- Email: [email protected]
Effects of physical phenomena on the distribution of nutrients and phytoplankton productivity in a coastal lagoon
Estuarine, Coastal and Shelf Science (1982)
X5,3 17-335
Effects of Physical Phenomena on the Distribution of Nutrients and Phytoplankton Productivity in a Coastal Lagoon
Roberto Millan-Ntiez,” and David M. Nelson*
Saul Alvarez-Borregob
“School of Oceanography, Oregon State University, Cowallis, Oregon 97331, U.S.A. and Tentro de Investigation Cientifica y Education, Superior de Ensenada, Espinoza 843, Ensenada, Baja California, Mexico Received 19 April
1981 and in revised form 21 October 1981
Keywords: time series; spectral analysis; nutrients; coastal lagoons; Baja California coast
productivity;
upwelling;
Sea level, salinity, temperature, nitrate, nitrite, phosphate, silicate, chiorophylls u, b and c and their phaeophytins, phytoplankton abundance and phytoplankton productivity time series were generated for the mouth and three interior locations of Bahia San Quintin, Baja California, Mexico, for IO days during summer of 1979. The samples were taken once every 2 h. This was done to describe space and time variability of these ecological properties and to elucidate the main factors that cause this variability. Upwelling events bring nutrient reach waters near the bay mouth and tidal currents propagate those waters throughout the bay. Nutrient remineralization at the sediments and the effect of turbulence induced by tidal currents and winds increase nutrient concentrations in the interiors of the bay. In comparison with available information on nutrients limited growth of planktonic algae, nutrients seemed not to be limiting to phytoplankton growth during the sampling period. Phytoplankton cell abundances at the extremes of the lagoon are an order of magnitude lower than at the mouth due to greater turbidity. Chlorophyll concentrations at the extremes are about one-third of those of the mouth. Primary productivity decreases from the mouth to the interiors in the same manner as chlorophyll does. There is not a significant difference in cell size between phytoplankton at the bay mouth and those at the extremes of the bay. Primary productivity in the bay is comparable to the productivity maxima of other upwelling areas. There is no clear permanent dominance of diatoms over dinoflagellates, or vice versa, at any location in the bay. The alternation of upwelling and nonupwelling played an important role, together with that of the spring-neap tide cycle, in producing low frequency (< 0.01 cycles h-l) temporal variability of ecological properties throughout the bay.
Introduction During the last eight years, there has been an increased interest in developing maricultures in the coastal lagoons of the Baja California peninsula. Most of these coastal lagoons are very 3x7 0272~7714/82/090717+19
$03.00/o
@ 1982 Academic Press Inc. (London)
Limited
318
R. Millan-Nuiiez,
S. Alvarez-Borrego
& D. M. Nelson
much in their natural state. There is still a unique opportunity to carry on basic ecological studies in some of them before significant changesare made by man’s activities. These studiescan give us the background ecology againstwhich the situationsof the future may be compared.Also, the studiescan be designedto gain useful information that might be applied to make rational decisionsasmaricultures are developed. The objectives of this work were to study Bahia San Quintin to determine the effects of the diurnal and semidiurnal tides, the alternation of the spring-neap tides, the alternation of upwelling events off the bay mouth and other physical factors on the space and time variability of nutrients, phytoplankton abundanceand phytoplankton productivity.
PACIFIC OCEAN
Figure
I. Bahia
San Quintin.
Time
series anchor
stations
(A).
Bathymetry
inmeters.
Study area Bahia San Quintin is a coastal lagoon located (30%.+‘-30°30’N, II~~~~‘-II~~~I’W) on the Pacific coast of Baja California, Mexico (Figure I). The bay is some 300 km south of the Mexico-U.S.A. border. The bay is ‘Y’ shapedwith a single permanent entrance at the foot of the Y. It has a north-south orientation, and an area of about 41.6 kms. The lagoon is extremely shahow, and at lower low tide approximately 20% of the bottom is exposedto the
Nutrient
distribution
and phytoplankton
productivity
319
air. There are narrow channelsthat rarely exceed 8 m in depth. The western arm is named Bahia Faka and the easternarm is called specifically Bahia San Quintin (Barnard, IgGz). The climate is arid along the coast and in the mountains. Annual precipitation (j-10 cm) occurs mostly in winter. The relatively cool California Current offshore of Bahia San Quintin is partly responsiblefor the benign climate of the region. Upwelling occurs in the open oceanimmediately off the mouth of the bay during spring and summer(Dawson, 1g51), a result of north-westerly winds during theseseasons.Bakun (1973) hascalculatedupwelling indices for the west coastof North America, and his calculationsshow favourable upwelling conditions throughout the whole year for latitudes 27-33”N. Maximum upwelling indices occur from March to June. Influence of upwelling on seawaterproperties at the mouth of San Quintin Bay was demonstratedby Lara-Lara et al. (1980). The mainly shallow mudflat character of the bay provides for two kinds of dominant vegetation. One is a marine flora consisting of eelgrass,Zostera marina, which forms broad, densestrands occupying the greater part of the muddy bottom of the lagoon. The other is saltmarshflora of extensive development along nearly half of the low-lying margins of the lagoon subjectedto tidal flooding (Dawson, 1962). Non-synoptic samplingof surfacewater, covering the whole bay in about 8 h once every month, showedhorizontal salinity, temperature, inorganic phosphate and silicate gradients, with values increasing from the mouth to the extremes of the lagoon (Chavez-de-Nishikawa & Alvarez-Borrego, 1974; AlvarezBorrego et al., 1975; Alvarez-Borrego & Chee-Barragan, 1976); and highest chlorophyll a concentrations were always found in the area between the mouth and the vertex of the Y, with values decreasingtoward the extremes (Lara-Lara & Alvarez-Borrego, 1975). Phytoplankton abundancewasfound to decreasetoward the extremesespeciallytoward the headof the easternarm, where valuesare an order of magnitude smallerthan at the mouth (AlvarezBorrego & Lopez-Alvarez, 1975). Due to shallow depths and the turbulence causedby tidal currents, there are no significant vertical gradients in the different seawaterproperties in most of the bay. At the mouth (approximately IO m depth) surface and bottom values of seawaterproperties may differ significantly. But, due to the strong tidal currents, sometimes the gradients reverse.Temperature differencesare usually a few tenths of a degree; although, sometimesthey are ashigh as3 “C with warmer water at the surface. Salinity differencesare ashigh aso-2%,,, but usually much lower. Chlorophyll a concentrationsdo not show a significant vertical gradient at the mouth (Alvarez-Borrego et aE., xg77a). Alvarez-Borrego et al. (rg77a, b) generated 26-hour time series of salinity, temperature, oxygen, phosphate, nitrate, chlorophylls and meteorologicalvariables once every seasonat the mouth of the bay. Wowever, theseinvestigators realized that sampling for such short periods was like looking at reality through slits, and general conditions could not easily be separatedfrom irregular or episodicevents. Lara-Lara et al. (1980) generatedan IS-day time series,alsoat hourly intervals, of several ecological variables for the mouth of Bahia San Quintin, during the summer of 1977. Variableswere: sealevel, current velocity, temperature, salinity, oxygen, inorganic phosphate, chlorophyll a, seston, phytoplankton speciesabundance, particulate organic carbon and nitrogen and primary productivity. They concludedthat alternation of upwelling events was the main causeof variability for all properties except temperature. Semidiurnal tides were the main cause of variability for temperature. Diatoms were always the most abundant phytoplankton group. Primary productivity was always greatestat the surface, with a mean value of 27 mg C mW3h-l through the sampling period. Maximum surface productivity valueswere obtained for the upwelling relaxation period (up to ++rng CmW3h-l). The mean surface assimilationratio was6.6 mg C (mg chl. a)-rh-l, which indicatesnutrient-rich waters.
326
R. Milian-Nu?iez,
S. Alvarez-Borrego
& D. M. Nelson
Methods Field sampling methods Time series sampling was carried out, day and night, simultaneously at four anchor stations (Figure I), from 25 June to 5 July 1979. Samples were collected only at the surface. Tide height was measured at Molino Viejo (Station D, Figure I) by a Fisher and Porter Model 1550 digital tide gauge. In order to generate the sea level time series for the other three stations (A, B and C, Figure I) the phase lag was taken from Monreal(1980). Water temperatures were read off bucket thermometers every z h. Salinity was analysed at a shore-based laboratory (Figure I) with a conductivity salinometer, Beckman Model 118WAzoo. Salinity samples were taken every z h at Station D but only twice a day at the other stations. Nutrients, chlorophylls and phytoplankton samples were always taken from the same Van-Dorn bottle, sampling every z h. Two drops of a saturated solution of HgCl, were added to each nutrient sample immediately after collection. The samples were frozen and transported to the School of Oceanography, Oregon State University, where they were analysed for phosphate, silicate, nitrate and nitrite, using a Technicon II AutoAnalyzer (Atlas et al., 1971). Chlorophyll samples were obtained using o.45-l.rrn pore-sized MilliporeR filters. Filters were frozen to be transported to the laboratory of Centro de Investigation Cientifica y de Education Superior de Ensenada. Chlorophyll analysis was done basically by the SCORUNESCO (1966) method, but with some modifications. Second readings at 665, 645 and 630 nm were done after acidification, following Lorenzen (1967). A r-to-r volume solution of 90% acetone and dimethyl s&oxide was used as a solvent to improve the pigment extraction (Shoaf & Lium, 1976). Spectrophotometric equations developed by Millan-Nuiiez & Alvarez-Borrego (1978) were used to estimate concentration of chlorophylls a, b and c and phaeophytins a, b and c. The equation for chlorophyll a is exactly the same as that from Lorenzen (1967) due to the chlorophyll b : phaeopigment 6 and chlorophyll c : phaeopigment c ratios at 665 nm are equal to one. Phytoplankton abundance by gross taxonomic groups was determined by the ctermiihl (1958) inverted scope technique using a Carl Zeiss invertoscope D microscope. Three times a day during daylight hours, surface (N 0.5 m) carbon-14 incubations of I h duration were done at high, intermediate, and low tide. Seawater samples for carbon-r.+ incubations were not taken from the same Van Dorn sampling for chlorophyll and phytoplankton. Sampling was done specifically for the incubations. Carbon-14 samples were obtained using o.45-prn pore sized Millipore R filters. The vials containing the filtered samples were transported to the O.S.U. School of Oceanography where the radioactivity of the samples was determined in a scintillation spectrometer. Inorganic carbon-14 was purged from the vials with nitrogen gas before the radioactivity measurements. Conversion of radioactivity to carbon productivity was done as indicated by Strickland & Parsons (1972). Statistical analysis We subjected our temperature, salinity, sea level, nutrient and chlorophyll time series to spectral analysis. This statistical operation may be regarded as an analysis of variance in which the total variance of a variable or property fluctuation is partitioned into contributions arising from processes with different characteristic time scales (Platt & Denman, 1975). Thus, spectral analysis of a record of observations results in a sorting of total variance of the record into its component frequencies. The spectral analysis results presented here were
Nutrient
distribution
and phytoplankton
productivity
321
computed with a fast Fourier transform algorithm. The output presents the frequency componentsin cyclesh-l. Results Description
of time series of seawater properties
Tidal height time seriesshoweda characteristic semidiurnal behaviour and the sequenceof spring and neap tides. Maximum tidal height range was about 2 m (Figure 2). Salinity time series at Station D also had a semidiurnal behaviour, with high values corresponding in general with low tides, and vice versa. Salinity throughout the whole bay had a general tendency to increasewith time during the sampling. Salinity increasedfrom the bay mouth to the extremes of the bay with a mean difference of about 2.2x, between Stations A and D (Figure 2). Salinity rangeswere: 33*40-34.57x0for Station A; 33&+-34a42%o for Station B; 33*93-34.76x0 for Station C; and 34.63-3~69%~for Station D. Temperature time seriesshowed a long wave feature at all sampling points (Figure 3). The time seriesat Station A showslong wave (IO days), diurnal and semidiurnalvariability, 3.0 2.5 -!z i .P 2! f i-
2.0 I.5
0.5
38i
35
(b)
-
341
z![!;
0
24
40
72
96
120
144
168
192
216
240
264
Time(h)
Figure z. (a) Tide height and (b) salinity time series (middle) station was sampled every z h. (c) Salinity time series (lower) B (A) and C (0). These stations were sampled at times of high
at Station D; this at Stations A (3), and low tide.
