Chlorophyll-a thin layers in the Magellan fjord system: The role of the water column stratification

Continental Shelf Research 124 (2016) 1–12

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Chlorophyll-a thin layers in the Magellan fjord system: The role of the water column stratification Francisco Ríos a,n, Rolf Kilian a,b, Erika Mutschke b a b

University of Trier, Germany University of Magallanes, Chile

art ic l e i nf o

a b s t r a c t

Article history: Received 10 June 2015 Received in revised form 12 April 2016 Accepted 13 April 2016 Available online 10 May 2016

Fjord systems represent hotspots of primary productivity and organic carbon burial. However, the factors which control the primary production in mid-latitude fjords are poorly understood. In this context, results from the first fine-scale measurements of bio-oceanographic features in the water column of fjords associated with the Strait of Magellan are presented. A submersible fluorescence probe (FP) was used to measure the Chlorophyll-a (Chl-a) concentration in situ, along with conductivity, temperature, hydrostatic pressure (depth) and dissolved oxygen (CTD-O2) of the water column. The Austral spring results of 14 FP-CTD-O2 profiles were used to define the vertical and horizontal patches of the fluorescent pigment distribution and their spatial relations with respect to the observed hydrographic features. Three zones with distinct water structures were defined. In all zones, the ‘brown’ spectral group (diatoms and dinoflagellates) predominated accounting for 480 wt% of the phytoplankton community. Thin layers with high Chl-a concentration were detected in 50% of the profiles. These layers harbored a substantial amount (30–65 wt%) of the phytoplankton biomass. Stratification was positively correlated to the occurrence of Chl-a thin layers. In stable and highly stratified water columns the integrated Chl-a concentration was higher and frequently located within thin layers whereas well mixed water columns displayed lower values and more homogeneous vertical distribution of Chl-a. These results indicate that mixing/stability processes are important factors accounting to the vertical distribution of Chl-a in Magellan fjords. & 2016 Elsevier Ltd. All rights reserved.

Keywords: Chlorophyll-a Thin-layers Stratification Spectrofluorometer Fjord Patagonia

1. Introduction The superhumid continental margin of the southern Patagonian Andes is located within the current core of the southern westerly wind belt (SWW). Intensity and latitudinal changes of the SWW are associated with the climate conditions, characterized by high precipitations (Garreaud et al., 2013; Lamy et al., 2001; Varma et al., 2012), extreme high freshwater addition to the fjord system (Kilian et al., 2013), and strong salinity gradients on the coastal zone (Dávila et al., 2002). Consequently, the high freshwater runoff is accompanied by high rates of terrestrial nutrient input, particularly dissolved silica (Torres et al., 2011, 2014) and organic terrestrial carbon (Vargas et al., 2011) that often incorporates essential micronutrient ions (e.g., Fe, Zn, Cu, Mn; Iriarte et al., 2014a; n Correspondence to: Lehrstuhl für Geologie, Fachbereich Geographie/ Geowissenschaften (FB VI), Campus II, University of Trier, Behringstrasse 21, 54286 Trier, Germany. E-mail addresses: [email protected] (F. Ríos), [email protected] (R. Kilian), [email protected] (E. Mutschke).

http://dx.doi.org/10.1016/j.csr.2016.04.011 0278-4343/& 2016 Elsevier Ltd. All rights reserved.

Muller et al., 2005). In addition, marine nutrients are provided by the advection of oceanic waters, which enter the fjord system as bottom water (Antezana and Hamamé, 1999) and lead to high primary productivity in some areas of the aquatic system (Iriarte et al., 2007). In recent years, efforts have been made to understand better the biogeochemical processes bound to the vertical water structure at different spatial scales (Iriarte et al., 2014b and references therein). However, information about fine-scale structures that indicates the scale of biological variability at the level of the primary producers is still missing. The term ‘thin layer’ is used to describe highly-concentrated patches of organisms, or particles, that have vertical extents on the order of centimeters to a few meters, yet can extend horizontally for many kilometers and persist for hours to weeks (Sullivan et al., 2010a). Specifically, these fine-scale biological structures can harbor an important fraction of the primary producers within small depth intervals (Durham and Stocker, 2012). Such narrow and highly-concentrated patches of phytoplankton are a common feature in several coastal marine environments of the Northeast Pacific (Alldredge et al.,

