Introduction
The biological carbon pump, defined as the export of biologically fixed
carbon dioxide (CO2) from the surface to the deeper ocean mainly in the
form of sinking particles (Volk and Hoffert, 1985), influences atmospheric
CO2 concentration and affects ecosystem structure and elemental
distributions in the ocean. The total amount of carbon export as well as the
efficiency of the biological carbon pump, i.e., the ratio between export and
primary production, are highly dynamic (Buesseler and Boyd, 2009; Lam et
al., 2011). Changes in the efficiency of the biological carbon pump may have
been responsible for past atmospheric CO2 variability between
glacial–interglacial transition periods (Kohfeld and Ridgewell, 2009) and
play a key role for future climate predictions (Heinze et al., 2015).
Most of the POM being exported below the surface mixed layer
(< 200 m in general) is solubilized and remineralized within the
mesopelagic layer, i.e., between depths of 200 and 1000 m (Bishop et al.,
1978; Suess, 1980). The shallower the carbon remineralization depth, the more
likely CO2 is to exchange with the atmosphere and hence drive a shorter
carbon storage time in the ocean (Volk and Hoffert, 1985; Kwon et al., 2009).
The factors driving export flux attenuation in the mesopelagic therefore have a
large influence on CO2 sequestration in the ocean. The vertical profile
of sinking particulate organic carbon (POC) flux has often been described by
a normalized power function: Fz=F100(z/100)-b, where Fz is
the particle flux as a function of depth z, F100 is the flux at 100 m
depth and b is the flux attenuation coefficient (Martin et al., 1987;
hereafter M87). The authors of the M87 study derived an
“open ocean composite” for POC export fluxes from North Pacific data with a
F100=50.3 mg m-2 d-1 and b=0.86. However, strong
regional variations of both total export POC fluxes and b values are
observed (Martin et al., 1987; Buesseler et al., 2007a; Torres Valdes et al.,
2014; Marsay et al., 2015) with several factors proposed to control export
flux attenuation. Increased attenuation, i.e., higher b values, have been
related to increased temperature (Marsay et al., 2015), zooplankton feeding
activity (Lampitt et al., 1990), coprophagy, coprorhexy and coprochaly
(Belcher et al. 2016), microbial cycling (Giering et al., 2014) and lack of
ballast (Le Moigne et al., 2012). Decreased flux attenuation, i.e., lower
b values, and thus higher transfer efficiencies (Teff) have
been associated to high particle sinking velocity depending on plankton
community composition, especially the presence of larger phytoplankton cells
(Buesseler, 1998; Buesseler and Boyd, 2009), particle aggregates (Alldredge
and Gotschalk, 1989) and fecal pellets (Cavan et al., 2015). Organic
polymers, such as transparent exopolymer particles (TEP), increase the rate of
aggregate formation due to their high stickiness (Alldredge et al., 1993;
Engel, 2000; Passow, 2002; Chow et al., 2015) and supposedly play an
important role in particle export fluxes (Passow, 2002; Arrigo, 2007; Chow et
al., 2015). TEP are carbon-rich particles that form from dissolved
polysaccharides (Engel et al., 2004). When included in sinking POM
inventories, TEP may increase carbon relative to nitrogen export fluxes, a
mechanism that potentially counteracts rising CO2 concentration in the
atmosphere (Schneider et al., 2004; Arrigo, 2007; Engel et al., 2014).
However, TEP themselves are non-sinking due to a high water content and low
density (Azetzu-Scott and Passow, 2004), and little quantitative data are
available on TEP export by sinking particles so far (Passow et al., 2000;
Martin et al., 2011; Ebersbach et al., 2014). Thus, the role of TEP in carbon
export is still unresolved.
Map of (a) the study area and (b) depth distribution of
oxygen concentration (mol kg-1) in the eastern tropical North Atlantic (ETNA) during the RV Meteor 105 cruise, when two
surface-tethered drifting sediment traps (STDT) were deployed (c).
Depth distribution of oxygen concentration (mol kg-1) at stations
visited in the deployment area showed an oxygen minimum zone in the upper
mesopelagic (d).
![]()
Reduced POC flux attenuation has also been suggested for oxygen minimum zones
(OMZs) (Martin et al., 1987; Haake et al., 1992; Devol and Hartnett, 2001;
Van Mooy et al., 2002; Keil et al., 2016) as a consequence of reduced
zooplankton feeding and microbial degradation activities in suboxic
(< 5 µmol O2 kg-1) waters. So far, the vast
majority of mesopelagic downward POM flux measurements originate from well-oxygenated waters (> 100 µmol O2 kg-1). In
the M87 study, five sets of drifting sediment traps were deployed in
the oxygenated North Pacific and four sets were deployed in the eastern
tropical North Pacific (ETNP) OMZ. The flux attenuation coefficients (b)
for the oxygenated North Pacific averaged 0.90 ± 0.06, while lower b
values averaging to 0.66 ± 0.24 were measured in the ETNP OMZ. In
agreement, Devol and Hartnett (2001) and Van Mooy et al. (2002) observed low
particle attenuation in the OMZ of the ETNP off Mexico, yielding b
coefficients of 0.36 and 0.40 respectively. Keil et al. (2016) found b
values of 0.59–0.63 in the suboxic Arabian Sea. These studies thus indicate
that a greater proportion of the sinking POM escapes degradation while
sinking through suboxic waters. However, influence of oxygen on organic
matter degradation may vary between individual components. For instance,
degradation of hydrolyzable amino acid (PHAA) under suboxic conditions was found to
continue with the same rate as compared to oxic conditions (Van Mooy et al.,
2002; Pantoja et al., 2004), suggesting that anaerobic and micro-aerobic
bacteria preferentially utilize nitrogen-rich components.
