Benthic oxygen fluxes in a coastal upwelling system (Ria de Vigo, NW Iberia) measured by aquatic eddy covariance
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Vol. 670: 15–31, 2021 MARINE ECOLOGY PROGRESS SERIES
Published July 22
https://doi.org/10.3354/meps13770 Mar Ecol Prog Ser
OPEN
ACCESS
Benthic oxygen fluxes in a coastal
upwelling system (Ria de Vigo, NW Iberia)
measured by aquatic eddy covariance
M. Amo-Seco1, 2,*, C. G. Castro1, N. Villacieros-Robineau1, F. Alonso-Pérez1, 5,
R. Graña3, G. Rosón4, P. Berg2
1
Instituto de Investigacións Mariñas (IIM), CSIC, Vigo 36208, Spain
2
Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22904, USA
3
Centro Oceanográfico de Gijón, IEO, Gijón 33212, Spain
4
Departamento de Física Aplicada, Universidade de Vigo, Vigo 36310, Spain
5
Present address: Centro Oceanográfico de Vigo, IEO, Vigo 36390, Spain
ABSTRACT: Organic carbon mineralization and nutrient cycling in benthic environments are
critically important for their biogeochemical functioning, but are poorly understood in coastal up-
welling systems. The main objective of this study was to determine benthic oxygen fluxes in a
muddy sediment in the Ria de Vigo (NW Iberian coastal upwelling), by applying the aquatic eddy
covariance (AEC) technique during 2 campaigns in different seasons (June and October 2017).
The main drivers of benthic fluxes were studied and compared among days in each season and
between seasons. The 2 campaigns were characterized by an upwelling-relaxation period
followed by a downwelling event, the last of which was due to the extratropical cyclone Ophelia
in October. The mean (± SD) seasonal benthic oxygen fluxes were not significantly different for
the 2 campaigns despite differences in hydrodynamic and biogeochemical conditions (June: −20.9
± 7.1 mmol m−2 d−1 vs. October: −26.5 ± 3.1 mmol m−2 d−1). Benthic fluxes were controlled by dif-
ferent drivers depending on the season. June was characterized by sinking labile organic mate-
rial, which enhanced benthic fluxes in the downwelling event, whereas October had a signifi-
cantly higher bottom velocity that stimulated the benthic fluxes. Finally, a comparison with a large
benthic chamber (0.50 m2) was made during October. Despite methodological differences
between AEC and chamber measurements, concurrent fluxes agreed within an acceptable mar-
gin (AEC:benthic chamber ratio = 0.78 ± 0.13; mean ± SD). Bottle incubations of water sampled
from the chamber interior indicated that mineralization could explain this difference. These
results show the importance of using non-invasive techniques such as AEC to resolve benthic flux
dynamics.
KEY WORDS: Benthic fluxes · Aquatic eddy covariance · Benthic chamber · Dissolved oxygen ·
Muddy sediments · Upwelling system · Rias
1. INTRODUCTION areas (Wollast 1998), and they support approximately
50% of the total benthic carbon mineralization (Mid-
Coastal regions are active biogeochemical areas delburg et al. 1997). Primary production generates a
which play an important role in the global carbon large amount of labile organic matter in the coastal
cycle. Although coastal regions occupy only 7% of margins, which, to a large extent, is deposited on the
the total oceanic surface, between 20 and 50% of the sediment surface. This particulate matter can sub-
total oceanic primary production occurs in these sequently be subjected to resuspension, advection,
© The authors 2021. Open Access under Creative Commons by
*Corresponding author: amoseco@iim.csic.es Attribution Licence. Use, distribution and reproduction are un-
restricted. Authors and original publication must be credited.
