Introduction

Sebastián Vizcaíno Bay (SVB), the largest coastal water body in the northeastern region of the Pacific Ocean, is located on the west coast of the Baja California Peninsula (Mexico), in the southern region of the California Current System (CCS) (Fig. 1a). Situated in a transition zone between temperate and subtropical waters, its physical and biological characteristics make it an important habitat for phytoplankton and zooplankton, and several species of high commercial value are caught in its waters, including Pacific sardine, sole, lobster, shrimp, sharks, and rays. Given the importance of this area, a better understanding is needed of the temporal and spatial variability of the environmental conditions and phytoplankton biomass, which forms the basis of the epipelagic food chain.

Figure 1 (a) Location of the hydrographic stations occupied during the IMECOCAL cruises (1998-2012) in Sebastián Vizcaíno Bay (Baja California Peninsula, Mexico). The bathymetry is given in meters (taken from NOAA: http://www.ngdc.noaa.gov/mgg/bathymetry/relief.html). The transect used for the vertical sections of the variables measured during the cruises is indicated with a continuous black line. Vertical profiles for long-term average (b) temperature ^(oC), (c) salinity, (d) dissolved oxygen (mL L^-1), and (e) chlorophyll a (mg m^-3); the dashed line indicates the change in transect direction at station 120.30. The distance (km) refers to the distance between stations 113.35 and 120.40. 

According to long-term data available for the CCS, the region off the Baja California Peninsula has recently been affected by diverse climatic and oceanographic events, especially during the period from 1997 to 2012. The most notable events because of their magnitude and effects on the pelagic ecosystem have been the 1997-1998 El Niño and the 1998-1999 La Niña (^{Lynn et al. 1998}; ^{Hayward et al. 1999}; ^{Durazo and Baumgartner 2002}; ^{Lavaniegos et al. 2002}, ²⁰⁰³). From 2002 to 2006, an anomalous intrusion of a large volume of subarctic water affected the epipelagic ecosystem of the CCS off the west coast of the peninsula (^{Venrick et al. 2003}; ^{Durazo et al. 2005}; ^{Gaxiola-Castro et al. 2008}, ^2010b), causing changes in phytoplankton biomass and production (^{Herrera-Cervantes et al. 2014}, ^{Espinosa-Carreón et al. 2015}) and in zooplankton abundance (^{Lavaniegos 2014}, ^{Lavaniegos et al. 2015}). Other interannual events that have had a more minor impact are the moderately strong El Niño events of 2002-2003 (^{Venrick et al. 2003}) and 2009-2010 (^{Bjorkstedt et al. 2010}), and less intense La Niña events mainly during 2007-2009 (^{McClatchie et al. 2009}) and 2010-2011 (^{Bjorkstedt et al. 2011}). While information exists on the effects of these large-scale events on the CCS, and especially the region off Baja California covered by the IMECOCAL (Spanish acronym for Mexican Research of the California Current) program, the spatial and temporal effects on the hydrography and phytoplankton biomass within SVB have not been specifically examined.

In this study we evaluate the effects of the interannual oceanographic variability observed in the southern region of the California Current (CC) during the period from 1997 to 2012 on some environmental variables and the phytoplankton biomass in SVB, in order to better understand the regional oceanography and assess the effects on phytoplankton production.

Materials and methods

Results

Based on a north-south transect of hydrographic stations of the IMECOCAL grid in the central part of SVB (Fig. 1a), vertical sections were elaborated with the time-series average of the variables measured in the period 1998-2012. Temperature showed a steep vertical gradient (thermocline) between 20 and 50 m depth (Fig. 1). Surface temperature values were highest (17.5 ^oC) towards the central-southern part of the bay as a result of the water residence time associated with the predominantly southward circulation. Salinity values were homogeneous in the upper 100 m of the water column (~33.5), increasing below this depth to 34.2 at 200 m (Fig. 1c). On average, there was a difference of approximately 70 m between the position of the thermocline (shallowest) and the halocline (deepest). Water from SVB showed similar characteristicas to water transported by the CC, with more changes in temperature than in salinity. Dissolved oxygen values were high (>5.0 mL L^-1) in the upper 50 m (Fig. 1d) and phytoplankton biomass was >1.0 mg m^-3 (Fig. 1e).