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2002; Benoit-Bird et al., 2009; Cowles et al., 1998; Strickland, 1968), Northwest Pacific (Clayton et al., 2014), Northeast Atlantic (Churnside and Donaghay, 2009; Farrell et al., 2014; Lunven et al., 2005; O’Boyle and McDermott, 2014; Velo-Suárez et al., 2008), Northwest Atlantic (Shroyer et al., 2014), North Sea (Nielsen et al., 1990; Pedersen, 1994) and Baltic Sea (Möller et al., 2012). Fjords systems have been underestimated on the organic carbon burial budget (Smith et al., 2015) and such underestimations can be of constraint when trying to improve estimates of paleoprimary production from sediments of the Patagonian fjords. These estimations use proxies that are affected by Glacial-Holocene coastlines changes, the timing of marine transgression into the proglacial lakes and the structure of the water column (Kilian et al., 2007a, 2007b). In the Strait of Magellan and the associated fjord system, the peak of primary productivity is primarily related to seasonal blooms of diatoms and to lesser extent of dinoflagellates (Alvesde-Souza et al., 2008; Hamamé and Antezana, 1999; Iriarte et al., 2001; Pizarro et al., 2005; Uribe and Ruiz, 2001). Consequently, silica-frustule plankton plays a leading role in the entire circulation of nutrients, affecting atmospheric exchange and burial rates (Aracena et al., 2011; Treguer and Pondaven, 2000). The time-dependent stability or mixing of the water column, which affects the nutrient availability and the buoyancy of non-motile plankton, could impose an external physical influence on the primary productivity and associated phytoplankton assemblages (Saggiomo et al., 2011). Spatial and temporal variability of Chlorophyll-a (Chl-a) concentration provides global primary productivity estimates (Papageorgiou and Govindjee, 2004). The use of satellite measurements has largely contributed to model the global net of primary production in open oceans (Antoine et al., 1996; Behrenfeld and Falkowski, 1997; Lee et al., 2015; Platt and Sathyendranath, 1988). However, ocean color satellite data require in situ information to yield better estimates in turbid coastal areas (Longhurst et al., 1995) or coastal upwelling systems (Williamson et al., 2015) and to extend the open-ocean relationships between the surface measurements of Chl-a and depth-integrated Chl-a predictions into coastal ecosystems (Frolov et al., 2012). In situ fluorometry measures Chl-a concentrations which can be used to determine the biomass of phytoplankton assemblages (Falkowski and Kiefer, 1985), within critical vertical scales that indicate the fine-scale structures. By using variable light-emitting diodes (LEDs) emission spectra, in situ fluorometers can be also used to taxonomically discriminate bulk fluorescence properties (Beutler et al., 2002). This study examines the vertical and horizontal Chl-a distribution within the water column and its relations to the hydrographic features. The results from fluorescence measurements and CTD-O2 profiles provide an outline of phytoplankton patchiness in the Strait of Magellan and an assessment of the environmental conditions that are favorable to the occurrence of strong vertical and horizontal Chl-a gradients.

2. Materials and method The study area includes the western sector of the Strait of Magellan between 52° and 53°S and the closer associated fjord system, namely Beaufort Bay, Glacier Sound, Jerónimo Channel and Otway Sound, a semi enclosed basin at the Eastern side of the super-humid climate divide of the Andes (Kilian et al., 2007a) and characterized by high Chl-a concentration (Pizarro et al., 2005). The eastward influence of Pacific waters reaches Carlos III Island, where a narrow constriction and a shallow sill are placed (Panella et al., 1991). Eastward form this island, it is denoted the influence of the Atlantic waters (Antezana, 1999; Valdenegro and Silva,

Fig. 1. a) Location of the sampling stations and profiles. (1) Los Glaciares, (2) Glacier, (3) Pan de Azúcar, (4) Nolasco, (5) Tamar, (6) Santa Ana, (7) Shelter, (8) Santa Inés, (9) Spider, (10) Crosside, (11) York, (12) Cutter, (13) Hammond and (14) Zorrilla. Inset showing the location of the study area. b) Salinity, temperature and Chl-a concentration profiles. Three sectors can be distinguished; the first zone nearby the Gran Campo Nevado Ice Field (GCN; Fig. 1(a)), from Los Glaciares to Santa Ana station, shows the transition between the highly glacial influence sector to the more marine environment; the second zone, from Shelter to York station, represent the Pacific domain of the Strait of Magellan (Paso Largo), where the Atlantic Ocean influence could be observed at the York station, near to the Carlos III Island. The third zone is defined by Otway Sound domain, which include the Jerónimo Channel, and is represented by Cutter, Hammond and Zorrilla stations.

2003; Fig. 1(a) and (b)). The west flank of the Patagonian Andes ecosystem is largely affected by the variability of the SWW. This shows a strong correlation between the precipitation rates (Garreaud et al., 2013), the westward transport of glacial clay plumes (Breuer et al., 2013; Kilian et al., 2007a, 2013) and the offshore movement of the fjord water outflow (Dávila et al., 2002). Furthermore, fjord currents depending on the wind distribution and intensity, as well as tidal currents and the particular bathymetry, control the water exchanges between the marine and freshwater and the depth of the brackish layer (Valdenegro and Silva, 2003; Valle-Levinson and Blanco, 2004). These conditions are particularly important at the Glacier Bay, an up to 200 m deep semi-enclosed bay with a o25 m deep sill toward its mouth (Kilian et al., 2007a). The relatively warm coastal water, from the southward migrating Cape Horn Current (Strub et al., 1998), enters in the fjord system as a saline bottom water (salinity 430 psu) below the pronounced superficial brackish layer (salinity .5–30 psu). It is

