Progress in Oceanography 119 (2013) 32–47

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Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean

Land–ocean gradient in haline stratification and its effects on plankton

dynamics and trophic carbon fluxes in Chilean Patagonian fjords
(47–50°S)
H.E. González a,b,c,d,⇑, L.R. Castro b,c,e, G. Daneri b,c,d, J.L. Iriarte b,c,d,f, N. Silva g, F. Tapia b,c,e, E. Teca a,
C.A. Vargas h
a
Instituto de Ciencias Marinas y Limnológicas, Universidad Austral de Chile, Valdivia, Chile
b
Centro de Investigación Oceanográfica en el Pacífico Sur-Oriental (COPAS), Universidad de Concepción, Concepción, Chile
c
COPAS Sur Austral (PFB-31-2007), Concepción, Chile
d
Centro de Investigación en Ecosistemas de la Patagonia (CIEP), Coyhaique, Chile
e
Departamento de Oceanografía, Universidad de Concepción, Concepción, Chile
f
Instituto de Acuicultura, Universidad Austral de Chile, Puerto Montt, Chile
g
Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile
h
Unidad de Sistemas Acuáticos, Centro de Ciencias Ambientales (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: Patagonian fjord systems, and in particular the fjords and channels associated with the Baker/Pascua
Available online 20 June 2013 Rivers, are currently under conspicuous natural and anthropogenic perturbations. These systems dis-
play very high variability, where limnetic and oceanic features overlap generating strong vertical and
horizontal physicochemical gradients. The CIMAR 14-Fiordos cruise was conducted in the Chilean fjords
located between 47° and 50°S during the spring (October–November) of 2008. The main objectives
were to study vertical and horizontal gradients in physical, chemical and biological characteristics of
the water column, and to assess plankton dynamics and trophic carbon fluxes in the fjords and chan-
nels of central-south Patagonia.
The water column was strongly stratified, with a pycnocline at ca. 20 m depth separating a surface
layer of silicic acid-rich freshwater discharged by rivers, from the underlying nitrate- and orthophos-
phate-rich Subantarctic waters. The outflows from the Baker and Pascua Rivers, which range annually
between 500 and 1500 m3 s1, generate the strong land–ocean gradient in salinity (1–32 psu) and inor-
ganic nutrient concentrations (2–8 and 2–24 lM in nitrate and silicic-acid, respectively) we observed
along the Baker Fjord. The POC:chl-a ratio fluctuated from 1087 near the fjord’s head to 175 at its oce-
anic end in the Penas Gulf. This change was mainly due to an increase in diatom dominance and a con-
current decrease in allochthonous POC towards the ocean.
Depth-integrated net primary production (NPP) and bacterial secondary production (BSP) fluctuated
between 49 and 1215 and 36 and 150 mg C m2 d1, respectively, with higher rates in oceanic waters.
At a time series station located close to the Baker River mouth, the average NPP was lower (average
360 mg C m2 d1) than at more oceanic stations (average 1063 mg C m2 d1), and numerically domi-
nated (45%) by the picoplankton (<2 lm) and nanoplankton (2–20 lm) size fractions. The high average
vertical carbon flux (234 mg m2 d1) and high export production (65% of the NPP) support the idea
that Patagonian fjords may behave as a net sink for CO2 during the productive (spring) season. Trophic
fluxes near the head of the fjords, with oligotrophic low-salinity waters, were dominated by heterotro-
phic nanoflagellates (HNF) and small copepods (52 mg C m2 d1, each), suggesting that the microbial
food web is the main trophic pathway in these environments.
Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Chilean Patagonia constitutes a large (>1600 km from 41° to

55°S), extensive (240,000 km2) and unique ecosystem consti-
⇑ Corresponding author at: Instituto de Ciencias Marinas y Limnológicas,
tuted by semienclosed highly haline-stratified areas. The region
Universidad Austral de Chile, Valdivia, Chile. Tel.: +56 (63) 221559; fax: +56 (63)
221455.
is made up mainly of fjords and channels, characterized by
E-mail address: hgonzale@uach.cl (H.E. González). intertangled geomorphologies where water inputs from terrestrial

0079-6611/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.pocean.2013.06.003
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47 33

and marine ecosystems overlap and mix. These highly vulnerable and fjords down to 50°S during the austral spring of 2008 (30 Octo-
ecosystems have been intensively used, providing socio-economic ber–24 November) on board the AGOR ‘Vidal Gormáz’ of the Chil-
(aquaculture, tourism, hydroenergy, etc.) and other less conspicu- ean Navy (Fig. 1). Three research approaches were implemented.
ous ecosystem services, such as the CO2 uptake capacity during
the productive season and carbon export to the deep sea. Patago- 2.1. Time series stations
nian systems play an important role in biological productivity,
with highly seasonal production that results in efficient carbon ex- Data on the volume of freshwater discharged by the Baker and
port to the sediments in spring (González et al., 2010). This also re- Pascua Rivers were obtained from the Chilean General Water Direc-
sults in the transport and exchange of important amounts of torate (DGA; www.dga.cl) for 2008–2010. A string of temperature
organic matter between terrestrial and marine systems, being the and light intensity sensors was moored at ca. 20 m depth near the
main contributors to carbon flux in coastal oceans (Walsh, 1991). Baker River mouth. Light intensity was recorded at 6 m depth,
The potential impacts of local (anthropogenic) as well as remote whereas four thermistors were located at 0, 5, 10 and 15 m depths
(global warming) perturbations on these ecosystem services need (Fig. 2). Both variables were measured at 10 m intervals.
to be taken into consideration for future sustainable uses. The average spring–summer distribution of freshwater along
The fjords and channels of Patagonia receive Subantarctic Water the Baker Basin was characterized using satellite-derived data on
(SAAW) with high loads of nitrate and phosphate from the ocean, total suspended sediments gathered by the MERIS-ENVISAT mis-
and freshwater with high loads of silicic acid from land. The surface sion, during the rare clear-sky days encountered between October
freshwater layer that is formed by river discharges, high precipita- 2005 and January 2011, to make a composite of 25 MERIS images
tion, and glacier melting, gradually mixes with the deeper and salty (Fig. 3).
SAAW layer through estuarine circulation. The strong pycnocline
thus formed may in some cases act as a barrier for nutrient exchange
and zooplankton vertical migration (Silva et al., 1998; Sievers and 2.2. Oceanographic transects
Silva, 2008; Sánchez et al., 2011). Events of mixing across this den-
sity barrier may be caused by fluctuations in freshwater input, and Five oceanographic transects were conducted from the Penas
may enhance new primary production (Gargett et al., 2003) and fa- Gulf (47°S) to Trinidad Gulf (50°S). (1) The Penas Gulf–Martinez
vor diatom blooms due to a reduction in macro-nutrient limitations Fjord transect comprised 9 stations (St. 92, 2, 93, 4, 96, 97, 14,
within the thin photic zone (Goebel et al., 2005). Such enhancement 13, 12 and 16) arranged in an E–W orientation, and will be referred
in nutrient conditions seems to compensate for the reduction in light to as the ‘‘Martinez transect’’. (2) The Baker Fjord transect included
penetration that is caused by the often high loads of particulate and 6 stations (St. 5, 6, 7, 8, 9 and 10), arranged in an E–W orientation
dissolved organic and inorganic matter associated to river dis-
charges. It has been shown that changes in near-surface salinity
may explain a large fraction of temporal variability in light extinc-
tion in fjord environments (Gibbs, 2001; Goebel et al., 2005).
Physical and chemical conditions along the Baker Basin
(47°470 S; 73°370 W) are strongly influenced by allochthonous mate-
rial, including organic matter, discharged into the Martinez and Ba-
ker Fjords by the Baker and Pascua Rivers, respectively. These
rivers have outflows that range annually between 500 and
3000 m3 s1, and originate from the large General Carrera
(46°310 S; 71°440 W) and O0 Higgins (48°550 S; 73°070 W) lakes,
respectively. This basin is located in between the two large fresh-
water reserves made up by the Northern (46–47°S) and the South-
ern (48–52°S) Ice Fields, from which glacier-melt freshwater flows
into the Steffen Fjord and Pascua River, respectively. Most proba-
bly, a great fraction of the organic matter carried by these freshwa-
ter inputs originates from the extensive evergreen and deciduous
forests, dominated by species of the family Nothofagaceae (Rodrí-
guez et al., 2008; V. Sandoval, pers. comm.), and subsequent trans-
port to the estuary due to intensive run-off driven by an active
precipitation regime that ranges between 1000 and 7000 mm y1
(National Water Directorate; www.dga.cl). Recent studies focused
on stable-isotope signatures have shed light on the contribution
of terrestrial versus marine carbon inputs in this region (Sepúlveda
et al., 2011; Silva et al., 2011; Vargas et al., 2011).
The aims of this contribution were: (1) to describe the vertical
and horizontal gradients in physical, chemical and biological fea-
tures, and (2) to assess the plankton dynamics, trophic carbon
fluxes and carbon export in the highly haline-stratified Baker Basin,
focusing on the Martinez, Baker and Eyre Fjords, as well as the
Trinidad and Messier Channels.

