Progress in Oceanography xxx (2014) xxx–xxx

Contents lists available at ScienceDirect

Progress in Oceanography

journal homepage: www.elsevier .com/ locate /pocean

Springtime size-fractionated primary production across hydrographicand PAR-light gradients in Chilean Patagonia (41–50�S)

http://dx.doi.org/10.1016/j.pocean.2014.08.0030079-6611/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author at: Programa COPAS Sur-Austral, Universidad de Con-cepción, Concepción, Chile.

E-mail address: bjacob@udec.cl (B.G. Jacob).

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionated primary production across hydrographic and PAR-light gradientsean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.pocean.2014.08.003

Bárbara G. Jacob a,b,⇑, Fabián J. Tapia a,c, Giovanni Daneri a,d, Jose L. Iriarte a,e, Paulina Montero a,d,Marcus Sobarzo a,c,f, Renato A. Quiñones c,f

a Programa COPAS Sur-Austral, Universidad de Concepción, Concepción, Chileb Centro de Ciencias Ambientales (EULA-Chile), Universidad de Concepción, Concepción, Chilec Departamento de Oceanografía, Universidad de Concepción, Concepción, Chiled Centro de Investigación en Ecosistemas de la Patagonia (CIEP), Coyhaique, Chilee Instituto de Acuicultura, Universidad Austral de Chile, Campus Puerto Montt, Chilef Centro Interdisciplinario para la Investigación Acuícola (INCAR), Universidad de Concepción, Chile

a r t i c l e i n f o a b s t r a c t

Article history:Available online xxxx

We combined on-deck and in situ measurements and satellite-derived data to study the spatial variabilityof springtime size-fractionated primary production and chlorophyll-a biomass along gradients of hydro-graphic conditions and surface PAR in central and northern Chilean Patagonia (41–50�S). This extensiveand fragmented region encompasses numerous fjords and channels, as well as the northern and southernicefields (46–47�S, 48–52�S). Primary production displayed a latitudinal pattern decreasing southwards(6-fold lower), particularly toward areas influenced by rivers with a nival regime. Micro-phytoplankton(>20 lm) dominated the primary production (57–93%) and chlorophyll-a (43–91%) of northern sites,where warmer and more saline surface waters exhibit greater PAR irradiance. Small phytoplankton cells(<2 lm; 2–20 lm) contributed > 50% of carbon fixation and chlorophyll-a in the southernmost sites,especially those located near glaciers and major rivers, where surface temperature, salinity, and PAR irra-diance were lowest. The long-term (2002–2012) average field of springtime PAR derived from satelliteimagery showed a southward increase in longitudinal gradients, which indicates that spatial changesin surface light attenuation along this region are largely driven by glacier-derived freshwater inputs. Aprincipal component analysis of surface temperature, salinity, and PAR produced an ordination of sitesthat was consistent with spatial changes in the balance of oceanic versus riverine influence on surfaceconditions along this region. Total primary production was significantly correlated (r = 0.61, p = 0.007)with the first principal component, which explained 65% of joint variability in hydrographic conditionsand PAR. The same principal component clearly separated sites in northern Patagonia where micro-phy-toplankton dominated total primary production – along the Reloncavi fjord and Inner Sea of Chiloe – fromthose located further south where other size fractions were equally or more important. We stress theneed to include spatial variability in nutrient concentrations, which together with the strong light atten-uation induced by glacier-derived freshwater may further explain the spatial patterns in primary produc-tivity, phytoplankton biomass, and carbon fluxes along Chilean Patagonia.

� 2014 Elsevier Ltd. All rights reserved.

Introduction

Chilean Patagonia (41–56�S) is characterized by its highly com-plex geomorphology and hydrographic conditions, and by strongseasonal and latitudinal patterns in primary production, freshwa-ter discharge, precipitation, and glacier coverage (Pantoja et al.,2011 and references therein). This region includes extensive inlets

that make up 84,000 km of coastline (Silva and Palma, 2008). Estu-arine circulation is driven by the interaction of freshwater inputsfrom river outflows and heavy rainfall (2–5 m year�1, Strub et al.,1998) with the sub-surface intrusions of Sub-Antarctic Waters(SAAW) into the channels and fjords (Silva et al., 1998; Dávilaet al., 2002; Acha et al., 2004). The surface outflow of buoyantfreshwater carries high concentrations of dissolved silicon fromrivers, whereas the sub-surface oceanic waters transport nitrateand orthophosphate into the inlets (Silva et al., 1997; Silva,2008). In fjords, turbulent mixing between the two resulting layersof differing densities and the resulting vertical transport of heat,

in Chil-

Fig. 1. Map of the study region, from the Reloncaví Fjord (41�420S) to theConcepción Channel (50�090S). Sites where total and size-fractionated primaryproduction experiments and oceanographic measurements were conducted areshown as dots.

2 B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx

salt, and nutrients are promoted by a combination of frictionalforces, chiefly those driven by tides and wind stress forcing(Farmer and Freeland, 1983). Such vertical mixing and the avail-ability of light in near-surface waters largely determine the tempo-ral and spatial variability of phytoplankton biomass in fjordenvironments (Goebel et al., 2005).

Estimates of primary productivity and phytoplankton biomassfor the region spanning the Inner Sea of Chiloe (41–44�S) to theMagellan Strait region (52–55�S) have shown a latitudinal gradi-ent, with highest values at the northern end of this region(González et al., 2010, 2011) and a steady decrease toward thesouth (Aracena et al., 2011). Although such latitudinal patternmay stem from higher nutrient and light availability during theproductive season in northern Patagonia (Aracena et al., 2011),the southward increase in ice coverage and a concurrent transitionin river regimes from pluvial (i.e., rain dominated) to nival (i.e.,meltwater dominated) along the same region (Dávila et al., 2002)must be taken into consideration in order to better understandspatial–temporal patterns of productivity. Glacier melting duringthe warm season produces the release of inorganic matter knownas glacial silt, which attenuates light penetration into the watercolumn, limits the depth of the euphotic zone, and consequentlylimits primary production (Montecino and Pizarro, 2008).

