Particle sinking is a major form of transport for photosynthetically fixed
carbon to below the euphotic zone via the biological carbon pump (BCP).
Oxygen (O2) depletion may improve the efficiency of the BCP.
However, the mechanisms by which O2 deficiency can enhance
particulate organic matter (POM) vertical fluxes are not well understood.
Here, we investigate the composition and vertical fluxes of POM in two deep
basins of the Baltic Sea (GB: Gotland Basin and LD: Landsort Deep). The two
basins showed different O2 regimes resulting from the intrusion of
oxygen-rich water from the North Sea that ventilated the water column below
140 m in GB, but not in LD, during the time of sampling. In June 2015, we
deployed surface-tethered drifting sediment traps in oxic surface waters (GB:
40 and 60 m; LD: 40 and 55 m), within the oxygen minimum zone (OMZ; GB:
110 m and LD: 110 and 180 m) and at recently oxygenated waters by the North
Sea inflow in GB (180 m). The primary objective of this study was to test
the hypothesis that the different O2 conditions in the water column
of GB and LD affected the composition and vertical flux of sinking particles
and caused differences in export efficiency between those two basins.
The composition and vertical flux of sinking particles were different in GB and
LD. In GB, particulate organic carbon (POC) flux was 18 % lower in the
shallowest trap (40 m) than in the deepest sediment trap (at 180 m).
Particulate nitrogen (PN) and Coomassie stainable particle (CSP) fluxes
decreased with depth, while particulate organic phosphorus (POP), biogenic
silicate (BSi), chlorophyll a (Chl a) and transparent exopolymeric particle
(TEP) fluxes peaked within the core of the OMZ (110 m); this coincided with
the presence of manganese oxide-like (MnOx-like) particles aggregated with
organic matter. In LD, vertical fluxes of POC, PN and CSPs decreased by 28 %,
42 % and 56 %, respectively, from the surface to deep waters. POP, BSi and
TEP fluxes did not decrease continuously with depth, but they were higher at
110 m. Although we observe a higher vertical flux of POP, BSi and TEPs
coinciding with abundant MnOx-like particles at 110 m in both basins, the
peak in the vertical flux of POM and MnOx-like particles was much higher in
GB than in LD. Sinking particles were remarkably enriched in BSi, indicating
that diatoms were preferentially included in sinking aggregates and/or there
was an inclusion of lithogenic Si (scavenged into sinking particles) in our
analysis. During this study, the POC transfer efficiency (POC flux at 180 m
over 40 m) was higher in GB (115 %) than in LD (69 %), suggesting that
under anoxic conditions a smaller portion of the POC exported below the
euphotic zone was transferred to 180 m than under reoxygenated conditions
present in GB. In addition, the vertical fluxes of MnOx-like particles were
2 orders of magnitude higher in GB than LD. Our results suggest that
POM aggregates with MnOx-like particles formed after the inflow of
oxygen-rich water into GB, and the formation of those MnOx–OM-rich particles may
alter the composition and vertical flux of POM, potentially contributing to
a higher transfer efficiency of POC in GB. This idea is consistent with
observations of fresher and less degraded organic matter in deep waters of
GB than LD.
Introduction
Particle sinking is the primary mechanism for transporting
photosynthetically fixed carbon below the euphotic zone via the biological
carbon pump (BCP) (Boyd and Trull, 2007; Turner, 2015). Previous studies
suggested that the transfer of particulate organic carbon (POC) from the
euphotic zone to the ocean interior is enhanced in oxygen minimum zones
(OMZs) (Cavan et al., 2017; Devol and Hartnett, 2001; Engel et al., 2017;
Keil et al., 2016; Van Mooy et al., 2002). Possible mechanisms explaining
the higher POC transfer include the following: (i) the reduction of aggregate fragmentation
due to the lower zooplankton abundance within the OMZ (Cavan et al.,
2017; Keil et al., 2016); (ii) the potentially high contribution of
refractory terrestrial organic matter (OM) to the POC flux (Keil et al.,
2016; Van Mooy et al., 2002); (iii) a decrease in heterotrophic microbial
activity due to oxygen (O2) limitation (Devol and
Hartnett, 2001); (iv) the preferential degradation of nitrogen-rich organic
compounds (Kalvelage et al., 2013; Van Mooy et al., 2002; Engel et al.,
2017);
and (v) changes in ballast materials that may alter the sinking velocity and
protect OM from degradation (Armstrong et al., 2002).
Currently, the study of POC vertical flux in OMZs has been mostly focused
on the tropical ocean (Cavan et al., 2017; Devol and Hartnett, 2001;
Engel et al., 2017; Keil et al., 2016; Van Mooy et al., 2002), whereas how
low O2 concentration would affect the composition and fate of sinking
OM, and the efficiency of the BCP in oxygen-deficient zones of
temperate–boreal regimes such as the Baltic deep basins, has been less
studied.
The semi-enclosed, brackish Baltic Sea is a unique environment with strong
natural gradients of salinity and temperature (Kullenberg and Jacobsen,
1981), primary productivity, nutrients (Andersen et al., 2017), and
O2 concentrations (Carstensen et al., 2014a). New production,
defined as the fraction of the autotrophic production supported by
allochthonous sources of nitrogen (Dugdale and Goering, 1967), is considered
equivalent to the particulate OM export (Eppley and Peterson, 1979; Legendre
and Gosselin, 1989) on appropriate timescales. In the Baltic Sea, new
production varies seasonally (Thomas and Schneider, 1999), with periods of
high new production during spring and summer, supported by the
diatom-dominated spring bloom and by diazotrophic cyanobacteria, respectively
(Wasmund and Uhlig, 2003). Based on sediment trap data collected at 140 m
of depth in the Gotland Basin (GB), Struck et al. (2004) reported that the
highest fluxes of POC occurred in fall, followed by summer and spring. Using
δ15N, they showed that during the summer, N2
fixation by diazotrophic species is the primary source (∼41 %) of
the exported nitrogen and that the majority of the sedimentary particulate
organic matter (POM) in the central Baltic Sea is of pelagic origin.
OM export from the euphotic zone to the seafloor has a dual significance in
the deep basins of the Baltic Sea. On the one hand, it contributes to the
long-term burial of POC and consequently to the removal and long-term
storage of CO2 from surface waters (Emeis et al., 2000; Leipe et
al., 2011); on the other hand, it connects the pelagic and the benthic
systems contributing to the O2 consumption and hence deoxygenation at
depth. Environmental and anthropogenic changes may alter the magnitude and
composition of OM transferred from the surface to the seafloor in the Baltic
Sea (Tamelander et al., 2017). The reduction of nutrient inputs as targeted
by the Baltic Marine Environment Protection Commission (HELCOM) may reduce
the OM downward flux and limit the oxygen depletion at depth. However, since
hypoxia occurred naturally in the Baltic Sea due to physical processes,
mitigating eutrophication will only decrease the spatial extent and
intensity of the O2 deficiency in the deep basins.
GB (248 m) and Landsort Deep (LD; 460 m) are the deepest basins of the
Baltic Sea. They exhibit permanent bottom-water hypoxia (Conley et al.,
2009) caused by a combination of limited water exchange with the North Sea
through the Kattegat, strong vertical stratification, and high production–remineralization of OM due to eutrophication (Carstensen et al., 2014b;
Conley et al., 2009). A permanent transition zone of about 2 to 10 m
thickness separates the oxygenated surface and the oxygen-deficient waters,
with a pelagic redoxcline located approximately between 127 and 129 m in GB
and between 79 and 85 m in LD (Glockzin et al., 2014). From the 1950s to
1970s, the hypoxic zones (<60µM) in the Baltic Sea
expanded fourfold (Carstensen et al., 2014a). Saltwater inflows from the
North Sea are the primary mechanism renewing deep water in the central Baltic
Sea (Matthäus et al., 2008). A major Baltic inflow (MBI) occurred in
2014–2015 (Mohrholz et al., 2015); this event ventilated bottom
waters for
5 months between February and July 2015 (Holtermann et al., 2017). This
MBI caused the intrusion of O2 to deep hypoxic waters, substantial
temperature variability (Holtermann et al., 2017), displacement of remnant
stagnant water masses by new water that changed the chemistry of the water
column (Myllykangas et al., 2017), and high turbidities that may be
associated with redox reactions products (Schmale et al., 2016). At the time
of sampling (June 2015), the MBI had reached GB but did not affect LD,
located further northwest. The oxygenated water inflow reached GB at the
beginning of March and created a secondary near-bottom redoxcline (Schmale et
al., 2016); the bottom-water anoxia started to reestablish in July 2015
(Dellwig et al., 2018). In LD, water properties did not change due to the
MBI, the sulfidic layer was maintained (hydrogen sulfide, H2S
concentrations of 20.7–21.2 µM), and salinity varied between 10.6
and 10.9 (Holtermann et al., 2017).
Pelagic redoxclines are the suboxic transition between oxic and anoxic –
even sulfidic – waters. A steep redox gradient characterizes this transition
zone where electron acceptors and their reduced counterparts are vertically
segregated, and biogeochemical transformations mediated by microbial
processes are actively occurring (Bonaglia et al., 2016; Brettar and
Rheinheimer, 1991; Neretin et al., 2003). For instance, iron (Fe) and
manganese (Mn) undergo rapidly reversible transformations at the redox
interface. Mn is an essential electron donor and acceptor in redox processes
occurring in brackish, pelagic systems with anoxic conditions like the deep
basins of the Baltic Sea. Redox conditions control the biogeochemical
transformations between dissolved Mn2+ and insoluble oxides and
hydroxides of Mn4+. Under anoxic conditions dissolved and reduced Mn
forms dominate, while in the presence of O2 the formation of
particulate manganese oxides (MnOx) is favored. The concentration of
dissolved Mn may reach 0.3 µM in GB and a maximum value of about
3 µM in the LD (Dellwig et al., 2012). Van Hulten et al. (2017)
estimated an aggregation threshold for manganese oxides of 25 pM and
suggested that a minimal concentration of dissolved Mn is required for an
efficient aggregation and removal of MnOx. Therefore, in GB and LD, the
balance between dissolve Mn and the formation of MnOx is controlled by the
O2 availability (e.g., Neretin et al., 2003). LD is characterized
by a permanently stratified water column and sulfidic bottom waters; these
conditions favored the accumulation of high concentrations of dissolved Mn
(Dellwig et al., 2012).
In contrast, GB is periodically affected by lateral intrusions of
O2 and the oxygenation of deep water as a result of MBIs that occur
every 1 to 4 years (Matthäus and Franck, 1992), favoring the
occurrence of MnOx-containing particles. MnOx production may be microbially
mediated (Richardson et al., 1988) or authigenic (Glockzin et al., 2014). In
sulfidic waters, the reduction of MnOx with sulfide occurs within a scale of
seconds to minutes (Neretin et al., 2003) and is inhibited by nitrate
(Dollhopf et al., 2000). The oxygenation of the deep water of GB by the
2014–2015 MBI combined with the release of Mn from the sediments into the
water column (Lenz et al., 2015) generated appropriate conditions to enhance
particulate MnOx formation and vertically expand the zone where they could be
observed in the water column.
MnOx-containing particles have previously been observed at pelagic
redoxclines in the Baltic Sea (Glockzin et al., 2014; Neretin et al., 2003).
They are amorphous or star-shaped particles and occur as single particles or
form aggregates with OM (Neretin et al., 2003), specifically with transparent
exopolymer particles (TEPs) (Glockzin et al., 2014). The sinking velocity
(0.76 m d-1) of those mixed aggregates containing MnOx and TEPs was
lower than what was predicted by the Stokes law, possibly due to their star-shaped
morphology and the high OM content. TEPs are highly sticky,
polysaccharide-rich particles that can enhance particle aggregation rates and
the formation of marine snow (Engel, 2000; Logan et al., 1995). Thus, the
sinking of MnOx–OM aggregates may contribute to the downward flux of POC.