So far, little is known on sinking POM flux attenuation in hypoxic waters
(< 60 µmol O2 kg-1), which are more widespread
(∼ 4 % of ocean volume) compared to suboxic waters
(< 0.05 % of ocean volume). Laboratory studies indicated that
particle aggregates sinking through hypoxic waters can become suboxic within
their interior due to oxygen diffusion limitation and evolve microbial
degradation processes typical for suboxic waters (Alldredge and Cohen, 1987;
Ploug et al., 1997; Stief et al., 2016). For example, at an ambient O2
concentration of 60 µmol kg-1, the O2 uptake by a 2 mm
(diameter) aggregate was diffusion-limited and a 0.5 mm wide anoxic core
occurred within its interior (Ploug and Bergkvist, 2015). Since OMZs are
expected to expand in the future as a consequence of global warming and
altered circulation patterns (Stramma et al., 2008), the role of oxygen in
controlling the biological pump efficiency needs to be better constrained for
predicting ocean–climate feedbacks. In order to assess what controls carbon
flux attenuation and depth-related changes in sinking particle composition in
hypoxic waters, we determined downward POM fluxes in the eastern tropical North Atlantic (ETNA) off the coast
of Mauritania, which exhibits an extensive hypoxic OMZ between 300 and
500 m. We used two parallel drifting, surface-tethered sediment trap devices
with particle interceptor traps (PITs) at seven to eight different depths between
60 and 600 m to estimate fluxes to and within the OMZ.
Methods
The study area
The study was conducted from 17 March to 16 April 2014 during a cruise of the
RV Meteor to the ETNA region off the coast of Mauritania (Fig. 1a). The study
area included hypoxic waters with minimum values of oxygen concentration of
40 µmol kg-1 as determined by CTD (Seabird) casts with two
calibrated oxygen sensors at midwater depths of 350–500 m (Fig. 1b)
(Visbeck, 2014).
Sediment trap operation and sample analysis
Free-drifting surface-tethered sediment trap devices were deployed for 196 h
during the first deployment and 281 h during the second deployment
(Fig. 1c). The first trap device was deployed on the 24 March 2014
(11:00 UTC) at 10.00∘ N 21.00∘ W with 12
PITs at each of eight depths: 60, 100, 150, 200,
300, 400, 500 and 600 m. The device was recovered on the 1 April 2014
(14:30 UTC) at 10.46∘ N, 21.39∘ W. The second device was
deployed on the 27 March 2014 (16:00 UTC) at 10.25∘ N,
21∘ W with 12 PITs at each of seven depths: 100, 150, 200, 300, 400,
500 and 600 m. The second trap device was recovered on the 8 April 2014
(09:00 UTC) at 10.63∘ N, 21.50∘ W. Both devices slowly
drifted northwest and were recovered approximately 37 nm away from their
deployment location (Fig. 1c). Within the drifting area, oxygen concentration
in the OMZ resembled the overall pattern of the Mauritanian upwelling with
fully hypoxic conditions between 300 and 500 m (Fig. 1d).
The design of the trap devices and the drifting array basically follows
Knauer et al. (1979), with 12 PITs mounted on a polyvinyl chloride (PVC) cross
frame. The PITs were acrylic tubes with an inside diameter of 7 cm, an
outside diameter of 7.6 cm and a height of 53 cm, leading to an aspect
ratio of 7.5. The aspect ratio and a baffle system consisting of smaller
acrylic tubes attached to the top end of each PIT help to reduce drag-induced
movement within the trap (Soutar et al., 1977). PVC crosses with PITs were
attached to a free-floating line, which was buoyed at the surface and
weighted
at the bottom. The surface buoys of the arrays carried GPS/Iridium devices
and flashlights.
Prior to each deployment, each PIT was filled with 1.5 L of filtered surface
seawater (0.2 µm pore size cartridge) collected from the ship's
underway seawater system, up to three-quarters of the PIT's height. A brine solution
was prepared by dissolving 50 g L-1 sodium chloride with filtered
surface seawater and subsequently filtered through a 0.2 µm
cartridge to remove excess particulates. Then 20 mL of formalin was added
per liter of the solution to achieve a brine solution with 2 % formalin. The
preservative solution was then slowly transferred into each PIT beneath the
1.5 L of filtered seawater using a peristaltic pump. PITs were covered with
lids immediately to minimize contamination before deployment.