F. Ríos et al. / Continental Shelf Research 124 (2016) 1–12

derived from the mixing with the freshwater input from the high precipitation rate ( 410,000 mm yr
1; Schneider et al., 2003), coastal runoff and melting ice (Dávila et al., 2002). The 20–30 m thick surface brackish water layer (Acha et al., 2004) is relatively cold during the summer and spring. It shows slightly lower salinity during the summer compared to winter season; however, a yearround low salinity surface water anomaly has been described for this area (Kilian et al., 2007a, 2013). The thickness of this layer has been related to the amount of freshwater input from river and glacial discharges from the ice caps (Calvete and Sobarzo, 2011). During the 2012 Austral spring Cruise of the R/V Gran Campo II (28 September–04 October), were carried out 14 profiles of Chl-a concentration, temperature (T), conductivity-salinity (S) and oxygen content (O2) of the water column. The fluorescence spectra of the algae populations were measured in situ using a submersible spectrofluorometer (FuoroProbe II, bbe-Moldaenke, Kiel, Germany). This allows a fast deployment and estimation of the phytoplankton biomass (expressed in mg l
1 of Chl-a) and their spectral group compositions. The FluoroProbe (FP) contains five LEDs that emit pulsed light at selected wavelengths (450, 525, 570, 590, and 610 nm) for the excitation of the pigments present in the phytoplankton, and a 370 nm LED to measures fluorescing substances that are not algae (i.e., ‘yellow substances’) and to correct Chl-a estimates. Emission is measured at 685 nm by a photomultiplier at an angle of 90 degrees to the exciting light source. According to the excitation spectra resulting from the composition of their peripheral antenna, the device enables the discrimination of four spectral algal groups. In the ‘green’ group (Chlorophyta) the peripheral antenna contains Chl-a, Chl-b and xanthophyll. In the ‘blue’ group (Cyanobacteria) phycobilisomes function as peripheral antennae (mainly phycocyanin). The members of the ‘brown’ group (Bacillariophyceae and Dinophyceae) contain Chl-a, Chl-c and xanthophyll (often fucoxanthin or peridinin). Whereby it should be noted that ‘brown’ does not mean Phaeophyta. The ‘red’ group (Cryptophyta) has a combination of Chl-a and Chl-c with one phycobiliprotein that can be either phycoerythrin or phycocyanin. Here, just the phycoerythrin-containing members of the ‘red’ group are considered (Beutler et al., 2002). The excitation spectrum obtained is compared to the calibration data (norm curves or ‘fingerprints’) stored in the probe and the amount of individual groups is calculated. Essentially, fluorometer's calibration relies on Chl-a solutions or on phytoplankton cultures. However, for the Magellan region, there is no reliable data set to calibrate the measurements of Chl-a concentration. Thus, the spectral ranges setup on the instrument must be used by default. This does not dismiss a future recalibration to confirm or adjust in situ concentrations through calibration with natural samples. The bbe-FluoroProbe software estimates the best sum of the four theoretic components (i. e., the four specific excitation norm spectra corresponding to each of the four algal groups) from the measured fluorescence signal by curve fitting and estimates the Chl-a concentration corresponding to each algal group (Catherine et al., 2012). The presence of high Chl-a concentration in a restricted depth range corresponds to fine-scale planktonic structures (Strickland, 1968). Following Dekshenieks et al. (2001), such thin layers were identified by using three criteria: (i) the feature must be present in two or more subsequent profiles; (ii) It must be o5 m thick. The thickness must have been measured where the Chl-a concentration was half of the maximum concentration; (iii) Chl-a concentration must be higher than the profile average (Chl-aav) plus one standard deviation (Chl-astd), both calculated within the depth range where the Chl-a concentration was 40 mg l
1. Subsequently, the integrated Chl-a concentration of the thin layers was calculated using the area under the curve where Chl-a 4 Chl-aav þ

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Chl-astd. To evaluate the hydrography of the water column, CTD-O2 measurements were performed with the CTD-SD204 (SAIV A/S Environmental Sensors and System) at the stations shown in Fig. 1. The profiles and sections data correspond to the downward cast from the first meter of depth. The data set was regularly interpolated to obtain a consistent data set of .5 m depth bins, according to average resolution of the CTD-O2 and the FP casts. Density anomalies (sigma-t) were computed with the Gibbs-SeaWater (GSW) Oceanographic Toolbox for Matlab (McDougall and Barker, 2011). Sigma-t was used to calculate the vertical gradient of the density. Buoyancy frequency (N2) calculations and interpolation of the profiles into sections were carried out using Ocean Data View 4 software, and the DIVA gridding routines (Schlitzer, 2014). Statistical correlations between buoyancy frequency and Chl-a concentration were performed using the Curve Fitting Tool of Matlab. We used a quadratic polynomial curve because the biooceanographic data included all the distribution range of the phytoplankton.

3. Results In situ measurements with the FP revealed the vertical patterns of the Chl-a concentration and their association to salinity, temperature and dissolved oxygen concentration within the water column. High Chl-a concentrations were measured only in a restricted range of absolute salinity (SA from 23 to 31 g kg
1) and conservative temperature (Θ from 3.3 to 6.8 °C; Fig. 2). This range was narrower for the patches of high Chl-a concentration dominated by ‘brown’ group algae (25–29 g kg
1; 3.9–6.7 °C; Fig. 3). Moreover, it was possible to distinguish three different oceanographic zones with distinctive water structures and Chl-a vertical distribution (Fig. 1(b)). The first zone denoted a high influence of fresh water input, originated from the glaciated area of the Gran Campo Nevado (GCN), through the Glacier Sound and the Xaultegua Gulf. The second zone, in the Paso Largo sector of the Strait of Magellan, displayed a more heterogeneous hydrology, related to the effluence of the diverse channels and sounds and the

Fig. 2. Conservative temperature (Θ) – Absolute Salinity (SA) diagram, showing the concentration of Chl-a for the water profiles. The Chl-a concentration over 30 g kg
1 correspond to the ‘blue’ group at the Shelter station (Fig. 3(7)). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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Fig. 3. Salinity (red), temperature (blue), dissolved oxygen (green) and Chl-a concentration (black) profiles. Colored areas represent the concentration of the different groups of fluorescent particles determined by the FP. Yellow substances are not including for the total Chl-a concentration. Note: the scales are equal within zones, except for salinity scale at Los Glaciares and Glacier stations and the temperature at Los Glaciares station. Oxygen concentration at Shelter and Santa Inés stations also display different scale. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

