Consequences of winter upwelling events on biogeochemical and phytoplankton patterns in a western Galician ria (NW Iberian peninsula)

Estuarine, Coastal and Shelf Science 73 (2007) 409e422 www.elsevier.com/locate/ecss

Consequences of winter upwelling events on biogeochemical and phytoplankton patterns in a western Galician ria (NW Iberian peninsula) Ricardo Prego a,*, Dafne Guzma´n-Zu~ niga a,b, Manuel Varela c, Maite deCastro d, Moncho Go´mez-Gesteira d a

Instituto de Investigaciones Marinas (CSIC), 6, Eduardo Cabello, 36208 Vigo, Spain Centro de Ciencias y Ecologı´a Aplicada (Universidad del Mar), 258-1548 Vi~na del Mar, Chile c Centro Oceanogra´fico de La Coru~na (IEO), 15001 La Coru~na, Spain d Grupo de Fisica de la Atmo´sfera y del Oce´ano (Universidad de Vigo), 32004 Ourense, Spain

b

Received 16 August 2006; accepted 1 February 2007 Available online 26 March 2007

Abstract The consequences of two upwelling events in mid- (MW) and late (LW) winter on biogeochemical and phytoplankton patterns were studied in the Pontevedra Ria and compared with the patterns measured under typical winter conditions and under a summer upwelling event. Thermohaline patterns measured during the mid-winter upwelling event (MW-up) revealed the intrusion of saltier seawater (35.9) into the ria associated with the Iberian Poleward Current (IPC). During the late-winter upwelling event (LW-up), the seawater which had welled up into the ria showed characteristics of the Eastern North Atlantic Central Water mass (ENACW). In both cases the measured water residence time (4 days during MW-up and 10 days during LW-up) was related to both meteorological and fluvial forcing. This residence time contrasts with that of summer upwelling (7 days) and with that estimated under unfavorable upwelling atmospheric conditions (2e4 weeks). During MW-up, the ria became poor in nutrients due to continental freshwater dilution, associated with the shorter residence time of the water, and the intrusion of IPC, which is a water body poor in nutrient salts: 2.9 mM of nitrate, 0.1 mM of phosphate and 1.5 mM of silicate. During this event, the ria exported 3.4 molDIN s1, compared with 6.9 molDIN s1 in non-upwelling conditions. Phytoplankton showed a uniform distribution throughout the ria, as during unfavorable upwelling conditions, and was characterized by the dominance of diatoms, mainly Nitzschia longissima and Skeletonema costatum. During LW-up, a nutrient depletion in the photic layer also occurred, but as a result of a phytoplankton spring bloom developing at this time. The ria was a nutrient trap where 4.1 molDIN s1 were processed by photosynthesis. This budget is three times higher than the one under non-upwelling conditions. In contrast with the MW-up, which had no effect on primary production, during LW-up the ria became more productive, although not as productive as during a summer upwelling event (9.9 molDIN s1). The taxonomic composition of the phytoplankton community did not change noticeably during LW-up and the summer upwelling, with the same species present and changing only in relative proportions. Diatoms were always the dominant microphytoplankton community, with Pseudonitzschia pungens, Thalassionema nitzschioides and several species of Chaetoceros as characteristic taxons. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: upwelling; winter; biogeochemistry; phytoplankton; landesea exchange; LOICZ; ria; NW Spain

1. Introduction Coastal upwelling systems have been largely studied along the worldwide eastern boundary system because of * Corresponding author. E-mail address: [email protected] (R. Prego). 0272-7714/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2007.02.004

its biological importance. These events re-fertilize superficial levels of water, increasing the biological productivity of the coastal zones (Hickey and Banas, 2003) in the main world upwelling systems: Benguela (Monteiro and Largier, 1999), California (Di Lorenzo, 2003), Canary (Pelegrı´ et al., 2005), and Humboldt Currents (Nixon and Thomas, 2001).

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The North Atlantic Upwelling System extends from 10 to about 44 N (Wooster et al., 1976). During the summer, the western coast of the Iberian Peninsula is characterized by the presence of southerly winds blowing at the shelf and by a southward surface current. Upwelling events occur from May to September (McClain et al., 1986) favouring nutrient input towards the surface waters and producing major primary productivity (Prego et al., 1999). During winter, the weakening and southward migration of the Azores High leaves the western Iberian Peninsula under the influence of northerly winds. The upper layer circulation pattern is characterized by a poleward slope current that flows from November to March (Sordo et al., 2001; Gil, 2003) over 1500 km along the upper continental slope-shelf break zone off the Atlantic Iberian and French coasts (Frouin et al., 1990; Haynes and Barton, 1990). This has been called the Iberian Poleward Current (IPC), and according to these authors this water, warmer and saltier than that of spring and summer, is 25e40 km wide, about 200 m in depth and has velocities of 0.2e0.3 m s1 moving in the continental margin area. The northernmost limit of the North Atlantic Upwelling System is the NW Iberian upwelling zone (Fraga, 1981). The NW Iberian shoreline presents incised valleys called rias, where the estuarine zone can move according to climatic changes (Evans and Prego, 2003). The four Western Galician Rias receive nutrient salts as a result of springesummer upwelling events favored by north winds flowing along the coast (Blanton et al., 1984; Go´mez-Gesteira et al., 2001). These upwelling events inject cold nutrient-rich Eastern North Atlantic Central Water mass (ENACW, Fraga, 1981; Fiuza et al., 1998) into the rias. During autumn and winter, continental run-off is the dominant nutrient supply (Dale et al., 2004). Springesummer upwelling events, a typical feature on the Galician coast, have been described in detail in the Western  Galician Rias (Alvarez-Salgado et al., 1993; Prego et al., 1999; Varela et al., 2005). However, winter upwelling events have been reported during the last decade along the west Iberian Peninsula (Santos et al., 2001; Vitorino et al., 2002;  Alvarez et al., 2003; deCastro et al., 2006). The evolution of the upwelling regime off the Iberian margin during the 20th century is an interesting topic not exempt from controversy. Considering the upwelling season, Bakun (1990) found that winds favoring upwelling had become stronger. In contrast, other authors (Lemos and Pires, 2004; Lemos and Sanso´, 2006) found evidence of a decreasing trend in the upwelling signal along the west Iberian Peninsula during the same period. In spite of the fact that several winter upwelling events have been reported during the last decade along the west Ibe rian Peninsula (Santos et al., 2001; Alvarez et al., 2003; deCastro et al., 2006), no clear trend in the evolution of upwelling has been reported so far. Santos et al. (2005) provide some information about the variability of the Canary Islands upwelling system during the last two decades of the 20th century. They observe that the Iberian coast in winter was also experiencing weak but persistent upwelling during the 1992e 2001 strong phase of upwelling. With regard to the Galician coast, the upwelling index (UI) is available from 1966 at the