2. Materials and methods

Fig. 1. Study area showing both transects (lines) and stations (dots) between the
Penas Gulf and Trinidad Gulf, Chile. Black star: location of the process station (St.
A research cruise (CIMAR 14 Fiordos) was conducted in the Ba- 14); black square: location of the temperature and solar radiation time series
ker Basin (47°56.00 S, 74°29.60 W), spanning several inner channels stations at Caleta Tortel, close to the Baker and Pascua Rivers.
34 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 2. Discharge of the Baker and Pascua Rivers (top panel), as well as precipitation in the area (middle, red line), obtained from DGA monitoring stations. Light intensity at
ca. 6 m below the surface (middle, black line) and temperature profiles (bottom panel) were measured at a 20-m depth mooring near the Baker River mouth. Black contours
on the bottom panel correspond to 10 °C.
and in the text will be referred to as the ‘‘Baker transect’’. (3) The
Picton Channel–Penas Gulf transect included 11 stations (St. 80,
83, 84, 85, 86, 87, 88, 89, 90, 91 and 91R) along a N–S axis and will
be referred to as the ‘‘Trinidad transect’’. (4) The Wide Channel–
Messier Channel transect included 10 stations (St. 40, 35, 31, 24,
23, 22, 20, 19, 18 and 17), arranged in a N–S orientation and in
the text will be referred to as the ‘‘Messier transect’’. (5) The Wide
Channel–Eyre Fjord included 7 stations (St. 40, 35, 31, 25, 26, 27
and 28), arranged in a N–S orientation and in the text will be re-
ferred to as the ‘‘Eyre transect’’. Stations 40, 35 and 31 were also
included in the last transect to distinguish the spatial transition to-
wards a fjord that ends in an extensive ice-field (Fig. 1). At these
stations, water samples for plankton, dissolved oxygen and inor-
ganic nutrients were collected at discrete depths (see details be-
low). The physical structure of the water column (temperature,
salinity) was recorded with a Seabird 19 CTD. The salinity sensor
was calibrated by measuring salinity with an Autosal salinometer-
in discrete water samples. To estimate water column stability at
every station, the Brunt-Väisälä frequency (N2) was computed as
N 2 ¼ ½ðg=qÞ  ðDdh =DzÞ (IOC, SCOR and IAPSO, 2010).
2.3. Process-oriented time-series station
This fixed station (St. 14) in the middle of the Martinez Fjord
and near the mouth of the Steffen Fjord was occupied for a pro-
cess-oriented study. Measurements conducted at St. 14, hereafter
referred to as ‘process station’, were aimed at establishing the pos-
sible fate of photosynthetically generated organic carbon through
classical or microbial food webs. Measurements were conducted
over 5 days (6–10 November, 2008) where primary production
(PP) and bacterial secondary production (BSP) were estimated on
days 1, 3 and 5, whereas micro- and meso-zooplankton grazing
experiments were conducted on days 2, 3 and 5. The vertical flux
of particulates was estimated using sediment traps deployed for
two periods of ca. 2 days each (days 1–2 and 3–4). Although no
data on freshwater discharge are available for the Steffen Fjord,
most of the freshwater input to the area corresponded to glacier
meltwater from the Steffen Glacier located at this fjord’s head. This
process station represents average conditions of the inner/middle
area of the Martinez Fjord, characterized by a high input of both
freshwater and suspended particulate matter.
We estimated size-fractionated PP, BSP, nano-, micro-, and
mesozooplankton grazing, and vertical fluxes of particulate mate-
rial. Additionally, we measured the abundance and carbon-based
biomass of the following planktonic components: phytoplankton,
bacteria, heterotrophic and autotrophic nanoflagellates (HNF,
ANF), dinoflagellates and ciliates (see below). Size-fractionated PP
and BSP were also estimated at stations 17, 22 and 40, located in
the northernmost, central and southernmostpart of the Messier
Channel (Fig. 1 and Table 1).
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 3. Average spring–summer distribution of suspended sediments in the study area (left panel) and an enlarged view of the Martinez and Baker Fjords, showing the Pascua
and Baker River mouths and the Steffen Fjord (right panel). Data correspond to a composite of 25 MERIS images gathered by the ENVISAT satellite during clear-sky days
between October 2005 and January 2011.
The different physical, chemical and biological parameters mea-
sured/estimated during the cruise are summarized in Table 1, and
a detailed description of all measurements is given below.
2.4. Size-fractionated chl a and POC
For chl a and phaeopigments, 200 mL of seawater were filtered
(MFS glass fiber filters, 0.7 lm nominal pore size) in triplicate and
immediately frozen (20 °C) until later analysis via fluorometry,
using acetone (90% v/v) for the pigment extraction (Turner Design
TD-700) according to standard procedures (Parsons et al., 1984).
Chl a size fractionation was done as for the PP (see below). In addi-
tion, water samples were collected to determine POC and PON con-
centrations in the water column, including stable isotopes (13C) at
selected oceanographic stations. These samples (from 0.5 to 1.0 L)
were filtered through precombusted MFS filters and stored frozen
until later analysis following standard procedures (von Bodungen
et al., 1991). The autochthonous POC contribution was estimated
as the sum of the phytoplankton, bacterial, and microzooplankton
carbon. The latter fraction included flagellates (thecate and athe-
cate dinoflagellates), ciliates (loricate and aloricate ciliates) and
crustacean larvae (nauplii). Carbon estimates were based on car-
bon:plasma volume ratios (see below). Allochthonous POC was
estimated as total POC minus autochthonous POC.
For dissolved oxygen and nutrient (nitrate, orthophosphate, silicic
acid) analyses, water samples were collected using a CTD-rosette
equipped with 24 Niskin bottles from the following depths: 1, 5, 10,
25, 50, 75, 100, 150, 200, 250, 300, 350 and 400 m, with maximum
depth of each profile determined by water depth at each station. Dis-
solved oxygen was analyzed on board with the Winkler method (Car-
penter, 1965). Nutrient samples (50 mL) were stored at 20 °C in acid-
cleaned high-density polyethylene bottles and analyzed later in a
nutrient autoanalyzer (Mod. Technicon) according to Atlas et al.
(1971).
2.5. Plankton abundance and biomass
Bacterioplankton, protozoan and phytoplankton counts were
done for water samples collected at selected depths (0, 5, 10, 25,
35
50 m) in the upper 50 m of the water column. Bacterioplankton
abundance (cells mL1) was measured on polycarbonate membrane
filters (Nuclepore 0.2 lm) stained with the fluorochrome DAPI (Por-
ter and Feig, 1980) and using epifluorescence microscopy. Bacterial
biomass was estimated using a factor of 20 fg C cell1 (Lee and Fuhr-
man, 1987). For the enumeration of nanoflagellates, 20 mL sub-sam-
ples were filtered on a 0.8 lm polycarbonate membrane filter and
stained with Proflavine (0.033% w/v in distilled water) according
to Haas (1982) and fixed with glutaraldehyde. Sub-samples for dia-
tom counts (300 mL) were preserved in an acid Lugol’s solution (1%
final conc.). Sub-samples of 50 mL were placed in settling chambers
for 30 h before analysis under an inverted microscope (Zeiss Axio-
vert 200, 400 magnification) using the standard methodology
(Utermöhl, 1958); a carbon:plasma volume ratio of 0.11 pg C lm3
was applied for diatom carbon estimations (Edler, 1979). For dino-
flagellate and ciliate counts, 10–30 L of seawater from different
depths (surface, 5, 10, 25 m) were filtered gently through a 10 lm
mesh sieve, then concentrated up to a final volume of 100 mL
and preserved with buffered formalin (5% final conc.). Car-
bon:plasma volume ratios of 0.3 and 0.19 pg C lm3 were used for
heavily thecate and athecate dinoflagellate forms, respectively (Les-
sard unpubl. data fide Gifford and Caron, 2000), and 0.148 pg C lm3
was applied for ciliates (Ohman and Snyder, 1991).
Zooplankton samples were collected by oblique tows using a
Tucker trawl net (1 m2 catching area, 300 lm mesh size) within
the upper 75 m of the water column. Samples were preserved in
borax buffered formalin (10% final conc.) for later analyses of the
dominant zooplankton groups (large copepods and euphausiids).
Additional tows using a WP-2 net (200 lm mesh size) were con-
ducted to estimate the abundance of small calanoid copepods.
2.6. Primary production (PP) and bacterial secondary production (BSP)
Water samples for PP determinations were incubated in 100 mL
borosilicate glass bottles (2 clear replicate bottles and 1 dark bottle
for each depth) and placed in a natural-light incubator for 4 h (usu-
ally from 10:00 to 14:00). Temperature was controlled by running
surface seawater over the incubation bottles. For incubations
Table 1

