Science of the Total Environment 669 (2019) 49–61

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Science of the Total Environment

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

Greenhouse gases, nutrients and the carbonate system in the Reloncaví

Fjord (Northern Chilean Patagonia): Implications on aquaculture of the
mussel, Mytilus chilensis, during an episodic volcanic eruption
Mariela A. Yevenes a,b, Nelson A. Lagos c,d, Laura Farías e,f, Cristian A. Vargas d,g,h,⁎
a
Departamento de Sistemas Acuáticos, Facultad de Ciencias Ambientales, Centro EULA, Universidad de Concepción, Chile
b
Centro de Recursos Hídricos para la Agricultura y la Minería (CRHIAM), Chile
c
Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Facultad de Ciencias, Universidad Santo Tomas, Santiago, Chile
d
Center for the Study of Multiple-Drivers on Marine Socio-Ecological Systems (MUSELS), Universidad de Concepción, Concepción, Chile
e
Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Chile
f
Centro de Ciencia del Clima y la Resiliencia (CR)2, Chile
g
Millennium Institute of Oceanography (IMO), Universidad de Concepción, Concepción, Chile
h
Aquatic Ecosystem Functioning Lab (LAFE), Department of Aquatic Systems, Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile, Universidad de Concepción, Chile

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• A large bloom of phytoplankton was de-

tected in the surface waters of the
Reloncaví fjord following the Calbuco
volcano eruption.
Sal O2
• Subsequent to the eruption, higher N2O, Low due to low salinity/low
CH4 and SO42− concentrations were ob- alkalinity waters driven by
freshwater runoff
served in Fjord surface waters.
• Optimal juvenile mussel growth was Optimum for mussel
observed in refugee subsurface depths growth and calcification

coinciding with increased aragonite sat-

uration.
Low due to high pCO2
• The observed trends may be valuable for Low O2 waters by organic
developing effective management strat- matter remineralization

egies for mussel aquaculture in the

Fjord.

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

Article history: This study investigates the immediate and mid-term effects of the biogeochemical variables input into the
Received 19 November 2018 Reloncaví fjord (41°40′S; 72°23′O) as a result of the eruption of Calbuco volcano. Reloncaví is an estuarine system
Received in revised form 1 March 2019 supporting one of the largest mussels farming production within Northern Chilean-Patagonia. Field-surveys were
Accepted 3 March 2019
conducted immediately after the volcanic eruption (23–30 April 2015), one month (May 2015), and five months
Available online 7 March 2019
posterior to the event (September 2015). Water samples were collected from three stations along the fjord to de-
Editor: Daniel Wunderlin termine greenhouse gases [GHG: methane (CH4), nitrous oxide (N2O)], nutrients [NO3−, NO2−, PO43−, Si(OH)4, sul-
phate (SO42−)], and carbonate systems parameters [total pH (pHT), temperature, salinity, dissolved oxygen (O2),
Keywords: and total alkalinity (AT)]. Additionally, the impact of physicochemical changes in the water column on juveniles
Chilean Patagonian Fjord of the produced Chilean blue mussel, Mytilus chilensis, was also studied. Following the eruption, a large phyto-
Carbonates system plankton bloom led to an increase in pHT, due to the uptake of dissolved-inorganic carbon in photic waters, po-
Nutrients tentially associated with the runoff of continental soil covered in volcanic ash. Indeed, high surface SO42− and GHG
were observed to be associated with river discharges. No direct evidence of the eruption was observed within the

⁎ Corresponding author at: Aquatic Ecosystem Functioning Lab (LAFE), Department of Aquatic Systems, Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile,
Universidad de Concepción, P.O. Box 160-C, Concepción, Chile.
E-mail address: [email protected] (C.A. Vargas).

https://doi.org/10.1016/j.scitotenv.2019.03.037
0048-9697/© 2019 Elsevier B.V. All rights reserved.
50 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

Mussel farming carbonate system. Notwithstanding, a vertical pattern was observed, with an undersaturation of aragonite (ΩAr
Volcanic event b 1) both in brackish surface (b3 m) and deep waters (N10 m), and saturated values in subsurface waters (3 to
7 m). Simultaneously, juvenile mussel shells showed maximized length and weight at 4 m depth. Results suggest
a localized impact of the volcanic eruption on surface GHG, nutrients and short-term effects on the carbonate sys-
tem. Optimal conditions for mussel calcification were identified within a subsurface refuge in the fjord. These
specific attributes can be integrated into adaptation strategies by the mussel aquaculture industry to confront
ocean acidification and changing runoff conditions.
© 2019 Elsevier B.V. All rights reserved.

1. Introduction increase in volcanic ash covering soils may result in high levels of dis-
solved silica in rivers, thus increasing the flux into fjord environments.
Natural disasters such as earthquakes and volcanic eruptions pro- As a result, phytoplankton productivity and community structure may
vide excellent opportunities to evaluate effects of mesoscale and large be affected (Balseiro et al., 2014; Vandekerkhove et al., 2016). More-
disturbances on ecosystems (Wang et al., 2012). These disturbances over, ash fallout can also induce acidification of soils (Borie et al.,
can leave ephemeral or long lasting ecological effects on spatial and 2002), thus leading to low pH events in adjacent fjord areas (Santana-
temporal patterns of marine communities (e.g. Jaramillo et al., 2017). Casiano et al., 2013). It is well known that low pH/high pCO2 conditions
Thus, disasters within ecosystem have a fundamental effect on material can have a negative impact on marine calcifiers, such as corals, sea ur-
flux (minerals) across the land-ocean interface. Fjords are good exam- chins, gastropods, and mussels (Kroeker et al., 2010). Specifically, the
ples of these events; they cover approximately 7 to 10% of the global endemic Chilean mussel, Mytilus chilensis, is present in the intertidal
ocean (Sauer et al., 2016) and represent an important interface and reg- zone down to 25 m depth throughout the Chilean coastline. This specie
ulating area between freshwater systems (i.e., lakes and rivers), glaci- can withstand high salinity and brackish water, for example in river
ated terrain, and the coastal ocean. Moreover, fjord ecosystems are mouths or close to glaciers, subsisting through the filtration of
highly valuable in terms of different ecosystems services, such as nutri- microalgae (Molinet-Flores et al., 2015; Ríos et al., 2018). Mytilus
ent availability, carbon cycling, water quality for aquaculture produc- chilensis is the main farmed shellfish, and represents a considerable frac-
tion, and pollution control (Iriarte et al., 2010). In consequence, many tion of aquaculture production in Chile of up to approximately 238,088
studies highlight the threat of global changes on estuarine and fjord tons annually, representing the 96,6% shellfish production (Sauer et al.,
coastal systems (Iriarte et al., 2010; Letelier et al., 2011; Silva and 2016; Molinet-Flores et al., 2015; Castillo et al., 2016). Relative to this,
Vargas, 2014; Vargas et al., 2017a). the Reloncaví Fjord is one of the most important areas for mussel seed
The impacts of anthropogenic activities (such as land use changes, production (with 99% of production concentrated within these waters),
nutrient loading, river damming, fishing, mussel farming) on biogeo- predominantly made up by the Chilean mussel specie, Mytilus chilensis.
chemical cycles have been well documented for fjord environments, Therefore, the treat of volcanic eruptions also has major implications
for example research by Filgueira et al. (2010) in Sweden and Norway. on the socio-ecological systems of mussel farming in the region. Re-
Recently, similar impacts have also been documented in fjord ecosys- cently, Salas-Yanquin et al. (2018) identified the physiological impact
tems of Chilean Patagonia (Silva and Vargas, 2014; Mayr et al., 2014; of the presence of volcanic ash from Calbuco Volcano on the diet of
Iriarte et al., 2017; Farías et al., 2017; Vargas et al., 2017b; Yevenes Mytilus chilensis and their ability to select particles during feeding.
et al., 2017). Aquaculture production in fjord ecosystems largely de- This study aims to investigate the posteriori potential effect of a high
pends on the integrity of different ecological, biophysical, and biogeo- magnitude volcanic eruption through the study of greenhouse gases
chemical processes, which are subjected to multiple sources of (such as CH4 and N2O), nutrients, and the carbonate system in the
variability (Barria et al., 2012; Lara et al., 2016). Fjords are sensitive to Reloncaví Fjord during autumn (April), winter (May) and spring (Sep-
local acidification processes, mostly due to the influence of riverine wa- tember) 2015. Furthermore, this study aims to determine the impact
ters with a low total alkalinity (AT), which in turns reduces the buffering of potential changes in the carbonate system on the condition of mussel
capacity of receiving waters (Chierici and Fransson, 2009). Thus, an in- shells in a nearby farming area.
crease in freshwater fluxes into fjord ecosystems has the potential not
only to decrease seawater pH and reduce the saturation state of calcium 2. Materials and methods
carbonate (Ω), but also induce a shift in the NH3–NH4+ equilibrium to-
wards NH4+ (Freing et al., 2012), affecting nitrification and associated 2.1. Study area
N2O generation. Moreover, fjords store large amounts of organic carbon,
with burial rates exceeding double the average rates in global oceans This study was carried out in the Reloncaví Fjord (41° 40′S–72° 32′W
(Smith et al., 2015; Mohr et al., 2017). However, the influence of epi- ′) located in northern Chilean Patagonia (Fig. 1). From the head to the
sodic disturbances, such as volcanic eruptions, in mobilizing nitrogen, mouth, the fjord has a total length of 55 km and a width of almost
carbon and greenhouse gases in fjord environments remains poorly 3 km in its widest section, and is characterized to have a glacial origin
studied (Mohr et al., 2017). (Valle-Levinson et al., 2007; Araya-Vergara, 2008). The main source of
The Reloncaví Fjord area has been affected numerous times by the freshwater comes from the Puelo River, with an annual average of
eruption of the Calbuco Volcano (41°20′S, southern Chile), with erup- 650 m3 s−1 (León-Muñoz et al., 2013). Winds have a marked seasonal
tions registered in 1961, 1972, and more recently during April 22th variability, during winter predominant winds are from the north
2015. During the last eruption, Calbuco Volcano ejected a significant while during summer winds from the south and southeast are preva-
ash plume that required the evacuation of nearby areas, disrupted aerial lent, with magnitudes that are generally between 9 m s−1 to 15 m s−1
traffic, and damaged buildings in Chile (Van Eaton et al., 2016). The vol- (Saavedra et al., 2010; Castillo et al., 2012). The fjord area presents a
canic eruption produced a stratospheric column (N15 km height; marked hydrographical variability, related to regimes of high rainfall
0,27 km3) of porphyritic basaltic andesite (SiO2). The tephra fall oc- and ice melt (Castillo and Pizarro, 2009). High levels of freshwater
curred over the northeast area of the volcano, while the finest ash was input from tributary rivers generate considerable salinity variations
transported and deposited over northern Patagonia in Chile and that characterize the distinct water masses present in this region,
Argentina (Romero et al., 2016). It is widely acknowledged that an made up of channels and fjords (León-Muñoz et al., 2013). As a result
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 51

