, J.T.O., 1994. Light and photosynthesis in aquatic ecosystems. Cambridge University Press, New York, 509p. Lewis, M.R., Cullen, J.J., Platt, T., 1983. Phytoplankton and thermal structure in the upper ocean: consequences of nonuniformity in chlorophyll profile. Journal of Geophysical Research 88, 2565–2570. Liu, K.-K., Chao, S.-Y., Shaw, P.-T., Gong, G.-C., Wang, D.P., Olson, D.B., 2002. Monsoon-forced chlorophyll distribution and primary production in the South China Sea: observations and a numerical study. Deep-Sea Research I 49, 1387–1412. ! E., Holligan, P.M., Varela, M., Mourin˜o, B., Bale, Maran˜on, A.J., 2000. Basin-scale variability of phytoplankton biomass, production and growth in the Atlantic Ocean. DeepSea Research I 47, 825–857. Mee, L.D., Ram!ırez-Flores, A., Flores-Verdugo, F., Gonz!alezFar!ıas, F., 1985. Coastal upwelling and fertility of the southern Gulf of California: impact of the 1982–1983 ENSO event. Tropical Ocean and Atmosphere Newsletter, vol. 31, University of Miami, Miami, FL, pp. 9–10. Morel, A., Berthon, J.F., 1989. Surface pigment algal biomass profiles and potential production of the euphotic layer: relationships reinvestigated in view of remote sensing applications. Limnology and Oceanography 34, 1572–1586. Morel, A., Maritorena, S., 2001. Bio-optical properties of oceanic waters: a reappraisal. Journal of Geophysical Research 106, 7163–7180. Platt, T., Sathyendranath, S., Caverhill, C.M., Lewis, M.R., 1988. Ocean primary production and available light: further algorithms for remote sensing. Deep-Sea Research I 35, 855–879. Platt, T., Caverhill, C.M., Sathyendranath, S., 1991. Basin-scale estimates of oceanic primary production by remote sensing: the North Atlantic. Journal of Geophysical Research 96, 15147–15159. Ripa, P., Marinone, S.G., 1989. Seasonal variability of temperature, salinity, velocity, vorticity and sea level in the central Gulf of California, as inferred from historical data. Quaternary Journal of the Royal Meteorological Society 115, 887–913. Santamar!ıa-Del-Angel, E., Alvarez-Borrego, S., Muller-Karger, . F.E., 1994. The 1982–1984 El Nin˜o in the Gulf of California as seen in coastal zone color scanner imagery. Journal of Geophysical Research 99, 7423–7431. Santamar!ıa-Del-Angel, E., Alvarez-Borrego, S., Mill!an-Nun˜ez, R., Muller-Karger, F.E., 1999. Sobre el efecto de las ! surgencias de verano en la biomasa fitoplanctonica del Golfo de California. Revista de la Sociedad Mexicana de Historia Natural 49, 207–212.
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Sathyendranath, S., Platt, T., Horne, E.P.W., Harrison, W.G., Ulloa, O., Outerbridge, R., Hoepffner, N., 1991. Estimation of new production in the ocean by compound remote sensing. Nature 353, 129–133. Sathyendranath, S., Longhurst, A., Caverhill, C.M., Platt, T., 1995. Regionally and seasonally differentiated primary production in the North Atlantic. Deep-Sea Research I 42, 1773–1802. Simpson, J.H., Souza, A.J., Lavin, M.F., 1994. Tidal mixing in the Gulf of California. In: Beven, K.J., Chatwin, P.C., Millbank, J.H. (Eds.), Mixing and Transport in the Environment. Wiley, London, pp. 169–182. Soto-Mardones, L., Marinone, S.G., Par!es-Sierra, A., 1999. Time and spatial variability of sea surface temperature in the Gulf of California. Ciencias Marinas 25, 1–30. Strickland, J.D.H., Parsons, T.R., 1972. A Practical Handbook of Seawater Analysis. Bulletin of the Fisheries Research Board of Canada 167.
Thunell, R.C., 1998a. Seasonal and annual variability in particle fluxes in the Gulf of California: a response to climate forcing. Deep-Sea Research I 45, 2059–2083. Thunell, R.C., 1998b. Particle fluxes in a coastal upwelling zone: sediment trap results from Santa Barbara Basin, California. Deep-Sea Research I 45, 1863–1884. Trees, C.C., Clark, D.K., Bidigare, R.R., Ondrusek, M.E., Mueller, J.L., 2000. Accessory pigments versus chlorophyll a concentrations within the euphotic zone: A ubiquitous relationship. Limnology and Oceanography 45, 1130–1143. Valdez-Holgu!ın, J.E., Alvarez-Borrego, S., Trees, C.C., 1999. Seasonal and spatial characterization of the Gulf of California phytoplankton photosynthetic parameters. Ciencias Marinas 25, 445–467. Watts, L.J., Sathyendranath, S., Caverhill, C.M., Maass, H., Platt, T., Owens, N.J.P., 1999. Modelling new production in the northwest Indian Ocean region. Marine Ecology Progress Series 183, 1–12.
