Contribution of allochthonous organic carbon across the Serrano River Basin and the adjacent fjord...

Progress in Oceanography 129 (2014) 98–113

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Progress in Oceanography

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Contribution of allochthonous organic carbon across the SerranoRiver Basin and the adjacent fjord system in Southern ChileanPatagonia: Insights from the combined use of stable isotopeand fatty acid biomarkers

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⇑ Corresponding author. Tel.: +56 41 2204032; fax: +56 41 2207076.E-mail address: [email protected] (C.A. Vargas).

Alejandra Lafon a,b, Nelson Silva c, Cristian A. Vargas d,⇑a Interdisciplinary Center for Aquaculture Research (INCAR), Km 4.5, Coyhaique, Chileb Universidad Austral de Chile, Coyhaique & Doctoral Program in Environmental Sciences, Environmental Sciences Center EULA Chile, Universidad de Concepción, PO Box 160-C,Concepción, Chilec Escuela de Ciencias del Mar, Pontificia Universidad Católica de Valparaíso, PO Box 1020, Valparaíso, Chiled Aquatic Ecosystem Functioning Lab (LAFE), Aquatic System Unit, Environmental Sciences Center EULA Chile, Universidad de Concepción, 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 1 April 2014

Chilean Patagonia is characterized by an irregular geography involving many islands, peninsulas, chan-nels, sounds and fjords, that prevent direct interaction between oceanic water masses and freshwaterriver discharges at the head of the continental fjords. In this paper, we evaluate the potential sourcesand composition of organic matter along the Serrano River basin and the adjacent channels and fjordsin Southern Chilean Patagonia (51–52�S), as well as their importance for marine planktonic organisms.In spring of 2009, evidence of C:N ratio, d13C, d15N and fatty acids composition in particulate organic car-bon (POC), surface sediment, soil, plankton, and vegetal tissue, as well some physical and chemical char-acteristics (i.e. salinity, dissolved oxygen, NO3

�, NH4+, PO4

�3, Si(OH)4), were measured in samples collectedduring the CIMAR 14 Fiordos oceanographic cruise. Significant differences in d13C-POC were foundbetween the terrestrial and marine environments but not within fjord stations. Along the fjord region,the high C:N ratio and depleted d13C values in POC samples suggest that particulate organic matter(POM) in the upper level of the water column (0–10 m depth) is supported by different sources. Terres-trial organic carbon exported by rivers may constitute a significant subsidy, up to 70% based on two end-member mixing model, to the fjord ecosystem. Furthermore, terrestrial carbon might account for a sig-nificant percentage of the zooplankton body carbon, estimated both by using isotopic (�24–61%) andfatty acid analysis (�14–61%). Isotopic analyses in marine sediment samples suggest that POC seemsto be decoupled from terrestrial-influenced surface sources at the fjord stations, and the contributionof surrounding vegetation seemingly unimportant for carbon export to the benthos. Local hydrographicand geomorphological characteristics might determine the presence of oceanographic frontal zones,which in turn might explain differences in carbon sources found between POM and the surfacesediments.

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Introduction

Fjords are highly dynamic and complex estuarine ecosystemsthat act as a zone of interaction between fresh water (lakes, rivers,glaciers) and adjacent coastal systems (McLeod and Wing, 2007;Mayr et al., 2011). These zones may also support many importantecosystem functions, including biogeochemical cycling and move-ment of nutrients (Silva et al., 2011; Vargas et al., 2011). In order to

understand the role of fjords in global biochemical cycles, as wellas their vulnerabilities to anthropogenic stressors, the knowledgeof different sources of organic matter and their fluctuations isneeded. Understanding ecological processes across ecosystems isof growing importance as human interference, such as deforesta-tion, aquaculture, and dam construction, will likely affect climatechange with potentially devastating economic and ecological con-sequences, seriously impairing reciprocal energy exchange amongecosystems (Vargas et al., 2011).

The Chilean Patagonian fjords occur within a large region, fromReloncaví Fjord (41�200S) to Cape Horn (56�S), which is character-ized by about 84,000 km of coast line broken up by the contours of

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A. Lafon et al. / Progress in Oceanography 129 (2014) 98–113 99

its multiple islands and peninsulas, and numerous waterways(Silva and Prego, 2002). Formed by erosion, due to the advance-ment and retreat of glaciers in the last ice age, this study areahas a particularly irregular geography (Borgel, 1970–1971), whichmakes direct communication between water masses of oceanic ori-gin and fresh-river water difficult at the head of the continentalfjords. Because fjords are transition areas between rivers andcoastal seas, the terrestrial input is usually relatively high in theinner sea area.

Fjords are fed by freshwater discharges from continental runoff,rivers, and glacial tributaries, which are characterized by lownitrate and phosphate, but high silicic acid concentration. However,they are also fed by oceanic Subantartic waters (SAAW) inputs withelevated nutrient concentration (NO3

� > 12 lM and PO4: >1 lM)(Silva and Guzman, 2006; Vargas et al., 2008, 2011; Gonzalezet al., 2011). This condition results in an inner fjord region with dif-ferent hydrographic characteristics that depend on the volume andthe source of the freshwater inputs (Silva et al., 2001), which mod-ulate the autochthonous primary production and the contributionof terrestrial allochthonous sources (Vargas et al., 2011). Conse-quently, the dissolved (DOM) and particulate organic matter(POM) might originate from both the marine primary productionand the terrestrial land-plants sources transported by rivers andoverland runoff (Sepulveda et al., 2011). For the Chilean fjordregion, primary production has been reported as highly seasonaland limited by the amount of light and nutrients (Iriarte et al.,2007; Gonzalez et al., 2011). Nevertheless, some studies in northernChilean Patagonian fjords have shown strong allochthonouscontribution in both POM and surface sediments associated toriver-plumes areas or those located at the heads of the fjords(Sepulveda et al., 2011; Silva et al., 2011; Vargas et al., 2011).

A better understanding of the sources and composition of POMmay be highly relevant for determining the importance of terres-trial subsidies of POM in fjord ecosystems.

Stable isotopes (d13C, d15N) and C:N ratios have been widelyused for tracing the source and fate of organic matter in aquaticecosystems (Canuel et al., 1995; Graham et al., 2001; Mc Callisteret al., 2006; Alt-Epping et al., 2007; Liu et al., 2007; McLeod andWing, 2007). The analysis of d13C in POC and surface sedimentsmight indicate the origin of organic matter if the sources have dif-ferent isotopic signals (Thornton and McManus, 1994). Due to thecomplexity of organic matter sources in estuarine systems, biogeo-chemical approaches that use multiple techniques are strongly rec-ommended (Canuel et al., 1997; Hu et al., 2006; Waterson andCanuel, 2008). The application of chemical biomarkers to providemore specific and sensitive information rather than bulk elementaland isotopic techniques has become widespread (Bianchi, 2007).Fatty acids have been used extensively for assessing the sourcesand fates of organic matter in marine, coastal, and estuarine eco-systems (Mannino and Harvey, 1999; Meziane and Tsuchiya,2000; Countway et al., 2007; Waterson and Canuel, 2008). In thisstudy, our main objective was to assess the relative contributionsof allochthonous (i.e., terrigenous) and autochthonous sources tothe POM pool along a gradient from Serrano River Basin to the Nel-son Strait, adjacent to the Pacific Ocean, by employing nutrientstoichiometry (N, P, Si:N ratios), isotopic analyses (d13C), lipid bio-markers (fatty acid composition), and standard measurements ofbacterial, protozoan, and phytoplankton carbon biomasses. Theresults of this study on organic matter reservoirs have been com-pared with additional measurements in zooplankton organisms,in order to explore the potential utilization of allochthonous OMin the planktonic food webs of this particular Chilean fjord ecosys-tem. Based on the ultra-oligotrophic nature of Patagonian Rivers,the insignificant riverine autotrophic productivity and theirsubsequent exportation to the fjord environment we hypothesizethat there is a significant contribution (>50%) of allochthonous

terrestrial organic matter signature in the POM and in the zoo-plankton communities inhabiting the surface brackish waters ofsouthern Chilean fjords, which demonstrates a significant terres-trial organic carbon is reaching those fjords.

Methods

Study area

The present study comprises of a large region in Southern Chil-ean Patagonia (from �50�500 to �52�260�S), including the SerranoRiver Basin and the adjacent Última Esperanza-Smyth Fjords (estu-arine–marine system), located approximately 50 km SE of theSouth Patagonian Ice Field (51�S; 72�W, Fig. 1). Sampling was con-ducted during the course of an austral oceanographic researchcruise during the spring of 2009 and during a field survey alongthe adjacent watersheds (i.e. October, 2009).

