The Effect of Vertical Mixing on Primary Production in a Bay of the Gulf of California

Estuarine, Coastal and Shelf Science (1997) 45, 135–148

The Effect of Vertical Mixing on Primary Production in a Bay of the Gulf of California F. Delgadillo-Hinojosaa, G. Gaxiola-Castrob, J. A. Segovia-Zavalaa, A. Mun˜oz-Barbosaa and M. V. Orozco-Borbo´na a

Instituto de Investigaciones Oceanolo´gicas, Universidad Auto´noma de Baja California, Carretera Tijuana-Ensenada km 105, Ensenada, Baja California, Me´xico b Divisio´n de Oceanologı´a, Centro de Investigacio´n Cientı´fica y de Educacio´n Superior de Ensenada, Carretera Tijuana-Ensenada km 107, Apdo. Postal 2732. Ensenada, Baja California, Me´xico Received 31 October 1995 and accepted in revised form 27 June 1996 Short-term variability of primary production was studied during Summer 1986 in Bahia de Los Angeles, Mexico. An 8-day time series of temperature, salinity, nutrients and chlorophyll a was performed. Simultaneously, primary productivity was measured using the 14C method. The water column was stratified during the first 3 days, and mixed when the wind speed was up to 10 m s "1. Wind stress played a major role in producing vertical mixing and forcing surface circulation in the Bay. Higher chlorophyll a values (>3 mg m "3) were recorded at 10 m depth during the first 3 days, and were 2–3-fold greater than those measured on the following days. The inverse relationship between the integrated phytoplankton biomass and the calculated euphotic depth (Zeu) suggests that light penetration in the water column was mainly controlled by the phytoplankton biomass. The photosynthetic assimilation ratio (PB) ranged from 3·7 mgC (mg chla) "1 h "1, measured during stratification of the water column, to 9·3 mgC (mg chla) "1 h "1, measured with water-mixed conditions. PB variability was a result of the combined effect of vertical mixing in the water column and the increased light availability. Short-term integrated primary production ranged from 26 to 62 mgC m "2 h "1, and its temporal variability was associated with phytoplankton biomass and the light availability. The averaged daily integrated production was related to nitrate concentrations in the water column. These results suggest that limitation of primary production from both light and nutrients occurred simultaneously in Bahia de Los Angeles during Summer 1986. ? 1997 Academic Press Limited

Keywords: primary production; short-term variability; vertical mixing; inorganic nutrients; Gulf of California

Introduction It is traditionally accepted that the productivity of marine phytoplankton is controlled by nutrients and/or light. These two factors show an important short-term variability that has been scarcely studied on its appropriate time scale (Litaker et al., 1987). Likewise, it is now well established that phytoplankton responses occur on a scale of hours to days (Ferris & Christian, 1991; Prezelin et al., 1991). Thus, any discussion of the variability or control of the primary production on a certain time scale, must be done on the appropriate environmental scale (Harris, 1986). A good point to study the short-term variability of primary productivity and environmental factors is found at the borders of hydrodynamically active areas, because they have particular conditions of nutrient and underwater light climate (Demers et al., 1989). Such areas represent transition zones between high 0272–7714/97/010135+14 $25.00/0/ec960167

and low levels of energy provided by tides, winds or freshwater runoff (Margalef, 1978). A high proportion of this energy is available to mix the water column vertically, and modify its stratification structure. Therefore, the vertical mixing of the water column plays a major role in controlling the variability of nutrient concentrations and the exposure of phytoplankton cells to the light gradient (Demers et al., 1986). In this context, the study of the short-term variability of vertical mixing may be the key to understanding the effects of physical processes on primary production on the scale of hours to days. Bahia de Los Angeles is a small open bay located at the border of a very dynamic region known as Ballenas Channel in the Gulf of California. Satellite imagery has revealed a pool of cold water in the area outside the Bay as a persistent feature (Badan-Dangon et al., 1985; Bray & Robles, 1991), and has a marked fortnightly modulation (Paden, 1990). The Ballenas ? 1997 Academic Press Limited

136 F. Delgadillo-Hinojosa et al.

ali n for

Pacific Ocean

ia

Bahia de Los Angeles (BLA) is located on the eastern coast of the Baja California Peninsula, between latitude 28)54*N and 29)04*N, and longitude 113)30*W and 113)30*W (Figure 1). The Bay is located in a desertic region, with scarce rain and high evaporation during the entire year. The tide is typically semidiurnal with a maximum tidal range of 2·0 m. The Bay is one of the deepest (240 m) embayments of the Gulf of California, and is 16 km long and 6·4 km at the widest section. In spite of some small islands which partially isolate BLA from the adjacent zone, its waters have an open interchange with the Ballenas Channel. Unfortunately, the hydrodynamics of the area and the interaction between these two systems remain poorly understood. Wind stress is the main factor controlling the surface circulation in the Bay, producing strong surface water exchange with the Ballenas Channel (AmadorBuenrostro et al., 1991). These authors have reported tidal currents of 23 cm s "1, and wind-forced currents with velocities up to 25 cm s "1. During summer, the wind blows predominantly E-SE with speeds up to 10 m s "1, lasting several days (Merrifield et al., 1987). Amador-Buenrostro et al. (1991) numerically modelled the wind-forced sea surface circulation of BLA. Their model predicts that, during summer, the water input flows through the southern mouth of the