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Total and new production in the Gulf of California estimated from ocean color data from the satellite sensor SeaWIFS ! Alvarez-Borrego* Raquel M. Hidalgo-Gonza! lez, Saul ! de Oceanolog!ıa, CICESE, Km. 107 Carretera Tij-Ens, Ensenada, BC, Mexico Division Received 10 February 2003; accepted 3 May 2004 Available online 3 August 2004
Abstract Integrated total (PTint) and new production (Pnewint) (g C m2 d1) were calculated for the Gulf of California with semi-analytical models from the literature, using chlorophyll a concentrations (Chlsat) and the vertical attenuation coefficients of light (K490) from monthly composites of the satellite sensor SeaWIFS (1997–2002). The phytoplankton biomass vertical distribution associated with Chlsat, and the vertical distribution of the f-ratio (f(z)=Pnew(z)/PT(z)), were deduced from historic oceanographic data. The year was divided into two seasons: cool and warm. Values for PTint had a large seasonal variation (e.g., 1.16–1.91 for the cool season, and 0.39–0.49 for the warm season). Values for Pnewint for the cool season increased from the entrance region to the big islands region and then it remained the same from there to the northern Gulf, with values up to twice as large in the two latter regions (up to 1.33 g C m2 d1) with respect to those of the entrance (up to 0.48). Values of Pnewint for the warm season were less than half those of the cool season (0.25– 0.31). In spite of the limited data, a clear interannual PTint variability is evident for the entrance region, with lowest values for the 1997–1999 ENSO event. This kind of variation was also present for the central Gulf, but the effect was much weaker due to its strong dynamics. r 2004 Elsevier Ltd. All rights reserved.
1. Introduction Oceanic total primary production (PT) has two components: new and regenerated production (PT=Pnew+Pr). New production (Pnew) is the fraction of total primary production that is supported by external or ‘‘new’’ input of nutrients (Dugdale and Goering, 1967). Phytoplankton cells use nutrients recycled within the euphotic zone for *Corresponding author. CICESE, P.O. Box 434844, San Diego, CA 92143–4844, USA. Fax: +1-52-646-175-1545. E-mail address: [email protected] (S. Alvarez-Borrego).
regenerated production (Pr). Eppley and Peterson (1979) assumed that Pnew is quantitatively equivalent to the organic matter that can be exported from the total production in the euphotic zone without the production system running down. These latter authors defined the ratio of Pnew to PT as the f-ratio (f=Pnew/PT) and showed that f was an asymptotic function of the magnitude of total production. The processes of fixation of inorganic carbon in organic matter during photosynthesis, its transformation by trophodynamics, physical mixing, transport and gravitational settling are referred to
0967-0645/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2004.05.006
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collectively as the ‘‘biological pump’’ (Ducklow et al., 2001). The ratio of sinking flux to primary production (e-ratio) and the f-ratio vary as functions of the pathways by which nitrogen flows among different organisms (phytoplankton, large and small grazers and bacteria), but the only way to change the absolute amount of export is to change Pnew, which is usually controlled by physical factors (Frost, 1984). Thus, the description of the temporal and spatial variability of Pnew may give us an idea of the variability of the flux of organic matter out of the surface layer. Measuring PT and Pnew with bottle incubation experiments using compounds labelled with 14C and 15N, respectively, has been the basic methodology to generate direct estimates. But it is very time consuming and yields very limited data with low temporal and spatial coverage. The alternative is to make indirect estimates of PT and Pnew. For example, Dugdale et al. (1989), Sathyendranath et al. (1991), and Alvarez-Salgado et al. (2002) used remotely sensed temperature and color to estimate PT and Pnew. The Gulf of California is a very productive and dynamic sea with strong seasonal and interannual variations (Alvarez-Borrego and Lara-Lara, 1991; Alvarez-Borrego, 2002). However, 14C incubations have provided a very limited view of the temporal and spatial variation of the Gulf’s total primary production, and there are no reports on Pnew for the Gulf of California. Satellite ocean-color data give us the opportunity to generate a more complete description of the Gulf’s PT and Pnew variability. Remote sensors provide information on the photosynthetic pigment concentration for the upper 22% of the euphotic zone. To model primary production in the water column from satellite-derived photosynthetic pigments, estimates of the vertical distribution of pigment concentration are required. The assumption of a mixed layer with a homogeneous pigment distribution could lead to inaccurate estimates of integrated primary production (Platt et al., 1991). The deep chlorophyll maximum (DCM) is a consistent feature in the ocean (Dandonneau, 1979; Cullen and Eppley, 1981). Generally, accounting for its presence increases estimates of
integrated production, and since the DCM often appears below the mixed layer, it would seem likely that most of its production is new production (Sathyendranath et al., 1995). A difficulty in estimating oceanic production from surface measurements arises from the regional differences in the vertical distribution of Chl. Following Lewis et al. (1983) and Platt et al. (1988), HidalgoGonza! lez and Alvarez-Borrego (2001) used chlorophyll concentration (Chl(z)) historical data to fit a Gaussian distribution function to represent the pigment vertical profile for different seasons and regions within the Gulf of California. The objective of this work is to quantify the spatial and temporal variation of PT and Pnew for the Gulf of California. To accomplish this, we used SeaWIFS imagery, the Gaussian vertical distribution of Chl(z) as proposed by HidalgoGonza! lez and Alvarez-Borrego (2001) for seasons and regions within the Gulf, and the average photosynthetic parameters proposed by ValdezHolgu!ın et al. (1999) for the whole Gulf. The Gulf of California has clear impacts from interannual events such as El Nin˜o-La Nin˜a cycles (Santamar!ıa-Del-Angel et al., 1994).