322
R. Millan-NuSez,
S. Alvarez-Borrego
& D. M. Nelson
while time seriesat Stations B, C, D, show only the long wave and diurnal features. High temperature values correspondedin generalwith low tides and vice versa. Diurnal temperature rangeswere smaller in the middle of the samplingperiod, due to neaptides. The ranges of temperature were: 12*8-19.8 “C for Station A; 16.4-22.8 “C for Station B; 17.7-21.8 “C for Station C; and 19*2-25.2“C for Station D. 20 19 16 17 16 I5 14 13 12
s e L g i:
23 22 21 20 I9 I6 17
‘6
Time(h) Figure 3. Temperature time series at the four sampling C, D) indicate the stations. Numbers mark midnight.
stations.
The
letters
(A, B,
Nitrate time seriesfor Station A showed the long wave feature very clearly, with high values at the beginning and at the end (Figure 4), whereasthosefor Stations B, C and D did not show the feature clearly, although values at the beginning of the sampling were in generalhigher than those towards the end. Nitrite tended to showa similar behaviour to that of nitrate (not illustrated). The rangesof nitrate and nitrite (PM), were respectively: 0.1-12.5 and c~oo-oq for Station A; 0.1-41 and o.oo-o.30 for Station B; 0.3-4’5 and 0~07-0~25for Station C; and 0.2-28 and 0~01-0~25 for Station D. Phosphate and silicate time seriesfor Station A alsoshowed the long wave feature with high values at the beginning and end of the samplingperiod, and lower values in the middle (Figures 5,6). Their time seriesfor Stations B, C and D did not show the long wave. Spikes in phosphateconcentration occurred at Station B on the sixth and ninth samplingdays, but no such spikeswere obvious at the other samplingpoints. Possiblythe smallphosphatespike shown at Station A, on the sixth samplingday wascorrelated with the first spike at Station B
Nutrient distribution and phytoplankton productivity
323
4-
C
2O-
Time(h)
Figure
4. Nitrate
time series at the four
sampling
stations.
Numbers
mark
midnight.
(Figure 5). There was no clear tendency for phosphate to increase or decrease from the mouth to the interiors of the bay. Silicate concentration in general increased from the bay mouth to the extremes (Figure 6). The ranges of phosphate and silicate (PM) were, respectively: 0.5-2.48 and 4.9-232 for Station A; 0.72-2.86 and 1.2-19.7 for Station B; 0.62-1.59 and 66-245 for Station C; and 0.36-1.93 and 10.7-32.8 for Station D. The time seriesat Station A for chlorophyll a, 6 and c showed a general tendency to increasewith time during sampling(Figure 7, chlorophylls b and c not illustrated). Generally, the highest values for all three pigments at the bay mouth station were found at the end of the sampling period. Pigment time seriesat Stations B, C and D showed a complicated patchiness. The ranges of chlorophylls a, b and c (mg mW3)were respectively: 0’5-37.9, oo-3.8 and oa-16.1 for Station A; 0.5-18.7, 0.0-1.9 and oo-12.6 for Station B; 0.5-4.8, oo-2.7 and 0.2-8.7 for Station C; and 0.5-4.9, 0.0-2.0 and 0.1-7.0 for Station D. Phaeopigment time seriesshoweda very patchy distribution at all four sampling points. Phaeophytins b and c often were not significantly different from zero (not illustrated). Phaeophytin a concentrations were lower than their respective chlorophyll concentrations (Figure 8). Phytoplankton abundance time seriesat the four locations did not show the long wave feature of temperature and nutrients; instead, these time series showed a very patchy distribution (Figure 9). In general phytoplankton total abundance decreasedfrom the bay mouth to the bay extremes. At the extremes, abundancewas an order of magnitude lessthan at the bay mouth. At Station B there were patchesof high abundanceduring the first half of the sampling period. Cell abundance at Station B was similar to that at Stations C and D during the secondhalf of the samplingperiod. There wasno clear, permanent dominanceof diatoms over dinoflagellates,or vice versa, at any of the samplingstations except Station B,
324
R. Mdlun-NuEezs,
3.0
’
2.5
-
2.0
-
I.5
-
I.0
-
S. Alvarez-Borrego
&? D. M. Nelson
A
0.5
-
2.5
0 0
I
I
I
I
24
48
72
96
I I20
I 144
I 168
I 192
I 216
I 240
264
Time(h)
Figure 5. Phosphate midnight.
time
series
at the
four
sampling
stations.
Numbers
mark
where diatoms outnumbered dinoflagellatesfor most of the sampling period (Figure IO). For any given taxonomic group there was no consistent difference in cell size between Stations A, B, C and D. The rangesof phytoplankton total abundance(cells ml-l) were: 42-1815 for Station A; 43-2580 for Station B; 20-182 for Station C; and 18-246 for Station D. Phytoplankton productivity time seriesshowed a very irregular variation at Stations A and B (Figure II). There was a tendency for productivity to increasewith time during sampling at Station A, but not at Station B. This correspondedwith pigment changeswith time at the two stations. Primary productivity alsoshoweda tendency to decreasefrom the bay mouth to the extremes. Assimilation ratios showedirregular variation with time at all stations; however, mean values at each location were not significantly different from one another. Means and rangesof phytoplankton primary productivity (mg C m-8 h-r) were respectively: 33.4, 5gq.4 for Station A; 16.5, 16-63’0 for Station B; 12’5, 2’2-23.4 for Station C; and 12’3, 1y-z7~4 for Station D. Means and rangesof assimilationratios (mg C (mg chl. ~a)-1h-l) were respectively: 6*4,06-13.7 for Station A; 7.8,0.8-262 for Station B; 5.4, ~6-12.5 for Station C; and 6.0,0.8-15-o for Station D.
Nutrient
distribution
and phytoplankton
productivity
32.5
25 20
0
24
48
72
96
120
144
168
192
216
240
264
Time ( h 1 Figure
6. Silicate
time series at the four
sampling
stations.
Numbers
mark
midnight.
Spectral analysis of time series
The tide variance spectrum showedmost of the variance at the diurnal (frequency -0.041 cycles h-r) and semidiurnal (frequency ~50.083 cycles h-l) periods (Figure 12). The variance spectra of all other seawaterproperties tended to show high variance components at these two frequencies although distinct peakswere not always obvious (Figures 12-14). Salinity, temperature, nitrate (Figures 12-14), and phosphate, silicate and sometimes chlorophyll a (not illustrated) clearly showed a high variance component at the lowest frequency (N 0.0025 cycles h-l). Discussion Alvarez-Borrego & Alvarez-Borrego (in press) generated r-year hourly temperature time seriesfor the samefour locationsasthis work from May 1979 to May 1980. Their time series for the Bahia San Quintin mouth showsthe alternation of upwelling events in the adjacent oceanic area from May to September. Lara-Lara et al. (1980) clearly showedthat summer seawatertemperatures near 12 “C at the Bahia San Quintin mouth are the product of upwelling, becausedissolvedoxygen percentagesaturation was found to be as low as 60% and this is characteristic of the upwelling water. Mixing by tidal currents during spring tides is
326
R. Millan-Nufiez,
S. Alvcwex-l3onego
f9 D. M. Nelson
50
0
24
48
72
96
120
144
168
192
216
240
264
Time(h)
Figure 7. Chlorophyll midnight.
c1time series at the four sampling stations. Numbers mark
not causing these low temperature values. During winter, tidal height ranges are greater and minimum temperatures at the bay mouth are only about 13.5 “C (Alvarez-Borrego & Alvarez-Borrego, in press). Alvarez-Borrego & Alvarez-Borrego’s temperature time series indicates that samplingfor the work reported here started at the beginning of an upwelling relaxation period, and ended when the strongest upwelling event of the year was about to begin. Also, samplingfor our study started at spring tides, continued through neaptides, and ended at the beginning of the following spring tides (Figure 2). Miniium temperatures during the upwelling event previous to our samplingwere about 12 “C, while they were about II “C for the one after our sampling (Alvarez-Borrego & Alvarez-Borrego, in press). Upwelling previous to our sampling was weaker than the first upwelling detected by Lam-Lara et al. (1980). Their minimum temperatures were below 12 “C, compared with a minimum temperature of 12-8 “C in our sampling; and their mazimum salinity was3~*78%~ comparedwith a maximum salinity of 34’57ymin our sampling at the bay mouth. They measuredphosphate values higher than 3 pi, compared with a maximum of ~5 pi in our case.Within the lagoon, the effects of the alternation of upwelling events and those of spring and neap tides on the variation of seawaterproperties are not easy to separate,becausetheir periods aresimilar.