Fig. 1. Study area and stations located in Reloncaví Fjord, Northern Chilean Patagonia.

a strong spatial salinity gradient exists in the surface fraction (González (CTDO) (SeaBird 25) to 50 m depth. Chlorophyll measurements
et al., 2010), with a stratified water column characterized by a marked (Chl-a) were conducted with a Fluoroprobe sensor (bbe-Moldaenke,
pycnocline between the upper layer (0 to 5 m depth) and the subsurface Kiel, Germany) (Beutler et al., 2002); a highly sensitive measuring
layer below 5 m depth (Valle-Levinson et al., 2007). Below this narrow instrument for the analysis of chlorophyll, including the determina-
layer, there is a relatively homogenous layer of marine water predomi- tion of algal class. Chlorophyll measurements were calibrated by
nantly from sub-Antarctic origin, described as modified sub-Antarctic contrasting with fluorometry analysis (Turner Design TD-700),
water or MSAAW (Sievers and Silva, 2006). using acetone (90% v/v) for the pigment extraction of discrete sam-
ples according to standard procedures (Parsons et al., 1984). Sub-
2.2. Water sampling samples for pH measurements were stored in borosilicate BOD
bottles with ground-glass stoppers without air bubbles and
Seasonal water sampling was made during autumn (30th April), transported to the field lab where pH was measured within 2 h of
winter (29th May 2015) and spring (25th September 2015). Water collection. Water samples for AT were poisoned with 50 μL of satu-
samples from three stations (st.1: −41° 43′ 57′ S–72° 32′ 50.8″W′; rated HgCl2 solution and stored in 500 mL borosilicate BOD bottles
st.2: −41° 41′ 40.4′ S–72° 26′ 24.6″W′; st.3: −41° 37′ 50.3′ S–72° 20′ with ground-glass stoppers, lightly coated with Apiezon L® grease,
55.6″W′) were collected along the Reloncaví estuary over five depths and kept in darkness at room temperature (Dickson et al., 2007).
(1, 5, 10, 25, 50 m depth) (Fig. 1). Our study was focused on the For logistic support, samples for N2O and CH4 analysis were only col-
short-term response during autumn, winter and the long-term con- lected in April and May, in 20 mL glass vials (by triplicate), treated
sequences on early spring conditions. The longitudinal distribution with 50 μL of saturated HgCl2 solution (6 g L−1) and sealed with her-
of sampling stations was based on the location of one of the largest metic stoppers and aluminium caps (Wilson et al., 2018). These sam-
mussel-farming sites near the fjord mouth (ORIZON Company near ples were stored at ambient temperature for posterior analysis in the
Chaparano Bay, Stn. 1), and the location of one of the main river dis- laboratory. Additionally, water samples for nutrient analysis were
charges in the area (Puelo River in the mid- portion of the fjord at Stn filtered through a 0.45 μm Cellulose acetate (CA) membrane and col-
3). Discrete water samples were collected in triplicate using Niskin lected in 15 mL falcon tubes, and then frozen for later analysis in the
bottles (General Oceanic®, GO-FLO Niskin bottles sampling), for laboratory. Samples for SO42− concentrations were collected in falcon
SO42−, Chlorophyll a (Chl-a), Total pH (pHT), Total Alkalinity (AT), conical tubes of 50 mL and analysed with ion chromatographic
N2O, CH4 and nutrients (i.e., NO3−, NO2−, PO43−, Si(OH)4). Continuous method with chemistry suppression, based on standard methods
profiles of temperature, salinity, and dissolved oxygen were ob- 4110 B, using Dionex ICS2100 equipment, through an anionic AS11
tained using a Conductivity-Temperature-Dissolved Oxygen Sonde High Capacity, with concentrations above 0.1 mg L−1.
52 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

