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Marine Chemistry
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Nitrogen turnover during the spring outflows of the nitrate-richCuronian and Szczecin lagoons using dual nitrate isotopes
Frederike Korth a,⁎, Brian Fry b, Iris Liskow a, Maren Voss a
a Leibniz Institute for Baltic Sea Research Warnemünde, Seestr. 15, 18119 Rostock, Germanyb Australian Rivers Institute, Nathan Campus, Griffith University, 170 Kessels Road, QLD 4111, Australia
⁎ Corresponding author at: Leibniz Institute for BaltiSeestrasse 15, D-18119Rostock, Germany. Tel.:+49 381 51
Coastal zones that receive high nitrogen loads from rivers often suffer from intense eutrophication. This is the casein the Baltic Sea, where nutrient concentrations decrease rapidly offshore, but uptake and turnover processes in thehighly eutrophic near-shore areas are not well understood. The Oder and Nemunas Rivers, the second and thirdlargest nitrogen contributors (70 and 45 kt N y−1), drain into the Szczecin and Curonian lagoons, respectively,and thus into the coastal waters of the Baltic. In this study, nitrate turnover processes in the coastal zones of theBaltic Sea were determined in March 2009 by measuring nutrient concentrations, nitrate uptake rates, and dualisotopes in nitrate (δ15N-NO3
− and δ18O-NO3−) in the lagoon outflows. While mixing processes dominated in the
outflow of the Curonian lagoon, a phytoplankton spring bloom largely accounted for the nitrogen processes inthe outflow of the Szczecin lagoon. Here, nitrate assimilation in the surface waters was evidenced by a parallelenrichment of 15N and 18O. In the near-bottomwaters of the Szczecin lagoon, a deviation from the 1:1 relationshipbetween δ18O-NO3
− and δ15N-NO3−, typical of denitrification, suggested the coupling of nitrification and denitrifica-
tion, triggered by the presence of organic material from the spring bloom. The particulate material may be rapidlysequestered in the sandy sediments off the outflow and generate the isotope signal of nitrate. The highly enrichedδ15N-NO3
− and δ18O-NO3− values (up to 28‰) in the near-bottom layer implied that the impact of isotopic enrich-
Human activities, such as the use of artificial fertilizers in agricultureand the burning of fossil fuels, accompanied by population growth inmany regions of the world have more than doubled nitrogen inputsinto aquatic systems (Galloway et al., 2004; Gruber and Galloway,2008; Seitzinger et al., 2005; Vitousek et al., 1997). Every year, up to50 Tg of reactive nitrogen enters the world's coastal zones via rivers(Gruber and Galloway, 2008), resulting in the eutrophication of coastalwaters and an expansion of dead zones (Diaz and Rosenberg, 2008). Inthe coastal regions of the Baltic Sea, which are among the mosteutrophied in the world (Cloern, 2001), the annual river load is 641–1000 kt of total nitrogen (HELCOM, 2009). Eutrophication has led to anincrease in both the frequency of cyanobacterial blooms (Finni et al.,2001) and the size of hypoxic zones (Conley et al., 2009, 2011).
More than half of the total nitrogen input in the Baltic is delivered bythe Vistula, Oder, Nemunas, Daugava and Neva Rivers (HELCOM, 2009;Stalnacke et al., 1999). Based on isotopic as well as nutrient concentra-tion data, Voss et al. (2005) suggested that riverine nitrogen is seques-tered in the Baltic's coastal zones. These findings are supported by the
c Sea Research Warnemünde,97 256; fax:+49381 5197 440.e (F. Korth).
rights reserved.
anticlockwise circulation of its waters and thus the restricted transportof riverine material into the sea's central basins (Neumann et al., 2002;Radtke et al., 2012). By upscaling the denitrification rates in the BalticSea it was determined that 48–73% of external nitrogen inputs deliveredvia rivers, coastal point sources, and atmospheric deposition are removedvia sedimentary denitrification (Deutsch et al., 2010). The same rangewas reported for water column denitrification (Dalsgaard et al., 2013).These findings are in line with reports in which denitrification wasshown to be the most important benthic removal process for nitrogen,accounting for about one-third to one-half of total nitrogen losses fromthe ocean (Middelburg et al., 1996; Seitzinger et al., 2006). However,most denitrification rate estimates have been based onmuddy sediments,with high organic carbon contents, and not from permeable sandysediments. For the latter, only a few such estimates have been publishedthus far (Gao et al., 2012). Permeable sediments usually lack anoxichorizons at their surfaces; instead, water and particles are transportedthrough the sediment structure thus initiating high microbial turnover,such as nitrification (Ehrenhauss et al., 2004) and denitrification (Gao etal., 2012).
