science of the total environment - eula€¦ · received in revised form 1 march 2019 accepted 3...

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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 Oceanográcas, 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 HIGHLIGHTS A large bloom of phytoplankton was de- tected in the surface waters of the Reloncaví fjord following the Calbuco volcano eruption. Subsequent to the eruption, higher N 2 O, CH 4 and SO 4 2concentrations were ob- served in Fjord surface waters. Optimal juvenile mussel growth was observed in refugee subsurface depths coinciding with increased aragonite sat- uration. The observed trends may be valuable for developing effective management strat- egies for mussel aquaculture in the Fjord. GRAPHICAL ABSTRACT O 2 Sal Low due to high pCO 2 Low O 2 waters by organic matter remineralization Low due to low salinity/low alkalinity waters driven by freshwater runoff Optimum for mussel growth and calcification abstract article info Article history: Received 19 November 2018 Received in revised form 1 March 2019 Accepted 3 March 2019 Available online 07 March 2019 Editor: Daniel Wunderlin This study investigates the immediate and mid-term effects of the biogeochemical variables input into the Reloncaví fjord (41°40S; 72°23O) as a result of the eruption of Calbuco volcano. Reloncaví is an estuarine system supporting one of the largest mussels farming production within Northern Chilean-Patagonia. Field-surveys were conducted immediately after the volcanic eruption (2330 April 2015), one month (May 2015), and ve months posterior to the event (September 2015). Water samples were collected from three stations along the fjord to de- termine greenhouse gases [GHG: methane (CH 4 ), nitrous oxide (N 2 O)], nutrients [NO 3 , NO 2 , PO 4 3, Si(OH) 4 , sul- phate (SO 4 2)], and carbonate systems parameters [total pH (pHT), temperature, salinity, dissolved oxygen (O 2 ), and total alkalinity (AT)]. Additionally, the impact of physicochemical changes in the water column on juveniles of the produced Chilean blue mussel, Mytilus chilensis, was also studied. Following the eruption, a large phyto- plankton bloom led to an increase in pH T , due to the uptake of dissolved-inorganic carbon in photic waters, po- tentially associated with the runoff of continental soil covered in volcanic ash. Indeed, high surface SO 4 2and GHG were observed to be associated with river discharges. No direct evidence of the eruption was observed within the Keywords: Chilean Patagonian Fjord Carbonates system Nutrients Science of the Total Environment 669 (2019) 4961 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. Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv

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Page 1: Science of the Total Environment - EULA€¦ · Received in revised form 1 March 2019 Accepted 3 March 2019 Available online 07 March 2019 ... 50 M.A. Yevenes et al. / Science of

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

Contents lists available at ScienceDirect

Science of the Total Environment

j ourna l homepage: www.e lsev ie r .com/ locate /sc i totenv

Greenhouse gases, nutrients and the carbonate system in the ReloncavíFjord (Northern Chilean Patagonia): Implications on aquaculture of themussel, 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, Chileb Centro de Recursos Hídricos para la Agricultura y la Minería (CRHIAM), Chilec Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Facultad de Ciencias, Universidad Santo Tomas, Santiago, Chiled Center for the Study of Multiple-Drivers on Marine Socio-Ecological Systems (MUSELS), Universidad de Concepción, Concepción, Chilee Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Chilef Centro de Ciencia del Clima y la Resiliencia (CR)2, Chileg Millennium Institute of Oceanography (IMO), Universidad de Concepción, Concepción, Chileh 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 phytoplanktonwas de-tected in the surface waters of theReloncaví fjord following the Calbucovolcano eruption.

• Subsequent to the eruption, higher N2O,CH4 and SO4

2− concentrations were ob-served in Fjord surface waters.

• Optimal juvenile mussel growth wasobserved in refugee subsurface depthscoinciding with increased aragonite sat-uration.

• The observed trendsmay be valuable fordeveloping effective management strat-egies for mussel aquaculture in theFjord.

⁎ Corresponding author at: Aquatic Ecosystem FunctionUniversidad de Concepción, P.O. Box 160-C, Concepción, C

E-mail address: [email protected] (C.A. Vargas).

https://doi.org/10.1016/j.scitotenv.2019.03.0370048-9697/© 2019 Elsevier B.V. All rights reserved.

O2 Sal

Low due to high pCO2 Low O2 waters by organic matter remineralization

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

Optimum for mussel growth and calcification

a b s t r a c t

a r t i c l e i n f o

Article history:Received 19 November 2018Received in revised form 1 March 2019Accepted 3 March 2019Available online 07 March 2019

Editor: Daniel Wunderlin

This study investigates the immediate and mid-term effects of the biogeochemical variables input into theReloncaví fjord (41°40′S; 72°23′O) as a result of the eruption of Calbuco volcano. Reloncaví is an estuarine systemsupporting one of the largestmussels farming productionwithinNorthernChilean-Patagonia. Field-surveyswereconducted immediately after the volcanic eruption (23–30 April 2015), onemonth (May 2015), and fivemonthsposterior to the event (September 2015).Water sampleswere collected from three stations along the fjord to de-termine greenhouse gases [GHG:methane (CH4), nitrous oxide (N2O)], nutrients [NO3

−, NO2−, PO4

3−, Si(OH)4, sul-phate (SO4

2−)], and carbonate systems parameters [total pH (pHT), temperature, salinity, dissolved oxygen (O2),and total alkalinity (AT)]. Additionally, the impact of physicochemical changes in the water column on juvenilesof the produced Chilean blue mussel, Mytilus chilensis, was also studied. Following the eruption, a large phyto-plankton bloom led to an increase in pHT, due to the uptake of dissolved-inorganic carbon in photic waters, po-tentially associatedwith the runoff of continental soil covered in volcanic ash. Indeed, high surface SO4

2− andGHGwere observed to be associatedwith river discharges. No direct evidence of the eruptionwas observedwithin the

Keywords:Chilean Patagonian FjordCarbonates systemNutrients

ing Lab (LAFE), Department of Aquatic Systems, Faculty of Environmental Sciences & Environmental Sciences Center EULA Chile,hile.