2.3. Carbonate system parameters The nutrient analyses (NO3−, PO43− and Si(OH)4) were carried out
using colorimetric techniques (Grasshoff et al., 1983), with an
Samples for pH measurement were collected and directly autoanalyzer SEAL analytical (AA3). Calibration curves were performed
transported inland so that pH was measured within a 2 h timeframe previous to each set of measurements, using primary standard. The pre-
after collection (Vargas et al., 2016). pH samples were collected in cision and detection limit of the method was, ±50 nM and 20 nM for
50 mL syringes and immediately transferred to a 25 mL thermo stated NO3−, ±30 nM and 110 nM for PO4−3− and ±70 nM and 0.030 μM for
cell at 25.0 ± 0.1 °C for standardization, with a pH meter Metrohm® Si(OH)4, respectively.
using a glass combined double junction Ag/AgCl electrode (Metrohm
model 6.0258.600) calibrated with 8.089 Tris buffer at 25.0 °C (DOE, 2.5. Biological sampling
1994), and therefore registered on the total hydrogen ion scale (pHT).
AT was determined using the open cell titration method (Dickson During May 2015, juvenile individuals of M. chilensis (b2 cms, mus-
et al., 2007), using an automatic Alkalinity Tritrator Model AS-ALK2 sels' seeds) from the same cohort were randomly collected from pegged
Apollo SciTech. The AS-ALK2 system is equipped with a combination ropes (6 m in length) at three different depths (1, 3 and 4 m). At each
pH electrode (8102BNUWP, Thermo Scientific, USA) and temperature depth, all mussels that were attached along ca. 10 cm length of the set-
probe for temperature control (Star ATC probe, Thermo Scientific, tlement ropes were collected. Among 90–105 mussel seeds were col-
USA) connected to a pH meter (Orion Star A211 pH meter, Thermo Sci- lected from each depth level, transported (ca. 4 °C using ice-pack
entific, USA). All samples were analysed at 25 °C (±0.1 °C) with temper- lasting for ca. 6 h), to the laboratory under chilled conditions, and
ature regulation using a water bath (Lab Companion CW-05G). The then frozen (−20 °C) for posterior processing in the laboratory, which
accuracy was controlled against a certified reference material (CRM, was performed during Sept. 2015. Taxonomic identification based on
supplied by Andrew Dickson, Scripps Institution of Oceanography, San shell shape and lack of external ribs was used to minimize potential
Diego, USA) and the AT repeatability averaged 2–3 μM kg−1. bias in including other species mussels in the processing. Several mor-
pHT and AT data were applied to the program CO2SYS (Pierrot et al., phometric variables were recorded for each mussel, including total
2006) to calculate aragonite saturation state (ΩAr), and other carbonate wet weight, dry shell weight, and soft tissue weight (after 6 h at 60 °C,
parameters (e.g. pCO2). The dissociation constants for carbonic acid (K1 Memmert®) using an analytical balance (Metler Toledo); maximum
and K2) were used by Dickson et al. (2007) for salinities between N30 shell length, shell height, and shell thickness (measured using a digital
PSU, Millero (2010) for estuarine waters between 1 and 30 PSU, and caliper, Mitutoyo®). Shell thickness corresponds to the average of 4 sep-
for freshwater samples in the mid- and upper river sampling stations. arate measurements taken from newly forming shell growth along the
KHSO4 was determined for both freshwater and seawater samples edge of the mussel valves (e.g., Lagos et al., 2016). Finally, the relative
(Dickson et al., 2007). shell condition index is estimated through calculating the total dry
shell weight as a percentage of the total weight (i.e., [Dry shell weight
/ Total weight] × 100).
2.4. Determination of nutrients, nitrous oxide and methane
2.6. Statistical analysis
N2O and CH4 detection was made via the generation of a 5 mL ultra-
pure helium headspace into the vial, by a gas-tight syringe, and main- The Pearson correlation coefficient and lineal regression were used
taining the gas and liquid phases in equilibrium at 40 °C within the to define relationships among variables, including GHG, nutrient con-
vial, allowing for the equilibrium of the headspace in the vial (Farías centrations and the carbonate system as parameters (Munro, 2005).
et al., 2015). N2O dissolved in the seawater was measured through Mussel measurements were subjected to descriptive statistical analysis
gas–liquid equilibration in the vial at 40 °C for 15 min under agitation, to define trends in the frequency distribution of variables over depth.
using a headspace autosampler device (HP Agilent) followed by quanti- The Kolmogorov-Smirnov test for normality was applied, and several
fication via gas chromatography (GC). N2O was analysed in a distribution moments were also calculated (e.g., mean, standard devia-
SHIMADZU-17A gas chromatograph equipped at 350 °C, using a capil- tion, median and its 95% confidence interval), due to the fact distribu-
lary column and injector operated at 60 °C and 300 °C, respectively, tions presented significant deviations from the normality (see
and connected to the autosampler (Farías et al., 2015). Ar/CH4 gas mix Supplementary material S1). The Kruskal-Wallis test was applied to
was used as a carrier gas with a flux of 6.5 mL min−1. compare the medians of each variable between mussels collected over
CH4 was analysed in a Shimadzu 17A gas chromatograph equipped different depths, and results were described using median (±IQR,
by a flame ionization detector (FID) at 250 °C, through and injector Inter Quartile Range). A Principal Component Analysis was also esti-
and a capillary column GS-Q at operated to 180° and 30 °C, respectively, mated to describe the variation in the set of physical-chemical and bio-
using N2 as carrier gas with a flux of 3 mL min−1, and GC connected to logical variables.
the mentioned autosampler (Farías et al., 2015).
A calibration curve was made using several concentrations for N2O 3. Results and discussion
(0.10 air, 0.5 and 1 ppmv) and CH4 (1, air, 5 and 10 ppmv) using
Matheson gas standards whose nominal concentrations were checked The eruption of Calbuco volcano released high levels of particles and
using set of high-pressure primary gas standards, prepared for the gases throughout its area of influence, including the estuarine waters of
SCOR Working Group by John Bullister and David Wisegarver at NOAA Reloncaví fjord. Throughout the three periods of field sampling, the
Pacific Marine and Environmental Laboratory (PMEL). One batch, re- fjord presented a vertical salinity distribution that clearly divided the
ferred to as the air ratio standard (ARS), had N2O and CH4 mole fractions water column into two layers, separated by a marked halocline. In the
similar to modern air, and the other batch, referred to as the water ratio upper 5 m of the surface water salinity was approximately 8.84 to
standard (WRS), had higher had N2O and CH4 mole fractions for the cal- 15.2, and in the subsurface layer below the 5 m from 28.2 to 32.87
ibration of high-concentration water samples (Wilson et al., 2018). (Fig. 2a–i). Several studies have identified that the water in the
Both, the ECD and FID detectors responded linearly to these concentra- Reloncaví fjord are seasonally dominated by estuarine waters (EW) in
tion ranges. The analytical error of the N2O and CH4 analyses was b3% the upper layer to 5 m depth, and in the deeper layer there is more
and 5%, respectively. The uncertainty of the measurements was calcu- cold and dense modified subantarctic water (MSAAW) (González
lated from the standard deviation of the triplicate measurements by et al., 2010; Castillo et al., 2016). In this study surface temperature
depth. Measurements with a variation coefficient N10% were not in- fluctuated between 10.4 °C and 13.3 °C, with the lowest values recorded
volved in the gas record (Farías et al., 2015). in Stn. 1 during May, and the highest at Stn. 1 in April. In terms of
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 53

Fig. 2. Physical-chemical distribution for the three stations along the Reloncaví Fjord, including Temperature (°C) (A, B, C), Salinity (D, E, F), and Dissolved Oxygen (mL L−1) (G, H, I), during
field visits in April (A, D, G), May (B, E, H) and September (C, F, I).

dissolved oxygen, well-oxygenated waters of approximately 8 mL L−1 3.1. Biogeochemistry of estuarine waters
were observed at the surface of brackish waters, but surface O2 falls
below 4 mL L−1 during the second sampling period, especially at Stn. The occurrence of volcanic eruptions in Patagonia has led high con-
1, which is the station closest to the mouth of the Reloncaví fjord centrations of SO42− in surrounding areas (Bia et al., 2015). As a conse-
(Fig. 2a–i). Castillo et al. (2016) has described the oceanographic quence high levels of SO42− have been observed in surface waters
conditions of Reloncaví fjord to have a well-stratified water column, in- (0–5 m depth) of the fjord, after April relatively high levels were re-
cluding a thin surface layer of brackish water with mean salinities be- corded (Table 1), between b500 to 2300 mg L−1 that decreased over
tween 10.4 ± 1.4 (spring) and 13.2 ± 2.5 (autumn). time due to dilution from precipitation and snowmelt. During May,
Additionally, Chilean Patagonia is characterized by continual humid the lowest surface SO42− concentrations were recorded in the surface
conditions throughout the year, subjected to abundant precipitation layer (b500 mg L−1). The fact that field sampling was carried out imme-
(around 3000 mm year−1) during winter (June to August) and glacial diately after the eruption, and in conditions of zero rainfall during the
meltwater during spring/summer (September–January) (Garreaud, eruption event may explain the SO42− increase in surface waters.
2009; León-Muñoz et al., 2013). Throughout the study period the pre- Flaathen and Gislason (2007) suggest that the effect of H2SO4 coming
cipitation was recorded at the Puelo meteorological station (41° 39′ from volcanic eruptions is both temporally and spatially dependent;
3.96″S 72° 18′42.12″O); 353,4 mm recorded during April; 834 mm dur- for example the location of Calbuco volcano is high latitude and is ex-
ing May, and 2430 mm during September 2015 (available at http:// posed to high solar radiation during daytime (during autumn), thus
explorador.cr2.cl). This precipitation will eventually contribute to river leading to an intense local H2SO4 contamination due to the high oxida-
runoff. Thus, river discharges of glacial origin (Petrohué, Puelo and tion rate of SO2 into SO42−. However, in general, studies in Patagonian
Cochamo Rivers) towards the Reloncaví fjord can reach a maximum surface waters have indicated that SO42− concentrations do no exceed
flow from July to September, with flow intensities reaching up to the detection limits of the instrumental methods (Beamud et al., 2013).
~1500 m3 s−1 (Castillo et al., 2016), in turn this is an important driver Volcanic fallout into aqueous environments leads to the dissolution
of biogeochemical activity in the case of a volcanic eruption. of adsorbed metal salts and aerosols, increasing the bioavailability of

Table 1
Average of environmental variables (mean ± standard deviation) values for the three stations along the Reloncaví fjord at different depth.