reference point 43 N 11 W. The mean upwelling index for November has increased significantly from 1980 to 2001 (deCastro et al., 2006), although it is still negative (unfavorable for upwelling) on average. In particular, deCastro et al. (in press) have analyzed several events from 2000 to 2005. All of them are characterized by the pumping of ENACW  into the ria. However, the event described in Alvarez et al. (2003), and now analyzed in detail here, is the only example of IPC upwelling observed along the west Iberian Peninsula. The biogeochemical and phytoplankton patterns related to these out-of-season upwelling events have not yet been described. Therefore, the aim of this study was to investigate winter upwelling consequences with respect to the riaeocean water and nutrient exchange and the biological effects on phytoplankton growth and species composition in the Pontevedra Ria. Two different winter upwelling events were considered in order to compare their biogeochemical and phytoplankton patterns with winter conditions of rain and prevalent southerly winds, and with those of a typical summer upwelling. 2. Materials and methods 2.1. Survey zone The Pontevedra Ria, the second western ria from south to north (Fig. 1), can be considered as the paradigm of the west ern Galician Rias from a hydrodynamic point of view (Alvarez et al., 2005). It is a partially mixed estuary with a positive residual circulation. Stratification is supported by lower salinity during the rainy season and by the solar warming of superficial waters during the dry season (Prego et al., 2001). As with the rest of the Western Galician Rias, the high primary productivity of the Pontevedra Ria is due to springesummer coastal upwelling events (Varela et al., 2005), and diatoms are the most important group in the phytoplankton biomass (Bode et al., 1994; Bao et al., 1997). The input of new inorganic nutrients into the ria can be increased by remineralization of the organic matter synthesized inside the ria (Dale and Prego, 2002). Thus, the annual average of primary production in a Western Ria is in the order of 260 g C m2 y1 (Prego, 1993), decreasing one order of magnitude in winter. 2.2. Sampling and analysis Field measurements were obtained in the Pontevedra Ria (Fig. 1) during the biweekly sampling program ‘PONT98’ held in 1998 on board the R/V Mytilus. Upwelling indexes were calculated at a point located at 43 N and 11 W, using geostrofic wind measurements and following the methodology of Bakun (1973) and Lavin et al. (1990). The selected cruises for this study were: January 13 and 27 (Mid-Winter: MW), March 10 and 24 (Late-Winter: LW) and June 9eJuly 7 (Summer: S). Cruises carried out at the end of January, March and in the early days of July (MW-up, LW-up and S-up, respectively) were selected due to the existence of wind conditions favorable to upwelling lasting at least 1 week before the sampling date (Fig. 2). McClain et al. (1986) considered

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422 8º 54' W

411

8º 42' W Lérez River

10 30

20

Cabicastro Point

42º 24' N

Tambo Isle 8 7 6 20 10

40

Marín Town

5

30

Onza and Ons Islands 4

3 50

Muros

100

2 Udra Cape

60

Arosa

1 Pontevedra 1000

3 km 70

200

42º 19' N

Vigo

WESTERN GALICIAN RIAS

Fig. 1. Map and bathymetry of the Pontevedra Ria. Circles represent the sampling stations. This ria is the second biggest of the Western Galician Rias, having a surface area of 141 km2, a mean depth of 31 m and a volume water content of 3.47 km3.

that the coastal circulation inertia to wind stress is at least 3 days. The other cruises carried out in January, March and June (MW-nu, LW-nu and S-nu, respectively) were considered as winter situations (characterized by negative upwelling indices) and a non-upwelling summer situation (Fig. 2). Vertical profiles of temperature and salinity were registered in eight selected stations by means of CTD models Seabird 19 and 25 (salinity error 0.001). Water samples were taken in the main channel of the ria (Fig. 1) using General Oceanic Niskin 5-L bottles at standard levels (0, 5, 10, 20, 30, 40, and 60 m depth). Dissolved oxygen was measured following the Winkler method (Aminot, 1983), and percentage oxygen saturation calculated using the equations from that reference. Aliquots of 50 ml of water were separated into HDPE bottles to analyze the inorganic nutrients nitrate, nitrite, ammonium,

January

February

March

phosphate and silicate following the autoanalyzer methods of Hansen and Grasshoff (1983) in Technicon AAII equipment consisting of five lines, one for each nutrient. The precision of the analysis based on 10 aliquot replicates of nutrients of equal concentration was: NO 3 0.01 mM (within the 0 to 10 mM range); NO 0.01 mM (0 to 2 mM); NHþ 2 4 0.02 mM (0 to 2 2 mM); HPO4 0.02 mM (0 to 2 mM); and H4SiO4 0.02 mM (0 to 25 mM). The discharge of the main continental contribution to the Pontevedra Ria, the Le´rez River, was measured daily in a gauging station located on the boundary of the tidal influence (Prego et al., 2001). Freshwater flow data were averaged for every cruise based on the residence time of the ria water. Samples for the determination of chlorophyll a were filtered through glass fiber filters (Whatman GF/F), and

April

May

June

July

Upwelling Index (m3s-1km-1)

4000 2000 0 -2000 -4000 -6000 MW-nu MW-up

LW-nu LW-up

S-nu

S-up

Fig. 2. Daily values of the Upwelling Index measured at 43 N, 11 W from January to July 1998. Sampling dates are indicated by arrows, where ‘MW’ is MidWinter, ‘LW’ Late-Winter, ‘S’ Summer, ‘up’ upwelling and ‘nu’ non-upwelling conditions.

