Coupling between the thermohaline , chemical and biological fields during summer 2006 in the northeast continental shelf of the Gulf of Cádiz ( SW Iberian Peninsula )

The coupling between the thermohaline, chemical and biological variables on the northeast continental shelf of the Gulf of Cádiz was determined during the Emigas I survey in summer 2006. Samples were collected to chemically characterize the different water types and to analyze the chlorophyll a distribution. Four different water masses were identified: North Atlantic Central Water (NACW), Surface Atlantic Water (SAW), considered a modification of NACW, and South and North Surface Waters. The highest nutrient levels were found in subsurface NACW, while surface waters were almost nutrientdepleted except in the Guadalquivir region. The isopycnal level of 26.3 kg m-3 marked the limit between nutrient-rich NACW and nutrient-poor surface waters. At the offshore stations, the subsurface cholorophyll a maximum was located at the depth of nitracline and associated with the 26.3 kg m-3 isopycnal level rather than with the pycnocline depth. At the inshore stations, chlorophyll a maxima were observed at the bottom, except for the surface maximum in the River Guadalquivir region.


INTRODUCTION
From a geochemical and biological point of view, coastal areas are very active sites where major exchang-es with the open ocean take place (Gattuso et al., 1998).About 25% of total oceanic primary production occurs on the continental shelves (Wollast, 2002), associated with continental nutrient input (Wollast, 1993) and up-welling processes (Wollast, 1998).The Gulf of Cádiz is a basin that connects the North Atlantic Ocean and the Mediterranean Sea through the Strait of Gibraltar.The flux of Atlantic waters affects the oceanographic characteristics of surface waters in the Gulf of Cádiz and plays an important role in the regulation of circulation in the Mediterranean Sea (Navarro and Ruiz, 2006).In the basin three different structures were identified (Stevenson 1977): the upwelling Portuguese zone off Cape San Vicente (Fiuza et al., 1982;Fiuza, 1983), the thermal front southeastward of Cape Santa Maria (Huelva front), correlated with the wind regime (Fiuza et al., 1982;Fiuza, 1983;Folkard et al., 1997), and the anticyclonic circulation of the Tarifa Eddy at Cape Trafalgar (Stevenson, 1977) (Fig. 1).In general, the circulation in the Gulf of Cádiz is predominantly anticyclonic with short-term variations during summer (Garcia et al., 2002;Criado-Aldeanueva et al., 2006b) and likely to switch to cyclonic in winter (Garcia-Lafuente and Ruiz, 2007).Different water masses were found in the Gulf of Cádiz (Gascard and Richez, 1985;Criado-Aldeanuvea et al., 2006a).At surface, two different water types were described: Surface Atlantic Water (SAW) and Surface Water (SW).SAW is located in the central part of the gulf in the anticyclonic meander while SW, warmer and fresher than the latter, is observed over the continental shelf.At intermediate depth, the basin is filled by North Atlantic Central Water (NACW) lying between 100 and 700 m (Folkard et al., 1997) and characterized by a linear relationship in the TS diagram.The NACW upwells on the south and west coast of Portugal, off Cape St. Vincent and Cape St. Maria (Fiuza, 1983;Folkard et al., 1997;Revals and Barton, 2002;Sanchez and Revals, 2003).Below a certain depth (<700 m) the basin is occupied by Mediterranean water (MW) identified by its high salinity (>36.1).
Previous studies have shown that the Gulf of Cádiz experiences strong oligotrophic conditions during summer, as surface nitrate levels were almost depleted for the entire region except the River Guadalquivir outflow (García et al., 2002;Huertas et al., 2005;Navarro et al., 2006;Navarro and Ruiz, 2006;Ruiz et al., 2006;Huertas et al., 2006).All these studies were devoted to analyzing the chlorophyll a distribution in the Gulf of Cádiz and its relationship with the physical variables on a basin scale,, but no detailed survey of the continental shelf has been carried out yet.Furthermore, few studies have dealt with the chemical characterization of the water masses in the area and they mainly focus on horizontal distributions of nutrients in the upper 50 m (Prieto et al., 1999;García et al., 2002;Huertas et al., 2005;Ruiz et al., 2006;Huertas et al., 2006).Only Navarro et al. (2006) reported nutrient concentrations at 200 m depth and Garcia et al., (2002) at 100 m depth.
In this context, this paper aims to 1) chemically characterize the water types on the northeast continental shelf of the Gulf of Cádiz and 2) analyze the relationship between the thermohaline field and chemical and biological variables in the region during a summer situation.