Depth N2O (nM) N2O (nM) AOU (μM) AOU (μM) % saturation % saturation CH4 (nM) CH4 (nM) % saturation % saturation SO2−
4 SO24-
April May April May N2 O N2O April May CH4 CH4 (mg L−1) (mg L−1)
April May April May April May

1 22.9 ± 3.75 9.7 ± 0.34 120 ± 8.0 95 ± 25.2 219 ± 33.2 84.3 ± 4.1 15.8 ± 13.1 36.3 ± 10.5 553 ± 456 1169 ± 318 1991 ± 379 257 ± 144
5 30.7 ± 1.52 11.9 ± 1.23 143 ± 16.5 125 ± 12.7 316 ± 14.9 119 ± 12.9 6.30 ± 5.19 6.00 ± 3.93 243 ± 200 227 ± 149 1292 ± 128 –
10 29.8 ± 4.52 12.9 ± 1.44 145 ± 8.2 136 ± 6.70 304 ± 46.0 131 ± 14.4 2.44 ± 0.78 2.18 ± 1.01 94.3 ± 30.4 83.6 ± 38.7 – –
25 31.7 ± 4.94 12.9 ± 0.34 38.8 ± 7.0 32.6 ± 14.6 319 ± 48.3 130 ± 3.40 2.93 ± 1.16 3.32 ± 2.65 112 ± 43.6 191 ± 15.4 – –
50 34.0 ± 1.50 13.5 ± 0.18 62.6 ± 18.1 56.8 ± 83.9 342 ± 15.8 137 ± 2.00 1.63 ± 0.67 8.74 ± 9.10 62.2 ± 25.6 335 ± 349 – 1794 ± 347
54 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

Fig. 3. Nutrient distribution for the three stations along the Reloncaví Fjord: NO− 3−
3 (μM) (A, B, C), PO4 (μM) (D, E, F), Si(OH)4 (μM) (G, H, I) and N:P (J, K, L).

key nutrients (Jones and Gislason, 2008). However, low NO3− and PO43− entrainment of nutrients between layers, from subsurface waters to sur-
values (b5 μM) were found in the Reloncaví Fjord. NO3− concentrations face waters, as observed in other estuarine systems (Silva and Vargas,
in the entire water column varied between 0.77 μM and 23.3 μM, with 2014).
the lowest concentrations in the surface waters up to 5 m depth within The region of Patagonia is understood to undergo a potential light
the estuary (Stn. 1). These low concentrations are mainly due to the di- limitation during autumn (Iriarte et al., 2017), resulting in low chloro-
lution effect of freshwater discharges from the Puelo River, due to melt- phyll and phytoplankton biomass in surface waters. However, this
waters and rainfall (León-Muñoz et al., 2013). In contrast, the highest study indicated that a maximum Chl-a of 20–25 mg L−1 was observed
NO3− concentrations in subsurface waters (Stn. 3) were observed near during the April sampling period, in surface waters, at approximately
to the Puelo River in April during the first sampling period (Fig. 3a–c). 4 m depth (Fig. 4a). Thus indicating that the phytoplankton bloom is po-
NO3− concentrations increased in subsurface waters as salinity in- tentially associated with the utilization of available nutrients. However,
creased, this is a characteristic of sub-Antarctic waters entering the es- during May, Chl-a concentration decreased and was homogeneous
tuary (Fig. 3a–c). The nutrient results are consistent with the previous throughout the entire water column (b2 μg L−1, Fig. 4b). Another phy-
results reported by several authors, indicating that freshwater from riv- toplankton bloom, but deeper and less intense, was observed in the sub-
ers inputs silicic acid into the surface waters, due to meltwater and rain- surface layer during September, reaching a Chl-a maximum of 15 μg L−1
fall (León-Muñoz et al., 2013; Farías et al., 2017). Instead, the overlaying between 10 and 15 m depth (Fig. 4c). This has been previously reported
marine subsurface water is nutrient rich in both nitrogen and phospho- during spring (Iriarte et al., 2007).
rus (Yevenes et al., 2017; Farías et al., 2017; Iriarte et al., 2017). It is
likely that the highest Si(OH)4 levels recorded post eruption led to 3.2. Distribution of the carbonate system and greenhouse gases
high biogenic productivity in the area and contributed to the atypical
phytoplankton bloom (Fig. 3j–l). One important characteristic of north- Volcano eruptions can disturb the carbonate system, inducing
ern Chilean Patagonia is the presence of andosol-type soil, that brings abrupt acidification in the top layer of the ocean (Flaathen and
about abundant dissolved Si(OH)4 concentrations in the surrounding Gislason, 2007). These results indicate that pHT and AT values ranged
aquatic system as a product of river runoff (Vandekerkhove et al., from 7.67 up to 8.06 and 144 to 2136 in the upper 10 m depth of the
2016). High salinity and nutrient-rich subsurface waters were present brackish layer, respectively (Fig. 4g–i). Relative to these results, no
under 10 m depth (Fig. 3a–c), which is typically associated with the clear effect of the volcanic eruption on local acidification events were
intrusion of deep water masses, which is modified sub-Antarctic observed in the surface waters of the fjord during April and the subse-
water entering through the mouth of Reloncaví estuary (Castillo et al., quent months. It is likely that surface pHT decreased due to the CO2 up-
2016). Nevertheless, estuarine stratification could limit mixing and take associated with the high Chl-a concentration during these periods
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 55

Fig. 4. Carbonate system distribution for the three stations along the Reloncaví Fjord: Chla (A, B, C), pHT (D, E, F), AT (G, H, I), pCO2 (J, K, L), ΩAr Ñ during field visits in April (A, D, G, J, M), May
(B, E, H, K, N) and September (C, F, I, L, Ñ) during 2015.

(Fig. 4a, c), mainly due to the development of a large bloom of phyto- brackish waters are associated with low-salinity conditions in these
plankton during the days following the eruption. Vergara et al. (2016) permanently stratified waters. In turn, it is likely that corrosive waters
continuously studied the carbonate system within the top surface for CaCO3 in the surface layer (i.e. upper 4 m depth) are a frequent oc-
layer of the fjord continually for one month after the eruption, using currence (Torres et al., 2011; Silva et al., 2011; Alarcón et al., 2015).
high temporal resolution data (every 1 h) and with pH values as low Low pHT, high pCO2, and CaCO3 sub-saturated waters (ΩAr) were ob-
as 7.6 (≈0.4 pH units) during June. This value was closely related to served in subsurface waters below 10 m depth, mainly during April
the minimum pHT values (7.2). It apparently took a few weeks after and May field sampling periods, mostly associated with respiration of
the precipitation events to flush out the readily soluble constituents both autochthonous and allochthonous organic matter (Waldbusser
near to the headwaters of the Reloncaví Fjord. pHT also decreased and Salisbury, 2014). Zhai et al. (2015) discovered that bivalve species
below 7.7 in subsurface waters, similar to the situation observed for were affected by the presence of short-term aragonite corrosive waters
O2 concentration. A good correlation between pHT and the Apparent (ΩAr) in the very shallow waters of the Northern Yellow Sea below 15 m
Oxygen Utilization (AOU) implied the influence of organic matter respi- depth. This raised the concern that a greater effort is required by the lo-
ration on the pHT levels (Fig. 5c), however; this was not the case for the cally cultured bivalve species in order to calcify.
pCO2 and/or ΩAr (Fig. 5b, d). Instead, AT was highly correlated with sa- Unexpectedly high N2O concentrations (22.9 ± 3.75 nM) were re-
linity due to the influence of low AT in freshwater, especially during corded in the surface layer of the Reloncaví Fjord, predominantly during
April (r2 = 0.81, r = p b 0.05), and very highly correlated during Sep- April. In comparison, previous studies report that the maximum average
tember (r2 = 0.96, r = p b 0.05) (Fig. 5a). Certainly, surface waters reached 12 ± 2 nM (Yevenes et al., 2017). Higher concentrations were
were undersaturated in CO2, with pCO2 b 400 μatm mainly during observed in Stn. 3, which is closer to Puelo River discharge. However,
April and September, however levels rapidly increased with depth, no significant correlations were found between N2O and salinity in the
from subsurface waters up to N1000 μatm. The low pCO2 conditions in surface water layer, implying a continental origin (Fig. 7a, b). Similarly,
56 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