Nutrient
distribution
and phytop2ankton
productivity
2 0
0
24
48
72
96
120 Time
Figure 8. Phaeophytin midnight.
a time
series
144
168
192
216
240
264
Numbers
mark
(h 1
at the four
sampling
stations.
Lara-Lara et al. (1980) concluded that variability at the mouth of Bahia San Quintin during summer was to a great extent caused by upwelling events, the tidal cycles and the solar radiation cycle. However, seston variability was mainly due to turbulence induced by winds and tidal currents; and inorganic phosphate was also greatly affected by this factor. Analyses of our time series from Stations B, C and D (Figures 12-14) show that variability of seawater properties is mostly controlled by the same main factors throughout the bay. The low frequency variance components are associated with the alternation of upwelling events and the alternation of spring and neap tides. Variance components at high frequencies (70.1 cycles h-l) are probably related to turbulence and irregular mixing conditions created by the lagoon bathymetry and associated heating by solar radiation input. The bay region between Stations A and B is very much affected by conditions in the oceanic region adjacent to the bay mouth. The greater residence times in the extremes cause different conditions to develop at Stations C and D. Salinity and temperature are higher at Stations C and D due to solar heating and evaporation. At Station D, higher temperatures and salinities indicate greater residence times than at Station C. The temperature long wave feature of Stations C and D (Figure 3) may be due to alternation of spring and neap tides, to the alternation of upwelling events that make their impact in the whole bay, or both. If this long wave feature was only due to the alternation of spring and neap tides, it would mean that spring tides were bringing colder water from the mouth region to Stations C and D while during neap tides the water was moving in and out near Stations C and D without much exchange with the oceanic region, the net effect being to warm the water relative to the spring tides. The salinity time series at Station D shows that this is not what happened (Figure 2). If it were, salinity values at the spring tide would be lower than those for neap tides. But they are not lower, they are indeed higher. Thus, the temperature long wave feature for Stations
328
R. M&n-Nuiiea,
S. Alvarez-Borrego
& D. M. Nelson
-I 2.5
2.5 0 24
46
72
96
120
144
Time
Figure g. Phytoplankton Numbers mark midnight.
abundance
time
166
192
216
240
264
(h)
series
at the
four
sampling
stations.
C and D (Figure 3) is partly due to the alternation of upwelling events. Upwelling is propagated throughout the bay. Our time seriesaretoo short to estimatethe lag of this propagation between the mouth and Stations C and D. Alvarez-Borrego & Alvarez-Borrego (in press) found that the upwelling lag, measuredby temperature change,is practically that of the tide. During spring tides, up to 80% of the bay water may go out. When an upwelling event occurs, water from the bay mixesto a certain extent with the newly upwelled water. Then, the flood flow brings water with changedproperties into the bay. Ultimately a dynamic equilibrium is reached unless properties outside the bay change again before equilibrium is established. Upwelled water has lower temperature, chlorophyll concentration, oxygen, phytoplankton abundance,primary productivity and higher inorganic nutrient concentrations and salinity (Lara-Lara et al., 1980). During the relaxation of upwelling, greater water residence time in the bay allows for an increasein chlorophyll concentration and assimilation
Nutrient
distribution
and pkytoplankton
productierity
329
80 60
0 24
40
72
96
120
144
Time
(h I
168
192
216
240
264
Figure IO. Percentage of the total phytoplankton abundance. The dashed corresponds to the fraction of dinoflagellates, below it the fraction of diatoms above the fraction of microflagellates. Numbers mark midnight.
area and
ratios and increasedconsumption of inorganic nutrients. High nitrate, nitrite, phosphateand silicate values at Station A at the beginning of the sampling (Figures 4-6) were due to an ending upwelling event. Lara-Lara et al. (1980) reported ratesof phytoplankton primary productivity in Bahia San Quintin mouth about two to three times greater than averagerates in the Gulf of California (Zeitzchel, of Oceanography, 1969),in the upwelling areasoff the west coastof Baja California (Scripps Institute data report, 1969) and off Oregon (Curl & Small, 1965). Productivity in Bahia San Quintin mouth during summer is similar to the highest productivity found by Small & Menzies (1981) in narrow bands of the nearshoreOregon upwelling system. High rateshave beenreported by Beerset al. (1971) and Barber et al. (I 971) for the Peru upwelling zone and by Huntsman & Barber (1977) and Smith et al. (1977) for the north-west Africa
330
R. MiUan-Nufiez,
S. Alvarex-Borrego
& D. M. Nelson
c
so
1
I
80 70
60 50 40 15 30 IO 20 i
Jz
5 IO
IO 20 5 IO 30
0 15
20
IO
IO
5
0
0 Time(h)
Figure I I. Phytoplankton productivity (mg C m- * h -‘) (U) ratio (mg C (mg chl. a)-3 (0 - - 0). Numbers mark midnight, numbers mark the dark period.
and assimilation the line above the
upwelling zone. Our results for phytoplankton primary productivity and assimilationratio for the bay mouth are very similar to those found by Lara-Lara et al. (1980). Surface primary productivity decreasesfrom the bay mouth to the two extremes, along with chlorophyll concentration (Figures 7, II). Mean assimilationratios are not significantly diierent at the four sampling points. At the extremes, while both primary productivity and chlorophyll Q values are about one-third of those at the bay mouth, total phytoplankton cell abundanceis only about onetenth (Figures 7, g, II). This indicates that chlorophyll content per cell at the extremes is about three times that at the mouth. There is not much difference in cell size between phytoplankton at the bay mouth and thoseat the extremesof the bay for any given taxonomic group. Beardall & Morris (1976) showed that the diatom Pheodactylum tricornutum can adapt to low light intensity, and this adaptation consistsof an increasedchlorophyll content
Nutrient
distribution
and phytoplankton
productivity
331
per cell and a decreasedrate of light-saturated photosynthesisper unit chlorophyll. If this observation is applicable to the natural phytoplankton assemblages in Bahia San Quintin, the higher chlorophyll per cell may be dueto the turbidity being greater,and light penetration less, at the extremes than at the bay mouth. Water at the extremes is more turbid (Secchi disc reaching about a half (1.5 m) of that of the bay mouth), resulting in lesslight penetration, and perhaps causing the phytoplankton cells to increasetheir chlorophyll content. At the extremeswe found IO times lower phytoplankton abundance,three timeslower productivity, three times lower total chlorophyll, three times higher chlorophyll per cell, higher turbidity (shallower Secchi disc depth) and shallowerbottom depth (2 vs 9 m) than at the bay mouth. Therefore, light limitation, probably resulting from absorption of light by resuspended bottom sediments,is probably the most important factor causingphytoplankton abundance and productivity to be much lower at the extremes.
(0) I I I02
iO-3
A I I 1O-2
10-l
IO’
10-2
10-3
II Frequency
(cycles
Figure 12. Spectral density of (a) tidal height mark the diurnal and semidiumal frequencies.
10-l
IO0
h-l)
and (b) salinity
at Station
D. Arrows
Seawater samplesfor carbon-14 incubations and phytoplankton abundanceanalyseswere not taken from the samesampling, so resultsof thesetwo setsof measurementsmight not be directly comparable. At Station B, phytoplankton abundancewaslow the last 5 days of the samplingperiod, while primary productivity washigh the seventh and eighth samplingdays (Figures 9, I I). A possibleexplanation for theselatter higher values is that they corresponded to patchesof high chlorophyll concentrations. Farfan (1981) sampledfor ammoniaconcentrations at the bay mouth at the sametime we did our sampling. She estimatedammoniaconcentrations ashigh as 3 pM. The mean of her results was around 0.7 FM, with somevalues near o PM. If we assumeRedfield’s model to apply roughly (Redfield et al., r963), reduced forms of nitrogen should have concentrations of at least a few PM. Comparison of measurednutrient concentrations (Figures 4-6) with numerous reported studies of the kinetics of nutrients limited growth of planktonic algae (Eppley et al., 1969; Paasche,1973; Fineko & Krupatkina-Akinina, 1974; Conway, 1977) indicates that nutrient concentrations were almost never low enough to limit phytoplankton growth during the sampling period at any of the four locations of the bay. At the mouth,
332
R. MiLTan-NuEez,
S. Alvare.z-Borrego
A
& D. M. Nelson
I04
IO3
IO2
IO’
IOa
, _
I lo! Y IO-
.I
104,
0
I
I02
IO’
,o-3
,o-2
10-l
100 Frequency
Figure 13. Spectral density the diurnal and semidiumal
of temperature frequencies.
I00 iI
10-3
(cycles
10-2
10-i
IO0
sampling
stations.
Arrows
h-‘1
at four
mark
during the relaxation of upwelling (Figures 4-Q the effect of nutrient uptake by the phytoplankton is clear. All inorganic nutrients were in high concentration at the beginning of the upwelling relaxation period and decreaseduntil the eighth or ninth samplingday. At the end of the samplingperiod all nutrient concentrationswere starting to increaseagain, asa result of the following upwelling event. At the bay mouth, during the first and Iast parts of sampling, with upwelling ending and starting respectively, greater nutrient concentrations correaponded to high tides (Figures z,4-6). The phosphatetime seriesfor Stations C and D showthat remineralization by bacterial oxidation of organic matter, mostly in the sediments,increase nutrient concentrations in the interiors of the bay (Figure 5). Mixing by tidal currents and winds stirs up the sediments bringing the nutrients into the water column. Uptake of phosphateand nitrogen compoundsby seagrasses may also be of importance in the spatial distribution of nutrients, but its effects cannot be estimatedfrom present data. Horizontal gradientsof nutrients within the bay are highly variable. Sometimesnutrient concentrations arehigher at the mouth than at the extremes. Such is the casefor nitrate, nitrite and phosphate
-
Nutrient
distribution
and planklankton
production
333
---
f104
II
to3
~ IY 1
to2
s c g z 5L
to’
“, ::
IO3
I
I
I=
L-
I
K
C
iI
I to*
to’ 4
too
II
L
to-3
L
to-*
10-l
I00 Frequency
Figure diurnal
ii:i
~
1
14. Spectral density of nitrate and semidiurnal frequencies.
10-3 (cycles
at four
10-2
to-’
IQ0
h-’ 1
sampling
stations.