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chlorophyll was extracted with 90% acetone (UNESCO, 1994) and its concentration determined by spectrofluorimetry following the methods described by Neveux and Panouse (1987). Primary production was estimated by the 14C method, using 2 h incubations in simulated in situ conditions such as those described by Bode et al. (1994). Phytoplankton samples were taken at the above-mentioned depths, preserved with Lugol’s solution and kept in the dark until they were studied. Samples were counted as cells ml1 using a Nikon Diaphot TMD inverted microscope following the technique described by Utermo¨hl (1958). A magnification of 100 was used for large forms, 250 for intermediate forms and 400 for microflagellates. When organisms were too small (from 3 mm to 10 mm) to be classified at the species or even genus level, they were recorded as dinoflagellates or microflagellates. Species nomenclature was validated according to Tomas (1997). Analysis of variance (ANOVA) was carried out on chlorophyll and diatom abundances to determine whether significant differences existed among periods during upwelling and nonupwelling conditions. According to the ANOVA results, discriminant analysis was performed using the groups MW, LW and S. Sixty-five samples and around 30 species with a relative frequency higher than 20%, to avoid the effect of rare species (Varela et al., 2005), were used for the discriminant analysis. Prism from GraphPad Software Inc. and the SPSS statistical packages were used for ANOVA and discriminant analysis, respectively.

surface were negligible during the sampling days. Therefore, the water budget is:

2.3. Exchange model of water and nutrient salts

Sm ¼

dV ¼ Qr þ Qs þ Qin  Qout ¼ 0 dT

where the ria inputs are positive and the ria outputs negative. The Le´rez River provides the main freshwater input into the ria (mean annual discharge of 25.9 m3 s1; Ibarra and Prego, 1997). During 1998 the river flow was recorded daily and averaged for every cruise (under winter, spring and summer conditions) according to the iterative procedure followed by Dale et al. (2004). The salt budget, which must be constant, was also considered in the reservoir modeling to quantify the water flow exchange. The sources of freshwater have practically null salinity in the Pontevedra Ria. In this way, the riaeocean flows can be evaluated: dM ¼ ðQin $Sin  Qout $Sout Þ ¼ 0 dT

ð2Þ

where Sin and Sout are the averaged salinities of incoming and outgoing flows. The salinity in the incoming and outgoing flows was calculated assuming that the separation level between the two opposite residual currents coincides with the depth of the mean salinity, Sm (Prego and Fraga, 1992; Roso´n et al., 1997; Taboada et al., 1998):  0  X Sz $Az h

The protocol established by the LOICZ (Land Ocean Interactions in the Coastal Zone) and developed by Gordon et al. (1996) for a quasi-steady state ‘mass-budget model’ was used to determine the water budget inside the Pontevedra Ria. This protocol has been already applied to the Western Galician Rias by Prego and Fraga (1992). The Pontevedra Ria can be considered as a single partially mixed reservoir with two layers: an upper water layer flowing out of the reservoir and a lower incoming seawater layer. The sea-boundary is located at the cross-section between Udra and Cabicastro Capes (dashed line in Fig. 1). The defined crosssection is the natural boundary of the inner and middle ria zones with respect to its external or oceanic zone (Dale et al., 2004). In addition, it is the best location for oceane ria exchange quantification (Go´mez-Gesteira et al., 2003) because it is narrow and the currents are strong and parallel to the ria axis, minimizing the errors due to transverse currents (Kjerfve et al., 1981; Taboada et al., 1998). The reservoir has a volume of 1.47 km3 and a surface area of 69 km2. The water budget of a reservoir with a volume V can vary due to freshwater contributions by river run-off (Qr), sewage (Qs), direct precipitation, groundwater and losses by evaporation. The sum of these contributions is the net residual flow of water, i.e. the incoming ria flow (Qin) plus the outgoing ria flow (Qout). In the Pontevedra Ria underground inputs have not been observed, and the rain and evaporation from the ria

ð1Þ

Az

ð3Þ

where A corresponds to the area at each meter depth, z, in the cross-section of the ria and h is 40 m, the depth of St.3. The separation level between currents (zero velocity level) varied from 9 to 17 m depth during the six ria cruises. From the incoming and outgoing water flows, the nutrient salt exportation (Fout) and importation (Fin) of the ria can be quantified as: Fout ¼ Cout $Qout and Fin ¼ Cin $Qin

ð4Þ

where Cout and Cin are the averaged nutrient salt concentrations in the incoming and outgoing water flows through the selected cross-section of the ria. Finally, the nutrient budget, B, is quantified as the difference between the incoming and outgoing nutrient flux of the ria with offshore seawaters: B ¼ SF ¼ Fout  Fin

ð5Þ

3. Results 3.1. Thermohaline variables Cruises carried out in January reflected the mid-winter thermohaline conditions (MW). Under an upwelling event (Fig. 3a),

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422 17

(a)

Upwelling events

16 MW IPC 15 LW

Temperature (ºC)

14 13

S

St. 1 St. 3

ENACW 35.2

35.4

35.6

(b)

35.8 Salinity 36.0

Non-upwelling conditions

16

MW

15

LW

14 S 13 St. 1 St. 3

ENACW

12

Fig. 3. TS diagrams corresponding to the water column at St.1 (the main ria mouth) and at St.3 (reservoir boundary) during Mid-Winter (MW), LateWinter (LW) and Summer (S). (a) corresponds to cruises carried out under upwelling conditions and (b) to cruises under non-upwelling conditions. The distance between points is one meter. The line represents the ENACW water mass along the Galician coast (Fraga, 1981). The dashed square delimits the water body of IPC in the continental margin (150e200 m depth) near Vigo Ria, according to Frouin et al. (1990).