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50 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

carbonate system. Notwithstanding, a vertical pattern was observed, with an undersaturation of aragonite (ΩAr

b 1) both in brackish surface (b3 m) and deep waters (N10 m), and saturated values in subsurface waters (3 to7m). Simultaneously, juvenilemussel shells showedmaximized length andweight at 4m depth. Results suggesta 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. Thesespecific attributes can be integrated into adaptation strategies by the mussel aquaculture industry to confrontocean acidification and changing runoff conditions.

© 2019 Elsevier B.V. All rights reserved.

Mussel farmingVolcanic event

1. Introduction

Natural disasters such as earthquakes and volcanic eruptions pro-vide excellent opportunities to evaluate effects of mesoscale and largedisturbances on ecosystems (Wang et al., 2012). These disturbancescan leave ephemeral or long lasting ecological effects on spatial andtemporal patterns of marine communities (e.g. Jaramillo et al., 2017).Thus, disasters within ecosystem have a fundamental effect on materialflux (minerals) across the land-ocean interface. Fjords are good exam-ples of these events; they cover approximately 7 to 10% of the globalocean (Sauer et al., 2016) and represent an important interface and reg-ulating area between freshwater systems (i.e., lakes and rivers), glaci-ated terrain, and the coastal ocean. Moreover, fjord ecosystems arehighly valuable in terms of different ecosystems services, such as nutri-ent availability, carbon cycling, water quality for aquaculture produc-tion, and pollution control (Iriarte et al., 2010). In consequence, manystudies highlight the threat of global changes on estuarine and fjordcoastal systems (Iriarte et al., 2010; Letelier et al., 2011; Silva andVargas, 2014; Vargas et al., 2017a).

The impacts of anthropogenic activities (such as land use changes,nutrient loading, river damming, fishing, mussel farming) on biogeo-chemical cycles have been well documented for fjord environments,for example research by Filgueira et al. (2010) in Sweden and Norway.Recently, similar impacts have also been documented in fjord ecosys-tems of Chilean Patagonia (Silva and Vargas, 2014; Mayr et al., 2014;Iriarte et al., 2017; Farías et al., 2017; Vargas et al., 2017b; Yeveneset al., 2017). Aquaculture production in fjord ecosystems largely de-pends on the integrity of different ecological, biophysical, and biogeo-chemical processes, which are subjected to multiple sources ofvariability (Barria et al., 2012; Lara et al., 2016). Fjords are sensitive tolocal acidification processes, mostly due to the influence of riverine wa-terswith a low total alkalinity (AT), which in turns reduces the bufferingcapacity of receiving waters (Chierici and Fransson, 2009). Thus, an in-crease in freshwater fluxes into fjord ecosystems has the potential notonly to decrease seawater pH and reduce the saturation state of calciumcarbonate (Ω), but also induce a shift in the NH3–NH4

+ equilibrium to-wards NH4

+ (Freing et al., 2012), affecting nitrification and associatedN2O generation. Moreover, fjords store large amounts of organic carbon,with burial rates exceeding double the average rates in global oceans(Smith et al., 2015; Mohr et al., 2017). However, the influence of epi-sodic disturbances, such as volcanic eruptions, in mobilizing nitrogen,carbon and greenhouse gases in fjord environments remains poorlystudied (Mohr et al., 2017).

The Reloncaví Fjord area has been affected numerous times by theeruption of the Calbuco Volcano (41°20′S, southern Chile), with erup-tions registered in 1961, 1972, and more recently during April 22th2015. During the last eruption, Calbuco Volcano ejected a significantash plume that required the evacuation of nearby areas, disrupted aerialtraffic, and damaged buildings in Chile (Van Eaton et al., 2016). The vol-canic eruption produced a stratospheric column (N15 km height;0,27 km3) of porphyritic basaltic andesite (SiO2). The tephra fall oc-curred over the northeast area of the volcano, while the finest ash wastransported and deposited over northern Patagonia in Chile andArgentina (Romero et al., 2016). It is widely acknowledged that an

increase in volcanic ash covering soils may result in high levels of dis-solved silica in rivers, thus increasing the flux into fjord environments.As a result, phytoplankton productivity and community structure maybe affected (Balseiro et al., 2014; Vandekerkhove et al., 2016). More-over, ash fallout can also induce acidification of soils (Borie et al.,2002), thus leading to low pH events in adjacent fjord areas (Santana-Casiano et al., 2013). It is well known that low pH/high pCO2 conditionscan have a negative impact on marine calcifiers, such as corals, sea ur-chins, gastropods, and mussels (Kroeker et al., 2010). Specifically, theendemic Chilean mussel, Mytilus chilensis, is present in the intertidalzone down to 25 m depth throughout the Chilean coastline. This speciecan withstand high salinity and brackish water, for example in rivermouths or close to glaciers, subsisting through the filtration ofmicroalgae (Molinet-Flores et al., 2015; Ríos et al., 2018). Mytiluschilensis is themain farmed shellfish, and represents a considerable frac-tion of aquaculture production in Chile of up to approximately 238,088tons annually, representing the 96,6% shellfish production (Sauer et al.,2016; Molinet-Flores et al., 2015; Castillo et al., 2016). Relative to this,the Reloncaví Fjord is one of the most important areas for mussel seedproduction (with 99% of production concentrated within thesewaters),predominantly made up by the Chilean mussel specie,Mytilus chilensis.

Therefore, the treat of volcanic eruptions also hasmajor implicationson the socio-ecological systems of mussel farming in the region. Re-cently, Salas-Yanquin et al. (2018) identified the physiological impactof the presence of volcanic ash from Calbuco Volcano on the diet ofMytilus chilensis and their ability to select particles during feeding.This study aims to investigate the posteriori potential effect of a highmagnitude volcanic eruption through the study of greenhouse gases(such as CH4 and N2O), nutrients, and the carbonate system in theReloncaví Fjord during autumn (April), winter (May) and spring (Sep-tember) 2015. Furthermore, this study aims to determine the impactof potential changes in the carbonate system on the condition of musselshells in a nearby farming area.