Arrows
mark
the
during an upwelling event (Figures 4,s). And sometimesthe situation reverses,suchasduring the relaxation period. In general,the spatial distribution of nutrients is very patchy, asis the case for chlorophylls and phytoplankton abundance. In general, silicate concentration increasesfrom the mouth to the extremeseven during an upwelling event (Figure 6). At the extremesdissolutionsof exoskeletons,mainly of diatoms,may be the main sourceof dissolved silicate. The phosphatespike detected at Station B on the sixth sampling day and the more moderatespike detected on the ninth sampling day did not have a clear correspondences with the other nutrient values in the samestation, or with similar phosphatespikeson the other three samplingstations (Figures 4-6). At Station A there are small phosphatespikeslagging those at Station B by about I day (Figure 5). Lara-Lara et aE. (1980) detected a phosphate spike at the Bahia San Quintin mouth, which was correlated, to a certain extent, with an inorganic seston spike. They explained these spikes in terms of stirring of sedimentsby wind-induced turbulence. Station B, being at the baseof the ‘Y’ may have greater turbulence causedby tidal currents during ebb flow. If this is coupled with relatively strong winds, it may causea greater stirring effect in the sediments.If wind-induced turbulence alone were
R. Millan-NuZez, S. Alvarez-Borrego W D. M. Nelson
334
the causeof these spikes,they would have been detected at all four samplingpoints (or at least in a similar fashion at Stations B and C). The fact that the other nutrients did not show similar spikes indicates different remineralization processesfor them. Nitrogen from the sedimentsmay exist mostly in reduced forms. It is difficult to explain why there are no silicate spikes in correspondencewith phosphate spikes. Silicate had high values, but no pronouncedspikesat any time. Lara-Lara et al. (1980) found that diatomswere the mostabundant group at the bay mouth, followed by dinoflagellatesand microflagellates.They also found dinoflagellatesand microflagellateswere in greater abundance than diatoms toward the bay extremes. Our results show that diatomswere not always more abundant than dinoflagellatesat the mouth (Figure IO). Also, diatoms were often more abundant than dinoflagellatesat Stations B, C and D. Thus, there is no clear, permanent pattern for these phytoplankton groups throughout Bahia San Quintin. As the percentage of the total number of phytoplankton cells, microflagellatesshow a generalincreasefrom the bay mouth to the extremes(Figure IO). However, there is no increasein the absolute number of microflagellatesfrom the bay mouth to the extremesrather, their relative numerical contribution to the phytoplankton increasesbecause they maintain roughly constant number while both the diatomsand dinoflagellatesdecrease greatly in abundance.
Acknowledgements This work was supported by a graduate fellowship from the ConsejoNational de Ciencia y Tecnologia of Mexico to Roberto Millan-Nuiiez. It representsa segment of a long-term project by the Centro de Investigation Cientifica y de Education Superior de Ensenada. We thank Lawrence F. Small and Luis A. Codispoti for their criticisms and suggestions.
References Alvarez-Borrego, J. & Alvarez-Borrego, S. in press Temporal and spatial variability of temperature in two coastal lagoons. CalCoFi Reports. Alvarez-Borrego, S. & Chee-Barragan, A. 1976 Distribution superficial de fosfatos y silicates en BahiaSanQuintin,B.C.CiencinslMatis3(1), p-61. Alvarez-Borrego, S. & Lopez-Alvarez, C. 1975 Distribution de biomasa de fitoplancton por grupos taxonomicos en Bahia San Quintin, B. C. a traves de un ciclo anual. Reporte para I.N.P. de la S.I.C. y la Direccibn de Acuacultura de la S.R.H. (unpublished). Alvarez-Borrego, S., Ballesteros-Grijalva, G. & Chee-Barragan, A. 1975 Estudio de algunas variables fisicoquimicas supeficiales en Bahia San Quintin, en verano, otofio e inviemo. Ciencios Marinas
2 (21,I-9.
Alvarez-Borrego, S., Acosta-Ruiz, M. de J. & Lara-Lara, J. R. rg77a Hidroloda comparativa de las bocaz de dos antieatuarios de Baja California. Ciencias Marinas 4 (I), I-I I. Alvarez-Borrego, S., Lara-Lara, J. R. & Acosta-Ruiz, M. de J. 19773 Parametros relacionados con la productividad organica primaria en dos antiestuarios de Baja California. Cienckzs Marinas 4 (I), 1211.
Atlas,
I. E., Gordon, L. I., Hager, S. W. &Park, P. K. 1971 A practical manual for use of the Technicon’2 Auto Analyzer@ in seawater nutrient analyses. Revised Technical Report 215. Department of Oceanography, School of Science, Oregon State University, Corvallis. B&m, A. 1973 Coastal upwelling indices, west coast of North America, 1964-71. NOAA Technical Report NMFS SSRF-671.103 pp. Barber, T. R., Dugdale, R. C. MacIsaac, J. J. & Smith, R. L. 1971 Variations in phytoplankton growth associated with the source and conditioning of upwelling water. Investigation Pesque~a 35,171-x93. Barnard, J. L. 1962 Benthic marine exploration of Bahia de San Quintin, Baja California, Ig6o-1961. Poci& Naturalist a, 25 1-269. Beardall, J. & Morris, J. 1976 The concept of light intensity adaptation in marine phytoplankton: some experiments with Phaeodactylum triwrnutum. Marine Biology 37,377-387.
Nutrient
Beers,
distribution
andphytoplankton
productivity
335
J. R., Stevenson, M. R., Eppley, R. W. & Brooks, E. R. 1971 Plankton populations and upweiling off the coast of Peru, June 1969. Fishery Bulletin 69,85g-876. Chavez-de-Nishikawa, A. G. & Alvarez-Borrego, S. 1974 Hidrologia de Bahia San Quintin en inviemo y primavera. Ciencias Marinas I (z), 31-62. Conway, H. L. 1977 Interactions of inorganic nitrogen in the uptake and assimilation by marine phytoplankton. Marine Biology 39,221-232. Curl, H., Jr. & Small, L. F. 1965 Variations in photosynthetic assimilation ratios in natural marine phytoplankton communities. Limnology and Oceanography IO, Supplement R67-R73. Dawson, E. Y. 1951 A further study of upwelling and vegetation along Pacific Baja California, Mexico. Journal of Marine Research IO, 39-58. Dawson, E. Y. 1962 Marine and marsh vegetation. Benthic marine exploration of Bahia de San Quintin, Baja California. 1960-61. PaciJic Naturalist 3,275-280. Eppley, R. W., Roger, J. N. & McCarthy, J. J. 1969 Half saturation constant for uptake of nitrate and ammonium by marine phytoplankton. Limnology and Oceanography IO, grz-gzo. Farfan, B. C. rg8r Variability and tidal exchange of dissolved inorganic nitrogenous nutrients and suspended organic matter in San Quintin Bay, Baja California. M.S. Thesis, San Diego State University, San Diego, California. 58 pp. Fineko, 2. 2. & Krupatkina-Akinina, D. I<. rg74 Effect of inorganic phosphorus on the growth rate of diatoms. Marine Biology 26, 193-201. Huntsman, S. A. & Barber, R. T. 1977 Primary productivity off Northwest Africa: the relationship to wind and nutrient conditions. Deep-Sea Research 24,25-33. Lara-Lara, J. R. & Alvarez-Borrego, S. 1975 Ciclo anual de clorofilas y production organica primaria en Bahia de San Quintin, B. C. Ciencias Marinas 2 (I), 77-97. Lara-Lara, J. S., Alvarez-Borrego, S. & Small, L. F. 1980 Variability and tidal exchange of ecological properties in a coastal lagoon. Estuarine and Coastal Marine Science II, 613-637. Lorenzen, C. J. 1967 Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnology and Oceanoffraphy 12,343-346. Millan-Nufiez, R. & Alvarez-Borrego, S. 1978 Ecuaciones espectrofotometricas tricromaticas para la determination de clorofilas a, b, c y sus feofitinas. Ciencius Murims 5 (I), 47-55. Monreal-Gomez, M. A. 1980 Aplicaciones de un modelo de dispersion en Bahia San Quintin, Baja California, Mexico. M.S. Thesis, Centro de Investigation Cientifica y de Education Superior de Ensenada, Baja California. 88 pp. Paasche, E. 1973 Silicon and the ecology of marine plankton diatoms. II Silicate uptake kinetics in five diatoms species. Marine Biology 19,26z--269. Platt, T. & Denman, K. L. 1975 Spectral analysis in ecology. Annual Review of Ecology and Systematics 6,18g-zro. Redfield, A. C., Ketchum, B. H. & Richards, F. A. 1963 The influence of organisms on the composition of seawater. In The Sea volume 2 (Hill, M. N. ed.). Wiley-Interscience, New York. pp. 26-77. SCOR-UNESCO. 1966 Determination of photosynthetic pigments. Monographs in Oceanographic Methodology. pp. 1-18. Scripps Institution of Oceanography 1969 Cruise TO-64-1 and cruise TO-64-2 data report. University of California at San Diego, Scripps Institution of Oceanography Reference 69-4.57 pp. Shoaf, W. T. & Lium, B. W. 1976 Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnology and Oceanography 21,gz6-928. Small, L. F. & Menzies, D. 1981 Patterns of primary productivity and biomass in a coastal upwelling region. Deep-Sea Research A 28, rz3-149. Smith, W. O., Jr., Barber, R. T. & Huntsman, S. rg77 Primary production off the coast of Northwest Africa: Excretion of dissolved organic matter and its heterotrophic uptake. Deep-Sea Research 24, 35-47. Strickland, J. D. & Parsons, T. R. 1972 A practical hand-book of seawater analysis (2nd ed.). Bulletin of the Fisheries Research Board of Canada. 167 pp. Utermiihl, H. 1958 Zur Vervollkommnung der quentitativen Phytoplankton-Methodik. Mitteilungen der Internationalen Vereinigung fiir Theoretische und Angewandte Limnologie 9, x-38. Zeitzchel, B. 1969 Primary productivity in the Gulf of California. Marine Biology 3, zor-207.