There is a paucity of studies that focus on spatial patterns insize-fractionated photosynthetic rates and their association withpatterns in surface irradiance along Chilean Patagonia. Establishingsuch relationship has important implications for the study of pri-mary production, community structure and carbon fluxes in theregion, and for the changes in these patterns that may be expectedunder a future scenario of regional-scale changes in glacier meltingrates and freshwater inputs. Here, we focus on spatial patterns intotal and size-fractionated primary production and phytoplanktonbiomass (as chlorophyll-a), and their association with spatialchanges in hydrographic conditions (Temperature, Salinity) andPhotosynthetically Available Radiation (PAR) between 41� and50�S in Patagonia. We hypothesized that spatial patterns of pri-mary production in Patagonian fjords and channels are morestrongly associated to spatial changes in surface PAR than tohydrographic conditions, and that larger phytoplankton shouldbe dominant in areas with greater surface irradiance. Based onpublished data on nutrient concentrations along this region, wediscuss other factors that may shape the observed patterns in pri-mary production.

Materials and methods

Study area and oceanographic setting

The study area spans a wide latitudinal range from the Relon-caví Fjord (41�330S; 72�200W) to the Concepción Channel(50�090S; 74�420W) (Fig. 1, Table 1). This area includes the InnerSea of Chiloé and numerous channels and fjords, as well as theextensive Northern and Southern Icefields (46–47�S and 48–52�S,respectively). Water masses and circulation in these channelsand fjords have been characterized based on hydrographic datacollected during annual cruises (CIMAR-FIORDOS) sponsored bythe Chilean National Oceanographic Committee (e.g., Silva et al.,1995, 1997; Sievers et al., 2002; Sievers and Silva, 2008). Theseobservations have shown that, below a freshwater surface layer,the main oceanic water masses in this region correspond to Sub-Antarctic Water (SAW) between the sub-surface and 150 m depth,and to remnants of Equatorial Subsurface Waters (ESSW) betweenca. 150 and 300 m depth. The degree of mixing between SAW andsurface freshwater depends on the contributions from rivers, gla-ciers, coastal runoff, and rain, as well as on the distance to point

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionateean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.p

sources of freshwater (Sievers and Silva, 2008). Water that resultsfrom this mixing in the region has been referred to as ModifiedSub-Antarctic Water and Estuarine Water (Silva et al., 1998).

Vertical distributions of hydrographic and chemical propertiesindicate a general two-layer structure with a strong vertical gradi-ent in nutrient concentration (i.e., nutricline) at depths of 20–30 m(Sievers and Prado, 1994; Silva et al., 1995, 1997; Sievers et al.,2002). Phosphate and nitrate are delivered mainly from the ocean(1.2–2.4 lM phosphate; 12–24 lM nitrate; Silva, 2008), sincefreshwater from rivers, precipitation, and glacial melting is rela-tively low in these nutrients (0–0.8 lM phosphate; 0–8 lM nitrate;Silva, 2008). Freshwater from rivers is enriched in dissolved silicon(40–150 lM) and makes an important contribution to the surfacelayer in these estuarine environments (Silva, 2008).

Oceanographic observations

Sampling was conducted during three consecutive CIMAR-FIORDOS cruises, in the austral spring (November) of 2006, 2007and 2008. Sampling stations visited during these cruises spannedthree sections of the region of interest: from the Reloncaví fjordto Boca del Guafo (2006), from the northern entrance of MoraledaChannel to the Cupquelán Fjord (2007), and from Steffen Channelto Concepción Channel (2008). At all stations shown in Fig. 1,

d primary production across hydrographic and PAR-light gradients in Chil-ocean.2014.08.003

Table 1Summary of springtime CTD profiles used to compute the mean profiles shown on Fig. 2 and depth-integration used for PP estimates.

Site Code Number of casts Mean latitude (S) Mean longitude (W) Depth (m) integration

Degrees Minutes Degrees Minutes

Reloncaví Fjord [upper] FREu 24 41 33.966 72 20.118 0–25Reloncaví Fjord [middle] FREm 41 40.872 72 24.558 0–25Reloncaví Fjord [lower] FREl 41 42.954 72 38.202 0–25Comau Fjord FCO n.d 42 27 72 25.002 0–25Chiloe Inner Sea [east] CISe 24 42 21.528 72 57.408 0–30Chiloe Inner Sea [west] CISw 42 58.068 73 39.756 0–30Guafo Mouth GUA 5 43 44.442 74 13.02 0–30Moraleda Channel CMO 1 44 25.998 73 28.002 0–25Puyuhuapi Fjord FPU 4 44 39 72 43.998 0–20Aysén Fjord FAY 3 45 21.666 73 4.002 0–25Elefantes Channel CEL 1 46 25.998 73 46.002 0–20Steffen Channel CST 11 47 47.472 73 43.83 0–20Messier Channel CME n.d 48 02.23 74 38.7 0–20El Indio Channel CEI 1 49 3.012 74 26.022 0–20Concepción Channel CCO 1 50 9.03 74 42.498 0–20

B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx 3

and during all three cruises, vertical profiles of temperature andsalinity were gathered using SBE19 and SBE25 CTDs (Sea-Bird Elec-tronics, USA). Summary of springtime CTD profiles used to com-pute the mean profiles (Fig. 2) were shown in Table 1.Additionally, we used primary production (PP) estimates andhydrographic measurements obtained in November 2012 fromthree stations in the Puyuhuapi fjord. At all stations, discrete watersamples from standard depths (2, 10, 20, 30 m) were gathered formeasurements of total and size-fractionated chlorophyll-a and PP.

Photosynthetically Available Radiation (PAR)

To characterize the spatial patterns in surface light conditionsalong our study region, we used estimates of PAR (Photosyntheti-cally Available Radiation) produced from the Moderate ResolutionImaging Spectroradiometer (MODIS) aboard NASA’s Aqua satellite.The PAR product corresponds to a daily estimate of the total down-welling flux of photons just below the sea surface, hence it

Fig. 2. Mean vertical profiles of temperature and salinity in the upper 50 m at the 10 locathat were averaged for each area. Codes indicate the 10 sites detailed in Fig. 1 and Tabl

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionatedean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.po

provides a proxy for light conditions in the surface layers of thewater column. We used Level-3 composite images (8-day means,4 km resolution) gathered during November and December of2002–2012, to produce a springtime mean PAR field along theregion, as well as a latitudinal profile of average (±SD) PAR esti-mates at points near the study sites. These long-term means pro-vided reference values against which PAR estimates for theperiods spanned by the CIMAR-FIORDOS cruises were compared.Additionally, point-estimates of surface PAR for each PP experi-ment were obtained from the weekly MODIS image that spannedthe corresponding sampling date.