Fig. 5. Relationship between A) Salinity and Alkalinity (AT), B) AOU and pCO2, C) AOU and pHT, D) AOU and ΩAr. Each figure includes data from the three field visits, April (Green), May
(blue), September (red). (*) Indicates a significant relationship between variables.

riverine waters within the surface layer showed N2O concentrations CH4 in fjords originates from anoxic sediments (Borges and Abril, 2011;
that were twice as high as recorded by Yevenes et al. (2017), with satu- Borges et al., 2016). However, Farías et al. (2017) identified that the bot-
ration levels reaching as high as 342% in April. This coincided with min- tom waters of the Reloncaví Fjord did not suggest consistently higher
imum nitrate (NO3−) levels during the same field-sampling period. The CH4 concentrations compared to surface layers (Fig. 6c, d).
observed N2O saturation is apparently the result of overall denitrifica-
tion in brackish water, since denitrification should not occur in well- 3.3. Implications for shellfish farming industry
oxygenated waters (Yevenes et al., 2017). Excess N2O (ΔN2O) is one
of the most relevant biogeochemical factors in estimating N2O produc- Calcifying organisms, such as marine molluscs, are exceptionally vul-
tion. If AOU and NO3− are associated with ΔN2O, it may indicate that nerable to fluctuations in carbon chemistry (Byrne, 2011; Gazeau et al.,
N2O is of biogeochemical origin (Yoshinari, 1976). This is supported 2013). Figs. 9 and S1 as supplementary material show the morphomet-
by the significant linear relationship between ΔN2O and AOU, and ric measurements recorded from juvenile's edible mussels, Mytilus
ΔN2O and NO3−, during April and May, respectively (Fig. 8a, c). Apparent chilensis, collected from settlement ropes within the Reloncaví Fjord.
N2O production can also be estimated through the consumption of O2 With the exception of shell thickness, that was homogeneous across
(AOU), based on the remineralization of particulate organic matter as- depth [Median ± IQR; Depth 1: 0.10 mm ± 0.05; Depth 3 m:
sociated with nitrification (Nevison et al., 2003). Oxygen consumption 0.09 mm ± 0.03; Depth 4 m: 0.10 mm ± 0.04; Kruskal Wallis, H =
due to the oxidation of organic matter suggests that NO3− is formed dur- 3.62; p = 0.164], the rest of variables showed significantly low values
ing nitrification, and as a result N2O is also produced (Farías et al., 2015). in the upper 3 m of the water column, however maximum values are
CH4 concentrations varied between 0.27 and 44.4 nM throughout consistently attained at 4 m depth (p b 0.05). In fact, we found increased
the entire water column during April and May, with a maximum CH4 shell thickness in the less favorable conditions in the upper depth layer,
concentration of 44.4 nM, equivalent to 1411% saturation, observed at which may result as compensation in order to maintain shell strength
1 m depth (Stn. 3) in May (Fig. 6c, d) near to the mouth of Puelo and functionality. Previous studies also evidenced that under favorable
River. The observed concentrations of CH4 in surface waters were within environmental conditions for shell precipitation (NΩAr), mussel seeds
the same range reported by previous studies between 16.97 and 151 nM adapt to elongate a thin shell with a thicker periostracum, however, in
(Farías et al., 2017). Towards Stn. 3, surface CH4 concentrations doubled less favorable conditions the strategy is to increase the shell thickness
throughout both campaigns. Moreover, a strong correlation between (Osores et al., 2017). Moreover, shell weight showed a significant in-
surface CH4 concentrations with the pCO2 and Si(OH)4 confirm the crease at 4 m depth (0,10 mg ± 0,04;) respect to more surface levels
input into the fjord of continental CH4 sources from soils. Surface waters (Depth 1 and 3 m: 0.05 mg ± 0.08) (H = 10.55; p = 0.005). Similar pat-
were over-saturated with CH4, mainly during May. It is well known that tern was found in the soft tissue weight of the mussel seeds (Depth 1:
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 57

Fig. 6. Greenhouse gas distribution for the three stations along the Reloncaví Fjord: (N2O and CH4) during April and May field visits, including N2O (nM) (A, B) and CH4 (nM)(C, D).
September was not recorded.

0.07 mg ± 0.05; Depth 3 m: 0.07 mm ± 0.07; Depth 4 m: 0.10 mm ± increments in length and weight of the mussel seeds as increased the
0.11; H = 6.96; p = 0.031). Molinet-Flores et al. (2015) also observed deep levels, the shell condition index, an integrative measure, indicate
that in natural banks, the condition index recorded in mussels living a progressive increment of the shell weight in relation to tissue weight
in the upper 7 m depth was significantly greater than in mussels col- of the individuals raised at 4 m depth (Shell condition index: 41.1% ± 9;
lected from deeper habitats. In addition, shell size measurements Depth 3 m: 44% ± 8; Depth 4 m: 48% ± 6; H = 6.56; p = 0.038). Inter-
showed the same significant pattern of vertical variability (e.g., Shell estingly, morphometric analyses of mussel seeds demonstrated that at
Length: Depth 1: 13.3 mm ± 5.9; Depth 3 m: 12.8 mm ± 5.77; Depth 4 m depth (or the “optimum layer”) some attributes related with shell
4 m: 15.2 mm ± 6.8; H = 6.56; p = 0.038). Finally, the proportional length, weight, and biomass reached maximum levels (Fig. 10). For

Fig. 7. Relationship between surface salinity, and N2O and CH4 during two field visits (April and May); N2O (A, B) and CH4 (C, D). (*) Indicates a significant relationship between variables.
58 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

Fig. 8. Relationship between ΔN2O vs. AOU and ΔN2O vs. NO−
3 during two field visits in April (A, B) and May (C, D). (*) Indicates a significant relationship between variables.

the Reloncaví areas previous studies indicated that a high load of seston mussels, as it is necessary to spend extra energy to eliminate these par-
(Mohr et al., 2017) and an increase in more corrosive waters may have ticles to their bodies (Salas-Yanquin et al., 2018). Therefore, under vol-
an impact on the suspension feeding processes and shell thickness in canic effects this finding may have significant implications for mussel

0.25 H = 8.23 0.12 H = 10.55 0.12 H = 6.96 16 H = 6.56

DF = 2 DF = 2 DF = 2 DF = 2
P = 0.016 P = 0.005 P = 0.031 15.5 P = 0.038
0.1 0.1
0.20 N total = 306
Dry shell weight (mg)

N total = 299 N total = 299 N total = 296

Total weight (mg)

Shell Length (mm)

15
0.08 0.08
Tissue (mg)

0.15 14.5
0.06 0.06 14
0.10 13.5
0.04 0.04
13
0.05
0.02 0.02
12.5
0 0 0 12
1 3 4 1 3 4 1 3 4 1 3 4

9 H = 7.08 0.105 H = 3.62 50 H = 23.35

DF = 2 DF = 2 DF = 2
8.5 P = 0.029 P = 0.164 48 P < 0.001
0.100
Shell Condition (%)

N total = 295 N total = 291 N total = 295

Shell thickness (mm)
Shell Height (mm)

46
8
0.095 44
7.5
0.090 42
7
40
0.085
6.5 38

6 0.080 36
1 3 4 1 3 4 1 3 4
Depth (meter)

Fig. 9. Median (±SE) in the morphometric measurements recorded in Mytilus chilensis seeds collected over three depths in a mussel farm located in the Reloncaví Fjord. Inset presents a
summary of the Kruskal-Wallis statistic (H) test, measuring the equality of medians of mussel characteristics over different depths. DF = degrees of freedom; N total is the overall number
of mussel seeds used in the test; Significant p values (b0.05) are showed in bold.
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 59

Sal O2
Low due to low salinity/low
alkalinity waters driven by
freshwater runoff

Optimum for mussel

growth and calcification

Low due to high pCO2

Low O2 waters by organic
matter remineralization

Fig. 10. Conceptual model of mussel calcification with an optimal refugee at 4 m depth in the Reloncaví Fjord.