Publisher: Inter-Research · www.int-res.com
16 Mar Ecol Prog Ser 670: 15–31, 2021 or biogeochemical transformations, which promote in permeable sediments, whereas traditional benthic the benthic mineralization of organic carbon and chambers cannot mimic the natural porewater ex- benthic regeneration of nutrients (Wollast 1998). change produced by horizontal pressure gradients Conversely, these recycled nutrients support the well (Cook et al. 2007, Berg & Huettel 2008). In fact, large primary production of coastal areas (Grenz et most of the previous coastal studies relying on the al. 2010). Oxygen is the most energetically favour- AEC technique have been carried out in permeable able oxidant to react in the direct mineralization of sediments (Huettel et al. 2014 and references there- organic carbon and also to re-oxidize reduced prod- in, Attard et al. 2015, Reimers et al. 2016). Only a ucts of anaerobic mineralization. Thus, benthic oxy- small number of AEC measurements have been car- gen uptake is the most common proxy used to quan- ried out in muddy coastal sediments (Berg et al. 2003, tify the total mineralization rate of organic carbon on Glud et al. 2010, 2016, Holtappels et al. 2013, Attard the seafloor, because it is relatively easy to measure et al. 2016). compared to dissolved inorganic carbon fluxes (Froe- Our study was conducted in the Ria de Vigo lich et al. 1979, Glud 2008). Among coastal margins, (Fig. 1), located in the NW Iberian coastal upwelling coastal upwelling regions constitute the most biolog- system. This area is characterized by high prima- ically productive areas due to the upwelling of cold ry production during the upwelling season when and nutrient-rich subsurface waters. Additionally, nutrient-rich subsurface waters reach the sea surface these regions are highly dynamic and are character- and trigger substantial phytoplankton blooms (up to ized by the occurrence of upwelling/downwelling 5 mg chlorophyll a m−3, Figueiras et al. 2002). This events, which potentially influence benthic reminer- enables the Rias Baixas, including the Ria de Vigo alization. Consequently, in these regions, it is partic- (Fig. 1), to support the highest mussel production in ularly important to measure benthic oxygen fluxes Europe (Figueiras et al. 2002). In spite of the impor- over different time scales to integrate the most im- tance of benthic mineralization as a source of nutri- portant biogeochemical processes (Berelson et al. ents to sustain primary production in coastal systems, 2013, Reimers et al. 2016). there are few previous investigations of benthic flux- In the context of global climate change, global es in the Rias Baixas (Alonso-Pérez & Castro 2014, warming and coastal eutrophication are altering ben- Alonso-Pérez et al. 2015). These studies estimated thic dynamics of coastal zones. The synergistic effect that benthic mineralization is responsible for 40% of of these stressors increases benthic organic matter the total inorganic nitrogen that supports primary mineralization, which intensifies benthic fluxes, and production in the Ria de Vigo. These studies were consequently, decreases oxygen concentrations. The carried out in muddy sediments, which are abundant number of hypoxic coastal areas have increased 10- in the ria, playing a key role in organic carbon miner- fold since the first half of the 20th century and have alization and in benthic nutrient regeneration (Vilas triggered a severe loss of biodiversity (Diaz & Rosen- et al. 2005, Alonso-Pérez & Castro 2014). berg 2008). This increase supports the idea that the Based on this background, the main objectives of distribution and exchange of oxygen between the this study were to (1) determine the magnitude of water column and the sediment are critical parame- benthic mineralization in a muddy area of the Ria de ters to determine the biological status of the coastal Vigo by implementing the AEC technique and (2) environment (Glud 2008). establish the principal forcing factors that control the The non-invasive aquatic eddy covariance (AEC) benthic oxygen flux dynamics during the study peri- technique (Berg et al. 2003) to determine benthic ods. In order to do this, AEC benthic fluxes were oxygen fluxes has several advantages over traditio- measured during 2 campaigns, June 2017 (upwelling nal methods. This technique calculates fluxes from season) and October 2017 (transition from upwelling measured turbulent fluctuations of the vertical velo- to downwelling season), with different hydrodyna- city and oxygen concentration (Berg et al. 2003). mic and biogeochemical conditions. AEC has a greater temporal resolution than tradi- tional techniques like benthic chambers and inte- grates benthic fluxes over a larger area (10−100 m2) 2. MATERIALS AND METHODS (Berg et al. 2007, Rheuban & Berg 2013). It is a non- intrusive technique, as the benthic fluxes can be de- 2.1. Study area termined without disturbing natural hydrodynamic conditions and without resuspending the benthic The Ria de Vigo is 1 of the 4 Rias Baixas (temperate surface. Moreover, AEC can measure benthic fluxes coastal embayments, Evans & Prego 2003) located in
Amo-Seco et al.: Benthic oxygen fluxes in NW Iberia 17
Fig. 1. (a) Bathymetry of the Ria de Vigo, showing the inner ria (IR) sampling site and the different locations of the measuring
instruments (inset): Nortek Aquadopp Profiler (42° 15.870’ N, 8° 42.132’ W, blue dot), CTD (42° 16.186’ N, 8° 41.985’ W, green
triangle), benthic chamber (42° 16.226’ N, 8° 41.860’ W, black open circle), and aquatic eddy covariance (42° 16.217’ N,
8° 41.849’ W, red cross). (b) Aquatic eddy covariance frame. Photo credit: Manuel E. Garci (UMIMAG, IIM-CSIC)
the NW Iberian coastal upwelling system (Fig. 1). It is Shelf winds are the main factor controlling the sub-
characterized by a V-shaped transversal profile with tidal circulation of the ria, although other important
a NE−SW central channel. It has a length of 21 km factors can modify this circulation, such as river dis-
from Cíes Islands to the Rande Strait. The inner part charge (Piedracoba et al. 2005). Our sampling site
and central axis of the ria consist of predominately was located in the main channel in the inner part of
fine-grained sediment, compared to coarser-grained the ria (Fig. 1). This area is characterized by unvege-
sediment that dominates the outer part of the ria tated muddy sediments and is mainly exposed to
(Vilas et al. 2005). NE−SW currents (Villacieros-Robineau et al. 2013).