fC lf o

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Bahia de Los Angeles

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Channel area has been associated with high nutrient concentrations (Alvarez-Borrego et al., 1978), and high primary productivity values related to vertical mixing (Gaxiola-Castro et al., 1995), mainly generated by strong tidal currents in excess of 1·5 m s "1 (Badan-Dangon et al., 1991). Although the water of Bahia de Los Angeles has a great communication with the Ballenas Channel, the wind is the main factor controlling the surface circulation in the Bay (Amador-Buenrostro et al., 1991). High primary productivity values have been measured in the Bay (Canino-Herrera et al., 1990), with high variability in short periods of time (hours to days) as a result of vertical mixing by wind stress (Mun˜oz-Barbosa et al., 1991). However, no one has attempted to explain the short-term variability of primary productivity in terms of the factors controlled by the mixing processes, such as phytoplankton light availability and nutrient concentrations in this Bay. Therefore, to acquire a better understanding of the factors controlling production in this Bay, the short-term variability of primary production in relation to environmental changes was studied in Bahia de Los Angeles.

113°30' W

F 1. Location of the study area and sampling station ( ) in Bahia de Los Angeles.

Bay, at which point the current is divided into two branches (Figure 2). The first branch is advected to the west, with the major volume of water exiting BLA by flowing north-easterly through the channel located between the two large islands, and the remaining volume flowing towards the north end of the Bay. The second branch of water is advected along the coastal line surrounding the Bay. Both branches join together at the north end of the Bay and flow out through the north mouth, where the present study’s sampling station was located. Methods During Summer 1986, an 8-day (26 August to 2 September) time series was conducted at the north end of BLA (Figure 1). Water samples were collected every 2 h from surface and 10 m depths, using 2·5 l Van Dorn bottles. At each depth, a total of 95 samples were collected for salinity, nutrients and chlorophyll a analyses. Temperature for 10 m depth was recorded using reversible thermometers (precision 0·1 )C), and bucket thermometers for surface data. Water transparency was measured with a 30 cm diameter Secchi disk.

Vertical mixing and primary production 137

F 2. Residual currents generated by a wind-forced numerical model during summer condition in Bahia de Los Angeles. The open arrow indicates eastern wind direction (redrawn from Amador-Buenrostro et al., 1991).

Chemical analysis Salinity was measured with a Beckman induction salinometer. Samples for chlorophyll a analyses were filtered using 25 mm GF/C filters, and extracted with 90% acetone for 24 h in a cold, dark place. Chlorophyll a concentration was determined fluorometrically with a Turner 111 fluorometer, following Holm Hansen et al. (1965). Nutrient concentrations were analysed with a spectrophotometer Spectronic 1001, according to Strickland and Parsons (1972). In the present work, the daily variabilities of all the variables measured are shown using averaged data for the maximum light irradiance period (10.00–16.00h), when the primary productivity experiments were done. Primary productivity measurements Primary productivity was determined from several different experiments, and a total of 40 measurements were collected. The present work reports the primary

productivity determinations carried out in two different ways: (1) from 26 to 31 August, daily experiments were performed at noon from the surface and 5 m depths; (2) during the first 2 days of September, productivity determinations were done at depths corresponding to 100, 50, 25, 10 and 1% of the irradiance measured just below the sea surface (Eo). Primary productivity was determined using the 14C method (Steeman-Nielsen, 1952). Next, 3 ìCi of NaH14CO3 was added to each 125 ml water sample (one dark and two light glass bottles), and incubated for 2 h at the same depths from which they were collected. Following incubation, samples were filtered through 0·45 ìm pore membrane filters. Filters were placed in glass vials with 10 ml of scintillation cocktail, and the radioactivity was measured with a Beckman LS-100 counter. Inorganic carbon uptake was calculated according to Strickland and Parsons (1972). Carbon uptake from the dark bottle was subtracted from the mean light bottle uptake to give an estimate of net productivity (Pz; mgC m "3 h "1). The ambient irradiance (Ea; W m "2) and underwater irradiance (Ez; W m "2) during the sample incubation were measured with a Kahlsico photometer. The measured primary productivity data generated from both experiments described above were integrated for the upper 5 m. From this integration, an hourly integrated productivity value for each day (HIP; mgC m "2 h "1) was obtained. The photosynthetic assimilation ratio [PB; mgC (mg chla) "1 h "1] was calculated by dividing HIP by the integrated chlorophyll a profile. The definition of major variables and their units used in this work are given in Table 1. Daily primary production (DIP) Empirical models can be used as an alternative for estimating integrated phytoplankton production. One avenue is using light data together with the physiological parameters of the phytoplankton, derived from the photosynthesis-irradiance (P-I) curve; Pm (maximum, primary productivity at light saturation; mgC m "3 h "1) and á [initial slope at low irradiance; mgC m "3 h "1 (W m "2) "1] (Platt et al., 1977; Keller, 1988). Although standard practice is to normalize the primary production to phytoplankton biomass, and obtain the photosynthetic parameters from the P-I curves, Keller’s (1988, 1989) approach was followed in the present study. Thus, the daily primary production was calculated from light data and photosynthetic parameters non-normalized to phytoplankton biomass. The maximum measured primary productivity value for each day was used as Pm. All available