farmers in this fjord environment, as the installation of mussels ropes in pattern of Mytilus chilensis beds in the Reloncaví Fjord. At this depth,
this layer. Supposedly present optimal conditions for mussel seed pro- of the optimal range for mussel growth and production in this estuarine
duction, could implement a management strategy to reduce the impacts environment was evidenced for a good correlation between variables.
of changes during different climatic scenarios, such as carbon chemistry For instance, the first PCA component explained 66% of the total vari-
in surface waters, both for ocean acidification processes and/or chang- ance, and showed a positive correlation with Temperature, Salinity, AT,
ing runoff conditions. Furthermore, this layer of aragonite-saturated ΩAr, N2O, NO3−, PO43−, pCO2, and Shell condition (Fig. 11). This area con-
waters could be an additional factor explaining the spatial distribution stitute one of the most important areas for larval mussel recruitment
(Molinet-Flores et al., 2015; Lara et al., 2016), and hosts important ben-
thic fisheries such as the king crab, gastropods, and sea urchins, all of
−2 −1 0 1 2
which are liable to impacts from decreasing pHT. Furthermore, reduc-
tion in ΩAr could be a significant challenge for other calcifying pelagic
0.4

Tissue
Total.weight
Shell.height
Shell.length
Dry.shell.weight and benthic organisms inhabiting similar fjord ecosystems in the South-
1.5

ern Patagonia, such as pelagic pteropods (Roberts et al., 2011), echino-

derms, and gastropods (Newcombe and Cárdenas, 2011).
Nitrous.oxide
1.0
0.2

Depth 4. Conclusion
0.5

Shell.thickness
Silicate
This study investigates the potential effect of a high magnitude vol-
Methane
PC2

0.0

0.0

canic eruption through the study of nutrients, greenhouse gases, and

Chl_a pCO2
Temperature
Salinity
Nitrate the carbonate system in the Reloncaví Fjord during autumn (April and
O2 Phosphate
Alcalinity
Aragonite May) and spring (September) 2015. Additionally, the impact of poten-
−0.5

tial changes was study in the carbonate system on the condition of mus-
sel shells in a nearby farming area. The outputs indicated a localized
−0.2

Shell.condition
−1.0

impact of the volcanic eruption on surface greenhouses gases mainly ni-

trous oxide, nutrients and short-term effects on the carbonate system.
pH
Despite our results indicate the presence of CaCO3 corrosive waters
−1.5

(ΩAr) in the Reloncaví Fjord, however no direct relation with the vol-
−0.4

cano eruption was found. Best conditions for mussel calcification were
recognized within a subsurface band, or refuge at 4 m depth, within
−0.4 −0.2 0.0 0.2 0.4 the estuarine environment, which appear to be resilient to catastrophic
PC1 events such as volcanic eruptions occurring in the Patagonian region.
These specific aspects can be integrated into adaptation strategies by
Fig. 11. Principal components analysis (PCA) of biological and physicochemical variables the mussel aquaculture industry to tackle ocean acidification and
from the Reloncaví fjord waters. changing runoff conditions.
60 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