according to the positive upwelling index (UI) (Fig. 2), water temperatures showed thermal inversion with values ranging from 14.2  C (at the ria mouth: St.1, Fig. 1), 14.6  C (in the inner part of the estuary: St.3, Fig. 1) near the surface to 15.5  C near the bed. Surface salinity ranged from 35.1 at the ria mouth to 35.4 in the inner part. Near bed salinity values were greater than 35.9 throughout the ria. Under non-upwelling conditions (Fig. 3b), the influence of the river near the surface was more noticeable (with salinities lower than 26.0) than during the upwelling event (salinities higher than 35.4). Water temperatures showed a slight thermal inversion and bed salinities were close to 35.5 throughout the ria. Cruises carried out in March reflected the late-winter thermohaline conditions (LW). Under upwelling event (Fig. 3a), thermohaline variables varied along the water column and along the ria. Surface salinity ranged from values close to 35.6 at the ria mouth to 35.1 in the inner part of the ria due to the river influence. In contrast, the surface temperature was practically constant along the estuary (15.5  C). Salinity and temperature (TS) near the bed reached values higher than 35.8 and 14  C, respectively, along the ria. Under non-upwelling conditions (Fig. 3b), the TS profile was homogeneous along the water column and along the ria with near-surface salinity values of 34.0 due to the river influence and bottom salinity values higher than 35.6 at the ria mouth and close to 35.4 in the inner part of the estuary due to the different station depths. Temperature values were constant throughout the ria with values close to 15  C.

413

Cruises carried out in June and July reflected the summer thermohaline conditions (S). Under an upwelling event (Fig. 3a), surface salinity values were higher than 35.5 along the ria, showing the negligible influence of the river discharge. Surface temperature was higher than 16  C, showing the solar heating of the surface water typical of summertime. Bottom salinity and temperature values were close to those of ENACW (salinity higher than 35.7 and temperature lower than 13  C). Under non-upwelling conditions (Fig. 3b) thermohaline variables were homogenous along the ria. The river influence on surface salinity was still patent, with values lower than 34.0. Bottom salinity and temperature values distant from those of ENACW were observed. 3.2. Nutrient salts and oxygen Dissolved oxygen and nutrient salt concentrations were evaluated in the ria during cruises carried out in MW (Fig. 4a), LW (Fig. 4b) and S (Fig. 4c) by means of vertical profiles along the main channel of the ria under upwelling and non-upwelling conditions. In addition, the nitrate, phosphate and silicate concentrations were analyzed as a function of the density both under upwelling-favorable and -unfavorable conditions (Fig. 5). During cruises carried out in MW the water was well oxygenated (91e106%; Fig. 4a) and nutrient concentrations were in the  range of 2e38 mM for NO 3 , 0e1.2 mM for NO2 , 0e1.2 mM for þ 2 NH4 , 0.02e0.24 mM for HPO4 and 1e64 mM for H4SiO4 (Figs. 4a and 5, circles). The highest concentrations were always measured near the surface at the ria head. In addition, these concentration values showed an inverse relationship with density, decreasing with depth (Fig. 5, circles). In LW the percentage of dissolved oxygen decreased from 115% near the surface to 80% near the bed in the inner-middle zone of the ria (Fig. 4b). Nutrient concentrations were in  the range of 0e8 mM for NO 3 , 0e0.8 mM for NO2 , þ 2 0.1e2.1 mM for NH4 , 0.01e0.29 mM for HPO4 and 1e 31 mM for H4SiO4 (Figs. 4b and 5, black points). Nutrient depletion was observed near the surface throughout the ria with the exception of the area close to the river mouth. Water column remineralization was detected on this date. Nutrient salts increased with depth, reaching their maximum concentrations near the bed. Nitrate reached its maximum value during upwelling conditions and ammonium during non-upwelling ones. In addition, these concentration values showed an increase with density (Fig. 5, black points). In summer, nutrient levels were in the range of 0e11 mM  þ for NO 3 , 0e0.8 mM for NO2 , 0e3.9 mM for NH4 , 2 0.03e1.58 mM for HPO4 and 1e16 mM for H4SiO4 (Figs. 4c and 5, asterisks). In the first 20 m of the water column nutrients were depleted and an enrichment of oxygen (100e125% saturation) was observed, except in the ria head where nitrate and ammonium concentrations were low but þ not null (4 mM for NO 3 and 0.4 mM for NH4 ). Below 20 m depth, nutrients increased towards the bottom, mainly during upwelling, and nitrate, phosphate and silicate reached the highest values measured during the period of study.

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depth (m)

(a)

Upwelling 0

1

Station

2

3

4

5

100

6

7

8

Non-Upwelling 1

2

3

95

4

5

6

7

100

8 100

20

40

Dissolved Oxygen (%) 0

4

Dissolved Oxygen (%)

5 2

20

25

20

15

8

3

6

2

4 3

40

Nitrate (µM)

Nitrate (µM) 0 0.8

0.4

0.2 20

1.0

0.6

0.6

0.4

40

Nitrite (µM)

Nitrite (µM) 0

1.2 0.4

0.8

0.8

20 0.4 0.4

40

Ammonium (µM) 20

15

10

5

km

Ammonium (µM) 0

20

15

10

5 km

0

Mid-Winter (MW) Fig. 4. Contour maps of dissolved oxygen, nitrate, nitrite and ammonium along the main channel of the ria in (a) Mid-Winter, (b) Late-Winter and (c) Summer under upwelling and non-upwelling conditions.

Ammonium and nitrite showed higher values during non-upwelling conditions only. In the sub-surface layer, remineralization decreased oxygen saturation to 57% during upwelling and 85% during non-upwelling conditions.

3.3. Chlorophyll, primary production and phytoplankton species During MW, chlorophyll a (Chl-a) was low in both upwelling and non-upwelling cases. Values ranged from 7 to 16 mg Chl-a m2. Microflagellates were the dominant group with abundances exceeding 1500 cells ml1. Diatoms dominated the microphytoplankton with average values ranging from 20 to 40 cells ml1. Representative species or taxons of this group (Table 1) were Navicula spp., Thalassiosira spp., Pseudo-nitzschia pungens, Skeletonema costatum and Nitzschia longissima. Dinoflagellates were poorly represented with values ranging from 1 to 3 cells ml1, with Scrippsiella

trochoidea and Amphidinium flagellans as the most characteristic species. During LW an increase in chlorophyll and phytoplankton abundance was noticeable during both conditions. Chlorophyll concentrations ranged from 81 mg Chl-a m2 during nonupwelling conditions to 114 mg Chl-a m2 during upwelling events. Microflagellate abundance was in the range of MW values. The increase in diatoms was remarkable compared with MW, reaching abundances higher than 700 cells ml1 under non-upwelling conditions and higher than 1000 cells ml1 during upwelling. Several species of Chaetoceros, Leptocylindrus danicus and Pseudonitzschia pungens were the species with higher abundance. Dinoflagellates showed a reduced increase, and abundance kept around 8 cells ml1 during both cruises. Heterocapsa niei, Amphidinium flagellans and Scrippsiella trochoidea were dominant within this group. During S there were two definite and opposite patterns with respect to phytoplankton biomass and abundance. While primary production was slightly higher during upwelling, the