138 F. Delgadillo-Hinojosa et al. T 1. Definition of major variables and their units Variable z g k Ea Eo Ez PE á Pm Pz PB HIP DIP PPz PHIP

Definition

Units

Depth Acceleration due to gravity Light attenuation coefficient Ambient irradiance Irradiance just below the surface Irradiance at depth z Stratification parameter Initial slope of the P-I curve Maximum primary productivity Primary productivity Photosynthetic assimilation ratio Hourly integrated primary production Daily primary production Predicted primary production Predicted hourly integrated primary production

m m s "2 m "1 W m "2 W m "2 W m "2 J m "2 mgC m "3 h "1 (W m "2) "1 mgC m "3 h "1 mgC m "3 h "1 mgC (mg chla) "1 h "1 mgC m "2 h "1 gC m "2 day "1 mgC m "3 h "1 mgC m "2 h "1

P-I, photosynthesis-irradiance.

primary productivity data (30 data points) collected from 26 to 31 August were plotted against Ez, and an averaged P-I curve was obtained for the 6 days [Figure 3(a)]. From the primary productivity data collected during September, two different P-I curves were obtained [Figure 3(b,c)]. In order to calculate á values from the P-I curves, a Quasi-Newton non-linear least squares procedure was used to obtain the best fit of the P-I data to the hyperbolic tangent function reported by Platt and Jassby (1976). The coefficient of determination (r2) ranged from 0·86 to 0·98. Light profiles in the water column were generated every 2 h throughout the time series, using the exponential equation: Ez =0·47 Ea exp("k z)

(1)

where Ea is the ambient irradiance (PAR; Wm "2), and k is the light attenuation coefficient calculated from the Secchi disc readings (Ds), using the relationship k=1·7/Ds. Predicted primary productivity (PPz; mgC m "3 "1 h ) every 0·5 m was calculated from the hyperbolic tangent function using the irradiance values (Ez) from Equation 1, and the parameters á and Pm: PPz = Pm · tanh (á · Ez/Pm)

(2)

The predicted hourly integrated production (PHIP; mgC m "2 h "1) was calculated by integrating numerically, from the surface to 5 m, the PPz profiles using the trapezoidal rule. The daily primary production (DIP; gC m "2 day "1) was calculated integrating the predicted hourly integrated production:

Furthermore, the stratification parameter (PE; J m "2) was calculated as a measure of the watercolumn stability, which is equivalent to the amount of energy required to vertically homogenize the water layer (Nelson et al., 1989): PE=(1/12)Äñ · g · z2, where g is the acceleration due to gravity (m s "2), Äñ (kg m "3) is the density gradient between surface and 10 m depths (ñ10 "ñ0), and z (m) is the depth of the surface layer (10 m). Linear correlation analyses were used to identify whether physical factors (temperature, salinity, irradiance, water-column stability) and biological factors (phytoplankton biomass, nutrients) were related to the different scales of productivity reported in this study. Moreover, to evaluate the influence of the biomass and light availability on productivity, HIP was related to the composite parameter BEoZeu (Cole & Cloern, 1984), where B is the integrated phytoplankton biomass (chlorophyll a; mg m "2), Zeu (4·6/k; m) is the depth of the euphotic zone, and Eo is the irradiance just below the sea surface. Results Sampling started during neap tide conditions (26 August), and concluded with spring tide conditions (2 September) (Figure 4). During the sampling period, the wind speed ranged from 0·5 to 13 m s "1, with wind blowing predominantly from the south-east until the 6th day, and from the south-west for the last 2

Vertical mixing and primary production 139 1.5

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F 4. Predicted tide height from 25 August (18.00h) to 2 September (18.00h) 1986. The tide height is referenced to lower low water level (LLWL). The lower numbers indicate the day sampled, and the upper numbers represent the hours.

12 8 4

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F 3. Photosynthesis (Pz) vs irradiance (Ez) curves generated from data of: (a) 26–31 August; (b) 1 September, and (c) 2 September. , observed values of hourly production. The lines represent the best fit to the hyperbolic tangent function described in Equation 2.

days (Figure 5). For the first 3 days, the water column was thermally stratified, showing temperature differences up to 2 )C between the surface and 10 m depth [Figure 6(a)]. Likewise, the salinity showed differences up to 0·05 during the same period, suggesting that the water column was vertically stratified [Figure 6(b)]. In contrast, on the 4th and 7th days, the water column became completely mixed [Figure 6(a–c)] as a result of strong vertical mixing induced by the wind. During those days, the stratification parameter (PE), and the salinity and temperature gradients were minima [Figure 6(a—c)], associated with wind speeds up to 10 m s "1 (Figure 5). On the 5th and 6th days, the wind speed decreased and the water column was again weakly stratified [Figure 6(c)].