The Serrano River basin (SRB) is located within the Torres delPaine National Park (A Biosphere Reserve), which covers an areaof approximately 8700 km2 and is comprised of a complex hydro-logical system developed east of the Southern Ice Field (Solari et al.,2010). On the western side of the SRB, melt water from the South-ern Ice Field makes up a system composed of proglacial lakes feed-ing many rivers; the Paine River flows into Lake Nordenskjöld,which in turn drains into Lake Pehoe and then into Lake Del Toro.The main outlet of Del Toro Lake is the Serrano River, while theGrey River links up with the Serrano River which flows into theÚltima Esperanza Fjord (Fig. 1). Most lakes in SRB are characterizedby low anthropogenic intervention (Soto et al., 1994) and the largedeep lakes (Del Toro, Sarmiento, Pehoe, Nordenskjöld) have beencharacterized as oligotrophic (Soto and De los Ríos, 2006; De losríos and Soto, 2009). The terrestrial flora along the basin is mostlydominated by deciduous forest (Nothofagus spp., Drymis winterii,Berberis microphylla, Maytenus disticha, Pernettya pumila, Empetrumrubrum, Sphagnum magallanicum) and Patagonian Magellan Steppe(Festuca gracillina, Stipa humilis, Chilotrichum diffusum, Deschampsiaantarctica) (CADE-IDEPE, 2004).

The Última Esperanza Fjord receives most of its freshwater dis-charges from the SRB, located on the eastern side of its headwatersand from the Balmaceda and Serrano glaciers on the west (Fig. 1).After reaching the fjord, the estuarine water flows into the Almir-ante Montt Gulf and to the Pacific Ocean through several inter con-nected channels such as Kirke, Santa Maria, Union, and Smyth(Fig. 1). The complex bathymetry of this area is characterized bya gradual increase in depth from the east (about 25 m) to the west(600 m). However, in the Kirke Channel, there is a constriction-sillapproximately 50 m deep and �200 m wide, which generates aneastern microbasin (Stn. 55, 54, 53, 52, 51, T1, T2 and T3). The ver-tical distribution of the water’s characteristics (temperature, salin-ity and rt) shows that in general this inlet region is a fairlystratified environment (Silva and Calvete, 2002). The general circu-lation scheme proposed suggests that the brackish surface water ofthe estuaries flows outward from Almirante Montt Gulf, while thedeeper, more saline water from Smyth and Union Channels flowsover the Kirke constriction-sill into Almirante Montt Gulf, fillingits basin (Sievers et al., 2002). The population density at the ÚltimaEsperanza Province is very low (�3 ind km�2; INE, 2012), but mostof the anthropogenic organic matter sources are limited to PuertoNatales town (18,507 inhabitants), some agriculture, tourism, andincipient aquaculture activities.

Hydrography, nutrients and plankton content of biomass

The oceanographic field work, including water, sediment,and marine plankton samples were obtained during the CIMAR 15

Fig. 1. Study area and locations of the sampling stations in Chilean Patagonia from Torres del Paine-Serrano River Basin (SRB) to an inner fjord-open sea channel transect:Última Esperanza Fjord to the more oceanic-influenced Smyth Channel. Spring season of 2009.

Table 1Summary of the physical and chemical values at the stations of study at 1 and 10 m depth in spring of 2009. Salinity, temperature, silicic acid, nitrate and orthophosphate.

Sector Station Surfacesalinity

10 msalinity

SurfaceT (�C)

10 mT (�C)

1 mSi(OH)4

10 mSi(OH)4

1 mNO3

�10 mNO3�

1 mPO4�3

10 mPO4�3

Terrestrial (SRB)Rivers 1 (Paine) 0 6.1 29.3 0.1 0.7

5 (Serrano) 0 8.1 16.0 0.05 0.24Lakes 2 (Nordenskjöld) 0 9.9 22.7 0.1 0.3

3 (Pehoe) 0 11.0 34.3 1.5 0.224 (Grey) 0 7.0 18.7 0.11 0.98

Última Esperanza T3 11.8 13.1 6.0 6.0 16 15 5.7 4.5 0.97 0.74Fjord T2 12.64 12.60 5.9 5.9 15 15 4.8 4.4 0.86 0.73

T1 13.27 13.39 6.3 6.3 13 13 3.0 4.2 0.75 0.83Señoret Channel 51 14.60 14.57 7.2 6.5 7 17 2.2 2.2 0.13 0.2

52 15.3 16.4 6.8 6.6 5 0 1.0 0.3 0.0 0.07A. Montt Gulf 53 16.30 16.28 6.5 6.5 2 0 0.4 0.3 0.0 0.09

54 17.59 17.96 6.8 6.6 4 4 1.6 2.3 0.0 0.06Kirke 55 17.91 17.92 6.3 6.2 1 0 1.5 1.1 0.18 0.1Channel 56 22.55 22.67 6.8 6.7 7 6 6.8 6.7 0.57 0.47Outer Channels 60 (Union Channel) 24.03 24.03 6.6 5.8 4 3 4.9 4.9 0.45 0.42

48 (Smyth channel) 29.27 29.28 7.0 6.8 2 0 3.0 2.3 0.5 0.46

100 A. Lafon et al. / Progress in Oceanography 129 (2014) 98–113

Fiordos expedition on board the R/V AGOR Vidal Gormaz (October12th to 30th, 2009). Twenty-one stations were located along aneast–west oceanographic section, from the headwaters of the Últi-ma Esperanza Fjord (Station T3) up to Smyth Channel (Station 48)(Fig. 1, Table 1). Simultaneously, a terrestrial field study was con-ducted among the rivers and lakes of the SRB (October 29th, 2009),whose freshwater drains into the channels and fjord ecosystem. Fiveriver-lake sampling stations were utilized in the SRB: Paine (Stn. 1)and Serrano (Stn. 5) Rivers and Nordenkskjöld (Stn. 2), Pehoe (Stn. 3)and Grey Lakes (Stn. 4) (Fig. 1).

During the cruise, temperature and conductivity profiles wererecorded with a CTD Seabird 19 Plus. Seawater samples (50 mL)for nutrient analysis were collected at discrete depths (1, 5, 10,25, 50, 75, and 100 m) with a Niskin bottle rosette system. Amoniasamples were measured immediately on board following the

Koroleff method (1976). Samples for nitrate (NO3�), phosphate

(PO4�3), and silicic acid (Si(OH)4) were kept frozen (–20 �C) in

acid-cleaned, high density plastic bottles until their analysis witha nutrient autoanalyzer following Atlas et al. (1971) at the MarineBiogeochemistry Laboratory of the Pontificia Universidad Católicade Valparaíso. Marine sediment samples were taken with a boxcorer, and preserved frozen at �20 �C until processed on land. Dur-ing the field study, fresh water nutrient samples were taken fromthe river and lake surfaces, using a 1.5 m stick with a sampling bot-tle attached at the end. Terrestrial soil samples were taken by handclose to the river and lake shores. Sediment and soil samples weredefrosted, dried (50 �C, 30 h), and filtered by 200 lm mesh sieve.

Water samples from several other fjords were used to deter-mine the abundance of pico-, nano, microplankton, and theirrespective carbon biomasses. The samples were collected at five

Table 2Corg:Ntotal ratio, d13C and d15N values for terrestrial plants, soils, sediments andplankton samples. For vegetation, each value corresponds to a pool of 5 individualplants.