However, high content of TEPs relative to more dense particles could reduce
the density of marine aggregates and decrease their sinking velocity (Engel
and Schartau, 1999). Another type of less studied exopolymer particles are
CSPs; they are protein-containing particles
that stain with Coomassie brilliant blue (Long and Azam, 1996). Little is
known about the characteristics and dynamics of those particles in marine
systems, and their potential to form aggregates with MnOx has not been
studied. Different to TEPs, CSPs have a limited role in the aggregation of
diatoms (Prieto et al., 2002;
Cisternas-Novoa et al., 2015), but seem to be
important for the aggregation of cyanobacteria (Cisternas-Novoa et al.,
2015). Mixed MnOx–OM aggregates may affect the cycling of particle-reactive
elements like phosphorus and trace metals via scavenging processes, and it
has been proposed that they could act as carriers of bacteria in the
redoxcline (Dellwig et al., 2010). To date, there are no measurements of the
density of MnOx–OM aggregates, their potential ballast effect on sinking OM,
or their biogeochemical role modifying the vertical flux of POM in the Baltic
Sea.
The objectives of this study are, first, to determine the amount and
composition of particles sinking out of the euphotic zone into the deep
basins of the Baltic Sea: GB and LD. The second objective is to study how the oxygenation of
deep waters (>140 m) caused by the 2014–2015 MBI may affect the
vertical flux of sinking particles. We therefore compared GB, which was affected by
the MBI, with LD, which was not affected and exhibited low O2
concentration (>74 m) and even sulfidic conditions (>180 m). We hypothesized that the MBI that altered the water column chemistry
and created different O2 conditions in GB compared with LD affected the
composition and vertical flux of sinking particles. Additionally, the higher
abundance and in situ formation of MnOx–OM aggregates may cause differences in
the degradation and export of OM between the two basins.
MethodsSampling location and water column properties
Samples were collected during the BalticOM cruise in the Baltic Sea onboard
the RV Alkor form 3 to 19 June 2015. We collected sinking
particles using surface-tethered drifting sediment traps (Engel et al.,
2017; Knauer et al., 1979) in GB and LD (Table 1). Additionally, water
column samples (Table 2) were collected using a Niskin-bottle rosette at the
locations of the trap deployments. Temperature, salinity and O2
concentration were determined at each station using a Sea-Bird (CTD) probe
equipped with an O2 sensor (Oxyguard, PreSens), calibrated with
discrete samples measured using the Winkler method (Strickland
and Parsons, 1968; Wilhelm, 1888).
Sediment trap deployment and recovery locations, dates, collection
times and depths. Two sediment traps were deployed at 40 m (A and B) to
evaluate replicability.
StationLat.Long.DateStationDeploymentTrap depthsdepthtime (d)(m)Gotland Basin57.21∘ N20.03∘ E8 June 2015248 m240A, 40B, 60,(GB)57.27∘ N20.25∘ E10 June 2015110, and 180 mLandsort Deep58.69∘ N18.55∘ E15 June 2015460 m140A, 40B, 55,(LD)58.68∘ N18.68∘ E16 June 2015110, and 180 m
Abundance of chlorophyll- and phycoerythrin-containing picoplankton and
nanoplankton measured by flow cytometry in GB and LD.
We deployed two surface-tethered drifting sediment traps for 2 days in GB and
1 day in LD (Fig. 1). Each trap collected particles at four depths: 40 m
(two arrays were deployed to evaluate replicability of particle collection),
60 m (55 m in LD), 110 m and 180 m (Table 1) to estimate POM fluxes to
and within the OMZ. 40 m was considered as the base of the euphotic zone
based on photosynthetically active radiation
measurements conducted during the cruise (data not shown). At each depth, 12
acrylic particle interceptor tubes (PITs) mounted in a PVC cross-frame were
deployed. Each PIT was equipped with an acrylic baffle at the top to minimize
the collection of swimmers (Engel et al., 2017; Knauer et al., 1979). The
PITs were 7 cm in diameter and 53 cm in height with an aspect ratio of 7.5
and a collection area of 0.0038 m-2. The cross-frame and PITs were
attached to a line that had a bottom weight and a set of surface and
subsurface floats. The procedures for PIT preparation and sample recovery
followed Engel et al. (2017). Shortly before deployment, each PIT was filled
with 1.5 L of seawater previously filtered through a 0.2 µm pore
size cartridge. A preservative solution of saline brine (50 g L-1) was
added slowly to each PIT underneath the 1.5 L of filtered seawater,
carefully keeping the density gradient. The PITs were kept covered until
deployment and immediately after recovery to avoid contamination. After
recovery, the density gradient was visually verified, and the supernatant
seawater was siphoned off the PIT. Then, we pooled together the remaining
water, containing the sinking material (∼0.6–0.8 L), of 12 tubes per
depth into a large container that we filled up to 10 L with filtered
seawater (between 0.4 and 1.5 L) to have the same volume per depth. After
that, the samples were screened with a 500 µm mesh to remove
swimmers (Conte et al., 2001). Subsequently, samples were split into aliquots
that were processed for the different biogeochemical analysis as described in
Engel et al. (2017).
Monthly averaged Chl a distribution derived from VIIRS for
June 2015 in the Baltic Sea. Black circle and “x” indicate the position of
the trap deployment and the seawater collection, respectively, in Gotland
Basin (GB) and Landsort Deep (LD). The lower panel shows the trajectory of the
trap deployed at GB and LD.
Biogeochemical analysis
Nutrients were measured in seawater samples collected at the deployment
stations. Ammonium (detection limit of 0.05 µM) was measured directly
on unfiltered seawater samples onboard after Solórzano (1969).
Phosphate, nitrate and nitrite (detection limit of 0.04 µM) were
filtered through a 0.2 µm pore size and stored frozen until their
analysis; samples were measured photometrically with continuous-flow
analysis on an auto-analyzer (QuAAtro; Seal Analytical) after Grasshoff et
al. (1999).
Particulate organic carbon (POC), nitrogen (PN), organic phosphorus (POP)
and chlorophyll a (Chl a) were determined as described in Engel et al. (2017).
Aliquots of 100 to 200 mL of the trapped material and 500 mL of the
seawater samples were filtered in duplicate for each parameter at low
vacuum (<200 mbar) onto precombusted GF/F filters (8 h at
500 ∘C). The filters were stored frozen (-20∘C) until
analysis. Prior to analysis, filters for POC–PN determination were exposed to
acid fumes (37 % hydrochloric acid) to remove carbonates and subsequently
dried for 12 h at 60 ∘C. POC and PN concentrations were determined
using an elemental analyzer (Euro EA, Hechatech) after Sharp (1974).
POP was analyzed after Hansen and Koroleff (1999). POP was oxidized to
orthophosphate by heating the filters in 40 mL of deionized water
(18.2 MΩ) with Oxisolv (Merck 112936) for 30 min in a pressure
cooker. Orthophosphate was determined spectrophotometrically at 882 nm in a
Shimadzu UV–Vis spectrophotometer UV1201.
Chl a was analyzed after extraction with 10 mL of 90 % acetone, and
the fluorescence of the samples was measured using a Turner fluorometer
(excitation 440 nm, emission 685 nm; Turner 10AU) according to Strickland et al. (1972). The
fluorometer was calibrated with a standard solution of Chl a (Sigma-Aldrich
C-5753).
Biogenic silica (BSi) was determined in aliquots of 50 to 100 mL, filtered
in duplicate onto 0.4 µm cellulose acetate filters. Samples were
stored at -20∘C until analysis. For the measurements, filters
were digested in NaOH at 85 ∘C for 135 min; the pH was adjusted to
8 with HCl. Silicate was measured spectrophotometrically according to Hansen
and Koroleff (2007).
Polysaccharide (TEP) and protein (CSP) exopolymer particles, from sediment
trap and water column samples, were analyzed by microscopy according to
Engel (2009). Duplicate aliquots of 5 to 20 mL were filtered onto
0.4 µm Nuclepore membrane filters (Whatmann) and stained with 1 mL
of Alcian blue solution, a dye that targets acidic polysaccharides, for TEPs
or 1 mL of Coomassie brilliant blue solution, a dye commonly used to stain
proteins (Bradford, 1976), for CSPs. Filters were transferred onto
Cytoclear® slides and frozen
(-20∘C) until microscopy analysis. For the analysis, 30 images
for each filter were captured under 200× magnification using a light
microscope (Zeiss Axio Scope.A1) connected to a color camera (AxioCam MRc).
Particle abundance and area were measured semiautomatically using an image
analysis system including the WCIF ImageJ software. The RGB was split into
three channels (red, blue and green), and the red was used to quantify the
amount of TEPs and CSPs. Additionally, TEPs and CSPs in water samples from
the stations where we deployed sediment traps were analyzed
spectrophotometrically (with higher vertical resolution than microscopy)
according to Passow and Alldredge (1995) and Cisternas-Novoa et al. (2014),
respectively. Concentrations of TEPs are reported relative to a xanthan gum
standard and expressed in micrograms of xanthan gum equivalent per liter
(µg XG eq. L-1), and concentrations of CSPs are reported
relative to a bovine serum albumin standard and expressed in micrograms of
bovine serum albumin equivalent per liter (µg BSA eq. L-1).
MnOx-containing particles have been commonly identified based on their
morphology, size and elemental composition, confirmed by scanning electron
microscopy (SEM) and energy-dispersive X-ray microanalysis (EDX) (Neretin et
al., 2003; Glockzin et al., 2014; Dellwig et al., 2010, 2018). In this study,
we did not measure the elemental composition of the particles. Thus, we
identified them as MnOx-like particles based on similar morphology, size
and association with organic matter (OM) as MnOx-containing particles
previously described in the Baltic Sea (eg., Neretin et al., 2003; Glockzin
et al., 2014). The abundance and size of MnOx-like particles were determined
using particle recognition on filters and image processing similar to the
method used by Neretin et al. (2003) but without the chemical composition
analysis of the particles. For the image analysis, we used the same images as
for TEP and CSP analysis and modified the image analysis procedure described
above as follows: 30 images per filter (200×) were analyzed
semiautomatically using ImageJ software. After RGB split, the blue channel
pictures were used to quantify MnOx-like particles in the water column and
sediment traps. In this manner, the MnOx-like particles were clearly visible
with a negligible disruption from TEPs or CSPs stained blue.
Total hydrolyzable amino acids (TAAs) were analyzed in unfiltered seawater and
trapped material. Samples were stored at -20∘C until analysis.
Duplicate samples were hydrolyzed at 100 ∘C in 6N HCl
(Suprapur® hydrochloric acid 30 %) and 11 mM ascorbic acid
for 20 h. Amino acids were separated and measured by high-performance liquid
chromatography (HPLC), after derivatization with ortho-phthaldialdehyde using
a fluorescence detector (excitation 330 nm, emission 445 nm) (Dittmar et al.,
2009; Lindroth and Mopper, 1979). TAA concentrations were reported as
µM of monomer. The quantitative degradation index (DI) of Dauwe et
al. (1999), based on changes in the amino acid composition of POM as it
undergoes degradation processes, was calculated using the factor coefficient
of Dauwe et al. (1999) and the average and standard deviation of the TAAs in
this data set.
Total combined carbohydrates (TCHOs) >1 kDa were determined
by HPAEC-PAD according to Engel and Händel (2011). TCHOs were analyzed in
the unfiltered seawater and sediment trap material. Samples were stored at
-20∘C until analysis. Prior to analysis, the samples were
desalted by membrane dialysis using dialysis tubes with a 1 kDa molecular
weight cutoff (Spectra Por). Desalination was conducted for 4.5 h at
1 ∘C. Then, a 2 mL subsample was sealed with 1.6 mL of 1 M HCl
in precombusted glass ampoules and hydrolyzed for 20 h at 100 ∘C.
After hydrolysis, the subsamples were neutralized by acid evaporation under
N2 atmosphere at 50 ∘C, resuspended with ultrapure Milli-Q
water and analyzed on a Dionex 3000 ion chromatography system. TCHO
concentrations were reported as µM of monomer.
Phytoplankton abundance
Phytoplankton composition and abundance at the stations where we deployed
sediment traps were evaluated using light microscopy and flow cytometry.
Counts of phytoplankton cells >5µm were made from 50 mL
of fixed samples (Lugol's solution, 1 % final concentration). Samples were
concentrated using gravitational settling and counted under a Zeiss Axiovert
inverted microscope (200× magnification) following the guidelines for
determination of phytoplankton species composition and abundance (HELCOM,
2012). The counts were made on either half (cyanobacteria, diatoms and
Dinophysis sp.) or two strips (Cryptophyta, unidentified dinoflagellates and
Chlorophyta) of the chamber. Individual filaments of cyanobacteria were
counted in 50 µm length units. The size of the counted phytoplankton
species ranged from 10 to 200 µm.