According to the data described above, warmer and saltier water arrived at the sampling station during the first 5 days. During that time, average water-column temperature rose at a mean rate of 0·38 )C day "1, with a sudden decline during the 7th and 8th days at a mean rate of 0·45 )C day "1 [Figure 6(a)]. Similarly, the averaged salinity had lower values during the first 3 days, and a trend to increase toward the end of the time series [Figure 6(b)]. The evidence of warmer and saltier water at the surface and 10 m depth suggests the effect of water advected from the inside of the Bay and piled up at the north end. However, the decrease of temperature and salinity values at the end of the

–1

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00 12 00 12 00 12 00 12 00 12 00 12 00 12 00 12 1 2 3 4 5 6 7 8 Time (days)

F 5. Wind speed recorded at sampling station from 26 August to 2 September 1986, using a Kahlsico anemometer. The lower numbers indicate the day sampled, and the upper numbers represent the hours.

140 F. Delgadillo-Hinojosa et al. 30

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Primary productivity The hourly integrated productivity ranged from 26 to 60 mgC m "2 h "1. Higher productivity values were

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study indicates a strong exchange with the persistent pool of cold, less salty water from the adjacent Ballenas Channel. Higher chlorophyll a values (>3 mg m "3) were recorded at 10 m depth during the first 3 days [Figure 7(a)]. These values were 2–3-fold greater than those measured on the following days. Changes in phytoplankton biomass (chlorophyll a) were a major factor influencing PAR attenuation. The inverse relationship between the integrated phytoplankton biomass and the calculated Zeu suggest that light penetration in the water column was mainly controlled by the phytoplankton biomass [Figure 7(b)]. For instance, at the beginning of the sampling period, the irradiance at 5 m depth was 22·5 W m "2 (14% Eo), associated with high integrated chlorophyll a concentrations (30 mg m "2). In contrast, at the end of the time series, the irradiance at the same depth was 38 W m "2 (25% Eo), with a low integrated chlorophyll a value (14 mg m "2). Thus, the attenuation coefficient of PAR ranged from 0·31 m "1 on the first day to 0·15 m "1 at the end of the study, resulting in an average increase of the euphotic depth of 1·3 m day "1 [Figure 7(c)]. Phytoplankton cell abundance (data not shown) during the whole time series was dominated by the pennate diatoms (60%), and included the species Asterionella sp., Thallassiothrix sp., Thallassionema sp. and Grammatophora sp. The centric diatoms abundance (30%) was characterized by Chaetoceros sp. and Thallassiossira sp. while the dinoflagellates were represented (9%) by Gymnodinium sp. and Prorocentrum sp. (Giles-Guzma´n, pers. comm.). Nitrate (NO3 " ) concentration differed between the surface and 10 m depth during stratified conditions for the first 3 days. Significantly higher values were measured at 10 m depth than at the surface (Figure 8). On the 4th day, when the water column became vertically homogeneous, nitrates decreased, reaching minimum values. On Day 7, higher nitrate concentrations (Figure 8) were reached under greater turbulence conditions [PE<3 J m "2; Figure 6(c)].

1

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F 6. Time series from 26 August to 2 September 1986 of: (a) temperature, (b) salinity and (c) stratification parameter. The points represent the daily averaged data from 10.00 to 16.00h. For temperature and salinity: , surface data; , 10 m depth data. The bars represent 1 standard deviation (n=4).

Vertical mixing and primary production 141 3

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F 8. Time series of nitrate (NO3 " ) concentration. The points represent the daily averaged data from 10.00 to 16.00h for surface ( ) and 10 m depth ( ). The bars represent 1 standard deviation (n=4).

Zeu (m)

24

measured during stratified and mixed conditions, while the lowest values were mainly associated with intermediate mixing conditions [Figures 9(a) and 6(c)]. The hourly carbon assimilation rate and the 5 m integrated phytoplankton biomass were positively correlated [Figure 9(b); r=0·70, P<0·05]. Both primary productivity and chlorophyll a had high values during water-stratified conditions, while a strong decrease in biomass and productivity was present during the 4th and 5th days [Figures 7(a) and 9(a)]. During stratified conditions, high levels of primary productivity were maintained because of the larger phytoplankton crop. Hourly integrated production could be predicted more accurately from changes in chlorophyll a for the first 5 days [Figure 9(b)]. The photosynthetic assimilation ratios (PB) measured in BLA ranged from 3·72 to 9·30 mgC (mg chla) "1 h "1 [Figure 10(a)]. These values are comparable to those reported previously for this Bay (Gilmartin & Revelante, 1978; Mun˜oz-Barbosa et al.,

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F 7. Time series from 26 August to 2 September 1986 of: (a) chlorophyll a [the points represent the daily averaged data from 10.00 to 16.00h for surface ( ) and 10 m depth ( )]; (b) relationship between the euphotic depth and the 10 m depth integrated chlorophyll a; and (c) euphotic depth. The bars represent 1 standard deviation (n=4).

142 F. Delgadillo-Hinojosa et al. 70

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F 9. Time series from 26 August to 2 September 1986 of: (a) hourly integrated primary production (HIP); and (b) relationship between 5 m depth integrated chlorophyll a concentration and the hourly integrated productivity in Bahia de Los Angeles. Numbers represent the day sampled.