Samples C:N %N %C d15N (‰) d13C (‰)

VegetationGrass (Plantago sp.) 30.7 1.3 40.9 �0.7 �30.5Gunnera magellanica 13.0 3.5 44.9 �0.5 �28.5Dry leaves 50.2 0.9 42.8 2.9 �27.6Mulinum spinosum 15.5 2.9 45.1 �2.7 �27.3Gaultheria mucronata 52.4 0.9 48.4 �7.7 �28.4Berberis microphylla 28.5 1.7 48.9 1.6 �26.5Nothofagus pumilio 17.2 2.7 46.7 �5.4 �28.9Nothofagus antarctica 15.8 2.8 45.0 2.5 �28.7

SoilStation 1 50.2 0.9 42.8 2.2 �28.3Station 3 46.8 0.6 30.3 2.2 �28.3Station 4 57.3 0.7 38.5 �2.4 �29.0Station 5 18.9 0.2 3.2 2.0 �27.9Station T3 23.5 1.7 40.8 0.2 �27.5

SedimentStation 51 6.8 0.3 1.8 7.9 �20.0Station 52 7.0 0.3 2.2 9.0 �21.1Station 53 7.0 0.2 1.5 8.8 �21.2Station 54 7.1 0.2 1.2 8.8 �21.6Station 55 6.5 0.4 2.7 9.9 �21.1Station 56 8.7 0.1 0.5 9.8 �21.2Station 60 8.3 0.2 1.3 9.7 �20.2

ZooplanktonBig copepods (Station 48) 9.3 0.2 2.2 9.4 �22.2Zoea (Station 62) 13.7 0.5 6.8 9.7 �22.4Big copepods (Station 62) 11.1 0.8 9.0 11.9 �22.6Small copepods (Station 60) 7.0 0.2 1.5 11.9 �23.7Zoea (Station 60) 8.6 1.0 8.6 10.9 �22.4Zoea (Station 62) 13.1 0.5 6.8 9.7 �24.4Big copepods (Station 63) 15.9 0.4 6.5 12.6 �25.7Big copepods (Station 54) 11.8 1.1 12.6 11.3 �24.2Amphipods (Station 54) 7.4 5.5 40.6 10.9 �22.6


discrete depths (1, 5, 10, 25, 50 m) and at the Última EsperanzaFjord only at two discrete depths (1, 10 m). In the rivers and lakesonly surface level samples were collected. Picoplankton and nano-plankton samples were preserved in glutaraldehyde (6% w/v in0.2 lm prefiltered seawater) whereas microplankton samples werepreserved in an alkaline solution of 1% Lugol (Levinsen and Nielsen,2002).

Bacterial counting was done by using epifluorescence micros-copy, following the methodology of Porter and Feig (1980). Forthe enumeration of nanoflagellates, 20 mL subsamples were fil-tered on a 0.8 lm polycarbonate membrane filter stained with pro-flavine (0.033% w/v in distilled water) following Haas (1982) andfixed with glutaraldehyde for subsequent analyses. Both bacteriaand nanoflagellates were counted with an inverted microscopeOLYMPUS IX-51 equipped with UV model UMWU2 (width bandpass 330–385 nm) and FITC model U-MWB2 (width band pass450–480 nm) filter sets. PNF cells were identified by autofluores-cence. Biovolumes were converted to carbon content measure-ments using the equation of Chrzanowski and Simek (1990).Subsamples of 50 mL were allowed to settle for 24 h in Utermöhlsedimentation chambers before diatoms, dinoflagellates and cili-ates were identified and counted under a Carl Zeiss AXIO invertedmicroscope using the software AxioVision 4 for measurements.Plasma volumes were calculated (Edler, 1979) and averaged 30cells per species. We assumed carbon:plasma volume ratios of0.11 pg C lm�3 for diatoms (Edler, 1979), 0.3 and 0.19 pg C lm�3

for heavily thecate and athecate dinoflagellate forms, respectively(E.J. Lessard, unpubl. data fide Gifford and Caron, 2000), and0.148 pg C lm�3 for ciliates (Ohman and Snyder, 1991).

Sampling and analytical methods for isotopic and lipid analysis

Plant tissue (mostly apical foliage, but also including somestem) and soil samples were collected upstream along the banksof the SRB and processed in the laboratory. Cleaned samples weredried to constant weight at 50 �C (30 h), homogenized and groundto a fine powder with an agate mortar and pestle. All material forstable isotopes was acid-fumed overnight with HCl 5%, subse-quently dried again at 55 �C, and held in a desiccator until analyses.

Water samples (5 L) for d13C, d15N and fatty acid analysis werecollected from near surface levels from rivers and lakes, and at 1and 10 m deep for samples collected in channels and fjords. Allof the water samples were pre-screened through a 200 lm sieveto remove any zooplankton or algal debris. Seston was then col-lected by vacuum filtration through pre-combusted (4 h at450 �C) MFS GF/G glass fiber filters (0.7 lm nominal pore size).Zooplankton samples were collected by oblique tows using aTucker trawl net (1 m2 mouth area, 300 lm mesh size) within a0–100 m depth stratum. Material for stable isotope analyses wasimmediately frozen onboard at �20 �C for a few days until sortingat the laboratory. From 100 to 200 copepods of small (<1 mmlength) and big copepods (>2 mm length) of the genus Calanus,Metridia, Acartia and Pseudocalanus, �30 amphipods, �30 zoea,�5 euphausiids were sorted and processed. The subsample ford13C analysis was washed with diluted HCl to remove carbonatesand redried. However subsamples for d15N analysis did not receivethis treatment, as it has been reported to affect d15N values (Bunnet al., 1995). Sediment and soil samples followed the same proce-dure prior to analysis.

Stable carbon and nitrogen isotope ratios were measured on aPDZ Europa Scientific 20/20 Mass Spectrometer with a 120� triplecollector mass spectrometer designed specifically for continuousflow analysis at the Center for Stable Isotope Biogeochemistry,UC Berkeley. Isotopic values were expressed in parts per thousandas deviations from standards (PDB for d13C and N2 in air for d15N).Results are presented in standard d notation.

The allochthonous vs. terrigenous relative proportions in POMand sediment samples were calculated according to their d13C con-tents, using a two-source-mixing equation (Bianchi, 2007). Themarine end member values (�20‰) were obtained from other oce-anic stations in Chilean Patagonian fjords (Sepulveda et al., 2011;Silva et al., 2011; Vargas et al., 2011). The terrestrial-vegetationend member value was obtained in this study (�29.37‰), andwas found to correspond to the mean isotopic signature betweenNothofagus spp and grasses, which are the dominant vegetationin the area (Table 2).

Zooplankton, glass fiber filters with POM, plant tissues and soilsamples were dried again at 50 �C for 24 h and held in a desiccatoruntil analyzed. Fatty acid analysis was performed in the Institute ofPharmacology at the Universidad Austral de Chile, in Valdivia,Chile. The fatty acid concentration was analyzed after extractionand methylation (Kattner and Fricke, 1986) with a Perkin ElmerSigma 300 chromatograph equipped with a programmable tem-perature vaporizer-injector, a fused Omegawax 53 capillary col-umn, and a flame ionization detector.

To determine the principal sources of organic matter to POC, therelative percentages of some biomarkers were used as source indi-cators. C15:0, was used for bacterioplankton (‘‘bacteria’’) (Mancusoet al., 1990; Kaneda, 1991; Canuel et al., 1995; Pancost andSinninghe, 2003; Hu et al., 2006), and poli-unsaturated fatty acids(PUFA) for phytoplankton and zooplankton labile OM sources(‘‘plankton’’) (Mayzaud et al., 1989; Colombo et al., 1996; Budgeand Parrish, 1999; Reuss and Poulsen, 2002; Dunn et al., 2008;Van der Meersche et al., 2009), and even-numbered long-chainfatty acids (ELCFA) > C24 for terrestrial sources associated withvascular plants (Ohkouchi et al., 1997). We also use the TARFA


index, as a measure of the sum of long chain even numbered satu-rated fatty acids compared to short chain even numbered saturatedfatty acids (modified from Meyers, 1997 fide Bianchi and Canuel,2011), representing terrestrial and marine (algal/plankton)sources.

Statistical differences of Corg/N, d13C, d15N in POM, nutrients,plankton biomass and vegetal tissue were carried out using thesoftware package Statistica 7.0 (StatSoft Inc., USA). One-wayANOVA and factorial ANOVA at 95% significance level were appliedin order to show differences between terrestrial and marine envi-ronment, between sectors and by depth. Then, an Unequal N HSDtest was used to estimate significant differences between groupmeans. For some analysis the stations were grouped according tofollowing areas: ‘Lakes’ (Stn. 2, 3,4), ‘Rivers’ (Stn. 1, 5), ‘Estuary’(Stn. T1, T2, T3), ‘Puerto Natales’’ (Stn. 51, 52), ‘‘Almirante MonttGulf’’ (Stn. 53,54), ‘Kirke Channel’ (Stn. 55, 56), and ’Outer chan-nels’ (48, 60) (see Fig. 1). Statistical power analysis for One-wayANOVA was conducted in R (Ver. 2.15.1), (Cohen, 1988).

A Kruskal–Wallis test was applied to the fatty acids in zoo-plankton data using the software package Statistica 7.0 (StatSoftInc., USA) in order to compare ELCFA, MUFA and PUFA contentsbetween external stations and Almirante Montt Gulf stations.