2. Study area The Gulf of California is very dynamic because of tidal currents, wind stress, upwelling, and high solar heating. It consists of a series of basins separated by sills. The basins have depths up to >3000 m at the entrance region, and they are very shallow in the northern Gulf (p200 m). Marked seasonal changes of temperature, salinity, currents, and sea level have been reported for the central Gulf of California (Ripa and Marinone, 1989; Soto-Mardones et al., 1999). However, information about the spatial and temporal variability of chemical and biological processes is scarce. Upwelling occurs off the eastern coast with northwesterly winds (‘‘winter’’ conditions from December to May), and off the Baja California coast with southeasterly winds (‘‘summer’’ conditions from July to October), with June and November as transition periods (Alvarez-Borrego and Lara-Lara, 1991). This wind cycle in the Gulf
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of California is called the Mexican monsoon (Douglas et al., 1993). With northwesterly winds upwelling is strong, it has a marked effect on phytoplankton communities (Chls values up to more than 10 mg m3), and due to eddy circulation it increases the phytoplankton biomass across the Gulf (Santamar!ıa-Del-Angel et al., 1994). However, because of strong stratification during summer, upwelling with southeasterly winds has a very weak effect on phytoplankton biomass (Santamar!ıa-Del-Angel et al., 1999). The northern Gulf of California exhibits spectacular tidal phenomena. With a range of >7 m during spring tides in the upper Gulf and >4 m in ! and Angel de la the big islands area (Tiburon Guarda), tidal energy dissipation rates are great. In the upper Gulf tidal energy dissipation rates are as large as >0.5 W m2, and in the big islands area they are >0.3 W m2 (Argote et al., 1995). The lowest surface temperatures of the whole Gulf of California are found here (Soto-Mardones et al., 1999). Tidal mixing over the sill between San Lorenzo and San Esteban islands produces a vigorous stirring of the water column down to >500 m depth (Simpson et al., 1994). Tidal mixing in the big islands area causes a net effect of carrying cold and nutrient-rich waters to the surface throughout the whole year (AlvarezBorrego, 2002). This produces patches of high Chl (up to >2 mg m3) in this area even during summer.
3. Data and methods Platt et al.’s (1991) non-spectral model with inhomogeneous biomass profile was used to estimate total primary production for each depth in case-II waters (Chl>1.5 mg m3) ¼ ½P Chl a PAR P TðzÞ
mðzÞ
ðzÞ
PARðzÞ
ðzÞ
Þ2 0:5 ½ðPmðzÞ Þ2 þ ðPARðzÞ aPAR ðzÞ ðmg C m3 h1 Þ; where PAR is the photosynthetically active radia is the assimilation number (mg C mg tion, Pm 1 1 Chl h ), and aPAR is the initial slope (mg C mg Chl1 h1 (mmol quanta m2 s1)1) of the
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photosynthesis–irradiance relationship (P–E curves). A modification to this model proposed by Giles-Guzma! n and Alvarez-Borrego (2000) was used for case 1 waters (Chlo1.5 mg m3) f Chl a% PTðzÞ ¼ ½PmðzÞ ðzÞ phðz;ChlÞ PARðzÞ max ½ð0:02315P Þ2 þ ðPAR a% mðzÞ
ðzÞ phðz;ChlÞ fmax Þ
2 0:5
:
This modification is a spectral model with inhomogeneous biomass profile and corrects the ) by the in situ spectral distribuinitial slope (aPAR tion of scalar PAR. Instead of aPAR in the Platt et al. (1991) expression, we used 43:2fmax a% phðz;ChlÞ (Giles-Guzma! n and Alvarez-Borrego, 2000). The maximum photosynthetic quantum yield at low irradiance (mol C (mol quanta)1) is fmax. The average specific absorption coefficient of phyto2 1 plankton is a% ph(z,Chl) (m mg Chl ), weighted by the in situ spectral distribution of PAR and calculated following Giles-Guzma! n and AlvarezBorrego (2000). The factor 43.2 converts mol C to mg C, seconds to hours, and mol quanta to mmol quanta. These expressions show that to estimate primary production we need not only the surface Chl value but also the vertical profiles of Chl and PAR. To define the chlorophyll vertical profile, Hidalgo-Gonza! lez and Alvarez-Borrego (2001) proposed to divide the year into two periods. The cool season is the period end of November– end of June, and the rest of the year is considered the warm season. They also proposed dividing the Gulf into four regions for the cool season and into two regions for the warm season (Fig. 1). SeaWIFS monthly composites of Chlsat and K490 with a spatial resolution of B9 km for the period September 1997–September 2002 were used to obtain representative averages for the seasons and regions of the Gulf. The Chlsat and K490 means were obtained from each season composite and for each Gulf region using the program Windows Image Manager (WIM), developed by Kahru, Scripps Institution of Oceanography, La Jolla. As a first approximation, we can represent Chlsat by the Chl(z) average for the first optical depth, weighted by the irradiance attenuated twice (when the light is going down and when it is backscattered up) (Kirk, 1994). For the available Gulf of California in situ Chl data, the Chl(z) weighted
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(a)
(b)
Fig. 1. Regions of the Gulf of California: (a) for the cool season; and (b) for the warm season.