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422

415

(b) depth (m)

Upwelling 0

1

Station

2

3

4

5

7

6

Non-Upwelling

8

1

2

4

3

5

6

8

7

110

110

100

90

20

100

80 90

40

Dissolved Oxygen (%)

Dissolved Oxygen (%)

0

12

20

2

1

6

4

1 40

Nitrate (µM)

Nitrate (µM)

0 0.2 20

0.2

0.6 0.4 0.2 0.4

40

Nitrite (µM)

Nitrite (µM) 0

0.8 0.4

0.4

0.8

20

0.8

1.6

40

Ammonium (µM) 20

15

10

5

km

Ammonium (µM) 0

20

15

10

5

km

0

Late-Winter (LW) Fig. 4 (continued).

chlorophyll increased from 36 mg Chl-a m2 during nonupwelling to nearly 150 mg Chl-a m2 during upwelling conditions. Microflagellates reached the highest abundance in summer compared with other periods (Table 1). They were especially important during non-upwelling conditions. Diatom abundance increased by more than a factor of 3 from nonupwelling to upwelling conditions (from 380 to 1400 cells ml1). Dinoflagellates reached higher values than during other periods but their abundance was much lower than that of diatoms, ranging from 40 to 50 cells ml1. Species of Chaetoceros, Leptocylindrus danicus and Pseudonitzschia pungens dominated the diatom community. Differences between upwelling and non-upwelling conditions were related to changes in abundance rather than changes in species composition. Within dinoflagellates, Scrippsiella trochoidea, Heterocapsa niei and Amphidinium flagellans were the dominant species. Other species belonging to other groups, such as the Prymnesiophyceae Phaeocystis pouchetii, were relevant during this period even though their abundance was consistently low compared to that of diatoms or dinoflagellates.

4. Discussion 4.1. Mid-winter upwelling event Salinity in MW-up was higher in comparison with the typical ria levels (Prego et al., 2001) and the thermohaline variables (Fig. 3) suggest that upwelled seawater may be associated with the subtropical watermass driven by the poleward current (Frouin, 1990). IPC flows at 150e200 m depth along the Galician margin (Sordo et al., 2001), penetrating into the continental shelf of the Western Rias and later being injected into the Pontevedra Ria as a result of meteorological forcing. Following this, a fast water riaeocean exchange occurs jointly with the thermohaline change of the ria properties. Salinity values and the continental contributions of freshwater make it possible to quantify the water flow exchanges and nutrient fluxes through the ria boundary and their budgets using equations (1) to (5) and the data of Table 2; the results are summarized in Table 3. The residence time of water inside the ria was only 4 days in MW-up, i.e. one-third

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depth (m)

(c)

Upwelling 0

1

Station

2

3

4

5

6

7 110

Non-Upwelling

8

1

2

120

4

3

5

6

7

8

110

20

100

100

80 60

90

40 Dissolved Oxygen (%)

Dissolved Oxygen (%) 0

2 1

20 8

4

2

4

6

2

1 2 3

10 4

11

40

5

Nitrate (µM)

Nitrate (µM)

0

20

0.2 0.4

0.2 0.4

0.6

0.6 40

Nitrite (µM)

Nitrite (µM) 0

0.8 0.4 0.4

20

1.2 2.0

0.8 1.6 2.0

2.4

40

3.2 Ammonium (µM)

Ammonium (µM) 20

15

10

5

km

0

20

15

10

5

km

0

Summer (S) Fig. 4 (continued).

of the annual average residence time proposed by GomezGesteira et al. (2003) for the same ria reservoir. The fast residual circulation is a consequence of both the offshore wind regime and the river flow. When one of these two forces is weak, the residual flows decrease. This may occur during the dry season under atmospheric conditions that favor upwelling but with scarce river flow (7 days of S-up residence time) and also during the wet season when the river discharge is large but there is no upwelling. On the other hand, the residence time increases to 2e4 weeks when the southern winds blow at the shelf, retaining the water inside the ria (Go´mez-Gesteira et al., 2001). The nutrient salt levels coming into the ria were also affected by the increase of residual circulation, which dilutes the fluvial nutrient concentrations, and also by the IPC water-body which is low in nutrients (Fig. 5). A combination of both processes results in a large decrease in nutrient concentrations (Fig. 4a) and, therefore, the outgoing water in the MW-up event had one-fourth of the nutrient content compared with the previous MW-nu situation (Table 2). In

contrast, in summer the upwelled seawater is ENACW, rich in nutrient salts (Fraga, 1981; Prego et al., 1999) and, in addition, there is no light limitation. Consequently, phytoplankton actively grows, and nutrient budgets are positive (Table 3), while in MW-up the ria budget is negative, as the nutrients are exported to the ocean. The flow depends on nutrient concentration and the outgoing flow of water, so that the nutrient flux budget in MW-up was half of dissolved inorganic nitrogen (DIN) compared with those measured in MW-nu conditions (Table 3). This assumption is not applicable to phosphate that may be retained by the reaction of inorganic adsorption onto clays (Prego, 1993), resulting in a low or slightly positive budget. The nutrient fluxes are in the same order of magnitude as those quantified in winter without upwelling in the neighboring Vigo Ria (Prego, 1994; Prego et al., 1995). Discriminant analysis of phytoplankton samples clearly segregated the four groups defined a priori according to the ANOVA (Fig. 6). Discriminant functions 2 and 3 group the characteristic species in each period. The separation is not as clear as that of the samples because most of species are

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422

Upwelling

417

Non Upwelling

12

Nitrate (μM)