36
Parameter measured/estimated during the CIMAR 14 cruise.

Station number Water column depth (m) Lat. and long. Chl (fractionated chlorophyll-a), POC (particulate organic carbon), BB (bacterial biomass), ANF-B (autotrophic nanoflagellate biomass), HNF-B
(heterotrophic nanoflagellate biomass), NUT (nitrate, phosphate, silicic acid), Microzoo-B (microzooplankton biomass), Cop-B (copepod biomass),
Eup-B (euphausiid biomass), HNF-G (heterotrophic nanoflagellate grazing), Microzoo-G (microzooplankton grazing), Cop-G (copepod grazing), Vert-F
(vertical flux of particulates) and PP (primary production)
Chl POC BB ANFB HNFB NUT Microzoo-B Cop-B Eup-B HNFG Microzoo-G Cop-G Vert-F BSP PP
Penas Gulf–Martinez Fjord transect
p p p p p p p p p p
92 200 47°31,190 S; 75°37,410 W
p p p p p p p p p
2 150 47°17,500 S; 75°00,100 W
p p p p p p p p p
93 156 47°22,200 S; 74°38,700 W
p p p p p p p p p
4 550 47°47,000 S; 74°32,000 W
p p p p p p p p p
96 246 47°48,000 S; 74°15,900 W
p p p p p p p p p
97 124 47°48,400 S; 74°03,900 W
p p p p p p p p p p p p p p p
14a 276 47°48,400 S; 73°45,000 W
p p p p p p p p p
13 188 47°49,900 S; 73°40,950 W
p p p p p p p p p
12 94 47°51,400 S; 73°35,900 W
p p p p p p p p p
16 285 47°59,380 S; 73°22,550 W

H.E. González et al. / Progress in Oceanography 119 (2013) 32–47

Baker Fjord transect
p p p p p p p p p
5 505 47°56,000 S; 74°29,600 W
p p p p p p p p p
6 706 48°00,000 S; 74°19,300 W
p p p p p p p p p
7 404 47°59,300 S; 74°04,300 W
p p p p p p p p p
8 841 48°01,800 S; 73°50,100 W
p p p p p p p p p
9 401 48°04,500 S; 73°38,200 W
p p p p p p p p p
10 278 48°12,750 S; 73°26,000 W
Trinidad Channel transect
p p p p p p p p p
80 210 49°57,120 S; 74°58,000 W
p p p p p p p p p
83 296 49°48,750 S; 75°09,800 W
p p p p p p p p p
84 236 49°37,400 S; 75°17,500 W
p p p p p p p p p
85 98 49°28,900 S; 75°24,900 W
p p p p p p p p p
86 290 49°18,500 S; 75°29,000 W
p p p p p p p p p
87 970 49°06,240 S; 75°15,250 W
p p p p p p p p p
88 630 48°56,500 S; 75°02,000 W
p p p p p p p p p
89 352 48°39,200 S; 74°59,200 W
p p p p p p p p p
90 550 48°23,400 S; 75°02,400 W
p p p p p p p p p
91 535 48°04,150 S; 75°14,000 W
p p p p p p p p p
91R 82 47°52,500 S; 75°35,000 W
Messier Channel transect
p p p p p p p p p p p
40 323 50°09,550 S; 74°43,200 W
p p p p p p p p p
35 939 49°58,100 S; 74°25,800 W
p p p p p p p p p
31 733 49°47,800 S; 74°21,900 W
p p p p p p p p p
24 225 49°24,300 S; 74°24,400 W
p p p p p p p p p
23 151 49°11,200 S; 74°22,500 W
p p p p p p p p p p p
22 168 49°02,800 S; 74°25,800 W
p p p p p p p p p
20 345 48°53,100 S; 74°24,700 W
p p p p p p p p p
19 300 48°39,000 S; 74°22,600 W
p p p p p p p p p
18 1173 48°30,000 S; 74°30,000 W
p p p p p p p p p p p
17 1238 48°02,010 S; 74°38,300 W
Eyre Fjord transect
p p p p p p p p
25 504 49°33,500 S; 74°12,600 W
p p p p p p p p
26 532 49°31,600 S; 74°04,300 W
p p p p p p p p
27 318 49°23,100 S; 74°05,700 W
p p p p p p p p
28 162 49°16,100 S; 74°04,000 W
a
The ‘‘process station’’ (St. 14).
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
corresponding to the sub-surface chl a maximum, 40% and 2% of
surface light intensity was simulated using screens to attenuate
light at depths where the water was collected. Sodium bicarbonate
(40 lCi NaH14CO3) was added to each bottle. Following incubation,
samples were manipulated under subdued light conditions prior to
and after the incubation periods. The contents were filtered
according to the fractionation procedure described below. Filters
(0.7 and 2.0 lm) were placed in 20 mL borosilicate scintillation
vials and kept at 20 °C until reading. To remove excess inorganic
carbon, the filters were treated with HCl fumes for 4 h. A cocktail
(10 mL, Ecolite) was added to the vials, and radioactivity was
determined in a scintillation counter (Beckmann). Depth-inte-
grated values of PP (mg C m2 h1) were calculated using trapezoi-
dal integration throughout the euphotic zone; the 4 depths
considered were the surface, sub-surface chl a maximum, and
40% and 2% surface irradiance depths. Integrated production rates
per hour were multiplied by daily light hours for the Baker Fjord.
Phytoplankton size-fractionation was performed post-incuba-
tion in 3 sequential steps: (1) for the nanoplankton fraction (from
2.0 to 20 lm), seawater (125 mL) was pre-filtered using a 20 lm
Nitex mesh and collected on a 2.0 lm Nuclepore; (2) for the pico-
plankton fraction (from 0.7 to 2.0 lm), seawater (125 mL) was pre-
filtered using a 2.0 lm Nuclepore and collected on a 0.7 lm MFS
glass fiber filter; and (3) for the whole phytoplankton community,
seawater (125 mL) was filtered through a 0.7 lm MFS glass fiber
filter. The microphytoplankton fraction was obtained by subtract-
ing the production estimated in steps 1 and 2 from the production
estimated in step 3.
BSP was estimated using water samples from the same oceano-
graphic bottle as for PP experiments. The incorporation of L-
[14C(U)]-leucine into proteins (Simon and Azam, 1989) was used
to estimate BSP through the increment of biomass. Incubations
were conducted at the in situ temperature and in darkness for
1 h, filtered over 0.22 lm membrane filters and extracted with cold
5% trichloroacetic acid (TCA). Samples were frozen on board and
counted in a liquid scintillation counter in the laboratory. From
each experiment, water samples were taken for bacteria cell num-
bers and biomass estimations (for a complete description see Mon-
tero et al., 2011).
The nanoflagellate and microzooplankton grazing experiments
were performed using the size-fractionation method (Kivi and Set-
ala, 1995; Sato et al., 2007). Water samples were collected from the
fluorescence maximum depth with a clean 10 L Go-Flo bottle-ro-
sette system. After collection, seawater was size-fractioned by re-
verse filtration into 3 fractions: (1) <2 lm (i.e. mostly bacteria
and cyanobacteria), (2) <10 lm (i.e. mostly bacteria, cyanobacteria,
ANF, and HNF), and (3) <115 lm (i.e. the whole photoheterotrophic
community). Grazing rates were estimated by comparing prey
growth rates in the presence and absence of predators selected
by reverse filtration as follows: for HNF grazing, by comparing
(1) and (2); and for microzooplankton (ciliates + dinoflagellates)
grazing on nanoflagellates (both PNF and HNF), by comparing (2)
and (3) (Gifford, 1993). Further descriptions of procedures and
methods are fully described in Vargas et al. (2008).
2.7. Copepod grazing
For copepod grazing estimations, animals were collected by
slow vertical hauls in the upper 20 m of the water column using
a WP-2 net (mesh size 200 lm) with a large non-filtering cod
end (40 L). Undamaged copepods were placed in 500 mL (from
4 to 8 small copepods) or 1000 mL (from 2 to 3 large copepods)
acid-washed polycarbonate bottles. These bottles were filled with
ambient water loaded with natural food assemblages of micro-
plankton pre-screened through a 200 lm net to remove most graz-
ers. Three control bottles without animals and 3 bottles with 2–4
37
animals each were placed in an incubator rack on deck for approx-
imately 19–25 h. The seawater incubation was mixed by hand
every hour and, to some extent, by the ship’s motion. Initial control
bottles were immediately preserved with 2% acid Lugol’s solution,
and a sub-sample was also preserved in glutaraldehyde (as above).
At the end of the incubation, sub-samples were taken from all the
bottles and preserved in glutaraldehyde for nanoflagellate counts
(20 mL) and acid Lugol’s solution (60 mL, as above) for cell concen-
trations. Ingestion rates, measured as cell removal, were calculated
according to Frost (1972), as modified by Marín et al. (1986).
2.8. Vertical flux of particulates
The vertical flux of POC was estimated by using surface-teth-
ered, cylindrical sediment traps (122 cm2 area and 8.3 aspect ratio)
deployed at 50 m water depth at the ‘process station’ (St. 14) for
periods of 1–1.5 days. Sub-samples were analyzed through micros-
copy using standard techniques (Utermöhl, 1958); for POC and
PON, 0.5–1.0 L were filtered through precombusted MFS filters
and stored frozen until later analysis.
3. Results
3.1. Environmental conditions
The Baker and Pascua Rivers provide average freshwater dis-
charges of 400–1500 m3 s1 each (DGA, www.dga.cl, 2008–2010),
reaching highest levels in summer and lowest levels from late win-
ter through early spring. Upon the occurrence of GLOF’s (Glacial
Lake Outburst Floods), driven by changes in hydrometeorological
conditions and resulting in the recurrent emptying of lakes such
as the Cachet (ca. 100 km upriver from the Baker’s mouth), river
outflow may reach peak levels that range between 2000 and
2500 m3 s1 (Fig. 2, upper panel).
At the Baker estuary mooring station, the light penetration fol-
lowed an inverse pattern with respect to freshwater discharge,
with highest sub-surface light intensities (100–1000 lx) during late
winter–early spring, and lowest intensities (<10 lx) during sum-
mer–autumn months. Temperature in the water column showed
strong temporal variability over the 2008–2010 period, with con-
spicuous seasonal changes and marked differences among years.
Summer temperatures were warm (10–14 °C) through most of
the water column in the 2008–2009 summer (December–March),
whereas the following year they ranged from 8 to 13 °C within
the upper 10 m of the water column. During winter–spring, an in-
verse thermal stratification was observed, with cold water (5–8 °C)
in the top 8 m of the water column and warmer waters (9–11 °C)
near the bottom (Fig. 2).
The spring–summer distribution of suspended sediments along
the Baker Basin (i.e. Martínez and Baker Fjords) showed that max-
imum concentrations (50–100 g m3) occurred at the Baker and
Pascua River mouths, while steadily decreasing towards the ocean,
reaching <1 g m3 at the Penas Gulf. The process station 14 was lo-
cated in the Martinez Fjord, close to the Steffen Fjord mouth
(Fig. 3), and also showed a very high concentration of suspended
particles (100 g m3).
At all transects, temperatures ranged from 8 to 10 °C. At the
Martinez and Baker transects, tongues of relatively cold (8 °C)
water projected from the mouths of the Baker and Pascua Rivers;
water was even colder (6.5 °C) at the station close to the Southern
Ice Fields (St. 28) on the Eyre transect. Below the surface layer, a
vertical quasi-homogeneous thermal distribution (8–9 °C) was
found (Fig. 4, upper panel).
Along the two E–W transects (Martinez and Baker), a strong
horizontal salinity gradient was evident with values ranging from
38 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47