average for the first optical depth is about 10% higher than the surface Chl (Chls), thus Chls =0.9 Chlsat (Hidalgo-Gonza! lez and Alvarez-Borrego (2001). Surface scalar PAR (PARz=0+) was estimated with the Bedford Institute of Oceanography (Halifax, Canada) program available through Internet at http://www.amigo.bio.dfo.ca. This program uses latitude, longitude, year, and Julian day. A representative mean geographic location
was chosen for each region within the Gulf, then PAR was obtained for each Julian day, and an average PAR was calculated for each region and season. Following Morel and Maritorena (2001), this value was multiplied by 0.965 to estimate PAR immediately under the sea surface (PARz=0). The PAR profile (PAR(z)) for case-I waters was calculated following Giles-Guzma! n and AlvarezBorrego (2000), with a variable KPAR (KPAR(z)) calculated with the Chl profile and taking into
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account the variation of the spectral distribution of light with depth. Average Chls was o1.5 mg m3 in all of our cases, but due to the deep Chl maximum in some cases Chl(z) was >1.5 mg m3. In those cases, the PAR profile for the near surface waters (with Chlo1.5 mg m3) was calculated following Giles-Guzma! n and Alvarez-Borrego (2000), and the PAR profile for deeper waters (with Chl>1.5 mg m3) was calculated with the Lambert–Beer law and an average vertical attenuation coefficient, KPAR, deduced from the satellite K490 average value. The regression models proposed by Cervantes-Duarte et al. (2000) (ZPAR1%=A+B/K490) were used to estimate the euphotic zone depth (ZPAR1%) as a function of K490 in each case, and KPAR was estimated (KPAR=4.6/ZPAR1%,). The regression parameters A and B have different values for different regions within the Gulf. Valdez-Holgu!ın et al. (1999) proposed the following working averages for the photosynthetic parameters for the whole Gulf of California and for the cool season (7 one standard error): a surface Pmax = 9.672.4 mg C mg Chl1 h1, with a linear variation between this and 3.770.3 at the middle of the euphotic zone, and then a constant value for deeper waters; a single value of =0.02970.004 mg C mg Chl1 h1 (mmol ainc quanta m2 s1)1 (incubator’s initial slope); and fmax=0.0670.01 mol C (mol quanta)1. And for =3.770.3, with a the warm season: a surface Pmax linear variation between this and 1.570.2 at the middle of the euphotic zone, and another linear variation between the latter and 0.470.1 at the bottom of the euphotic zone; a surface =0.01370.001, with a linear variation between ainc this and 0.001 at the bottom of the euphotic zone; and a single value fmax= 0.01470.002. Taking into consideration the spectral distribution of light in Valdez-Holgu!ın et al.’s (1999) incubator and following Giles-Guzma! n and Alvarez-Borrego ¼ 1:2a : In (2000), for surface waters ainsitu inc case-II waters, aðZÞ tends to maintain the value that corresponds to the spectral distribution of PAR at the surface. This is due to the strong absorption of both red and short-wavelength light because of the abundance of pigments, detritus and color-dissolved organic matter. Thus, we used
743
Platt et al.’s (1991) non-spectral model to estimate primary production for case-II waters, without any correction of aðZÞ for the spectral distribution of light at depth. We used NO3 data from 268 hydrographic stations sampled in oceanographic cruises from 1973 to 1993 to generate average NO3 profiles for each season and region of the Gulf. In all cases NO3 was determined by the spectrophotometric method following Strickland and Parsons (1972). Unfortunately, there are no newer NO3 available data for the Gulf. Harrison et al.’s (1987) expression was used to calculate the f-ratio for each depth (f(z)=fmax[1-exp(-mNO3(z)/fmax)]). Unfortunately, there are no reports on the f(z)–NO3(z) relationship for the Gulf of California. Thus, we chose the parameters m and fmax as reported by Harrison et al. (1987) for oceanographic conditions similar to those found in the Gulf. For the cool season we chose m=0.98 and fmax=0.77, which correspond to the coastal upwelling Peruvian zone, and for the warm season we chose m=12.1 and fmax=0.64, which correspond to the summer oligotrophic intrusion of the Southern California Bight. A sensitivity analysis was performed to assess the effect of uncertainties of variables and parameters on the estimates of average integrated total production for the whole euphotic zone and for the whole day (PTint) (g C m2 d1 or ton C km2 d1). One standard error (s n0.5) was added and subtracted to each input variable and parameter, one at a time, to assess the effect on PTint, and the difference was expressed as percentage. Due to the covariation of the photosynthetic ; a parameters (PmðZÞ PARðZÞ ; and fmax) (i.e., Cote and Platt, 1983; Valdez-Holgu!ın et al., 1999), when adding or subtracting one standard error we did it for all of them at the same time. It was not possible to do a sensitivity analysis with the uncertainties associated with KPAR(z) calculated for case-I waters following Giles-Guzma! n and Alvarez-Borrego (2000) because these latter authors did not provide values for the standard errors associated to their equations. They only mentioned that when comparing 30 PTint values estimated with calculated PAR profiles with the corresponding values estimated with measured profiles, the mean of the
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percent differences was 5.9%. But, as they indicated, PAR profiles that resulted from the model were smooth, whereas those that resulted from measurements in some cases had abrupt changes in the PAR vertical variation rate. Thus, possibly, most of the differences between measured and calculated PAR are due to errors in the measured PAR values. Also, a sensitivity analysis was done to assess the effect of the f-ratio uncertainties on estimates of integrated new production (Pnewint) (g C m2 d1 or ton C km2 d1).