10 8 6 4 2 0

MW LW S

Phosphate (μM)

0.6

0.4

0.2

0.0

Silicate (μM)

16 12 8 4 0 26.0

26.5

27.0

25.0

γt (kg·m-3)

25.5

26.0

26.5

27.0

γt (kg·m-3)

Fig. 5. Diagrams of gt (kg m3) versus nitrate, phosphate and silicate (in mM) in the water column at St.1 (the main ria mouth) and St.3 (reservoir boundary) under upwelling and non-upwelling conditions: Mid-Winter (MW; circles), Late-Winter (LW; black points) and Summer (S; asterisks).

present in all situations, and only changes in the relative contribution for each period were observed. Furthermore, MW-nu is characterized by a dominance of Nitzschia longissima and Skeletonema costatum. In MW-up there is no effect at all on phytoplankton because light rather than nutrients is the limiting factor for growth. Even without limiting light conditions, upwelling during winter could cause an enhancement of estuarine circulation and a dispersion of phytoplankton, thus preventing accumulation of biomass if speed of outflow is higher than phytoplankton growth. 4.2. Late-winter upwelling event At the end of the winter and after favorable atmospheric conditions for upwelling, the water entering the ria was saltier than LW-nu, but the IPC, observed in MW-up, did not play any role in LW-up. The IPC (also named the Christmas Current) is more intense from December to February (Pingree, 1993) and therefore the incoming ria seawater from the Galician Continental Margin may be different in January and March. Thus, the thermohaline properties (Fig. 3) indicated the presence of ENACW of subtropical origin. Therefore, the LW-up salinity range is higher than the one measured in S-up, because the salinity increases with the progressive influx

of central seawater of southern origin during the year (Rı´os et al., 1992). The LW-up nutrient concentrations were lower than those of the S-up (Fig. 5), in agreement with the regression equations of temperatureenutrients for ENACW transported by  the Portugal coastal countercurrent proposed by AlvarezSalgado et al. (2003). But LW-up nutrient inputs were higher than those observed during LW-nu. This is important with respect to the phytoplankton spring bloom that can occur on these dates (Casas et al., 1999; Varela et al., 2001, 2005) because there is an extra nutrient input into the ria. So, the DIN budget was three times higher than the one measured in LW-nu (Table 3). Consequently, an upwelling event in the second fortnight of March made the ria more productive than in the absence of upwelling, while an upwelling in January had no importance with respect to primary production. However, the upwelling season (MayeSeptember) is always the most productive period for the Western Galician Rias (Prego, 1993; Figueiras et al., 2002; Varela et al., 2004, 2005) as indicated by the S-up nutrient flow and budget, which was double that of the LW-up event (Table 3). During spring and summer, Western Rias are considered to be biogeochemical reactors (Prego, 1993), processing inorganic nutrients to synthesize organic compounds in the photic

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422

418

Table 1 Mean and standard deviation of selected species of the most important groups found in Mid-Winter (MW), Late-Winter (LW) and Summer (S) during upwelling (up) and non-upwelling (nu) conditions. Species abundances in cells ml1 GROUP/Species

MW-up

DINOFLAGELLATES Amphidinium flagellans Heterocapsa niei Prorocentrum micans Scrippsiella trochoidea DIATOMS Cerataulina pelagica Chaetoceros auxosporas Chaetoceros curvisetus Chaetoceros didymus Chaetoceros spp. Eucampia zoodiacus Guinardia delicatula Guinardia striata Leptocylindrus danicus Leptocylindrus minimus Melosira islandica Navicula spp. Nitzschia longissima Pseudonitzschia delicatissima Pseudonitzschia pungens Rhizosolenia imbricata Skeletonema costatum Thalassionema nitzschioides Thalassiosira levanderi Thalassiosira rotula Thalassiosira sp. OTHER GROUPS Phaeocystis pouchetii Eutreptia spp. MICROFLAGELLATES

MW-nu

LW-up

LW-nu

S-up

S-nu

1.0  0.5 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0

3.0  1.0 0.6  0.8 0.0  0.0 0.0  0.0 1.2  1.6

9.0  9.0 2.3  1.7 3.7  4.2 0.1  0.0 0.8  0.5

8.0  7.0 1.9  2.0 2.1  1.6 0.1  0.0 1.6  0.1

51.0  52.0 8.7  1.7 28.7  20.8 0.5  0.3 6.0  1.7

39.0  38.0 2.3  1.5 34.7  10.4 0.3  0.1 0.9  0.3

20.0  6.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 8.0  4.0 4.1  0.8 0.0  0.0 0.0  0.0 0.0  0.0 5.8  5.9 0.0  0.0 0.0  0.0 0.6  0.8 0.0  0.0

43.0  20.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 0.0  0.0 1.7  1.4 0.0  0.0 0.0  0.0 0.0  0.0 1.1  1.6 6.3  0.8 5.8  2.2 2.3  1.6 4.6  3.6 0.0  0.0 9.3  6.6 1.2  1.6 2.3  3.3 0.0  0.0 5.2  5.1

1104  984 6.1  4.3 20.1  19.7 17.0  9.1 2.2  1.9 554.0  565.4 3.6  4.9 2.2  0.7 18.9  19.4 13.2  4.5 4.3  5.5 0.0  0.0 0.0  0.0 3.4  2.0 0.0  0.0 494.3  28.2 2.1  1.6 0.5  0.6 3.9  3.0 0.0  0.0 0.0  0.0 0.0  0.0

749.0  292.0 3.5  1.3 3.0  2.8 33.1  14.8 19.5  13.2 436.7  71.8 0.0  0.0 1.2  0.7 0.6  0.1 41.0  17.7 6.9  3.2 0.0  0.0 0.3  0.2 2.3  0.3 0.3  0.5 173.0  25.2 0.3  0.2 0.8  0.8 7.8  2.1 0.0  0.0 0.0  0.0 0.0  0.0

1387  1474 0.1  0.0 3.2  2.2 3.9  2.6 9.0  4.5 138.7  91.8 5.0  3.6 1.2  0.5 9.1  4.3 132.3  62.3 0.0  0.0 0.0  0.0 0.3  0.4 1.9  0.3 19.5  11.3 947.0  355.1 10.9  1.0 3.5  2.5 4.2  0.8 0.0  0.0 3.5  0.6 42.9  32.2