MATERIALS AND METHODS
The study area was located on the northeastern shelf of the Gulf of Cádiz (SW Iberian Peninsula) (Fig. 1).The sampling stations selected covered an area from the Bay of Cádiz to the River Guadalquivir.The data were collected during the Emigas I oceanographic cruise, carried out from 17 to 29 June 2006 on board the R/V Mytilus.For this cruise a grid of 63 stations, shared in 9 transects, was sampled.At each station, continuous vertical profiles of temperature, salinity, pressure and fluorescence were obtained with a Seabird CTD probe coupled to a Seatech fluorometer and a Seabird 43 dissolved oxygen sensor.Photosynthetic available radiation (PAR) profiles were also measured using a Biospherical QSP 2000 sensor.Discrete water samples were collected at different depths (0, 20 and the deepest one depending on the bathymetry of the area) in the water column for analysis of nutrients and chlorophyll a (chl a).Samples for nitrate, phosphate and silicate were filtered on board through 0.45 µm Millipore filters, immediately frozen at -20°C and analyzed in the laboratory.Nutrients were determined by segmented flow analysis with Alpkem autoanalyzers following Grasshoff et al. (1983).The analytical errors were ±0.05 µM for nitrate and silicate, and ±0.01 µM for phosphate.Samples for chl a of about 500 mL were filtered on board using Millipore filters (0.45 µm), frozen at -20°C and then analyzed in the laboratory by fluorimetry after extraction with 90% acetone in the dark.Nitracline depth was defined as the shallowest depth at which nitrate concentration was higher than 1 µM, as described by Moran et al. (2001).The interpolation method used for the analysis of the thermohaline, chemical and biological fields distribution was kriging.

Thermohaline, chemical and chl a horizontal distributions
In Figure 2, the thermohaline, chemical and chl a surface horizontal distributions are described.Sea surface temperature varied typically between 21ºC and 24°C.This temperature distribution was marked by a strong north-south gradient with the highest values close to the River Guadalquivir.South of 36.6°N,temperature was lower than 22°C, with almost no ocean-shelf gradient.Sea surface salinity values ranged between 36.20 and T in °C, chl a in mg m -3 and nutrients in µM.
36.45 (Fig. 2).Surface nitrate and phosphate concentrations were almost depleted for the entire study area.Nitrate concentrations only reached values higher than 0.4 µM close to the mouth of the Bay of Cádiz, while the highest phosphate levels were observed in the north, close to the River Guadalquivir (>0.1 µM).Surface silicate distribution was characterized by a coast-oceanward gradient with maximum values (>1 µM) close to the River Guadalquivir.Chl a surface values were low for the whole area except close to the River Guadalquivir, where levels as high as 2.6 mg m -3 were recorded.
The subsurface temperature distribution at 20 m depth was similar to the sea surface distribution (Fig. 3), with temperatures ranging between 19ºC and 22°C.
We observed a north-south zonation in the temperature and salinity distributions.The north part was characterized by lower salinity values and an inshore-offshore temperature gradient, with minimum temperature close to the River Guadalquivir.In contrast, the subsurface temperature south of 36.6°N was mainly homogenous (20.6 ±0.7°C).At 20 m depth, nitrate and phosphate levels were still very low, with values not higher than 1 µM and 0.1 µM for nitrate and phosphate, respectively.Silicate distribution resembled the surface distribution, with a clear ocean-coastwards gradient.Finally, chl a concentrations at this depth were also higher close to the coast.The highest values were reached in the River Guadalquivir region (chl a ~2.5 mg m -3 ) (Fig. 3).T in °C, chl a in mg m -3 and nutrients in µM.