24 Zeu (m)

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10 y = –0.82x + 8.35 r2 = 0.50 8

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1991) and the central region of the Gulf of California (Alvarez-Borrego & Gaxiola-Castro, 1988). The lowest PB value [3·7 mgC (mg chla) "1 h "1] was measured under stratification of the water column, increasing to the highest value [9·3 mgC (mg chla) "1 h "1] during mixing conditions [Figures 10(a) and 6(c)]. PB showed an inverse relationship with the water-column stratification parameter [Figure 10(c); r= "0·71, P<0·05), and a positive association with light availability (Zeu) in the water column [Figure 10(b); r=0·85, P<0·05]. The estimated DIP ranged from 0·57 to 1·28 gC m "2 day "1 [Figure 11(a)]. These values are within the range reported previously for the Gulf of California (Alvarez-Borrego & Lara-Lara, 1991). Daily primary production values changed in a similar way to HIP, with higher productivity levels during stratified and mixed conditions, while the lower values were associated with intermediate mixing conditions. Daily primary production had values close to 1·0 gC

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F 10. (a) Daily variability of phytoplankton assimilation ratios (PB); (b) relationship between PB and calculated euphotic depth (Zeu); and (c) relationship between PB and the stratification parameter (PE).

m "2 day "1 during high stratification, decreasing to values of 0·6 gC m "2 day "1 on the 6th day [Figure 11(a)]. Lastly, the higher DIP values were found at the end of the study with greater turbulence conditions [PE<7 J m "2; Figure 6(c)]. The daily integrated primary production was positively correlated with the nitrate concentration [r=0·74, P<0·05; Figure 11(b)].

Vertical mixing and primary production 143 60

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F 12. Relationship between averaged wind speed (from 00.00 to 10.00h) and the two-hourly stratification parameter from 10.00 to 16.00h for each day sampled.

1.2 1.0 0.8 y = 0.086x + 0.446 2 r = 0.55

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6 – –2 NO3 (mmol m )

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F 11. (a) Daily variability of integrated primary production (DIP); (b) DIP vs 5 m depth integrated nitrate concentration in Bahia de Los Angeles from 26 August to 2 September 1986.

Discussion Hydrography Solar heating, wind stress and water exchange with the adjacent Ballenas Channel creates a vigorous circulation in BLA. During summer, a high heat flux occurs, promoting the vertical stratification in the northern Gulf of California (Lavin & Organista, 1988). However, excepting Amador-Buerrostro et al.’s model (1991) there is no information assessing the relative contribution of the tide and/or wind affecting the vertical mixing and surface circulation in BLA. Amador-Buerrostro et al. (1991) concluded that wind-induced currents in BLA are 10-fold greater than tide-induced currents. These authors pointed out that the bathymetry of BLA together with the wide communication with the adjacent Ballenas Channel creates a minor tidal effect on the surface circulation and the structure of the water column. Similarly, Figure 12 shows that wind speed was highly correlated with the stratification parameter. Thus, the relationship between wind speed and PE suggests that the

wind is the most important source of energy in BLA, which modifies the vertical structure of the water column producing vertical mixing in the Bay. The water column was thermally stratified for the first 3 days, the temperature differences up to 2 )C between the surface and 10 m depth [Figure 6(a)]. In contrast, on the 4th and 7th days, the water column became vertically homogeneous as a result of strong vertical mixing associated with wind speeds up to 10 m s "1. Therefore, under neap tide conditions, low wind speeds and, consequently, a higher residence time, the high heat flux promotes a stratified water column. Once the wind speed increased, it became an important source of energy for producing vertical mixing, and changing the water-column structure in this Bay [Figures 6(c) and 12]. Nevertheless, the wind is also an important factor controlling the surface circulation. For instance, for the first 5 days, warmer waters were recorded at the sampling station, while at the 7th and 8th days, the temperature suddenly declined [Figure 6(a)]. At least partially, this temperature pattern can be explained using Amador-Buenrostro et al.’s surface circulation model (1991) of BLA under typical summer conditions. During the whole time series, the wind speed ranged from 0·5 to 13 m s "1. The predominant wind direction was south-easterly until the 6th day, and then south-westerly for the last 2 days (Figure 5). Thus, the south-easterly wind induced the water from the Ballenas Channel in through the southern mouth. Surface water was advected in two main directions inside the Bay, then exited from the northern mouth (Figure 2). As the surface water travelled south to north inside the Bay, it had a long residence time,

144 F. Delgadillo-Hinojosa et al. 8 (a) 6 ∆ chl a (mg m–3)

gained heat and became saltier [Figure 6(a,b)]. This scenario explains the arrival of warmer water from inside the Bay at the sampled station during the first 5 days. The decrease of temperature during the last 2 days is explained by the advection of colder waters coming from outside the Bay due to the change in wind direction and increased water exchange with the adjacent Ballenas Channel. Thus, this study shows that the daily variability of temperature and salinity reflected the significance of the wind stress forcing the surface circulation and producing vertical mixing in this Bay.