Sample treatment after trap recovery followed recommendations given by
Buesseler et al. (2007b). After recovery, all PITs were capped to minimize
contamination. The density gradient was visually inspected and found intact
at the position of prior to deployment or at a maximum 2 cm above. Then,
seawater was pumped out of each PIT using a peristaltic pump down to 2–3 cm
above the density gradient. The remaining ∼ 0.6 L was subsequently
transferred to canisters, pooled from 11 tubes per depth. Added to each canister was 40 mL formalin. Samples from each depth were passed through a
500 µm nylon mesh. Swimmers were removed from the mesh with forceps
under a binocular microscope and the remaining particles, which stuck to the
mesh, were transferred back to the sample. Samples were subsequently split
into aliquots of the total sample. Therefore, the pooled sample was
transferred into a round 10 L canister and stirred at medium velocity with a
magnetic bar. Aliquots were transferred into 0.5 L Nalgene bottles with a
flexible tube using a peristaltic pump. Aliquots of samples were filtered
under low pressure (< 200 mbar) onto different filter types
(combusted GF/F 0.7 µm, polycarbonate 0.4 µm or
cellulose acetate 0.8 µm; see below) for different analyses and
stored frozen (-20 ∘C) until analyses.
Biogeochemical analyses
The following parameters were determined: total particulate mass (TPM),
POC, particulate nitrogen (PN), particulate
organic phosphorus (POP), biogenic silica (BSi), chlorophyll a (Chl a),
particulate PHAA and TEP.
TPM was analyzed in triplicate. The following aliquots were filtered in
triplicate onto pre-weighed 0.4 µm polycarbonate filters: 800 mL
(2 × 400 mL; 8 % of total sample) for the depths of 600 to
300 m of deployment no. 1, 400 mL (4 % of total sample) for the depths
of 200 and 150 m of deployment no. 1 and for all depths of deployment no. 2,
and
420 mL (4 % of total sample) for the depth of 100 and 60 m of
deployment no. 1. Filters were rinsed twice with Milli-Q water, dried at
60 ∘C for 4 h and stored until weight measurement on a Mettler
Toledo XP2U microbalance.
POC and PN aliquots were filtered in triplicate onto combusted (8 h at
500 ∘C) GF/F filters (Whatmann, 25 mm): 400 mL (4 % of total
sample) for the depths of 600 to 150 m of deployment no. 1, 420 mL (4 %
of total sample) for the depths of 100 and 60 m of deployment no. 1, and 100 mL
(1 % of total sample) for all depths of deployment no. 2. For the depths
of 150, 100 and 60 m of deployment no. 1, 400–420 mL (4 % of total
sample) was filtered onto two filters due to the high particle load at these
depths. Filters were exposed to fuming hydrochloric acid in a fuming box overnight to remove carbonate and subsequently dried (60 ∘C, 12 h). For
analysis, the filters were enclosed in tin cups and analyzed using an Euro EA
elemental analyzer calibrated with an acetanilide standard. For the depths of
150, 100 and 60 m of deployment no. 1 the sum of both filters was taken.
POP was determined in triplicate, except for 60 m depth of deployment no. 1,
which was only determined in duplicate. The following aliquots were filtered
onto combusted GF/F filters (Whatmann, 25 mm): 400 mL (4 % of total
sample) for the depths of 600 to 150 m of deployment no. 1, 420 mL (4 %
of total sample) for the depths of 100 and 60 m of deployment no. 1, and 100 mL
(1 % of total sample) for all depths of deployment no. 2. For the depths
of 200 to 60 m of deployment no. 1, the volume of 400 mL/420 mL (4 %
of total sample) was filtered onto two filters due to the high particle load
at these shallower depths. Organic phosphorus collected on the filters was
digested in the potassium peroxodisulfate-containing substance Oxisolv
(Merck) for 30 min in a pressure cooker and measured colorimetrically as
orthophosphate following the method of Hansen and Koroleff (1999).
PHAAs were determined in duplicate. The following aliquots were filtered onto
combusted GF/F filters (25 mm): 400 mL (4 % of total sample) for the
depths of 600 m to 150 m of deployment no. 1, 420 mL (4 % of total
sample) for the depths of 100 m and 60 m of deployment no. 1, and 100 mL
(1 % of total sample) for all depths of deployment no. 2. For the depths
of 150, 100 and 60 m of deployment no. 1, the volume of 400 mL/420 mL
(4 % of total sample) was filtered onto two filters due to the high
particle load at these shallower depths. PHAA analysis was performed
according to Lindroth and Mopper (1979) and Dittmar et al. (2009) with some
modifications. Duplicate samples were hydrolyzed for 20 h at 100 ∘C
with hydrochloric acid (30 %, Suprapur, Merck) and neutralized by acid
evaporation under vacuum in a microwave at 60 ∘C. Samples were
washed with water to remove remaining acid. Analysis was performed on a 1260
HPLC system (Agilent). Thirteen different amino acids were separated with a
C18 column (Phenomenex Kinetex, 2.6 µm, 150 × 4.6 mm)
after in-line derivatization with o-phthalaldehyde and mercaptoethanol. The
following standard amino acids were used: aspartic acid (AsX), glutamic acid
(GlX), histidine (His), serine (Ser), arginine (Arg), glycine (Gly),
threonine (Thr), alanine (Ala), tyrosine (Tyr), valine (Val), phenylalanine
(Phe), isoleucine (Ileu), leucine (Leu) and γ-amino butyric acid (GABA).
α-Amino butyric acid was used as an internal standard to account for
losses during handling. Solvent A was 5 % acetonitrile (LiChrosolv,
Merck, HPLC gradient grade) in sodium dihydrogen phosphate (Merck, Suprapur)
buffer (pH 7.0); solvent B was acetonitrile. A gradient was run from
100 % solvent A to 78 % solvent A in 50 min. The detection limit for
individual amino acids was 2 nmol monomer L-1. The precision was
< 5 %, estimated as the standard deviation of replicate
measurements divided by the mean. The degradation index (DI) was calculated
from the amino acid composition following Dauwe et al. (1999).