Results

Hydrographic conditions

Samples were collected over a wide range of environmentalconditions (Table 1). The results indicate that the influence of thefreshwater discharged into the fjord system gives rise to a lowsalinity surface layer (i.e. <14 psu; 0–30 m deep) in the ÚltimaEsperanza Fjord (<14 psu), which flows into the Almirante MonttGulf area and on to the ocean, where its salinity increases up to28 psu, as it mixes with the saltier (>33 psu) oceanic Sub AntarcticWater (SAAW), flowing into the fjords (Fig. 2A). As the SAAW flowsinto the fjords below surface level, it mixes with fresher surfacewater flowing out toward the ocean, giving origin to ModifiedSub Antarctic Water (MSAAW) demonstrating salinities between32 and 33 psu and Estuarine Water (EW), with salinities lower than32 psu (Sievers and Silva, 2008; Fig. 2A). The sub-surface portion ofthe EW flows inwards up to the Kirke constriction-sill where flowis constricted and only the upper layer flows over it, filling theAlmirante Montt Sound micro-basin with salinities between 20and 24 psu.

In general, mean temperatures from lacustrine-river waterswere slightly higher than the fjord surface waters (8.4 vs. 6.5 �C;Table 1). Nevertheless, the fresh river waters flowing through theÚltima Esperanza Fjord should result in lower temperatures atthe headwaters, since they come from the Balmaceda Glacier andthe Campos de Hielo Sur Glacier (Stn, T3; Fig. 2B; Table 1). Thefjord’s brackish surface waters were well oxygenated(7.1–7.8 mL L�1) and decreased progressively with depth(<6 mL L�1 at 50 m, Fig. 2C).

Si(OH)4 concentrations in the upper surface layer were signifi-cantly different between the terrestrial and marine stations(one-way ANOVA, F = 11.23, df = 1, p = 0.005). Ner the mouth ofthe Serrano River, in the lacustrine-river environment, Si(OH)4 con-centrations were high (16–29 lM, with the lowest value at Stn. 5(Table 1). In the upper 10 m of surface water in the fjord, the high-est Si(OH)4 concentration was observed at the Última EsperanzaFjord (�13–16 lM). However, its concentration decreased in direc-tion to Señoret Channel and to the more oceanic-influenced sta-tions (<1 lM; Fig. 2D). Si(OH)4 concentration increases withdepth; nevertheless, the Kirke constriction-sill allows the originof an horizontal concentration difference between the Smyth-Kirke

micro-basin (�4–8 lM) and the Almirante Montt micro-basin(�8–70 lM) (Fig. 2D). PO4

�3 concentrations at the upper surfacelayer were significantly different between the terrestrial and mar-ine stations (one-way ANOVA, F = 7.66, df = 1, p = 0.015), but nosignificant differences were found for NO3

� concentrations (one-way ANOVA, F = 2.58, df = 1, p = 0.131, power = 0.07). The surfacePO4�3 and NO3

� concentrations at the SRB ranged between 0.22–0.98 lM and 0.05–1.5 lM, with the highest values at Stn. 4 andStn. 3 respectively. In the fjord’s surface layer (�0–10 m depth),the highest concentrations of PO4

�3 and NO3� were recorded in the

Última Esperanza Fjord (0.73–0.97 lM and 4–6 lM, respectively),(Table 1; Fig. 2E and F). In the Señoret Channel and AlmiranteMontt Gulf area, both nutrients decreased, giving origin to a mini-mum concentration layer of <0.2 lM and <2 lM, respectively. Inthe sample areas located near the mouth of the fjord, these valuesincreased slightly to >0.4 lM and >2 lM (Fig. 2E and F). Below thesurface layer, the PO4

�3 and NO3� nutrient concentrations increased

with depth, much like the levels of the Si(OH)4. Nevertheless, theKirke constriction-sill allows the origin of an horizontal concentra-tion between the Smyth-Kirke micro-basin (�0.8–1.6 lM and �8–16 respectively) and the Almirante Montt micro-basin(�0.8–2.4 lM and �8–20 respectively) (Fig. 2E and F). The NH4

+

concentrations across the inner fjord-open sea channel transectranged between 0.16 and 2.68 lM, with the highest concentrationsin the surface layer of the Smyth Channel (Stn. 48; >2.4 lM) andthe Señoret Channel (Stn. 51; >1.6 lM) (Fig. 2G). These concentra-tions were relatively low in all the other sampling stations(�0.2–0.8 lM).

Pico-nano and microplankton biomassThe study period was characterized by a low plankton biomass

in most of the sampled stations (Fig. 3A and B). Bacterial carbonshowed a higher contribution to the total carbon biomass of theplankton sampled in the freshwater environment (54.3–93.1%)than found in the adjacent marine-fjord areas (18–61%) (one-wayANOVA, F = 29.59, df = 1, p = 0.00009), where the highest valueswere observed at Stn. 5, Stn. T3 and Stn. 48 (Fig. 3A).

Bacterioplankton biomass ranged between 10.8 and118.2 lgC L�1. At the surface level no differences were foundbetween the terrestrial and fjord environments (one-way ANOVA,F = 2.94, df = 1, p = 0.108, power = 0.20). Nanoflagellates werescarce in terms of biomass along the rivers and lakes (0.2–11.2 lgC L�1), although their presence was more significant inthe fjords (10.7–49.8 lgC L�1) (one-way ANOVA, F = 6.273, df = 1,p = 0.025) (Fig. 3A). No differences were found in the quantity ofbacteria biomass nor in the abundance of nanoflagellates biomassbetween the surface and 10 m depth of the fjord (one-way ANOVA,F = 0.75, df = 1, p = 0.399, power = 0.19) (one-way ANOVA, F = 0.12,df = 1, p = 0.73, power = 0.1). There were also no significant differ-ences in bacteria biomass (one-way ANOVA, F = 1.62, df = 4,p = 0.215, power = 0.21) or nanoflagellates biomass (one-wayANOVA, F = 2.14, df = 4, p = 0.120, power = 0.40) between differentsectors of the fjord.

At the surface significant differences were found in the totalbiomass of microplankton between terrestrial and marine environ-ments (one-way ANOVA, F = 4.92, df = 1, p = 0.044), with lower bio-mass in the terrestrial stations (0.56–12.51 lg L�1 and 27.21–341.02 lg L�1 respectively). In the fjord, the total biomass ofmicroplankton groups varied among the different study sites, butnot between depth (one-way ANOVA, F = 5.064, df = 4, p = 0. 007and F = 0.0002, df = 1, p = 0.997, power = 0.1 respectively). A higherbiomass was discovered at Almirante Montt Gulf and its outerchannels (e.g. Unión and Smyth), while a lower biomass wasobserved at the Última Esperanza Fjord, Señoret and Kirke chan-nels (Fig. 3). Among the plankton groups there were also significantdifferences (i.e. factorial ANOVA, F = 42.949, df = 3, p = 0.0000). The

Fig. 2. Vertical oceanographic section of (A) salinity, (B) temperature (�C), (C) dissolved oxygen (mL L�1), (D) silicic acid (lM), (E) phosphate (lM), (F) nitrate (lM), and (G)ammonium (lM), across an inner fjord-open sea channel transect, from Última Esperanza Fjord to the Smyth Channel. Spring season of 2009.


most abundant microplankton groups were ciliates (e.g. Mesodini-um, Strombidium), followed by dinoflagellates (e.g. Alexandrium,Protoperidinium, Dinophysis, Gyrodinium, Heterocapsa), and

different diatom genera (e.g. Thalassiosira, Rhizosolenia, Stepha-nopyxis, Guinardia, Melosira, Fragilaria, Cocconeis). Statistical analy-sis showed differences between test sites and microplankton

Fig. 3. Biomass (lgC L�1) of the major taxonomics groups of planktonic autotrophic and heterotrophic carbon along a land-ocean section from SRB to the outer oceanic fjordstations in southern Chilean Patagonia at (A) 1 m depth and (B) 10 m depth.


groups (factorial ANOVA, F = 17.0184, df = 4, p = 0.00000;F = 42.9488, df = 3, p = 0.00000; ‘sector’ � ‘microplankton’ interac-tion F = 16.58, df = 12, p = 0.0000), and ciliates contributed themost to total biomass. However, these differences were evidentonly in the Señoret Channel and Almirante Montt Gulf stations,whereas significant differences in plankton groups were notobserved at other sites. The highest ciliate biomass was observedat Stn. 53 (311 lgC L�1 at 10 m depth), where it accounted formore than 80% of the total biomass (Fig. 3B). Dinoflagellates wereabundant in more oceanic-influenced stations (Stn. 48 and St. 60),with a biomass of around 111 lgC L�1, which comprised 50% oftotal biomass. Diatom biomass was higher in surface waters ofthe more oceanic areas (Stn. 48, 106 lgC L�1), making up 23%of total microplankton biomass, while having a minimal presencein the area of Almirante Montt Gulf and Kirke Channel (Fig. 3A).