Supplementary data to this article can be found online at https://doi. Filgueira, R., Grant, J., Strand, O., Asplin, L., Aure, J., 2010. A simulation model of carrying
capacity for mussel culture in a Norwegian fjord. Role of induced upwelling. Aquacul-
org/10.1016/j.scitotenv.2019.03.037. ture 308 (1–2), 20–27.
Flaathen, T.K., Gislason, S.R., 2007. The effect of volcanic eruptions on the chemistry of
surface waters: the 1991 and 2000 eruptions of Mt. Hekla, Iceland. J. Volcanol.
Acknowledgments Geotherm. Res. 164, 293–316.
Freing, A., Wallace, D.W.R., Bange, H.W., 2012. Global oceanic production of nitrous oxide.
This work was supported by the Millennium Nucleus “Center for the Philos. Trans. R. Soc. B Biol. Sci. 367, 1245–1255. https://doi.org/10.1098/
rstb.2011.0360.
Study of Multiple-drivers on Marine Socio-Ecological Systems (MUSELS)” Garreaud, R.D., 2009. The Andes climate and weather. Adv. Geosci. 7, 1–9.
funded by MINECON NC120086, and the Center for Climate and Resilience Gazeau, F., Parker, L.M., Comeau, S., Gattuso, J.P., O'Connor, W.A., Martin, S., Pörtner, H.O.,
Research Center (CR)2, CONICYT-Chile. Additional support from the Mil- Ross, P.M., 2013. Impacts of ocean acidification on marine shelled molluscs. Mar. Biol.
160, 2207–2245.
lennium Institute of Oceanography (IMO) funded by MINECON IC120019 González, H.E., Calderón, M.J., Castro, L., Clément, A., Cuevas, L.A., Daneri, G., Iriarte, J.L.,
is also acknowledged. The authors would like to thank to Pia Leon for lab Lizárraga, L., Martínez, R., Menschel, E., Silva, N., Carrasco, C., Valenzuela, C., Vargas,
processing, the Mussel Farming Company ORIZON for logistical support C.A., Molinet, C., 2010. Primary production and plankton dynamics in the Reloncaví
Fjord and the Interior Sea of Chiloé, Northern Patagonia, Chile. Mar. Ecol. Prog. Ser.
during our fieldwork, as well as the logistical support from the Techno- 402, 13–30. https://doi.org/10.3354/meps08360 ([RP4] [Sur Austral]).
logical Institute for the Mussel Farming Industry (INTEMIT) and the Fisher- Grasshoff, K., Ehrhardt, M., Kremling, K., 1983. Methods of Seawater Analysis. Verlag
ies Development Institute (IFOP). CAV was supported by the CONICYT/ Chemie, Weinheim/Deerfield Beach, Florida (ISBN 3–527-2599-8 (Weinheim)
0–89573-7 (Deerfield Beach), Second, Revised and Extended Edition.–With 108
FONDECYT/1170065 during the manuscript preparation. MAY was sup-
figs, 26 tab., 419 pp.).
ported by CONICYT/FONDAP/15130015 during the stage of the manu- Iriarte, J.L., González, H.E., Liu, K.K., Rivas, C., Valenzuela, C., 2007. Spatial and temporal
script writing. NAL also acknowledge support by PIA CONICYT variability of chlorophyll and primary productivity in surface waters of southern
ANILLOS ACT 172037 during the last stages of the manuscript. Chile (41.5–43 S). Estuar. Coast. Shelf Sci. 74 (3), 471–480.
Iriarte, J.L., González, H.E., Nahuelhual, L., 2010. Patagonian Fjord ecosystems in Southern
Chile as a highly vulnerable region: problems and needs. Ambio 39 (7), 463–466.
References https://doi.org/10.1007/s13280-010-0049-9.
Iriarte, J.L., León-Muñoz, J., Marcé, R., Clément, A., Lara, C., 2017. Influence of seasonal
Alarcón, E., Valdés, E., Torres, R., 2015. Saturación del carbonato de calcio en un area de freshwater streamflow regimes on phytoplankton blooms in a Patagonian fjord. N.
cultivo de mitílidos en el Seno de Reloncaví, Patagonia Norte, Chile. Lat. Am. Z. J. Mar. Freshw. Res. 51 (2), 304–315.
J. Aquat. Res. 43 (2), 227–281. Jaramillo, E., Melnick, D., Baez, J.C., Montecino, H., Lagos, N.A., Acuña, E., Manzano, M.,
Araya-Vergara, J., 2008. The submarine geomorphology of the Chilean Patagonian fjords and Camus, P.A., 2017. Calibrating coseismic coastal land-level changes during the 2014
piedmonts. In: Silva, N., Palma, S. (Eds.), Progress in the Oceanographic Knowledge of Iquique (Mw = 8.2) earthquake (northern Chile) with leveling, GPS and intertidal
Chilean Interior Waters, From Puerto Montt to Cape Horn. Comité Oceanográfico biota. PLoS ONE 12 (3), e0174348.
Nacional - Pontificia Universidad Católica de Valparaíso, Valparaíso, pp. 25–27. Jones, M.T., Gislason, S.R., 2008. Rapid releases of metal salts and nutrients following the
Balseiro, E., Souza, M.S., Serra Olabuenaga, I., Wolinski, Bastidas, L., Navarro, M., deposition of volcanic ash into aqueous environments. Geochim. Cosmochim. Acta
Laspoumaderes, C., Modenutti, B., 2014. Effect of the Puyehue–Cordon Caulle volcanic 72, 3661–3680.
complex eruption on crustacean zooplankton of Andean lakes. Ecol. Austral 24, Kroeker, K.J., Kordas, R.L., Crim, R.N., Singh, G.G., 2010. Meta-analysis revealsnegative yet
75–82. variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434.
Barria, A., Gebauer, P., Molinet, C., 2012. Spatial and temporal variability of mytilid larval Lagos, N.A., Benítez, S., Duarte, C., Lardies, M.A., Broitman, B.R., Tapia, C., Vargas, C.A., 2016.
supply in the Seno de Reloncaví, southern Chile. Rev. Biol. Mar. Oceanogr. 47, Effects of temperature and ocean acidification on shell characteristics of Argopecten
461–473. purpuratus: implications for scallop aquaculture in an upwelling-influenced area.
Beamud, G., Baffico, G., Pedrozo, F., Díaz, M., 2013. First record of the invasive algae Aquac. Environ. Interact. 8, 357–370.
Didymosphenia geminata in the Lake Nahuel Huapi: Argentina, Patagonia. Rev. Chil. Lara, C., Saldías, G.S., Tapia, F.J., Iriarte, J.L., Broitman, B.R., 2016. Interannual vriability
Hist. Nat. 86, 493–496. in temporal pattern of chlorophyll-a and their potential influence on the supply
Beutler, M., Wiltshire, K.H., Meyer, B., Moldaenke, C., Lüring, C., Meyerhöfer, M., Hansen, of mussel larvae to inner waters in northern Patagonia (41–44°S). J. Mar. Syst.
U.P., Dau, H., 2002. A fluorometric method for the differentiation of algal populations 155, 11–18.
in vivo and in situ. Photosynth. Res. 72 (1), 39–53. León-Muñoz, J., Marcé, R., Iriarte, J.L., 2013. Influence of hydrological regime of an Andean
Bia, G., Borgnino, L., Gaiero, D., García, M.G., 2015. Arsenic-bearing phases in South An- river on salinity, temperature and oxygen in a Patagonia fjord, Chile. N. Z. J. Mar.
dean volcanic ashes: implications for As mobility in aquatic environments. Chem. Freshw. Res. 47 (30), 515–528.
Geol. 393–394, 26–35. Letelier, J., Soto-Mardones, L., Salinas, S., Osuna, P., López, D., Sepúlveda, H.H., Pinilla, E.,
Borges, A.V., Abril, G., 2011. Carbon dioxide and methane dynamics in estuaries. In: Rodrigo, C., 2011. Variability of wind, waves and currents in the northern region of
Wolanski, E., McLusky, D.S. (Eds.), Biogeochemistry, Treatise on Estuarine and Coastal the Chilean Patagonian fjords. Rev. Biol. Mar. Oceanogr. 46, 363–377.
Science. vol. 5. Academic Press, Waltham, pp. 119–161. Mayr, C., Rebolledo, L., Schulte, K., Schuster, A., Zolitschka, B., Försterra, G., Häussermann,
Borges, A.V., Champenois, W., Gypens, N., Delille, B., Harlay, J., 2016. Massive marine V., 2014. Responses of nitrogen and carbon deposition rates in Comau Fjord (42 S,
methane emissions from near-shore shallow coastal areas. Sci. Rep. 6, 27908. southern Chile) to natural and anthropogenic impacts during the last century. Cont.
https://doi.org/10.1038/srep27908. Shelf Res. 78, 29–38. https://doi.org/10.1016/j.csr.2014.02.004.
Borie, G., Peirano, P., Zunino, H., Aguilera, M., 2002. N-pool in volcanic ash-derived soils in Millero, F.J., 2010. Carbonate constants for estuarine waters. Mar. Fresh Water Res. 61,
Chile and its changes in deforested sites. Soil Biol. Biochem. 34, 1201–1206. 139–142. https://doi.org/10.1071/MF09254.
Byrne, M., 2011. Impact of ocean warming and ocean acidification on marine invertebrate Mohr, C.H., Korup, O., Ulloa, H., Iroumé, A., 2017. Pyroclastic eruption boosts organic car-
life history stages: vulnerabilities and potential for persistence in a changing ocean. bon fluxes into Patagonian fjords. Glob. Biogeochem. Cycles 31, 1626–1638.
Oceanogr. Mar. Biol. Annu. Rev. 1–42. Molinet-Flores, C.M., Díaz-Gomez, C., Arriagada-Muñoz, L., Cares-Pérez, S., Arribas, Marín,
Castillo, M., Pizarro, O., 2009. Some aspects of the physical oceanography off central Chile. Astorga-Opazo, M., Niklitschek-Huaquin, E., 2015. Spatial distribution pattern of
Exposición. Workshop Gordon and Betty Moore Foundation, Concepción, Chile. Mytilus chilensis beds in the Reloncaví fjord: hypothesis on associated processes.
Castillo, M.I., Pizarro, O., Cifuentes, U., Ramirez, N., Djurfeldt, L., 2012. Subtidal dynamics in Rev. Chil. Hist. Nat. 88, 1–12. https://doi.org/10.1186/S40693-015-0041-7.
a deep fjord of southern Chile. Cont. Shelf Res. 49, 73–89. Munro, B.Z., 2005. Statistical Methods for Health Care Research. 5th edn. Lippincott Wil-
Castillo, M.I., Cifuentes, U., Pizarro, O., Djurfeldt, L., Caceres, M., 2016. Seasonal hydrogra- liams & Wilkins, Philadelphia.
phy and surface outflow in a fjord with a deep sill: the Reloncaví fjord, Chile. Ocean Nevison, C., Butler, J.H., Elkins, J.W., 2003. Global distribution of N2O and the ΔN2O-AOU
Sci. 12 (2), 533. yield in the subsurface ocean. Glob. Biogeochem. Cycles 17 (4).
Chierici, M., Fransson, A., 2009. Calcium carbonate saturation in the surface water of the Newcombe, E.M., Cárdenas, C.A., 2011. Rocky reef benthic assemblages in the Magellan
Arctic Ocean: undersaturation in freshwater influenced shelves. Biogeosciences 6, Strait and the South Shetland Islands (Antarctica). Rev. Biol. Mar. Oceanogr. 46 (2),
2421–2431. 177–188.
Guide to best practices for ocean CO2 measurement. In: Dickson, A.G., Sabine, C.L., Osores, S.J.A., Lagos, N.A., Martin, V.S., Manriquez, P.H., Vargas, C.A., Torres, R., Navarro, J.,
Christian, J.R. (Eds.), Sidney, British Columbia, North Pacific Marine Science Organiza- Poupin, M.J., Saldías, G.S., Lardies, M.A., 2017. Plasticity and inter-population variabil-
tion (191 pp., PICES Special Publication 3). http://hdl.handle.net/11329/249. ity in physiological and life-history traits of the mussel Mytilus chilensis: a reciprocal
DOE, 1994. Handbook of methods for the analysis of the various parameters of the carbon transplant experiment. J. Exp. Mar. Biol. Ecol. 490, 1–12.
dioxide system in seawater; version 2. In: Dickson, A.G., Goyet, C. (Eds.), ORNL/ Parsons, T.R., Maita, Y., Lalli, C.M., 1984. A Manual of Chemical and Biological Methods for
CDIAC-74. Seawater Analysis. Pergamon Press, Oxford (173 pp.).
Farías, L., Florez-Leiva, L., Besoain, V., Sarthou, G., Fernández, C., 2015. Dissolved green- Pierrot, D., Lewis, E., Wallace, D.W.R., 2006. MS Excel Program Developed for CO2 System
house gases (nitrous oxide and methane) associated with the naturally iron- Calculations, ORNL/CDIAC-105, Carbon Diox- ide Inf. Anal. Cent., Oak Ridge Natl. Lab.,
fertilized Kerguelen region (KEOPS 2 cruise) in the Southern Ocean. Biogeosciences U.S. Dep. of Energy, Oak Ridge, Tenn.
12 (6), 1925–1940. Ríos, V., Ocampo, N., Astorga, M.S., 2018. Composición química proximal y morfométría
Farías, L., Sanzana, K., Sanhueza-Guevara, S., Yevenes, M., 2017. Dissolved methane distri- de cholga (Aulacomya ater, Molina, 1782) y chorito (Mytilus chilensis, Hupé, 1854)
bution in the Reloncaví Fjord and adjacent marine system during austral winter comercializados en la Región de Magallanes. Anales Instituto Patagonia (Chile) 46
(41°–43° S). Estuar. Coasts https://doi.org/10.1007/s12237-017-0241-2 (April, 1–15). (1), 49–58.
 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61 61