2. Materials and methods

2.1. Study area

This studywas carried out in the Reloncaví Fjord (41° 40′S–72° 32′W′) located in northern Chilean Patagonia (Fig. 1). From the head to themouth, the fjord has a total length of 55 km and a width of almost3 km in its widest section, and is characterized to have a glacial origin(Valle-Levinson et al., 2007; Araya-Vergara, 2008). The main source offreshwater comes from the Puelo River, with an annual average of650 m3 s−1 (León-Muñoz et al., 2013). Winds have a marked seasonalvariability, during winter predominant winds are from the northwhile during summer winds from the south and southeast are preva-lent, with magnitudes that are generally between 9 m s−1 to 15 m s−1

(Saavedra et al., 2010; Castillo et al., 2012). The fjord area presents amarked hydrographical variability, related to regimes of high rainfalland ice melt (Castillo and Pizarro, 2009). High levels of freshwaterinput from tributary rivers generate considerable salinity variationsthat characterize the distinct water masses present in this region,made up of channels and fjords (León-Muñoz et al., 2013). As a result

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

51M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

a strong spatial salinity gradient exists in the surface fraction (Gonzálezet al., 2010), with a stratified water column characterized by a markedpycnocline between theupper layer (0 to 5mdepth) and the subsurfacelayer below 5 m depth (Valle-Levinson et al., 2007). Below this narrowlayer, there is a relatively homogenous layer of marine water predomi-nantly from sub-Antarctic origin, described as modified sub-Antarcticwater or MSAAW (Sievers and Silva, 2006).

2.2. Water sampling

Seasonal water sampling was made during autumn (30th April),winter (29th May 2015) and spring (25th September 2015). Watersamples from three stations (st.1: −41° 43′ 57′ S–72° 32′ 50.8″W′;st.2: −41° 41′ 40.4′ S–72° 26′ 24.6″W′; st.3: −41° 37′ 50.3′ S–72° 20′55.6″W′) were collected along the Reloncaví estuary over five depths(1, 5, 10, 25, 50 m depth) (Fig. 1). Our study was focused on theshort-term response during autumn, winter and the long-term con-sequences on early spring conditions. The longitudinal distributionof sampling stations was based on the location of one of the largestmussel-farming sites near the fjord mouth (ORIZON Company nearChaparano Bay, Stn. 1), and the location of one of the main river dis-charges in the area (Puelo River in themid- portion of the fjord at Stn3). Discrete water samples were collected in triplicate using Niskinbottles (General Oceanic®, GO-FLO Niskin bottles sampling), forSO4

2−, Chlorophyll a (Chl-a), Total pH (pHT), Total Alkalinity (AT),N2O, CH4 and nutrients (i.e., NO3

−, NO2−, PO4

3−, Si(OH)4). Continuousprofiles of temperature, salinity, and dissolved oxygen were ob-tained using a Conductivity-Temperature-Dissolved Oxygen Sonde

(CTDO) (SeaBird 25) to 50 m depth. Chlorophyll measurements(Chl-a) were conducted with a Fluoroprobe sensor (bbe-Moldaenke,Kiel, Germany) (Beutler et al., 2002); a highly sensitive measuringinstrument for the analysis of chlorophyll, including the determina-tion of algal class. Chlorophyll measurements were calibrated bycontrasting with fluorometry analysis (Turner Design TD-700),using acetone (90% v/v) for the pigment extraction of discrete sam-ples according to standard procedures (Parsons et al., 1984). Sub-samples for pH measurements were stored in borosilicate BODbottles with ground-glass stoppers without air bubbles andtransported to the field lab where pH was measured within 2 h ofcollection. Water samples for AT were poisoned with 50 μL of satu-rated HgCl2 solution and stored in 500 mL borosilicate BOD bottleswith ground-glass stoppers, lightly coated with Apiezon L® grease,and kept in darkness at room temperature (Dickson et al., 2007).For logistic support, samples for N2O and CH4 analysis were only col-lected in April and May, in 20 mL glass vials (by triplicate), treatedwith 50 μL of saturated HgCl2 solution (6 g L−1) and sealed with her-metic stoppers and aluminium caps (Wilson et al., 2018). These sam-ples were stored at ambient temperature for posterior analysis in thelaboratory. Additionally, water samples for nutrient analysis werefiltered through a 0.45 μm Cellulose acetate (CA) membrane and col-lected in 15 mL falcon tubes, and then frozen for later analysis in thelaboratory. Samples for SO4

2− concentrations were collected in falconconical tubes of 50 mL and analysed with ion chromatographicmethod with chemistry suppression, based on standard methods4110 B, using Dionex ICS2100 equipment, through an anionic AS11High Capacity, with concentrations above 0.1 mg L−1.

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52 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

2.3. Carbonate system parameters

Samples for pH measurement were collected and directlytransported inland so that pH was measured within a 2 h timeframeafter collection (Vargas et al., 2016). pH samples were collected in50 mL syringes and immediately transferred to a 25 mL thermo statedcell at 25.0 ± 0.1 °C for standardization, with a pH meter Metrohm®using a glass combined double junction Ag/AgCl electrode (Metrohmmodel 6.0258.600) calibrated with 8.089 Tris buffer at 25.0 °C (DOE,1994), and therefore registered on the total hydrogen ion scale (pHT).AT was determined using the open cell titration method (Dicksonet al., 2007), using an automatic Alkalinity Tritrator Model AS-ALK2Apollo SciTech. The AS-ALK2 system is equipped with a combinationpH electrode (8102BNUWP, Thermo Scientific, USA) and temperatureprobe for temperature control (Star ATC probe, Thermo Scientific,USA) connected to a pH meter (Orion Star A211 pHmeter, Thermo Sci-entific, USA). All sampleswere analysed at 25 °C (±0.1 °C)with temper-ature regulation using a water bath (Lab Companion CW-05G). Theaccuracy was controlled against a certified reference material (CRM,supplied by Andrew Dickson, Scripps Institution of Oceanography, SanDiego, USA) and the AT repeatability averaged 2–3 μM kg−1.

pHT and AT data were applied to the program CO2SYS (Pierrot et al.,2006) to calculate aragonite saturation state (ΩAr), and other carbonateparameters (e.g. pCO2). The dissociation constants for carbonic acid (K1and K2) were used by Dickson et al. (2007) for salinities between N30PSU, Millero (2010) for estuarine waters between 1 and 30 PSU, andfor freshwater samples in the mid- and upper river sampling stations.KHSO4 was determined for both freshwater and seawater samples(Dickson et al., 2007).