Carbon isotopic composition in terrestrial vegetation, POM and surfacesediments

The results showed large variability in the isotopic compositionof primary producers and soil samples collected across the habitatmatrix of the SRB. The estimates of d13C and d15N in terrestrial pri-mary producers (including herbs, shrubs and trees leaves), rangedbetween�30.5‰ to �26.5‰ and �7.7‰ to 2.9‰ respectively, witha carbon and nitrogen percentage of 42.8–48.7% and 0.9–3.5%respectively (Table 2). The C:N ratio of plant samples were widelyvariable, ranging from 13 in Gunnera magellanica (i.e. a perennialherb) to 52.4 in Gaultheria mucronata (i.e. a shrub with coriaceousleaves). The one-way analysis of variance did not show significantdifferences in the mean of d13C (F = 3.02, df = 2; p = 0.159,power = 0.54) or d15N (F = 0.19, df = 2, p = 0.835, power = 0.057)among the different plant groups. Surface soil samples, near lakesand rivers, showed a d13C and d15N from �29.0%0 to �27.5%0 and�2.4‰ to 2.2‰ respectively, with ratio of carbon to organic nitro-gen between 18.9 and 57.3 (Fig. 4A, Table 2).

In the surface layer (surface to 1 m depth) the C:N ratio in POMwere highly variable across the river-lakes-estuary-fjord contin-uum, ranging from 7.8 to 30.5 (Fig. 4B), with lower values at theStn. 4 and 5 in the complex SRB and in the stations located atthe mouth of the fjord (Stn. 55, 60). The differences in the C:N ratioin POM between freshwater and marine ecosystems were not

statistically different (one-way ANOVA, F = 1.34, df = 1, p = 0.26,power = 0.13) (Fig. 4C).

d13C-POC ranged between �29‰ and �23.7‰ from freshwaterto marine stations, being significantly different among samplingstations at surface levels (one-way ANOVA, F = 6.996, df = 1,p = 0.019). Clearly, rivers and lakes showed the most depleted val-ues. In contrast, in fjords and channels, there were no significantdifferences in d13C values between depths (one-way ANOVA,F = 2.62, df = 1, p = 0.12, power = 1). Levels of d13C were found tobe different among sectors within the fjord system (one-wayANOVA, F = 3.73, df = 4, p = 0.023). According to the Unequal NHSD test, the Almirante Montt Gulf exhibited the most differentd13C in POC. In general, d13C values were more enriched in theouter fjord stations (e.g. Smyth Channel, Stn. 48) (Fig. 4B and C).

The d15N isotope signature found in surface waters suggest atendency to become more positive closer to the mouth of the fjord.In fact, it also showed statistically significant differences betweenmarine and the terrestrial environments (one-way ANOVA,F = 10.85, df = 1, p = 0.053). We did not find any significant differ-ences in d15N values between depths (one-way ANOVA,F = 0.0001, df = 4, p = 0.99, power = 0.1) or test sites throughoutthe fjord environment (one-way ANOVA, F = 0.36, df = 4,p = 0.831, power = 0.1). However, it was clear there were slightlyhigher d15N values (>3‰) for the Stations 52 and 54 (1 and 10 mdepth) (Fig. 4B and C).

According to the two-source-mixing model estimations, thepercentage of allochthonous terrestrial carbon varied between81% and 96% at the SRB complex. In the adjacent fjord environ-ment, the proportion of terrestrial organic carbon was slightlyhigher at 10 m depth than at the surface layer (Fig. 4). At the wholesampling stations situated within the fjord system, the terrestrialOM percentage was equal to or higher than 70%, with the excep-tion of Stn. 48, which mixed most directly with oceanic watermasses (40–58% at 1 m and 10 m depth respectively). Higher val-ues were observed between the A. Montt Gulf and Señoret Channelstations (70–96%) (Fig. 5).

Surface sediment organic C and N values ranged from 0.5% to2.7% and 0.1% to 0.4% dry wt., respectively (Table 2). Spatial varia-tions of the C:N ratio along the fjord ranged between 6.5 and 8.7closer to marine reference values. In contrast with the POC in sur-face and sub-surface waters, the contribution of terrestrial organic

Fig. 4. C/N ratio, d13C and d15N along a land-ocean section from SRB to the outer oceanic fjord stations in the Southern Chilean Patagonia. (A) Terrestrial soils and marinesediment; (B) POM at 1 m depth; (C) POM at 10 m depth.

Fig. 5. Salinity and relative contribution (%) of allochthonous-terrestrial organic matter in POM and sediment along a land-ocean section from SRB to the outer oceanic fjordstations in the Southern Chilean Patagonia. Samples of POM were collected at 1 and 10 m depth.


carbon to surface sediments was relatively low along the fjord eco-systems, with a contribution lower than 20% (Fig. 5).

Fatty acids compositionThe concentration of total fatty acids (FAs) in plant samples ran-

ged from 415 to 4276 lg g�1, where the lowest values were foundin Melinum spinosum and Berberis microphylla (i.e. shrubs), and thehigher values in Gunnera magellanica and Nothofagus leaves. Themajor FAs group in vegetation were ELCFA (25.38–87.6%), followed

by C16:0, C18:(1n-9), C18:3(n-3), C18:2(n-6) and C18:00. Themajor FAs groups in soil samples were PUFAs (49.4–65.6%), andELCFA (17.5–28%).

FA concentration in POM ranged from 3.4 to 14.2 lg L�1 (Fig. 6)and no significant differences were found between 1 and 10 mdepth at the fjord (one-way ANOVA, F = 2.761, df = 1, p = 0.112,power = 0.35). The highest values were recorded in surface watersbetween the Señoret Channel and the Almirante Montt Gulf sta-tions (8.9–14.2 lg L�1 respectively), and two stations situated in

Fig. 6. Fatty acids (lg L�1) concentrations of POM sorted by stations at 1 m depth in POM at (A) 1 m depth and (B) 10 m depth, along a land-ocean section from SRB to theouter oceanic fjord stations in the Southern Chilean Patagonia. SAFA means saturated fatty acids, MUFA Monounsaturated fatty acids, PUFA Polyunsaturated fatty acids andELCFA Even long chain fatty acids.


Pehoe and Grey Lakes (Stn. 3 and Stn. 4 with 10.3 and 12.8 lg L�1

respectively) (Table 3).In the fjord surface waters, the highest proportion of fatty acids

corresponded to saturated fatty acids SAFA (24.6–69.9%) followedby PUFA (24.6–60.4%) (Fig. 6A). Even long-chain fatty acids (ELCFA)accounted for the largest percentage of SAFA and were moreprevalent in the Almirante Montt Gulf and the Señoret Channel(52.3–67.6%), where they comprised >91% of the total SAFA. Thecontribution of polyunsaturated FA (PUFA) to total FA concentra-tion varied among the different stations between 24.6% and60.5%, where eicosapentanoic acid (C20:5(n-3)) was the dominantcompound. In subsurface waters at 10 m depth, FA concentrationswere slightly lower than surface waters (Fig. 6B), but PUFA concen-tration still maintained concentrations between 1.9 and 5 lg L�1

(39.1–71.3% of the total FA), whereas concentrations of SAFA andELCFA decreased drastically to levels under 29.7% and 48.9%respectively (Fig. 6B).

In surface freshwaters of the SRB, both the index TARFA and thehigh contribution of ELCFA suggested an important input of allo-chthonous OM along the river basin continuum (Figs. 6A and 7A).In the adjacent fjord ecosystem, this terrestrial contribution washigher between the Almirante Montt Gulf and the Señoret Channelareas (TARFA = 3.7–9.6; ELCFA = 50–66%). In subsurface waters,both the TARFA index and contribution of ELCFA to the total FAshowed lower values than found in surface waters (Figs. 6B and7B). Nevertheless, FAs associated with planktonic sourcesincreased substantially from 23% to 58% at 1 m depth to 36% to69% at 10 m depth. Both in surface and subsurface waters, the bio-markers potentially derived from bacterial sources were negligiblein all sites (<1%) (Fig. 7A and B).

Zooplankton organisms

The overall values of d13C values in zooplankton samples wereslightly enriched than the range of the d13C-POC recorded in thisstudy (�25.7‰ to �22.2‰ vs. �29‰ to �23.7‰). The d15N valuesranged between 9.4% and 12.6‰ (Fig. 8E, F, Table 2). By using the

d13C two-source mixing model, terrestrial organic carbon contribu-tion for zooplankton samples ranged between 28% and 45% in theAlmirante Montt Gulf, between 24% and 40% in the Smyth-UnionChannels and between 28% and 61% in Stn. 62 and 63 (outer fjordchannels, Fig. 1).