BSi was determined in triplicate. The following aliquots were filtered onto
cellulose acetate filters (0.8 µm): 400 mL (4 % of total
sample) for the depths of 600 m to 150 m of deployment no. 1, 420 mL
(4 % of total sample) for the depths of 100 m and 60 m of deployment
no. 1, and 200 mL (2 × 100 mL; 2 % of total sample) for all depths
of deployment no. 2. Filters were incubated with 25 mL NaOH (0.1 M) at
85 ∘C for 2 h 15 min in a shaking water bath. After cooling of the
samples, analysis was conducted according to the method for determination of
Si(OH)4 by Hansen and Koroleff (1999). Fluxes of biogenic opal were
calculated assuming a water content of ∼ 10 % and therefore the
chemical formula SiO2 × 0.4H2O with a density of
∼ 2.1 g cm-3 (Mortlock and Fröhlich 1989).
Chl a was determined in duplicate. The following aliquots were filtered
onto GF/F filters (25 mm): 400 mL (4 % of total sample) for the depths
of 600 to 150 m of deployment no. 1, 420 mL (4 % of total sample) for
the depths of 100 m and 60 m of deployment no. 1, and 100 mL (1 % of total
sample) for all depths of deployment no. 2. For the depths of 200 to 60 m of
deployment no. 1, the volume of 400 mL/420 mL (4 % of total sample) was
filtered onto two filters due to the high particle load at these shallower
depths. Samples were analyzed after extraction with 10 mL of acetone
(90 %) on a Turner fluorimeter after Welschmeyer (1994). Calibration of
the instrument was conducted with spinach extract standard (Sigma Aldrich).
TEP were determined in quadruplet by microscopy after Engel (2009). Between
3.5 and 10 mL (0.03–0.1 % of total sample) for the depths of deployment
no. 1 and no. 2 were filtered onto 0.4 µm Nuclepore membrane
filters (Whatmann) and stained with 1 mL Alcian Blue solution. Filters were
mounted onto Cytoclear© slides and stored at -20 ∘C
until microscopy analysis using a light microscope (Zeiss Axio Scope A.1)
connected to a camera (AxioCam MRc). Filters were screened at 200x
magnification. Thirty pictures were taken randomly from each filter in two
perpendicular cross sections (15 pictures each; resolution
1040 × 1040 pixel, 8-bit color depth). Image analysis software WCIF
ImageJ (version 1.44, public domain, developed at the US National Institutes
of Health, courtesy of Wayne Rasband, National Institute of Mental Health,
Bethesda, Maryland) was used to semiautomatically analyze particle numbers
and area.
The carbon content of TEP (TEP-C) was estimated after Mari (1999) using the
size-dependent relationship:
TEP-C=aΣi(niriD),
with ni being the number of TEP in the size class i and ri the
mean equivalent spherical radius of the size class. The constant a=0.25×10-6 (µg C) and the fractal dimension of aggregates D=2.55 were proposed by Mari (1999). TEP-C was only calculated for the size
fraction < 5 µm, including mainly free TEP, because larger
TEP included TEP covered aggregates with solid particles. Estimating carbon
content of these larger particles would overestimate TEP-C as the volume of
the other particles would be included.
Calculations and statistics
Fluxes of CaCO3 and lithogenic matter (lith) were calculated as
[CaCO3+lith]=[TPM]-[POM]-[Opal].
Total mineral ballast (ballasttotal) was calculated as
[ballasttotal]=[TPM]-[POM].
The percentage of ballasttotal (%ballasttotal)
was calculated as
[%ballasttotal]=([TPM]-[POM])/[TPM]×100.
The transfer efficiency (Teff) of particulate components was
calculated as the ratio of fluxes at 600 m to those at 100 m.
Calculated mean values include replicate measurements of both deployments.
Data fits and statistical tests were performed with the software packages
Microsoft Office Excel 2010, Sigma Plot 12.0 (Systat) and Ocean Data View 4
(ODV) (Schlitzer, 2015). Weighted-average gridding was used in ODV to display
data according to data coverage with automatic scale lengths. The overall
significance level was p<0.05.
Results and discussion
Fluxes of different compounds
Export fluxes of TPM and particulate organic elements determined during both
trap deployments showed good overall agreement and a decrease with depth,
fitting well to the power law function of M87 (Figs. 2a–d, 3a–d
and Table 1). Averaging fluxes from both deployments yielded a total mass
flux of 240 ± 34 mg m-2 d-1 at 100 m decreasing to
141 ± 8.8 mg m-2 d-1 in the core of the OMZ (400 m)
(Fig. 2a). Fluxes of POC, PN and POP at 100 m depth were 73 ± 8.8,
13 ± 1.4 and 0.67 ± 0.06 mg m-2 d-1, respectively,
and decreased to 26 ± 4.5, 3.0 ± 0.41 and
0.19 ± 0.04 mg m-2 d-1 at 400 m depth (Fig. 2b–d). The
contribution of POC flux to total mass flux (% OC) decreased from about
30 % at 60–150 m depth to 17–20 % at 400 m depth and showed only
a minor decrease below 400 m, to 14–16 % at 600 m depth. Similarly,
the percentage of PN flux to total mass flux (% N) showed the largest
decrease between 60 and 400 m, i.e., from 6.6 to 2.0–2.3 %, with less decline observed below, reaching 1.7–1.8 % at 600 m. The percentage of POP flux
to total mass flux (% P) decreased from 0.37 % at 60 m depth to
0.11–0.16 % at 400 m depth and remained constant below 400 m depth.