Hydrography and residual circulation in the ria are The presence of molluscs, ophiuroids, and penna-
largely modulated by the seasonal pattern of shelf tulacean anthozoans has been documented in the
winds caused by the meridional migration of the main channel of the Ria de Vigo (Aneiros et al. 2015).
Azores High. Responding to shelf winds, the Ria de
Vigo presents a classical estuarine circulation. Nor-
therly winds (prevalent from March/April to Septem- 2.2. Water sampling
ber/October) produce an offshore Ekman transport
of surface waters and the upwelling of cold and Data collection occurred during 2 different sea-
nutrient-rich subsurface waters. Conversely, souther- sons: summer (12−30 June) and autumn (2−20 Octo-
ly winds generate an onshore Ekman transport trig- ber) of 2017. Our sampling site (Fig. 1) was located
gering the accumulation of oceanic water onto the in the inner ria (42° 16.186’ N, 8° 41.985’ W) with an
coast and the downwelling of surface waters (Fraga average depth of 21.8 m. During each campaign, the
1981, Nogueira et al. 1997, Figueiras et al. 2002). site was sampled 3 times a week over a 3 wk period.
However, this seasonal cycle only explains about Data collection was carried out during research cam-
10% of the variability in the wind regime off north- paigns on board the RV ‘Mytilus’.
west Spain, whereas more than 70% of the variabil- Vertical profiles of temperature, salinity, oxygen,
ity arises from periods < 30 d (Álvarez-Salgado et al. and fluorescence were obtained with a CTD SBE 911
2003). In fact, the upwelling/downwelling seasons in plus (Sea-Bird) coupled to a bottle rosette system
the region are described as a succession of upwelling/ with 12 Niskin bottles of 10 l capacity to obtain sea-
downwelling events lasting between 3 and 10 d (No- water samples for oxygen, chlorophyll a (chl a), and
gueira et al. 1997, Gilcoto et al. 2017). particulate organic carbon (POC). Three or 4 water
18 Mar Ecol Prog Ser 670: 15–31, 2021
column depths were sampled depending on the loca- October campaigns (Table 1). The ADV measuring
tion of the subsurface chlorophyll maximum depth volume was approximately 11 cm above the bottom. A
determined through CTD fluorescence. Dissolved stable dual oxygen−temperature optode (miniDOT,
oxygen was determined by Winkler potentiometric PME) was attached to the frame for independent oxy-
titration. The precision of the method was ± 0.32 μM. gen concentration measurements every 5 min.
To measure chl a, 100 ml of seawater were filtered us-
ing GF/F filters with a pore size of 0.7 μm. After filtra-
tion, samples were frozen (−20°C) until pigment ex- 2.5. Benthic chamber
traction in 90% acetone over 24 h in the dark at 4°C.
Chl a was analysed through fluorometric determina- Benthic oxygen fluxes were also measured in a de-
tion using a Turner Designs fluorometer (Yentsch & ployed benthic chamber to complement the AEC re-
Menzel 1963). The precision of the method was sults. Benthic chamber deployments were carried out
± 0.07 μg l−1. For POC analysis, 0.5 l seawater samples at our field site (42° 16.226’ N, 8° 41.860’ W, Fig. 1) at
were filtered on pre-weighted and pre-combusted an average depth of 21.1 m. The chamber was care-
(4 h, 450°C) GF/F filters of 0.7 μm pore size. Measure- fully deployed for the same days as the AEC deploy-
ments of POC were determined with a Perkin Elmer ments using a mooring line. The deployment opera-
2400 CNH analyser. The precision was ± 0.3 μM. tion was checked by divers. Details of the benthic
chamber measurements are described by Ferrón et
al. (2008). In short, the benthic chamber has a large
2.3. Residual and total current volume of 140 l and covers a large total sediment
area of 0.50 m2 (one of the largest benthic chambers
Total current was obtained using an upward look-
ing 400 kHz Nortek Aquadopp Profiler moored at Table 1. Aquatic eddy covariance (AEC) and benthic cham-
25.8 m depth at the study site (42° 15.870’ N, 8° 42. ber (BC) deployment duration and oceanographic character-
132’ W, Fig. 1), between 8 June (20:00 h UTC) and istics of each deployment. BC fluxes for the June campaign
13 July (09:45 h) 2017 for the June campaign and were not considered due to technical difficulties during
the deployment. Temperature and salinity were obtained
between 25 September (20:00 h) and 30 October from the deepest depth recorder with a CTD profiler. Veloc-
(11:40 h) 2017 for the October campaign. Twelve ity was measured with an acoustic Doppler velocimeter
cells (bin size 200 cm) were established through the (mean ± SD)
water column. The residual current was extracted
using a low-pass symmetric digital filter (PL33) with Date Duration (h) T (°C) Salinity Velocity
a cutoff period of 33 h (Flagg et al. 1976, Beardsley et AEC BC (cm s−1)
al. 1985) to remove tidal frequencies. This analysis
June
was carried out in MATLAB.