4

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Phytoplankton biomass 2

∆ NO3 (mmol m–3)

It is difficult to distinguish the effect of vertical mixing and advection upon phytoplankton biomass in coastal systems. However, in BLA, the phytoplankton biomass was controlled by the intensity of turbulence and advection. At the beginning of the study, higher water stratification promoted an increase of phytoplankton biomass at 10 m depth, associated with the higher nutrient concentrations [Figures 7(a) and 8]. When the water column was mixed, smaller differences of chlorophyll a between the surface and 10 m depths were recorded. In contrast, greater chlorophyll a differences were measured during stratification [Figure 13(a)]. This figure suggests that the phytoplankton had a moderated vertical transport due to smaller turbulent energy during water-stratified conditions (PE>40 J m "2). In contrast, with water-mixed conditions (PE<20 J m "2) and wind speeds up to 3 m s "1 (Figure 12), the phytoplankton cells were vertically mixed as a result of the higher turbulent energy, indicating that the wind-induced mixing plays a major role controlling the vertical gradient of phytoplankton in the Bay. It is difficult to distinguish between in situ phytoplankton growth and advection of cells when data are collected at one point alone (Balch, 1981). Likewise, the phytoplankton biomass can only accumulate when the growth rate exceeds advective loss (Day et al., 1989) and grazing rates. Thus, the increase of phytoplankton biomass at 10 m depth suggests a higher growth rate of phytoplankton under stratified conditions. On the 4th day, stronger winds (up to 10 m s "1) coming from the south-east were recorded, thus promoting the more intense circulation in agreement with Amador-Buenrostro et al.’s model (1991). A drastic decrease in biomass at 10 m depth was recorded on the 4th day, indicating that washout is very important in removing phytoplankton cells from BLA [Figure 7(a)].

(b)

1

r2 = 0.49 y = 0.020x + 0.15

0 0

15

30 PE (J m–2)

45

60

F 13. Relationship between: (a) chlorophyll a gradient and the stratification parameter (PE); and (b) nitrate gradient and PE. The gradients were calculated as the difference between 10 m depth and surface values.

The negative relationship between the integrated phytoplankton biomass and Zeu suggests that the light attenuation in the water column was controlled mainly by the phytoplanktonic biomass [Figure 7(b)]. Therefore, Zeu presented an increased trend from Day 1 to the end of the time series, suggesting an enhanced availability of light levels at the first 5 m throughout the sampled period [Figure 7(c)]. Photosynthetic assimilation ratio The effects of vertical mixing on phytoplankton are generally not direct. Rather, the effects are mediated through the agency of light and/or nutrient fluctuations (Demers et al., 1986). It has been suggested that intense vertical mixing can produce changes in phytoplankton light availability, which fluctuate faster than physiological adjusting of the phytoplankton cells (Falkowski, 1980; Demers et al., 1986). In contrast, under moderated vertical mixing, the cells can adjust

Vertical mixing and primary production 145

–1

–1

h )

10

8

6

y = 21.14x – 742.4 r2 = 0.73

B

P (mg C mg chl a

their metabolic activity (Vincent, 1980). From the present data, the authors deduced that phytoplankton cells had moderated vertical transport under stratified conditions (PE >40 Jm "2), while phytoplankton cells were vertically mixed when PE was less than 20 Jm "2. The effect of vertical mixing on phytoplankton was reflected in the photosynthetic assimilation ratios. In BLA, PB values were 1·8 times higher under mixed conditions than those measured under stratification, showing an inverse relationship with PE [Figure 10(c)], and a positive correlation with Zeu [Figure 10(b)]. The lowest PB value [3·7 mgC (mg chla) "1 h "1] was measured in stratified water-column conditions (PE >40 Jm "2), and with low levels of light for photosynthesis (k=0·31 m "1). In contrast, PB values were higher with enhanced light availability (k=0·15 m "1) and increased vertical mixing (PE <20 Jm "2) at the end of the study. These results suggest that the increase of PB was a product of the combined effect of vertical mixing of the phytoplankton through the light gradient in the water column, and the increased light availability throughout the time series. An inverse relationship was found between PB and PE [Figure 10(c)]. Similar observations were reported from experiments carried out in Bedford Basin (Cote & Platt, 1983), and during the summer in the Gulf of California (Alvarez-Borrego & Gaxiola-Castro, 1988). However, in estuaries (Demers & Legendre, 1982), fjords (Erga, 1989), the central Gulf of California (Gaxiola-Castro et al., 1995), and the Pacific coast of Baja California (Gonzalez-Morales et al., 1993), a positive relationship between PB and PE has been reported. The differences with the present results can possibly be attributed to the different environmental scales involved. In the above environments, the stratification processes occur over the long term, and this allows physiological adjustment of the photosynthetic system to varying light intensities (Demers & Legendre, 1982), favouring the positive relation between PB and PE. In contrast, the present authors studied the short-term variability of photosynthesis and water-column characteristics using the time series approach with daily experimentation in a very dynamic system; thus, recording the phytoplankton responses and the environmental variability on a scale of days. The short-term variability of the photosynthetic assimilation ratio was a result of the combined effect of the vertical mixing of the phytoplankton through the light gradient, and the increased light availability in the water column on a scale of days. These observations suggest that the vertical mixing of the water column is an important factor controlling the photosynthesis of the phytoplankton, and its scale

4 35.3

35.4

35.5

35.6

Salinity

F 14. Relationship between photosynthetic assimilation ratios (PB) and the 5 m depth averaged salinity in Bahia de los Angeles from 26 August to 2 September 1986.