Total and size-fractionated primary production (PP) and chlorophyll-a(Chl-a)

All PP and chlorophyll-a estimates were obtained in australspring months (November) between 2006 and 2012 (Table 1).Gross primary production (GPP) from in situ experiments was

lities included in this study. Numbers in parentheses indicate the number of profilese 1.

primary production across hydrographic and PAR-light gradients in Chil-cean.2014.08.003

4 B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx

performed only in the Puyuhuapi Fjord (44�S). Water samples wereobtained from within the euphotic zone; three water depths (i.e., 2,5, 20 m in 28 and 29 November) and three water depths (i.e., 2, 5,10 m in 30 November). Water for GPP incubations and Chl-a phy-toplankton samplings were obtained from the same depth. Theeuphotic zone was determined as the depth where the scalar pho-tosynthetically active radiation (PAR) fell to 1% of the surface val-ues. In situ GPP were estimated from changes in dissolvedoxygen concentrations observed after incubating in situ light(Strickland, 1960). Water samples were collected at dawn. Waterfrom the Niskin bottles was transferred to 125 mL borosilicate bot-tles (gravimetrically calibrated) using a silicone tube; five time-zero bottles, five light bottles, and five dark bottles were used foreach incubation depth. The light and dark bottles were incubatedin situ, in a surface-tethered mooring system for 12 h; the time-zero bottles were fixed at the beginning of each experiment. GPPvalues were converted from oxygen to carbon units using a conser-vative photosynthetic quotient (PQ) of 1.25. Primary production(PP) was also estimated using the 14C method (Steeman-Nielsen,1952). Water samples for chlorophyll-a biomass measurementsand primary production (PP) experiments were collected using2.5-L PVC Niskin bottles at 0, 10, 20 and 30 m. Depths of integra-tion for PP estimates in Table 1. Samples for PP experiments wereincubated in 100-mL borosilicate glass bottles (two clear + onedark) and placed in a natural light incubator for 4 h during the timeof day with highest irradiance (approximately between 11 AM and3 PM). Temperature was regulated by running surface seawaterover the incubation bottles. Primary production was estimatedusing the 14C method (Steeman-Nielsen, 1952), adding 40 lCilabeled sodium bicarbonate (NaH14CO3) to each bottle. Sampleswere manipulated under subdued light conditions during pre-and post-incubation periods. Excess inorganic carbon was removedwith HCl fumes for 24 h. Filters were placed in 20-mL plastic scin-tillation vials and kept at �15 �C until radioactivity readings in aBeckman Liquid Scintillation Counter with 10 mL Ecolite. Chloro-phyll-a samples were analyzed at the same stations and depthswhere PP experiments were carried out. Seawater samples(200 ml) were filtered extracted in 90% v/v acetone and analyzedusing a digital PS-700 Turner fluorometer as recommended byParsons et al. (1984). A total of 17 vertical profiles of size-fraction-ated primary production and chlorophyll-a were obtained, usingthe following three size classes to segregate the phytoplanktonassemblage: microphytoplankton (>20 lm), nanophytoplankton(2–20 lm), and picophytoplankton (<2 lm). Phytoplankton sizefractionation was performed post-incubation in three sequentialsteps: (1) seawater (100 mL) for the nanophytoplankton fraction(2–23 lm) was pre-filtered using 23-lm Nitex mesh and collectedon a 2-lm Nuclepore filter; (2) the picophytoplankton fraction(0.7–2 lm) was collected on a 0.7-lm MFS (Microfiltration Sys-tems) glass-fiber filter; and (3) seawater (100 mL) for the wholephytoplankton community was filtered through a 0.7-lm MFSglass-fiber filter. The microphytoplankton fraction was obtainedby subtracting the production estimated in steps 1 and 2 fromthe production estimated in step 3. Depth-integrated values of pri-mary production (gC m�2 h�1) and chlorophyll-a biomass(mg m�2) were calculated using trapezoidal integration. To com-pare PP estimates among areas, we used hourly depth-integratedPP rates.

Statistical analysis

Given the co-variation known to occur among the three envi-ronmental variables considered in this analysis (i.e. temperature,salinity and surface PAR), a Principal Component Analysis (PCA)was conducted (1) to group sampling stations according to thejoint variability of all three variables, and (2) to combine these

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionateean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.p

original variables into statistically independent environmentalpredictors for primary production. Temperature and salinity dataused in this analysis corresponded to depth-averages calculatedover the top 20 m, whereas surface PAR values were extracted fromthe weekly MODIS image that spanned each PP experiment (seeabove). Data were standardized prior to the computation of princi-pal components (PC) and their respective loadings on each originalvariable. Linear correlation among the log-transformed PP esti-mates and the first principal component (PC1) was computed toassess the degree of association between total primary productionand the combined variability of hydrographic conditions and sur-face PAR.

Results

Hydrography

Spatial variability in the intensity of vertical mixing betweenlow-salinity surface waters and Sub-Antarctic Waters (SAW) hasbeen observed across Chilean Patagonia (Sievers and Silva, 2008).This variability became apparent when we compared mean spring-time temperature and salinity profiles from 10 areas (Fig. 2). Stron-ger haline stratification in the surface layer (i.e., top 10 m) wastypical of fjords such as the Reloncaví (FRE), Puyuhuapi (FPU),and Aysén (FAY) (Fig. 2). Hydrographic profiles from the InnerSea of Chiloé (CIS) and Boca de Guafo (GUA) indicated strong mix-ing with no thermal or haline stratification through the upper 50 mof the water column (Fig. 2), and temperature/salinity values (10–12 �C and �30 psu) indicating a strong influence of oceanic water.Southern areas similarly exposed to oceanic influence, such aschannels El Indio (CEI) and Concepción (CCO), showed similarhydrographic characteristics (Fig. 2). Profiles for the northern andsouthern tips of the Moraleda Channel (CMO and CEL) showedno thermal or haline stratification, although they differed consis-tently through the top 50 m. Differences in temperature and salin-ity detected among these sites, with salinity and temperaturebeing higher at CMO than at CEL, can be ascribed to geomorpholog-ical features along the Moraleda Channel that may generate dis-tinct physical and biological conditions (González et al., 2011).While the northern section of the Moraleda Channel is influencedby intrusions of SubAntarctic Water through Boca del Guafo(Fig. 1) (Silva and Guzmán, 2006), the southern section receiveslow-salinity meltwater from the northern Ice field and the SanRafael Lagoon (González et al., 2011).