F. Ríos et al. / Continental Shelf Research 124 (2016) 1–12

thermohaline front near the Carlos III Island (Fig. 1(a) and (b)). The last zone was located in the Otway Sound domain, which is connected with the Strait of Magellan through the Jerónimo Channel. The Otway Sound was characterized by high Chl-a concentration. In this study, it displayed both maximum Chl-a concentration and integrated Chl-a concentration (Fig. 5(c)). 3.1. Glacier-Beaufort zone The Glacier-Beaufort zone exposes the transition between the water structure from a highly glacial influenced fjord system and the occidental sector of the Strait of Magellan, with more open marine characteristics. The transect starts in the Glacier Bay that has frequent drift ice derived from the Gran Campo Nevado (GCN) ice field. The transect ends at the mouth of the Xaultegua Gulf, which is connected to the Skyring Sound through the Gajardo Channel (Fig. 1(a)). 3.1.1. Profiles description and thin layers The vertical distribution of the Chl-a showed a close relation to the termohalocline position. The stations Los Glaciares, Glacier and Pan de Azúcar displayed the maximum Chl-a concentration just over the halocline and below the inverted thermocline, which started from the water surface. Above the termohalocline (o 2–

Fig. 4. The histograms show the integrated concentration of the fluorescent pigments. Black dots indicate the total integrated Chl-a concentration for phytoplankton spectral groups. The pie charts show the percentage in weight of each phytoplankton spectral group for the three zones.

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5 m water depth) the water did not contain fluorescence particles. These stations were characterized by relatively low salinities (o24 psu) and higher temperatures (4–6.5 °C) (Fig. 3(1), (2) and (3)). At the other stations (Nolasco, Tamar and Santa Ana), the surface-warmed layer showed a higher salinity (425 psu) and a lower Chl-a concentration (2–5 mg l
1). Nevertheless, the maximum Chl-a concentration appeared close to the base of the inverted thermocline and the halocline (Fig. 3(4), (5) and (6)). The maximum Chl-a concentration range was 7.7–27.6 mg l
1 and occurred within a depth range from 6.5 to 10.5 m (Figs. 1(b) and 5 (a)). The spectral group differentiation showed the predominance of the ‘brown’ group (82 wt%) followed by ‘green’ (16 wt%) and ‘red’ groups (2 wt%) (Fig. 4(a)). The presence of the last two groups was related to the narrow high Chl-a concentration layer. The yellow substances were mostly distributed on the superficial waters, with concentrations o2 mg l
1. The dissolved oxygen showed the highest concentration in a depth range from 8 to 12 m. This depth range is similar to the high Chl-a concentration layer (Fig. 5(a)). The Nolasco station showed a relatively homogeneous vertical distribution of the Chl-a. Hence, it did not include all conditions to define a thin layer. All remaining stations showed a thin layer structure in a water depth range of 6.5–10.5 m. The width of the thin layers was 2–4.7 m. The contribution of the thin layers to the total integrated Chl-a concentration was 31–65 wt%. Integrated values of Chl-a concentration reached an average of 72 mg m
2. 3.1.2. Water structure and fluorescence particles distribution In the Glacier-Beaufort zone, the fluorescent pigments were mostly concentrated in the subsurface layer between 5 and 15 m water depth. Despite of the local variability in the vertical patterns of the Chl-a distribution, the higher concentrations were restricted to a narrow layer at o4.7 m water depth, limited by a strong vertical gradient of the water density (Fig. 5(a)). The high Chl-a concentration patch was observed along the coast towards the Strait of Magellan for over 80 km (Fig. 1(a) and (b)) and the minimum temporal persistence was four days (28 Sep.–1 Oct.). The dissolved oxygen section showed the effect of the relatively cold and low-oxygen freshwater input of the runoff from Glacier Sound (Fig. 1(a)). The higher concentrations were observed in the subsurface, below the seasonally warmed top layer, probably derived from the photosynthetic activity within the high Chl-a concentration layer. Oxygen and Chl-a vertical distributions showed a notable spatial similarity within the water column (Fig. 5 (a)). At the most wind-exposed station -Nolasco- the unstable layer was deeper (  10 m depth) and the dissolved oxygen was relatively lower than in the stations with more stable conditions of the water column (Fig. 5(a)). The unstable conditions were denoted by the negative values of the buoyancy frequency (Fig. 6). From Los Glaciares to Pan de Azúcar stations, the variations of sigma-t typified the transition between the head and mouth of a high-runoff fjord. The stations closer to the Strait of Magellan -Nolasco, Tamar and Santa Inés- displayed relatively higher surface salinities and subsequently higher density values. This reflected more oceanic influence to the detriment of glacier influence nearby the Strait of Magellan. The horizontal and vertical distributions of the different layers were defined by strong vertical gradients of sigma-t (Fig. 5(a)) and derived buoyancy frequencies (Fig. 6). Excluding the Nolasco station, the buoyancy frequency showed a significant correlation to the Chl-a concentration (R-square ¼ 0.2936), which displayed the higher concentrations within the intermediate layer restricted by strong pycnoclines (Figs. 5(a) and 6).

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Fig. 5. Vertical distribution of Chl-a, dissolved Oxygen (O2), Sigma-t (st) and vertical gradient of st. a) Glacier-Beaufort zone. b) Paso Largo zone. c) Otway Sound zone.