Phytoplankton, <20µm, cell abundance was quantified using a
flow cytometer (FACSCalibur, Becton Dickinson, Oxford, UK). 2 mL samples were
fixed with formaldehyde (1 % final concentration) and stored frozen
(-80∘C) until analysis (2 weeks later). Red and orange
autofluorescence was used to identify chlorophyll and phycoerythrin cells.
Cell counts were determined with CellQuest software (Becton Dickinson);
picoplankton and nanoplankton populations of naturally containing chlorophyll
and/or phycoerythrin (i.e., Synechococcus) were identified and enumerated.
Statistics
Significant differences between two parameters were tested using the
Mann–Whitney U test. The results of statistical analyses were assumed to be
significant at p values <0.05. Statistical analyses were performed
using MATLAB software (MatlabR2014a).
ResultsBiogeochemistry of the water column
At both stations, GB and LD, the water column was stratified during the
study. In GB, the seasonal thermocline was located between 22 and 37 m, with
temperature decreasing rapidly from 9.8 ∘C in the surface mixed layer
to 4.7 ∘C below 37 m (Fig. 2a). Deeper in the water column, a
pycnocline (halocline) coincided with the oxycline and was located between
65 m (S=7.6) and 80 m (S=10.2); below 80 m the salinity gradually
increased up to 13.5 (220 m). A hypoxic layer (<40µM O2) was located between 74 and 140 m; the core
of the OMZ (<10µM O2) was located between 96
and 125 m. The O2 concentration increased from
35 µM O2 at 140 m to 79 µM O2 at
220 m (Fig. 2a). In LD, the seasonal thermocline was located between 10 and
39 m, where the temperature decreased gradually from 12 to 4.0 ∘C
(Fig. 2b). The pycnocline was between 55 (S=7.2) and 75 m (S=9); below
that the salinity was constant (S=10.7) until the bottom of the station
(430 m). The O2 concentration was below the detection limit
(<3µM O2) from 74 m to the deepest point
sampled in LD (430 m).
Water column profiles at the location of the sediment trap
deployments in (a) GB, and (b) LD. Left panels: oxygen (blue), temperature
(red) and salinity (black). Middle panels: nitrate (NO3, white
squares), nitrite (NO2, grey circles), ammonium (NH4, black
triangles) and hydrogen sulfide (H2S, black diamonds). Right panels: phosphate (PO4, grey diamond) and silicate
(Si(OH)4, black circles). Grey lines indicate the depths at which we
deployed sediment traps.
The vertical profile of nutrients was different at both stations (Fig. 2).
In GB, nitrate concentration increased from below the detection limit in the
upper 10 m to 0.17 µM at 40 m (Fig. 2a). Concentrations were
variable within the OMZ with 6 µM in the upper (80 m) and lower
oxycline (140 m) and 0.12 µM in the core of the OMZ (110 m). The nitrate
concentration was 4.8 µM in the deepest sample (220 m). Nitrite was
below the detection limit in most of the water column except for
60 m (0.09 µM) and 110 m (0.11 µM).
Ammonium increased from 0.14 µM in
the upper 10 m to 1.15 µM at 40 m; concentrations were variable
within the OMZ with less than 0.15 µM in the upper (80 m) and lower
oxycline (140 m) and a maximum concentration of 3.28 µM in the core of
the OMZ (110 m). Vertical profiles of phosphate and silicate at GB were
similar; the concentrations steadily increased from the upper 10 m of
the water column (0.29 and 10.36 µM, respectively) to the OMZ
(2.67 and 39.07 µM, respectively) and gradually decreased
below the OMZ (Fig. 2a). H2S was not detectable in GB.
Phytoplankton abundance analyzed microscopically for samples
collected at the location of trap deployment in GB and LD.
* Filamentous cyanobacteria were counted in 50 µm length
units (>90 % were Aphanizomenon sp.). ** Includes mixotrophs.
In LD, nitrate and nitrite concentrations were below the detection limit
between the surface and 250 m (<0.04µM) (Fig. 2b).
Nitrite showed a maximum of 0.22 µM at 350 m, and nitrate a
maximum of 6.0 µM at 400 m. Ammonium concentrations varied between
0.06 and 0.59 µM in the upper 70 m and increased to 5.97 and
8.03 µM in the OMZ (>74 m). The lowest ammonium
concentration (0.07 µM) was measured in the surface and the highest
(8.03 µM) at 110 m. Phosphate and silicate concentrations were
relatively low within the mixed layer, gradually increased below the
pycnocline, and decreased again between 110 and 180 m. Phosphate
concentrations varied between 1.5 and 2.5 µM in the upper 110 m of
the water column, decreased to 0.22 µM at 180 m and increased to
2.7 µM at 430 m (deepest sample). Silicate ranged between 25 and
38 µM in the upper 110 m of the water column, decreased to
7.4 µM at 180 m, and increased to 38.9 µM at 430 m.
H2S was detectable below 180 m, with the highest concentration
(3.97 µM) at 250 m and the lowest (0.04 µM) between 300
and 350 m (Fig. 2b).
Particulate organic matter concentration in the water column
Chl a concentration in the upper 10 m was slightly higher in GB
(1.5–1.7 µg L-1; Fig. 3b) than in LD (1.4–1.2 µg L-1; Fig. 3e). At
both stations, more than 90 % of the total smaller phytoplankton
(<20µm, picophytoplankton and nanophytoplankton) abundance, determined by
flow cytometry, was measured in the upper 60 m, although phytoplankton was
detectable in the entire water column. Picophytoplankton and nanophytoplankton
abundances
were 10 % higher in GB than in LD (Table 2). Picocyanobacteria determined
by phycoerythrin fluorescence accounted for 92 % and 96 % of the total
picophytoplankton abundance in GB and LD, respectively. Picocyanobacteria
abundance was 30 % higher in GB than in LD.
Vertical profiles of the concentration of particulate organic carbon
(POC), particulate nitrogen (PN) and particulate organic phosphorus (POP) in
GB (a) and LD (d); vertical profiles of the concentration of
chlorophyll a (Chl a) and biogenic silicate (BSi) in GB (b) and
LD (d); and vertical profiles of the concentration of transparent
exopolymeric particles (TEPs) and Coomassie stainable particles (CSPs) in GB
(c) and LD (f). Grey lines as Fig. 2.
Phytoplankton (>5µm) abundance, determined by microscopy,
was 63 % higher in LD than in GB (Table 3). Filamentous cyanobacteria
dominated the phytoplankton community at both stations with up to 90 %
corresponding to Aphanizomenon sp. Cyanobacteria represented 56 % of the phytoplankton
counts in GB and up to 74 % in LD. Dinoflagellates (including mixotrophs),
dominated by Dinophysis sp., were significant at both stations (19 % of the
phytoplankton counts), whereas chlorophytes (dominated by filaments of
Planctonema sp. containing cylindrical cells) were more abundant in GB than in LD
(25 % and 4 % of the phytoplankton counts, respectively). Diatoms
represented less than 1 % of the phytoplankton at both stations, and they
were slightly more abundant at 40 m in LD (Table 3). BSi was higher in the
upper 10 m (0.4–0.5 µM) and decreased with depth in GB (Fig. 3b),
whereas in LD, BSi showed a peak at 40 m and then decreased with depth (Fig. 3e).
Vertical profiles of POC, PN and POP concentration were similar in the
water column of the two stations (Fig. 3a, d). In GB, the concentrations
were higher in the upper 10 m of the water column (POC: 40.38±0.80,
PN: 3.89±0.01, POP: 0.26±0.04µM) and decreased
gradually with depth until 110 m where relatively high concentrations (POC: 18±0.63, PN: 2±0.08, POP: 0.2 µM) were observed. The
lowest concentrations were found at 180 m (POC: 11.97±1.03, PN:
1.05±0.02, and POP <0.03µM) (Fig. 3a). In LD, POM
decreased with depth from the surface (POC: 35±0.99, PN: 4±0.09, POP: 0.2 µM) to 40 m, remained relatively constant between 40
and 80 m, and decreased again between 110 and 250 m (Fig. 3d).
We observed high concentrations of TEPs and CSPs in the upper 10 m at both
stations. The highest TEP concentration was determined at 1 and 10 m at both
stations, and it was slightly higher (19 %) in GB than in LD (Fig. 3c,
f). TEP and CSP vertical profiles were different from each other in GB
(Fig. 3c) and covaried in LD (Fig. 3f). Like observed for POC, PN and POP,
TEP concentrations showed a peak at 110 m (50.29±6.17µg XG eq. L-1) in GB. The highest concentration of
CSPs at this station was observed in the shallowest (1 m) sample; the CSP
concentration decreased quickly below 10 m, and then it increased at 140 and
220 m (the deepest sample, approximately 28 m above the seafloor)
(Fig. 3c). In LD, the highest concentrations of TEPs and CSPs were measured at
the surface (1 and 10 m) and at 110 m (Fig. 3f). TEPs and CSPs decreased with
depth in the first 80 m (from 53.26±7.10 to 18.39±4.57µg XG eq. L-1 and from 53.26±7.10 to 31.57±18.78µg BSA eq. L-1). Both types of gel-like particles
showed an increase in concentration at 110 m (49.25±4.08µg XG eq. L-1 and 66.89±22.33µg BSA eq. L-1, respectively). Below 110 m, TEP
concentrations stayed relatively constant, while CSP concentrations decreased
at 180 m and remained relatively constant below that depth.
MnOx-like particle vertical distribution in the water column
Dark, star-shaped MnOx-like particles (Glockzin et al., 2014; Neretin et al.,
2003) were only observed below the fully oxygenated mixed layer in GB and, in
less abundance, in LD (Fig. 4). In GB, MnOx-like particles were observed from
80 to 220 m; they appear as single particles and forming large aggregates
containing several MnOx-like particles associated with OM. Relatively high
concentrations of MnOx-like particles (2×106 particles L-1)
were observed in the upper (80 m, 25 µM O2) and lower
(140 m, 36 µM O2) oxycline and at 220 m
(79 µM O2; 4×106 particles L-1) (Fig. 4a).
The lowest abundance of MnOx-like particles
(7×105 particles L-1) was observed at 110 m
(6 µM O2), i.e., in the core of the OMZ. The equivalent
spherical diameter (ESD) of MnOx-like particles varied between 0.6 and
30.5 µm, with a median size of 3.0 µm. The largest
aggregates (up to 30.5 µm) were observed in the upper oxycline
(80 m). In LD, MnOx-like particles were less abundant, smaller and had a
narrow distribution in the water column than in GB. MnOx-like particles were
not detected in the fully oxic (0–40 m) or fully anoxic (180 to 430 m)
water column. At 60 m (135 µM O2), right above the
oxycline, MnOx-like particles began to appear, but in relatively low
abundance. The maximum abundance of MnOx-like particles,
9×105 L-1, was observed in the oxycline at 70 m
(27 µM O2, Fig. 4b). The ESD ranged between 0.6 and
13.4 µm, and the largest aggregates were observed at 70 m.
Vertical profiles of MnOx-like particles and O2
concentration in the water column at the location of the sediment trap
deployments. (a) GB and (b) LD. Grey lines as in Fig. 3.
Vertical flux of sinking particles
Vertical fluxes of POC and PN varied little with depth in GB (Fig. 5a). POC
flux slightly increased by 18 % from the shallowest (40 m) to the
deepest (180 m) sediment trap. Fluxes of PN (Fig. 5a) and CSPs (Fig. 6b) were
higher at 40 and 60 m and decreased (19 % and 70 %) from 60 to
180 m,
respectively. On the other hand, fluxes of POP, BSi, Chl a (Fig. 5b) and
TEPs (Fig. 6a) peaked in the sediment trap located in the core of the OMZ
(110 m). The increment of fluxes at 110 m coincided with the high abundance
of MnOx-like particles associated with TEPs (Fig. 6a). In addition, TEP size
distribution, determined by image analysis, indicated an increase in large
TEPs at 110 m (data not shown). In contrast, in LD, POC, PN (Fig. 5c) and CSP
(Fig. 6d) fluxes steadily decreased with depth by 28 %, 42 % and
56 % from 40 to 180 m. Similar to the fluxes measured in GB, the POP,
BSi (Fig. 5d) and TEPs (Fig. 6c) showed a smaller peak in the sediment trap
located at 110 m.