1 psu at the Baker and Pascua River mouths to 32 psu at the Penas
Gulf. Instead of a major river, the SW–NE Eyre section has a glacier
(Pio XI) at its head; melt water from this glacier, however, does not
set horizontal gradient in salinity or silicate (Figs. 4 and 5), as in the
Baker or Pascua Rivers. The N–S oriented transects showed a more
homogeneous structure, with salinity values between 24 and
26 psu at the surface (Fig. 4, middle panel). The vertical structure
showed a strong halocline (from 20 to 32.5 psu) along the N–S
transects with differences of up to 30 psu in the upper 25 m of
the E–W transects at stations close to the river mouth. In addition,
a quasi-homohaline (33–34 psu) distribution was found from 25 m
depth down to the bottom. A strong halocline was set at the head
of the Martinez and Baker Fjords, which in turn generates a thin
layer of high stability in the water column (N2 = 0.02–
0.06 (rad s1)2) at depths of ca. 20–30 m. This layer diminished in
intensity toward the fjords mouths, where it almost vanished
(N2 < 0.001 (rad s1)2), in parallel with the halocline gradient
(Fig. 6). As already mentioned, in the Eyre section the Pio XI glacier
does not release enough fresh water from ice melting to generate a
high stabilty layer at its head. Nevertheless, it shows a surface sta-
bility peak at its mid section (St. 35; 0.02 (rad s1)2) due to the
higher fresh water input from the Europa Fjord (Fig. 6).
The dissolved oxygen concentration showed a similar
vertical structure in all transects, with high values close to the sur-
face (7 mL L1) that steadily decreased towards the bottom
(3.5 mL L1). Slightly elevated dissolved oxygen concentrations
(>8 mL L1) were found in association with the river discharges
into the Martinez and Baker Fjords (Fig. 4, lower panel). The dis-
solved oxygen concentrations in the Eyre section showed similar
characteristics to the Martinez and Baker sections, although near-
bottom concentrations were not as low (Fig. 4).
The nitrate and orthophosphate concentrations showed sharp
land–ocean gradients, with very low values in the low-salinity sur-
face tongue that extended up to St. 4 along the Martinez Fjord and
along the entire Baker Basin. The N–S transects showed low surface
concentrations of nitrate (2–4 lM) and orthophosphate (0.2–
0.4 lM), which increased below 300 m depth to 24 and 2 lM,
respectively (Fig. 5). On the other hand, the distributional pattern
of silicic acid showed highest concentrations within the freshwater
plume, with values up to 26 lM, which decreased down to 4–8 lM
in sub-surface waters down to 50 m depth, and then increased
again in deeper waters. The N–S transect showed low values close
to the surface (4–8 lM) and a steady increase below 100 m depth
(Fig. 5). The distribution of inorganic nutrients along the Eyre sec-
tion showed features similar to the Martinez and Baker sections,
except for the lack of high surface concentrations near the fjord’s
head (Fig. 5).
3.2. Chl-a and POC concentrations
Depth-integrated (upper 25 m water column) chl a concentra-
tions were very low, with average values of total chl a ranging from
10 to 17 mg chl a m2 at the Martinez Fjord and Messier Channel,
respectively. Only the Trinidad Channel displayed a slight increase
in chla a concentration, with an average of 33 mg m2. The domi-
nant chl a size fraction was <5 lm contributing with 55% of total
chl a, while the size fraction of 5–20 and >20 lm accounted for
18.5% and 26.5%, respectively (Fig. 7A). The size-fractionated chl
a was dominated by small phytoplankton (autotrophic flagellates
<5 lm), with some increase in diatom abundance at the Trinidad
Channel and Eyre Fjord (3.3  105 cells L1), and thecate dino-
flagellates at the Baker Fjord and Messier Channel (1.1  105 -
cells L1). Interestingly, one of the key species was the diatom
Guinardia delicatula, which contributed with >50% of the large,
chain-forming diatoms at St. 14, 17 and 40. Only the oceanic SAAW
of the Penas Gulf (St. 92 and 91R), exhibited a more conspicuous