Particularly conspicuous in the time series (1997-2012) of the mean values of the variables measured at 10 m depth at the IMECOCAL stations are the high temperature (~25 ^oC) and salinity (~34.4) values in October 1997 and January 1998 (Fig. 2a, b), during the intense 1997-1998 El Niño event (http://www.ggweather.com/enso/oni.htm). Subsequently, the moderate 1998-2000 La Niña event caused temperature to decrease abruptly by 10^oC and salinity by 0.8 (http://www.ggweather.com/enso/oni.htm). The phytoplankton chlorophyll a values were close to the average (1.2 mg m^-3) during El Niño but increased to 3.5 mg m^-3 during La Niña (Fig. 2c). Both physical variables decreased over the 14-year period, temperature by 4 ^oC and salinity by 0.4, whereas chlorophyll did not show the same trend (Fig. 2c). From the beginning of 2003 to the end of 2006, average salinity decreased (~0.5) but temperature was apparently not affected (Fig. 2 a, b). This decrease in salinity coincided with the lowest chlorophyll concentration of all the time series (Fig. 2c), which continued until August 2007. The highest mean temperature and salinity values were recorded at the end of 1997 and beginning of 1998, and the low salinity and chlorophyll values showed a 4-year sequence (2003-2006).

Figure 2 Time series of mean temperature (a), salinity (b), and chlorophyll a (c) values at 10 m depth for Sebastián Vizcaíno Bay derived from IMECOCAL data. The bars represent the standard deviation of the mean. 

The satellite-derived SST climatology for 1997-2012 showed a marked seasonal sequence, with lower values from December to May/June (Fig. 3). SST was generally <16 ^oC from February to May due to the influence of cold water derived from coastal upwelling in spring and summer and still evident in June and July in the central bay (Fig. 3 f, g). On average, SST was >20 ^oC in August, September, and October (Fig. 3 h-j). From May to November, the north-south spatial gradient intensified, warmer water occurring in the southern part of the bay. The climatology showed a moderate signal of warm surface water that entered by the southern mouth between July and November, which was not very extensive.

Figure 3 Sea surface temperature (SST, ^oC) climatology (1997-2012) constructed from remote sensing data. 

The satellite-derived chlorophyll climatology showed, more clearly than SST, the influence of upwelled water in the bay, with higher values from March to June (>5 mg m^-3) along the northeastern coast (Fig. 4c-f). From August to January the chlorophyll values were very low (~0.3 mg m^-3), and this period could be characterized as oligotrophic. Unlike SST, the NE-SW gradient was not evident for chlorophyll, since the influence of upwelled water advected southwards along the coast is more apparent. Chlorophyll concentrations are highest in the bay in spring and summer, associated with the intensification of the equatorward flow of the CC and with the coastal upwelling that typically occurs during this period off the west coast of the northern and central regions of the Baja California Peninsula.

Figure 4 Chlorophyll (CHL, mg m^-3) climatology (1997-2012) constructed from remote sensing data. 

Based on MEI, at least 4 El Niño events occurred in the Pacific Ocean during the period from 1997 to 2012, but the most dominant in terms of duration and magnitude was the 1997-1998 event (Fig. 5a). With regard to La Niña, the 1998-2000 event and the moderate 2007-2008 and 2010-2011 events were identified in the subtropical Pacific region (Fig. 5a) (http://www.ggweather.com/enso/oni.htm). The 1997-2012 time series of monthly mean SST anomalies showed positive values greater than 0.5 ^oC in several years, the most prominent being the values of ~3.7^o C in 1997-1998 (Fig. 5b); the 1997-1998 El Niño event has been identified as one of the strongest, similar to that of 1982-1983. The ADT anomalies showed a similar temporal trend to that of SST, the highest positive value (~20 cm) occurring at the end of 1997 and beginning of 1998 (Fig. 5c). The effects derived from the weak and moderate El Niño events of 2006-2007 and 2010 were lower (Fig. 5c), but with positive values (~5 cm). Except for some negative chlorophyll anomalies mainly during 1998, 2006-2007, and 2009-2010 (Fig. 5d), the weak and moderate El Niño events did not greatly affect the phytoplankton biomass near the surface. The satellite-derived chlorophyll time series revealed high positive anomalies in 2002 and 2003, and to a lesser extent in 2011 and 2012 (Fig. 5d), without any direct relation to the ENSO cycle. The SST and ADT series revealed that 2 events clearly impacted SBV: the 1997-1998 El Niño (high positive anomalies) and the 2010-2012 La Niña (negative anomalies).