X5,3 17-335
Effects of Physical Phenomena on the Distribution of Nutrients and Phytoplankton Productivity in a Coastal Lagoon
Roberto Millan-Ntiez,” and David M. Nelson*
Saul Alvarez-Borregob
“School of Oceanography, Oregon State University, Cowallis, Oregon 97331, U.S.A. and Tentro de Investigation Cientifica y Education, Superior de Ensenada, Espinoza 843, Ensenada, Baja California, Mexico Received 19 April
1981 and in revised form 21 October 1981
Keywords: time series; spectral analysis; nutrients; coastal lagoons; Baja California coast
productivity;
upwelling;
Sea level, salinity, temperature, nitrate, nitrite, phosphate, silicate, chiorophylls u, b and c and their phaeophytins, phytoplankton abundance and phytoplankton productivity time series were generated for the mouth and three interior locations of Bahia San Quintin, Baja California, Mexico, for IO days during summer of 1979. The samples were taken once every 2 h. This was done to describe space and time variability of these ecological properties and to elucidate the main factors that cause this variability. Upwelling events bring nutrient reach waters near the bay mouth and tidal currents propagate those waters throughout the bay. Nutrient remineralization at the sediments and the effect of turbulence induced by tidal currents and winds increase nutrient concentrations in the interiors of the bay. In comparison with available information on nutrients limited growth of planktonic algae, nutrients seemed not to be limiting to phytoplankton growth during the sampling period. Phytoplankton cell abundances at the extremes of the lagoon are an order of magnitude lower than at the mouth due to greater turbidity. Chlorophyll concentrations at the extremes are about one-third of those of the mouth. Primary productivity decreases from the mouth to the interiors in the same manner as chlorophyll does. There is not a significant difference in cell size between phytoplankton at the bay mouth and those at the extremes of the bay. Primary productivity in the bay is comparable to the productivity maxima of other upwelling areas. There is no clear permanent dominance of diatoms over dinoflagellates, or vice versa, at any location in the bay. The alternation of upwelling and nonupwelling played an important role, together with that of the spring-neap tide cycle, in producing low frequency (< 0.01 cycles h-l) temporal variability of ecological properties throughout the bay.
Introduction During the last eight years, there has been an increased interest in developing maricultures in the coastal lagoons of the Baja California peninsula. Most of these coastal lagoons are very 3x7 0272~7714/82/090717+19
$03.00/o
@ 1982 Academic Press Inc. (London)
Limited
318
R. Millan-Nuiiez,
S. Alvarez-Borrego
& D. M. Nelson
much in their natural state. There is still a unique opportunity to carry on basic ecological studies in some of them before significant changesare made by man’s activities. These studiescan give us the background ecology againstwhich the situationsof the future may be compared.Also, the studiescan be designedto gain useful information that might be applied to make rational decisionsasmaricultures are developed. The objectives of this work were to study Bahia San Quintin to determine the effects of the diurnal and semidiurnal tides, the alternation of the spring-neap tides, the alternation of upwelling events off the bay mouth and other physical factors on the space and time variability of nutrients, phytoplankton abundanceand phytoplankton productivity.
PACIFIC OCEAN
Figure
I. Bahia
San Quintin.
Time
series anchor
stations
(A).
Bathymetry
inmeters.
Study area Bahia San Quintin is a coastal lagoon located (30%.+‘-30°30’N, II~~~~‘-II~~~I’W) on the Pacific coast of Baja California, Mexico (Figure I). The bay is some 300 km south of the Mexico-U.S.A. border. The bay is ‘Y’ shapedwith a single permanent entrance at the foot of the Y. It has a north-south orientation, and an area of about 41.6 kms. The lagoon is extremely shahow, and at lower low tide approximately 20% of the bottom is exposedto the
Nutrient
distribution
and phytoplankton
productivity
319
air. There are narrow channelsthat rarely exceed 8 m in depth. The western arm is named Bahia Faka and the easternarm is called specifically Bahia San Quintin (Barnard, IgGz). The climate is arid along the coast and in the mountains. Annual precipitation (j-10 cm) occurs mostly in winter. The relatively cool California Current offshore of Bahia San Quintin is partly responsiblefor the benign climate of the region. Upwelling occurs in the open oceanimmediately off the mouth of the bay during spring and summer(Dawson, 1g51), a result of north-westerly winds during theseseasons.Bakun (1973) hascalculatedupwelling indices for the west coastof North America, and his calculationsshow favourable upwelling conditions throughout the whole year for latitudes 27-33”N. Maximum upwelling indices occur from March to June. Influence of upwelling on seawaterproperties at the mouth of San Quintin Bay was demonstratedby Lara-Lara et al. (1980). The mainly shallow mudflat character of the bay provides for two kinds of dominant vegetation. One is a marine flora consisting of eelgrass,Zostera marina, which forms broad, densestrands occupying the greater part of the muddy bottom of the lagoon. The other is saltmarshflora of extensive development along nearly half of the low-lying margins of the lagoon subjectedto tidal flooding (Dawson, 1962). Non-synoptic samplingof surfacewater, covering the whole bay in about 8 h once every month, showedhorizontal salinity, temperature, inorganic phosphate and silicate gradients, with values increasing from the mouth to the extremes of the lagoon (Chavez-de-Nishikawa & Alvarez-Borrego, 1974; AlvarezBorrego et al., 1975; Alvarez-Borrego & Chee-Barragan, 1976); and highest chlorophyll a concentrations were always found in the area between the mouth and the vertex of the Y, with values decreasingtoward the extremes (Lara-Lara & Alvarez-Borrego, 1975). Phytoplankton abundancewasfound to decreasetoward the extremesespeciallytoward the headof the easternarm, where valuesare an order of magnitude smallerthan at the mouth (AlvarezBorrego & Lopez-Alvarez, 1975). Due to shallow depths and the turbulence causedby tidal currents, there are no significant vertical gradients in the different seawaterproperties in most of the bay. At the mouth (approximately IO m depth) surface and bottom values of seawaterproperties may differ significantly. But, due to the strong tidal currents, sometimes the gradients reverse.Temperature differencesare usually a few tenths of a degree; although, sometimesthey are ashigh as3 “C with warmer water at the surface. Salinity differencesare ashigh aso-2%,,, but usually much lower. Chlorophyll a concentrationsdo not show a significant vertical gradient at the mouth (Alvarez-Borrego et aE., xg77a). Alvarez-Borrego et al. (rg77a, b) generated 26-hour time series of salinity, temperature, oxygen, phosphate, nitrate, chlorophylls and meteorologicalvariables once every seasonat the mouth of the bay. Wowever, theseinvestigators realized that sampling for such short periods was like looking at reality through slits, and general conditions could not easily be separatedfrom irregular or episodicevents. Lara-Lara et al. (1980) generatedan IS-day time series,alsoat hourly intervals, of several ecological variables for the mouth of Bahia San Quintin, during the summer of 1977. Variableswere: sealevel, current velocity, temperature, salinity, oxygen, inorganic phosphate, chlorophyll a, seston, phytoplankton speciesabundance, particulate organic carbon and nitrogen and primary productivity. They concludedthat alternation of upwelling events was the main causeof variability for all properties except temperature. Semidiurnal tides were the main cause of variability for temperature. Diatoms were always the most abundant phytoplankton group. Primary productivity was always greatestat the surface, with a mean value of 27 mg C mW3h-l through the sampling period. Maximum surface productivity valueswere obtained for the upwelling relaxation period (up to ++rng CmW3h-l). The mean surface assimilationratio was6.6 mg C (mg chl. a)-rh-l, which indicatesnutrient-rich waters.
326
R. Milian-Nu?iez,
S. Alvarez-Borrego
& D. M. Nelson
Methods Field sampling methods Time series sampling was carried out, day and night, simultaneously at four anchor stations (Figure I), from 25 June to 5 July 1979. Samples were collected only at the surface. Tide height was measured at Molino Viejo (Station D, Figure I) by a Fisher and Porter Model 1550 digital tide gauge. In order to generate the sea level time series for the other three stations (A, B and C, Figure I) the phase lag was taken from Monreal(1980). Water temperatures were read off bucket thermometers every z h. Salinity was analysed at a shore-based laboratory (Figure I) with a conductivity salinometer, Beckman Model 118WAzoo. Salinity samples were taken every z h at Station D but only twice a day at the other stations. Nutrients, chlorophylls and phytoplankton samples were always taken from the same Van-Dorn bottle, sampling every z h. Two drops of a saturated solution of HgCl, were added to each nutrient sample immediately after collection. The samples were frozen and transported to the School of Oceanography, Oregon State University, where they were analysed for phosphate, silicate, nitrate and nitrite, using a Technicon II AutoAnalyzer (Atlas et al., 1971). Chlorophyll samples were obtained using o.45-l.rrn pore-sized MilliporeR filters. Filters were frozen to be transported to the laboratory of Centro de Investigation Cientifica y de Education Superior de Ensenada. Chlorophyll analysis was done basically by the SCORUNESCO (1966) method, but with some modifications. Second readings at 665, 645 and 630 nm were done after acidification, following Lorenzen (1967). A r-to-r volume solution of 90% acetone and dimethyl s&oxide was used as a solvent to improve the pigment extraction (Shoaf & Lium, 1976). Spectrophotometric equations developed by Millan-Nuiiez & Alvarez-Borrego (1978) were used to estimate concentration of chlorophylls a, b and c and phaeophytins a, b and c. The equation for chlorophyll a is exactly the same as that from Lorenzen (1967) due to the chlorophyll b : phaeopigment 6 and chlorophyll c : phaeopigment c ratios at 665 nm are equal to one. Phytoplankton abundance by gross taxonomic groups was determined by the ctermiihl (1958) inverted scope technique using a Carl Zeiss invertoscope D microscope. Three times a day during daylight hours, surface (N 0.5 m) carbon-14 incubations of I h duration were done at high, intermediate, and low tide. Seawater samples for carbon-r.+ incubations were not taken from the same Van Dorn sampling for chlorophyll and phytoplankton. Sampling was done specifically for the incubations. Carbon-14 samples were obtained using o.45-prn pore sized Millipore R filters. The vials containing the filtered samples were transported to the O.S.U. School of Oceanography where the radioactivity of the samples was determined in a scintillation spectrometer. Inorganic carbon-14 was purged from the vials with nitrogen gas before the radioactivity measurements. Conversion of radioactivity to carbon productivity was done as indicated by Strickland & Parsons (1972). Statistical analysis We subjected our temperature, salinity, sea level, nutrient and chlorophyll time series to spectral analysis. This statistical operation may be regarded as an analysis of variance in which the total variance of a variable or property fluctuation is partitioned into contributions arising from processes with different characteristic time scales (Platt & Denman, 1975). Thus, spectral analysis of a record of observations results in a sorting of total variance of the record into its component frequencies. The spectral analysis results presented here were
Nutrient
distribution
and phytoplankton
productivity
321
computed with a fast Fourier transform algorithm. The output presents the frequency componentsin cyclesh-l. Results Description
of time series of seawater properties
Tidal height time seriesshoweda characteristic semidiurnal behaviour and the sequenceof spring and neap tides. Maximum tidal height range was about 2 m (Figure 2). Salinity time series at Station D also had a semidiurnal behaviour, with high values corresponding in general with low tides, and vice versa. Salinity throughout the whole bay had a general tendency to increasewith time during the sampling. Salinity increasedfrom the bay mouth to the extremes of the bay with a mean difference of about 2.2x, between Stations A and D (Figure 2). Salinity rangeswere: 33*40-34.57x0for Station A; 33&+-34a42%o for Station B; 33*93-34.76x0 for Station C; and 34.63-3~69%~for Station D. Temperature time seriesshowed a long wave feature at all sampling points (Figure 3). The time seriesat Station A showslong wave (IO days), diurnal and semidiurnalvariability, 3.0 2.5 -!z i .P 2! f i-
2.0 I.5
0.5
38i
35
(b)
-
341
z![!;
0
24
40
72
96
120
144
168
192
216
240
264
Time(h)
Figure z. (a) Tide height and (b) salinity time series (middle) station was sampled every z h. (c) Salinity time series (lower) B (A) and C (0). These stations were sampled at times of high
at Station D; this at Stations A (3), and low tide.