of occurrence must be considered independently of the environment. It is known that the phytoplankton responses occur on the scale of hours to days (Ferris & Christian, 1991; Pre´zelin et al., 1991). Thus, the study of the vertical mixing effect on primary production must be made to the appropriate environmental scale. On the other hand, PB short-term variability can be explained using the circulation pattern under summer conditions proposed by Amador-Buenrostro et al. (1991). The present authors found a positive correlation between PB and salinity (Figure 14). Salinity showed an increasing trend from the 3rd day to the end of the time series [Figure 6(b)], with saltier water coming from inside the Bay for the first 6 days. In this context, the authors were recording the photosynthetic activity of phytoplankton that would be advected along the Bay from the south end. This explanation suggests that the increasing PB behaviour is a result of a physiological adjustment in the photosynthetic apparatus to increased light availability. Falkowski (1981) has suggested that changing light conditions lead to physiological photo-acclimations of the photosynthetic apparatus. Likewise, Tilzer (1989) has pointed out that nutrient variability is frequently associated to changes in the adaptive advantages among populations with different nutrient requirements. Thus, another possibility for increasing PB values could be the change in phytoplankton species composition in BLA; unfortunately, the present authors do not have sufficient data to prove this. Integrated primary productivity The higher values for the hourly integrated productivity were measured during stratified and mixed

146 F. Delgadillo-Hinojosa et al.

short-term variability of the HIP in this Bay was associated with variations in biomass and light availability.

80 2 r = 0.84

HIP (mg C m

–2

–1

h )

y = 0.00206x – 1.38

60

Nutrient limitation 40

20 140

210

280

350

BEo Zeu

F 15. Relationship between the hourly integrated primary production (HIP) and the composite parameter BEoZeu (#10 "2) from 26 August to 2 September 1986 in Bahia de Los Angeles.

conditions, while the lowest values were mainly associated with intermediate mixing conditions [Figures 9(a) and 6(c)]. The variable related to HIP was phytoplankton biomass (r=0·70, P<0·05). Hourly integrated production could be predicted from the integrated biomass during the first 5 days [Figure 9(b)]. Hourly integrated production had low values with intermediate mixing conditions [Figures 9(a) and 6(c)] due to low phytoplankton biomass [Figure 7(a)] and medium PB values [Figure 10(a)]. On the other hand, under water-stratified conditions, the high productivity value (58 mgC m "2 h "1) was due to the higher phytoplankton biomass relative to that recorded during the remainder of the time series [Figure 7(a)]. Furthermore, under mixed conditions, the HIP reached values of 60 mgC m2 h "1 due to the 1·8 times increase in PB during the last 2 days relative to the averaged PB for the first 3 days [Figure 10(a)]. It has been frequently demonstrated that primary productivity is a function of the phytoplankton biomass and light availability in nutrient-rich environments. For instance, in estuaries, the composite parameter BEoZeu has been used to evaluate the influence of the biomass and light availability on productivity. Cole and Cloern (1984) explained 80% of the variance in measured primary productivity of San Francisco Bay using the composite parameter BEoZeu. Keller (1988), De Madariaga and Orive (1989), and Cole (1989) used the same parameter to explain 80, 79 and 90% of the variability in productivity in the Narrangansett Bay, Guernica Estuary and Tomales Bay, respectively. The present authors found that 84% of the variation in HIP in Bahia de Los Angeles was explained with the parameter BEoZeu (Figure 15). The present results support the conclusion that the

Traditionally, it is believed that light and/or nutrients control the phytoplankton production in the marine environment. However, the consideration of a single parameter as the factor controlling phytoplankton productivity is often not totally satisfactory. In general, the effects of light and/or nutrients on phytoplankton are direct; however, the vertical mixing of the water column plays a major role in controlling the variability of nutrient concentrations and the exposure of phytoplankton cells to the light gradient in the water column (Demers et al., 1986). Therefore, changing light conditions lead to physiological photo-acclimation of the photosynthetic apparatus (Falkowski, 1981), while nutrient variability is frequently associated with changes in the adaptive advantages among populations with different nutrient requirements (Tilzer, 1989). It is known that phytoplankton responses occur on the scale of hours to days (Ferris & Christian, 1991; Pre´zelin et al., 1991). Thus, the variability or control of the productivity at a certain time scale must be discussed at the appropriate environmental scale (Harris, 1986). The present study attempted to show that the effects of light and nutrients on the primary productivity occurred at the same time in the BLA, promoted by hydrodynamics. These effects were reflected in different measures of productivity. For instance, the effect of irradiance on photosynthesis in the water column was shown by HIP and PB; measurements that reflect short-term (hours) responses of the phytoplankton. The effect of nutrients on productivity was also evident when the productivity was estimated on a scale of days (DIP). The nutrient limitation on primary production, particularly nitrogen, in the marine environment is a controversial subject matter (Hecky & Kilham, 1988; Howarth, 1988). For the first 6 days, the mean nitrate concentration at 10 m depth decreased at an approximate rate of 0·16 mmoles m "3 day "1 (Figure 8), suggesting that it is consumed in the Bay. Likewise, the averaged DIP was 0·95 gC m "2 day "1. In order to support these high mean daily productivities, a high nutrient supply rate is also required. Figure 11(b) shows that DIP increased when nitrate concentration increased. This relationship suggests that the increase in productivity is due to the rapid uptake and incorporation of the nitrogen to the phytoplanktonic biomass. It is generally considered that the primary