12 8.3 − 14.1 35.69 3.1 ± 1.2
14 7.5 − 13.8 35.68 2.3 ± 1.2
16a − − 13.4 35.69 −
2.4. Aquatic eddy covariance 19 6.9 − 13.3 37.71 1.1 ± 0.5
21 7.5 − 13.5 35.66 1.5 ± 0.9
23 7.8 − 14.5 35.62 2.2 ± 0.7
Benthic oxygen fluxes were measured with the AEC 26 7.0 − 14.8 35.61 3.5 ± 1.3
technique (Berg et al. 2003). Instrumentation for the 28 7.3 − 16.0 35.52 3.0 ± 1.5
AEC measurements was mounted on a light frame 30 7.3 − 14.9 35.59 1.5 ± 0.7
(Berg & Huettel 2008) and consists of a Nortek Vector October
acoustic Doppler velocimeter (ADV) and a dual sensor 02a − 6.7 14.7 35.59 −
(RINKO EC, JFE Advantech), which allows high-fre- 04 7.3 6.2 13.9 35.62 3.4 ± 1.2
06 7.3 6.2 14.0 35.59 6.0 ± 2.9
quency (64 Hz) recording of temperature and oxygen 09 7.5 6.0 14.1 35.58 4.1 ± 1.4
concentrations at the same volume of water (Berg et al. 11b 9.6 8.5 13.7 35.60 0.7 ± 0.3
2016). The AEC system was deployed at our sampling 13b 8.0 6.7 14.0 35.59 1.0 ± 0.3
site (42°16.217’ N, 8°41.849’W, Fig. 1) at an average 16b 8.7 7.5 14.8 35.55 0.7 ± 0.5
18 7.0 6.1 15.4 35.48 3.0 ± 0.7
depth of 20.1 m. It was deployed by divers and care
20 6.9 6.0 15.6 35.44 5.0 ± 1.8
was taken to direct the ADV x-axis into the main cur-
a
rent direction. A total of 18 deployments, lasting be- AEC instrument failure
b
Accurate fluxes could not be obtained because of the
tween 7 and 9 h to preferentially cover either tidal in- low bottom velocity
flow or outflow, were carried out during the June and
Amo-Seco et al.: Benthic oxygen fluxes in NW Iberia 19
available) (Ferrón et al. 2008). Water height inside code 2248) anchored at a depth of 600 m. These
the chamber was 28 cm. A constant tangential veloc- hourly data were provided by Puertos del Estado
ity of 2.5 cm s−1 was kept inside the chamber during (www.puertos.es). Wind data measured by the Cape
the deployment. Inside the benthic chamber, there Silleiro buoy at a 3 m height were converted to 10 m
are sensors to record continuous measurements of height winds by applying a logarithmic profile with a
temperature (SBE 39, Sea-Bird), turbidity (Seapoint roughness length of 0.002 m (Herrera et al. 2005).
Turbidity Meter), oxygen (SBE 43, Sea-Bird), and pH Shelf wind data were filtered using a low-pass filter.
(SBE 18, Sea-Bird) with a sample interval of 30 s. The The upwelling index (UI) was calculated from the
mean chamber incubation time in this study was shelf winds following Bakun (1973):
approximately 7 h (Table 1). Benthic chamber fluxes
ρair C D V Vy
were calculated from changes in oxygen concentra- UI = – (1)
ρsw f
tions during the incubation period by an empirical
linear fitting. Uncertainties of fluxes were related to where ρair is the average density of the air (1.22 kg
the fit of the data to a linear function and the propa- m−3 at 15°C), CD is the empirical drag coefficient
gation of random errors (Ferrón et al. 2008). (1.3 × 10−3 according to Hidy 1972), f is the Coriolis
On 2 occasions during the October campaign, 6 re- factor at 42° latitude, and ρsw is the density of the sea
plicate samples of seawater from the benthic chamber water (1025 kg m−3). |V | is the module and Vy is the
interior were manually collected in 125 ml Winkler north component of the wind velocity at a height of
flasks by divers just before the beginning of the benthic 10 m. Positive values of UI correspond to upwelling
chamber incubation period. Three replicates were conditions and negative values indicate downwelling.