322
R. Millan-NuSez,
S. Alvarez-Borrego
& D. M. Nelson
while time seriesat Stations B, C, D, show only the long wave and diurnal features. High temperature values correspondedin generalwith low tides and vice versa. Diurnal temperature rangeswere smaller in the middle of the samplingperiod, due to neaptides. The ranges of temperature were: 12*8-19.8 “C for Station A; 16.4-22.8 “C for Station B; 17.7-21.8 “C for Station C; and 19*2-25.2“C for Station D. 20 19 16 17 16 I5 14 13 12
s e L g i:
23 22 21 20 I9 I6 17
‘6
Time(h) Figure 3. Temperature time series at the four sampling C, D) indicate the stations. Numbers mark midnight.
stations.
The
letters
(A, B,
Nitrate time seriesfor Station A showed the long wave feature very clearly, with high values at the beginning and at the end (Figure 4), whereasthosefor Stations B, C and D did not show the feature clearly, although values at the beginning of the sampling were in generalhigher than those towards the end. Nitrite tended to showa similar behaviour to that of nitrate (not illustrated). The rangesof nitrate and nitrite (PM), were respectively: 0.1-12.5 and c~oo-oq for Station A; 0.1-41 and o.oo-o.30 for Station B; 0.3-4’5 and 0~07-0~25for Station C; and 0.2-28 and 0~01-0~25 for Station D. Phosphate and silicate time seriesfor Station A alsoshowed the long wave feature with high values at the beginning and end of the samplingperiod, and lower values in the middle (Figures 5,6). Their time seriesfor Stations B, C and D did not show the long wave. Spikes in phosphateconcentration occurred at Station B on the sixth and ninth samplingdays, but no such spikeswere obvious at the other samplingpoints. Possiblythe smallphosphatespike shown at Station A, on the sixth samplingday wascorrelated with the first spike at Station B
Nutrient distribution and phytoplankton productivity
323
4-
C
2O-
Time(h)
Figure
4. Nitrate
time series at the four
sampling
stations.
Numbers
mark
midnight.
(Figure 5). There was no clear tendency for phosphate to increase or decrease from the mouth to the interiors of the bay. Silicate concentration in general increased from the bay mouth to the extremes (Figure 6). The ranges of phosphate and silicate (PM) were, respectively: 0.5-2.48 and 4.9-232 for Station A; 0.72-2.86 and 1.2-19.7 for Station B; 0.62-1.59 and 66-245 for Station C; and 0.36-1.93 and 10.7-32.8 for Station D. The time seriesat Station A for chlorophyll a, 6 and c showed a general tendency to increasewith time during sampling(Figure 7, chlorophylls b and c not illustrated). Generally, the highest values for all three pigments at the bay mouth station were found at the end of the sampling period. Pigment time seriesat Stations B, C and D showed a complicated patchiness. The ranges of chlorophylls a, b and c (mg mW3)were respectively: 0’5-37.9, oo-3.8 and oa-16.1 for Station A; 0.5-18.7, 0.0-1.9 and oo-12.6 for Station B; 0.5-4.8, oo-2.7 and 0.2-8.7 for Station C; and 0.5-4.9, 0.0-2.0 and 0.1-7.0 for Station D. Phaeopigment time seriesshoweda very patchy distribution at all four sampling points. Phaeophytins b and c often were not significantly different from zero (not illustrated). Phaeophytin a concentrations were lower than their respective chlorophyll concentrations (Figure 8). Phytoplankton abundance time seriesat the four locations did not show the long wave feature of temperature and nutrients; instead, these time series showed a very patchy distribution (Figure 9). In general phytoplankton total abundance decreasedfrom the bay mouth to the bay extremes. At the extremes, abundancewas an order of magnitude lessthan at the bay mouth. At Station B there were patchesof high abundanceduring the first half of the sampling period. Cell abundance at Station B was similar to that at Stations C and D during the secondhalf of the samplingperiod. There wasno clear, permanent dominanceof diatoms over dinoflagellates,or vice versa, at any of the samplingstations except Station B,
324
R. Mdlun-NuEezs,
3.0
’
2.5
-
2.0
-
I.5
-
I.0
-
S. Alvarez-Borrego
&? D. M. Nelson
A
0.5
-
2.5
0 0
I
I
I
I
24
48
72
96
I I20
I 144
I 168
I 192
I 216
I 240
264
Time(h)
Figure 5. Phosphate midnight.
time
series
at the
four
sampling
stations.
Numbers
mark
where diatoms outnumbered dinoflagellatesfor most of the sampling period (Figure IO). For any given taxonomic group there was no consistent difference in cell size between Stations A, B, C and D. The rangesof phytoplankton total abundance(cells ml-l) were: 42-1815 for Station A; 43-2580 for Station B; 20-182 for Station C; and 18-246 for Station D. Phytoplankton productivity time seriesshowed a very irregular variation at Stations A and B (Figure II). There was a tendency for productivity to increasewith time during sampling at Station A, but not at Station B. This correspondedwith pigment changeswith time at the two stations. Primary productivity alsoshoweda tendency to decreasefrom the bay mouth to the extremes. Assimilation ratios showedirregular variation with time at all stations; however, mean values at each location were not significantly different from one another. Means and rangesof phytoplankton primary productivity (mg C m-8 h-r) were respectively: 33.4, 5gq.4 for Station A; 16.5, 16-63’0 for Station B; 12’5, 2’2-23.4 for Station C; and 12’3, 1y-z7~4 for Station D. Means and rangesof assimilationratios (mg C (mg chl. ~a)-1h-l) were respectively: 6*4,06-13.7 for Station A; 7.8,0.8-262 for Station B; 5.4, ~6-12.5 for Station C; and 6.0,0.8-15-o for Station D.
Nutrient
distribution
and phytoplankton
productivity
32.5
25 20
0
24
48
72
96
120
144
168
192
216
240
264
Time ( h 1 Figure
6. Silicate
time series at the four
sampling
stations.
Numbers
mark
midnight.
Spectral analysis of time series
The tide variance spectrum showedmost of the variance at the diurnal (frequency -0.041 cycles h-r) and semidiurnal (frequency ~50.083 cycles h-l) periods (Figure 12). The variance spectra of all other seawaterproperties tended to show high variance components at these two frequencies although distinct peakswere not always obvious (Figures 12-14). Salinity, temperature, nitrate (Figures 12-14), and phosphate, silicate and sometimes chlorophyll a (not illustrated) clearly showed a high variance component at the lowest frequency (N 0.0025 cycles h-l). Discussion Alvarez-Borrego & Alvarez-Borrego (in press) generated r-year hourly temperature time seriesfor the samefour locationsasthis work from May 1979 to May 1980. Their time series for the Bahia San Quintin mouth showsthe alternation of upwelling events in the adjacent oceanic area from May to September. Lara-Lara et al. (1980) clearly showedthat summer seawatertemperatures near 12 “C at the Bahia San Quintin mouth are the product of upwelling, becausedissolvedoxygen percentagesaturation was found to be as low as 60% and this is characteristic of the upwelling water. Mixing by tidal currents during spring tides is
326
R. Millan-Nufiez,
S. Alvcwex-l3onego
f9 D. M. Nelson
50
0
24
48
72
96
120
144
168
192
216
240
264
Time(h)
Figure 7. Chlorophyll midnight.
c1time series at the four sampling stations. Numbers mark
not causing these low temperature values. During winter, tidal height ranges are greater and minimum temperatures at the bay mouth are only about 13.5 “C (Alvarez-Borrego & Alvarez-Borrego, in press). Alvarez-Borrego & Alvarez-Borrego’s temperature time series indicates that samplingfor the work reported here started at the beginning of an upwelling relaxation period, and ended when the strongest upwelling event of the year was about to begin. Also, samplingfor our study started at spring tides, continued through neaptides, and ended at the beginning of the following spring tides (Figure 2). Miniium temperatures during the upwelling event previous to our samplingwere about 12 “C, while they were about II “C for the one after our sampling (Alvarez-Borrego & Alvarez-Borrego, in press). Upwelling previous to our sampling was weaker than the first upwelling detected by Lam-Lara et al. (1980). Their minimum temperatures were below 12 “C, compared with a minimum temperature of 12-8 “C in our sampling; and their mazimum salinity was3~*78%~ comparedwith a maximum salinity of 34’57ymin our sampling at the bay mouth. They measuredphosphate values higher than 3 pi, compared with a maximum of ~5 pi in our case.Within the lagoon, the effects of the alternation of upwelling events and those of spring and neap tides on the variation of seawaterproperties are not easy to separate,becausetheir periods aresimilar.