The concentration of total FAs in copepods ranged from 216.9 to287.6 lg individual�1 in copepods, 380.6 lg individual�1 in eup-hausiids and 641.4 lg individual�1 in amphipods (Table 4). Eicosa-pentanoic acid (C20:5(n-3)) accounts for 32.2–39% of total FAs incopepods, around 37% in euphausiids and 17.6% in amphipods.ELCFA reported 14.5–14.6% in copepods from stations located nearthe mouth of the fjords (48, 60, 62, 63). In the Almirante Montt Gulfstations, the ELCFA concentration was higher, reporting 33.9% incopepods, 22.14% in euphausiids and 17.6% in amphipods.

A Kruskal Wallis analysis showed significant differences inELCFA content between zooplankton from both external stationsand Almirante Montt Gulf stations (H = 4.5, p < 0.05) but no signif-icant differences were found in MUFA, PUFA, plankton biomarkersor bacteria biomarkers.

Discussion

Main sources of Particulate Organic Carbon in the study area

The POM in estuaries originates from heterogeneous allochtho-nous and autochthonous sources. Its composition varied spatiallyand temporally according to the relative importance of each sourcewithin the individual estuary (Maksymowska et al., 2000). Never-theless, for inland waters in the study area, it is clear that, giventhe oligotrophic conditions of the watershed, the autotrophic pro-duction in the river basin is almost insignificant. However, it is pos-sible that some benthic algae contributed to autochthonous carbonproduction. Therefore, allochthonous contribution based in d13Cvalues could have been over-estimated. In fact, allochthonous con-tribution based on fatty acid analyses suggests a mean rangebetween 20 up to 54% of the POM, in contrast with ca. 70–90%based in d13C estimates.

Table 3Fatty acids concentrations of POM at 1 and 10 m depth (lg L�1) in different sectors of the study area.

Area Outer Channels Kirke Channel A. Montt Gulf Señoret Channel Última Esperanza Fjord SRB

Stations 48 48 60 60 56 56 55 55 54 54 53 53 52 52 51 51 T1 T1 T2 T2 T3 T3 5 4 3 2 1Depth 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 10 m 1 m 1 m 1 m 1 m 1 m

C12:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C14:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C15:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C16:0 0.3 0.4 0.4 0.5 0.5 0.4 0.2 0.3 0.5 0.7 0.3 0.3 0.3 0.3 0.6 0.6 0.4 0.3 0.2 0.5 0.2 0.5 0.5 0.9 0.6 0.5 0.5C16:1 0.2 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.1 0.1 0.0 0.1 0.1 0.1 0.0 0.0 0.1 0.0 0.1 0.1 0.1 0.1 0.1 0.1C17:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C17:1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C18:0 0.1 0.3 0.2 0.2 0.2 0.1 0.1 2.0 0.2 0.7 0.1 0.1 0.1 0.1 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.2 0.2 0.3 0.2 0.2 0.2C18:1 n-9 0.4 0.8 0.4 0.5 0.4 0.4 0.2 0.3 0.5 0.6 0.3 0.3 0.3 0.2 0.6 0.5 0.4 0.2 0.2 0.5 0.2 0.4 0.5 0.8 0.5 0.4 0.4C18:2 n-6 0.2 0.3 0.1 0.2 0.2 0.1 0.1 0.2 0.2 0.2 0.1 0.1 0.3 0.1 0.2 0.2 0.1 0.1 0.1 0.2 0.1 0.2 0.2 0.3 0.2 0.2 0.2C18:4 n-3 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.1 0.2 0.1 0.1 0.1C18:3 n-3 0.1 0.1 0.2 0.2 0.2 0.2 0.0 0.1 0.2 0.3 0.1 0.2 0.1 0.2 0.3 0.3 0.2 0.1 0.1 0.2 0.1 0.2 0.3 0.4 0.3 0.2 0.2C20:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0C20:1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0C20:4 n-3 0.2 0.2 0.2 0.3 0.2 0.2 0.1 0.1 0.3 0.3 0.1 0.2 0.1 0.1 0.3 0.3 0.2 0.1 0.1 0.3 0.1 0.2 0.3 0.4 0.3 0.2 0.2C22:0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0C22:1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C20:5 n-3 3.5 1.4 2.0 2.4 2.2 1.9 2.3 1.4 2.4 3.2 1.4 1.6 2.0 2.4 2.9 2.8 1.9 1.2 1.1 2.4 1.2 2.3 2.6 4.1 2.7 2.2 2.3C22:3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0C22:6 n-3 0.8 1.0 0.5 0.6 0.5 0.5 0.4 0.4 0.6 0.7 0.3 0.4 0.9 0.3 0.7 0.7 0.4 0.3 0.3 0.6 0.3 0.5 0.6 1.0 0.6 0.5 0.5C24:0 0.3 0.8 0.3 0.3 0.3 0.2 0.2 0.2 0.3 0.4 0.2 0.2 0.3 0.1 0.4 0.4 0.2 0.2 0.1 0.3 0.1 0.3 0.3 0.5 0.3 0.3 0.3C24:1 0.3 0.3 0.3 0.3 0.3 0.2 0.2 0.2 0.3 0.4 0.2 0.2 0.2 0.2 0.4 0.4 0.2 0.2 0.1 0.3 0.2 0.3 0.3 0.5 0.3 0.3 0.3C26:0 0.2 0.2 0.2 0.3 0.3 0.2 0.2 0.2 0.3 0.4 0.2 0.2 0.2 0.2 0.3 0.3 0.2 0.1 0.1 0.3 0.1 0.3 0.3 0.5 0.3 0.3 0.3C28:0 1.0 0.1 0.1 0.0 0.1 0.2 0.9 0.1 2.5 0.5 2.8 0.1 0.7 0.0 3.4 0.0 0.1 0.1 1.4 0.1 0.1 1.0 0.0 2.2 0.1 0.1 0.3C30:0 0.0 0.0 0.2 0.0 0.0 0.4 0.3 0.0 1.5 0.0 1.5 0.0 2.0 0.0 1.7 0.0 0.0 0.0 0.9 0.3 0.7 0.2 0.0 0.0 0.1 0.1 0.2C32:0 0.0 0.0 0.0 0.0 0.0 0.4 0.1 0.0 1.2 0.0 1.0 0.0 5.9 0.0 1.2 0.0 0.1 0.1 0.7 0.0 0.0 0.1 0.4 0.2 0.4 0.0 0.0

A.Lafon

etal./Progress

inO

ceanography129

(2014)98–

113107

Fig. 7. TARFA index and relative contributions (%) of terrestrial, planktonic and bacterial sources to POM along a land-ocean section from SRB to the outer oceanic fjordstations in the Southern Chilean Patagonia at (A) 1 m and (B) 10 m depth. The relative contributions of sources were estimated from fatty acids biomarkers concentrations.


The fjord area seems to be a large reservoir of allochthonous OMdue to the edaphic organic matter that is generated by the localforests and mixed with the fjords, due to rain-induced surface run-off. The mouth of the Serrano River receives an average rainfall of1550 mm year�1, while the average rainfall at Torres del Paine was726 mm year�1 between the years 1983 and 2008; (INE, 2012). Infact, the Serrano River receives freshwater from the entire SRB,which flows into the Última Esperanza Fjord, (annual average flowof 394 m3 s�1; INE, 2012).

The influence of the seaward extension of the allochthonousorganic matter at the Última Esperanza-Smyth fjord is reflectedin several variables: d13C, C:N ratio, salinity, silicic acid and thecomposition of POM by fatty acids. This is seen when these vari-ables are plotted as a function of the distance from the headwatersof the fjord (Figs. 2, 4 and 5). In this area, most of the vegetation ischaracterized as Caducifoli Magellanic forest and the EvergreenMagellan forest (C-3 type). Within rivers and lake surface waterand soil samples, d13C values were depleted in the SRB (Fig. 4A,Table 2). In the adjacent marine system, d13C values at surfaceand/or sub-surface estuarine waters remain depleted (<�26‰)along the entire transect sampled, with the exception of the Stn.48, which is located closest to the open sea (�23.71‰ and�25.46‰ respectively).