The Aysén Fjord (>45�S; FAY) marked a north–south transitionin near-surface temperatures (top 10 m), from >10 �C to <10 �C(Fig. 2). This temperature transition is consistent with latitudinalchanges in the river regimes described by Dávila et al. (2002), frompluvial at 35–43�S, to mixed at 43–47�S, to nival at 47–54�S.According to this regional pattern, fjords and channels locatedsouth of Elefantes channel (�47�S) are strongly influenced by riv-ers with maximum discharges of colder freshwater during the aus-tral summer, when the ice melt takes place. Finally, the SteffenChannel is strongly affected by the glacial melt and shows a deeperhalocline (�20 m) due to the influence of both freshwater dis-charges and marine water.

Total and size-fractionated primary production (PP) and chlorophyll-a(Chl-a)

Depth-integrated PP rates (Fig. 3) and chlorophyll-biomass dur-ing spring season (Fig. 4) showed a trend to decrease with increas-ing latitude, although not monotonically. The highest PP rates(0.63 gC m�2 h�1) and chlorophyll-a biomass (298.92 mg m�2)occurred at the northern section, and more specifically at Reloncaví

d primary production across hydrographic and PAR-light gradients in Chil-ocean.2014.08.003

Fig. 3. Depth-integrated primary production at 20 localities during springtime,from 41�S (Reloncaví Fjord) to 50�S (Concepción Channel) in Chilean Patagonia.

Fig. 4. Depth-integrated Chlorophyll-a biomass at 20 localities during springtime,from 41�S (Reloncaví Fjord) to 50�S (Concepción Channel) in Chilean Patagonia.

B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx 5

fjord, Inner Sea of Chiloé, and Boca de Guafo (Table 2). The averagePP rates in the northern section was 0.38 gC m�2 h�1 (0.089–0.63 gC m�2 h�1). In the central section (Moraleda Channel, Puy-uhuapi and Aysén Fjord) the average PP was 0.12 gC m�2 h�1

(0.044–0.18 gC m�2 h�1), whereas in the southern section (Elefan-tes, Steffen, Messier, Indio and Concepcion Channel) it reached0.058 gC m�2 h�1 (0.006–0.12 gC m�2 h�1). The northern sectioncorresponded with the highest contribution of microphytoplank-ton (>20 lm) to total carbon fixation (mean: 78%; range: 57–93%) and chlorophyll-a biomass (mean: 61%; range: 43–91%).Finally, the relative contribution of small phytoplankton cells (2–20 and <2 lm) to total carbon fixation and chlorophyll-a biomasswas >50% in the central and southern section. (Figs. 5 and 6).

Photosynthetically Available Radiation (PAR)

Springtime PAR exhibited a latitudinal trend to decrease south-wards, which was apparent in semi-enclosed coastal waters butnot in continental waters (Fig. 7a). There was a clear drop in PARnear channels and fjords from the central to southern section,which was not paralleled by PAR estimates for large lakes in these

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionatedean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.po

same sections. We ascribe the differences in surface PAR betweenlakes and fjords to spatial differences in (1) relative contributionof glacier melt to freshwater inputs into lakes/fjords, (2) residencetimes, and (3) density stratification. The zonal gradient in surfacePAR becomes more apparent in central-southern Patagonia (e.g.,Lake General Carrera 46.5�S), as freshwater discharges from gla-ciers take place closer to river mouths, or directly into fjords/chan-nels. Shorter residence times and stronger density stratification inestuarine areas would prevent or substantially slow down thesinking of fine particles of glacial origin from surface waters. Con-sistently, fjords and channels in this southern section had substan-tially lower long-term means for springtime PAR, as well as valuesobserved during the primary production experiments (Fig. 7b).There was a significant trend for mean springtime PAR to decreasesouthwards, both when regression analyses were performed onlong-term (2002–2012) springtime means (slope = �1.83 E m�2 -d�1 per degree of latitude, p < 0.001) and on PAR values obtainedfor the dates on which during primary production experimentswere conducted (slope = �4.04 E m�2 d�1 per degree of latitude,p < 0.001).

The Principal Component Analysis performed on surface tem-perature, salinity and PAR produced a first and second principalcomponent that explained 65% and 29% of total variance, respec-tively. All three variables contributed similarly to the ordinationof sites along the PC1 axis, which separated sites with stronger oce-anic influence from sites more strongly influenced by water thatwas colder, less saline and with lower surface PAR (Fig. 8a). Salinitywas the main variable determining the ordination of sites along thePC2 axis, which clearly separated sites located at similar latitudesbut different distances to freshwater sources, such as the Puyuhu-api and Reloncavi sites (e.g. FPU, FRE, see Fig. 8a). Total primaryproduction was significantly correlated with PC1 (r = 0.61,p = 0.007, Fig. 8b). As for spatial variability in the fraction of totalPP that corresponded to large-cell phytoplankton, it was signifi-cantly correlated with PC1 (r = 0.72, p = 0.006) but not with PC2(Fig. 9), suggesting that the dominance of large-cell phytoplanktonin sites of northern Patagonia such as Reloncavi fjord (FRE), Bocadel Guafo (BGU), and the Chiloe Inner Sea (CIS) is determined bythe combination of warmer, more saline, and more transparentsurface waters.