4. Results The high number of pixels allowed for a relatively small standard error for Chls and K490, about 74% in both cases. Average Chls values for the cool season had a clear interannual variation, with lower values in 1997–1998 than during the other winters, in all regions of the Gulf (Table 1). This is the effect of an El Nin˜o event, and it is more evident in region I, the entrance to the Gulf, where it can also be seen in 1998–1999. During the cool seasons of 1997–1998 and 1998–1999 there was a Chls gradient with values increasing from south-to-north. During the other cool seasons (1999–2000, 2000–2001, and 2001–2002) there was no clear south-north gradient. During the warm
season, Chls average values for the whole Gulf were similar to those for the entrance region during the cool season and with an El Nin˜o event. In general, average K490 values were minimal for the southernmost regions (I and 1) and maximal for the big islands region (III). There was a slight tendency for higher K490 average values during the cool season than those for the warm season, but there was no clear interannual variation (Table 1). As expected, average incident PAR(z=0+) had a clear seasonal change and decreased from southto-north, but its interannual variation was not significant (not illustrated). The absolute values of the standard error for NO3 were similar for different depths, regions and seasons (most of them between 0.2 and 0.4 mM), but the relative values changed from B20% at low-NO3 values to B3% at high values (Fig. 2). In general, average surface and near-surface NO3 values increase from the entrance region to the interior of the Gulf, up to the big islands region (III), and then they decrease a little from there to the north (region IV) (Fig. 2). The nutricline is up to 40 m deeper at the entrance to the Gulf (regions I and 1) than in the internal regions, with relatively low-NO3 values from the surface down to 60 m during the cool season. The shallowest nutriclines were those of regions III and IV, with the highest average surface NO3 values in the big islands region (III).
Table 1 Satellite-derived average values for seasons and regions in the Gulf of California of surface chlorophyll (Chls=0.9 Chlsat mg m3) and light-attenuation coefficient (K490 m1). The standard error (s n0..5) for both variables is B4% in all cases Years
I
II
III
IV
Years
1
2
Chls (mg m )
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.36 0.48 0.92 0.86 0.83
0.48 0.66 0.77 0.98 0.81
0.45 0.69 0.83 0.69 0.79
0.70 0.88 0.89 1.15 0.96
1997 1998 1999 2000 2001 2002
0.30 0.24 0.41 0.55 0.46 0.43
0.42 0.37 0.43 0.45 0.42 0.41
K490 (m1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.06 0.10 0.11 0.10 0.09
0.11 0.13 0.15 0.18 0.16
0.16 0.15 0.20 0.19 0.18
0.13 0.17 0.16 0.17 0.16
1997 1998 1999 2000 2001 2002
0.07 0.06 0.08 0.10 0.08 0.09
0.13 0.12 0.12 0.12 0.15 0.14
3
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Fig. 2. Average NO3 profiles for the seasons and regions in the Gulf of California as shown in Fig. 1. Horizontal bars represent 7 one standard error (s n0.5).