In a previous study, Voss et al. (2010) examined nitrogen turnover inthe Szczecin lagoon bymeans of stable isotopes and there by determinedthe importance of denitrification, nitrate assimilation, and nitrificationpathways (Voss et al., 2010). However, why the isotopic signature ofriver nitrate could not be identified further offshore and how the riverine
2 F. Korth et al. / Marine Chemistry 154 (2013) 1–11
load was processed in near-shore regions remained unclear. Stableisotope data have facilitated the identification of nitrogen processesin ocean waters (Granger et al., 2011; Sigman et al., 2005, 2009).The main goal of our study was to expand our understanding ofnitrogen cycling and to identify major processes in the coastalregions of the Baltic Sea. Therefore, we measured nitrate uptake,δ15N-NO3
−, and δ18O-NO3− both at stations close to the outflows of
the Curonian and Szczecin lagoons and further offshore, in surfacewaters and in the near-bottom layer, during the peak nitrateoutflow season of 2009.
2. Material and methods
2.1. Study areas
The Nemunas River drains an area of 97,860 km2 and flows throughthe Curonian lagoon, where it delivers 98% of its total freshwater runoff(mean discharge 22 km3 yr−1) before it enters the Baltic Sea (Fig. 1).The lagoon, which has an area of 1584 km2 and a mean depth of3.8 m, is located on the southeast rim of the Baltic Sea, borderingLithuania and the Kalingrad Oblast region of Russia. The watershedarea of the Nemunas River is 62 times larger than the lagoon itself and50% of that area is used for agriculture (personal communication,Christoph Humborg). The exchange of water between the lagoon andthe Baltic Sea is limited since the lagoon's only outlet is the KlaipedaStrait (Fig. 1). In the Curonian lagoon, freshwater plumes spread north-ward under the influence of the permanent northerly current. The adja-cent coast is dominated by sandy sediments (Bitinas et al., 2005).
The Szczecin lagoon lies along the southern coast of the Baltic Sea andhas a mean depth of 4 m (Fig. 1). Its dominant freshwater source is theOder River, with an average flow of 15.2 km3 yr−1. The river drains awatershed area of 118,840 km2, whereas the lagoon covers an area ofonly 687 km2. The 15.5 million people living within the Oder catchmentcomprise about 19% of the total population of the Baltic Sea basin and60% of the area is in agricultural use. The lagoon is connected to the BalticSea via three outlets, although 75% of the water outflow enters thePomeranian Bay through the Świna Strait (Lass et al., 2001). The prevail-ing wind direction over the Pomeranian Bay is westerly, with riverine
Fig. 1. Maps showing the Szczecin Lagoon (A) and Curonian Lagoon (B). The gray scale denindicates the prevailing current direction.
waters transported along its eastern coasts (Pastuszak et al., 2003). Thesediments of the Pomeranian Bay are mainly sandy and the averagedepth is 14 m.
In both the Nemunas and the Oder Rivers, the δ15N values for nitrateare typical for rivers draining catchments with mainly agricultural land,with higher δ15N values than in more pristine rivers (Deutsch et al.,2006; Voss et al., 2006). The Szczecin and Curonian lagoons are intenselyeutrophied water bodies (Aleksandrov, 2010; Andrulewicz, 1997). Theresidence time of their water masses is about 50 to 80 days, but poten-tially much shorter during peak outflow periods (Gasiunaite et al.,2008;Mohrholz et al., 1998). The relatively short residence times togeth-erwith the ongoing eutrophication result in the annual export of 50–88%of the total nitrogen load from the Oder River into the Baltic Sea(Grelowski et al., 2000; Sileika et al., 2006; Voss et al., 2010). In thespring, nitrate concentrations may be as high as 100 μmol l−1 in theSzczecin lagoon and 115 μmol l−1 in the Curonian lagoon (Pilkaitytéand Razinkovas, 2006; Voss et al., 2010). Consequently, both the Pomer-anian Bay and the Lithuanian coast are clearly impacted by riverinenitrate discharges, which are characterized by low salinity, high nitrateconcentrations, and high δ15N-NO3
− values (Pastuszak et al., 2003; Vosset al., 2006).