Discussion

Our knowledge of the main ecological factors that controlmesoscale variability of primary productivity in Chilean Patagoniaremains limited. Synoptic snapshots of the PhotosyntheticallyAvailable Radiation (PAR), in addition to hydrographic conditions,may shed light on the complex interactions that determine thespatial distribution of primary productivity. Light is the basicenergy source for microalgae and, consequently, it is one of themost important parameters to be addressed. However, there is lit-tle published information on the mesoscale distribution of PARalong the Chilean Patagonia. Studies on the optical properties ofthe water column have been conducted in Magallanes (Pizarroet al., 2000), Aysén (Pizarro et al., 2005) and in the Inner Sea ofChiloé (Montecino et al., 2009), with the lowest PAR valuesreported for the southern region, between Golfo de Penas (47�S)and Concepcion Channel (50�S) (Table 3). The highest PAR extinc-tion coefficients (KPAR) were also found in the southern region, andwere intermediate and low in the central and northern sections,respectively. The north–south increase in KPAR was reflected by anorth–south drop in euphotic zone depth (i.e. 1% of surface PAR)(Table 3). Low PAR values found south of 47�S stem from the exten-sive ice coverage and major rivers. Here, the Northern and South-ern Icefields release high loads of inorganic matter, known as

primary production across hydrographic and PAR-light gradients in Chil-cean.2014.08.003

Table 2Summary of springtime (November) of primary production rates and chlorophyll-a biomass, depth-averages of temperature and salinity calculated over the top 20 m of the watercolumn, PAR-light weekly values (8-day means) and daily average (±SD) PAR estimates at points near the study sites.

Area Code Date PP (gC m�2 h�1) Chl-a (mg m�2) Temp (�C) (0–20 m) Sal (psu) (0–20 m) PAR (8d) E m�2 d�1 PAR (1d) E m�2 d�1

Reloncaví FREl 4-Nov-06 0.089 86.13 11.3 31.15 51.52 58.23Reloncaví FREm 6-Nov-06 0.372 226.14 11.54 26.81 51.52 58.70Reloncaví FREu 8-Nov-06 0.629 298.92 11.64 26.66 51.52 58.63Chiloé Inner Sea CIS 9-Nov-06 0.273 30.44 23.31 32.11 43.26 58.38Comau F. FCO 5-Nov-05 0.164 75.71 n.d n.d n.d n.dGuafo M. GUA 10-Nov-06 0.554 25.54 11.36 32.2 37.26 46.11Moraleda C. CMO 3-Nov-07 0.165 33.54 10.14 30.79 37.57 36.57Puyuhuapi F. FPU 28-Nov-12 0.172 21.14 12.21 26.35 41.26 64.33Puyuhuapi F. FPU 29-Nov-12 0.044 10.79 18.83 21.54 41.26 57.87Puyuhuapi F. FPU 30-Nov-12 0.047 6.05 13.81 16.23 41.26 12Aysén F. FAY 9-Nov-07 0.186 22.19 9.58 27.1 36.83 18.42Aysén F. FAY 11-Nov-07 0.108 36.52 9.66 25.8 36.83 28.94Elefantes C. CEL 4-Nov-07 0.065 17.32 8.61 22.74 22.48 11.78Steffen C. CST 4-Nov-08 0.044 7.24 9.97 19.41 24.90 11.87Steffen C. CST 7-Nov-08 0.005 2.09 8.89 20.2 24.90 9.39Steffen C. CST 8-Nov-08 0.035 4.07 8.36 14.72 26.39 11.41Steffen C. CST 10-Nov-08 0.024 5.5 8.64 14.91 26.39 13.63Messier C. CME 11-Nov-08 0.072 24.04 n.d n.d n.d n.dEl Indio C. CEI 13-Nov-08 0.114 19.18 8.29 27.18 20.80 43.68Concepción C CCO 15-Nov-08 0.12 13.26 8.08 28.09 16.61 9.77

n.d: No data.

Fig. 5. Spatial variability of the contribution of phytoplankton size fractions (>20, 2–20, and <2 lm) to total primary production at 17 localities during springtime from 41�S(Reloncaví Fjord) to 50�S (Concepción Channel) in Chilean Patagonia.

6 B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx

glacial silt and characterized by its milky appearance, which leadsto strong PAR light attenuation (Pizarro et al., 2005; Montecino andPizarro, 2008). The erosive action caused by marginal runoff andprecipitation produces large amounts of suspended particulatematerial from organic and inorganic sources, further increasingthe light extinction coefficient through the water column (Pizarroet al., 2000). In addition to fine sediments derived from snowand ice melting, large inputs of freshwater along this region mayinclude factors such as chromophoric dissolved organic matter(CDOM) from terrigenous sources. CDOM absorbs sunlight, andmay further preclude light penetration through the water column.Furthermore, the ultraviolet and visible-light absorption by CDOMmay strongly influence euphotic zone depth in coastal waters(Osburn et al., 2009). The presence of CDOM (as quinine sulfateequivalent) has been recognized in Patagonian waters. CDOM aver-ages 0.085 ± 0.032 mg L�1 at 41–45�S; 0.21 ± 0.15 mg L�1 at 45–47�S, and 0.5 ± 0.14 mg L�1 at 47–50�S (S. Pantoja, unpublishedresults). Even though no systematic measurements have been

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionateean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.p

carried out and sources of CDOM in this region are unknown, thehighest concentrations are found in sites near the continent andwhere freshwater discharges are important, suggesting that CDOMmay be mostly supplied to the coastal ocean from terrestrialsources.

The study of latitudinal variability of springtime surface PARshowed a clear latitudinal decrease for semi-enclosed coastalwaters but not for continental waters (Fig. 7A). There was a largedrop in PAR near channels and fjords in the southern section,whereas PAR estimates for large lakes were relatively homoge-neous throughout the study area. In estuarine waters, the highestPAR irradiance fluxes were observed between 41 and 43�S (37–51 E m�2 d�1), intermediate values between 44 and 45�S (36–41 E m�2 d�1), and lowest values south of 46�S (<30 E m�2 d�1)(Table 2). In contrast, average PAR for lakes in the region rangedbetween 40 and 60 E m�2 d�1. These results indicate two distinctspatial patterns in surface irradiance between estuarine and conti-nental waters, and suggest latitudinal changes in the optical

d primary production across hydrographic and PAR-light gradients in Chil-ocean.2014.08.003

Fig. 6. Spatial variability of the contribution of phytoplankton size fractions (>20, 2–20, and <2 lm) to total chlorophyll-a biomass at 16 geographical areas during springtimefrom 41�S (Reloncaví Fjord) to 50�S (Concepción Channel) in Chilean Patagonia.