Vertical mixing and primary production 147

organic productivity is limited by a specific nutrient, thus, when it is added the productivity increases (Howarth, 1988). Also, the N/P ratio measured during the summer in the BLA was 1·19. An N/P ratio >30 indicates phosphorus limitation,. while ratios <10 indicate nitrogen limitation (Goldman et al., 1979; Dortch & Whitledge, 1992). Under these criteria, during Summer 1986, the productivity estimated as DIP in Bahia de Los Angeles was limited by the availability of nitrate. These results show the relative importance of nitrogen dynamics to primary production in this productive environment. Nevertheless, the positive relationship between the water-stratification parameter and the nitrate gradient suggests that wind-induced vertical mixing is controlling the vertical nutrient gradient, but not the nitrate availability [Figure 13(b)]. For instance, on the 4th day, when the highest wind speed was recorded, the lowest average integrated nitrate concentration—a measure of the nitrate availability—was found (23 mmol m "2). The advection of nutrient-rich water from outside of the Bay could be the main factor controlling the nutrient availability to the Bay. The authors propose the following scenario for the interaction between the circulation, primary productivity and nutrient availability in BLA. Outside the Bay, tidal mixing promotes the surface enrichment of nutrients (Alvarez-Borrego et al., 1978; BadanDangon et al., 1985), with a marked fortnightly frequency (Paden et al., 1991). Under typical summer conditions with wind blowing from the south-east, nutrient-rich water is advected into the Bay through the southern mouth, and a large volume of this water travels along the whole Bay coming out by the north mouth. During advection, phytoplankton nutrient uptake decreases the nutrient concentration to low levels. Thus, during summer, a clear nitrate–primary productivity relationship on a scale of days can be found in BLA [Figure 11(b)]. Outside the Bay, the neap/spring tidal cycle is very important and, combined with the intense wind forcing and solar heating, creates a vigorous circulation in BLA. Daily sampling must be carried out to describe properly the effect of circulation and vertical mixing on the phytoplankton biomass, primary productivity and nutrient availability in BLA. The patterns presented in this study would not be detectable without such frequent sampling. The ecology of coastal phytoplankton populations is extremely complicated, and the appreciation of this variability is closely related to the sampling strategy used (Roden, 1994). Finally, the findings presented here suggest that the physical structure of the water column, the energy

available for mixing, the advective processes associated, and the scale of environmental variability are important factors explaining the temporal differences of phytoplankton production of the coastal zone. Acknowledgements This research was funded by the Universidad Autonoma de Baja California (UABC) and the Secretarı´a de Educacio´n Pu´blica of Me´xico, under Project C-87-01-0137. The second author had a fellowship from the UABC during his sabbatical year at the Instituto de Investigaciones Oceanologicas. The chemical and physical variables were collected and analysed by R. Canino-Herrera, H. Castro-Castro and S. Ibarra-San˜udo. The authors also thank G. Hemingway, Scripps Institution of Oceanography (UCSD), for the facilities to count the primary productivity samples. Discussions with A. AmadorBuenrostro were very useful from the physical point of view of the work. Drawings were done by J. M. Dominguez and F. Ponce. The authors are grateful to David S. Tager for language corrections and syntax review of the final version of the manuscript. The comments and corrections of Brian E. Cole and an anonymous reviewer improved the final version of the manuscript significantly. References Alvarez-Borrego, S., Rivera, J., Gaxiola-Castro G., Acosta-Ruiz, M. J. & Schwartloze, R. 1978 Nutrientes en el Golfo de California. Ciencias Marinas 5, 53–71. Alvarez-Borrego, S. & Gaxiola-Castro, G. 1988 Photosynthetic parameters of Northern Gulf of California Phytoplankton. Continental Shelf Research 8, 37–47. Alvarez-Borrego, S. & Lara-Lara, J. R. 1991 The physical environment and primary productivity of the Gulf of California. In The Gulf and Peninsular Province of the Californias (Dauphin J. P. & Simoneit B. R., eds). AAPG Memoir 47, 555–567. Amador-Buenrostro, A., Serrano-Guzma´n, S. & Argote-Espinoza, M. L. 1991 Numerical model of the circulation induced by the wind at Bahia de Los Angeles, B.C., Mexico. Ciencias Marinas 17, 39–57. Badan-Dango´n, A., Koblinsky, C. J. & Baumgartner, T. 1985 Spring and summer in the Gulf of California: observations of surface thermal patterns. Oceanologica Acta 8, 13–22. Badan-Dango´n, A., Hendershott, M. C. and Lavin, M. F. 1991 Underway Doppler current profiles in the Gulf of California. Transactions American Geophysics Union 72, 209–218. Balch, W. M. 1981 An apparent lunar tidal cycle of phytoplankton blooming and community succession in the Gulf of Maine. Journal of Experimental Marine Biology and Ecology 55, 65–77. Bray, N. A. & Robles, J. M. 1991 Physical oceanography of the Gulf of California. In The Gulf and Peninsular Province of the Californias (Dauphin J. P. & Simoneit B. R., eds). AAPG Memoir 47, 511–553 Canino-Herrera, R., Gaxiola-Castro, G. & Segovia-Zavala, J. A. 1990 Effect of physical processes on the variation of chlorophyll, seston and primary productivity in the northern inlet of Bahia de Los Angeles (summer 1986). Ciencias Marinas 16, 67–85.

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