Vertical fluxes of particulate organic carbon (POC) and
particulate nitrogen (PN) as well as oxygen concentration in GB (a) and LD
(c). Vertical fluxes of particulate organic phosphorus (POP), biogenic
silica (BSi) and chlorophyll a (Chl a) in GB (b) and LD (d).
MnOx-like particles were drastically less abundant in sediment trap samples
from LD than in GB, and when present, they appeared as single particles, not
aggregated with TEPs or CSPs (Fig. 6c, d). At both stations, and similar to
the water column samples, MnOx-like particles were not observed in sediment
trap samples collected in fully oxygenated waters (40 and 60 m). The flux of
MnOx-like particles at 110 and 180 m was 2 orders of magnitude larger in
GB than in LD (Table 4). In GB, MnOx-like particles occurred as single
particles as well as aggregates with each other and OM such as TEPs and CSPs
(Fig. 6a, b, and e), phytoplankton cells, or detrital material. The ESD of
MnOx-like particles and aggregates collected in the traps ranged from 0.6 to
167 µm (median 2.8 µm) at 110 m and from 0.6 to 153 µm
(median 3.3 µm) at 180 m. In LD, only a few single MnOx-like particles
were observed at 110 m (Fig. 6c, d), and their size ranged from 0.6 to 16.5 mm
(median 1.8) (Table 4).
MnOx-like particle fluxes and size as equivalent spherical diameter
(ESD) determined by image analysis in GB and LD.
TEP and CSP fluxes in GB (a, b) and LD (c, d). In addition
to vertical fluxes, each profile is complemented with microscopic images
(200×) of material collected at each depth. In GB, star-shaped MnOx-like
particles are clearly visible as single particles and forming aggregates
with TEPs (a) and CSPs (b). MnOx-like particles were less abundant in LD (c, d). (f) A larger
magnification (400×) image of MnOx-like particles at
110 m showing more detail on the shape of particles and aggregates
formed with TEPs.
TAA flux ranged from 371±12 to 501±33µmol m-2 d-1 in GB and from 502±84 to 785±54µmol m-2 d-1 in LD (Fig. 7a). In GB, the flux
steadily decreased from the surface to depth, whereas in LD the TAA flux at 40 m
was lower than at 60 m and decreased with depth from 60 to 180 m (Fig. 7b).
The vertical profile of TCHO flux was similar at both stations, although the
magnitude of the flux was higher at LD. The TCHO flux varied between 303±8 and 428±14µmol m-2 d-1 in GB (Fig. 7a) and
between 503±19 and 584±8µmol m-2 d-1 in LD
(Fig. 7b). At both stations, TCHO fluxes increased from 40 to 110 m, where
the highest flux was measured, and then it decreased at 180 m.
Vertical fluxes of total hydrolyzable amino acids (TAAs) and total
carbohydrates (TCHOs) as well as oxygen concentration in (a) GB and (b) LD.
Chemical composition of sinking and suspended particles
Comparing molar elemental ratios of sinking (from sediment trap material)
and suspended (from water column) particles to the revisited Redfield ratio
for living plankton (106C:16N:15Si:P; Redfield et al., 1963; Brzezinski,
1985), our results showed that the POC : PN ratio of sinking particles was
slightly above this ratio at both stations. The POC : PN ratios of sinking
particles in GB and LD were not significantly different. In GB, however,
ratios increased with depth from 9.8 to 12.6, while in LD they varied between
11.1 and 15.4 without a clear trend with depth. The POC : POP ratio of sinking
particles was lower (p<0.05; Mann–Whitney U test) in GB (90.1–244)
than in LD (230–772) with the highest value observed at 40 m and the lowest
at 110 m. At both stations the POC : BSi ratios varied between 1.7 and 4.2, and
PN : BSi ratios varied between 0.2 and 0.4; the lowest values were observed at
110 m (Table 5).
Amino acids (AAa), carbohydrates (CHOs), elemental molar ratios and
amino-acid-based degradation index of sinking and suspended particles in GB
and in LD.
Contrastingly, in suspended particles, POC : PN ratios were higher in GB than
in LD (p<0.001). In GB, they varied between 8.4 and 12 without a
clear trend with depth, while in LD, they decreased with depth from 8.7 (at
1 m) to 6.2 (at 400 m), and a slightly higher value of 7.8 was observed at
430 m.
The POC : PN and POC : POP ratios were significantly higher (p<0.01) in
sinking than in suspended particles (Table 5). The POC : BSi and the PN : BSi
ratios were much lower in sinking than in suspended particles at both
stations (GB: p<0.05; LD: p<0.01). In sinking particles, the
POC : BSi ratio was below the Redfield ratio of 7, whereas it was 1 to 2 orders of magnitude higher in suspended particles (Table 5). The PN : POP
ratio was significantly lower in sinking (0.15–0.43) than in suspended
particles (9.7–44.5) at both stations (p<0.001). In sinking
particles, it was always below the Redfield ratio of 16, while in suspended
particles, it was in the range of the Redfield ratio in the upper 80 m in GB and
always above in LD.
At both stations, the contribution of AA to POC was more significant in
sinking than in suspended particles. Similarly, the carbon contained in TCHOs
made up a larger percentage in sinking than in suspended particles (Table 5).
The amino-acid-based degradation index (DI; Dauwe et al., 1999) varied from
0.1 to 1.14 in sinking OM and was higher than in suspended OM (-1.25 to
-0.42) at both stations. In sinking OM, the DI decreased with depth in GB,
whereas in LD, there was not a clear trend with depth (Table 5). The DI was
higher in GB than in LD in sinking as well as in suspended OM.
Discussion
In this study, we (1) characterized the biogeochemistry of the water column
and the sinking particles in GB and LD, during early summer 2015, and
(2) determined the vertical flux of sinking particles in two deep
basins of the Baltic Sea. Our results suggested that the intrusion of
oxygenated water to GB, as a consequence of the 2014–2015 MBI, caused changes
in the water chemistry that affected the chemical composition and degradation
stage of the sinking and suspended particles. Consequently, the composition
and magnitude of the sinking particle flux were different in GB and LD.
Physical and biogeochemical conditions in GB and LD
In general, physical and biogeochemical conditions (temperature, salinity,
O2 and inorganic nutrient concentrations) were similar in the
euphotic zone of both stations. Moreover, though there were slight
differences between the stations concerning phytoplankton abundance and
composition, as well as the concentration and chemical composition of POM, in the
surface water column, those were not significant. The concentration of
Chl a (Fig. 3) and the abundance of picoplankton and nanophytoplankton (Table 2)
were slightly higher (20 % and 10 %, respectively) in GB than in LD.
This agrees with estimates of integrated total primary production (PP), which
were 10 % higher in GB (380 mg C m-2 d-1) than in LD
(334 mg C m-2 d-1; Piontek et al., unpublished). At both
stations, the abundance of picophytoplankton (<2µm)
was an order of magnitude higher than nanoplankton (Table 2). These findings
coincided with what was described previously for early summer in the Baltic
Sea, indicating that during this period productivity is sustained
mostly by picophytoplankton and nanophytoplankton communities (Leppanen et al.,
1994) that coexisted with cyanobacteria and other phytoplankton species
(Kreus et al., 2015). Microscopic analysis, on the other hand, indicated that
phytoplankton (>5µm) abundance was 47 % higher
in LD than in GB. At both stations, filamentous cyanobacteria (>90 % Aphanizomenon sp.) were numerically the predominant
phytoplankton type (55 % and 74 % of the phytoplankton counts in GB
and LD, respectively); dinoflagellates (including mixotrophs) correspond to
20 %, and diatoms correspond to >1 % of the
phytoplankton abundance in the upper 40 m (Table 3). Diatoms were slightly
higher in LD than in GB, and this coincided with a small peak in BSi
concentration (1.5 µM, Fig. 3e) at 40 m in LD. Although at both
stations the diatom proportion from the total phytoplankton abundance was
negligible, they could make a difference in the composition of sinking
particles leaving the euphotic zone in LD due to the selective aggregation of
diatoms (Passow et al., 1991); however, at both stations sinking particles
showed a similar enrichment in BSi. The low abundance of diatoms relative to
cyanobacteria in the euphotic zone indicated that at both stations, the
spring bloom was terminated and cyanobacteria were starting to build up the
summer bloom that generally occurs in June–July (Kreus et al., 2015).
Aphanizomenon sp. and Nodularia spumigena are known to
form summer blooms, in which they accumulate at the sea surface of the thermally
stratified water column (Bianchi et al., 2000; Nausch et al., 2009; Wasmund,
1997).
The concentration of particulate elements (POC, PN, POP, BSi) was slightly
higher in the surface waters of GB compared to LD, while exopolymeric particles containing polysaccharide (TEPs)
and protein (CSPs) were in similar abundance
at both stations. TEPs and CSPs were more abundant in the euphotic zone, which
supports the idea of a phytoplankton origin; however, the concentration of
TEPs in this study was 69 % (in GB) and 76 % (in LD) lower than
previously reported for summer in the central Baltic Sea (Engel et al.,
2002). Likewise, our dissolved inorganic nitrogen concentrations were below
the detection limit in the surface, while phosphate concentrations were
higher (>0.3µM) than observed in the Engel et
al. (2002) study. Mari and Burd (1998) reported that TEP concentration peaked
during the spring bloom and in summer in the Kattegat. TEP production may be
enhanced by environmental conditions, such as nutrient limitation (Mari et
al., 2005; Passow, 2002), which are characteristic of late summer in the
Baltic Sea (Mari and Burd 1998). In the Baltic Sea, the spring bloom
(March–April) is usually followed by a period of reduced PP (Chl a∼2µg L-1) that precedes the cyanobacteria summer bloom
typically observed in June–July (Kreus et al., 2015). Surface
satellite-derived Chl a concentrations (MODIS) in GB constantly increase
from mid-May to mid-June 2015 (Le Moigne et al., 2017); our monthly Chl a
concentrations derived from VIIRS for June 2015 in the Baltic Sea (Fig. 1)
showed similar Chl a concentrations. Considering this trend in Chl a
concentration and the availability of phosphate in the water column, we could
assume that our samples were collected at the beginning of the summer bloom
(middle June). In general, ecosystem models from the Baltic Sea indicate that
the termination of the summer bloom depends upon phosphate availability
(Kreus et al., 2015). Thus, TEP concentrations likely had not reached the
higher value previously observed after the summer bloom when inorganic
nutrients were depleted. Although satellite-derived Chl a concentrations is
a valuable tool to evaluate the trend of PP, the magnitude of the
concentration of Chl a from remote sensing is difficult to estimate in the
Baltic Sea (Darecki and Stramski, 2004). The concentrations of Chl a in GB
and LD derived from direct measurements were much lower (∼1.5µg L-1), suggesting that our samples were collected
during a period of low phytoplankton biomass typically observed before the
summer bloom. In any case, the concentration of phosphate was not limiting
the system. Another possible explanation for the rather low concentrations of
TEPs could be their removal from the surface by aggregation and subsequent
sedimentation during the spring bloom due to the high abundance of cells and
detrital particles during this time (Engel et al., 2002) and the relatively
low grazing pressure that lead to higher export after the spring bloom
(Lignell et al., 1993).
Although the composition and amount of OM in the surface waters at the two
trap stations were similar, below the euphotic zone (40 m) the vertical
profile of nutrients and particulate matter concentrations were distinctly
different, likely due to the 2014–2015 MBI (Holtermann et al.,
2017) that reached the deep waters of GB. This inflow replaced the old
stagnant water masses with new water masses (Schmale et al., 2016),
changing the salinity in the deepest waters and the vertical distribution of
O2, limiting the oxygen-deficient layer from 74 to 140 m, and
ventilating the water column below 140 m. The combination of physical
effects (the displacement of water masses, turbulent mixing and lateral
transport) and the consequent development of redox conditions through 2015
may have impacted the distribution of MnOx-like particles and POM in GB. In
addition to changes in O2 concentration, the MBI altered the redox
conditions in GB by creating a secondary redoxcline at 140 m, where
concentrations of O2 and MnOx-like particles increased. One
consequence of those changes is the vertical extension of the layer in which
MnOx-containing aggregates could form (Schmale et al., 2016); a previous
study showed that MnOx might precipitate from the water column of GB
following an MBI event (Lenz et al., 2015). POC and PN concentrations peaked
at 110 m, and this higher concentration at 110 m was even more evident in POP
and TEPs, while CSP concentration peaked at 140 m (Fig. 3); this is the first
study that examines the potential role of CSPs in forming aggregates with
MnOx-containing particles. The highest concentration of MnOx-like particles
(Fig. 4a) in the water column was not observed at 110 m (the core of the
OMZ), but at 80 m (oxycline) and below 140 m in the newly oxygenated water
layers.