Fig. 4. Vertical distribution of the physical and chemical variables recorded in the study area. The different panels show the distributions of temperature, in °C (upper panel),
salinity, in psu (middle panel) and dissolved oxygen, in mL L1 (bottom panel) throughout the water column in November 2008.
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 5. Vertical distribution of the macro-nutrients recorded in the study area. The different panels show the distribution of (upper panel) nitrate, in lM, (middle panel)
orthophosphate in lM, and (bottom panel) silicic acid, in lM, throughout the water column in November 2008.
diatom community with Skeletonema spp., Leptocylindrus minimus,
Thalassiosira spp., Chaetoceros spp., and Pseudonitzschia spp.
Integrated POC concentrations in the upper 25 m of the water
column showed only small changes through the study area, with
an average of 6186 ± 484 mg C m2, and a slight increase in the Pe-
nas Gulf (11,370 ± 3265 mg C m2) (Fig. 7B). Surface-layer POC was
made up mostly by allochthonous POC, with contributions that
ranged from 82% at St. 17 to 100% at St. 13. At 10 m depth there
was a gradient in allochthonous POC, decreased from ca. 89% near
the Baker and Pascua River mouths (St. 10 and 12) to 49% at the
northern tip of the Messier Channel (St. 17) (Fig. 8). This feature
was corroborated by the d13C stable isotope signature, which at
the surface showed a strong terrestrial input near the river mouths
(d13C range: 25.0 to 26.5) and a slight increase in marine influ-
ence at St. 17 (23.5). At 10 m depth, on the other hand, a domi-
nance of marine input was evident (d13C range: 25.0 to 22.5)
(Fig. 8).
3.3. Plankton biomass (bacterioplankton, nanoflagellates, ciliates,
mesozooplankton)
Depth-integrated bacterioplankton biomass (upper 25 m)
showed high variability at the station level (within transects) and
changed relatively little at the transect level (i.e. mean ± SD:
217 ± 98; 212 ± 67 and 211 ± 109 mg C m2 in the Martinez Fjord,
Trinidad Channel and Eyre Fjord) and a slightly higher biomass
in the Baker Fjord and Messier Channel (303–372 mg C m2)
(Fig. 7C). No clear E–W or N–S spatial pattern could be identified,
and bacterial carbon only represented an average of 5% (range 3–
6%) of total POC.
The overall integrated biomass of NF was 410 ± 318 mg C m2,
with a 4-fold increase along the Martinez and Trinidad transects
39
(752 ± 52 mg C m2), as compared to the other three transects
(182 ± 79 mg C m2) (Fig. 7D). The ANF biomass was, on average,
2.6 times higher (289 ± 236 mg C m2) than the HNF
(112 ± 85 mg C m2).
The overall mean depth-integrated (upper 25 m water column)
microzooplankton abundance was 298 mg C m2. The dominant
group was thecate dinoflagellates (238 ± 178 mg C m2), which
contributed 70% to total microzooplankton biomass. Crustacean
nauplii contributed 46 ± 13 mg C m2 or 20% of total biomass,
while both loricate and aloricate ciliates contributed with 2% each
(Fig. 7E). At St. 22, 23 and 25, large numbers of small (<20 lm) and
large (>20 lm) dinoflagellates were present, with carbon biomass
1 g C m2.
The abundance of small copepods (<1500 lm prosome length)
integrated within the upper 20 m was numerically dominated by
Paracalanus parvus, copepodites and the genera Acartia and Centro-
pages. Among the large copepods (>1500 lm PL), Calanus chilensis
and the genera Neocalanus and Rhincalanus dominated. The
overall mean depth-integrated abundance of copepods was
7928 ± 2327 ind. m2, with maximum values at the Trinidad Chan-
nel (10,939 ind. m2) and at St. 88 (40,919 ind. m2). Euphausiid
abundance integrated within the upper 25 m was 91 ± 75 ind. m2
throughout the study area and was largely accounted for by Eup-
hausia vallentini (>90%), (Fig. 7F). It must be noted that these pat-
terns were derived from daytime and nighttime plankton tows,
which may strongly underestimate abundance due to active verti-
cal migration.
3.4. Productivity, pelagic food web and carbon export flux
At the stations where PP and BSP were estimated, chl a was low
within the upper 25 m (5–20 mg m2), and dominated by the
40 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 6. Vertical distribution of the Brunt-Väisälä stability index (N2) and salinity (psu) at three stations along the Martinez (St. 16, 97, 2), Baker (St. 10, 7, 5) and Eyre (St. 40, 35,
27) transects, located at the head, center and mouth of the fjords, respectively.
picoplankton size fraction (<2 lm). The >20 lm fraction was dom-
inated by the diatom Guinardia delicatula, with minor contributions
by Skeletonema spp., Leptocylindrus minimus, Pseudo-nitzschia spp.,
Thalassionema nitzschioides and Navicula spp. Only at St. 22 were
dinoflagellates important (Fig. 9, upper panel).
On average, the POC:Chl a ratio was very high at the process
station (St. 14), with a value (596 ± 422) similar to that found
at St. 22 (550). Stations 17 and 40, which receive a lesser load
of suspended sediments, exhibited ratios of 286 and 295, respec-
tively. The PP:chl a ratio did not display a clear trend, with rela-
tively low values that ranged between 33 and 110 for all stations
(Fig. 9, middle panel).
Depth-integrated PP was low at Stn. 14, with an average
of 422 ± 255 mg C m2 d1, while it was twice as high
(1063 mg C m2 d1) at stations located along the Messier Channel
(St. 17, 22 and 40). On average, picophytoplankton contributed the
bulk (44.5%) of PP at St. 14, while nanophytoplankton was most
important (44.3%) at stations along the Messier Channel.
There were no apparent spatial patterns in estimated BSP rates
and bacterioplankton biomass, with an average depth-integrated
production of 113 ± 495 mg C m2 d1. The PP:BSP ratio was al-
ways >1, with both extreme values (1.4 and 11.6) observed at St.
14, and a mean rate of 6.2 ± 3.5 for this and the three stations along
the Messier Channel (Fig. 9, lower panel).
Estimates for the vertical flux of particles were highly variable,
with 149 ± 45 mg C m2 d1 (n = 2) during the 6–7 November trap
deployment, and 320 ± 10 mg C m2 d1 (n = 2) during 8–9
November (average of 234 mg C m2 d1). At 50 and 90 m depth,
the estimated fluxes were similar, although the C:N ratio was high-
er at 50 m (14.9) than at 90 m depth (11.2). The highest grazing
rates were those estimated for HNF and small copepods
(52 mg C m2 d1) (Fig. 10). Our results are summarized in
Fig. 10, and presented in the context of carbon fluxes through the
pelagic food web. They are further discussed in the following
section.
4. Discussion
The rugged coastline of the study area is characterized by (1) a
hydrographical scenario impinged on by freshwater inflow from
the Baker and Pascua Rivers, and (2) a geomorphological scenario
consisting of 5 different channels with different orientations and
connections between them and with the open ocean.
The oceanic, salty SAAW enter the study area mainly from the
north (Penas Gulf) and through the Martinez and Baker Fjords,
mixing with surface freshwater from rivers (Sievers and Silva,
2008). Clearly, depending on their geographic orientation (E–W
versus S–N) the Patagonian channels and fjords will be affected
in different ways by haline stratification and, therefore, will exhibit
different degrees of water column stablity. Along the E–W Fjords,
the horizontal salinity gradients and vertical extent of the upper
brackish layer were very conspicuous. The former took the form
of a freshwater plume extending from the river mouth to the coast-
al ocean, whereas in the vertical dimension there were strong
pycnoclines and layers of high stability between 5 and 30 m depth
(1–30 psu; 0.02–0.06 (rad s1)2). This highly stable surface layer
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47 41