F. Ríos et al. / Continental Shelf Research 124 (2016) 1–12

Fig. 6. Buoyancy frequencies (colored scale) and Chl-a concentrations (mg l
1) contours (black lines) for the study area. Dashed line limits negative values zones of the buoyancy frequency. For the station names see Fig. 1(b).

3.2. Paso Largo zone The Paso Largo zone is located in the Strait of Magellan, between the Abra Channel and the Carlos III Island. The main fresh water input comes from the Santa Inés Island, through small sounds and river discharges. The five stations of this transect were characterized by the influence of the oceanic waters that enter from the Pacific Ocean in the Strait of Magellan until the Carlos III Island. Nearby this island, the abrupt density change (York station, Fig. 1(a), (b)) denoted the localization of the oceanic front between the Pacific (westward) and Atlantic Oceans (eastward). 3.2.1. Profiles description and thin layers The Chl-a concentration showed relatively low values, except for the high concentration layer at the Shelter station. This fluorescence-rich layer was related to a strong thermohalocline at 40 m depth (Fig. 3(7)). In this layer, the phytoplankton spectral groups were exclusively ‘green’ and ‘blue’, which contributed to the overall phytoplankton fluorescent pigments with the 10 wt% and 7 wt% respectively. At all other stations, ‘brown’ algae were the exclusive spectral group, accounting 82 wt% for the whole transect. The ‘brown’ algae were distributed in a relatively wide depth ranges, from the surface to a maximum depth of 54 m (Spider station), without high-concentration layers (Fig. 3(7)–(11)). Therefore, thin layers were not described in this zone. The yellow substances showed comparatively higher concentration values at the Santa Inés, Crosside and York stations. They represented more than the half of the fluorescence pigments detected in the water column (Fig. 4(b)). The dissolved oxygen displayed different patterns, however, values were lower at the surface ( o8.5 mg l
1). They increased downward, steadily at Shelter station and abruptly at Santa Inés station. The latter station exhibited a relative maximum of oxygen, which coincided with a shallowest thermocline (Fig. 3(8)). The remaining stations showed a decreasing general trend below the subsurface maximum (Fig. 3(9)–(11)). 3.2.2. Water structure and fluorescence particles distribution The vertical distribution of the fluorescence particles exhibited a large variation among the stations. While the Shelter station showed the deepest conspicuous maximum of Chl-a concentration, the York station displayed the absolute minimum of Chl-a concentration (Fig. 3(11)). Although the high relative values of Chla concentration were not randomly distributed and they presented a spatial relationship to particular density conditions in the water column (Fig. 5(b)), the Chl-a concentration did not show a correlation to the buoyancy frequencies (R-square ¼0.0192). The dissolved oxygen also did not show a vertical stratification structure. Only the most superficial layer (o 3 m depth) displayed lower oxygen content. However, a horizontal change in oxygen

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distribution was clearly observable from the Pacific to the Atlantic domain, which exhibited the lowest concentrations (Fig. 5(b)). The western sector was characterized by the influence of waters from the Pacific Ocean, which formed a dense underlying water column below 40 m depth. The overlying less dense layer presented a homogeneous density structure. Eastward, in the central part of the Paso Largo zone, the sigma-t values were lower, probably caused by the freshwater input from small sounds and river discharges (Figs. 1(a), (b) and 5b). The isopycnals were widely spaced until the density discontinuity below 40 m depth. The intermediate brackish layer was extended eastward through the Strait of Magellan and it reached the oceanographic barrier located nearby the Carlos III Island. Here, an abrupt upward deflection of the isopycnals evidenced the oceanic front and the beginning of the Atlantic Ocean domain. The position of this front probably restrained the water exchange from the Otway Sound. Buoyancy frequency values were close to zero in the overall section with a tendency to negative values, which reflected the unstable stratification conditions of the water column (Fig. 6). 3.3. Otway Sound zone This transect along the Otway Sound includes its water exchange path towards the Strait of Magellan (Jerónimo Channel, Fig. 1(a)). Despite the channel exhibited oceanographic similarities with the Strait of Magellan (i.e., salinity, temperature and oxygen) it is more similar to the Otway Sound zone due to its relatively higher concentration of fluorescent particles (Fig. 3(12)). The others two stations were placed inside the sound. 3.3.1. Profiles description and thin layers The Hammond station displayed both the highest Chl-a concentration and the integrated Chl-a concentration among all stations in this study (Figs. 3(13) and 4(c)). At Hammond and Zorrilla stations, the peaks of Chl-a appeared at the depth of the halocline and the inverted thermocline (Fig. 3(13) and (14)). The Cutter station exhibited a more homogeneous structure of the water column, with two minor termohaloclines (3 and 40 m depth). In this station, a soft peak of the Chl-a was related to the presence of the ‘green’ spectral group (Fig. 3(12)). The spectral group differentiation indicated the predominance of ‘brown’ group (85 wt%), followed by ‘red’ (8 wt%) and ‘green’ (7 wt%) groups (Fig. 4(c)). Yellow substances showed higher concentration at Cutter station, underneath the peak of Chl-a. Inside the Otway Sound, they were distributed along with the fluorescent particles. The dissolved oxygen showed higher concentration in a coincident depth to the highest Chl-a concentration. Downward, the oxygen concentration exhibited a decreasing general trend (Fig. 3(13) and (14)). Thin layers were defined at Hammond and Zorrilla stations. These layers were characterized by the increment of the Chl-a concentration together with the rise of the concentrations of ‘green’ and ‘red’ groups (Fig. 3(13) and 3(14)). The vertical width of the thin layer was 2.4 m in Hammond and 3.6 m in Zorrilla. The Chl-a within the thin layer accounted for 39 wt% and 65 wt% of the total integrated Chl-a concentration respectively. 3.3.2. Water structure and fluorescence particles distribution The stations in the Otway Sound zone displayed both maximum integrated Chl-a concentration and vertical single values (Figs. 3.12 to 3.14 and 4(c)). However, the vertical distribution of the fluorescent pigments showed a remarkable difference between the Jerónimo Channel (i.e., Cutter station) and the inner sound domain. While in the channel the vertical structure of the Chl-a was relatively homogeneous, the stations in the sound evidenced the formation of a thin layer at  15 m depth (Fig. 5(c)). However,