In contrast, LD maintained permanent suboxic (<5µM O2) waters below 74 m and H2S was
detectable below 180 m. Below 100 m the vertical profiles of POM and BSi
did not change with depth. The only exception was TEP and CSP concentration
that, similar to in GB, peaked at 110 m and MnOx-like particles showed a small
increment at 70 m (in the oxycline). This suggests that, similar to the
results of Glockzin et al. (2014), the MnOx-like particles abundant in the
oxycline may form sinking aggregates with TEPs and CSPs; then, when those
aggregates sunk to anoxic waters (below 74 m), the MnOx-like particles may
have dissolved, releasing TEPs and CSPs to the water column where CSP concentration
decreased quickly, likely due to microbial degradation, but the concentration
of TEPs remained constant to the bottom of LD.
MBIs can have a significant impact on nutrient recycling. In GB the nitrate
concentration increased, possibly as a consequence of the oxidation of reduced
nitrogen compounds (e.g., ammonium, ammonia and organic nitrogen compounds
like urea) (Le Moigne et al., 2017) that accumulated during the stagnation
(anoxic) period prior to the MBI (Hannig et al., 2007). Scavenging of
phosphate onto Mn or Fe oxides has been shown in previous studies (Neretin et
al., 2003). Phosphate can bind to Fe hydroxides and MnOx and settle down
during oxic conditions, building up a phosphate pool in the sediments that
later, when the O2 decreases, may become a source of phosphate
(Gustafsson and Stigebrandt, 2007). Moreover, Myllykangas et al. (2017)
reported that the new water masses intruded during the 2014–2015 MBI displaced
the stagnant water masses in GB. Thus, the low concentrations of silicate and
phosphate that we measured in the deep waters of GB may also be a direct
consequence of the intrusion of oxygenated, low-nutrient waters associated
with the MBI. In contrast, in LD, the water column remained anoxic down to
the seafloor (430 m), and below the oxycline an increase in ammonium was
observed (Fig. 2b), which could be an indicator for the anaerobic respiration of
OM, e.g., denitrification (Bonaglia et al., 2016; Hietanen et al., 2012).
In summary, though GB and LD had similar surface conditions in terms of
phytoplankton production and POM stocks, during this study, we found
differences in the vertical concentration of nutrients (Fig. 2) and POM
(Fig. 3) between GB, ventilated by the MBI, and LD, a station that remained
suboxic. Our results suggest that the MBI caused differences in the vertical
profile of O2 that modified the redox conditions of the water column
and enhanced the in situ formation of MnOx-like particles (Fig. 4). Alternatively,
the inflow may transport new MnOx-like particles to GB. Those abundant
MnOx-like particles may aggregate with POM in GB, influencing the vertical
distribution of POM in the water column.
Potential influence of O2 concentration and redox conditions on vertical flux of sinking particles in GB and LD
During this study, we also investigated the effect of different O2
concentrations and redox conditions on the fluxes of particles. Our
measurements of POC flux at 40 m, below the euphotic zone, were 11.7±0.82 mmol C m-2 d-1 in GB and 19.8±1.22 mmol C m-2 d-1 in LD. Extrapolating those measurements to
annual flux, we obtain 4.37±0.31 mol C m-2 yr-1 in GB and
7.44±0.46 mol C m-2 yr-1 in LD. Our results from GB are in
the same range as the estimation derived from a biogeochemical model; i.e.,
3.8–4.2 mol C m-2 yr-1 (Kreus et al., 2015; Sandberg et al.,
2000; Stigebrandt, 1991) for the Baltic Sea. However, our results from LD are
higher than the annual POC fluxes predicted by those models. The high POC
flux observed in this study is not surprising since it represented one (in
LD) and two (in GB) days in June when the POC vertical flux out of the
euphotic zone is relatively high in the Baltic Sea compared with late fall
and winter. The biogeochemical model by Markus
Kreus (personal communication, 2015) estimated that POC flux in June ranged
between 8 and 13 mmol m-2 d-1; this is in the same range as our observations.
One of the main advantages of our sediment traps is that we can study the
flux of sinking particles at various depths simultaneously (i.e., higher
vertical resolution). Therefore, we measured the POM flux in oxic waters
(40 m and 60 (55) m) at the core of the OMZ (110 m) and at 180 m in both
basins. Traps located at 180 m of depth collected particles in sulfidic waters
at LD and in recently oxygenated waters (affected by the MBI) in GB. The
vertical flux of POM and BSi was different at the two studied basins; for
example, POC flux was between 25 % and 40 % higher in the upper
110 m of the LD than in GB (even though the PP was 10 % higher in GB).
However, the POC fluxes at 180 m (deepest trap) were similar in both basins,
indicating a substantial decrease in the POC flux between 110 and 180 m at
the LD. The POC flux (and the PN flux, which showed a similar vertical
profile) did not decrease with depth in the GB. In contrast, in the LD there
was a reduction of 17 % and 16 % of the POC flux from 40 and 60 m
(in the oxycline) and from 110 to 180 m, respectively; the POC flux did not
change from 60 to 110 m when a large section of the water column was suboxic
(O2<5µM from 74 m to the bottom of the
station). From 110 to 180 m the water column was completely anoxic, and
H2S was detectable at 180 m. The high flux of POC at GB coincided
with the appearance of dark, star-shaped particles that we defined as
MnOx-like particles, particularly evident at GB (Fig. 6a, b, e), but also
present in LD. Based on their morphology, size and aggregation with OM, we
propose that those particles correspond to MnOx-containing particles enriched
in OM that have been previously described at GB (Neretin et al., 2003; Pohl
et al., 2004; Glockzin et al., 2014; Dellwig et al., 2010, 2018) and LD
(Glockzin et al., 2014; Dellwig et al., 2010). The higher flux of MnOx-like
particles in GB than in LD is probably due to the oxygenation and changes in
the deep water redox conditions that enhance the formation of MnOx-like
particles associated with OM. This suggests that the reduction of the POC
flux below 110 m in the LD may be related to the O2 depletion and
the absence of MnOx–OM aggregates in the anoxic zone.
The POP flux was similar in the oxic water column (up to 60 m) in both
basins; however, it was almost 2 and 3 times higher at 110 and 180 m,
respectively, in GB than in LD. A peak in the POP and BSi flux was observed
at 110 m in both basins, but the magnitude of the increment was much higher
in GB than in LD. In GB the POP flux increased 62 % from 60 to 110 m (OMZ)
and then decreased by 28 % from 110 to 180 m. Vertical fluxes of POP, BSi
and Chl a (Fig. 5) were enhanced at 110 m, which coincided with the high flux
of MnOx-like particles. This high flux of MnOx-like particles is maintained
at 180 m, while the POP, BSi and Chl a flux decreased at this depth. This
vertical distribution is likely due to the enhanced formation of
MnOx-like particles in the hypoxic layer (<40µM O2)
located between 74 and 140 m that may scavenge POP and aggregate with cells
or phytodetritus containing BSi and Chl a. Although the POP flux peaked at
110 m in LD as well, the increment was only 30 % from 60 m (suboxic) to
110 m (anoxic), and it decreased by 78 % from 110 to 180 m (sulfidic
waters); these variations with depth were also observed in the BSi flux. In
LD, the flux and size of MnOx-like particles were much smaller than in GB,
and they were more abundant at 110 m than at 180 m.
Similar to the vertical distribution of POM in the water column discussed in
Sect. 4.1, differences in POM and BSi fluxes between basins are likely
associated with the large inflow of oxygen-rich saltwater that displaced the
old stagnant water masses and changed the chemistry of the water column
(Myllykangas et al., 2017). Under euxinic conditions (e.i., scenario observed
in LD without the influence of the MBI), the maximum concentration of
particulate Mn is found in the oxycline (Glockzin et al., 2014). Below the
oxycline, and due to the presence of H2S, the particulate Mn
concentration decreased drastically. During this study, we observed a high
concentration of MnOx-like particles at 110 and 180 m (Table 5) in GB,
in agreement with the high flux of particulate Mn measured in sediment traps
located at 186 m in June 2015 (Dellwig et al., 2018). The oxygenation of the
deep water layers of GB by the MBI caused the absence of H2S
(Schmale et al., 2016) and provided redox conditions favorable for the
formation of MnOx, resulting in the high MnOx-like particle fluxes measured in
the sediment trap located in the core of the OMZ (110 m) and at 180 m
(oxygenated deep water). There were two possible sources of MnOx associated
with the 2014–2015 MBI in GB: the lateral transport of
low-density aggregates formed by MnOx and OM (Glockzin et al., 2014) and the in situ formation and deposition of MnOx
following the oxygenation of the water column (Dellwig et al., 2018). In
clear contrast to the oxygenated deep layers of GB, in LD, we measured
H2S below 180 m; this could explain why although those aggregates
were present in this station at 110 m, they may dissolve in sulfidic waters
and thus were not as abundant and did not form aggregates with TEPs (Fig. 6c).
The presence of MnOx-like particles in aggregates (Fig. 6a) may have
implications for the vertical flux of POC, PN and POP in a stratified system
with a pelagic redoxcline like the Baltic Sea. Under steady state, the upward
diffusion and oxidation rates of the dissolved Mn are balanced by the sinking
and dissolution rates of MnOx. During Mn oxidation, the MnOx could aggregate
with POM and trace metals. Then, in the sulfidic waters, slow-sinking MnOx
enriched in OM will be dissolved, liberating the OM and altering the vertical
distribution and the flux of all associated particle elements (Glockzin et
al., 2014). This has been previously observed in other anoxic basins; for
example, in the Cariaco Basin, total particulate phosphorus reached a
maximum flux in sediment traps close to the redoxcline (Benitez-Nelson et
al., 2004, 2007). Moreover, even in the anoxic zone, the abundant aggregate-associated bacteria (Grossart et al., 2006) could partially or entirely
degrade the organic compounds in particles using NO3- or
MnOx as an electron acceptor. This may explain why we observed a clear peak
in the vertical fluxes of POP, BSi, Chl a (Fig. 3a, b), TEPs (Fig. 6a) and
TCHOs (Fig. 7a) at 110 m, followed by a small decrease at 180 m in GB. In LD
a smaller increment in the vertical fluxes of POP, BSi (Fig. 3d), TEPs
(Fig. 6c) and TCHOs (Fig. 7b) was also observed. The vertical fluxes of those
compounds coincided with the abundance of MnOx-like particles; we assume that
the MnOx aggregated not only with TEPs as described before (Glockzin et al.
2014) and observed in this study (Fig. 6a), but also with aggregates
containing phytoplankton cells and phytodetritus that may enhance POP, BSi,
Chl a and TCHO export. On the other hand, nitrogen-rich components of POM
like PN (Fig. 3a), TAA (Fig. 7a) and CSPs (Fig. 6a) gradually decreased with
depth in GB, suggesting that those compounds were less scavenged by MnOx–OM-rich aggregates.
PP in GB was 10 % higher than in LD during our study (Piontek et al.,
unpublished data). However, the POC flux below the euphotic zone (at 40 m)
was 42 % higher in LD than in GB and comparable at both stations at
180 m. The fraction of PP exported as POC is termed export production (the
e ratio) (Buesseler et al., 1992), and it is calculated as the POC
flux below the euphotic zone divided by the PP. We calculated the e
ratio using 14C-based PP measurements (Piontek et al.,
unpublished data) and carbon flux at 40 m (shallowest sediment trap depth
considered at the base of the euphotic zone). The e ratio was
larger in LD (0.77) compared to GB (0.41); i.e., the percentage of the PP
exported as POC below the euphotic zone was 77 % in LD versus 41 % in
GB. This suggests that either a higher proportion of the PP was remineralized
in the euphotic zone of GB compared with LD, or particles were sinking faster
in LD than in GB, likely due to differences in composition. On the other
hand, the transfer efficiency of POC to the deeper water column (i.e., the
ratio of POC flux at 180 m over POC flux at 40 m) was higher in GB
(115 %) than in LD (69 %). The transfer efficiency of POM is largely
controlled by the remineralization rate and the sinking velocity of particles
(De La Rocha and Passow, 2007; McDonnell et al., 2015; Trull et al., 2008).