No previous data are available for POM export fluxes at our study site for
direct comparison. However, our trap data compare well to carbon export
fluxes estimated from particle size data (i.e., 10–300 mg
C m-2 d-1) reported for 100 m depth in the area off Cape Blanc
(Mauritania) by Iversen et al. (2010).
Fluxes of (a) total mass and (b) particulate organic carbon
(POC), (c) particulate nitrogen (PN) and (d) particulate
organic phosphorus (POP) during the deployment of two STDT in the
ETNA. Solid symbols are used for deployment no. 1 and open symbols for deployment no. 2.
![]()
Fluxes of (a) chlorophyll a (Chl a), (b) opal, (c)
TEP and (d) PHAA during the deployment of two STDT in
the ETNA. Solid symbols are used for deployment no. 1 and open symbols for deployment no. 2.
![]()
Fluxes of particulate components at 100m depth (F100) and in
the core of the OMZ at 400m (FOMZ), as well as the associated
attenuation coefficients (b values) and transfer efficiencies
(Teff, %) over the depth range of 100 to 600 m during two traps
deployments in the ETNA. All units are in mg m-2 d-1 except for
TEP fluxes, which is reported in total particle area
cm-2 m-2 d-1. Mean values and standard deviations (SD) were
calculated from analytical replicates.
Component
F100
FOMZ
b value
Teff ( %)
mean
SD
mean
SD
mean
SD
r2
(600/100 m)
Mass
I
249
48.9
141
6.8
-0.429
0.090
0.987
41
II
231
16.3
141
12.1
-0.355
0.033
0.998
52
POC
I
69.4
9.23
23.8
5.4
-0.795
0.031
0.989
23
II
76.3
8.43
28.1
3.0
-0.741
0.044
0.989
22
PN
I
11.9
1.29
2.76
0.46
-1.013
0.026
0.992
15
II
13.5
1.12
3.26
0.19
-1.00
0.020
0.990
16
POP
I
0.71
0.07
0.15
0.02
-1.081
0.074
0.992
18
II
0.64
0.03
0.22
0.02
-0.80
0.034
0.990
23
Opal
I
44.6
1.76
34.0
1.7
-0.0195
0.038
0.987
65
II
48.6
4.16
30.7
2.0
-0.345
0.052
0.987
44
Chl a
I
0.10
0.00
0.035
0.001
-0.820
0.024
0.990
21
II
0.12
0.01
0.053
0.005
-0.625
0.082
0.988
24
TEP
I
1650
548
1190
368
-0.498
0.014
0.548
33
II
2990
348
1644
95
-0.451
0.069
0.810
37
PHAA-C
I
3.21
–
3.71
0.47
-1.324
0.067
0.994
11
II
1.28
0.10
5.24
0.79
-0.978
0.096
0.991
14
Fluxes of phytoplankton biomass, as indicated from Chl a, were similar at
100 m during both deployments, with 104 ± 1.5 µg
Chl a m-2 d-1 during the first and
116 ± 6.2 µg m-2 d-1 during the second
deployment, but behaved differently below, with a stronger flux attenuation
above the OMZ during the first compared to the second deployment (Fig. 3a).
Fluxes within the OMZ core were
35 ± 0.1 µg m-2 d-1 (no. 1) and
53 ± 0.5 µg m-2 d-1 (no. 2) respectively.
Opal fluxes were also similar during both deployments, yielding an average of
47 ± 3.6 mg m-2 d-1 at 100 m, steadily decreasing to
32 ± 2.4 mg m-2 d-1 at 400 m depth (Fig. 3b). Similar to
Chl a, opal fluxes were slightly higher above the OMZ during the second
compared to the first deployment but quite similar or even lower below the
OMZ. This may indicate that the second trap device, which drifted more
northerly (Fig. 1c), exploited waters of a more recent diatom bloom compared
to the first deployment.
Fluxes of [CaCO3+ lith] were similar to opal fluxes during the first
deployment (F100= 52 mg m-2 d-1) but considerably lower
during the second (F100= 14.8 mg m-2 d-1) (data not
shown).
During this study, export fluxes of TEP were estimated from decrease over
depth of total particle area and showed the strongest depth attenuation
between 60 and 100 m during the first deployment (Fig. 3c). Like Chl a
fluxes, TEP export fluxes were slightly higher during the second compared to
the first deployment. At 100 m depth, average TEP flux was
2323 ± 859 cm2 m-2 d-1 and decreased to
1418 ± 342 cm2 m-2 d-1 at 400 m. Using a TEP size to
carbon conversion according to Mari (1999) yielded to an average TEP-C
(< 5 µm) flux of 1.73 ± 0.35 mg
C m-2 d-1 at 100 m depth, slightly decreasing to
1.64 ± 0.28 mg m-2 d-1 at 400 m and further to
0.90 ± 0.32 mg m-2 d-1 at 600 m. Although TEP supposedly
play an important role in particle export fluxes (Passow, 2002; Arrigo, 2007;
Chow et al., 2015), only a few previous estimates for TEP export fluxes based
on sediment traps have been given so far to which we can compare our data.