Total production, PT(z), had maxima at shallower depths than those of the Chl(z) maxima (Fig. 3) due to greater PAR(z) near the surface. On the other hand, PT(z) maxima were often in subsurface waters due to the relatively low-surface Chl(z) values. With relatively high surface Chl, maximum PT(z) was at the surface, such as in region IV, where the deep chlorophyll maximum was at B20 m. Pnew maxima had the same depths as those of PT(z) maxima. Production of the deep Chl maximum, both PT and Pnew, was relatively low compared to that of near-surface waters due to low-light levels at the former (Fig. 3). Greatest uncertainties of the estimates for average integrated total production for the whole euphotic zone and for the whole day (PTint) (g C m2 d1 or ton C km2 d1) are due to uncertainties in the photosynthetic parameters. When augmenting or diminishing the photosynthetic parameters by one standard error, PTint changed as much as 17% with low Chls, and as much as 19% with high Chls. This is due to the few degrees of freedom in the P–E parameters. Since we are using single average values for the whole Gulf, these large intervals do not affect the comparisons of PTint between regions, but it does affect the comparisons between seasons and years. When changing Chls by one standard error, PTint changed only p2%, and when changing K490 by one standard error, PTint changed B2.7%. The probability of having all these errors added
together simultaneously is low due to the multiplication rule. Average integrated total production (PTint) shows a regular annual cycle as the dominant feature of these time series while the interannual changes were usually of smaller magnitude (Table 2). During the cool season, the effect of El Nin˜o 1997–1998 can be appreciated throughout the whole Gulf, with lower values of PTint than during the other cool seasons. However, the most intense effect of El Nin˜o, and possibly the only significant one, was recorded for the entrance region. During the warm season there was no clear El Nin˜o effect in any region of the Gulf. Even at the entrance to the Gulf, changes of PTint due to the seasonal cycle were more intense than the interannual changes due to El Nin˜o. At the entrance to the Gulf, during the cool season, El Nin˜o reduced PTint down to B65% with respect to non-El Nin˜o years. During non-El Nin˜o years PTint for the warm season was reduced down to B20% with respect to that for the cool season. On the other hand, there was no south–north PTint significant gradient, for any particular season. The PTint range for the whole Gulf was 1.16–1.91 g C m2 d1 for the cool season, and it was 0.39–0.49 for the warm season. The f-ratio estimates did not change significantly when changing the NO3 profiles by one standard error. Thus, uncertainties in the new production estimates are only those associated to uncertainties of total production.
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Fig. 3. Examples of the average chlorophyll, total primary production, and new production profiles for regions I and IV in the Gulf of California.
Average integrated new production for the euphotic zone (Pnewint) (g C m2 d1 or ton C km2 d1) increased from the entrance region
(I) to the big islands region (III) and then it was practically the same in region IV as in region III, during the cool seasons (Table 3), with values up
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Table 2 Satellite-derived integrated total primary production (PTint) per unit area ( g C m2 d1 or ton C km2 d1) and for whole regions in the Gulf of California (ton C d1) I
II
III
IV
Year
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
1.16 1.20 1.85 1.80 1.78
5.8 104 6.0 104 9.3 104 9.0 104 8.9 105
1.52 1.67 1.74 1.91 1.87
9.0 104 9.8 104 10.3 104 11.3 104 11.0 104
1.45 1.60 1.73 1.62 1.66
3.1 104 3.5 104 3.7 104 3.5 104 3.6 104
1.52 1.60 1.60 1.68 1.65
2.6 104 2.7 104 2.7 104 2.8 104 2.8 104
1
2
Year
PTint (g C m2 d1)
PTint (ton C d1)
PTint (g C m2 d1)
PTint (ton C d1)
1997 1998 1999 2000 2001 2002
0.42 0.39 0.43 0.49 0.48 0.47
4.6 104 4.3 104 4.7 104 5.3 104 5.2 104 5.1 104
0.43 0.42 0.45 0.44 0.43 0.43
0.93 104 0.91 104 0.97 104 0.95 104 0.93 104 0.93 104
to more than double in regions III and IV (up to 1.33 g C m2 d1) with respect to those of region I (up to 0.48 gC m2 d1). However, there was no clear south–north Pnewint gradient during the warm season. Again, the dominant temporal change was the seasonal cycle. We could not detect any significant effect of the El Nin˜o event on the Pnewint average values for the cool or the warm season. The Pnewint range for the whole Gulf was 0.38–1.33 g C m2 d1 for the cool season, and it was 0.25–0.31 g C m2 d1 for the warm season.