The higher POC transfer efficiency in GB than in LD can be attributable to
differences in the sinking velocities of the particles at those two stations.
Particulate MnOx may sink through the redoxcline in GB (Neretin et al.,
2003), acting as ballast material and a nucleus for MnOx–OM-rich aggregate
formation. Those aggregates could have sunk more quickly, limiting the time
spent in the water column and the degradation by particle-attached microbes.
Assuming that MnOx-like particles had a density between 1.5 and
2.0 g cm-3 (Glockzin et al., 2014), the largest particles measured at
GB (167 µm, Table 4) will have a sinking velocity based on Stokes'
law between 508 and 1014 m d-1. If we consider a mixed aggregate that
is 50 % TEPs (density 0.9 g cm-3) (Azetsu-Scott and Passow, 2004)
and 50 % MnOx (density 1.5 g cm-3), its density would be
1.2 g cm-3, and its theoretical sinking velocity will be
204 m d-1. This indicates that, theoretically, the largest mixed
aggregates composed of MnOx and TEPs observed in GB could reach 180 m (the
location of our deepest sediment trap) in less than 1 day. However, the
average measured sinking velocity of MnOx-containing particles in the
laboratory for particles between 2 and 20 µm was 0.76 m d-1,
which is significantly lower than the theoretical value (Glockzin et al.,
2014). Glockzin et al. (2014) suggested that the star shape and the content
of OM were responsible for the lower-than-predicted sinking velocity. There
is no information about the amount of OM relative to MnOx-containing
particles in those mixed aggregates or how the MnOx-to-OM ratio may affect
the density and sinking velocity of larger aggregates like the ones we
observed. Due to the shape and size of MnOx–OM aggregates observed in our
study (Fig. 6e), we could assume those are the same type of aggregates
described before by Glockzin et al. (2014). Although we did not measure the
sinking velocity of those aggregates, we did observe a higher abundance of
them associated with TEPs at 110 and 180 m in GB than in LD. Thus, the
formation of MnOx aggregates rich in OM could represent an additional
mechanism (see the Introduction) to explain why the efficiency of OM export
is different under anoxic than under oxic conditions in the Baltic Sea. The
oxygenation of anoxic deep water in GB caused by the 2014–2015 MBI may have
led to enhanced precipitation of manganese, iron and phosphorus particles
(Dellwig et al., 2010, 2018). For example, the formation of P-rich metal
oxide precipitates occurs in the anoxic waters of the Black Sea (Shaffer,
1986) and Cariaco Basin (Benitez-Nelson et al., 2004, 2007) where higher
concentrations of particulate inorganic and organic phosphorus have been
observed in sediment traps close to the redoxcline.
Alternatively, BSi could also act as ballast material incrementing the
sinking velocity of marine aggregates (Armstrong et al., 2002; Klaas and
Archer, 2002). Our results showed that sinking particles were strongly
enriched in BSi relatively to C and N and compared to suspended particles
that were depleted in BSi (Table 5). Diatoms are the major phytoplankton
group that produces BSi to build their cell walls (Martin-Jézéquel et al., 2000), and they are the
dominant phytoplankton species during the spring bloom. However, during our
study, diatoms represented less than 1 % of the phytoplankton abundance in
the water column, and even though there was a strong enrichment in BSi in
the sinking particles, this was similar in GB and LD (Table 5). Therefore,
neither the differences in export production nor in transfer efficiency
between GB and LD could be solely explained by the amount of diatoms
cells, phytodetritus or BSi in sinking particles at the two basins.
Differences in composition and lability of sinking and suspended organic matter in GB and LD
In the sections above we compared the biogeochemical conditions and the size
of the POM pool in the euphotic zone of GB and LD. We then looked at how the
sinking flux of OM was affected by the different O2 concentrations in
the water column. Now, we focus on the influence of O2 in the chemical
composition of sinking and suspended particles. Suspended or slow-sinking
particles that spend more time in the water column should theoretically
show a more substantial degree of degradation (Goutx et
al., 2007) relative to the Redfield molar ratio: 106 POC : 16 PN : 15 BSi : POP.
POM showed enrichment in POC relative to PN and POP, especially in sinking
particles from LD and suspended particles from GB. Our measured values of
POC : PN (∼10) and POC : POP (between 89 and 506) in suspended OM
coincide with the simulated ratio reported immediately after the culmination
of the spring bloom by Kreus et al. (2015). The same study had
suggested that POC : POP higher than the Redfield ratio might lead to an
enhancement of particle export (Kreus et al., 2015); however, no
direct observations had confirmed this hypothesis. Our measurements showed
that the relative higher POC : POP ratios in sinking OM from LD, compared with
GB, do not lead to a higher transfer efficiency at this station. Compared to
the suspended OM in LD, the POP content was lower in GB, possibly related to
scavenging of POP into MnOx aggregates (see Sect. 3.4).
In addition, at both stations, sinking particles were strongly enriched in
BSi (Table 5), probably due to the preferential sinking of diatoms and
remnant diatom-rich detritus from the spring bloom. Differently, suspended
particles had a relatively low content of BSi; this is not surprising
considering the small proportions of diatoms in the euphotic zone at the
time of our sampling. The concentration of BSi decreased below the detection
limit from 60 m in the GB and 70 m in the LD. This observation coincides
with previous studies reporting the selective incorporation of diatoms into
sinking aggregates in the Baltic Sea (Engel et al., 2002; Passow, 1991),
whereas non-diatom species, although they may be abundant in the suspended
phytoplankton, may not be present in sinking particles (Passow,
1991).
Another explanation for higher BSi content in sinking particles may be
the inclusion of lithogenic Si in our measurements; lithogenic Si may have
been present in the water column or transported by laterally adverted
material. A recent study suggests that contributions of non-biogenic sources
could be significant during alkaline extraction (Barão et
al., 2015). The even more substantial enrichment in BSi observed in sinking
particles from 110 m in both basins may result from adsorption and/or
coprecipitation of silica in sinking particles containing MnOx (Dellwig
et al., 2010; Hartmann, 1985) or from the formation of aggregates that are
enriched in MnOx as well as in phytodetritus of diatom origin.
The TAA-based degradation index, DI (Dauwe et al. 1999), covers a wide range
of alteration stages; the more negative the DI, the more degraded the
samples, and positive DI indicates fresh organic matter. In our study, the
sediment trap material had a DI between 0.10 and 1.14, while suspended OM
has a DI between -0.26 and -1.25 (Table 5). These values coincide with what
was reported earlier by Dauwe et al. (1999) and indicate
that, first, the sinking particles collected in the sediment traps were less
altered (they have a more positive DI) than the suspended OM collected in
the Niskin bottle. Second, sinking particles from GB were fresher than the
ones from LD, and the degradation stage increased with depth at both
stations. The higher contribution of AA and CHO to the POC pool in sinking
than in suspended OM and the AA-DI indicates that suspended OM was more
degraded than sinking OM. The highest degree of degradation in suspended OM
and sinking OM from LD may be the result of a long time that light-suspended
OM or slow-sinking particles spend exposed to degradation in fully
oxygenated surface waters than dense, fast-sinking particles collected in
sediment traps.
The higher abundance of aggregates, formed by a combination of MnOx-like
particles and OM, observed at 110 and 180 m in GB could act as bacteria hot
spots that, combined with a higher O2 concentration in GB, may increase
the microbial degradation on sinking particles collected in GB. However, the
AA-DI indicated that sinking OM was less altered and therefore more labile
than the sinking OM in LD. This implied that in addition to the higher
transfer efficiency of POC in GB (see discussion above), the OM reaching the
seafloor was fresher and less degraded. This supports the idea that mixed
aggregates composed of MnOx and OM may be larger and faster sinking than
previously described by Glockzin et al. (2014). This explanation
is mostly speculative and based on the observation of large mixed
aggregates in the 110 and 180 m traps (Fig. 6, Table 4). However, as
mentioned
in the previous section, further work on directly determining sinking
velocity is required to prove this hypothesis.
Conclusions
The fluxes and composition of sinking particles were different in two deep
basins in the Baltic Sea (GB and LD) during early summer 2015. The two
stations had similar surface characteristics and POM stock; however, at
depth, the vertical profile of the POM concentration, as well as the
vertical flux of sinking particles, was different, likely related to
differences in the O2 concentration. The 2014–2015 MBI supplied
oxygen-rich waters to GB, transporting solid material from shallower areas
and modifying the O2 vertical profile and the redox conditions in the
otherwise permanent suboxic deep waters. This event did not affect LD,
allowing for the comparison of POM fluxes and composition under two
different O2 concentrations with similar surface water conditions.
Export efficiency (e ratio) derived from in situ PP measurements and POC flux
derived
from sediment traps indicated higher export efficiency in LD than in GB.
However, the transfer efficiency (POC flux at 180 m over POC flux at 40 m)
suggested that under the anoxic conditions found in LD, a smaller portion of the
POC exported below the euphotic zone was transferred to 180 m than under the
oxygenated conditions present in GB. The MBIs also transport solid Mn from
shallower areas towards GB that may have contributed to the higher
abundance of MnOx–OM in GB. Our results suggest that a new possible
mechanism to explain the differences in OM fluxes under different
O2 concentrations could be the formation and prevalence of aggregates
composed of MnOx and organic matter in GB. Those aggregates were
significantly larger and more abundant in GB compared to LD where sulfidic
waters constrained their presence. Our results indicate that at GB not only
a higher proportion of the POM leaving the euphotic zone reached our deepest
sediment trap, but also that this POM was fresher and less degraded. We
propose that after an MBI in GB, aggregates containing MnOx-like
particles and organic matter could have reached the sediments relatively
fast and unaltered, scavenging not only phosphorus and TEPs, as described
previously, but also other compounds like BSi, POP and CSPs. The higher
fraction of sinking particles exported below the euphotic zone and reaching
180 m in GB suggests that at this station a significant fraction of the POM
could reach the sediments, 50 m below our deepest sediment trap, relatively
unaltered. The remineralization of the organic matter reaching the sediments
may contribute to the quick reestablishment of anoxic conditions in the
sediment–water interface in GB. The relevance of this process needs to be
further investigated in order to be included in O2 budget and long-term
predictions of the MBI impact on O2 and OM cycles.
Data availability
All data
will become available at 10.1594/PANGAEA.898738 upon publication.
Author contributions
CCN designed and performed the sediment trap work at sea, analyzed
samples, and wrote the paper. FACLM designed and performed the
sediment trap work at sea and contributed to the writing of the paper. AE
designed and participated in the scientific program at sea and discussed and
commented on the paper.
Competing interests
The authors declare that they have no conflict of
interest.
Acknowledgements
This research was supported by the DFG Collaborative Research Center 754
“Climate-Biogeochemistry Interactions in the Tropical Ocean” (to Anja Engel,
Carolina Cisternas-Novoa and Frédéric A. C. Le Moigne), by a Fellowship of the Excellence Cluster “The Future
Ocean” (CP1403 to Frédéric A. C. Le Moigne), and by a DAAD short-term grant (57130097 to
Carolina Cisternas-Novoa). We thank Jon Roa, Tania Klüver, Scarlett Sett, Angela
Stippkugel, Carola Wagner, Clarissa Karthäuser, Moritz Ehrlich, Sonja
Endres, Hannes Wagner, Ruth Flerus, Sven Sturm and Christian Begler for
support during trap preparation and deployments, as well as help with experiment or
analyzed samples. We thank Judith Piontek for her contribution to the design
of the scientific program at sea, Jaime Soto-Neira for valuable discussion
and help with figure preparation, Annegret Stuhr for useful discussion about
phytoplankton data, and Cindy Lee for helpful advice. We gratefully
acknowledge the reviewers, Monika Nausch and Tom Jilbert, and the associated
editor Marcel van der Meer for their time and effort in reviewing and
editing the paper, which significantly improved this
publication.
The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association.
Edited by: Marcel van der Meer
Reviewed by: Tom Jilbert and one anonymous referee
References
Andersen, J. H., Carstensen, J., Conley, D. J., Dromph, K.,
Fleming-Lehtinen, V., Gustafsson, B. G., Josefson, A. B., Norkko, A.,
Villnäs, A., and Murray, C.: Long-term temporal and spatial trends in
eutrophication status of the Baltic Sea, Biol. Rev., 92, 135–149,
2017.