2.4. Determination of nutrients, nitrous oxide and methane

N2O and CH4 detection wasmade via the generation of a 5 mL ultra-pure helium headspace into the vial, by a gas-tight syringe, and main-taining the gas and liquid phases in equilibrium at 40 °C within thevial, allowing for the equilibrium of the headspace in the vial (Faríaset al., 2015). N2O dissolved in the seawater was measured throughgas–liquid equilibration in the vial at 40 °C for 15 min under agitation,using a headspace autosampler device (HP Agilent) followed by quanti-fication via gas chromatography (GC). N2O was analysed in aSHIMADZU-17A gas chromatograph equipped at 350 °C, using a capil-lary column and injector operated at 60 °C and 300 °C, respectively,and connected to the autosampler (Farías et al., 2015). Ar/CH4 gas mixwas used as a carrier gas with a flux of 6.5 mL min−1.

CH4 was analysed in a Shimadzu 17A gas chromatograph equippedby a flame ionization detector (FID) at 250 °C, through and injectorand a capillary columnGS-Q at operated to 180° and 30 °C, respectively,using N2 as carrier gas with a flux of 3 mL min−1, and GC connected tothe mentioned autosampler (Farías et al., 2015).

A calibration curve was made using several concentrations for N2O(0.10 air, 0.5 and 1 ppmv) and CH4 (1, air, 5 and 10 ppmv) usingMatheson gas standards whose nominal concentrations were checkedusing set of high-pressure primary gas standards, prepared for theSCOR Working Group by John Bullister and David Wisegarver at NOAAPacific Marine and Environmental Laboratory (PMEL). One batch, re-ferred to as the air ratio standard (ARS), hadN2O and CH4mole fractionssimilar to modern air, and the other batch, referred to as thewater ratiostandard (WRS), had higher had N2O and CH4mole fractions for the cal-ibration of high-concentration water samples (Wilson et al., 2018).Both, the ECD and FID detectors responded linearly to these concentra-tion ranges. The analytical error of the N2O and CH4 analyses was b3%and 5%, respectively. The uncertainty of the measurements was calcu-lated from the standard deviation of the triplicate measurements bydepth. Measurements with a variation coefficient N10% were not in-volved in the gas record (Farías et al., 2015).

The nutrient analyses (NO3−, PO4

3− and Si(OH)4) were carried outusing colorimetric techniques (Grasshoff et al., 1983), with anautoanalyzer SEAL analytical (AA3). Calibration curves were performedprevious to each set of measurements, using primary standard. The pre-cision and detection limit of the method was, ±50 nM and 20 nM forNO3

−, ±30 nM and 110 nM for PO4−3− and ±70 nM and 0.030 μM for

Si(OH)4, respectively.

2.5. Biological sampling

During May 2015, juvenile individuals of M. chilensis (b2 cms, mus-sels' seeds) from the same cohortwere randomly collected frompeggedropes (6 m in length) at three different depths (1, 3 and 4 m). At eachdepth, all mussels that were attached along ca. 10 cm length of the set-tlement ropes were collected. Among 90–105 mussel seeds were col-lected from each depth level, transported (ca. 4 °C using ice-packlasting for ca. 6 h), to the laboratory under chilled conditions, andthen frozen (−20 °C) for posterior processing in the laboratory, whichwas performed during Sept. 2015. Taxonomic identification based onshell shape and lack of external ribs was used to minimize potentialbias in including other species mussels in the processing. Several mor-phometric variables were recorded for each mussel, including totalwet weight, dry shell weight, and soft tissue weight (after 6 h at 60 °C,Memmert®) using an analytical balance (Metler Toledo); maximumshell length, shell height, and shell thickness (measured using a digitalcaliper,Mitutoyo®). Shell thickness corresponds to the average of 4 sep-arate measurements taken from newly forming shell growth along theedge of the mussel valves (e.g., Lagos et al., 2016). Finally, the relativeshell condition index is estimated through calculating the total dryshell weight as a percentage of the total weight (i.e., [Dry shell weight/ Total weight] × 100).

2.6. Statistical analysis

The Pearson correlation coefficient and lineal regression were usedto define relationships among variables, including GHG, nutrient con-centrations and the carbonate system as parameters (Munro, 2005).Mussel measurements were subjected to descriptive statistical analysisto define trends in the frequency distribution of variables over depth.The Kolmogorov-Smirnov test for normality was applied, and severaldistribution moments were also calculated (e.g., mean, standard devia-tion, median and its 95% confidence interval), due to the fact distribu-tions presented significant deviations from the normality (seeSupplementary material S1). The Kruskal-Wallis test was applied tocompare the medians of each variable between mussels collected overdifferent depths, and results were described using median (±IQR,Inter Quartile Range). A Principal Component Analysis was also esti-mated to describe the variation in the set of physical-chemical and bio-logical variables.