Thermohaline, chemical and chl a vertical distributions
In order to analyze the vertical distribution of the variables in the study area, we selected two transects corresponding to the north and south part (Figs. 4  and 5, respectively).The northern transect is located off the River Guadalquivir (transect F) and the south transect off the Bay of Cádiz (transect B) (Fig. 1).The maximum surface temperatures were recorded in the northern transect, causing a stronger stratification for this region compared with the south.For the northern transect, we observed a temperature variation of approximately 3.5°C in the upper 30 m (Fig. 4), compared with 2°C in the upper 30 m for the southern transect (Fig. 5).Below 30 m, the thermohaline properties were similar for the two transects.For the upper metres, the most striking feature in the salinity distributions was the lens of lower salinity in the southern transect, that it was as deep as 15 m (Fig. 5).In spite of this marked salinity minimum, the density distributions for the two transects were clearly controlled by temperature (distributions not shown).The nitrate dis-tribution for both transects showed that surface waters were completely depleted, with values lower than 1 µM from the surface to about 40-50 m depth.However, the position of the nitracline differs between the two transects.For the northern transect, it was as deep as 48 m at the most oceanic station and shoaled coastwards, being 23 m deep at station F4 (Fig. 4).In contrast, for the southern transect the nitracline deepened coastward following the 18°C isotherm (Fig. 5).The phosphate distribution of the southern transect was similar to the nitrate distribution, with values lower than 0.1 µM from the surface to about 45 m depth.However, the northern transect also showed higher values for the upper 40 m, with the maximum phosphate levels close to the River Guadalquivir (>0.15 µM) (Fig. 4).Silicate distributions followed the same trend as nitrate ones, except at the coastal stations, where levels >1 µM were recorded (Figs. 4 and 5).In transect F, the chl a distribution showed low values (chl a <0.5 mg m -3 ) in shallow waters except close to the Guadalquivir River (Fig. 4).At the offshore stations, the chl a maximum was observed at the depth of the nitracline, while it was located close to the bottom at the inshore stations, with values as high as 2.6 mg m -3 .The chl a distribution for the southern transect B was similar to the northern distribution but with lower values, showing a subsurface chl a maximum.The greatest difference was the low surface values for the entire transect (<0.1 mg m -3 ; Fig. 4 and 5).

Thermohaline and chemical characterization of water masses
Based on the previous results and applying a TS diagram, four different water types in the study area were differentiated (Fig. 6a).The cluster of points following a linear TS relationship corresponds to North Atlantic Central Water (NACW), with temperatures of 14-18°C and salinity of 36.0-36.3.Between this water mass and the salinity maximum, the water samples corresponded to Surface Atlantic Water (SAW) as described by Navarro et al. (2006).According to these authors SAW is considered as a modification of NACW due to stratification and air-sea interactions.SAW had a temperature of 18-22°C and a salinity of 36.3-36.5.Taking into account the north-south zonation described in the previous section, we discerned two different surface waters (SW): South Surface Waters with a temperature of 17-22°C and a salinity of ~36.4,and North Surface Waters with higher temperature (ΔT =20-24°C) and a salinity of 36.3-36.4.
From a chemical point of view, the nutrient vs. temperature relationships (Fig. 6b, c and d) show that colder waters are characterized by high nutrient levels, while warmer waters are characterized by low nutrient levels.The NACW was characterized by high nutrient  levels, with values between 0.06 and 9.6 µM for NO 3 , 0.12 and 0.5 µM for PO 4 and 1 and 5.5 µM for SiO 2 and with significant correlations between nutrients and temperature (P<0.05).No significant correlations between nutrients and thermohaline properties were found for SAW and North and South Surface Waters except for nitrate and silicate vs. temperature for the southern part (P<0.05)(Table 1).Significant nutrient relationships for NACW were observed, such as those between silicate and phosphate vs. nitrate (Table 1).Phosphate and silicate concentrations for surface and SAW were significantly different except for silicate concentrations of SAW and northern surface waters.
For the shallow waters, nitrate and phosphate levels were almost zero but silicate concentrations were >1 µM (Table 2).

Thermohaline characterization of water masses in the Gulf of Cádiz
Based on the thermohaline properties, four different water masses were discerned for the continental shelf of the Gulf of Cádiz in summer 2006: NACW, SAW and North and South Surface Waters.Strictly speaking, the last three can not be defined as water masses though we use this terminology for practical purposes.With some differences, the characterization is similar to that reported by Criado-Aldeanueva et al. (2006a) and Navarro et al. (2006), who state that central waters in the Gulf of Cádiz can be divided into pure NACW and modified central water, coined as SAW.On our cruise, the NACW samples showed a linear TS relationship (Fig. 6a), whereas SAW samples diverged from this linear relationship probably due to air-sea interactions (Criado-Aldeanueva et al., 2006a).SAW showed a higher temperature (between 21 and 24°C, typical of the summer season for the area [Peliz et al., 2007;Sanchez-Lamadrid et al., 2003]) and salinity than NACW, with a salinity maximum of 36.5.The isopycnal level of 26.66 kg m -3 was  proposed as the limit between NACW and SAW by Navarro et al. (2006), who observed the winter mixed layer in the Gulf of Cádiz to have a density anomaly of 26.66 kg m -3 and high nutrient levels.As the seasonal stratification proceeds, the winter mixed layer nutrient concentrations were consumed due to phytoplankton activity, so during the summer period the water volume had salinities of NACW but higher temperatures and very low nutrient levels.These authors defined this water volume as SAW and established its lower isopycnal level at 26.66 kg m -3 .We also established the limit between SAW and NACW at the nitracline depth (as explained in the next section) but in our case this limit was established at a shallower isopycnal level: 26.3 kg m -3 .Fiuza (1984) studied the central waters between 35°N and 42°N and east of the Mid-Atlantic ridge.He differentiated between ENACW (Eastern North Atlantic Central Water) of subtropical origin (ENACW T ), with T>12°C and S<35.70 and formed south of 43°N; and ENACW of subpolar origin formed north of 43°N and with colder temperatures (<10°C) and S >35.70.If we compare our data with this reference TS relationship, NACW found in the Gulf of Cádiz in June 2006 corresponded to ENACW of subtropical origin, though slightly modified.We found NACW with a slope of 12.2, which is higher than the T/S slope of 7.06 of Criado-Aldeanueva et al. (2006a) .
These two TS relationships had a higher slope than Fiuza's TS, based on the climatology for the Central Waters, so they may have shown a seasonal warming.We distinguished two types of surface waters because our study region is closer to shore and consequently more affected by continental inputs: North and South Surface Waters.This differentiation was corroborated by the TS diagram, since the northern water was less salty and warmer than the southern one, due to the influence of the River Guadalquivir.