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the lack of an intermediate station did not allow interpolating them as singular structure. This pattern was also reflected by the dissolved oxygen, which showed a relatively homogeneous concentration at the Cutter station and higher values in the Chl-a rich layer at the Hammond and Zorrilla stations. The vertical distribution of the density discontinuities evidenced a more complex stratification of the water column. The Otway Sound exhibited a strong layer (  15 m depth) and at least two minor. In the Jéronimo Channel only one surface layer was detected (Fig. 5(c)). Despite of this complexity, it was possible to correlate spatially the stronger vertical gradients and the buoyancy frequencies with the high fluorescence patches (Fig. 5(c); R-square ¼0.3118). In the Jerónimo Channel, the negative values of the buoyancy frequency were close to zero, that is, a water column relatively unstable. Within the Otway Sound the superficial and unstable layer reached 7 m depth, followed by a stable layer until 20 m depth. Then, two slightly stable layers were located at 25 and 40 m depth. The deeper was coincident with a slightly stable layer in the Jerónimo Channel. However, the lack of intermediate stations did not allow interpolating them as a single structure (Fig. 6).

4. Discussion 4.1. Vertical and horizontal Chl-a distribution, thin phytoplankton layers and water structure The horizontal and vertical patterns of Chl-a concentration presented in this study reveal the influence of the water structure in the vertical distribution of the fluorescent pigment in the Strait of Magellan and associated fjord and sounds (Fig. 6). Our results show the first observations of thin phytoplankton layers in southern Patagonian fjords. Previous studies, in the northernmost region of the Chilean fjords, reported the occurrence of high cell densities (0.5–3  103 cells l
1) of Dinophysis spp. in a restricted depth range that is related to the position of the pycnocline. (Alves-de-Souza et al., 2014). In our study, 50% of the water profiles show thin layer structures. Similar values have been reported from the East Sound, Washington. Here, 54% of profiles displayed thin layers (Dekshenieks et al., 2001). In Monterey Bay, California, thin layers were found only at 15% of the profiles acquired (BenoitBird et al., 2009). In tropical waters the thin layers occurrence range from 21% in the Red Sea (Steinbuck et al., 2010) to 69% in the Hawaiian coast (McManus et al., 2012). The integrated Chl-a concentration within the thin layers account for a significant fraction (31–67 wt%) of the total integrated Chl-a (Fig. 4). Comparatively, in the Monterey Bay this fraction ranged from 33–47% (Sullivan et al., 2010b). The formation and persistence of phytoplankton-rich thin layers is often connected to the particular oceanographic settings that affect the balance of mixing/stability and divergence/convergence processes (Sullivan et al., 2010a). Our profiles and integrated sections indicate that the existence of strong pycnoclines plays a key regulatory role in the vertical distribution of thin phytoplankton layers (Fig. 3). The density values (sigma-t) are closely related to salinity, which plays a major role in defining the density distribution and discontinuities in high latitude oceanic waters (Carmack, 2007). At the Glacier-Beaufort and Otway Sound sites, the layers with highest Chl-a concentration show a spatial relationship with the highest vertical density gradient (Fig. 5(a) and (c)). In these two zones, the Chl-a concentration is correlated with the buoyancy frequencies. In contrast, along the Strait of Magellan the superficial patches of phytoplankton and the vertical density gradients are more homogeneously distributed (Fig. 5(b)). Here, the correlation