Martin et al. (2011) measured TEP export fluxes during a spring bloom in the
Iceland Basin (northeast Atlantic Ocean) using the PELAGRA neutrally buoyant
sediment traps and determined values in the range of 30–120 mg xanthan gum
equivalent m-2 d-1. Ebersbach et al. (2014) obtained lower values
of 0.03–5.14 mg xanthan gum equivalent m-2 d-1 during the
LOHAFEX iron fertilization experiment in the Southern Ocean. Assuming a
conversion factor of 0.63 µg C µg-1 xanthan gum
after Engel (2004), these previous estimates suggest TEP-C export fluxes
ranging from 0.02 to 3 mg m-2 d-1 for the Southern Ocean and
from 19 to 75 mg m-2 d-1 for the North Atlantic spring bloom.
Our data on TEP export fluxes for ETNA region are within the range of these
previous studies but closer to the lower estimates for the Southern Ocean.
It has to be emphasized, though, that our calculated TEP-C fluxes are likely
underestimates, since only suspended, i.e., “free” TEP
< 5 µm, were taken into account. TEP-C associated to
aggregates cannot be determined with the applied microscopic technique.
Overall, TEP-C export fluxes in the ETNA were significantly related to
Chl a fluxes, yielding [TEP-C, mg m-2 d-1] = 11.9
[Chl a; mg m-2 d-1] + 0.74 (r2=0.59, n=15,
p<0.01).
A strong decrease at shallow depth (60–100 m) was also observed for PHAA
fluxes during the first deployment (Fig. 3d). Average PHAA fluxes were
330 ± 51 µmol m-2 d-1 at 100 m and
90 ± 20 µmol m-2 d-1 in the OMZ core at 400 m.
These fluxes are equivalent to amino-acid-related fluxes of 16.8 ± 2.6
(100 m) and 4.48 ± 1.0 mg C m-2 d-1 (400 m),
respectively, which are typical values for PHAA-C fluxes in the ocean (Lee
and Cronin, 1984). PHAA fluxes decreased slightly within the OMZ, i.e., from
300 to 500 m.
Flux attenuation in the ETNA OMZ
Fluxes from both deployments were fitted to the exponential decrease model
(Martin et al., 1987) and attenuation coefficients (b values) were
estimated for all components (Table 1). Higher b values suggest stronger
attenuation and may hint to either reduced sinking velocities of particles or
faster degradation of more labile components. During this study, PHAAs were
the most rapidly attenuated components of sinking particles, followed by POP,
PN, POC, Chl a and TEP (Table 1). Attenuation of mineral fluxes was less
pronounced than for TPM.
Attenuation coefficient of POC export fluxes was 0.80 during the first and
0.74 during the second deployment. These values are in the intermediate range
of previously determined b values for POC attenuation in the mesopelagic,
shown to vary between 0.51 as determined in the North Pacific (K2) and 1.59
as determined for the North Atlantic subpolar gyre (NASG) (Buesseler et al., 2007a; Marsay et al., 2015).
Based on trap data from fully oxygenated water columns, Marsay et al. (2015)
recently suggested a linear relationship between POC flux attenuation and
median water temperature within the upper 500 m of the water column
according to b=0.062T+0.303. Applying this relationship to our study area,
with temperature decreasing from 26 ∘C at the surface to
9 ∘C at 500 m and a median temperature value of 12.01 ∘C,
would give a b value of 1.05. This estimated b value is higher than the
values observed in this study (0.74–0.80) and suggests that oxygen
deficiency may reduce attenuation of POC fluxes in the ETNA, resulting in
higher Teff of organic matter though the OMZs compared to well-oxygenated waters.
Differences in flux attenuation coefficients translate into different
Teff for individual components, with PHAA being the least and TEP
being the most efficiently exported organic component (Table 1). In
particular, values of Teff for TEP and therewith for TEP-C were
about 3 times higher than for PHAA-C and even higher than for
bulk POC, suggesting a preferential export of carbon included in TEP below
100 m. However, a steep decrease of TEP flux was observed between 60 and
100 m during the first deployment. TEP are produced by a variety of
organisms, i.e., different phytoplankton and bacterial species, and cannot be
considered as of homogenous composition. Several mechanisms may therefore be
responsible for a change in TEP transfer efficiency with depth: (1) change of
TEP degradability with depth; (2) differences in TEP composition over depth
related to association with particles of different settling speed; (3) new
production of TEP, abiotically or by bacteria, during solubilization and
degradation of sinking particles; (4) capture of suspended TEP by sinking
aggregates; or (5) reduced degradation rate of TEP at lower oxygen. In
support of the latter hypothesis, an attenuation of TEP fluxes within the OMZ
(300–500 m) was not detectable but did occur again below the OMZ.
Changes in POM composition during export
POM, assumed to be 2.2 × [POC] following Klaas and Archer (2002),
made the greatest contribution to TPM flux at 60 m but decreased below.
Conversely, [%ballasttotal] increased with depth, namely from
30 % w/w at 60 m to 68 % w/w at 600 m.