fixed on board to measure oxygen concentration at the
starting point of the incubation, and the other 3
samples were incubated in situ during the benthic 2.8. Data processing
chamber deployment time. Dissolved oxygen was
measured by a Winkler potentiometric titration as de- 2.8.1. Aquatic eddy covariance
scribed in Section 2.2 for the water column. Oxygen
consumption in the water column inside the benthic Fluxes of oxygen were extracted from the raw eddy
chamber was calculated as the oxygen concentration covariance data following the multi-step AEC process
difference at the initial and final time of the incubation. described below and shown in Fig. 2. First, oxygen
concentration was calibrated against the stable inde-
pendent dual oxygen−temperature sensor data
2.6. Sediment samples (Fig. 2b). All 64 Hz data were then reduced to 8 Hz
data, which reduces noise while still providing suffi-
Surface sediment samples were collected using a cient resolution to contain the full frequency spectrum
Van Veen grab sampler on 3 different days (8 June, carrying the flux signal (Berg et al. 2009). Benthic
13 July, and 30 November). A total of 3 replicate sam- oxygen fluxes were then computed using the software
ples were obtained for each day. Granulometric package Eddy Flux version 3.2 (P. Berg unpubl.).
analysis was carried out using an LS 13 320 Beckman Benthic oxygen fluxes were calculated using high-
Coulter system on non-homogenized sub-samples of resolution data of vertical velocity (vz) and oxygen
–
roughly 1 g after removal of organic matter and car- concentration. The mean benthic oxygen flux (F ) was
bonates by adding 10% H2O2 and 25% HCl, respec- computed as the average over 15 min intervals of the
tively. Organic carbon content analysis was per- vertical turbulent fluctuations in velocity (v ’z) times
formed on triplicates of 20 mg sub-samples after the turbulent fluctuations in oxygen concentration
eliminating carbonates by repeatedly adding 10 μl of (C ’) (Eq. 2; Berg et al. 2003). Turbulent fluctuating
25% HCl (Zúñiga et al. 2016). Organic carbon was components, v ’z and C ’, were calculated as vz – v––z and
analysed using a Perkin Elmer 2400 CNH analyser as C –C ⁻⁻ applying a linear detrending where v––z and C ⁻⁻
previously explained for POC water samples. are the least-square linear fits to the 8 Hz measured
data, vz and C, in each 15 min burst (Lee et al. 2004,
Berg et al. 2009):
2.7. Upwelling index
F = v ’z C ’ (2)
Shelf winds were obtained from the Seawatch Due to the response time of the fast-responding
buoy located in Cape Silleiro (42° 7.2’ N, 9° 25.8’ W, oxygen sensor combined with its position down-
20 Mar Ecol Prog Ser 670: 15–31, 2021
Fig. 2. Examples of aquatic eddy covariance (AEC) measurements and processed time series for 9 October. (a) Bottom velocity
components: vx (red line), vy (green line), and vz (blue line) and mean current velocity (black line). (b) Bottom oxygen concen-
tration measured by miniDOT (blue dotted line) and RINKO EC (red line). (c) Cumulative fluxes. Red lines indicate fluxes
discarded in the data quality check. (d) Benthic oxygen 15 min fluxes
stream from the ADV’s measuring volume, a time A data quality check was performed to remove er-
shift correction was applied (Berg et al. 2016). Fol- roneous measurements produced by collisions be-
lowing the standard practice for eddy covariance tween floating particles and the RINKO EC sensor.
data processing (Fan et al. 1990, Lorrai et al. 2010), Cumulative fluxes (Fig. 2c) were calculated by a run-
this was done by repeating the outlined flux extrac- ning sum of instantaneous vertical fluxes (v ’z C ’) over
tion procedure, while shifting the 8 Hz oxygen con- time within each 15 min interval. In each burst, the
centration data back in time, 1/8 s at a time, until the cumulative flux was verified for any anomalous fluc-
numerically largest flux was identified (Eddy Flux tuation that was not due to natural turbulence
3.2, P. Berg unpubl.). (Fig. 2c; Berg et al. 2013). Data recorded when the
Amo-Seco et al.: Benthic oxygen fluxes in NW Iberia 21 flow came from behind of the oxygen sensor were ing the downwelling (26−29 June), residual current excluded. Fluxes calculated for 15 min bursts with changed to a negative circulation pattern with inflow low mean velocity (
22 Mar Ecol Prog Ser 670: 15–31, 2021
Fig. 3. Hydrodynamic and biogeochemical conditions of the water column during the June campaign: (a) upwelling index (UI);
(b) temperature; (c) total and (d) residual current velocity (E−W component), where negative values (blue) represent outgoing
currents and positive values (red) represent incoming currents to Ria de Vigo; (e) oxygen concentration; (f) particulate organic