Nutrient
distribution
and phytop2ankton
productivity
2 0
0
24
48
72
96
120 Time
Figure 8. Phaeophytin midnight.
a time
series
144
168
192
216
240
264
Numbers
mark
(h 1
at the four
sampling
stations.
Lara-Lara et al. (1980) concluded that variability at the mouth of Bahia San Quintin during summer was to a great extent caused by upwelling events, the tidal cycles and the solar radiation cycle. However, seston variability was mainly due to turbulence induced by winds and tidal currents; and inorganic phosphate was also greatly affected by this factor. Analyses of our time series from Stations B, C and D (Figures 12-14) show that variability of seawater properties is mostly controlled by the same main factors throughout the bay. The low frequency variance components are associated with the alternation of upwelling events and the alternation of spring and neap tides. Variance components at high frequencies (70.1 cycles h-l) are probably related to turbulence and irregular mixing conditions created by the lagoon bathymetry and associated heating by solar radiation input. The bay region between Stations A and B is very much affected by conditions in the oceanic region adjacent to the bay mouth. The greater residence times in the extremes cause different conditions to develop at Stations C and D. Salinity and temperature are higher at Stations C and D due to solar heating and evaporation. At Station D, higher temperatures and salinities indicate greater residence times than at Station C. The temperature long wave feature of Stations C and D (Figure 3) may be due to alternation of spring and neap tides, to the alternation of upwelling events that make their impact in the whole bay, or both. If this long wave feature was only due to the alternation of spring and neap tides, it would mean that spring tides were bringing colder water from the mouth region to Stations C and D while during neap tides the water was moving in and out near Stations C and D without much exchange with the oceanic region, the net effect being to warm the water relative to the spring tides. The salinity time series at Station D shows that this is not what happened (Figure 2). If it were, salinity values at the spring tide would be lower than those for neap tides. But they are not lower, they are indeed higher. Thus, the temperature long wave feature for Stations
328
R. M&n-Nuiiea,
S. Alvarez-Borrego
& D. M. Nelson
-I 2.5
2.5 0 24
46
72
96
120
144
Time
Figure g. Phytoplankton Numbers mark midnight.
abundance
time
166
192
216
240
264
(h)
series
at the
four
sampling
stations.
C and D (Figure 3) is partly due to the alternation of upwelling events. Upwelling is propagated throughout the bay. Our time seriesaretoo short to estimatethe lag of this propagation between the mouth and Stations C and D. Alvarez-Borrego & Alvarez-Borrego (in press) found that the upwelling lag, measuredby temperature change,is practically that of the tide. During spring tides, up to 80% of the bay water may go out. When an upwelling event occurs, water from the bay mixesto a certain extent with the newly upwelled water. Then, the flood flow brings water with changedproperties into the bay. Ultimately a dynamic equilibrium is reached unless properties outside the bay change again before equilibrium is established. Upwelled water has lower temperature, chlorophyll concentration, oxygen, phytoplankton abundance,primary productivity and higher inorganic nutrient concentrations and salinity (Lara-Lara et al., 1980). During the relaxation of upwelling, greater water residence time in the bay allows for an increasein chlorophyll concentration and assimilation
Nutrient
distribution
and pkytoplankton
productierity
329
80 60
0 24
40
72
96
120
144
Time
(h I
168
192
216
240
264
Figure IO. Percentage of the total phytoplankton abundance. The dashed corresponds to the fraction of dinoflagellates, below it the fraction of diatoms above the fraction of microflagellates. Numbers mark midnight.
area and
ratios and increasedconsumption of inorganic nutrients. High nitrate, nitrite, phosphateand silicate values at Station A at the beginning of the sampling (Figures 4-6) were due to an ending upwelling event. Lara-Lara et al. (1980) reported ratesof phytoplankton primary productivity in Bahia San Quintin mouth about two to three times greater than averagerates in the Gulf of California (Zeitzchel, of Oceanography, 1969),in the upwelling areasoff the west coastof Baja California (Scripps Institute data report, 1969) and off Oregon (Curl & Small, 1965). Productivity in Bahia San Quintin mouth during summer is similar to the highest productivity found by Small & Menzies (1981) in narrow bands of the nearshoreOregon upwelling system. High rateshave beenreported by Beerset al. (1971) and Barber et al. (I 971) for the Peru upwelling zone and by Huntsman & Barber (1977) and Smith et al. (1977) for the north-west Africa
330
R. MiUan-Nufiez,
S. Alvarex-Borrego
& D. M. Nelson
c
so
1
I
80 70
60 50 40 15 30 IO 20 i
Jz
5 IO
IO 20 5 IO 30
0 15
20
IO
IO
5
0
0 Time(h)
Figure I I. Phytoplankton productivity (mg C m- * h -‘) (U) ratio (mg C (mg chl. a)-3 (0 - - 0). Numbers mark midnight, numbers mark the dark period.
and assimilation the line above the
upwelling zone. Our results for phytoplankton primary productivity and assimilationratio for the bay mouth are very similar to those found by Lara-Lara et al. (1980). Surface primary productivity decreasesfrom the bay mouth to the two extremes, along with chlorophyll concentration (Figures 7, II). Mean assimilationratios are not significantly diierent at the four sampling points. At the extremes, while both primary productivity and chlorophyll Q values are about one-third of those at the bay mouth, total phytoplankton cell abundanceis only about onetenth (Figures 7, g, II). This indicates that chlorophyll content per cell at the extremes is about three times that at the mouth. There is not much difference in cell size between phytoplankton at the bay mouth and thoseat the extremesof the bay for any given taxonomic group. Beardall & Morris (1976) showed that the diatom Pheodactylum tricornutum can adapt to low light intensity, and this adaptation consistsof an increasedchlorophyll content
Nutrient
distribution
and phytoplankton
productivity
331
per cell and a decreasedrate of light-saturated photosynthesisper unit chlorophyll. If this observation is applicable to the natural phytoplankton assemblages in Bahia San Quintin, the higher chlorophyll per cell may be dueto the turbidity being greater,and light penetration less, at the extremes than at the bay mouth. Water at the extremes is more turbid (Secchi disc reaching about a half (1.5 m) of that of the bay mouth), resulting in lesslight penetration, and perhaps causing the phytoplankton cells to increasetheir chlorophyll content. At the extremeswe found IO times lower phytoplankton abundance,three timeslower productivity, three times lower total chlorophyll, three times higher chlorophyll per cell, higher turbidity (shallower Secchi disc depth) and shallowerbottom depth (2 vs 9 m) than at the bay mouth. Therefore, light limitation, probably resulting from absorption of light by resuspended bottom sediments,is probably the most important factor causingphytoplankton abundance and productivity to be much lower at the extremes.
(0) I I I02
iO-3
A I I 1O-2
10-l
IO’
10-2
10-3
II Frequency
(cycles
Figure 12. Spectral density of (a) tidal height mark the diurnal and semidiumal frequencies.
10-l
IO0
h-l)
and (b) salinity
at Station
D. Arrows
Seawater samplesfor carbon-14 incubations and phytoplankton abundanceanalyseswere not taken from the samesampling, so resultsof thesetwo setsof measurementsmight not be directly comparable. At Station B, phytoplankton abundancewaslow the last 5 days of the samplingperiod, while primary productivity washigh the seventh and eighth samplingdays (Figures 9, I I). A possibleexplanation for theselatter higher values is that they corresponded to patchesof high chlorophyll concentrations. Farfan (1981) sampledfor ammoniaconcentrations at the bay mouth at the sametime we did our sampling. She estimatedammoniaconcentrations ashigh as 3 pM. The mean of her results was around 0.7 FM, with somevalues near o PM. If we assumeRedfield’s model to apply roughly (Redfield et al., r963), reduced forms of nitrogen should have concentrations of at least a few PM. Comparison of measurednutrient concentrations (Figures 4-6) with numerous reported studies of the kinetics of nutrients limited growth of planktonic algae (Eppley et al., 1969; Paasche,1973; Fineko & Krupatkina-Akinina, 1974; Conway, 1977) indicates that nutrient concentrations were almost never low enough to limit phytoplankton growth during the sampling period at any of the four locations of the bay. At the mouth,
332
R. MiLTan-NuEez,
S. Alvare.z-Borrego
A
& D. M. Nelson
I04
IO3
IO2
IO’
IOa
, _
I lo! Y IO-
.I
104,
0
I
I02
IO’
,o-3
,o-2
10-l
100 Frequency
Figure 13. Spectral density the diurnal and semidiumal
of temperature frequencies.
I00 iI
10-3
(cycles
10-2
10-i
IO0
sampling
stations.
Arrows
h-‘1
at four
mark
during the relaxation of upwelling (Figures 4-Q the effect of nutrient uptake by the phytoplankton is clear. All inorganic nutrients were in high concentration at the beginning of the upwelling relaxation period and decreaseduntil the eighth or ninth samplingday. At the end of the samplingperiod all nutrient concentrationswere starting to increaseagain, asa result of the following upwelling event. At the bay mouth, during the first and Iast parts of sampling, with upwelling ending and starting respectively, greater nutrient concentrations correaponded to high tides (Figures z,4-6). The phosphatetime seriesfor Stations C and D showthat remineralization by bacterial oxidation of organic matter, mostly in the sediments,increase nutrient concentrations in the interiors of the bay (Figure 5). Mixing by tidal currents and winds stirs up the sediments bringing the nutrients into the water column. Uptake of phosphateand nitrogen compoundsby seagrasses may also be of importance in the spatial distribution of nutrients, but its effects cannot be estimatedfrom present data. Horizontal gradientsof nutrients within the bay are highly variable. Sometimesnutrient concentrations arehigher at the mouth than at the extremes. Such is the casefor nitrate, nitrite and phosphate
-
Nutrient
distribution
and planklankton
production
333
---
f104
II
to3
~ IY 1
to2
s c g z 5L
to’
“, ::
IO3
I
I
I=
L-
I
K
C
iI
I to*
to’ 4
too
II
L
to-3
L
to-*
10-l
I00 Frequency
Figure diurnal
ii:i
~
1
14. Spectral density of nitrate and semidiurnal frequencies.
10-3 (cycles
at four
10-2
to-’
IQ0
h-’ 1
sampling
stations.