Fig. 7. (A) Satellite-derived mean field of PAR (Photosynthetically Available Radiation) calculated from MODIS-Aqua composite images (8-day means) for November–December of 2002–2012; study sites are shown as black dots. (B) Mean springtime PAR and its temporal variability (± SD) at each site for the 2002–2012 period (blue symbolsand line) and PAR values corresponding to the dates on which in situ measurements of PP were conducted (red symbols). (For interpretation of the references to color in thisfigure legend, the reader is referred to the web version of this article.)

B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx 7

properties of estuarine waters that promote light attenuation, par-ticularly in areas with high freshwater inputs from snow and gla-cier melting (Pizarro et al., 2000).

The average depth of the euphotic zone in the southern section(13.8 m; Table 3) suggests that light availability may limit the pri-mary production to the top 15 m of the water column, especially atsites with high optic density due to suspended detritus in the col-umn water (Pizarro et al., 2000). The north–south decrease of PPobserved in this study is consistent with a previous study that con-nects PP estimates along 41–55�S with its imprint on sedimentaryrecords, i.e. biogenic opal, organic carbon, molar C/N, bulk

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionatedean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.po

sedimentary d13Corg (Aracena et al., 2011). The study documenteda clear north–south gradient in PP, with highest values at the InnerSea of Chiloé (41–44�S) and lowest values near Caleta Tortel(47.5�S), the latter being strongly influenced by river dischargeswith high loads of glacial sediments. Biogenic opal in sedimentsreflected the latitudinal pattern of PP which was directly relatedto the water column silicic acid concentrations (Aracena et al.,2011). Regional features in PP and phytoplankton biomass couldresult from latitudinal variability in day length and insolation(i.e., total solar radiation reaching the surface). It is recognized thatday-length affects several aspects of phytoplankton physiology,

primary production across hydrographic and PAR-light gradients in Chil-cean.2014.08.003

Fig. 8. (A) Ordination of sites produced by a Principal Component Analysis based on temperature, salinity, and surface PAR (see Fig. 1 for site codes); eigenvectors and relativeweight of each variable on the PC1/PC2 plane are shown in blue. (B) Correlation between total primary production and the first principal component representing the jointvariability of temperature, salinity, and surface PAR.

Fig. 9. Variability of the fraction of primary production corresponding to large-size phytoplankton as a function of the first principal component (PC1) representing the jointvariability of temperature, salinity, and surface PAR (see Fig. 1 for site codes).

Table 3Mean, standard deviation and range of optical properties of the water column in the Chilean Patagonia. PAR: Photosynthetic Active Radiation, K(PAR): PAR extinction coefficient,Zeu: depth of the euphotic layer.

Area PAR (lmol m�2 s�1) K(PAR) (m�1) Zeu (m) References

NorthernMean n.d 0.24 27.2 Montecino et al. (2009)d.s 0.17 13.9Range 0.09–0.610 7.5–51.1

CentralMean 465 0.25 21.5 Pizarro et al. (2005)d.s 117 0.107 8.28Range 330–632 0.12–0.48 10–38

SouthernMean 407 0.35 13.8 Pizarro et al. (2000)d.s 132 0.086 5.5Range 212–640 0.16–0.44 10–27.2

n.d: No data.

8 B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx

such as maximum phytoplankton growth (Eppley, 1972), cellulardivision and enzymatic activities (Hobson et al., 1979), synthesisof macromolecules (Foy and Smith, 1980) and growth rate(Redalje and Laws, 1983; Bouterfas et al., 2006). Data on the annualcycle in day-length at four sites spanning Chilean Patagonia(Fig. 10), and the latitudinal distribution of insolation over an

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionateean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.p

annual cycle (Fig. 11), show that spring – summer days are twohours longer in the south (53–54�S) than in the north (41–46�S),whereas daily insolation is rather homogenous across this region.Together, these observations suggest that, despite a latitudinal gra-dient in day-length, its effect on primary productivity may benegligible.

d primary production across hydrographic and PAR-light gradients in Chil-ocean.2014.08.003

Fig. 10. Annual cycle of day-length at four sites from 41 to 54�S gathered from theChilean Navy’s Hydrographic and Oceanographic Service (SHOA, http://www.shoa.cl).

B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx 9

Surface PAR was highly and positively correlated with depth-averaged temperature and salinity, indicating that improved lightconditions occur in association with warmer and more salinewaters. On the other hand, decay of light conditions occurred inassociation with colder and less saline waters. The PCA and corre-lation analyses showed that sites do ordinate along a principal axisdetermined jointly by temperature, salinity and surface PAR, andthat PP is strongly associated to the simultaneous spatial changesin these three variables (Fig. 8). Despite a lack of information onthe concentrations of macronutrients during the PP experiments,our results and available evidence on the optical properties inthe water column (Pizarro et al., 2000, 2005; Montecino et al.,2009) suggest that light attenuation is one of the key factorsbehind the spatial structure of size-fractionated PP along ChileanPatagonia. Here, we found that springtime phytoplankton is dom-inated by large cells in the northernmost section of Patagonia (41–43�S), whereas small flagellates and picophytoplankton dominatefurther south. A dominance of large-size phytoplankton is oftenassociated with optimal growth conditions (i.e., light availabilityand nutrient concentrations). When both nutrients concentrationsand light availability are low, size-dependent constraints onresource acquisition have been observed in large-sized phyto-plankton species, which may therefore by out-competed bysmall-celled phytoplankton (Chisholm, 1992; Kiørboe, 1993). Cur-rently, there is a paucity of studies that focus on the availability ofinorganic nutrients and their effect on primary productivity in Pat-

Fig. 11. Annual monthly insolation values (W m�2) in 2007, which were obtainedfor every 2� latitude between 40�S and 50�S from the atmosphere–ocean modelprovided by NASA’s Goddard Institute for Space Studies (http://aom.giss.nasa.gov/srmonlat.html).