carbon (POC) concentration; black dots indicate water sample depthsAmo-Seco et al.: Benthic oxygen fluxes in NW Iberia 23 Fig. 4. As in Fig. 3, but for the October campaign
24 Mar Ecol Prog Ser 670: 15–31, 2021
In the first period of the autumn campaign, there to these sediment characteristics, this site is subject
was a maximum oxygen concentration at the sea sur- to the formation of a fluff layer over the seabed. Daily
face and minima beginning at 10 m (Fig. 4e). POC mean benthic fluxes were obtained from high resolu-
showed the same pattern with a sea surface maxi- tion 15 min interval flux data (Fig. 2). All of the fluxes
mum (Fig. 4f). These conditions persisted until wind determined in this study were negative, indicating
relaxation, when there was an intense mixing (6− oxygen uptake by the sediment. During the summer
13 October) that disrupted the previous surface max- campaign, bottom velocity ranged from 1.1 to 3.5 cm
ima of oxygen and POC. During the subsequent s−1 (Fig. 5a). In the first period of the campaign (12−
downwelling period (15−20 October), oxygen con- 25 June), bottom velocity reached a minimum value
centrations increased, reaching values higher than on 19 June and increased during the following down-
200 μM (Fig. 4e). There was also a slight increase in welling event (26−30 June). Bottom oxygen concen-
POC in the last days of this period (18−20 October, trations increased progressively during the summer
Fig. 4f), but these POC concentrations were consis- campaign (Fig. 5b). Temperature showed a similar
tently lower than during the summer campaign. pattern with a minimum value on 19 June and maxi-
mum value on 28 June (Fig. 5b). Benthic fluxes were
low during the summer upwelling-relaxation period
3.3. Aquatic eddy covariance fluxes with a minimum of −15.1 mmol m−2 d−1 on 12 June
(Fig. 5c). In the subsequent downwelling period, flux-
The AEC system was deployed at a site above es were higher, reaching a maximum of −35.0 mmol
sandy mud sediment (clay 20%, silt 59%, sand 21%) m−2 d−1 on 26 June. Mean benthic oxygen flux was
according to Folk’s classification (Folk 1954), with an −16.4 ± 1.2 mmol m−2 d−1 during the first period and
organic carbon content of 3.1 ± 0.2% by weight. Due −28.6 ± 5.7 mmol m−2 d−1 during the second period,
Fig. 5. Benthic conditions measured by aquatic eddy covariance (AEC) during the June campaign: (a) bottom velocity; (b) bot-
tom oxygen concentration and temperature (black line); (c) daily AEC benthic oxygen fluxes. Measurements were recorded
at 11 cm above the sediment surface. Error bars represent ± SDAmo-Seco et al.: Benthic oxygen fluxes in NW Iberia 25
Fig. 6. As in Fig. 5, but for the October campaign
with a moderate monthly coefficient of variation of in October daily variability (13−37%) was much
34% for June. higher than monthly variability (12%). In fact, only
During the autumn campaign, bottom velocity on 18 October was daily variability of the same order
ranged from 0.7 to 6.0 cm s−1 with a maximum on 6 of magnitude as monthly variability.
October (Fig. 6a). Bottom oxygen concentrations in-
creased progressively during the campaign from val-
ues of 131 μM on 4 October to 200 μM on the last day 3.4. Benthic chamber fluxes
(20 October). Temperatures showed a similar pattern
to oxygen concentrations, with lower temperatures In situ benthic chamber fluxes showed similar pat-
during the upwelling-relaxation period and higher terns to those obtained by AEC for the October cam-
temperatures during the downwelling event. Benthic paign. The initial temperatures and oxygen concen-
fluxes were not computed for 11, 13, and 16 October, trations inside the benthic chamber (Fig. 7a) were
as bottom velocities were very low for these deploy- similar to daily mean values measured by the AEC
ments (26 Mar Ecol Prog Ser 670: 15–31, 2021
Fig. 7. Benthic conditions measured by benthic chamber during the October campaign: (a) initial oxygen concentrations and
temperature (black line) inside the benthic chamber; (b) daily benthic chamber oxygen fluxes (± SD)
coefficient of variation of 30%. The higher variabil- reported for fine-grained muddy sediments in the
ity was mainly due to the large fluxes found on 13 shallow bay of Aarhus (Berg et al. 2003) and the gla-
and 20 October. For comparison, mean benthic oxy- cial fjord Loch Etive (Holtappels et al. 2013). In fact,
gen fluxes using the same deployment days as AEC all of these values followed the simple power rela-
were −31.4 ± 3.0 mmol m−2 d−1 during the up- tionship between benthic oxygen uptake and water
welling-relaxation event and −39.8 ± 5.3 mmol m−2 depth described by Glud (2008) based on a global
d−1 during the downwelling event. Seawater col- database of benthic oxygen fluxes (Fig. 8).