Chemical characterization of water masses in the Gulf of Cádiz
The shallow waters in the Gulf of Cádiz during Emigas I in June 2006 were almost depleted in nitrate (<0.2 µM) and phosphate (<0.1 µM) except for the stations close to the River Guadalquivir.Similar situations were described for the summer period by García et al. (2002) and Ruiz et al. (2006).These authors found undetectable concentrations of nitrate in the upper water of the basin but with high levels in the River Guadalquivir region.Based on other studies (Ruiz et al., 2006;Huertas et al. 2006) and our own research, the system-except for the River Guadalquivir-seems to evolve from a situation of high nutrient conditions in winter to oligotrophic conditions in summer due to prolonged phytoplankton activity triggered by the spring phytoplankton bloom.At deeper levels, only Navarro et al. (2006) analyzed the nutrient distributions at the depth horizons of 75, 100 and 200 m.Our nitrate levels were similar to those reported by these authors, but their silicate values, ranging between 0.5 and -1.0 µM, were lower than our results at the same depths (silicate levels between 1.4 and 5.5 µM).It is evident that high levels of nutrients are associated with deep waters with low temperature and salinity, corresponding to NACW.This high correlation between nutrients and the thermohaline properties for NACW is clearly shown with the nitrate-categorized TS diagram (Fig. 7).The NACW samples showed higher nitrate concentrations (>1 µM), while the shallower waters (SAW and southern and northern surface waters) showed lower concentrations.Thus, based on this diagram, we establish the limit between nutrient-rich NACW and nutrient-poor water at the isopycnal level of 26.3 kg m -3 .It is important to note that our limit is shallower than the isopycnal level of 26.66 kg m -3 found by Navarro et al. (2006) in May 2001, as mentioned above.The Emigas I survey was carried out later in the year, so we should expect surface waters in June to have suffered stronger nutrient consumption since the spring phytoplankton bloom and the nitracline should therefore be deeper in the water column.However, the situation was just the opposite, with a shallower isopycnal level for June 2006.We suggest that this differentiation was due to different interannual winter conditions and important seasonal variability (Garcia-Lafuente et al., 2006), which could induce noticeable changes in the surface circulation according with Machin et al. (2006).
Only for NACW a significant correlation between nutrients was found (r 2 >0.75) (P<0.05).The nitratephosphate ratio (27.9±2.5) was higher than the Redfield ratio (Redfield et al. 1963).A high N:P ratio was also found by other authors for ENACW.During the Galicia VII cruise in the region east of 12°W and between 43 and 47°N, Fraga et al. (1985) reported an N:P ratio of 21 for the ENACW of subtropical and subpolar origin.N 2 fixation was invoked by Fanning (1987Fanning ( , 1992) ) to explain high N:P ratios in the thermocline waters of the western North Atlantic subtropical gyre.The nitrate-silicate ratio observed for NACW was 2.4 ±0.15.This ratio was almost the same as that determined by several authors in North Atlantic central waters (Treguer and Le Corre, 1979;Minas et al., 1991;Castro et al., 2006), suggesting a low incorporation of silicon relative to nitrogen.
In the River Guadalquivir we found an average N:P ratio of 37 ±4, which is higher than the Redfield ratio, indicating that the River Guadalquivir is P-limited, like most continental aquatic ecosystems (Turner et al., 2003).