Roberts, D., Howard, W., Moy, A., Roberts, J., Trull, T., Bray, S., Hopcroft, R., 2011. Interan- soil distribution and weathering. Earth Surf Process. Landf. 41, 499–512. https://doi.
nual pteropod variability in sediment traps deployed above and below the aragonite org/10.1002/esp.3840.
saturation horizon in the Sub-Antarctic Southern Ocean. Polar Biol. 34 (11), Vargas, C.A., Contreras, P., Pérez, C.A., Sobarzo, M., Saldías, G.S., Salisbury, J., 2016. Influ-
1739–1750. ences of riverine and upwelling waters on the coastal carbonate system off Central
Romero, J., Morgavi, D., Arzilli, A., Perugini, D., 2016. Eruption dynamics of the 22–23 April Chile and their ocean acidification implications. JGR Biogeosci. https://doi.org/
2015 Calbuco Volcano (Southern Chile): analyses of tephra fall deposits. J. Volcanol. 10.1002/2015JG003213.
Geotherm. Res. 317, 15–19. Vargas, C.A., Lagos, N.A., Lardies, M.A., Duarte, C., Manríguez, P.H., Aguilera, C., Broitman,
Saavedra, N., Müller, E., Fopiano, A., 2010. On the climatology of surface wind direction B., Widdicombe, S., Dupont, S., 2017a. Species-specific responses to ocean acidifica-
frequencies for the central Chilean coast. Aust. Meterol. Oceanogr. J. 60, 103–112. tion should account for local adaptation and adaptive plasticity. Nat. Ecol. Evol. 1,
Salas-Yanquin, L.P., Navarro, J.M., Pechenik, J.A., Montory, J.A., Chaparro, O.R., 2018. Volca- 0084. https://doi.org/10.1038/s41559-017-0084.
nic ash in the water column: physiological impact on the suspension- feeding bivalve Vargas, C.A., Cuevas, L.A., Silva, N., González, H.E., De Pol-Holz, R., Narváez, D.A., 2017b. In-
Mytilus chilensis. Original Research Article, pp. 342–351. fluence of glacier melting and river discharges on the nutrient distribution and DIC
Santana-Casiano, J.M., González-Dávila, M., Fraile-Nuez, E., de Armas, D., González, A.G., recycling in the Southern Chilean Patagonia. J. Biogeochem. Res. Biogeosci. https://
Domínguez-Yanes, J.F., Escánez, J., 2013. The natural ocean acidification and fertiliza- doi.org/10.1002/2017JG003907.
tion event caused by the submarine eruption of El Hierro. Sci. Rep. 3, 1140. https:// Vergara, M.J., Torres, R., Alarcon, E., Beatty, C., DeGrandpre, M., Cuevas, L.A., Iriarte, J.L.,
doi.org/10.1038/srep01140. 2016. Strong-short-term effects of a volcanic eruption on the carbonate system of a
Sauer, S., Hong, W.L.W.L., Knies, J., Lepland, A., Forwick, M., Klug, M., Eichinger, F., highly stratified fjord in the Northern Chilean Patagonia. 4th International Sympo-
Baranwal, S., Crémière, A., Chand, S., 2016. Sources and turnover of organic carbon sium on the Ocean in a High-CO2 World. Theme C: Changing Carbonate Chemistry
and methane in fjord and shelf sediments off northern Norway. Geochem. Geophys. of the Ocean. Tasmania, Australia.
Geosyst. 17 (10), 4011–4031. Waldbusser, G.G., Salisbury, J.E., 2014. Ocean acidification in the coastal zone from an
Sievers, H.A., Silva, N., 2006. Masas de agua y circulación en los canales y fiordos australes. organism's perspective: multiple system parameters, frequency domains, and habi-
In: Silva, N., Palma, S. (Eds.), Avances en el conocimiento oceanográfico de las aguas tats. Annu. Rev. Mar. Sci. 6 (1), 221–247. https://doi.org/10.1146/annurev-marine-
interiores chilenas, Puerto Montt a cabo de Hornos. Comité Oceanográfico Nacional— 121211-172238.
Pontificia Universidad Católica de Valparaíso, Valparaíso, pp. 53–58. Wang, L.N., Shao, G.X., Chen, X.H., Li, Y., Wang, D.G., 2012. Flood changes during the past
Silva, N., Vargas, C.A., 2014. Hypoxia in Chilean Patagonian Fjords. Prog. Oceanogr. 29, 50 years in Wujiang River, South China. Hydrol. Processes 26, 3561–3569. https://doi.
62–74. org/10.1002/hyp.8451.
Silva, N., Vargas, C.A., Prego, R., 2011. Land-ocean distribution of allochthonous organic Wilson, S.T., Bange, H.W., Arévalo-Martínez, D.L., Barnes, J., Borges, A.V., Brown, I.,
matter in surface sediments of the Chiloé and Aysén interior seas (Chilean Northern Bullister, J.L., Burgos, M., Capelle, D.W., Casso, M., de la Paz, M., Farías, L., Fenwick,
Patagonia). Cont. Shelf Res. 31, 330–339. L., Ferrón, S., Garcia, G., Glockzin, M., Karl, D.M., Kock, A., Laperriere, S., Law, C.S.,
Smith, R.W., Bianchi, T.S., Allison, M., Savage, C., Galy, V., 2015. High rates of organic car- Manning, C.C., Marriner, A., Myllykangas, J.P., Pohlman, J.P., Rees, A.P., Santoro, A.E.,
bon burial in fjord sediments globally. Nat. Geosci. 8 (6), 450–453. https://doi.org/ Tortell, P.D., Upstill-Goddard, R.C., Wisegarver, D.P., Zhang, G.L., Rehder, G., 2018.
10.1038/ngeo2421. An intercomparison of oceanic methane and nitrous oxide measurements. Biogeosci-
Torres, R., Pantoja, S., Harada, N., González, H.E., Daneri, G., Frangopulos, M., Rutllant, J.A., ences 15, 5891–5907.
Duarte, C.M., Rúiz-Halpern, S., Mayol, E., Fukasawa, M., 2011. Air-sea CO2 fluxes along Yevenes, M.A., Bello, E., Sanhueza-Guevara, S., Farías, L., 2017. Spatial distribution of ni-
the coast of Chile: from CO2 outgassing in central northern upwelling waters to CO2 trous oxide (N2O) in the Reloncaví estuary–sound and adjacent sea (41°–43° S),
uptake in southern Patagonian fjords. J. Geophys. Res. Oceans 116 (C9). Chilean Patagonia. Estuar. Coasts 40 (3), 807–821.
Valle-Levinson, A., Sarkar, N., Sanay, R., Soto, D., León, J., 2007. Spatial structure of hydrog- Yoshinari, T., 1976. Nitrous oxide in the sea. Mar. Chem. 4 (2), 189–202.
raphy and flow in a Chilean Fjord, Estuario Reloncaví. Estuar. Coasts 30 (1), 113–126. Zhai, W.D., Zang, K.P., Huo, C., Zheng, N., Xu, X.M., 2015. Occurrence of aragonite corrosive
Van Eaton, A., Amigo, A., Bertin, D., Mastin, L., Giacosa, R.E., Gonzalez, J., Valderrama, water in the North Yellow Sea, near the Yalu River estuary, during a summer flood.
Fontijn, K., Behnke, S., 2016. Volcanic lightning and plume behavior reveal evolving Estuar. Coast. Shelf Sci. 166-B, 199–208. https://doi.org/10.1016/J.ECSS.2015.02.010.
hazards during the April 2015 eruption of Calbuco volcano, Chile. Geophys. Res.
Lett. 43 (7), 3563–3571.
Vandekerkhove, E., Bertrand, S., Reid, B., Bartels, A., Charlie, B., 2016. Sources of dissolved
silica to the fjords of northern Patagonia (44–48°S): the importance of volcanic ash