Depleted d13C values at the headwaters of the fjords, or areas ofrestricted circulation, are described in a number of other estuariesand fjords systems studies. This situation has been attributed to ahigh contribution of organic matter from vascular plants (Goñiet al., 2005) or to an increase in riverine discharges that resultsin isotopically lower d13C values. Similarly, in our study, it seemedrelated to a substantial terrestrial input, probably from thesurrounding vegetation and low phytoplanktonic production in

the oligotrophic riverine freshwater. Another contributing factorthe restricted circulation associated with shallow sills and deepmicro-basins. In general, the higher C:N ratios and lower d13C val-ues indicated that the OM origin is mainly from terrestrial sourcesand lower C:N ratios and higher d13C values suggest a more prom-inent OM input derived from algae (Lü and Zhai, 2006). Theobserved values from both variables (Fig. 8 A and B) suggest amix of terrestrial and marine input, with a large influence of theallochthonous sources in the POC fraction that was associated withthe upper layer of the water column (upper 10 m depth). This mayconstitute a significant terrestrial contribution to the fjord ecosys-tem. This hypothesis is also supported by the results of a simpled13C two-source mixing-model that suggest that more than 70%of organic carbon is derived from terrestrial sources. The area withsignificant terrestrial OM contribution extends 120 km from thehead of the fjord (i.e. Station 60), After which the allochthonousinput decreased down to 40% as it near the ocean (Fig. 5). Never-theless, the values measured during our study are still higher thanthe values reported by Vargas et al. (2011) for more oceanic-influ-enced channels in the northern and central areas of Patagonia(Table 5). Fatty acid composition also showed that POM wasmainly derived from both terrestrial and phytoplankton organicmatter and, to a lesser extent from bacterial sources (Fig. 7A andB). This contrasts with the dominance of heterotrophs and a rela-tively lower diatom and nanoflagellate biomasses.

Our study also indicates the importance of hydrographic andbathymetric basin properties in modeling the extent of allochtho-nous organic matter that influences Patagonian fjords (i.e. from thefjords headwaters to the adjacent oceanic area). The spatial extentof this influence depends on the local contribution of freshwaterrunoff, as well as the complex system of current flow modulated

Fig. 8. C/N ratio, and stable isotopes signature (d13C and d15N) in: POM and surface sediments (A, B), Zooplankton and surface sediments (C, D), and Vegetation and soil (E, F)measured in this study. The graphs also show terrestrial and marine end members.


by sills and straits in sounds and channels. Fjord sills are also char-acterized by the presence of distinct temperatures, salinity anddensity fronts (Sievers et al., 2002), which might create areas withenhanced POM concentration. The highest fatty acid concentrationobserved in the micro-basin associated with the Señoret Channel,is consistent with other studies that point to the frontal areas asbeing highly concentrated in OM (Silva et al., 2001). This is alsosupported by salinity profiles that evidence a high water columnstratification at Stations 56 and 55 (i.e. where the Kirke constric-tion-sill is situated), which indeed produced a salinity horizontalfront with the surface water flowing outward of the micro-basin.This front seems to produce a POM accumulation with a large ter-restrial contribution in the surface waters of the micro-basin(Figs. 6 and 7). In fact, ELCFA associated with terrestrial-vascularplants sources are present even at stations near to open ocean(i.e. 200 km from the head of the fjord), suggesting the significantspatial extent of allochthonous OM across the land-oceancontinuum.

Sources of OM in surface sediments

Typically, d13C values in marine surface sediments increasefrom the headwaters to the mouth of the fjords, as reported in Chil-ean Patagonia by Canada, USA, and Scotland (Thornton andMcManus, 1994; Louchouarn et al., 1999; Walsh et al., 2008;Aracena et al., 2011; Silva et al., 2011) (Table 5). Terrigenousorganic matter originating from terrestrial vegetation is more

refractory and has a longer retention rate in estuarine sedimentsthan planktonic organic matter (Maksymowska et al., 2000). How-ever, the bulk of C:N and isotopic values in surface sediment fromthe Señoret Channel to the outer channels showed that the mainOM contribution came from marine rather than edaphic contribu-tions from the surrounding forest (Figs. 5 and 8C–F). The C:N ofmarine sediments (C:N = 6.6–8.7) was lower than our OM samples(C:N = 7.8–34), which suggests that terrestrial inputs are negligible(Fig. 4A). This conclusion is also supported by the values of d13Cand d15N that showed ranges closer to the marine end-member.Our results are consistent with a very low contribution of OM fromterrestrial sources (<20%) in the surface sediments of southernChilean Patagonian channels (Aracena et al., 2011). This has alsobeen reported by other studies of fjord ecosystems worldwide.For example, the Puget Sound fjords in Washington (USA) andthe margin zone between USA and Canada (Walsh et al., 2008).Nevertheless, our results contrast from those of Silva et al.(2011), where the allochthonous OM contribution to the sedimentfound at the fjord’s headwaters in the Northern Chilean PatagonianFjords (i.e 42.5–46.5�S) were higher. Their study found terrestrialcontributions between 50% and 97% in the upper 30 km of thefjord. These differences may be explained by a higher terrestrialriver load, since the northern Patagonian Fjord zone has longer riv-ers and is more heavily covered by forest than the study area.

Our results evidence a decoupling between the depleted d13C-POC in surface waters and the levels of d13C in sediment at theAlmirante Montt-Smyth fjord, which can be additionally explained

Table 4Fatty acids concentrations in zooplankton, by sampling station (lg ind�1).

Area Outer Channels Almirante Montt Gulf

Group Copepods Copepods Copepods Copepods Copepods Amphipod EuphausiidsStation 48 62 60 63 54 54 54

n 30 30 30 40 40 30 5C12:0 1.21 1.21 1.20 0.92 0.91 1.22 1.46C14:0 1.18 1.18 1.17 0.89 0.89 1.19 1.44C15:0 1.04 1.05 1.04 0.79 0.79 1.05 1.22C16:0 23.82 23.94 23.69 18.08 18.04 24.09 29.03C16:1 3.73 3.75 3.71 2.82 2.82 3.77 4.50C17:0 1.02 1.03 1.01 0.77 0.77 1.03 1.19C17:1 0.31 0.31 0.30 0.22 0.23 0.31 0.35C18:0 8.54 8.59 8.50 6.48 6.47 8.64 10.41C18:1 n-9 21.24 21.35 21.13 16.12 16.09 21.48 25.88C18:2 n-6 8.05 8.09 8.01 6.11 6.10 8.14 9.75C18:4 n-3 5.89 5.92 5.86 4.44 4.43 5.95 7.11C18:3 n-3 11.42 11.48 11.36 8.67 8.65 11.55 13.90C20:0 1.78 1.79 1.77 1.35 1.35 1.80 2.16C20:1 1.73 1.74 1.72 1.31 1.30 1.75 2.10C20:4 n-3 11.96 12.03 11.90 9.07 9.03 12.10 14.54C22:0 1.68 1.68 1.92 1.27 1.27 1.69 1.90C22:1 0.75 0.75 0.74 0.57 0.56 0.76 0.87C20:5 n-3 111.47 112.04 110.89 84.58 84.43 112.75 135.48C22:3 1.16 1.16 1.15 0.87 0.87 1.17 1.29C22:6 n-3 26.31 26.44 26.17 19.97 19.93 26.61 31.74C24:0 14.34 14.42 14.27 10.71 10.86 14.51 17.24C24:1 14.40 14.47 14.32 10.92 10.78 14.56 16.00C26:0 13.14 13.20 13.07 9.95 9.95 13.27 13.84C28:0 0.00 0.00 0.00 0.00 17.24 238.96 18.83C30:0 0.00 0.00 0.00 0.00 46.13 95.74 18.34C32:0 0.00 0.00 0.00 0.00 0.00 17.30 0.00

Total 286.15 287.62 284.92 216.88 279.89 641.42 380.56

Table 5Geochemistry of POM and surface sediment geochemistry from Patagonia Fjords, other estuaries and fjords and some antropogenic data.