Figure 5 Time series of the Multivariate ENSO Index (MEI) (a) and of the monthly sea surface temperature (SST) (b), absolute dynamic topography (ADT) (c), and chlorophyll (CHL) (d) anomalies derived from remote sensing data. Positive anomalies = El Niño; negative anomalies = La Niña.  

During the 1998 El Niño event (Fig. 6a), there was a layer (60 m) of homogeneous temperature (>18 ^oC), the thermocline sank 70 m, and temperature increased ~6 ^oC in the upper 100 m relative to the time-series average (1998-2012). While the vertical position of the halocline was similar to the average, salinity increased by ~0.9 in the upper 100 m (Fig. 6b) but below this depth there was no apparent change. The chlorophyll concentrations in the upper 50 m were similar to the average, with a decrease of ~0.5 mg m^-3 in the area of the vertical gradient (Fig. 6c). During the moderate El Niño events of 2003 and 2010, the effects on the water-column structure were not as strong but still evident (sinking of the thermocline by ~40 m). The impact was greater on the 2010 chlorophyll concentration, which in turn was ~30% lower relative to the 1998 event (data not shown). The temperature composite for January 1998 showed surface values of 19.5-20.5 ^oC, the relatively warmer water occurring in the central-southern part (Fig. 6d). In the same month, sea level was >70 cm for all the area (Fig. 6e) due to surface heating, with an anomalous, high ADT value towards the shore that was not associated with temperature. The satellite-derived chlorophyll was on average <0.5 mg m^-3, with some values >2 mg m^-3 in the coastal zone (Fig. 6f).

Figure 6 The upper panels show vertical sections of the variables measured in January 1998 along the transect shown in Figure 1a (dashed line indicates the change in direction at station 120.30): temperature (a), salinity (b), and chlorophyll a (c). The lower panels show composite satellite images for January 1998: sea surface temperature (SST) (d), absolute dynamic topography (ADT) (e), and chlorophyll (CHL) (f). 

During the moderate 1999 La Niña event (http://www.ggweather.com/enso/oni.htm), the hydrographic variables and phytoplankton biomass in the bay were similar to the average (Fig. 7). In January 1999, water temperature was <15 oC and salinity was ~33.6 in the upper 50 m throughout the bay (Fig. 7a, b). Water temperature was ~2.5 oC below the time-series average, while salinity did not change considerably. The homogeneous temperature and salinity layer deepened, and the thermocline and halocline were situated at ~60 m depth. Though chlorophyll increased during the 1999 La Niña (Fig. 7c), on average it was not more than 0.5 mg m^-3. The conditions in the bay during the moderate 2011 La Niña were very similar to those of 1999, except for a more shallow position of the thermocline (~30 m), and lower average temperature (0.5 ^oC) and chlorophyll (~1.0 mg m^-3) in the upper 50 m (data not shown). The SST values derived from the composite image for January 1999 ranged from 15.5 to 16.5 ^oC, with water temperatures of <15.5 ^oC to the northwest of the coastal zone (Fig. 7d). The ADT ranged from 52 to 58 cm (Fig. 7e), the lower values occurring in the central part of the bay and not directly associated with SST. This variable was on average 20 cm lower than in January 1998 because of the decrease in temperature (~3 ^oC) during this period (1999) related to the intense coastal upwelling and La Niña events. Average chlorophyll was 1.0 mg m^-3 in the central part of the bay, and values were higher (~2 mg m^-3) to the north and south along the coast (Fig. 7f).

Figure 7 The upper panels show vertical sections of the variables measured in January 1999 along the transect shown in Figure 1a (the dashed line indicates the change in direction at station 120.30): temperature (a), salinity (b), and chlorophyll a (c). The lower panels show composite satellite images for January 1999: sea surface temperature (d), absolute dynamic topography (e), and chlorophyll (CHL) (f). 

Based on the information for February 2004, period when the lowest salinity values of the time series were observed (Fig. 2b), we characterized the effect of the anomalous intrusion of subarctic water into the bay (Fig. 8). Temperature in the upper 50 m was <16 ^oC (Fig. 8a), which can be considered average for winter in the region, and a well-developed thermocline was observed at ~50 m depth in the northern section. The inflow of "fresh" water occurred mainly through the nothern mouth, where salinity values (33.2-33.3) were lower (by 0.3-0.4) than the average for the bay, forming a homogeneous water column in regard to salinity in the upper 60 m (Fig. 8b). Because of this low-salinity condition, the concentrations of dissolved oxygen (~0.6 mL L^-1; Fig. 8c) and phytoplankton chlorophyll a (~1.0 mg m^-3; Fig. 8d) were lower than average. The inflow of surface water with lower temperature into the bay (Fig. 8e), associated with low ADT values (Fig. 8f), occurred only in one coastal section in the northern part of the bay as a result of weak upwelling off Punta Canoas, which generated average phytoplankton biomass concentrations of ~0.5 mg m^-3 (Fig. 8g). Average SST in the bay was 16 ^oC and sea level rise was between 52 and 54 cm (Fig. 8e, f); these values are similar to those obtained during the moderate 1999 La Niña.