3. Results and discussion

The eruption of Calbuco volcano released high levels of particles andgases throughout its area of influence, including the estuarine waters ofReloncaví fjord. Throughout the three periods of field sampling, thefjord presented a vertical salinity distribution that clearly divided thewater column into two layers, separated by a marked halocline. In theupper 5 m of the surface water salinity was approximately 8.84 to15.2, and in the subsurface layer below the 5 m from 28.2 to 32.87(Fig. 2a–i). Several studies have identified that the water in theReloncaví fjord are seasonally dominated by estuarine waters (EW) inthe upper layer to 5 m depth, and in the deeper layer there is morecold and dense modified subantarctic water (MSAAW) (Gonzálezet al., 2010; Castillo et al., 2016). In this study surface temperaturefluctuated between 10.4 °C and 13.3 °C, with the lowest values recordedin Stn. 1 during May, and the highest at Stn. 1 in April. In terms of

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

53M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

dissolved oxygen, well-oxygenated waters of approximately 8 mL L−1

were observed at the surface of brackish waters, but surface O2 fallsbelow 4 mL L−1 during the second sampling period, especially at Stn.1, which is the station closest to the mouth of the Reloncaví fjord(Fig. 2a–i). Castillo et al. (2016) has described the oceanographicconditions of Reloncaví fjord to have a well-stratified water column, in-cluding a thin surface layer of brackish water with mean salinities be-tween 10.4 ± 1.4 (spring) and 13.2 ± 2.5 (autumn).

Additionally, Chilean Patagonia is characterized by continual humidconditions throughout the year, subjected to abundant precipitation(around 3000 mm year−1) during winter (June to August) and glacialmeltwater during spring/summer (September–January) (Garreaud,2009; León-Muñoz et al., 2013). Throughout the study period the pre-cipitation was recorded at the Puelo meteorological station (41° 39′3.96″S 72° 18′42.12″O); 353,4 mm recorded during April; 834 mmdur-ing May, and 2430 mm during September 2015 (available at http://explorador.cr2.cl). This precipitation will eventually contribute to riverrunoff. Thus, river discharges of glacial origin (Petrohué, Puelo andCochamo Rivers) towards the Reloncaví fjord can reach a maximumflow from July to September, with flow intensities reaching up to~1500 m3 s−1 (Castillo et al., 2016), in turn this is an important driverof biogeochemical activity in the case of a volcanic eruption.

Table 1Average of environmental variables (mean ± standard deviation) values for the three stations

Depth N2O (nM)April

N2O (nM)May

AOU (μM)April

AOU (μM)May

% saturationN2OApril

% saturationN2OMay

1 22.9 ± 3.75 9.7 ± 0.34 120 ± 8.0 95 ± 25.2 219 ± 33.2 84.3 ± 4.15 30.7 ± 1.52 11.9 ± 1.23 143 ± 16.5 125 ± 12.7 316 ± 14.9 119 ± 12.910 29.8 ± 4.52 12.9 ± 1.44 145 ± 8.2 136 ± 6.70 304 ± 46.0 131 ± 14.425 31.7 ± 4.94 12.9 ± 0.34 38.8 ± 7.0 32.6 ± 14.6 319 ± 48.3 130 ± 3.4050 34.0 ± 1.50 13.5 ± 0.18 62.6 ± 18.1 56.8 ± 83.9 342 ± 15.8 137 ± 2.00

3.1. Biogeochemistry of estuarine waters

The occurrence of volcanic eruptions in Patagonia has led high con-centrations of SO4

2− in surrounding areas (Bia et al., 2015). As a conse-quence high levels of SO4

2− have been observed in surface waters(0–5 m depth) of the fjord, after April relatively high levels were re-corded (Table 1), between b500 to 2300 mg L−1 that decreased overtime due to dilution from precipitation and snowmelt. During May,the lowest surface SO4

2− concentrations were recorded in the surfacelayer (b500mg L−1). The fact that field samplingwas carried out imme-diately after the eruption, and in conditions of zero rainfall during theeruption event may explain the SO4

2− increase in surface waters.Flaathen and Gislason (2007) suggest that the effect of H2SO4 comingfrom volcanic eruptions is both temporally and spatially dependent;for example the location of Calbuco volcano is high latitude and is ex-posed to high solar radiation during daytime (during autumn), thusleading to an intense local H2SO4 contamination due to the high oxida-tion rate of SO2 into SO4

2−. However, in general, studies in Patagoniansurface waters have indicated that SO4

2− concentrations do no exceedthe detection limits of the instrumental methods (Beamud et al., 2013).

Volcanic fallout into aqueous environments leads to the dissolutionof adsorbed metal salts and aerosols, increasing the bioavailability of

along the Reloncaví fjord at different depth.

CH4 (nM)April

CH4 (nM)May

% saturationCH4

April

% saturationCH4

May

SO42−

(mg L−1)April

SO42-

(mg L−1)May

15.8 ± 13.1 36.3 ± 10.5 553 ± 456 1169 ± 318 1991 ± 379 257 ± 1446.30 ± 5.19 6.00 ± 3.93 243 ± 200 227 ± 149 1292 ± 128 –2.44 ± 0.78 2.18 ± 1.01 94.3 ± 30.4 83.6 ± 38.7 – –2.93 ± 1.16 3.32 ± 2.65 112 ± 43.6 191 ± 15.4 – –1.63 ± 0.67 8.74 ± 9.10 62.2 ± 25.6 335 ± 349 – 1794 ± 347

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Fig. 3. Nutrient distribution for the three stations along the Reloncaví Fjord: NO3− (μM) (A, B, C), PO4

3− (μM) (D, E, F), Si(OH)4 (μM) (G, H, I) and N:P (J, K, L).