2.2. Sampling
Samples were collected aboard the RV Professor Albrecht Penck be-tween 23 February and 16 March 2009. Transects of six and 15–18stations were sampled three times in the plumes of the Curonian andSzczecin (Swina Strait) lagoons, respectively (Fig. 2). Each transectstarted close to the outflow of the lagoons and was directed towardsthe open Baltic Sea, where salinity is typically in the range of 7.5 to 8.Sampleswere taken both at 1 mdepth and close to the sediment surface(the frame of the CTD was roughly 0.5 m above the bottom) with aSeabird CTD rosette equipped with 10-l Niskin bottles and sensors fortemperature, pressure, conductivity, light, and oxygen. Additionally,samples were taken in the Curonian lagoon outflow at depths between4 and 7.5 m. Photosynthetically active radiation (PAR) measurementswere continuously recorded with the ship's sensory system set up onthe vessel's deck.
otes the water depth (right bar) and the boxes the investigation area. The dashed line
Fig. 2. In the Szczecin Lagoon outflow a grid of 15–18 stations and in the Curonian Lagoon outflow a grid of six stations were sampled three times. Surface salinities are shown forone grid of the Curonian lagoon and Szczecin lagoon outflows, respectively.
3F. Korth et al. / Marine Chemistry 154 (2013) 1–11
2.3. Analysis
Water samples collected for the determination of NO3−, NO2
−, andNH4
+ were filtered through Whatman GF/F filters and analyzed onboard according to the method of Grasshoff et al. (1983), with a preci-sion of ±0.02 μmol l−1. For chlorophyll a (Chl a) determinations,250–1000 ml of water was filtered through Whatman GF/F filters andstored at −20 °C. Chl a was extracted from the thawed filters using90% acetone. The absorbance of the extract wasmeasuredwith a Turnerfluorometer (10-AU-005) before and after sample acidification. Chl aconcentrations were calculated according to Jeffrey and Welschmeyer(1997).
NO3− uptake rates were measured using a 15N tracer assay. At seven
stations in the Curonian lagoon outflow and 12 stations in the Szczecinlagoon outflow, water samples (500 ml) were spiked with Na15NO3
(Sigma-Aldrich, 98 atom%). The final concentrations of the additionswere always close to 10% of the ambient NO3
− concentrations. Uptakerates were measured at depths of 1 m at both outflows, at 5 m in theCuronian lagoon outflow, and close to the sediment surface in theSzczecin lagoon outflow. The bottles were incubated for 4 h on deckand cooled with running surface water. Three bottles were exposed to75% light intensity, using a neutral-density screen, and two bottles wereincubated in total darkness. The incubationswere terminated byfiltrationonto precombusted Whatman GF/F filters (4 h at 450 °C). Particulateorganic matter (POM) concentrations were determined by filteringuntreated water (250–1000 ml) through precombusted Whatman GF/Ffilters (4 h at 450 °C). All filters were stored frozen at −20 °C. In thelaboratory, the filters were dried (60 °C, 24 h), packed into tin cups,and formed into pellets. The isotope content of the filters was measuredwith a Delta S (Thermo) isotopic ratio mass spectrometer connected toa CE1108 elemental analyzer via an open split interface (FinniganConflow II). The reference gases were ultra-high purity N2 and CO2
obtained from a gas cylinder and calibrated against standards from theInternational Atomic Energy Agency (IAEA N1, N2, N3, C3, C6 and, NBS22). Acetanilide and peptone (Merck) served as laboratory-internalelemental and isotope standards for daily calibrations. The precisionwas b±0.2‰. Nitrate uptake rates were calculated as described inDugdale and Goering (1967).