Figure 8 The upper panels show the hydrographic conditions along the transect shown in Figure 1a during February 2004 (the dashed line indicates the change in direction at station 120.30): temperature ^(oC) (a), salinity (b), dissolved oxygen (mL L^-1) (c), and chlorophyll a (mg m^-3) (d). The lower panels show composite satellite images for February 2004: sea surface temperature (SST) (e), absolute dynamic topography (ADT) (f), and chlorophyll (CHL) (g). 

Discussion

The time-series (1998-2012) average values indicate that in the upper 60 m of the SVB water column conditions are temperate (15-17 ^oC), salinity is characteristic of CC water (33.5-33.7), dissolved oxygen content is high (>5.0 mL L^-1), and phytoplankton concentrations are high (>1.0 mg m^-3). These values are similar to those measured by the IMECOCAL program in coastal zones of the northwestern region of the Baja California Peninsula (^{Gaxiola-Castro et al. 2010b}). The bay is thus a healthy epipelagic ecosystem with open circulation and sufficient ventilation, and with suitable hydrographic conditions for the respiration/oxidation processes of the organisms. In general, it is an area of high biological productivity, which generates a mesotrophic environment in relation to the phytoplankton biomass and maintains the conditions necessary for the growth and development of the marine food web.

The time series of the variables measured at 10 m depth reveal the effects of the anomalous intrusion of subarctic water and of the ENSO events that impacted all the region off Baja California (^{Durazo and Baumgartner 2002}; ^{Durazo et al. 2005}; ^{Gaxiola-Castro et al. 2008}, ^2010a; ^{Herrera Cervantes et al. 2014}). El Niño events seem to have a greater effect on surface conditions than La Niña events given that temperate to cold conditions generally prevail in the bay because of the influence of CC water and upwelling of subsurface water in the northern coastal zone. The effects of the strong 1997-1998 El Niño on the physical variables are more evident, with an increase in both temperature (~8 oC) and salinity (~0.9). The anomalous occurrence of warm, more saline water close to the surface has also been observed outside the bay (IMECOCAL line 120) during this event, caused by the poleward advection of subtropical water (^{Durazo and Baumgartner 2002}). While El Niño has an evident effect on the physics of the bay, it does not seem to have a big impact on chlorophyll, most likely because of changes in the dominant phytoplankton groups and/or selective grazing by zooplankton. ^{Arroyo-Loranca et al. (2015)} reported a decrease in satellite-derived chlorophyll off Punta Eugenia (immediately to the south of SVB) during the 1998 El Niño event. During this El Niño, in SVB ^{Lavaniegos et al. (2003)} observed high richness of phytoplankton groups other than diatoms, such as armored dinoflagellates, cryptomonads, and nanoflagellates.

As a result, the biomass may not undergo notable changes, but changes may occur in the composition of the plankton groups (phytoplankton and zooplankton size, functional groups, etc.) that could affect the food web. ^{Kahru and Mitchell (2000)} hypothesized that the increase in satellitederived chlorophyll in the oceanic zone off SVB during the 1997-1998 El Niño was the result of an increase in nitrogenfixing cyanobacteria.

The climatology obtained based on remote sensing data for the study period shows that SVB presents high seasonal variability, with marked differences in surface temperature and chlorophyll. This variability is mainly associated with changes in the flow of the CC (^{Durazo 2009}, ²⁰¹⁵) and with coastal upwelling events that are more intense in spring and summer (^{Palacios-Hernández et al. 1996}). The regional wind conditions change in summer and autumn (^{Castro and Martínez 2010}), modifying the equatorward transport of water and the coastal upwelling pattern. This affects SVB as surface temperature increases and chlorophyll concentration decreases because of greater stratification in the euphotic zone. In the region outside the bay, the flow is predominantly poleward in late summer and autumn (^{Durazo 2015}, ^{Zaitsev et al. 2014}), and there is limited inflow of warm water near the surface via the southern mouth. The seasonal and interannual effect on chlorophyll is also evident off Punta Eugenia, the concentrations being higher (>5 mg m^-3) from March to August and lower (~1.2 mg m^-3) from September to February (^{Arroyo-Loranca et al. 2015}).