Coupling between the chemical and biological fields
The distribution of chl a in the Gulf of Cádiz in June 2006 was similar to that of previous studies of the region (Huertas et al., 2005;Ruiz et al., 2006;Navarro et al., 2006;Huertas et al., 2006;Garcia et al., 2002), with a surface maximum close to the River Guadalquivir (>2 mg m -3 ) and a subsurface maximum for the rest of the area.At the offshore stations, the subsurface chl a maximum was located at the depth of the nitracline and associated with the 26.3 kg m -3 isopycnal level rather than with the pycnocline depth, as shown in Figure 8.In fact, a high correlation between nitracline depth and the chl a maximum depth for these stations (r >0.87) was obtained.Navarro et al. (2006) also found a strong correlation between the 26.66 kg m -3 isopycnal depth and the deep fluorescence maximum through the whole Gulf of Cádiz in May 2001.However, the situation changed completely for the inshore stations, where nitrate levels were lower than 1 µM for the entire water column and chl a maxima were observed at the bottom except at the River Guadalquivir stations.The chl a levels at the bottom depth were always higher than 0.1 mg m -3 , with a band of maximum values (>0.6 mg m -3 ) located approximately in the middle of each transect.These deep chl a maxima were not limited by light, as the photosynthetically available radiation was higher than 1% even at the bottom.We assumed that at these inshore stations the nutrient supply is due to efflux from the sediment based on the results by Ferrón et al. (2009), who measured positive nitrogen and phosphorous fluxes from the sediment to the water column at a series of stations off the Guadalquivir close to our stations (F3, F7 and G6, G3) and the Bay of Cádiz region during the same period of June 2006.The highest concentrations of nutrients were associated with NACW.In fact, at shallow waters low levels of nutrients were detected, except in the River Guadalquivir region.The limit between NACW and SAW was established at the isopycnal level of 26.3 kg m -3 .The high nitrate-phosphate ratio (27.9 ±2.5) suggests that phosphate is probably the limiting factor of primary production in this area during the summer period.Chl a distribution showed a surface maximum close to the River Guadalquivir and a subsurface maximum in the rest of the area.At the offshore stations, the subsurface chl a maximum was located at the depth of the nitracline and associated with the 26.3 kg m -3 isopycnal level.At the inshore stations chl a maxima were observed at the bottom except at the River Guadalquivir stations.

Fig. 1 .
Fig. 1. -Location map of the northeastern continental shelf of the Gulf of Cádiz located in the SW Iberian Peninsula.CSV, CSM and CT stand for Cape San Vicente, Cape Santa Maria and Cape Trafalgar.The grid indicates the sampling points for the Emigas I cruise, showing the reference transects analyzed in detail (transect F and B respectively).The isobar units are in metres.

Fig. 2 .
Fig. 2. -Horizontal distribution of sea surface temperature, salinity, nitrate , phosphate, chl a and silicate in the Gulf of Cádiz in June 2006.T in °C, chl a in mg m -3 and nutrients in µM.

Fig. 3 .
Fig. 3. -Horizontal distribution at 20 m depth of temperature, salinity, nitrate, phosphate, chl a and silicate in the Gulf of Cádiz in June 2006.T in °C, chl a in mg m -3 and nutrients in µM.

Fig. 4 .
Fig. 4. -Vertical distribution of temperature, salinity, nitrate, phosphate, chl a and silicate at transect F in the Gulf of Cádiz in June 2006.T in °C, chl a in mg m -3 , and nutrients in µM.

Fig. 5 .
Fig. 5. -Vertical distribution of temperature, salinity, nitrate, phosphate, chl a and silicate at transect B in the Gulf of Cádiz in June 2006.T in °C, chl a in mg m -3 , and nutrients in µM.

Fig. 6 .
Fig. 6. -Temperature-Salinity diagram (a) and relationship between temperature and nitrate (b), phosphate (c) and silicate (d) for all the collected samples during the Emigas I survey.NACW, SAW, South SW, North SW are the acronyms for North Atlantic Central Water, Surface Atlantic Water, North Surface Water and South Surface Water, respectively.NACW-TS refers line from Fiuza (1984).

Fig. 7 .
Fig. 7. -Temperature-Salinity diagram with nitrate concentration for all stations during the Emigas I survey.
CONCLUSIONS A strong vertical stratification typical of the summer season was observed in the Gulf of Cádiz in June 2006.The shallow waters close to the coast showed high salinity except close to the River Guadalquivir.We differentiated four different types of water based on the thermohaline properties: North Atlantic Central Water (NACW), Surface Atlantic Water (SAW), and South Surface and North Surface waters (SW).

Fig. 8 .
Fig. 8. -Relationship between nitrate (a), chl a (b) and density in the Gulf of Cádiz during the Emigas I survey.