Dual isotope analysis of nitrate (δ15N-NO3− and δ18O-NO3
−) wascarried out using the denitrifier method (Casciotti et al., 2002; Sigmanet al., 2001), in which nitrate and nitrite are quantitatively converted toN2O by the bacterium Pseudomonas aureofaciens (ATTC 13985), whichlacks N2O reductase activity. The produced N2O was automaticallyextracted, purified in a Finnigan GasBench II, and analyzed in a Delta
Plus (Thermo) isotope ratio mass spectrometer. The concentration ofthe sample size was adjusted to a final N2O concentration of 20 nmol.Nitrite was always less than 2% of the nitrate concentration and wasnot removed. The N and O isotope measurements of roughly 30% of thesampleswere replicated in separate batch analyses. Additionally, all sam-ples were measured for δ15N-NO3
− with Pseudomonas chlororaphis. Theinternational standards IAEA-N3: δ15N 4.7‰ vs. atmospheric N2; δ18O25.6‰ vs. VSMOW (Vienna standard mean ocean water), and USGS 34:δ15N −1.8‰ vs. atmospheric N2; δ18O −27.9‰ vs. VSMOW (Böhlke etal., 2003), were includedwith each batch of samples and used for isotopevalue corrections. The precision was b0.3‰ for δ15N and b0.6‰ for δ18O.The culture blank consisted of a vial to which no sample was added. Iso-tope ratios are reported using the delta notation in units of per mil (‰).
2.4. Mixing calculations
To examine the behavior of nitrate along the salinity gradient, con-servative mixing lines were calculated using the formulas reported byFry (2002):
Cmix ¼ f � CR þ 1−fð Þ � CM ð1Þ
where C denotes the concentration, the subscripts R andM indicate riv-erine and marine end-members, “mix” is the actual sample, consistingof both sources, and f denotes the freshwater fraction. Isotopic valuesof mixed estuarine samples (δmix) are expressed as:
δmix ¼ f � CR � δR þ 1−fð Þ � CM � δM½ �=Cmix ð2Þ
where δ denotes the isotopic value of riverine (R) and marine (M)end-members. For the marine end-member, the nitrate concentrationand isotopic composition were taken from a Baltic Sea sample (55°06.7021 N, 13° 18.0529 E) collected at the end of February 2009(Table 1). The nitrate concentration and nitrate isotope composition ofthe samples with lowest salinities (b4.5 and b3 for the Curonian andSzczecin lagoon outflows, respectively) were used as riverine end-member values. However, these are not truly riverine as they also reflectthe influence of lagoon processes.
3. Results
At all stations off both outflows, the water temperature was around2 °C (data not shown), which is typical for February/March (Pastuszaket al., 2003). The temperature did not change with depth so that
Fig. 3. Mean oxygen concentrations and PAR (photosynthetically active radiation) vs.depth for the Szczecin and Curonian Lagoon outflows. Note that maximal water depthswere 10 m and 30 m in the outflows of the Szczecin and Curonian lagoons, respective-ly. Mean oxygen concentrations were calculated in 1 m steps from the CTD profiles forall stations. The gray box denotes the range of the boundary layer.
4 F. Korth et al. / Marine Chemistry 154 (2013) 1–11
temperature differences did not induce any stratification. However, asalinity gradient was present in the water column at all except theoutermost stations, where the salinities were uniformly high from sur-face to depth. Close to the mouth of the lagoon, a lower-salinity surfacelayer overlies water of higher density. For both lagoons, the transitionzone between freshwater and Baltic Sea water occurred at the outflow.Samples were taken from salinity gradients ranging from 2.1 to 7.5 andfrom 3.2 to 7.9 in the Curonian and Szczecin lagoon outflows, respective-ly (Fig. 2).