Armstrong, R. A., Lee, C., Hedges, J. I., Honjo, S., and Wakeham, S. G.: A
new, mechanistic model for organic carbon fluxes in the ocean based on the
quantitative association of POC with ballast minerals, Deep-Sea Res. Pt. II, 49, 219–236, 2002.
Azetsu-Scott, K. and Passow, U.: Ascending marine particles: Significance of
transparent exopolymer particles (TEP) in the upper ocean, Limnol. Oceanogr., 49, 741–748, 2004.
Barão, L., Vandevenne, F., Clymans, W., Frings, P., Ragueneau, O., Meire,
P., Conley, D. J., and Struyf, E.: Alkaline-extractable silicon from land to
ocean: A challenge for biogenic silicon determination, Limnol.
Oceanogr.-Meth., 13, 329–344, 2015.
Benitez-Nelson, C. R., O'Neill, L., Kolowith, L. C., Pellechia, P., and
Thunel, R.: Phosphonates and particulate organic phosphorus cycling in an
anoxic marine basin, Limnol. Oceanogr., 49, 1593–1604, 2004.
Benitez-Nelson, C. R., O'Neill Madden, L. P., Styles, R. M., Thunell, R. C.,
and Astor, Y.: Inorganic and organic sinking particulate phosphorus fluxes
across the oxic/anoxic water column of Cariaco Basin, Venezuela, Mar. Chem., 105, 90–100, 2007.
Bianchi, T. S., Engelhaupt, E., Westman, P., Andrén, T., Rolff, C., and
Elmgren, R.: Cyanobacterial blooms in the Baltic Sea: Natural or
human-induced?, Limnol. Oceanogr., 45, 716–726, 2000.
Bonaglia, S., Klawonn, I., Brabandere, L. D., Deutsch, B., Thamdrup, B., and
Brüchert, V.: Denitrification and DNRA at the Baltic Sea oxic–anoxic
interface: Substrate spectrum and kinetics, Limnol. Oceanogr., 61,
1900–1915, 2016.
Boyd, P. W. and Trull, T. W.: Understanding the export of biogenic particles
in oceanic waters: Is there consensus?, Prog. Oceanogr., 72,
276–312, 2007.
Bradford, M. M.: A rapid and sensitive method for the quantitation of
microgram quantities of protein utilizing the principle of protein-dye
binding, Anal. Biochem., 72, 248–254, 1976.Brettar, I. and Rheinheimer, G.: Denitrification in the Central Baltic:
evidence for H2S-oxidation as motor of denitrification at the
oxic-anoxic interface, Mar. Ecol. Prog. Ser., 77, 157–169, 1991.
Brzezinski, M. A.: The Si-C-N Ratio of Marine Diatoms – Interspecific
Variability and the Effect of Some Environmental Variables, J. Phycol., 21,
347–357, 1985.Buesseler, K. O., Bacon, M. P., Kirk Cochran, J., and Livingston, H. D.:
Carbon and nitrogen export during the JGOFS North Atlantic Bloom experiment
estimated from 234Th:238U disequilibria, Deep-Sea
Res., 39, 1115–1137, 1992.
Carstensen, J., Andersen, J. H., Gustafsson, B. G., and Conley, D. J.:
Deoxygenation of the Baltic Sea during the last century, P. Natl. Acad. Sci.
USA, 111, 5628–5633, 2014a.
Carstensen, J., Conley, D. J., Bonsdorff, E., Gustafsson, B. G., Hietanen,
S., Janas, U., Jilbert, T., Maximov, A., Norkko, A., Norkko, J., Reed, D.
C., Slomp, C. P., Timmermann, K., and Voss, M.: Hypoxia in the Baltic Sea:
Biogeochemical Cycles, Benthic Fauna, and Management, AMBIO, 43, 26–36,
2014b.Cavan, E. L., Trimmer, M., Shelley, F., and Sanders, R.: Remineralization of
particulate organic carbon in an ocean oxygen minimum zone, Nat. Commun., 8,
14847, 10.1038/ncomms14847, 2017.
Cisternas-Novoa, C., Lee, C., and Engel, A.: A semi-quantitative
spectrophotometric, dye-binding assay for determination of Coomassie Blue
stainable particles, Limnol. Oceanogr.-Meth., 12, 604–616, 2014.
Cisternas-Novoa, C., Lee, C., and Engel, A.: Transparent exopolymer particles
(TEP) and Coomassie stainable particles (CSP): Differences between their
origin and vertical distributions in the ocean, Mar. Chem., 175, 56–71,
2015.
Conley, D. J., Björck, S., Bonsdorff, E., Carstensen, J., Destouni, G.,
Gustafsson, B. G., Hietanen, S., Kortekaas, M., Kuosa, H., Markus Meier, H.
E., Müller-Karulis, B., Nordberg, K., Norkko, A., Nürnberg, G.,
Pitkänen, H., Rabalais, N. N., Rosenberg, R., Savchuk, O. P., Slomp, C.
P., Voss, M., Wulff, F., and Zillén, L.: Hypoxia-Related Processes in
the Baltic Sea, Environ. Sci. Technol., 43, 3412–3420, 2009.
Conte, M. H., Ralph, N., and Ross, E. H.: Seasonal and interannual
variability in deep ocean particle fluxes at the Oceanic Flux Program
(OFP)/Bermuda Atlantic Time Series (BATS) site in the western Sargasso Sea
near Bermuda, Deep-Sea Res. Pt. II,
48, 1471–1505, 2001.
Darecki, M. and Stramski, D.: An evaluation of MODIS and SeaWiFS bio-optical
algorithms in the Baltic Sea, Remote Sens. Environ., 89, 326–350,
2004.
Dauwe, B., Middelburg, J. J., Herman, P. M. J., and Heip, C. H. R.: Linking
diagenetic alteration of amino acids and bulk organic matter reactivity,
Limnol. Oceanogr., 44, 1809–1814, 1999.
De La Rocha, C. L. and Passow, U.: Factors influencing the sinking of POC
and the efficiency of the biological carbon pump, Deep-Sea Res. Pt. II, 54, 639–658, 2007.
Dellwig, O., Leipe, T., März, C., Glockzin, M., Pollehne, F., Schnetger,
B., Yakushev, E. V., Böttcher, M. E., and Brumsack, H.-J.: A new
particulate Mn–Fe–P-shuttle at the redoxcline of anoxic basins, Geochim. Cosmochim. Ac., 74, 7100–7115, 2010.
Dellwig, O., Schnetger, B., Brumsack, H.-J., Grossart, H.-P., and Umlauf,
L.: Dissolved reactive manganese at pelagic redoxclines (part II):
Hydrodynamic conditions for accumulation, J. Marine Syst., 90,
31–41, 2012.
Dellwig, O., Schnetger, B., Meyer, D., Pollehne, F., Häusler, K., and
Arz, H. W.: Impact of the Major Baltic Inflow in 2014 on Manganese Cycling in
the Gotland Deep (Baltic Sea), Frontiers in Marine Science, 5, 248 pp., 2018.
Devol, A. H. and Hartnett, H. E.: Role of the oxygen-deficient zone in
transfer of organic carbon to the deep ocean, Limnol. Oceanogr.,
46, 1684–1690, 2001.
Dittmar, T., Cherrier, J., and Ludwichowski, K. U.: The analysis of amino
acids in seawater, in: Practical guidelines for the analysis of seawater,
edited by: Wurl, O., CRC Press, Boca Raton, 2009.
Dollhopf, M. E., Nealson, K. H., Simon, D. M., and Luther, G. W.: Kinetics
of Fe(III) and Mn(IV) reduction by the Black Sea strain of Shewanella
putrefaciens using in situ solid state voltammetric Au/Hg electrodes, Mar. Chem., 70, 171–180, 2000.
Dugdale, R. C. and Goering, J. J.: Uptake Of New And Regenerated Forms Of
Nitrogen In Primary Productivity, Limnol. Oceanogr., 12, 196–206,
1967.
Emeis, K. C., Struck, U., Leipe, T., Pollehne, F., Kunzendorf, H., and
Christiansen, C.: Changes in the C, N, P burial rates in some Baltic Sea
sediments over the last 150 years – relevance to P regeneration rates and
the phosphorus cycle, Mar. Geol., 167, 43–59, 2000.Engel, A.: The role of transparent exopolymer particles (TEP) in the
increase in apparent particle stickiness (α) during the decline of a
diatom bloom, J. Plankton Res., 22, 485–497, 2000.
Engel, A.: Determination of marine gel particles in Practical Guidelines for
the Analysis of Seawater, CRC Press Taylor & Francis Group, Boca Raton, FL,
2009.
Engel, A. and Händel, N.: A novel protocol for determining the
concentration and composition of sugars in particulate and in high molecular
weight dissolved organic matter (HMW-DOM) in seawater, Mar. Chem., 127,
180–191, 2011.
Engel, A. and Schartau, M.: Influence of transparent exopolymer particles
(TEP) on sinking velocity of Nitzschia closterium aggregates, Mar. Ecol.
Prog. Ser., 182, 69–76, 1999.
Engel, A., Meyerhöfer, M., and von Bröckel, K.: Chemical and
Biological Composition of Suspended Particles and Aggregates in the Baltic
Sea in Summer (1999), Estuar. Coast. Shelf S., 55, 729–741,
2002.Engel, A., Wagner, H., Le Moigne, F. A. C., and Wilson, S. T.: Particle
export fluxes to the oxygen minimum zone of the eastern tropical North
Atlantic, Biogeosciences, 14, 1825–1838,
10.5194/bg-14-1825-2017, 2017.Eppley, R. W. and Peterson, B. J.: Particulate organic matter flux and
planktonic new production in the deep ocean, Nature, 282, 677–680,
10.1038/282677a0, 1979.
Glockzin, M., Pollehne, F., and Dellwig, O.: Stationary sinking velocity of
authigenic manganese oxides at pelagic redoxclines, Mar. Chem., 160, 67–74,
2014.
Goutx, M., Wakeham, S. G., Lee, C., Duflos, M., Guigue, C., Liu, Z.,
Moriceau, B., Sempére, R., Tedetti, M., and Xue, J.: Composition and
degradation of marine particles with different settling velocities in the
northwestern Mediterranean Sea, Limnol. Oceanogr., 52, 1645–1664, 2007.
Grasshoff, K., Ehrhardt, M., and Kremling, K.: Methods of Seawater Analysis
3rd ed., in: Internationale Revue der gesamten Hydrobiologie und
Hydrographie, Wiley-VCH, Weinheim, Germany, 1999.
Grossart, H. P., Kiørboe, T., Tang, K. W., Allgaier, M., Yam, E. M., and
Ploug, H.: Interactions between marine snow and heterotrophic bacteria:
aggregate formation and microbial dynamics, Aquat. Microb. Ecol., 42, 19–26,
2006.Gustafsson, B. G. and Stigebrandt, A.: Dynamics of nutrients and
oxygen/hydrogen sulfide in the Baltic Sea deep water, J. Geophys.
Res.-Biogeo., 112, 10.1029/2006JG000304, 2007.
Hannig, M., Lavik, G., Kuypers, M. M. M., Woebken, D., Martens-Habbena, W.,
and Jürgens, K.: Shift from denitrification to anammox after inflow
events in the central Baltic Sea, Limnol. Oceanogr., 52, 1336–1345,
2007.
Hansen, H. P. and Koroleff, F.: Determination of nutrients, in: Methods of
Seawater Analysis, edited by: Grasshoff, K., Kremling, K., and Ehrhardt, M.,
Willey-VCH, Weinheim, Germany, 1999.
Hansen, H. P. and Koroleff, F.: Determination of nutrients, in: Methods of
Seawater Analysis, Wiley-VCH Verlag GmbH, Weinheim, Germany, 2007.
Hartmann, M.: Atlantis-II Deep geothermal brine system. Chemical processes
between hydrothermal brines and Red Sea deep water, Mar. Geol., 64,
157–177, 1985.
HELCOM: Guidelines for monitoring phytoplankton species composition,
abundance and biomass, in: Manual for Marine Monitoring in the COMBINE
Programme of HELCOM, Helsinki Commission, Helsinki, 2012.
Hietanen, S., Jäntti, H., Buizert, C., Jürgens, K., Labrenz, M.,
Voss, M., and Kuparinen, J.: Hypoxia and nitrogen processing in the Baltic
Sea water column, Limnol. Oceanogr., 57, 325–337, 2012.