Given that it is located in an oceanographic transition zone between temperate conditions, influenced by the equatorward flow of the CC in spring and summer, and subtropical conditions, influenced by the poleward transport of coastal water in late summer and autumn, SVB is affected by large-scale tropical events such as El Niño and by events that originate in the subpolar region of the Pacific. The 1997-1998 El Niño primarily impacted the hydrographic variables of the bay, but did not have a strong effect on phytoplankton chlorophyll. During La Niña events, however, none of the variables were strongly affected, except for chlorophyll that increased as a result of the intensification of coastal upwelling along the northern coastal zone. Nonetheless, neither the El Niño nor the La Niña events significantly affected the satellite-derived chlorophyll near the surface. Phytoplankton biomass does not change substantially in the bay during El Niño events because of local dynamic processes and/or because of the diverse response of the epipelagic ecosystem to other processes such as the remineralization of organic matter and the dominance of other phytoplankton and zooplankton groups. For example, the 1997-1998 El Niño had a greater effect on the physical variables than on chlorophyll, most likely because the most important changes in the biological aspects were related to the abundance of the phytoplankton species present in the epipelagic zone and to selective grazing by zooplankton.

^{Durazo and Baumgartner (2002)} identified the presence of Subtropical Subsurface Water in the exterior part of SVB during the 1997-1998 El Niño. In the present study, however, we did not identify this water inside the bay during the same period. According to the temperature-salinity relationship obtained with all the SVB data from the 1997-2012 IMECOCAL cruises, salinity was always <34.5 (data not shown), which corresponds to salinity associated with modified subarctic water (^{Durazo and Baumgartner 2002}, ^{Durazo et al. 2010}). According to ^{Zaitsev et al. (2014)}, to identify the presence of Subtropical Subsurface Water in this region, salinity values must be greater than 34.7, but there was no evidence of this water during the 1998, 2003, and 2010 El Niño events. Apparently, the predominant surface circulation in the northern part of the bay and the shallower depth at the southern mouth hinder the inflow of saltier subsurface water, both in late summer and autumn (after the upwelling season) and during El Niño events when there is increased poleward flow.

The intrusion of subarctic water was a large-scale event apparently not directly related to the ENSO cycle. In the CCS, this event was more dominant than the moderate 2003 El Niño, which began to decline during the first months of that year (^{Venrick et al. 2003}). The anomalous intrusion of subarctic water in the CCS was first observed in July 2002 off the coast of Oregon (^{Freeland et al. 2003}) and was still evident until 2004-2005 off California (^{Goericke et al. 2004}, ²⁰⁰⁵) and Baja California (^{Durazo et al. 2005}; ^{Gaxiola-Castro et al. 2008}, ^2010b; ^{Herrera-Cervantes et al. 2014}).

The inflow and permanence over several years (2003-2006) of less saline water (Fig. 2b) had strong repercussions on SVB. Salinity decreased, the halocline (nutricline) sinking to more than 80 m depth or to where the bottom permitted (Fig. 8b). The bay responded with low dissolved oxygen (~4.4 mL L^-1) and chlorophyll (0.3 mg m^-3) values, which may indicate high oxygen consumption associated with respiration (oxidation) and/or decreased biological production due to the sinking of the thermocline. ^{Gaxiola-Castro et al. (2008}, ^2010b) reported high positive macrozooplankton volume anomalies in the IMECOCAL region, asociated with high negative anomalies of integrated water-column chlorophyll levels. These authors associated the decline in phytoplankton biomass with zooplankton grazing and with strong stratification due to the large amount of low-density water in the upper 100 m that prevented vertical mixing and nutrient input to the euphotic zone. During this period, the IMECOCAL region was associated with positive anomalies of the main zooplankton groups, such as crustaceans, tunicates, and carnivores (^{Lavaniegos et al. 2015}), and thus with low phytoplankton biomass. During the anomalous intrusion of subarctic water, mean water-column chlorophyll concentration in SVB was 30% lower than that measured during the 1997-1998 El Niño, when the halocline structure was similar but with high salinity values. This caused a very different phytoplankton biomass response, also related to the zooplankton groups since there was a high abundance of salps (33.3 ind m^-3) in the bay during this period (^{Lavaniegos et al. 2015}).