The water column was well oxygenated in both study areas (Fig. 3).The highest annual riverine runoff was 860 m3 s−1 in the Curonianlagoon and 662 m3 s−1 in the Szczecin lagoon (Fig. 4). Among theoutflow nutrients of the Curonian lagoon, the concentrations of particu-late organic carbon (POC), particulate organic nitrogen (PON), and Chl awere highest at the lowest salinities and decreased with increasingsalinity, following conservative mixing lines (Fig. 5). Near-conservativemixing patterns were determined for δ15N-PON and δ13C-POC.Concentrations of NO3
−, NO2−, PON and POC significantly decreased with
depth (p b 0.05), whereas the Chl a concentrations were low (0.3–14 mg m−3), with no or only slight indications of a spring bloom (Fig. 6).
Chl a concentrations were significantly higher in the Szczecin lagoonoutflow than off the Curonian lagoon, reaching 25.8 mg m−3 (Fig. 5).PON and POC concentrations were three to four times higher in theSzczecin lagoon outflow (9.2 ± 3 μmol l−1 and 64.3 ± 20.3 μmol l−1,respectively) and togetherwith Chl a and nutrient concentrations clearlydiffered from the conservative mixing lines (Fig. 5). NO3
−, NO2−, Chl a,
PON, and POC concentrations were not significantly different in surfacevs. deeper waters (p > 0.05) (Fig. 6).
3.1. Nitrate concentrations, nitrate uptake, and δ15N-NO3− and δ18O-NO3
−
values
Maximum nitrate concentrations in the two lagoon outflows werevery similar (71.4 and 74.9 μmol l−1 in the Curonian and Szczecin la-goon outflows, respectively) and declined with increasing salinity toaround 3 μmol l−1 (Fig. 7). To construct mixing lines, we used the river-ine end-members with the lowest salinities (Table 1) since river watercould not be sampled at the same time that the cruise took place. Weare aware of the fact that mixing lines are impacted by the choice ofend-members and that the choice of other riverine end-members maylead to a slope that is slightly different from one based on concentrationsat lowest salinities. However, we found that nitrate mixing in theCuronian lagoon outflow was mostly conservative, in contrast to thenon-conservative behavior, indicating additional nitrate sources, in theSzczecin lagoon outflow.
In the Szczecin lagoon outflow, δ15N-NO3 and δ18O-NO3 increasedwith increasing salinity and clearly differed from the conservativemixing line (Fig. 7). Surface δ15N-NO3
− and δ18O-NO3− ranged from 7‰
to 14.9‰ and from 1.9‰ to 14.4‰, respectively. Bottom-water valueswere higher than those of the surface water, ranging from 7.9‰ to27.6‰ for δ15N-NO3
− and from 2.6‰ to 27.1‰ for δ18O-NO3−. In the
Curonian lagoon, δ15N-NO3− and δ18O-NO3
− mainly followed the conser-vative mixing lines. Surface δ15N-NO3
− and δ18O-NO3− ranged from 6.3‰
to 9.4‰ and 2.0‰ to 3.3‰ and bottom δ15N-NO3− and δ18O-NO3
− from4.4‰ to 7‰ and 1.7‰ to 6‰, respectively. The δ15N-NO3
− values stronglycorrelatedwith those of δ18O-NO3
− in the Szczecin lagoon outflow, with
Table 1Definitions of the marine (Baltic Sea) and riverine (Nemunas and Oder) end-members. Forthe definitions of end-member values see the section “Mixing calculations” in “Materialsand methods.”.
End-member NO3− (μmol l−1) δ15N-NO3
− (‰) δ18O-NO3− (‰) Salinity
Baltic Sea 2 4.7 5.1 8Nemunas River 71 8.6 2.5 b4.5Oder River 67 7.6 2.9 b3
a slope of 1.2:1, whereas in the Curonian lagoon outflow the slope was−0.3:1 (Fig. 8).
Nitrate uptake rates were five times higher in the Szczecin lagoonoutflow (1.6–235.2 nmol l−1 h−1) than in the Curonian lagoon outflow(Fig. 7), where the highest uptake rate was 20.8 nmol l−1 h−1.