Fig. 7. Integrated values of different parameters measured during November 2008 along the transects from the Penas to the Trinidad Gulfs. (A) Size-fractionated chl a, (B)
particulate organic carbon, (C) bacterial biomass, (D) heterotrophic and autotrophic nanoflagellates (HNF and ANF), (E) microzooplankton and (F) mesozooplankton.
Abundances of the different plankton groups were transformed into carbon biomass by using the following equations: Bacteria = 20 fg C cell1 (Lee and Fuhrman, 1987),
flagellates = 6500 fg C cell1 (Børsheim and Bratbak, 1987), tintinnids = pg C = (lm3)  0.053 + 444.5 (Verity and Langdon, 1984), thecate dinoflagellates = pg C = (lm3)  0.13
(Edler, 1979), copepod nauplii = ng C = 1.51  10–5LC2.94 (Uye et al., 1996), calanoid copepods = 26.9 lg C cop1 (González et al., 2000; Hirst et al., 2003), euphausi-
ids = 3812 lg C euph1 (Sánchez et al., 2011). All values were integrated throughout the upper 25 m of the water column.

became thinner towards the fjord’s mouth, where it almost disap- northern and central Patagonia. From observations made in fjords
peared. This pattern is consistent with the one documented by of central Patagonia during the 1970 HUDSON cruise, Guerrero
Bustos et al. (2008) and Landaeta et al. (2001) in the fjords of (2000) found maximum stability values of 0.02–0.06 (rad s1)2
42 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 8. Percentage of allochthonous (open bars) and autochthonous (black bars)
particulate organic carbon and d13C stable isotope at stations located along the
Martinez and Baker Fjords at the surface (A) and 10 m depth (B).
for the Baker, Steffen, and Europa Fjords, and lower than
0.02 (rad s1)2 at Eyre. These values are highly consistent with
our stability results for the CIMAR 14 Fiordos cruises, conducted
38 years after the HUDSON.
Overall, a layer of freshwater with high concentrations of silicic
acid spanned the top 15 m of the water column at the Martinez and
Baker Fjords. Below the pycnocline, a much thicker layer of marine
water loaded with nitrate and orthophosphate lead to the overlap-
ping of limnetic and marine characteristics in the fjords (Silva and
Neshyba, 1979; Silva et al., 1998), as previously reported for Chil-
ean Patagonia (Silva et al., 1998; Palma and Silva, 2004; Silva and
Palma, 2006; González et al., 2010, 2011). The ratio of nitrate
and orthophosphate available for phytoplankton in the study area
(ca. 10) was lower than the global mean ratio of nitrogen to phos-
phorous (N/P  15) (Deutsch and Weber, 2012), which suggests
that productivity in this area may be nitrate-limited. The N/P ratio
may determine overall cellular stoichiometry (Geider and La
Roche, 2002), since the organic molecules used for resource acqui-
sition (proteins and pigments) require substantially more N per
atom of P than does the molecular machinery of growth and repro-
duction, i.e. DNA and RNA (Arrigo, 2005). Thus, high stratification
set up in Patagonian fjords by inputs of oligotrophic freshwater
would strongly impact the N/P ratio and, in turn, the physiological
adaptation of phytoplankton (Finkel et al., 2006). Potential conse-
quences would be the dominance of different functional groups,
such as small-size phytoplankton (picophytoplankton), more
adapted to nutrient acquisition under limitation of micro- and/or
macro-nutrients (Iriarte and González, 2004), diatom species with
low N:P ratios (<11:1) (Bertilsson et al., 2003; Weber and Deutsch,
2010), or diazotrophs which are not reliant on the nitrate supplied
by SAAW.
The presence of a brackish upper layer significantly affects the
productivity and structure of planktonic communities (reviewed
by Wetzel, 1995; Pace et al., 2004). Primary production at
the process station (St. 14) was substantially lower
(422 ± 255 mg C m2 d1) than at stations located along the Mess-
ier Channel (1063 ± 166 mg C m2 d1). Two main factors seem to
constrain PP at St. 14: macro-nutrient concentrations and light
availability. Nitrate and orthophosphate concentrations at St. 14
were low enough to be considered limiting (2 and 0 lM, respec-
tively), whereas light intensity in the upper water column was at
its annual minimum, despite the seasonal increase in solar radia-
tion (Aracena et al., 2011). This is because freshwater discharged
by the Baker and Pascua Rivers enters the fjords with a very high
load of particulates (50–100 g m3 of suspended sediments as
can be seen in Fig. 3), coming mostly from the melting of glaciers
in the Northern and Southern Ice Fields. This combination of nutri-
ent and light limitation should impact the physiological condition
of phytoplankton at St. 14, lowering the PP:chl a ratio (i.e. P/B ra-
tio) which has been suggested as a proxy for healthy physiological
conditions, and dependent on daily maximum irradiance and ni-
trate concentration (González et al., 2009). Indeed, the mean inte-
grated P/B ratio in the upper 25 m at St. 14 (49.3 ± 34.2) was lower
than P/B values found along the Messier Channel (70.3 ± 35.5). In
general, P/B ratios were within the range of springtime values re-
ported for the channels and fjords of the Aysén Region, from 60
in the northern Moraleda Channel (44°S) to 20 in the Aysén Fjord
(45°S) (González et al., 2011). In the upwelling system off Concep-
ción, the P/B ratio ranges from <20 in winter to ca. 100 in spring
(González et al., 2009).
Contrasting with the spatial trends in P/B ratios, the POC:chl a
ratio was higher at St. 14 (595.7 ± 422.0) than at stations along
the Messier Channel (377.2 ± 149.9). Low values of this ratio have
been related to high productivity (108 during late summer in the
Skagerrak, Maar et al., 2004; 29–207 in the coastal region off Con-
cepción, Grunewald et al., 2002), whereas high values are charac-
teristic of unproductive areas or high-river-discharge winter
periods, when the input of allochthonous organic matter (probably
loaded with refractory carbon) increases. This seasonal pattern in
the POC:chl a ratio has been found in other fjord areas such as
the Reloncaví Fjord and the Interior Sea of Chiloe, in northern Pat-
agonia (41°S), which exhibit low average values (87) during spring,
and high values (487) during winter (González et al., 2010).
Global warming trends may affect the stratification regime and
productivity patterns in Patagonia over a variety of spatial and
temporal scales. For instance, the frequency of glacial-lake out-
burst floods (GLOF’s), such as those documented by Dussaillant
et al. (2009) for Lake Cachet 2, may be increasing. While five events
were reported in 2008–2009 (Dussaillant et al., 2009), six of these
events that doubled the river outflow (to 2000–2800 m3 s1) in a
matter of hours were recorded in 2009–2010 (Fig. 2). The large vol-
ume of freshwater released on each event (ca. 200 million m3, Dus-
saillant et al., 2009) may certainly alter stratification and
conditions for primary production near the Baker River mouth. An-
other potential impact of these GLOF’s is the increased reservoir
sedimentation due to a large sediment load, with unexpected im-
pacts on benthic fauna and biodiversity (Quiroga et al., 2012), as
well as on the functioning of the planned hydropower dams in
the Pascua and Baker Rivers (Dussaillant et al., 2009; Vince,
2010). Thus, natural and human activities may potentialy impact
Patagonian rivers, increasing sediment load on some, and decreas-
ing the flux in others through damming. Such catchment impacts,
together with rapid urbanization on delta plains, accentuate the
threats posed by natural hazards and climate change (Woodroffe
and Saito, 2011).
Phytoplankton was low and dominated by the small pico- and
nano-phytoplankton fractions. A dominance of diatoms was evi-
dent at the oceanic end of the transects, where the continuous sup-
ply of freshwater loaded with silicic acid and the enhanced light
availability during spring months seem to favor the development
of large, filamentous diatom blooms (Thalassiosira, Chaetoceros
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 9. From top to bottom: Distribution of fractionated chl a (<2, 2–20 and >20 lm) and the relative contribution of the dominant species of diatoms and thecate
dinoflagellates. Values of the POC:Chl a, PP:chl a and PP:BSP ratios, and estimated PP and BSP rates at the process station (St. 14) in the Martinez Fjord and the three stations
along the Messier Channel (St. 17, 22, 40).
and Skeletonema). This is a recurrent situation in fjords in both
southern (González et al., 2011) and northern (Thompson et al.,
2008) hemispheres.
The average bacterioplankton biomass at the Baker Fjord
(259 ± 195 mg C m2; n = 41, Fig. 7C) was similar to that found
near the Aysén Fjord at 45.3°S (307 mg C m2, González et al.,
2011), and nearly half that of that found at the Reloncaví Fjord at
41.4°S (507 mg C m2, González et al., 2010). In contrast to the re-