54 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

key nutrients (Jones and Gislason, 2008). However, low NO3− and PO4

3−

values (b5 μM) were found in the Reloncaví Fjord. NO3− concentrations

in the entire water column varied between 0.77 μM and 23.3 μM, withthe lowest concentrations in the surface waters up to 5 m depth withinthe estuary (Stn. 1). These low concentrations are mainly due to the di-lution effect of freshwater discharges from the Puelo River, due tomelt-waters and rainfall (León-Muñoz et al., 2013). In contrast, the highestNO3

− concentrations in subsurface waters (Stn. 3) were observed nearto the Puelo River in April during the first sampling period (Fig. 3a–c).NO3

− concentrations increased in subsurface waters as salinity in-creased, this is a characteristic of sub-Antarctic waters entering the es-tuary (Fig. 3a–c). The nutrient results are consistent with the previousresults reported by several authors, indicating that freshwater from riv-ers inputs silicic acid into the surfacewaters, due tomeltwater and rain-fall (León-Muñoz et al., 2013; Farías et al., 2017). Instead, the overlayingmarine subsurface water is nutrient rich in both nitrogen and phospho-rus (Yevenes et al., 2017; Farías et al., 2017; Iriarte et al., 2017). It islikely that the highest Si(OH)4 levels recorded post eruption led tohigh biogenic productivity in the area and contributed to the atypicalphytoplankton bloom (Fig. 3j–l). One important characteristic of north-ern Chilean Patagonia is the presence of andosol-type soil, that bringsabout abundant dissolved Si(OH)4 concentrations in the surroundingaquatic system as a product of river runoff (Vandekerkhove et al.,2016). High salinity and nutrient-rich subsurface waters were presentunder 10 m depth (Fig. 3a–c), which is typically associated with theintrusion of deep water masses, which is modified sub-Antarcticwater entering through the mouth of Reloncaví estuary (Castillo et al.,2016). Nevertheless, estuarine stratification could limit mixing and

entrainment of nutrients between layers, from subsurfacewaters to sur-face waters, as observed in other estuarine systems (Silva and Vargas,2014).

The region of Patagonia is understood to undergo a potential lightlimitation during autumn (Iriarte et al., 2017), resulting in low chloro-phyll and phytoplankton biomass in surface waters. However, thisstudy indicated that a maximum Chl-a of 20–25 mg L−1 was observedduring the April sampling period, in surface waters, at approximately4mdepth (Fig. 4a). Thus indicating that the phytoplankton bloom is po-tentially associated with the utilization of available nutrients. However,during May, Chl-a concentration decreased and was homogeneousthroughout the entire water column (b2 μg L−1, Fig. 4b). Another phy-toplankton bloom, but deeper and less intense, was observed in the sub-surface layer during September, reaching a Chl-amaximumof 15 μg L−1

between 10 and 15m depth (Fig. 4c). This has been previously reportedduring spring (Iriarte et al., 2007).

3.2. Distribution of the carbonate system and greenhouse gases

Volcano eruptions can disturb the carbonate system, inducingabrupt acidification in the top layer of the ocean (Flaathen andGislason, 2007). These results indicate that pHT and AT values rangedfrom 7.67 up to 8.06 and 144 to 2136 in the upper 10 m depth of thebrackish layer, respectively (Fig. 4g–i). Relative to these results, noclear effect of the volcanic eruption on local acidification events wereobserved in the surface waters of the fjord during April and the subse-quent months. It is likely that surface pHT decreased due to the CO2 up-take associated with the high Chl-a concentration during these periods

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Fig. 4.Carbonate systemdistribution for the three stations along theReloncaví Fjord: Chla (A, B, C), pHT (D, E, F), AT (G, H, I), pCO2 (J, K, L),ΩArÑ duringfield visits inApril (A, D,G, J,M),May(B, E, H, K, N) and September (C, F, I, L, Ñ) during 2015.

55M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

(Fig. 4a, c), mainly due to the development of a large bloom of phyto-plankton during the days following the eruption. Vergara et al. (2016)continuously studied the carbonate system within the top surfacelayer of the fjord continually for one month after the eruption, usinghigh temporal resolution data (every 1 h) and with pH values as lowas 7.6 (≈0.4 pH units) during June. This value was closely related tothe minimum pHT values (7.2). It apparently took a few weeks afterthe precipitation events to flush out the readily soluble constituentsnear to the headwaters of the Reloncaví Fjord. pHT also decreasedbelow 7.7 in subsurface waters, similar to the situation observed forO2 concentration. A good correlation between pHT and the ApparentOxygen Utilization (AOU) implied the influence of organicmatter respi-ration on the pHT levels (Fig. 5c), however; this was not the case for thepCO2 and/or ΩAr (Fig. 5b, d). Instead, AT was highly correlated with sa-linity due to the influence of low AT in freshwater, especially duringApril (r2 = 0.81, r = p b 0.05), and very highly correlated during Sep-tember (r2 = 0.96, r = p b 0.05) (Fig. 5a). Certainly, surface waterswere undersaturated in CO2, with pCO2 b 400 μatm mainly duringApril and September, however levels rapidly increased with depth,from subsurface waters up to N1000 μatm. The low pCO2 conditions in

brackish waters are associated with low-salinity conditions in thesepermanently stratified waters. In turn, it is likely that corrosive watersfor CaCO3 in the surface layer (i.e. upper 4 m depth) are a frequent oc-currence (Torres et al., 2011; Silva et al., 2011; Alarcón et al., 2015).Low pHT, high pCO2, and CaCO3 sub-saturated waters (ΩAr) were ob-served in subsurface waters below 10 m depth, mainly during Apriland May field sampling periods, mostly associated with respiration ofboth autochthonous and allochthonous organic matter (Waldbusserand Salisbury, 2014). Zhai et al. (2015) discovered that bivalve specieswere affected by the presence of short-term aragonite corrosive waters(ΩAr) in the very shallowwaters of theNorthern Yellow Sea below15mdepth. This raised the concern that a greater effort is required by the lo-cally cultured bivalve species in order to calcify.