Biogenic opal (density: 2.1 g cm-3) in the ocean is produced mainly by
diatoms and radiolaria. During this study, opal made a rather constant
contribution to TPM fluxes with 20–25 % weight below 100 m. Hence, the
observed increase in the [%ballasttotal] with depth was due to
an increasing contribution of CaCO3 and lithogenic material.
[CaCO3+ lith] to TPM increased from 10 to 15 % above 150 m to
45 % at 600 m. As a consequence, the ballast ratio, defined as
[Opal]:[CaCO3+ lith], changed from a dominance of opal above the OMZ to
a dominance [CaCO3+ lith] within and below the OMZ (Fig. 4). Slight
differences were observed between the two deployments. Contribution of opal
and of [CaCO3+ lith] to TPM at 100 m was almost equal during the first
deployment with a share of 18 and 22 % respectively. During the second
deployment the contribution of opal to TPM at 100 m was 21 % but only
6 % for [CaCO3+ lith]. Thus, the higher contribution of opal to TPM
fluxes together with higher Chl a fluxes indicated that diatomaceous
material had a higher share of particles sinking out of the euphotic zone
down to the OMZ core during the second compared to the first deployment.
Changes in mineral ballast ratios of sinking particles with depth
during the two deployments in the ETNA. Black bars are used for deployment no. 1 and gray
bars for deployment no. 2.
![]()
Changes in organic matter composition of particles sinking through
the OMZ during the deployment of two STDT in the ETNA. Solid symbols are used for deployment no. 1 and open symbols for deployment no. 2.
![]()
Molar [POC] : [PN] ratios were close to the Redfield ratio at depths
shallower than 100 m, increased to a ratio of 10 at 400 m depth and
remained constant between 400 and 600 m depth (Fig. 5a). [PN] : [POP]
ratios were much above Redfield, with values varying between 30 and 45
throughout the water column (Fig. 5b). Also, [POC] : [POP] ratios were much
higher than Redfield ratios and showed an increasing trend down to
300–400 m depth, while decreasing below (Fig. 5c). These changes in
elemental ratios suggested a preferential remineralization of POP in the
upper 300 m, followed by PN and POC deeper down.
The percentage of total organic matter in TPM fluxes decreased from 67 %
at 100 m to 32 % at 600 m (Fig. 6d). As a consequence of higher
Teff of TEP relative to bulk POC, contribution of TEP-C to POC
increased significantly with depth during both deployments
(p<0.01; r2 = 0.59, n=15) and was 2 % at 100 m
and 6 % within and 5 % below the OMZ (Fig. 5e). Because TEP are neutrally buoyant, their export to depth depends on their incorporation into
settling aggregates. In a laboratory study, Engel et al. (2009) observed that
decomposition of TEP was faster relative to bulk POC for aggregates formed
from calcifying and non-calcifying Emiliania huxleyi cultures. In
that experiment, aggregate decomposition was investigated under oxic
conditions. Other studies also showed fast microbial degradation of TEP under
oxic conditions (Bar-Zeev and Rahav, 2015). One possible explanation for
increasing [TEP-C] : [POC] in the hypoxic OMZ of the ETNA region could be
that TEP are mostly included in sinking aggregates, whereas POC could be
included in various particle types, such as large cells, detritus or fecal
pellets. Ploug et al. (1997) estimated that carbon turnover time inside
anoxic aggregates can be strongly reduced. Due to high microbial activity and
reduced water, exchange aggregates sinking into hypoxic waters are more likely
to experience anoxic conditions than individual particles (Ploug and
Bergkvist, 2015). Thus, TEP settling into hypoxic waters by aggregates may be
exposed to anoxia, and therewith to reduced microbial degradation, in
consequence leading to a preferential TEP transfer through the OMZ. This may
also explain the decrease of [TEP-C] : [POC] ratios below the OMZ at 600 m
water depth, which was, however, only observed during the second deployment.
Since PN was more rapidly degraded than POC this also implied that the ratio
of [PN] : [TEP-C] became lower with depth.
Molar percentages of selected amino acids contained in PHAA during
the deployment of two STDT in the ETNA. Solid symbols are used for deployment no. 1 and open symbols for deployment no. 2.
![]()
Degradation index (DI) of organic matter in trap-collected sinking
particles based on amino acid composition and calculated according to Dauwe et
al. (1999). Black bars are used for deployment no. 1 and gray
bars for deployment no. 2.
![]()
Composition (%Mol) and degradation index (DI) of PHAA collected
at different depths during two trap deployments (1 and 2) in the ETNA
region.