duced HNF grazing pressure during spring in the Reloncaví Fjord
(3.7 mg C m2), high HNF grazing rates in the Baker Fjord
(51.9 mg C m2) could exert a partial control on BSP and growth
during this season. The total nanoflagellate biomass was higher
at stations close to the Penas Gulf, with more oceanic conditions
than stations well within the fjords and channels. For example,
the average integrated flagellate biomass decreased from the Trin-
idad Channel (789 ± mg C m2) to the Messier Channel
(162 ± mg C m2) and Eyre Fjord (115 ± mg C m2). Flagellates
were dominated by rounded individuals 2–10 lm in size (domi-
nance of 5 lm). In marine upwelling environments off Central
Chile (37°S), this increase in nanophytoplankton has been linked
to lower coastal salinities (33 psu) during periods of high river
outflow and higher haline stratification (Morales and Anabalón,
2012). Thus, both in upwelling systems and in the more oceanic
sector of estuarine systems, nanoplankton has been reported as
the dominant size fraction, contributing to maintain the system’s
production and providing food for higher trophic levels such as
copepods and fish larvae (Anabalón et al., 2007). This suggests that
the classical view of upwelling and estuarine systems as exporters
43
of large-sized cells towards benthic environments (Legendre and
Le Fevre, 1989) is alternated with equally important periods of
nanoflagellate dominance.
The relatively low integrated variability shown by bacterial
biomass (Fig. 7) and average secondary production
(113 ± 49 mg C m2; n = 7) suggests that bacterial mortality and
growth rates are, at least, within the same order of magnitude. An-
other factor explaining the relatively low variability in bacterial
biomass might be high inputs of DOC, due to a subsidy of dissolved
organic matter (DOM) from Patagonian rivers (Perakis and Hedin,
2002; Pantoja et al., 2011). Freshwater inputs could mediate an
important flux of DOM/POM and macro- and oligo-elements into
coastal areas (Raymond and Bauer, 2000). These are compartments
still absent from, or scarcely represented in, global biogeochemical
models. High DOC inputs (1.4 g C m3) were observed at St. 14
(unpublished data), indicating that DOC input from the Baker and
Pascua Rivers into the Martinez and Baker Fjords could fluctuate
between 121 and 259 t C d1. In the upper 25 m of St. 14, the aver-
age integrated DOC (33 g C m2) was one order of magnitude high-
er than POC (3–4 g C m2). DOC/POC ratios vary widely, and our
estimations agree well with values observed for temperate forest
watersheds (10:1), while for rivers draining, predominantly grass-
land areas, ratios may be closer to 1:1 (Schlesinger and Melack,
1981). In estuarine systems, microbes as well as mesozooplankton
might rely on this OM for 5–80% of their production, which in-
creases exponentially with increasing river discharge (Maranger
et al., 2005; Hoffman et al., 2008). Although it is widely accepted
that allochthonous OM inputs into estuarine systems are quantita-
44 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
Fig. 10. Conceptual model of carbon flux at the process station in the Martinez
Fjord, showing the average values of primary production (PP), bacterial secondary
production (BSP), vertical carbon flux, and grazing rates through heterotrophic
nanoflagellates (HNF), microzooplankton (Microzoo), and mesozooplankton (Mes-
ozoo) split into euphausiids, large and small copepods during November 2008. All
values are given in mg C m2 d1 (modified from González et al. (2010)).
tively more important, autochthonous OM is likely to provide more
readily available substrates for bacteria (Maranger et al., 2005).
In lakes, grazing and microbial-detrital trophic pathways sup-
port higher consumers. For instance, it has been estimated that
22–50% of total zooplankton ingestion, in terms of daily body car-
bon, is associated with allochthonous terrigenous sources (Pace
et al., 2004). The same situation was found in the Baker River estu-
ary, with copepod dependence on allochthonous OM sources
declining with increasing fjord trophy or microplankton availabil-
ity (Vargas et al., 2011). The same study found that dominant cope-
pods in the Baker Estuary (Acartia tonsa, Paracalanus parvus and
Calanus patagoniensis) may switch from low ingestion (1–
2 lg C ind.1 d1) of microplankton (diatoms and flagellates of
marine origins) and slightly depleted d13C values (24‰), to high
microplankton ingestion (4 and 12 lg C ind.1 d1) and enriched
d13C values (21‰). Various recent reports suggest that a signifi-
cant fraction of the OM in Chilean fjords is of allochthonous origin,
and can be channeled either directly to higher trophic levels (zoo-
plankton and fish) through the ingestion of detrital particles, or
indirectly through microbial food webs (i.e. allochthonous DOC –
bacteria – HNF – Zooplankton) (González et al., 2010, 2011; Vargas
et al., 2011). Contrastingly, it has been shown that in shallow estu-
aries with a substantially lower freshwater discharge (e.g. Ythan
Estuary, UK, with mean discharge of 5–9 m3 s1) material of mar-
ine origin dominates sedimentary POC throughout the year (Zet-
sche et al., 2011). Mass-balance calculations indicate that
terrestrial organic carbon is limited to sediments within a rela-
tively short distance from the river mouth, where this distance is
a function of river outflow (Shultz and Calder, 1976).
Insights into the dominance of allochthonous versus autochtho-
nous processes in the study area can be obtained through the C/N
ratio of the particulate organic matter fraction. We measured an
average C/N ratio of 6.7 ± 1.6 (n = 160) within the upper 50 m of
the study area, which is well within the generally accepted range
for marine material of 6–8 (Richards et al., 1997; Andrews et al.,
1998) and suggests a dominance of marine processes. On the con-
trary, the stations located close to the Pascua and Baker River
mouths (St. 8, 9, 10 and 12, 13, 15, 16) showed ratios of 9.1 ± 3.0
and 12.0 ± 2.0, respectively, closer to values reported for terrestrial
material (Thornton and McManus, 1994). The highest ratios were
measured in material collected from sediment traps deployed at
50 and 90 m depth, with average values of 13.3 ± 2.3 at St. 14, sug-
gesting a rapid utilization of the labile marine fraction, leaving the
refractory terrestrial material to sink towards the sediments. Bac-
teria are known to preferentially utilize labile organic carbon from
marine diatoms when a mixed carbon pool is available (Dai et al.,
2008). The highly significant correlation between gross primary
production and microbial respiration in the Reloncaví Fjord (Mon-
tero et al., 2011) suggests a strong coupling between the synthesis
of organic matter by Patagonian phytoplankton and its usage by
the microbial heterotrophic community.
Discharging fluids, whether derived from land or composed of
re-circulated seawater, will react with water column and sediment
components. Thus, terrestrially-derived fluids represent a pathway
for new material fluxes and reactions that may substantially in-
crease the concentrations of nutrients, carbon and metals, and will
be a source of biogeochemically important constituents for estua-
rine areas and the coastal ocean (Burnett et al., 2003). In general,
the groundwater flux (estimated with naturally-enriched radium
isotopes) to these estuarine/coastal waters should be ca. 40% of
the river water flux (Moore, 1996; Charette et al., 2001). A strong
terrestrial signature was especially conspicuous at the surface
layer of the Martinez and Baker Fjords (>85% of allochthonous car-
bon and d13C range of 23.5 to 26.4). The river discharge forms a
plume constituted by organic and inorganic sediments that on
average produces an annual inflow of 2.4  106 t y1 (assuming a
sediment load and water discharge of 50 g m3 and 1500 m3 s1,
respectively). Overall, riverine/estuarine DOM/POM is considered
to be recalcitrant and transported conservatively to the adjacent
coastal areas, such as the Penas Gulf (Mantoura and Woodward,
1983). However, the sharp terrestrial-marine gradients in biologi-
cal and physico-chemical conditions results in changes in the up-
take of DOM by bacteria (Zweifel, 1999) and chemical removal
processes (Lisitzin, 1995). Furthermore, sedimentary POC and
DOC that is loosely bound to mineral surfaces can be released dur-
ing resuspension events (Komada and Reimers, 2001). All of these
processes can contribute to a nonconservative behavior in
estuaries.
4.1. Fate of autotrophic production and pelagic–benthic coupling in
the area
Seasonal and shorter-term changes in estuarine stratification,
influenced by the annual cycle in ice melting plus precipitation
and events such as GLOF’s, can have profound influences on the
marine ecosystem. The strong halocline gives rise to a thin layer