5. Discussion Total and new oceanic production calculated from remotely sensed data on ocean color, which depends on parameterizations developed from ship observations, yield more representative estimates of the large-scale average production than those calculated from ship data alone (Sathyendranath et al., 1991). Morel and Berthon (1989) indicated that it is unreasonable and probably superfluous to envisage the use of a light-production model on a
pixel-by-pixel basis when interpreting satellite imagery. Our objective was to obtain representative average production values for whole seasons and regions within the Gulf of California. Rigorous comparison of the satellite-derived time series of PTint with results from 14C incubations is difficult due to the different time and space characteristics of these measurements (Balch and Byrne, 1994). Nevertheless, it is interesting to compare both kinds of data. Alvarez-Borrego and Lara-Lara (1991) reported 26 14C-derived PTint point values for region II with an average of 1.43 g C m2 d1, compared with our range of 1.52–1.87; they reported 12 values for region III with an average of 2.1 g C m2 d1, compared with our range of 1.45–1.73; and they reported four values for region IV with a mean of 1.1 g C m2 d1 compared with our range of 1.52–1.68. These latter authors only reported five point values for the warm season and for the whole Gulf, which do not allow for comparisons. In spite of great differences in time and space scales, both methods provide average values that are very close, and given the uncertainties of our satellite-derived estimates,
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Table 3 Satellite-derived integrated new primary production (Pnewint) per unit area ( g C m2 d1 or ton C km2 d1) and for whole regions in the Gulf of California (ton C d1) I
II
III
IV
Year
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
1997–1998 1998–1999 1999–2000 2000–2001 2001–2002
0.38 0.39 0.48 0.46 0.38
2.2 104 2.3 104 2.9 104 2.7 104 2.2 104
0.71 0.75 0.75 0.81 0.79
4.2 104 4.4 104 4.4 104 4.8 104 4.7 104
1.11 1.22 1.33 1.29 1.31
2.4 104 2.6 104 2.9 104 2.8 104 2.8 104
1.16 1.22 1.26 1.29 1.25
1.95 104 2.05 104 2.07 104 2.17 104 2.10 104
1
2
Year
Pnewint (g C m2 d1)
Pnewint (ton C d1)
Pnewint (g C m2 d1)
Pnewint (ton C d1)
1997 1998 1999 2000 2001 2002
0.27 0.25 0.27 0.31 0.29 0.27
3.2 104 2.8 104 3.0 104 3.4 104 3.2 104 3.0 104
0.28 0.28 0.30 0.28 0.27 0.27
0.62 104 0.62 104 0.66 104 0.62 104 0.60 104 0.60 104
these differences are not significant. Kahru and Mitchell (2002) compared their satellite-derived primary productions for the California Current with 14C measurements and reported that the first overestimate the second by about 40%. In our case satellite estimates do not systematically over or underestimate PTint. In spite of possible errors, ocean-color satellite imagery are very consistent; their seasonal cycles and the spatial variation within the Gulf of California behave very much as expected according to physical phenomena such as the movement of water masses and the occurrence of upwelling. Trees et al. (2000) reported that, despite the various sampling periods and numerous geographic locations, there are consistent patterns in the ratios of the log accessory pigments to log total Chl (Chl a, Chl a allomer, Chl a epimer, and chlorophyllide a), and there is a strong log-linear relationship for these ratios. These latter authors indicated that this log-linearity largely explains the success in remotely sensed Chl algorithms, even though phytoplankton populations can vary in their composition and suite of pigments. The large
number of pixels within each of our Gulf of California regions allowed for relatively small Chl and K490 standard errors. The vertical distribution of model-derived primary production is also very consistent and behaves as expected from 14C experiments. The largest contribution to production is from the surface and near-surface waters (i.e., the upper 15 m), with a relatively small contribution from the deep Chl maximum (Fig. 3). This agrees with ! et al., 2000). reports in the literature (i.e. Maran˜on For the purpose of defining regions to apply primary production models to satellite color data, the larger the regions the better. For example, for the purpose of modeling production, ValdezHolgu!ın et al. (1999) proposed means of photosynthetic parameters (from P–E curves) for the whole Gulf of California as a single region. Sathyendranath et al. (1995) indicated that most boundaries between biogeochemical regions prove to have some significance for the depth of the chlorophyll maximum. That is the case for our Gulf of California regions. The Gulf of California has a spectrum of physical dynamics that affect the
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vertical distribution of phytoplankton biomass in different ways, so that it has to be divided into relatively small geographic regions. The underlying assumption of a Gaussian distribution function is that for a given region of the ocean, in a given season, the typical shape of the chlorophyll profile is stable. Gaussian biomass profiles derived for different regions of the Gulf, and with the same Chl surface value, produce different integrated production values (HidalgoGonza! lez and Alvarez-Borrego, 2001). The effect of nutrient concentrations is not explicit in our primary production models because it is implicit in Chl. Nutrients control phytoplankton biomass but have a very weak effect on photosynthetic parameters (Cullen et al., 1992). Nutrient concentrations have an explicit effect on the estimates of Pnew(z) through the f-ratio values. However, since there are no data to document the effect of El Nin˜o–La Nin˜a cycles on the nutrients of the Gulf of California, it is not possible to describe the temporal change of NO3, and our fratio values used to calculate Pnew(z) are constant with time. The strong warm season depletion of primary production in the Gulf is due to the invasion of the equatorial surface water (ESW). This warm surface water, up to >30 C, causes a very strong water-column stratification, greatly decreasing the effect of summer upwelling on the phytoplankton biomass (Santamar!ıa-Del-Angel et al., 1999) and on primary production. The energy required to move a parcel of water from 100 m to the surface during summer is 5–15 times that for winter (Corte! s-Lara et al., 1999). Our results suggest that the summer intrusion of the ESW into the Gulf of California produces every year an effect on primary production stronger than that of an El Nin˜o event with winter conditions. Watts et al. (1999) measured Pnew for the northwestern Indian Ocean using 15N stableisotope, tracer techniques, and found that both the integrated f-ratio (Pnewint/PTint) and Pnewint were larger during the monsoon, with ranges of 0.10–0.96, and 0.04–3.66 g C m2 d1, respectively, and lower during the intermonsoon, with ranges of 0.07–0.52, and 0.05–0.65 g C m2 d1, respectively. This was due to upwelling and greater wind-