Unexpectedly high N2O concentrations (22.9 ± 3.75 nM) were re-corded in the surface layer of the Reloncaví Fjord, predominantly duringApril. In comparison, previous studies report that themaximumaveragereached 12 ± 2 nM (Yevenes et al., 2017). Higher concentrations wereobserved in Stn. 3, which is closer to Puelo River discharge. However,no significant correlations were found between N2O and salinity in thesurface water layer, implying a continental origin (Fig. 7a, b). Similarly,

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Fig. 5. Relationship between A) Salinity and Alkalinity (AT), B) AOU and pCO2, C) AOU and pHT, D) AOU andΩAr. Each figure includes data from the three field visits, April (Green), May(blue), September (red). (*) Indicates a significant relationship between variables. (For interpretation of the references to color in this figure legend, the reader is referred to the webversion of this article.)

56 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

riverine waters within the surface layer showed N2O concentrationsthat were twice as high as recorded by Yevenes et al. (2017), with satu-ration levels reaching as high as 342% in April. This coincided withmin-imum nitrate (NO3

−) levels during the same field-sampling period. Theobserved N2O saturation is apparently the result of overall denitrifica-tion in brackish water, since denitrification should not occur in well-oxygenated waters (Yevenes et al., 2017). Excess N2O (ΔN2O) is oneof the most relevant biogeochemical factors in estimating N2O produc-tion. If AOU and NO3

− are associated with ΔN2O, it may indicate thatN2O is of biogeochemical origin (Yoshinari, 1976). This is supportedby the significant linear relationship between ΔN2O and AOU, andΔN2O andNO3

−, duringApril andMay, respectively (Fig. 8a, c). ApparentN2O production can also be estimated through the consumption of O2

(AOU), based on the remineralization of particulate organic matter as-sociated with nitrification (Nevison et al., 2003). Oxygen consumptiondue to the oxidation of organicmatter suggests that NO3

− is formed dur-ing nitrification, and as a result N2O is also produced (Farías et al., 2015).

CH4 concentrations varied between 0.27 and 44.4 nM throughoutthe entire water column during April and May, with a maximum CH4

concentration of 44.4 nM, equivalent to 1411% saturation, observed at1 m depth (Stn. 3) in May (Fig. 6c, d) near to the mouth of PueloRiver. The observed concentrations of CH4 in surfacewaterswerewithinthe same range reported by previous studies between16.97 and 151nM(Farías et al., 2017). Towards Stn. 3, surface CH4 concentrations doubledthroughout both campaigns. Moreover, a strong correlation betweensurface CH4 concentrations with the pCO2 and Si(OH)4 confirm theinput into the fjord of continental CH4 sources from soils. Surfacewaterswere over-saturatedwith CH4, mainly duringMay. It is well known that

CH4 in fjords originates from anoxic sediments (Borges and Abril, 2011;Borges et al., 2016). However, Farías et al. (2017) identified that the bot-tom waters of the Reloncaví Fjord did not suggest consistently higherCH4 concentrations compared to surface layers (Fig. 6c, d).

3.3. Implications for shellfish farming industry

Calcifying organisms, such asmarinemolluscs, are exceptionally vul-nerable to fluctuations in carbon chemistry (Byrne, 2011; Gazeau et al.,2013). Figs. 9 and S1 as supplementary material show the morphomet-ric measurements recorded from juvenile's edible mussels, Mytiluschilensis, collected from settlement ropes within the Reloncaví Fjord.With the exception of shell thickness, that was homogeneous acrossdepth [Median ± IQR; Depth 1: 0.10 mm ± 0.05; Depth 3 m:0.09 mm ± 0.03; Depth 4 m: 0.10 mm ± 0.04; Kruskal Wallis, H =3.62; p = 0.164], the rest of variables showed significantly low valuesin the upper 3 m of the water column, however maximum values areconsistently attained at 4mdepth (p b 0.05). In fact, we found increasedshell thickness in the less favorable conditions in the upper depth layer,which may result as compensation in order to maintain shell strengthand functionality. Previous studies also evidenced that under favorableenvironmental conditions for shell precipitation (NΩAr), mussel seedsadapt to elongate a thin shell with a thicker periostracum, however, inless favorable conditions the strategy is to increase the shell thickness(Osores et al., 2017). Moreover, shell weight showed a significant in-crease at 4 m depth (0,10 mg ± 0,04;) respect to more surface levels(Depth 1 and 3m: 0.05mg±0.08) (H=10.55; p=0.005). Similar pat-tern was found in the soft tissue weight of the mussel seeds (Depth 1:

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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.

57M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

0.07 mg ± 0.05; Depth 3 m: 0.07 mm ± 0.07; Depth 4 m: 0.10 mm ±0.11; H = 6.96; p = 0.031). Molinet-Flores et al. (2015) also observedthat in natural banks, the condition index recorded in mussels livingin the upper 7 m depth was significantly greater than in mussels col-lected from deeper habitats. In addition, shell size measurementsshowed the same significant pattern of vertical variability (e.g., ShellLength: Depth 1: 13.3 mm ± 5.9; Depth 3 m: 12.8 mm ± 5.77; Depth4 m: 15.2 mm ± 6.8; H = 6.56; p = 0.038). Finally, the proportional

Fig. 7. Relationship between surface salinity, and N2O and CH4 during two field visits (April and

increments in length and weight of the mussel seeds as increased thedeep levels, the shell condition index, an integrative measure, indicatea progressive increment of the shell weight in relation to tissue weightof the individuals raised at 4m depth (Shell condition index: 41.1%± 9;Depth 3 m: 44% ± 8; Depth 4 m: 48%± 6; H= 6.56; p=0.038). Inter-estingly, morphometric analyses of mussel seeds demonstrated that at4 m depth (or the “optimum layer”) some attributes related with shelllength, weight, and biomass reached maximum levels (Fig. 10). For

May); N2O (A, B) and CH4 (C, D). (*) Indicates a significant relationship between variables.

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Fig. 8. Relationship between ΔN2O vs. AOU and ΔN2O vs. NO3− during two field visits in April (A, B) and May (C, D). (*) Indicates a significant relationship between variables.