of Chl-a concentration with the buoyancy frequencies does not show a relationship. In the Otway Sound, the input of water with less salinity from the Skyring Sound (  17 psu at the surface, Kilian et al., 2007a), through the Fitz Roy Channel, reduces the surface density at the Zorrilla station and probably causes the sinking of the Chl-a rich layer. The surface density increases vertically and horizontally from the eastward side of the Otway Sound to the Strait of Magellan. The horizontal distribution of the isopycnals shows an abrupt upward deflection toward the Jerónimo Channel, which could limit the advection of the Otway’s waters to the Strait of Magellan and consequently, the horizontal distribution of the Chla rich layer. Seasonal changes influence the dynamics of water masses by means of variable physical stratification and mixing processes. The wind stress and the freshwater runoff rates modulate the dynamics of water columns in different depth intervals. In the Patagonian fjords of the Magellan region, the high runoff rates generate a low salinity surface layer throughout the whole year (Kilian et al., 2007a, 2013), especially in sectors with strong glacial influence and seasonal meltwater of snow from higher mountains (e.g., GCN, Santa Inés Island; Fig. 1(a)). The high flow of fresh water influences the stratification of the water column, and, as in the case of the Scottish fjord Loch Etive (McKee et al., 2002), acting as a source of buoyancy that affects the vertical distribution of the Chl-a (Fig. 6). Layering events recur more frequently in the southernmost area of Patagonia compared with the Northern area (Pérez-Santos et al., 2014). This latitudinal distribution is modified by the distinct oceanographic settings of such areas. In the sector between 46°48'S and 50°09'S, the well-mixed water columns occurs more frequently in gulfs and open channels (Bustos et al., 2011). They generate a deeper mixed layer and more homogeneous vertical distribution of the Chl-a (Fig. 6). In Northern Patagonia the layering events are less recurrent (Pérez-Santos et al., 2014) and the depth of the mixed layer have been related to mesoscale changes in wind forcing, which is connected to the timing of phytoplankton blooms (Montero et al., 2011). This study shows that the structure of the water column in the Strait of Magellan is slightly unstable and characterized by a low buoyancy frequency (N2 r0). The structure of the water column is modified by the wind stress that causes a stable stratification (N2 4 0) at the surface ( 3 m), while the mixed layer is deeper (Fig. 6). Close to Carlos III Island -Crosside and York stations- the low Chl-a concentration was unexpected due to the close location of the thermohaline front of the Strait of Magellan. The phytoplankton growth can be strongly modulated by horizontal and vertical motions associated with oceanic fronts (Clayton et al., 2014). Front areas are often linked to enhanced phytoplankton growth (Marra et al., 1990). The observation of high animal abundance -whales, penguins, cormorants- around the Carlos III Island, as in the case of open ocean fronts, may be explained by high phytoplankton biomass and primary production associated with extensive diatom patches (Yoder et al., 1994). However, discrete and relatively low zooplankton biomass concentrations have been reported to this area (Palma and Silva, 2004). Our results indicate that a deeper mixed layer is disadvantageous to the buoyant algae of the ‘brown’ group, which must spend more time on the low photosynthetically active radiation (PAR) layer. Changes in the dynamics of water masses that shift to more stratified waters could control the increase on the phytoplankton biomass. In the Glacier-Beaufort zone, the stations most exposed to the westerly winds -Nolasco, Tamar and Santa Ana- show unstable stratification (N2 o 0) at the surface. Below the surface, stable stratification conditions are provoked by high freshwater input, which overlays the saltier water (Figs. 1(b) and 6). Thin layers are partially sheltered from turbulent mixing by vertical gradients in

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density (Dekshenieks et al., 2001). The most conspicuous examples of persistent thin layers have been observed in such highly stratified waters (Fig. 5(a); Donaghay et al., 1992). In the Patagonian fjords, the interaction of cold freshwater input and the advection of ocean water has been demonstrated to produce layering in the first 60 m of the water column (PérezSantos et al., 2014). Although an increase in vertical stability is favorable for the growth and accumulation of phytoplankton, it does not cause an increase of biomass concentrations near the surface. The stratification and stability of the water structure interact with the photoadaptation of the phytoplankton to low PAR, which is an important factor that controls the biomass concentration (Pizarro et al., 2000). In the most stratified sector of the Glacier-Beaufort zone, Chl-a concentration variability is also related to the turbidity of the water generated by the suspended load in the runoff from glaciers. The input of suspended load is highest at the station closest to the glacier. This station -Los Glaciares- shows a relatively low integrated Chl-a concentration and the depth of the maximum concentration is the shallowest of this zone (Figs. 4 and 5(a)). In the Magellan fjord region, the vertical position of the thin layers is related to the pycnocline location (Fig. 3) and high Chl-a concentrations are positively correlated with the stratification of the water column (Fig. 6). Therefore, mechanisms involved in the formation of thin layers are probably derived by differences in the water density or by processes that occur at the pycnocline depth. On one hand, shear and stratification peaks are often aligned in both depth and thickness (Johnston and Rudnick, 2009) and thin layers are frequently observed at depths at which the vertical shear is enhanced, often corresponding to the location where the horizontal velocity changes direction (Birch et al., 2008; Cowles, 2004; Dekshenieks et al., 2001; Sullivan et al., 2010b). This mechanism -gyrotactic trapping- has been related to the formation of thin layers of motile phytoplankton (Durham et al., 2009) like in the case of dinoflagellates. On the other hand, due to the predominance of non-motile diatoms in this region (Almandoz et al., 2011; Alves-de-Souza et al., 2008; Avaria, 2008; González et al., 2011; Iriarte et al., 1993; Iriarte et al., 2007; Pizarro et al., 2000), the differential buoyancy (Durham and Stocker, 2012) in the water column is also a probable mechanism for the formation of the thin layers observed in this study. Further studies assessing a more detailed description of the hydrography of Magellan fjords need to be performed in order to full understand the mechanisms determining the formation of thin layers in these systems. 4.2. Phytoplankton spectral groups In the investigated profiles ‘brown’ group (Bacillariophyceae and Dinophyceae) is the predominant algae group, accounting for 480 wt% of the phytoplankton (Fig. 4). The Shelter station represents an exception: it contains a second and deeper phytoplankton patch, in which ‘green’ (Chlorophyta) and ‘blue’ (Cyanobacteria) algae predominate (Figs. 3(7) and 4(b)). This deeper layer is associated with a halocline at 40 m depth, which is probably a result of the intrusion of oceanic water through the Abra Channel (Fig. 1(a)). The ‘red’ group (Cryptophyta) is a less common spectral group. They account for o8 wt% of all calculated biomass (Fig. 4), and are found within phytoplankton patches with concentrations over 15 mg l
1 (Fig. 3(2), 3(3), 3(5), 3(13) and 3(14)). Taxonomic classification by spectral fluorescence signature is subject to bias in the signatures from inter- and intra-specific variation in the shape of signatures and in Chlorophyll-specific fluorescence, and in the relationship between fluorescence intensity and Chl-a concentration (MacIntyre et al., 2010). The spectral discrimination and the biomass estimated for the ‘red’ group could be not accurately attributed to cryptophytes because