lected from the benthic chamber interior and incu- A comparison between results from AEC and the
bated in situ in the Winkler flasks during the de- benthic chamber was carried out in October 2017
ployment time had an average oxygen uptake of using the same deployment days. The mean benthic
10.2 ± 1.8 mmol m−2 d−1. flux was −26.5 ± 3.1 mmol m−2 d−1 for AEC and
−34.8 ± 5.7 mmol m−2 d−1 for the benthic chamber
(Fig. 9). Although these fluxes are significantly dif-
4. DISCUSSION ferent (p = 0.04, Wilcoxon matched pair test), they
agree within an acceptable margin given the funda-
4.1. Benthic fluxes mental differences between the 2 approaches and
possible heterogeneity of the sediment surface at
The mean benthic oxygen flux of −23.1 ± 6.4 mmol our site. Specifically, the mean daily ratio between
m−2 d−1 obtained by AEC from 13 deployments over AEC and benthic chamber fluxes was 0.78 ± 0.13,
the muddy sediments of Ria de Vigo (Table 1) is com- which is comparable to other ratios ranging from 1.4
parable to those (−32.9 mmol m−2 d−1) derived from to 0.75 found in previous studies in muddy sedi-
global-scale sediment−water flux data for coastal ments (Holtappels et al. 2013 and references com-
regions (Boynton et al. 2018). In addition, the mean in piled by Attard et al. 2015). A likely explanation of
our study is close to the average oxygen demand the difference is that mineralization processes
(−34 ± 10 mmol m−2 d−1) obtained previously by occurred in the bottom water enclosed in the cham-
Alonso-Pérez & Castro (2014) using benthic cham- ber. Indeed, bottle incubations of water sampled
bers during 4-season campaigns in the Ria de Vigo. from the chamber interior after it was deployed in-
To our knowledge, the AEC technique has only been dicated an average oxygen consumption of 10.2 ±
applied in a handful of muddy coastal marine sedi- 1.8 mmol m−2 d−1. This result emphasizes the impor-
ments (Berg et al. 2003, Glud et al. 2010, 2016, tance of deploying the benthic chamber with the
Holtappels et al. 2013, Attard et al. 2016). Our mean utmost care, especially when the sediment is a fluffy
value for the Ria de Vigo is within the range of values muddy sediment as was the case at our study site.Amo-Seco et al.: Benthic oxygen fluxes in NW Iberia 27
when northerly winds predominate, causing the up-
lift of subsurface nutrient-rich waters and triggering
intense phytoplankton blooms inside the Rias Baixas.
In contrast, October usually corresponds to the tran-
sition period between the upwelling and down-
welling seasons (Nogueira et al. 1997, Figueiras et al.
2002). In June 2017, there was a strong upwelling
event that produced a proliferation of large diatoms
(M. Froján et al. unpubl. data). The stratified water
column of the following days favoured this phyto-
plankton growth, with chl a levels as high as 15 mg
m−3. During the subsequent downwelling, this labile
organic matter (senescent phytoplankton cells) be-
gan to sink, and conveyed by the water circulation it
was deposited on the sediment surface. In October
2017, there was an upwelling event with a slightly
Fig. 8. Comparison among (1) power function fit of benthic stratified water column followed by a wind relaxation
oxygen flux as a function of depth according to Glud (2008) during which there was a thermal homogenization.
(black line), (2) benthic oxygen fluxes obtained by aquatic Under these conditions, phytoplankton proliferation
eddy covariance (AEC) in coastal muddy zones (coloured
was much lower than during the phytoplankton
dots), and (3) mean AEC oxygen flux for the June and Octo-
ber campaigns obtained in this study (red dot). Power func- bloom of June 2017. Subsequently, the occurrence of
tion fit for AEC benthic fluxes in coastal muddy sediments is extratropical cyclone Ophelia triggered an intense
represented by a black dashed line downwelling, which caused the inflow of warm and
well-oxygenated oceanic surface waters into the en-
tire water column.
Changes in hydrodynamics and biogeochemical
conditions of the water column affect benthic oxygen
fluxes. Studies have shown the influence of oxygen,
temperature, and organic matter supply on the mag-
nitude of benthic oxygen fluxes (Cowan et al. 1996,
Lomas et al. 2002, Hopkinson & Smith 2005, Murrell
& Lehrter 2011, Alonso-Pérez & Castro 2014). Addi-
tionally, the way in which hydrodynamics control
benthic oxygen fluxes has been analysed in several
papers (Glud et al. 2007, Berg & Huettel 2008, Berg
et al. 2013).