Arrows
mark
the
during an upwelling event (Figures 4,s). And sometimesthe situation reverses,suchasduring the relaxation period. In general,the spatial distribution of nutrients is very patchy, asis the case for chlorophylls and phytoplankton abundance. In general, silicate concentration increasesfrom the mouth to the extremeseven during an upwelling event (Figure 6). At the extremesdissolutionsof exoskeletons,mainly of diatoms,may be the main sourceof dissolved silicate. The phosphatespike detected at Station B on the sixth sampling day and the more moderatespike detected on the ninth sampling day did not have a clear correspondences with the other nutrient values in the samestation, or with similar phosphatespikeson the other three samplingstations (Figures 4-6). At Station A there are small phosphatespikeslagging those at Station B by about I day (Figure 5). Lara-Lara et aE. (1980) detected a phosphate spike at the Bahia San Quintin mouth, which was correlated, to a certain extent, with an inorganic seston spike. They explained these spikes in terms of stirring of sedimentsby wind-induced turbulence. Station B, being at the baseof the ‘Y’ may have greater turbulence causedby tidal currents during ebb flow. If this is coupled with relatively strong winds, it may causea greater stirring effect in the sediments.If wind-induced turbulence alone were
R. Millan-NuZez, S. Alvarez-Borrego W D. M. Nelson
334
the causeof these spikes,they would have been detected at all four samplingpoints (or at least in a similar fashion at Stations B and C). The fact that the other nutrients did not show similar spikes indicates different remineralization processesfor them. Nitrogen from the sedimentsmay exist mostly in reduced forms. It is difficult to explain why there are no silicate spikes in correspondencewith phosphate spikes. Silicate had high values, but no pronouncedspikesat any time. Lara-Lara et al. (1980) found that diatomswere the mostabundant group at the bay mouth, followed by dinoflagellatesand microflagellates.They also found dinoflagellatesand microflagellateswere in greater abundance than diatoms toward the bay extremes. Our results show that diatomswere not always more abundant than dinoflagellatesat the mouth (Figure IO). Also, diatoms were often more abundant than dinoflagellatesat Stations B, C and D. Thus, there is no clear, permanent pattern for these phytoplankton groups throughout Bahia San Quintin. As the percentage of the total number of phytoplankton cells, microflagellatesshow a generalincreasefrom the bay mouth to the extremes(Figure IO). However, there is no increasein the absolute number of microflagellatesfrom the bay mouth to the extremesrather, their relative numerical contribution to the phytoplankton increasesbecause they maintain roughly constant number while both the diatomsand dinoflagellatesdecrease greatly in abundance.
Acknowledgements This work was supported by a graduate fellowship from the ConsejoNational de Ciencia y Tecnologia of Mexico to Roberto Millan-Nuiiez. It representsa segment of a long-term project by the Centro de Investigation Cientifica y de Education Superior de Ensenada. We thank Lawrence F. Small and Luis A. Codispoti for their criticisms and suggestions.
References Alvarez-Borrego, J. & Alvarez-Borrego, S. in press Temporal and spatial variability of temperature in two coastal lagoons. CalCoFi Reports. Alvarez-Borrego, S. & Chee-Barragan, A. 1976 Distribution superficial de fosfatos y silicates en BahiaSanQuintin,B.C.CiencinslMatis3(1), p-61. Alvarez-Borrego, S. & Lopez-Alvarez, C. 1975 Distribution de biomasa de fitoplancton por grupos taxonomicos en Bahia San Quintin, B. C. a traves de un ciclo anual. Reporte para I.N.P. de la S.I.C. y la Direccibn de Acuacultura de la S.R.H. (unpublished). Alvarez-Borrego, S., Ballesteros-Grijalva, G. & Chee-Barragan, A. 1975 Estudio de algunas variables fisicoquimicas supeficiales en Bahia San Quintin, en verano, otofio e inviemo. Ciencios Marinas
2 (21,I-9.
Alvarez-Borrego, S., Acosta-Ruiz, M. de J. & Lara-Lara, J. R. rg77a Hidroloda comparativa de las bocaz de dos antieatuarios de Baja California. Ciencias Marinas 4 (I), I-I I. Alvarez-Borrego, S., Lara-Lara, J. R. & Acosta-Ruiz, M. de J. 19773 Parametros relacionados con la productividad organica primaria en dos antiestuarios de Baja California. Cienckzs Marinas 4 (I), 1211.
Atlas,
I. E., Gordon, L. I., Hager, S. W. &Park, P. K. 1971 A practical manual for use of the Technicon’2 Auto Analyzer@ in seawater nutrient analyses. Revised Technical Report 215. Department of Oceanography, School of Science, Oregon State University, Corvallis. B&m, A. 1973 Coastal upwelling indices, west coast of North America, 1964-71. NOAA Technical Report NMFS SSRF-671.103 pp. Barber, T. R., Dugdale, R. C. MacIsaac, J. J. & Smith, R. L. 1971 Variations in phytoplankton growth associated with the source and conditioning of upwelling water. Investigation Pesque~a 35,171-x93. Barnard, J. L. 1962 Benthic marine exploration of Bahia de San Quintin, Baja California, Ig6o-1961. Poci& Naturalist a, 25 1-269. Beardall, J. & Morris, J. 1976 The concept of light intensity adaptation in marine phytoplankton: some experiments with Phaeodactylum triwrnutum. Marine Biology 37,377-387.
Nutrient
Beers,
distribution
andphytoplankton
productivity
335
J. R., Stevenson, M. R., Eppley, R. W. & Brooks, E. R. 1971 Plankton populations and upweiling off the coast of Peru, June 1969. Fishery Bulletin 69,85g-876. Chavez-de-Nishikawa, A. G. & Alvarez-Borrego, S. 1974 Hidrologia de Bahia San Quintin en inviemo y primavera. Ciencias Marinas I (z), 31-62. Conway, H. L. 1977 Interactions of inorganic nitrogen in the uptake and assimilation by marine phytoplankton. Marine Biology 39,221-232. Curl, H., Jr. & Small, L. F. 1965 Variations in photosynthetic assimilation ratios in natural marine phytoplankton communities. Limnology and Oceanography IO, Supplement R67-R73. Dawson, E. Y. 1951 A further study of upwelling and vegetation along Pacific Baja California, Mexico. Journal of Marine Research IO, 39-58. Dawson, E. Y. 1962 Marine and marsh vegetation. Benthic marine exploration of Bahia de San Quintin, Baja California. 1960-61. PaciJic Naturalist 3,275-280. Eppley, R. W., Roger, J. N. & McCarthy, J. J. 1969 Half saturation constant for uptake of nitrate and ammonium by marine phytoplankton. Limnology and Oceanography IO, grz-gzo. Farfan, B. C. rg8r Variability and tidal exchange of dissolved inorganic nitrogenous nutrients and suspended organic matter in San Quintin Bay, Baja California. M.S. Thesis, San Diego State University, San Diego, California. 58 pp. Fineko, 2. 2. & Krupatkina-Akinina, D. I<. rg74 Effect of inorganic phosphorus on the growth rate of diatoms. Marine Biology 26, 193-201. Huntsman, S. A. & Barber, R. T. 1977 Primary productivity off Northwest Africa: the relationship to wind and nutrient conditions. Deep-Sea Research 24,25-33. Lara-Lara, J. R. & Alvarez-Borrego, S. 1975 Ciclo anual de clorofilas y production organica primaria en Bahia de San Quintin, B. C. Ciencias Marinas 2 (I), 77-97. Lara-Lara, J. S., Alvarez-Borrego, S. & Small, L. F. 1980 Variability and tidal exchange of ecological properties in a coastal lagoon. Estuarine and Coastal Marine Science II, 613-637. Lorenzen, C. J. 1967 Determination of chlorophyll and phaeopigments: spectrophotometric equations. Limnology and Oceanoffraphy 12,343-346. Millan-Nufiez, R. & Alvarez-Borrego, S. 1978 Ecuaciones espectrofotometricas tricromaticas para la determination de clorofilas a, b, c y sus feofitinas. Ciencius Murims 5 (I), 47-55. Monreal-Gomez, M. A. 1980 Aplicaciones de un modelo de dispersion en Bahia San Quintin, Baja California, Mexico. M.S. Thesis, Centro de Investigation Cientifica y de Education Superior de Ensenada, Baja California. 88 pp. Paasche, E. 1973 Silicon and the ecology of marine plankton diatoms. II Silicate uptake kinetics in five diatoms species. Marine Biology 19,26z--269. Platt, T. & Denman, K. L. 1975 Spectral analysis in ecology. Annual Review of Ecology and Systematics 6,18g-zro. Redfield, A. C., Ketchum, B. H. & Richards, F. A. 1963 The influence of organisms on the composition of seawater. In The Sea volume 2 (Hill, M. N. ed.). Wiley-Interscience, New York. pp. 26-77. SCOR-UNESCO. 1966 Determination of photosynthetic pigments. Monographs in Oceanographic Methodology. pp. 1-18. Scripps Institution of Oceanography 1969 Cruise TO-64-1 and cruise TO-64-2 data report. University of California at San Diego, Scripps Institution of Oceanography Reference 69-4.57 pp. Shoaf, W. T. & Lium, B. W. 1976 Improved extraction of chlorophyll a and b from algae using dimethyl sulfoxide. Limnology and Oceanography 21,gz6-928. Small, L. F. & Menzies, D. 1981 Patterns of primary productivity and biomass in a coastal upwelling region. Deep-Sea Research A 28, rz3-149. Smith, W. O., Jr., Barber, R. T. & Huntsman, S. rg77 Primary production off the coast of Northwest Africa: Excretion of dissolved organic matter and its heterotrophic uptake. Deep-Sea Research 24, 35-47. Strickland, J. D. & Parsons, T. R. 1972 A practical hand-book of seawater analysis (2nd ed.). Bulletin of the Fisheries Research Board of Canada. 167 pp. Utermiihl, H. 1958 Zur Vervollkommnung der quentitativen Phytoplankton-Methodik. Mitteilungen der Internationalen Vereinigung fiir Theoretische und Angewandte Limnologie 9, x-38. Zeitzchel, B. 1969 Primary productivity in the Gulf of California. Marine Biology 3, zor-207.