9

the phycoerythrin pigments of cryptophyte origin can also be found in species of the dinoflagellate genus Dinophysis (GarciaCuetos et al., 2010; Rial et al., 2013) and also the mixotrophic ciliate Myrionecta rubra (Johnson et al., 2006), both of them frequently abundant in Chilean fjords (Alves-de-Souza et al., 2014). Particular difficulties arise if two different dominant phytoplankton species or groups have similar spectra ‘fingerprints’ (Hofmann and Peeters, 2013) or if more than four spectral groups are present (Kring et al., 2014). The predominance of non-motile diatoms during the high productivity season in Patagonian fjords lead to an increase in export production compared to the nano-pico phytoplankton assemblages (González et al., 2010), which are the dominant groups during the late summer-early autumn season in the Strait of Magellan (Magazzù et al., 1996). Moreover, the phytoplankton species which appear in harmful algae blooms (HABs) observed in Austral Chilean fjords (Lembeye, 2008) have been related to thin layer aggregation, e.g., Pseudo-nitzschia (McManus et al., 2008; Timmerman et al., 2014), Dinophysis spp. (Koukaras and Nikolaidis, 2004) and the gender Alexandrium (Townsend et al., 2005). Previous studies have reported comparable results between FP Chl-a estimates and biomass data obtained by standard spectrophotometry methods, high performance liquid chromatography (HPLC) and microscopic observations (e.g., Beutler et al., 2002; Escoffier et al., 2015; Gregor and Maršálek, 2004; Liu et al., 2012). However, in order to calibrate the spectral ranges used to differentiation between algal groups obtained by the FP, the HPLC method can give a detailed description of the algal pigments of the Patagonian phytoplankton assemblages. Improved information about the phytoplankton community structure and the identification of their functional groups is a key to understand the biochemical cycles (Isada et al., 2015) and to assess the paleoenvironmental conditions that could define changes in the primary production in the Patagonian fjords region.

5. Conclusions The use of fluorescence in situ coupled to CTD-O2 for fine-scale measurements provides an efficient means of assessing phytoplankton patchiness relative to the physical and chemical variables in the water column. The estimates of the primary production in the Patagonian fjords must consider the trophic importance of the formation of fine-scale structures (e.g., Landaeta et al., 2013; McManus et al., 2005) and should include more accurate sampling strategies. Within this approach, it is important to regard the micronutrients availability (e.g., dissolved Fe, Zn, Mn, Cu, Mo, Cd) as limiting factor to the formation and persistence of phytoplankton patches. In the Magellan region, the input of these micronutrients is favored by the acidification of soils derived by the volcanic activity (Kilian et al., 2006, 2013). Furthermore, the volcanic deposits and glacial clays have an important effect in the input of silica in the fjords system. The transport of these nutrients from the terrestrial to aquatic systems, could be controlled by the high precipitation rates, rivers discharges (Dávila et al., 2002) and its pH conditions, as well as the timing of glacial melting (Monahan and Ramage, 2010). The metric of the phytoplankton thin layer is directly related to processes that rely on encounter rates, such as the formation and subsequent settling of aggregates (Durham and Stocker, 2012). These processes are often linked to the production exported to the sediments (Guidi et al., 2009). Then, the mechanisms involved in the development of these structures play an important role in the primary productivity reconstruction models in the highly stratified waters of the Southern Patagonia.

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In the Southern Patagonian fjords the microphytoplankton spatial pattern shows a high heterogeneity in a sub-regional scale, which is explained mostly by the variability of the temperature and nutrients (Paredes et al., 2014). However, the interplay between the stratification and mixing processes is directly connected to the vertical distribution and abundance of phytoplankton. In a sub-regional scale, areas with higher freshwater input (e.g., Glacier-Beaufort zone) and stronger layering processes are favorable to the formation of thin layers with high Chl-a concentration. At the Los Glaciares station, the increment of the turbidity, caused by the suspended particles nearby the glacier ablation zone, affect inversely both integrated and maximum Chl-a concentration. In the Strait of Magellan, the subsuperficial advection of oceanic water causes a relatively deeper stratification on the water column and it probably provokes the ‘intrusion’ of phytoplankton groups from the ocean (Fig. 3(7)). This area shows, in general, a more homogeneous water column below the superficial stratification caused by the wind-induced currents. Thus, the vertical distribution of phytoplankton follows similar pattern without formation of thin layers (Fig. 6). The Chl-a concentration, both integrated and maximum, displays lower values compared to the areas with a higher stratification.

Acknowledgements This study was founded by grant number Ki-456-12 of the German Research Society (Deutsche Forschungsgemeinschaft: DFG). Marcelo Arévalo is thanked for his suggestions and collaboration during the fieldwork. Katja Gengenbach is thanked for the field assistance and Oscar Baeza-Urrea for his constant support. Professors Sven Thatje and Morty Ortega helped to improve the English. Comments from José Luis Iriarte and two anonymous reviewers improved the manuscript.

Appendix A. Supporting information Supplementary data associated with this article can be found in the online version at http://dx.doi.org/10.1016/j.csr.2016.04.011. These data include Google maps of the most important areas described in this article.

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