Depth(m)
AsX
GlX
Ser
Gly
Thr
Arg
Ala
GABA
Tyr
Val
Iso
Phe
Leu
DI
Deployment 1
60
13.89
14.69
8.36
12.94
7.57
5.89
12.26
0.21
0.02
6.13
5.12
4.05
8.86
0.34
100
13.48
14.23
8.46
14.12
7.56
5.68
12.55
0.22
0.00
6.21
5.01
3.85
8.62
0.23
150
13.80
13.90
9.10
14.27
7.20
6.12
11.57
0.27
0.04
6.19
5.07
3.97
8.49
0.29
200
14.58
14.63
8.35
15.16
7.75
5.56
11.75
0.26
0.14
5.62
4.51
3.82
7.88
0.07
300
14.06
13.01
8.72
16.45
7.99
5.55
11.74
0.44
0.79
5.54
4.33
3.77
7.59
0.03
400
14.08
12.90
8.75
16.48
7.59
5.69
11.81
0.37
0.30
5.94
4.62
3.80
7.66
0.02
500
13.62
12.55
9.16
17.02
7.95
5.75
11.23
0.42
0.38
5.87
4.61
3.88
7.55
0.02
600
13.55
12.29
8.96
17.57
7.63
5.63
11.40
0.46
1.09
5.88
4.47
3.71
7.36
0.07
Deployment 2
100
14.15
13.94
8.46
14.29
7.76
5.90
11.94
0.22
0.84
5.69
4.57
4.00
8.26
0.24
150
13.95
13.53
8.29
14.65
7.87
5.77
11.57
0.19
1.64
5.66
4.56
4.07
8.24
0.37
200
14.19
12.73
8.54
15.93
8.10
5.78
11.42
0.31
0.96
5.68
4.44
4.05
7.87
0.13
300
14.17
12.05
9.29
16.02
8.05
5.61
11.69
0.49
1.10
5.65
4.30
4.04
7.54
0.07
400
13.19
11.75
8.58
17.71
7.98
5.31
12.10
0.37
1.82
5.77
4.15
3.83
7.43
0.08
500
14.15
11.77
9.03
18.54
7.94
5.72
10.85
0.46
1.25
5.58
3.93
3.80
6.97
-0.09
600
14.06
11.89
9.55
18.70
7.18
6.01
11.02
0.55
1.29
5.19
3.86
3.65
7.05
-0.04
In contrast to [TEP-C] : [POC], values of [PHAA-C] : [POC] in POM fluxes
declined during both deployments above the OMZ. However, within the core of the
OMZ, at 400 m, [PHAA-C] : [POC] was higher than at 300 and 500 m
(Fig. 5f); the same pattern was also observed for [PHAA-N] : [PN] (data not
shown). A faster decline in PHAA in sinking particles mainly above but not
within the OMZ is different to observations gained for more extensively
oxygen-deficient to full anoxic waters of the eastern tropical South Pacific
(ETSP), which suggested that PHAAs are preferentially degraded under low-oxygen conditions (Van Mooy et al., 2002). In those studies, total
hydrolyzable amino acid (THAA) degradation under anoxic conditions was found
to continue with the same rate compared to oxic conditions, while degradation
of non-amino acid compounds was found to slow down (Pantoja et al., 2004; Van
Mooy et al., 2002). A preferential degradation of N-rich compounds
over POC suggests that microbes degrading organic matter under strongly
oxygen-deficient conditions via denitrification preferentially utilize
nitrogen-rich amino acids (Van Mooy et al., 2002). Our data on PHAA do not
suggest preferential amino acid loss due to components of sinking POM
degradation in the ETNA OMZ. This is in accordance with the absence of
microbial N-loss processes and absence of denitrifying bacteria in ETNA oxygen-deficient waters (Löscher et al., 2016). Instead, a slight increase of
[PHAA-C] : [POC] in the OMZ may point to higher protein production by
bacterial growth as previously observed for mesopelagic waters (Lee and
Cronin, 1982, 1984) and may be related to increased growth efficiency of
bacteria experiencing low-oxygen condition as suggested by Keil et
al. (2016).
Among all amino acids determined, GlX, Gly, GABA and Leu showed the most
pronounced variations with depth (Fig. 6a–d, Table 2). Whereas GlX and Leu
decreased with depth (Fig. 6a, c), Gly continuously increased. It has
been shown that Gly is enriched in the silica–protein complex of diatom
frustules (Hecky et al., 1973). Preservation of frustules relative to POM may
therefore explain the relative increase of Gly with depth in sinking
particles. GlX has been used as a biomarker (Abramson et al., 2010), since
GlX was shown to be enriched in calcareous plankton (Weiner and Erez, 1984).
During this study %Mol of GlX was higher during the first deployment,
which is in accordance with the observed higher contribution of
[CaCO3+ lith] to TPM flux. GABA has been used as an indicator for
bacterial decomposition activity (Lee and Cronin, 1982; Dauwe and Middelburg,
1998; Engel et al., 2009). During this study %Mol GABA behaved differently
during the first compared to the second deployment with similar values within
the OMZ, a pattern also observed for opal fluxes (Fig. 3b). Moreover, %Mol
of GABA showed a local peak at 300 m, i.e., within the upper oxycline, and
may point to high bacterial activity at this depth. Leu is an essential amino
acids and readily taken up by heterotrophic microorganisms. Little change in
%Leu in the OMZ core (Fig. 3d) compared to above (< 300 m)
indicated reduced microbial reworking of organic matter under hypoxic
conditions. Another indication of microbial reworking of organic matter can
be derived from the degradation index (Dauwe et al., 1999). During this
study, the DI decreased with increasing depth, but with differences between
the deployments (Fig. 7). During no. 2, DI was slightly higher above the OMZ,
indicating fresher material. During no. 1, the DI did not decrease within the OMZ,
but it continued to decrease from 300 to 500 m depth during
no. 2. Together with observations on Chl a and opal fluxes, as well as
changes in ballast ratio, data on DI suggest that the particles of more
diatomaceous origin likely continued to decompose under hypoxic conditions.