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionatedean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.po

agonia. Recent studies (Cuevas et al., unpublished) had indicatedthat there is no latitudinal variability of nitrate and orthophos-phate along Patagonia although higher concentrations of thesenutrients were observed at oceanic waters. In this study we havetaken data of nutrients published by Aracena et al. (2011) andwe used a Non-parametric statistics, i.e., Mann–Whitney U tests,to compare means between areas. No significant differences weredetected in the mean of nitrate (U = 30, p = 0.626) and orthophos-phate (U = 29.5, p = 0.059) between northern and central sections,respectively. While, there is significant differences in the mean ofnitrate (U = 15, p = 0.014) and silicate (U = 6, p = 0.002) betweencentral and southern sections, respectively. The synergistic effectof the optical properties in the column water and nutrients concen-trations particularly, the silicic acid input from rivers may furtherexplain the spatial patterns of variability in primary productivity,phytoplankton biomass, and carbon fluxes along Chilean Pata-gonia. Further studies must consider the joint variability of hydro-graphic conditions, surface irradiance, and nutrient concentrationsin order to better understand such patterns. The potential for lightlimitation induced by inorganic sediments (silt) and organic matter(CDOM), from terrestrial sources and the decrease of nutrients andtemperature in the southern part of Patagonia (47–51�S) must betaken into account when interpreting the spatial patterns of pri-mary production.

Concluding remarks

The river outflow regimes along Patagonia vary with latitude,from winter-centered pluvial regimes in the northern section(35–43�S) to mixed and summer-centered nival regimes in thesouthern section (43–54�S). Freshwater discharges are greatestwhere mixed and nival regimes dominate (Dávila et al., 2002).Here, we have shown that large-cell phytoplankton is dominantin the northernmost areas of Patagonia (41–43�S). In contrast,small flagellates and picophytoplankton dominated the primaryproduction and chlorophyll-a in the southermost areas, especiallyareas affected by the glacial melting. Total primary productionand large-cell fraction of PP were significantly correlated withthe first principal component, which explained 65% of joint vari-ability in hydrographic conditions and PAR. In addition, a clear lat-itudinal decrease in springtime PAR was observed for semi-enclosed coastal waters but not for continental waters. Theseresults indicates that spatial changes in surface light attenuationalong this region are largely driven by glacier-derived freshwaterinputs and suggest that light attenuation is one of the key factorsbehind the latitudinal pattern in size-fractioned PP.

Acknowledgements

We wish to thank Carolina Calvete and the National Center forHydrographic and Oceanographic Data (CENDHOC) for providinghydrographic data from CIMAR cruises 12, 13, and 14. BárbaraJacob was supported by a Doctoral Fellowship from the COPASSur-Austral Program at University of Concepción. Funding for G.Daneri, R.A. Quiñones, F. Tapia, M. Sobarzo, and J.L. Iriarte was pro-vided by COPAS Sur-Austral Program, grant #PFB-31. R.A. Quiñoneswas also funded by the Interdisciplinary Center for AquacultureResearch (INCAR; FONDAP Grant No. 15110027; CONICYT, Chile).Partial funding was provided by FONDECYT Grant 1070713.

References

Acha, E.M., Mianzan, H.W., Guerrero, R.A., Favero, M., Bava, J., 2004. Marine fronts atthe continental shelves of austral South America: physical and ecologicalprocesses. Journal of Marine Systems 44, 83–105.

Aracena, C., Lange, C.B., Iriarte, J.L., Rebolledo, L., Pantoja, S., 2011. Latitudinalpatterns of export production recorded in surface sediments of the Chilean

primary production across hydrographic and PAR-light gradients in Chil-cean.2014.08.003

10 B.G. Jacob et al. / Progress in Oceanography xxx (2014) xxx–xxx

Patagonian fjords (41–55 S) as a response to water column productivity.Continental Shelf Research 31, 340–355.

Bouterfas, R., Belkoura, M., Dauta, A., 2006. The effects of irradiance andphotoperiod on the growth rate of three freshwater green algae isolated froma eutrophic lake. Limnetica 25, 647–656.

Chisholm, S.W., 1992. Phytoplankton size. In: Falkowski, P.G., Woodhead, A.D.(Eds.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, NewYork, pp. 213–237.

Dávila, P., Figueroa, F., Muller, E., 2002. Freshwater input into the coastal ocean andits relation with the salinity distribution off austral Chile (35–55� S).Continental Shelf Research 22, 521–534.

Eppley, R.W., 1972. Temperature and phytoplankton growth in the sea. FisheryBulletin 70, 1063–1085.

Farmer, D.M., Freeland, H.J., 1983. The physical oceanography of fjords. Progress inOceanography 12, 147–220.

Foy, R.H., Smith, R.V., 1980. The role of carbohydrate accumulation in the growth ofplanktonic Oscillatoria species. British Phycological Journal 15, 139–150.

Goebel, N.L., Wing, S.R., Boyd, P.W., 2005. A mechanism for onset of diatom bloomsin a fjord with persistent salinity stratification. Estuarine, Coastal and ShelfScience 64, 546–560.

González, H.E., Calderón, M.J., Castro, L., Clement, A., Cuevas, L.A., Daneri, G., Iriarte,J.L., Lizárraga, L., Matínez, R., Menschel, E., Silva, N., Carrasco, C., Valenzuela, C.,Vargas, C.A., Molinet, C., 2010. Primary production and plankton dynamics inthe Reloncaví Fjord and the interior Sea of Chiloé, Northern Patagonia, Chile.Marine Ecology Progress Series 402, 13–30.

González, H.E., Castro, L., Daneri, G., Iriarte, J.L., Silva, N., Vargas, C.A., Giesecke, R.,Sánchez, N., 2011. Seasonal plankton variability in Chilean Patagonia fjords:carbon flow through the pelagic food web of Aysén Fjord and planktondynamics in the Moraleda Channel basin. Continental Shelf Research 31, 225–243.