380.0  1001 5.5  6.7 2.0  2.2 2.1  2.1 0.3  0.5 63.2  78.5 0.0  0.0 3.0  3.2 0.7  0.6 240.7  191.1 11.2  15.4 0.0  0.0 0.1  0.1 3.0  3.1 18.4  21.0 20.2  18.0 0.6  0.5 2.3  3.3 0.6  0.4 0.0  0.0 0.0  0.0 0.0  0.0

0.0  0.0 0.0  0.0

0.0  0.0 4.0  2.2

2.0  2.8 0.0  0.0

0.0  0.0 0.0  0.0

20.7  9.6 0.2  0.1

14.0  12.1 0.2  0.2

2460  909

4861  1006

2980  1060

1607  87

3465  718

8719  751

zone. Eventually, this organic matter sinks and becomes mineralized in the water column and/or sediments (Prego,  1994; Alvarez-Salgado et al., 1996). This biogeochemical cycle exists during an LW-up event but is more intense during the S-up period. The dissolved oxygen depletion near the

bottom bed decreases from LW to S. In parallel, nutrient salt concentrations increase at the same depths (Fig. 4b and c), although in both events the typical nitrateenitriteeammonium echelon (Prego et al., 1999) was observed. However, the displacement of the nitrate maximum towards the deeper ria

Table 2 Mean salinity values and nutrient salts concentrations (mM) in the incoming and outgoing flows of seawater trough the reservoir section defined in the Pontevedra Ria (Fig. 1) Season

Condition

Ria

Salinity

NO 3

NO 2

NHþ 4

DIN

HPO2 4

H4SiO4

Mid-Winter

Upwelling

Input Output Input Output

35.904 35.499 34.875 30.901

2.87 3.57 6.68 16.85

0.11 0.18 0.46 0.91

0.20 0.20 0.69 1.30

3.19 3.95 7.83 19.06

0.09 0.06 0.09 0.14

1.47 3.63 6.21 19.40

Input Output Input Output

35.902 35.507 35.283 34.690

2.37 0.07 0.73 0.49

0.08 0.01 0.11 0.02

0.31 0.30 0.85 0.28

2.76 0.37 1.69 0.79

0.19 0.08 0.09 0.02

1.49 0.37 2.58 1.33

Input Output Input Output

35.735 35.588 35.422 34.490

3.51 0.22 1.79 0.30

0.24 0.13 0.36 0.08

0.74 0.23 1.85 0.65

4.49 0.58 3.99 1.03

0.35 0.18 0.19 0.08

6.98 1.24 3.68 2.49

Non-upwelling

Late-Winter

Upwelling Non-upwelling

Summer

Upwelling Non-upwelling

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419

Table 3 Incoming and outgoing reservoir water flows (m3 s1), nutrient salts fluxes (mol s1) and their budgets in the Pontevedra Ria. A negative sign denotes a net loss of inorganic nutrients from the ria and a positive sign denotes a net input. DIN is the dissolved inorganic nitrogen Season

Condition

Ria

Watera

NO 3

NO 2

NHþ 4

DIN

HPO2 4

H4SiO4

Mid-Winter

Upwelling

Input Output Budget Input Output Budget

4222 4270 48 506 571 65

12.1 15.3 3.2  0.1 3.4 9.6 6.2  0.3

0.48 0.78 0.3  0.1 0.23 0.52 0.3  0.1

0.84 0.83 0.0  0.1 0.35 0.74 0.4  0.1

13.5 16.9 3.4  0.3 4.0 10.9 6.9  0.5

0.39 0.25 0.14  0.02 0.05 0.08 0.03  0.03

6.2 15.5 9.3  0.4 3.1 11.1 8.0  0.4

Input Output Budget Input Output Budget

1727 1746 19 1597 1624 27

4.1 0.1 4.0  0.1 1.2 0.8 0.4  0.2

0.14 0.01 0.1  0.1 0.18 0.03 0.2  0.1

0.54 0.52 0.0  0.1 1.35 0.46 0.9  0.2

4.8 0.7 4.1  0.3 2.7 1.3 1.4  0.5

0.33 0.14 0.19  0.02 0.15 0.03 0.12  0.02

2.6 0.7 1.9  0.5 4.1 2.2 1.9  0.5

Input Output Budget Input Output Budget

2536 2546 10 695 714 19

8.9 0.6 8.3  0.4 1.2 0.2 1.0  0.3

0.61 0.34 0.3  0.1 0.25 0.06 0.2  0.1

1.89 0.58 1.3  0.2 1.29 0.46 0.8  0.2

11.4 1.5 9.9  0.7 2.8 0.7 2.1  0.6

0.89 0.46 0.43  0.03 0.13 0.06 0.07  0.03

17.7 5.4 12.3  0.4 2.6 1.8 0.8  0.6

Non-upwelling

Late-Winter

Upwelling

Non-upwelling

Summer

Upwelling

Non-upwelling

a

Water budget is equal to the freshwater contribution to the ria.

mouth is more important in the S-up event because the residual current speed through the reservoir-boundary is higher than in the LW-up event (Table 3). In the same way, the chlorophyll increase (Fig. 7) is more significant in S-up because, during stratification (i.e. S-nu), nutrients become exhausted, limiting phytoplankton growth. The injection of new rich upwelled water increases the levels of nutrients, allowing

Discriminant Analysis for species 0.5 L. danicus

0.4

LW

C. pelagica

Discriminant function 3

0.3

S-up

Chaetocerosspp P. pungens

0.2

T. nitzschioides

Ch. curvisetus

0.1

H. niei

P. micans

Ch. didymus

Microflagellates S-nu

Chaetoceros aux. 0.0

P. pochetii -0.1

N. longissima

0.2

MW

P. delicatissima S. costatum

-0.3

phytoplankton growth and the subsequent accumulation of phytoplankton biomass (Bode and Varela, 1998). The taxonomic composition of the phytoplankton community does not change very much from non-upwelling to upwelling conditions in summer: diatoms such as Pseudonitzschia pungens, Thalassionema nitzschioides, Cerataulina pelagica and several species of Chaetoceros dominate (Fig. 6). The differences are merely quantitative, even though microflagellates and some species of dinoflagellates, such as Heterocapsa niei, are better represented during non-upwelling conditions (Fig. 6). From LW to S, the phytoplankton species composition (Fig. 6) does not vary noticeably. Diatoms were dominant during spring and summer upwelling blooms, with the same species present and changing only in relative proportions. This is a situation similar to that previously described for the Galician Rias (Figueiras and Niell, 1987; Varela et al., 2004, 2005). Only during the S-nu event was a relative increase of dinoflagellates and microflagellates observed. This mixture of species is probably a consequence of a surface output from the ria and a bottom input from the ocean, resulting in a continuous exporteimport of the same phytoplankton populations as upwelling pulses succeed each other (Figueiras and Niell, 1987).