749
induced vertical mixing during the monsoon. Their average integrated f-ratio and Pnewint for the monsoon, and for the whole northwestern Indian Ocean, were 0.60 and 1.55 g C m2 d1, respectively. These averages are close to those for the cool season of the northern Gulf of California regions. Liu et al. (2002) used a monsoon-forced model to describe the temporal and spatial variability of chlorophyll and primary production in the South China Sea (SCS), and found good agreement with data derived from SeaWIFS. In the SCS there are also two peaks of primary production, with the strongest during the winter monsoon, a weaker peak during the summer monsoon, and low production during the two inter-monsoon periods. Highest winter monsoon PTint values reported for the SCS by Liu et al. (2002) were between similar and 80% of the PTint warm season values for the entrance to the Gulf of California (region 1), and they were only B16% of the Gulf’s cool season values for non-El Nin˜o years. Based on a 6-year time series of sediment trap samples, Thunell (1998a) documented the seasonal and interannual changes in particles fluxes in Guaymas basin, at the northern part of region II. Sedimentation in this region of the Gulf of California is dominated by two seasonally varying components: biogenic silica during the late fallspring (cool season) and lithogenic material during the summer (warm season), this forms laminated diatomaceous sediments, and a couplet of laminae constitute a varve deposited in a year (Calvert, 1966). These varves in the central Gulf of California are formed where the basin slopes intersect the oxygen minimum in the water column. The seasonal variability in sediment fluxes described by Thunell (1998a) is a direct response to the reversing monsoon climate in the Gulf. The Gulf’s strong seasonal variability of Pnewint, with values up to more than double for the cool season with respect to those of the warm season, is in accordance with the seasonal variability of particle fluxes reported by Thunell (1998a). Thunell (1998b) reported that for the Santa Barbara basin, a coastal upwelling zone off southern California, export ratios are inversely related to total primary production, and this is due to increased advective
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transport during the highly productive upwelling season. This is not the case for the Gulf of California because it is a semienclosed sea with eddy circulation across the whole Gulf. It is not possible to describe interannual changes properly with only 5 years of data in our time series. However, it is interesting to notice that in the Gulf of California there was practically no interannual variation of PTint and Pnewint from warm to warm season in the period 1997–2002, but the physical forcing of large temporal and spatial scales affected the Gulf’s production during the cool seasons. There was a clear El Nin˜o effect on Chls and primary production mainly at the entrance to the Gulf but also evident throughout the whole Gulf during the 1997–1998 cool season. This effect was also present during 1998–1999 but only for the entrance region. At the entrance region, primary production decreased down to B65% during 1997–1998 with respect to their values in the cool seasons of 2000–2001 and 2001– 2002. Santamar!ıa-Del-Angel et al. (1994) described a similar El Nin˜o effect on Chlsat during the winters of 1982–1983 and 1983–1984 using ocean color data from the Coastal Zone Color Scanner. These latter authors reported a dramatic suppression of Chlsat at the entrance to the Gulf during El Nin˜o 1982–1983, with values down to B20% of those for non-El Nin˜o years, but with a relatively small impact in the big islands and northern regions. This was very consistent with Mee et al.’s (1985) Chl (1979–1983) time series obtained for a location at the mouth of the Gulf 30 km from the eastern coast, which showed that Chl values for winter dropped from B10 mg m3 during non-El Nin˜o years to o2 mg m3 in 1983. Santamar!ıaDel-Angel et al. (1994) concluded that the sequence of El Nin˜o and non-El Nin˜o events do not affect the phytoplankton assemblages in all regions of the Gulf of California in the same manner. Our results confirm this conclusion. In some areas of the Gulf, such as the big islands region and the northern Gulf, local physical phenomena causes strong turbulence as described above, reducing the effect of El Nin˜o. Based on his particle flux data, Thunell (1998b) indicated that production in the Santa Barbara basin is reduced during ENSO events. Thunell
(1998a) also observed interannual differences in the magnitude of sediment fluxes in Guaymas basin (region II), indicating that they appear to be related to El Nin˜o events, and he speculated that there might be higher primary production during non-El Nin˜o years. Our limited data show that for region II there was a PTint reduction of up to 15% during the 1997–1998 El Nin˜o, and although these reductions are not very dramatic and may not be significant, they are in agreement with Thunell’s (1998a) findings. The largest interannual change of our time series is for region I, with a PTint reduction of up to 35% during an El Nin˜o year, but no sediment flux has been reported for this region of the Gulf.
Acknowledgements We thank Dr. Trevor Platt and Dr. Charles C. Trees for their constructive comments and criticisms to an earlier version of this manuscript. We are very grateful to the National Council of Science and Technology of Mexico (CONACYT) for supporting the project J002/750/00C-834/00. J. M. Dominguez and F. Ponce did the artwork.
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