Hobson, L.A., Hartley, F.A., Ketcham, D.T., 1979. Effects of variations in daylengthand temperature on net rates of photosynthesis, dark respiration and excretionby Isochrysis galbana Parke. Plant Physiology 63, 947–951.

Kiørboe, T., 1993. Turbulence, phytoplankton cell size and the structure of pelagicfood webs. Advances in Marine Biology 29, 1–72.

Montecino, V., Pizarro, G., 2008. Primary productivity, biomass and phytoplanktonsize in the austral Chilean channels and fjords: spring–summer patterns. In:Silva, N., Palma, S. (Eds.), Progress in the oceanographic knowledge of ChileanInterior Water, from Puerto Montt to Cape Horn. Comité OceanográficoNacional & Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile, pp.93–97.

Montecino, V., Uribe, P., Soto, D., González, H., Riveros, J., Alarcón, G., Giglio, S.,Martínez, V., Paredes, M.A., 2009. Bio-optics and phytoplankton size diversityfrom in the inner Sea of Chile: spatial variability in winter–spring 2004 and2005. Ciencia y Tecnologia del Mar 32, 79–100.

Osburn, C.L., Retamal, L., Vincent, W.F., 2009. Photoreactivity of chromophoricdissolved organic matter transported by the Mackenzie River to the BeaufortSea. Marine Chemistry 115, 10–20.

Pantoja, S., Iriarte, J.L., Daneri, G., 2011. Oceanography of the Chilean Patagonia.Continental Shelf Research 31, 149–153.

Parsons, T.R., Maita, Y., Lalli, C., 1984. A Manual of Chemical and Biological Methodsfor Seawater Analysis. Pergamon Press, Oxford.

Pizarro, G., Iriarte, J.L., Montecino, V., Blanco, J.L., Guzmán, L., 2000. Distribución dela biomasa fitoplanctónica y productividad primaria máxima de fiordos y

Please cite this article in press as: Jacob, B.G., et al. Springtime size-fractionateean Patagonia (41–50�S). Prog. Oceanogr. (2014), http://dx.doi.org/10.1016/j.p

canales australes (47–50� S) en octubre 1996. Ciencia y Tecnologia del Mar(CONA) 23, 25–48.

Pizarro, G., Montecino, V., Guzmán, L., Muñoz, V., Chacón, V., Pacheco, H.,Frangópulos, M., Retamal, L., Alarcón, C., 2005. Patrones locales recurrentesdel fitoplancton en fiordos y canales australes (46–56�S) en primavera y verano.Ciencia y Tecnologia del Mar (CONA) 28, 63–83.

Redalje, D.G., Laws, E.A., 1983. The effect of environmental factors on growth andthe chemical and biochemical composition of marine diatoms. l. Light andtemperature effects. Journal of Experimental Marine Biology and Ecology 68,59–79.

Sievers, H.A., Prado, R., 1994. Contraste de las características oceanográficas delseno Aysén, Chile, entre invierno y verano (Lat. 45�200S). Revista de BiologíaMarina (Valparaíso) 29, 167–209.

Sievers, H.A., Silva, N., 2008. Water masses and circulation in austral Chileanchannels and fjords. In: Silva, N., Palma, S. (Eds.), Progress in the OceanographicKnowledge of Chilean Interior Waters, from Puerto Montt to Cape Horn. ComitéOceanográfico Nacional & Pontificia Universidad Católica de Valparaíso,Valparaíso, Chile, pp. 53–58.

Sievers, H.A., Calvete, C., Silva, N., 2002. Distribución de características físicas, masasde agua y circulación general para algunos canales australes entre el Golfo dePenas y el Estrecho de Magallanes (Crucero CIMAR Fiordo 2), Chile. Ciencia yTecnologia del Mar (CONA) 25, 17–43.

Silva, N., 2008. Dissolved oxygen, pH and nutrients in the austral Chilean channelsand fjords. In: Silva, N., Palma, S. (Eds.), Progress in the OceanographicKnowledge of Chilean Interior Waters, from Puerto Montt to Cape Horn.Comité Oceanográfico Nacional & Pontificia Universidad Católica de Valparaíso,Valparaíso, Chile, pp. 37–44.

Silva, N., Guzmán, D., 2006. Condiciones oceanográficas físicas y químicas, entreBoca del Guafo y Fiordo Aysén (Crucero CIMAR 7 fiordos). Ciencia y Tecnologiadel Mar 29, 25–44.

Silva, N., Palma, S., 2008. The CIMAR Program in the austral Chilean channels andfjords. In: Silva, N., Palma, S. (Eds.), Progress in the Oceanographic Knowledge ofChilean Interior Waters, from Puerto Montt to Cape Horn. Comité OceanográficoNacional & Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile, pp.11–15.

Silva, N., Sievers, H.A., Prado, R., 1995. Características oceanográficas y unaproposición de circulación, para algunos canales australes de Chile entre41�200S, 46�400S. Revista de Biología Marina 30, 207–254.

Silva, N., Calvete, C., Sievers, H.A., 1997. Características oceanográficas físicas yquímicas de canales australes chilenos entre Puerto Montt y laguna San Rafael(Crucero CIMAR-Fiordo 1). Ciencia y Tecnologia del Mar (CONA) 20, 23–106.

Silva, N., Calvete, C., Sievers, H.A., 1998. Masas de agua y circulación general paraalgunos canales australes entre Puerto Montt y Laguna San Rafael, Chile(Crucero Cimar- Fiordo 1). Revista Ciencia y Tecnología del Mar 21 (March), 17–48.

Steeman-Nielsen, E., 1952. The use of radiocarbon (14C) for measuring organicproduction in the sea. Journal du Conseil Permanent International pourl’Exploration de la Mer 144, 117–140.

Strickland, J.D.H., 1960. Measuring the production of marine phytoplankton.Bulletin Fisheries Research Board of Canada 122, 1–72.

Strub, P.T., Mesías, J.M., Montecino, V., Rutllant, J., 1998. Coastal ocean circulationoff western South America. In: Robinson, A.R., Brink, K.H. (Eds.), The GlobalCoastal Ocean. The Sea, vol. 11. Interscience, New York, pp. 273–313.

d primary production across hydrographic and PAR-light gradients in Chil-ocean.2014.08.003