58 M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

the Reloncaví areas previous studies indicated that a high load of seston(Mohr et al., 2017) and an increase in more corrosive waters may havean impact on the suspension feeding processes and shell thickness in

0

0.05

0.10

0.15

0.20

0.25

1 3 40

0.02

0.04

0.06

0.08

0.1

0.12

1 3

6

6.5

7

7.5

8

8.5

9

1 3 40.080

0.085

0.090

0.095

0.100

0.105

1 3 4

4

Tota

l wei

ght (

mg)

Dry

she

ll w

eigh

t (m

g)

Shel

l Hei

ght (

mm

)

Shel

l thi

ckne

ss (m

m)

Depth (meter)

H = 8.23 DF = 2 P = 0.016 N total = 306

H = 10.55 DF = 2 P = 0.005 N total = 299

H = 3.62 DF = 2 P = 0.164 N total = 291

H = 7.08 DF = 2 P = 0.029 N total = 295

Fig. 9.Median (±SE) in the morphometric measurements recorded inMytilus chilensis seeds cosummary of the Kruskal-Wallis statistic (H) test, measuring the equality of medians of mussel chof mussel seeds used in the test; Significant p values (b0.05) are showed in bold.

mussels, as it is necessary to spend extra energy to eliminate these par-ticles to their bodies (Salas-Yanquin et al., 2018). Therefore, under vol-canic effects this finding may have significant implications for mussel

0

0.02

0.04

0.06

0.08

0.1

0.12

1 3 412

12.5

13

13.5

14

14.5

15

15.5

16

1 3 4

36

38

40

42

44

46

48

50

1 3 4

Tiss

ue (m

g)

Shel

l Len

gth

(mm

)

Shel

l Con

ditio

n (%

)

H = 6.96 DF = 2 P = 0.031 N total = 299

H = 6.56 DF = 2 P = 0.038N total = 296

H = 23.35 DF = 2 P < 0.001N total = 295

llected over three depths in a mussel farm located in the Reloncaví Fjord. Inset presents aaracteristics over different depths. DF=degrees of freedom; N total is the overall number

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O2 Sal

Low due to high pCO2 Low O2 waters by organic matter remineralization

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

Optimum for mussel growth and calcification

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

59M.A. Yevenes et al. / Science of the Total Environment 669 (2019) 49–61

farmers in this fjord environment, as the installation of mussels ropes inthis layer. Supposedly present optimal conditions for mussel seed pro-duction, could implement amanagement strategy to reduce the impactsof changes during different climatic scenarios, such as carbon chemistryin surface waters, both for ocean acidification processes and/or chang-ing runoff conditions. Furthermore, this layer of aragonite-saturatedwaters could be an additional factor explaining the spatial distribution

−0.4 −0.2 0.0 0.2 0.4

−0.4

−0.2

0.0

0.2

0.4

PC1

PC2

−2 −1 0 1 2

−1.5

−1.0

−0.5

0.0

0.5

1.0

1.5

Depth

Chl_a

O2TemperatureSalinity

pH

Alcalinity

pCO2

Aragonite

Methane

Nitrous.oxide

NitratePhosphate

Silicate

Total.weightDry.shell.weight

TissueShell.lengthShell.height

Shell.thickness

Shell.condition

Fig. 11. Principal components analysis (PCA) of biological and physicochemical variablesfrom the Reloncaví fjord waters.

pattern of Mytilus chilensis beds in the Reloncaví Fjord. At this depth,of the optimal range for mussel growth and production in this estuarineenvironment was evidenced for a good correlation between variables.For instance, the first PCA component explained 66% of the total vari-ance, and showed a positive correlation with Temperature, Salinity, AT,ΩAr, N2O, NO3

−, PO43−, pCO2, and Shell condition (Fig. 11). This area con-

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 ofwhich are liable to impacts from decreasing pHT. Furthermore, reduc-tion in ΩAr could be a significant challenge for other calcifying pelagicand benthic organisms inhabiting similar fjord ecosystems in the South-ern Patagonia, such as pelagic pteropods (Roberts et al., 2011), echino-derms, and gastropods (Newcombe and Cárdenas, 2011).

4. Conclusion

This study investigates the potential effect of a high magnitude vol-canic eruption through the study of nutrients, greenhouse gases, andthe carbonate system in the Reloncaví Fjord during autumn (April andMay) and spring (September) 2015. Additionally, the impact of poten-tial changeswas study in the carbonate system on the condition ofmus-sel shells in a nearby farming area. The outputs indicated a localizedimpact of the volcanic eruption on surface greenhouses gasesmainly ni-trous oxide, nutrients and short-term effects on the carbonate system.Despite our results indicate the presence of CaCO3 corrosive waters(ΩAr) in the Reloncaví Fjord, however no direct relation with the vol-cano eruption was found. Best conditions for mussel calcification wererecognized within a subsurface band, or refuge at 4 m depth, withinthe estuarine environment, which appear to be resilient to catastrophicevents such as volcanic eruptions occurring in the Patagonian region.These specific aspects can be integrated into adaptation strategies bythe mussel aquaculture industry to tackle ocean acidification andchanging runoff conditions.

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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.org/10.1016/j.scitotenv.2019.03.037.

Acknowledgments

This work was supported by the Millennium Nucleus “Center for theStudy of Multiple-drivers on Marine Socio-Ecological Systems (MUSELS)”fundedbyMINECONNC120086, and theCenter for Climate andResilienceResearch Center (CR)2, CONICYT-Chile. Additional support from theMil-lennium Institute of Oceanography (IMO) funded byMINECON IC120019is also acknowledged. The authorswould like to thank to Pia Leon for labprocessing, the Mussel Farming Company ORIZON for logistical supportduring our fieldwork, as well as the logistical support from the Techno-logical Institute for theMussel Farming Industry (INTEMIT) and the Fisher-ies Development Institute (IFOP). CAV was supported by the CONICYT/FONDECYT/1170065 during themanuscript preparation. MAYwas sup-ported by CONICYT/FONDAP/15130015 during the stage of the manu-script writing. NAL also acknowledge support by PIA CONICYTANILLOS ACT 172037 during the last stages of the manuscript.

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