Thalassiosira sp

5. Conclusions and summary

-0.4 -0.5 -0.3

-0.2

-0.1

0.0

0.1

0.2

0.3

Discriminant function 2 Fig. 6. Projection of the approximate distribution of phytoplankton species within each period. The groups were defined as Mid-Winter (MW), LateWinter (LW) and Summer (S-up with upwelling and S-nu without it), according to the results of 2-way ANOVA.

Rias have usually been considered as an estuary type associated with the northwestern coastlines of Spain and Brittany, the southwestern coast of England and Ireland, several parts of the Mediterranean and the southeastern regions of China and Australia (Fairbridge, 1980). However, the landesea exchange may also be influenced by the ocean upwelling in the coastal systems of the eastern boundary of the North Atlantic Ocean

R. Prego et al. / Estuarine, Coastal and Shelf Science 73 (2007) 409e422

420

Water Column Chlorophyll (mg Chl a·m-2)

(a)

250 Non-upwelling conditions Upwelling events b

200 a 150

a 100

50

a

a a

0 Mid-Winter

Late-Winter

Summer

(b)2000

Diatom abundances (Cells·mL-1)

Non-upwelling conditions Upwelling events

a

b

1600

1200 a a

800

400

a

a

0 Mid-Winter

Late-Winter

Summer

Fig. 7. (a) Mean and standard deviation of water column chlorophyll a (mg Chl-a m2) integrated to Sts.2, 4 and 6 under non-upwelling (gray) and upwelling (dark gray) conditions. (b) Mean and standard deviation of water column diatom abundances (cells ml1) integrated to the Sts.2, 4 and 6 under non-upwelling (gray) and upwelling (dark gray) conditions. Means that are not significantly different at P < 0.05 (2-way ANOVA, Bonferroni post-tests) are labeled with the same letter.

(Wooster et al., 1976). In particular, this phenomenon (Fraga, 1981) has been profusely studied in the Western Galician Rias  during the upwelling period (Alvarez-Salgado et al., 1993; Prego et al., 1999). Out-of-season upwelling events have been recently analyzed in the Western Galician Rias, but  only from a hydrographical point of view (Alvarez et al., 2003; deCastro et al., 2006). In the present study, the consequences of a winter upwelling event on biogeochemical and phytoplankton patterns were analyzed. During the mid-winter-upwelling event the Pontevedra Ria is characterized by a fast outflow with a water residence time of 4 days. This upwelling event introduces the water-body driven by the IPC into the ria, but the riaeocean water exchange is not solely due to upwelling, as occurs when the river flow is very low. Therefore, the residual ria circulation in

winter results from upwelling and fluvial forcing, which increases the incoming IPC in the ria. The IPC seawater intrusion varies the thermohaline properties of the ria, making it much more salty and rendering it poor in nutrient salts. These patterns differentiate the winter upwelling event from the summer one, when ENACW makes the ria eutrophic (Dale and Prego, 2002). There is scarce information on the nutrient contents of the IPC water-body off the Galician coast, and there is none in connection with its ria upwelling. The measured values indicated 2.9 mM of nitrate, 0.1 mM of phosphate and 1.5 mM of silicate with a salinity of 35.90 and temperature of 15.2  C in upwelled seawater entering the Pontevedra Ria. No biological impact was observed in the mid-winter upwelling, but the March event increased the productivity of the spring bloom as a result of the extra nutrient input from the upwelled ENACW. Although the ria biogeochemical processes in the late winter were qualitatively similar to those of the summer upwelling, the primary production was not higher. Diatoms were dominant during both events, with the same species but in different relative proportions. In contrast, chlorophyll distribution was different along the axis ria during upwelling events: in late winter water upwells into the inner part where phytoplankton develops, but during summer the upwelling occurs in the outer part, where the chlorophyll maxima were measured. Consequently, variations in the properties of oceanic water due to seasonal changes can play a pivotal role in mediating the biogeochemical response of the ria systems to upwelling. Finally, winter upwelling events have a considerable impact on coastal ecosystems due both to the properties of the upwelled water and to the dispersal effect on biogeochemical elements and plankton organisms, including during the spawning season. The increase or decrease of these events during recent decades remains an open question. Further research, involving finer monitoring, should be conducted. Acknowledgments We thank Dr. Jose´ M. Cabanas (IEO) for the upwelling  index data; Dr. Manuel Alvarez Eijo (USC) for the calibration of the river gauging station; Captain Jorge Alonso, the crew of the RV Mytilus and our colleagues in the project for their kind assistance during cruises; and Paula Ferro for her technical assistance. This work is a contribution to the Spanish LOICZ program and was supported by CICYT under the projects PONTRIA (ref. MAR96-1782) and METRIA (ref. REN2003-04106-C03). References  Alvarez, I., deCastro, M., Prego, R., Go´mez-Gesteira, M., 2003. Hydrographic characterization of a winter-upwelling event in the Ria of Pontevedra (NW Spain). Estuarine, Coastal and Shelf Science 56, 869e876.  Alvarez, I., deCastro, M., Gomez-Gesteira, M., Prego, R., 2005. Inter- and intra-annual analysis of the salinity and temperature evolution in the Galician Rias Baixas-ocean boundary (northwest Spain). Journal of Geophysical Research 110, C04008. doi:10.1029/2004JC002504.

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