Sample and location Corg (%) TN (%) C:N d13C (‰) d15N (‰) Cterrestrial (%) Source

POMNorthern Patagonia, Chile 5.9–11.2 �22.7 to �18.3 7.7–11.5 Sepulveda et al. (2011)Central Patagonia, Chile �26 to �20.1 24–68 Vargas et al. (2011)Southern Patagonia, Chile 7.82–34.04 �29 to �23.7 �3.6 to 11.3 44.4–96 This studyYork River estuary, USA 4–16* �31.04 to � 20 Countway et al. (2007)Delaware estuary, USA 5–18 �25.8 to �16.4 3.8–18.7 Cifuentes et al. (1988)Delaware estuary, USA 18.7–30 �26.8 to �18.9 Mannino and Harvey (2000)Winyah Bay, USA �30.9 to �25.1 Goñi et al. (2005)Changjiang estuary, China 0.7 ± 0.1 0.13 ± 0.03 5.8 ± 0.8 �22.6 ± 0.9 1.6 ± 0.3 Zhou et al. (2006)

Surface sedimentNorthern Patagonia, Chile 0.5–3.42 0.04–0.38 9.6–16.9 �28.2 to �19.1 1.3–9 3–87 Sepulveda et al. (2011)Northern Patagonia, Chilea 0.1–2.8 0.02–0.41 6.8–16.1 �30.6 to �20.1 1.4–96.7 Silva et al. (2011)Outer channels, Central Patagonia b, Chile 0.2–2.8 0.02–0.41 8.1–9.3 �21.9 to �20.4 6.4–27.7 Silva et al. (2011)Southern Patagonia, Chile 0.5–2.7 0.1–0.4 6.5–8.7 �21.6 to �20 8.8–9.9 0–17.5 This studySouthern Patagonia, Chile 2.75 ± 3.44 7.7–13.4 �22.1 to �19.7 Aracena et al. (2011)Upper Muir Inlet, Canada 0.3 ± 0.03 5.5 ± 0.1 �22.4 ± 0.1 Walinski et al. (2009)Lower Muir Inlet, Canada 0.29 ± 0.0 2.9 ± 0.1 �20.4 ± 1.2 Walinski et al. (2009)Saguenay fjord, Canada �24.8 to �21.8 16–81 Louchouarn et al. (1999)Vancouver Island fjords, Canada 2.4–5.8 9.3–54 �25.6 to �21.2 43 ± 71 Walsh et al. (2008)Washington fjords, USA 0.12–2.2 7.5–17 �21.6 to �20.4 18 ± 11 Walsh et al. (2008)Margin area, USA�Canada 0.11–3.2 9.0 ± 0.1 �24 to �21.6 Walsh et al. (2008)Tay Estuary, Scotland 0.54–5.4 0.1–0.59 9.03–15.71 �26.6 to �23.2 2.6–10.6 Thornton and McManus (1994)

AntropogenicSewage effluent 12.57 �26.7 2.3 Thornton and McManus (1994)

a Corcovado Gulf-Boca del Guafo Gulf to Moraleda Channel – Elefantes Gulf.b King Channel and Pulluche Channel.* Approximate data from Figure 3.


by the local circulation pattern proposed for the study area bySievers et al. (2002). These authors consider that the circulationof the surface layer is predominantly characterized by an offshoreflow, which indeed, might export large amounts of terrestrialorganic matter and terrigenous sediments to the adjacent conti-nental shelf. On the contrary, a deep water flux containing OM ofmarine origin can flow to the inner fjord in the other direction.

Consequently, the terrestrial OM in surface waters would bemostly carried offshore, which prevents its accumulation in thesediments of the inner fjord area. Finally, we have to mention thatour results characterized by low C:N values (<9) and d15N (<10),suggest that the anthropogenic influences in the region are mini-mal. Therefore, this zone could be considered a pristine fjordenvironment.


Allochthonous sources of OM for zooplankton

Information on allochthonous sources of zooplankton in high-latitude fjord ecosystems is scarce, but some studies have sug-gested that zooplankton can use riverine detritus-POM in estuaries(Bouillon et al., 2000) and fjord ecosystems, especially under lowautochthonous carbon productivity and/or low chlorophyll condi-tions (Vargas et al., 2011). The study performed by Vargas et al.(2011), based on d13C content suggested that ca. 20–50% of thebody carbon of copepod species can be derived from terrestrialPOC. Despite the limited spatial and temporal coverage of ourresults, our d13C estimations in zooplankton showed similar valuesto those reported in the above-mentioned study. Occasionally, ter-restrial carbon may account for a significant percentage of the zoo-plankton body carbon (24–61%), which was also supported by theresults of fatty acid composition. Our results also showed signifi-cant differences between the inner and outer areas of the fjord(H = 4.5, p < 0.05). Around 22–61% of zooplankton fatty acids atthe Almirante Montt Gulf are related to vascular plants (chainlength >24 C). However, across outer channels only ca. 14.6% oftotal fatty acids correspond to terrestrial carbon sources. Thesefindings fit well with the estimates of allochthonous carbon contri-butions to surface sediments in the Patagonia region, where terres-trial organic carbon is associated with the riverine-influencedinner-fjord area. However, autochthonous organic carbon was pre-valent (50–90%) in marine influenced channels, sounds, and gulfs(Silva et al., 2011). For estuarine or river-influenced areas, ourresults contrast with those reported by other authors for similarenvironments. For instance, Martineau et al. (2004) reported that,in the St. Lawrence River, phytoplankton may even constitute amajor food component for estuarine consumers (cladoceran Bos-mina longirostris, and the copepod Eurytemora affinis, among oth-ers), with little of the terrestrial organic carbon passing into theestuarine food web. Sobczak et al. (2005) showed that phytoplank-ton was the dominant source of organic matter in the San Franciscoestuary’s freshwater delta. Van der Meersche et al. (2009) alsodemonstrated that the contribution of algae to zooplankton diets,as estimated from isotope ratios and fatty acid profiles, averaged41% and 75% respectively. Therefore, mesozooplankton relies pri-marily on grazing phytoplankton. Allochthonous particulateorganic matter in these estuarine systems can be an importantfood web component, supporting plankton growth and respiration,thus determining the heterotrophic status of these systems. Never-theless, the C:N ratio in large copepods was found to be C:N > 10for animals collected in the inner Almirante Montt Gulf area(Table 2), suggesting a shift to low quality non-protein sources(Postel et al., 2000) that occurs when allochthonous sources arerelatively important. Furthermore, zooplankton could also profitfrom allochthonous dissolved organic carbon (DOC) through thebacterial loop pathway, i.e. by grazing directly on bacterivorousheterotrophic nanoflagellates or ciliates. Nevertheless, furtherinformation about the correct pathway, i.e. the direct utilizationof terrestrial POC and/or indirect use of terrestrial DOC, mightrequire use of deliberate tracer techniques. These results are highlyrelevant for carbon flow and food-web models, considering thatmost studies in Chilean fjord ecosystems only consider the fateof primary production to the upper trophic levels, implying thetransfer of autochthonous materials throughout plankton foodwebs (e.g., Vargas et al., 2008; Gonzalez et al., 2011).

Chilean Patagonia is one of the last pristine ecosystems and iscurrently under serious threats due to climate change and futurehuman encroachment. There is growing concern surrounding theunderstanding of ecological processes across ecosystems as humaninterference, e.g. deforestation, aquaculture, and dam construction,will likely contribute to climate change resulting in potentiallydevastating economic and ecological consequences that could seri-

ously impair reciprocal energy and organic matter exchangeamong ecosystems. In this vein, the understanding of exchangesof allochthonous nutrients and organic matter among ecosystemlevels is appreciated as a key element to predict productivity, bio-diversity, and food web dynamics. The present study clearly provesthat the dynamics of seemingly distinct ecosystems (i.e., lakes, riv-ers, and/or fjords) can be intimately linked by spatial flows oforganic matter.

Conclusions

There are significant statistical differences between terrestrialand marine environments for d13C values, but no within marinefjord stations, which indicates the existence of a large degree ofmixing across the estuary-sound-channels-ocean continuum.

Terrestrial-allochthonous derived carbon accounts for about81–96% of POC in rivers and lakes from SRB and for 40–96% atthe fjord. In the latter, there is a decrease in carbon from the fjord’sheadwaters to its mouth (40%) due to mixing between allochtho-nous and autochthonous organic matter. This is also supportedby ELCFA, which allowed to us to better define the spatial extentof the influence of terrestrial vegetation (C3 vascular plants) inthe water column of the fjord. ELCFA also provides the evidencethat terrestrial carbon can support zooplankton biomass; there-fore, planktonic food-webs can be supported by allochthonousorganic matter source.

The bulk of C:N ratio and stable isotope (d13C; d15N) values inthe surface sediment along the transect between the Señoret Chan-nel and the outer Channels, allows us to conclude that it is com-posed mainly by OM derived from marine origin (>80%) and theOM derived from terrestrial origin is unsignificant (<20%).

Acknowledgements

This investigation was partially supported by the ComitéOceanográfico Nacional (CONA), Chile, through the projectsCONA-C15F 09-14 granted to Cristian A. Vargas and CONA-CF1409-12, granted to Nelson Silva. The authors would like to thankthe Captain and the crew of AGOR Vidal Gormaz for their help dur-ing the CIMAR Fiordos 15 cruise. We extend our gratitude to PaulinaY. Contreras as well as Ms. Paola Reinoso who performed the dis-solved oxygen and nutrient analyses. We are also grateful to thefollowing institutions for partial financial support: Centro de Inves-tigación en Ecosistemas de la Patagonia (CIEP), Centro Trapananda ofUniversidad Austral de Chile, and Pontificia Universidad Católica deValparaíso (PUCV).

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Contribution of allochthonous organic carbon across the Serrano River Basin and the adjacent fjord...

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