Based on the distinct water column conditions
measured during the June and October 2017 sam-
pling periods, we expected different magnitudes of
benthic oxygen fluxes for these 2 periods. Daily ben-
Fig. 9. Mean ± SD benthic oxygen fluxes in October meas- thic oxygen fluxes in June were characterized by
ured by benthic chamber and by aquatic eddy covariance
high variability, distinguished by significantly
(AEC), and oxygen consumption measured from bottle in-
cubations; n: number of deployments smaller benthic oxygen fluxes for the upwelling-
relaxation period (average of −16.4 ± 1.2 mmol m−2
d−1; Fig. 10a) compared to the mean value of −28.6 ±
4.2. Main forcing factors of the benthic fluxes 5.7 mmol m−2 d−1 during the downwelling event at
the end of June (26−30 June, Mann-Whitney U-test,
The intensive hydrographic and biogeochemical p = 0.03, Fig. 10a). The large benthic fluxes at the
sampling during the June and October 2017 cam- end of June are associated with significantly higher
paigns allowed us to investigate the controls of temperatures (Mann-Whitney U-test, p = 0.03,
changes in benthic oxygen fluxes during 2 different Fig. 10b), and relatively higher, though not signifi-
seasonal periods for the NW Iberian upwelling sys- cant, oxygen concentrations (Mann-Whitney U-test,
tem. June is part of a substantial upwelling season, p = 0.1, Fig. 10c) and bottom velocity (Mann-Whitney28 Mar Ecol Prog Ser 670: 15–31, 2021
Fig. 10. Average values of (a) aquatic eddy covariance
(AEC) benthic oxygen flux, (b) bottom temperature (T), and
(c) bottom oxygen concentration from RINKO EC; (d) bottom
velocity from the acoustic Doppler velocimeter; and (e) par-
ticulate organic carbon (POC) integrated along the water
column for the 2 different hydrodynamic periods during the
June and October campaigns: upwelling-relaxation period
(blue bars), downwelling period (red bars). Averages for
each campaign (June or October) are represented by the
white bars. * indicates significant differences between the
2 hydrodynamic periods (p < 0.05)
U-test, p = 0.5, Fig. 10d). Interestingly, it was during Thus, we suggest that the sinking of highly labile orga-
this summer downwelling event that the largest ben- nic matter formed during the previous upwelling-
thic oxygen fluxes for the entire study were meas- stratification conditions (maximum amount of POC
ured, larger than the mean benthic oxygen flux for was 548 ± 69 mmol m−2, Figs. 3f & 10e) would en-
the autumn downwelling event due to extratropical hance the benthic oxygen fluxes at the end of the
cyclone Ophelia. Even though the stronger bottom June campaign. In fact, M. Froján et al. (unpubl.
velocity in the October campaign (4.3 ± 1.2 cm s−1) data) also observed the sinking of large diatoms due
intensified benthic oxygen exchange, the highest to the circulation reversal (surface inflow and bottom
mean flux during the summer downwelling had rela- outflow) associated with the wind relaxation and
tively lower bottom velocities (2.3 ± 0.9 cm s−1) and subsequent downwelling after 23 June at different
similar temperature and oxygen concentrations. sites in the Ria de Vigo. This large supply of labileAmo-Seco et al.: Benthic oxygen fluxes in NW Iberia 29
organic matter triggered the high benthic oxygen Acknowledgements. We thank the captain and the crew of
fluxes for the summer downwelling. Consequently, the RV ‘Mytilus’, as well as the Oceanography Group from
the Instituto de Investigacións Mariñas (IIM-CSIC) for their
during the summer campaign, the principal forcing collaboration during the campaigns. We are grateful to the
factor that modulated the benthic oxygen fluxes was divers, Manuel E. Garci, Alexandre Chamorro, Rubén
the supply of organic matter. Chamorro, and Iñaki Ferreiro, for their invaluable help dur-
In October, no significant differences occurred in ing the deployments. We also acknowledge Puertos del
Estado for providing meteorological data. M.A.S. and N.V.R.
benthic oxygen fluxes between the upwelling-relax-
were funded by the Spanish Government through a Forma-
ation period (−25.7 ± 1.2 mmol m−2 d−1) and the strong ción de Profesorado Universitario fellowship (FPU 18/05051)
downwelling after 14 October (−27.7 ± 5.2 mmol m−2 and a Juan de la Cierva-Formación fellowship (FJCI-
d−1, Mann-Whitney U-test, p = 0.6, Fig. 10a). Addi- 2017−34290), respectively. Financial support was provided
by the Spanish Ministry of Science and Innovation through
tionally, no significant differences were observed in
the i-SMALL project (CTM2014-56119-R) and by the Euro-
any of the studied variables (temperature, oxygen pean Union FEDER project MarRISK (0262_MarRISK_1_E).
concentration, bottom velocity, and POC) between This study was also supported by grants from the US
both periods. Comparison of the mean benthic fluxes National Science Foundation (OCE-1550822, OCE-1824144)
for the June (−20.9 ± 7.1 mmol m−2 d−1) and October and the University of Virginia. We thank Rachel E. Michaels
for editorial assistance with the manuscript. Finally, we
(−26.5 ± 3.1 mmol m−2 d−1) campaigns resulted in thank Dr. Kristensen, Dr. Attard and 2 anonymous reviewers
similar values, even though available POC concen- for their helpful comments.
trations were much higher in June (Fig. 10e), and
bottom temperature and oxygen concentrations were
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