of high stability in the water column, defining a natural barrier
with an upper brackish layer dominated by small copepods and
cladocerans, and a lower layer dominated by marine copepods
and euphausiids. The grazing impact of mesozooplankton was
mainly due to the small calanoid copepods, which removed
14.3% of daily PP at the process station. Large calanoid copepods
and the euphausiid Euphausia vallentini exerted a minor role
(3.8% and 0.2%) (Table 2; Fig. 10). The grazing impact of euphausi-
ids, and probably also large copepods, should be treated with
 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
caution because their abundance may have been understimated
during daytime trawls, due to the active daily vertical migration.
In addition, the copepod impact refers only to the few species of
copepods that were studied (Paracalanus parvus, Acartia spp. and
Calanus spp.). Small cyclopod copepods such as Oithona spp. were
not included in this study, despite their numerical dominance in
numerous estuarine systems (Nielsen and Andersen, 2002; Maar
et al., 2004), because our zooplankton mesh was too coarse (300
and 200 lm) to adequately collect such small copepods. In the
northern Patagonian fjords and channels (e.g. Reloncaví Fjord,
Moraleda Channel), chain-forming diatoms dominate the copepod
diet during the productive season (spring–summer months), while
nanoflagellates (ANF and HNF) and dinoflagellates, along with tin-
tinnids and aloricate choeotrich ciliates (i.e. Strombidium sp.), are
the main food items for copepods in the much less productive
winter months (González et al., 2010). This change highlights the
trophic plasticity of copepods, which are able to adjust their met-
abolic demands to the in situ availability of prey (Vargas et al.,
2008).
Beyond stratification, several other physical–chemical features
of Patagonian fjords will be potentially altered in a climate-change
scenario. Changes in water temperature, circulation, nutrient in-
puts, oxygen content, and acidity may have far-reaching biological
effects, including the fluxes of carbon through the pelagic food
web. It has been shown that a 2 °C warming of the upper water col-
umn may produce a 37% increase in the growth rate of some phy-
toplankton species (Eppley, 1972), whereas increased freshwater
discharge and stratification in the Baker Fjord produced adverse
conditions for ichthyoplankton (Maurolicus parvipinnis and Sprattus
fuegensis), resulting in a lower prey consumption per individual
and a reduction of growth rates in low salinity water (Landaeta
et al., 2001).
On average, primary production (PP) was four times higher than
bacterial secondary production (BSP), with BSP:PP ratios of
0.25 ± 0.22. The ratio was lower (0.14) at the three Messier Channel
stations (St. 17, 22 and 40), indicating that PP was seven times
greater than BSP. Northern Patagonian fjords such as the Reloncavi
(41°S) showed low BSP:PP values during spring (0.2) and high val-
ues in winter (3.7) (González et al., 2010), highlighting the high PP
in northern Patagonia during the productive season. Overall, sea-
sonal changes in this ratio are related more to sharp spring-to-win-
ter decreases in PP than to changes in bacterial biomass or
production.
The average POC concentrations in the upper 25 m of the water
column (247 mg C m3) were in the lower range of the reported
Table 2
Average individual grazing rates (mg C ind.1 d1), average integrated (upper 25 m water column) abundance (no. ind. m2), and grazing rates exerted by the integrated
communities (mg C m2 d1) of heterotrophic nanoflagellates (HNF), microzooplankton (MICR), represented by thecate dinoflagellates, small copepods, and euphausiids of the
species Euphausia vallentini at the ‘‘process station’’ (St. 14).
HNF MICR (thecate dinoflagellates)
Grazing rate (mg C ind.1 d1)
9.8  109a 1.9  109b
2
Integrate abundance (no. ind. m )
5.3  109 9.1  106f
Integrated grazing rate (mg C m2 d1)
51.9 0.018
a
Range: 20–33 bact. HNF1 h1 (or 9–16  109 mg C ind.1 d1).
b
2.3  106–1.7  106 lg C ind.1 d1.
c
0.7–7.3 lg C ind.1 d1.
d
1.9–18.8 lg C ind.1 d1.
e
Average of E. vallentini juveniles and adults 78.7 lg C ind.1 d1 (Sánchez et al., 2011).
f
Thecate dinoflagellates >20 lm (mainly Protoperidinium spp.) and copepod nauplii.
g
Paracalanus spp. and Acartia tonsa.
h
Calanus chilensis and Rhyncalanus spp.
i
Average of E. vallentini juveniles and adults.
45
values for the northern Reloncaví Fjord (200–600 mg C m3) but
higher than values recorded in the southern Strait of Magellan
(76 mg C m3; Fabiano et al., 1999). This latitudinal decrease ap-
pears to parallel the percentage of organic carbon in the sediments
from the same areas (from 5.3% to 3.8%, respectively, Silva and
Prego, 2002). These gradients could be due to more efficient pela-
gic–benthic coupling in northern than in southern Patagonian
fjords, which may result from higher spring–summer PP in north-
ern than in southern fjords. For example, PP estimates for the
Reloncaví (41°), Aysén (46°) and Baker Fjords (48°) were 1893,
831 and 360 mg C m2 d1. Another factor is the higher diatom
abundance in northern than in southern fjords that results in high
vertical POC fluxes. Consistently, the POC vertical flux at our pro-
cess station on the Martinez Fjord was ca. threefold lower than
in the Reloncaví Fjord (234 versus 725 mg C m2 d1). In general,
its seems that the POC export depended more on the variable input
of both particulate and dissolved matter from terrestrial systems
and was less coupled with local PP than in coastal areas. This
was evident in the nearby Chiloé and Aysén channels and fjords,
where surface sediments contain up to 50% terrestrial material
(Sepúlveda et al., 2005; Silva et al., 2011). In the Martinez Fjord
(Stn. 14), the total seston recorded in the sediment traps was
50.2 g m2 d1, from which only 4.2% was organic matter. Further
south at 51.5°S, the Almirante Montt Gulf does not receive impor-
tant river discharges and indeed is not affected by freshwater in-
puts. In this system, the total seston flux collected in sediment
traps was one order of magnitude lower than in the Martinez Fjord
(5.47 g m2 d1), and the relative organic matter contribution in-
creased to 22% (González, unpublished data). In general, one of
the most conspicuous particles collected in sediment traps were
faecal pellets from planktonic crustaceans (copepods and eup-
hausiids). Faecal pellets from copepods and krill were loaded with
fine sediments and minerals of possible lacustrine and riverine ori-
gins. This material may act as ballast to exacerbate settling velocity
and POC transport to the sediments (Lewis and Syvitski, 1983).
Overall, carbon fluxes and fjord system functioning are highly
variable, both spatially (northern to southern fjords and channels)
and seasonally. In winter, community respiration (CR) exceeds PP
in many lakes (Pace et al., 2004) and northern Patagonian fjords,
as the Reloncaví Fjord located at 41°300 S (Montero et al., 2011),
which contrasts with >1 ratios in spring (González et al., 2010).
The metabolism of Patagonian fjords is dominated by prokariotic
and protistan heterotrophs, and the strong input of allochthonous
organic matter from rivers and underground watershed obscure
the local productive processes over a gradient from river mouths
Small copepods Large copepods Euphausiids
0.00294c 0.00945d 0.0787e
17,520g 1458h 8.4i
51.5 13.8 0.66
46 H.E. González et al. / Progress in Oceanography 119 (2013) 32–47
to the coastal ocean. Thus, basin and seasonal scales seem to be
adequate for comparative quantitative analyses of material and en-
ergy fluxes at all trophic and organizational levels in Patagonian
fjords. The suggested annual framework (see Wetzel, 1995) would
allow the analysis of seasonal variability (i.e. freshwater discharges
and solar radiation among others) in the context of processes and
mechanisms from Patagonian fjords and channels such as CO2
sequestration during the productive season, and the relevance of
the microbial loop in allochthonous versus autochthonous organic
matter mineralization.
Acknowledgements
We thank the entire crew and all the scientists of the CIMAR 14-
2008 oceanographic cruise. We thank María José Calderón, Cesar
Barrales, Paola Reinoso, Francisco Gallardo, Eduardo Menschel
and María Inés Muñoz for collaboration during the sampling and
data analysis and Leticia Cisternas for euphausiid identification
and counting. We also thank Eduardo Menschel, Nicolás Sánchez
and Ricardo Giesecke for stimulating discussions on plankton
dynamics in Patagonian systems. This study was funded by the
Projects CIMAR14-Fiordos (CONA-C14F 08-05 and CONA-CF14
08-13). Additional support is also acknowledged from COPAS Grant
FONDAP-15010007 and COPAS Sur-Austral Grant PFB-31/2007.
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