Holtermann, P. L., Prien, R., Naumann, M., Mohrholz, V., and Umlauf, L.:
Deepwater dynamics and mixing processes during a major inflow event in the
central Baltic Sea, J. Geophys. Res.-Oceans, 122, 6648–6667,
2017.
Kalvelage, T., Lavik, G., Lam, P., Contreras, S., Arteaga, L., Löscher, C.
R., Oschlies, A., Paulmier, A., Stramma, L., and Kuypers, M. M. M.: Nitrogen
cycling driven by organic matter export in the South Pacific oxygen minimum
zone, Nat. Geosci., 6, 228, 2013.Keil, R. G., Neibauer, J. A., Biladeau, C., van der Elst, K., and Devol, A.
H.: A multiproxy approach to understanding the “enhanced” flux of organic
matter through the oxygen-deficient waters of the Arabian Sea,
Biogeosciences, 13, 2077–2092, 10.5194/bg-13-2077-2016, 2016.
Klaas, C. and Archer, D. E.: Association of sinking organic matter with
various types of mineral ballast in the deep sea: Implications for the rain
ratio, Global Biogeochem. Cy., 16, 63-61–63-14, 2002.
Knauer, G. A., Martin, J. H., and Bruland, K. W.: Fluxes of particulate
carbon, nitrogen, and phosphorus in the upper water column of the northeast
Pacific, Deep-Sea Res., 26,
97–108, 1979.
Kreus, M., Schartau, M., Engel, A., Nausch, M., and Voss, M.: Variations in
the elemental ratio of organic matter in the central Baltic Sea: Part
I – Linking primary production to remineralization, Cont. Shelf. Res., 100, 25–45, 2015.
Kullenberg, G. and Jacobsen, T. S.: The Baltic Sea: an outline of its
physical oceanography, Mar. Pollut. Bull., 12, 183–186, 1981.Le Moigne, F. A. C., Cisternas-Novoa, C., Piontek, J., Maßmig, M., and
Engel, A.: On the effect of low oxygen concentrations on bacterial
degradation of sinking particles, Sci. Rep., 7, 16722,
10.1038/s41598-017-16903-3, 2017.
Legendre, L. and Gosselin, M.: New production and export of organic matter
to the deep ocean: Consequences of some recent discoveries, Limnol. Oceanogr., 34, 1374–1380, 1989.
Leipe, T., Tauber, F., Vallius, H., Virtasalo, J., Uścinowicz, S.,
Kowalski, N., Hille, S., Lindgren, S., and Myllyvirta, T.: Particulate
organic carbon (POC) in surface sediments of the Baltic Sea, Geo-Mar. Lett., 31, 175–188, 2011.Lenz, C., Jilbert, T., Conley, D. J., Wolthers, M., and Slomp, C. P.: Are
recent changes in sediment manganese sequestration in the euxinic basins of
the Baltic Sea linked to the expansion of hypoxia?, Biogeosciences, 12,
4875–4894, 10.5194/bg-12-4875-2015, 2015.
Leppanen, J., Rantajarvi, E., Maunumaa, M., Larinmaa, M., and Pajala, J.:
Unattended algal monitoring system-a high resolution method for detection of
phytoplankton blooms in the Baltic Sea, Wiley-IEEE Press, Piscataway, New Jersey, USA, I/461–463, vol. 461,
13–16 September 1994.Lignell, R. R., Heiskanen, A.-S., Kuosa, H., Kuuppo-Leinikki, P., Pajuniemi,
R., and Uitto, A.: Fate of phytoplankton spring bloom: Sedimentation and
carbon flow in the planktonic food web in the northern Baltic, Mar. Ecol.
Prog. Ser., 94, 239–252, 10.3354/meps094239, 1993.
Lindroth, P. and Mopper, K.: High performance liquid chromatographic
determination of subpicomole amounts of amino acids by precolumn
fluorescence derivatization with o-phthaldialdehyde, Anal. Chem.,
51, 1667–1674, 1979.
Logan, B. E., Passow, U., Alldredge, A. L., Grossartt, H.-P., and Simont,
M.: Rapid formation and sedimentation of large aggregates is predictable
from coagulation rates (half-lives) of transparent exopolymer particles
(TEP), Deep-Sea Res. Pt. II, 42,
203–214, 1995.
Long, R. A. and Azam, F. Abundant protein-containing particles in the sea,
Aquat. Microb. Ecol., 10, 213–221, 1996.Mari, X. and Burd, A.: Seasonal size spectra of transparent exopolymeric
particles (TEP) in a coastal sea and comparison with those predicted using
coagulation theory, Mar. Ecol. Prog. Ser., 163, 63–76,
10.3354/meps163063, 1998.
Mari, X., Rassoulzadegan, F., Brussaard, C. P. D., and Wassmann, P.:
Dynamics of transparent exopolymeric particles (TEP) production by
Phaeocystis globosa under N- or P-limitation: a controlling factor of the
retention/export balance, Harmful Algae, 4, 895–914, 2005.
Martin-Jézéquel, V., Hildebrand, M., and Brzezinski, M. A.: Silicon
metabolism in diatoms: implications for growth, J. Phycol., 36,
821–840, 2000.
Matthäus, W. and Franck, H.: Characteristics of major Baltic inflows – a
statistical analysis, Cont. Shelf. Res., 12, 1375–1400, 1992.
Matthäus, W., Nehring, D., Feistel, R., Nausch, G., Mohrholz, V., and Lass,
H. U.: The Inflow of Highly Saline Water into the Baltic Sea, in: State and
Evolution of the Baltic Sea, 1952–2005, Wiley-Interscience, Hoboken, 2008.
McDonnell, A. M. P., Boyd, P. W., and Buesseler, K. O.: Effects of sinking
velocities and microbial respiration rates on the attenuation of particulate
carbon fluxes through the mesopelagic zone, Global. Biogeochem. Cy.,
29, 175–193, 2015.
Mohrholz, V., Naumann, M., Nausch, G., Krüger, S., and Gräwe, U.: Fresh
oxygen for the Baltic Sea –An exceptional saline inflow after a decade of
stagnation, J. Marine Syst., 148, 152–166, 2015.Myllykangas, J.-P., Jilbert, T., Jakobs, G., Rehder, G., Werner, J., and
Hietanen, S.: Effects of the 2014 major Baltic inflow on methane and nitrous
oxide dynamics in the water column of the central Baltic Sea, Earth Syst.
Dynam., 8, 817–826, 10.5194/esd-8-817-2017, 2017.
Nausch, M., Nausch, G., Lass, H. U., Mohrholz, V., Nagel, K., Siegel, H.,
and Wasmund, N.: Phosphorus input by upwelling in the eastern Gotland Basin
(Baltic Sea) in summer and its effects on filamentous cyanobacteria,
Estuar. Coast. Shelf S., 83, 434–442, 2009.
Neretin, L. N., Pohl, C., Jost, G., Leipe, T., and Pollehne, F.: Manganese
cycling in the Gotland Deep, Baltic Sea, Mar. Chem., 82, 125–143,
2003.
Passow, U.: Species-specific sedimentation and sinking velocities of
diatoms, Mar. Biol., 108, 449–455, 1991.Passow, U.: Production of transparent exopolymer particles (TEP) by phyto-
and bacterioplankton, Mar. Ecol. Prog. Ser., 236, 1–12,
doi:10.3354/meps236001, 2002.
Passow, U. and Alldredge, A. L.: A dye-binding assay for the
spectrophotometric measurement of transparent exopolymer particles (TEP),
Limnol. Oceanogr., 40, 1326–1335, 1995.Pohl, C., Löffler, A., and Hennings, U.: A sediment trap flux study for
trace metals under seasonal aspects in the stratified Baltic Sea (Gotland
Basin; 57∘19.20′ N; 20∘03.00′ E), Mar. Chem., 84,
143–160, 2004.
Prieto, L., Ruiz, J., Echevarría, F., García, C. M., Bartual, A.,
Gálvez, J. A., Corzo, A., and Macías, D.: Scales and processes in the
aggregation of diatom blooms: high time resolution and wide size range
records in a mesocosm study, Deep-Sea Res. Pt. I, 49, 1233–1253, 2002.
Redfield, A. C., Ketchum, B. H., and Richards, F. A.: The Influence of
Organisms on the Composition of the Sea Water, in: The Sea, edited by: Hill,
M. N., Interscience Publishers, New York, 1963.Richardson, L. L., Aguilar, C., and Nealson, K. H.: Manganese oxidation in
pH and O2 microenvironments produced by phytoplankton, Limnol. Oceanogr., 33, 352–363, 1988.
Sandberg, J., Elmgren, R., and Wulff, F.: Carbon flows in Baltic Sea food
webs – a re-evaluation using a mass balance approach, J. Marine Syst., 25, 249–260, 2000.
Schmale, O., Krause, S., Holtermann, P., Power Guerra, N. C., and Umlauf,
L.: Dense bottom gravity currents and their impact on pelagic methanotrophy
at oxic/anoxic transition zones, Geophys. Res. Lett., 43,
5225–5232, 2016.Shaffer, G.: Phosphate pumps and shuttles in the Black Sea, Nature, 321,
515–517, 10.1038/321515a0, 1986.
Sharp, J. H.: Improved analysis for “particulate” organic carbon and
nitrogen from seawater, Limnol. Oceanogr.,
19, 984–989, 1974.
Solorzano, L.: Determination of Ammonia in Natural Waters by the
Phenolhypochlorite Method, Limnol. Oceanogr., 14, 799–801, 1969.
Stigebrandt, A.: Computations of oxygen fluxes through the sea surface and
the net production of organic matter with application to the Baltic and
adjacent seas, Limnol. Oceanogr., 36, 444–454, 1991.
Strickland, J. D. and Parsons, T. R.: Determination of dissolved oxygen, in:
A Practical Handbook of Seawater Analysis, Fisheries Research Board of
Canada, Nanaimo, British Columbia, 1968.
Strickland, J. D. H., Parsons, T. R., and Strickland, J. D. H.: A practical
handbook of seawater analysis, Fisheries Research Board of Canada, Ottawa,
1972.
Struck, U., Pollehne, F., Bauerfeind, E., and v. Bodungen, B.: Sources of
nitrogen for the vertical particle flux in the Gotland Sea (Baltic Proper) –
results from sediment trap studies, J. Marine Syst., 45, 91–101, 2004.
Tamelander, T., Spilling, K., and Winder, M.: Organic matter export to the
seafloor in the Baltic Sea: Drivers of change and future projections, Ambio,
46, 842–851, 2017.
Thomas, H. and Schneider, B.: The seasonal cycle of carbon dioxide in Baltic
Sea surface waters, J. Marine Syst., 22, 53–67, 1999.
Trull, T. W., Bray, S. G., Buesseler, K. O., Lamborg, C. H., Manganini, S.,
Moy, C., and Valdes, J.: In situ measurement of mesopelagic particle sinking
rates and the control of carbon transfer to the ocean interior during the
Vertical Flux in the Global Ocean (VERTIGO) voyages in the North Pacific,
Deep-Sea Res. Pt. II, 55, 1684–1695,
2008.
Turner, J. T.: Zooplankton fecal pellets, marine snow, phytodetritus and the
ocean's biological pump, Prog. Oceanogr., 130, 205–248, 2015.van Hulten, M., Middag, R., Dutay, J.-C., de Baar, H., Roy-Barman, M.,
Gehlen, M., Tagliabue, A., and Sterl, A.: Manganese in the west Atlantic
Ocean in the context of the first global ocean circulation model of
manganese, Biogeosciences, 14, 1123–1152,
10.5194/bg-14-1123-2017, 2017.
Van Mooy, B. A. S., Keil, R. G., and Devol, A. H.: Impact of suboxia on
sinking particulate organic carbon: Enhanced carbon flux and preferential
degradation of amino acids via denitrification, Geochim. Cosmochim. Ac., 66,
457–465, 2002.
Wasmund, N.: Occurrence of cyanobacterial blooms in the baltic sea in
relation to environmental conditions, Int. Rev. Ges. Hydrobio., 82, 169–184,
1997.Wasmund, N. and Uhlig, S.: Phytoplankton trends in the Baltic Sea, ICES J.
Mar. Sci., 60, 177–186, 10.1016/S1054-3139(02)00280-1, 2003.
Wilhelm, W. L.: Die Bestimmung des im Wasser gelösten Sauerstoffes,
Ber. Dtsch. Chem. Ges., 21, 2843–2854, 1888.