4. Discussion
Run-off and nitrogen loads from the Oder and Nemunas Rivers arehighest in spring, after the snow melt (Grelowski et al., 2000). This wasalso the case in 2009, when monthly discharges were highest duringthe spring sampling campaign (Fig. 4). Nitrate loads during the springwere about 6 ± 3 kt in the Oder River and about 4 ± 3 kt in theNemunas River (data taken from the Baltic Environmental Database,http://nest.su.se/models/bed.htm). Even though the two lagoons re-ceived similar amounts of nitrate inMarch and therewas little differencein their water temperature, Chl a concentrations were lower in theCuronian lagoon outflow than in the Pomeranian Bay, where a springbloom occurred whose timing and Chl a concentration were in accor-dance with previous blooms (Pastuszak et al., 2003). Off the Lithuaniancoast and in the Curonian lagoon, the spring bloom usually developslater, in April/May (Pilkaityté and Razinkovas, 2006). This difference inbloom timing is supported by the nitrate uptake rates determined inMarch 2009, which were on average six times higher in the Szczecinthan in the Curonian lagoon outflow. Nitrate uptake rates off the Polishcoast (1.6 to 235.2 nmol l−1 h−1) were in the same range as thosereported by Middelburg and Nieuwenhuize (2000) for six Europeantidal estuaries, where using the same 15N tracer techniques the authorsmeasured rates of 0.25 to 250 nmol N l−1 h−1.
4.1. Origin of particulate matter and nitrate
The influence of riverine water on the coastal areas was evidencedby the low δ13C-POC values, which indicated a strong terrestrialinfluence given that terrigenous matter is relatively depleted in 13C(δ13C >−25‰) compared to marine organic matter released fromphytoplankton (δ13C ~−20‰) (Fry and Sherr, 1984). The mean C:Nratios of 6.9 ± 0.7 and 8.5 ± 1.5 in the Szczecin and Curonian lagoonoutflows, respectively, were characteristic for phytoplankton C:N ratios(~7) (Hedges et al., 1986). The δ15N-PON values were comparable in
Fig. 4. Mean monthly run-off between 1980 and 2000, run-off for 2009, and NO2/3 loads from 1980 to 2000 for the Oder River (A) and Nemunas River (B).Source: Baltic Environmental Database, http://nest.su.se/models/bed.htm.
5F. Korth et al. / Marine Chemistry 154 (2013) 1–11
the two outflows and typical for coastal regions, whether of the BalticSea or elsewhere (Middelburg and Nieuwenhuize, 1998; Voss andStruck, 1997; Voss et al., 2005), that are impacted by anthropogenicnitrogen.
The highnitrate δ15N valueswere consistentwith the type of land usein the catchments since agricultural land is known to generate nitrateisotope signatures far above typical pristine values (Voss et al., 2006).In the lagoons, a substantial amount of this nitrate is eventually lostdue to long residence times and high denitrification activities (Voss etal., 2010). Thus, both lagoons are important sinks for nitrate (Andreaeet al., 1996; Žilius, 2011) they still export significant quantities to theBaltic Sea.
4.2. Surface water processes: nitrate assimilation and mixing
The surface δ15N-NO3− and δ18O-NO3
− values in both outflows agreedwell with other data sets from salinity gradients of estuaries (Table 2). Inthe San Francisco Bay, the nitrate isotope compositionwas dominated bya combination ofmixing fromdifferent sources andphytoplanktondraw-down during summer (Wankel et al., 2006). In the Monterey Bay(Wankel et al., 2007) and the German Bight (Dähnke et al., 2008), nitrateisotope valueswere shown to be influenced bymixing, NO3
− assimilationby phytoplankton, and nitrification. In the Curonian lagoon outflow,conservative mixing was inferred from N and O isotope data since bothfollowed the theoreticalmixing line. By contrast, the Szczecin lagoon out-flow was dominated by a well-developed phytoplankton bloom. Besidesphytoplankton bacteria also assimilate nitrate; together, they strongly in-fluence theNandO isotope values of nitrate.Moreover, assimilationwassupported by the high nitrate uptake rates and the plot of δ18O-NO3
−
over δ15N-NO3−. In surface water samples, the typical slope is 1:1, in-
dicative of simultaneous enrichment with both 15N and 18O becausethe fractionation factor (ε) for N is equal to that of O during nitrateuptake by phytoplankton (Granger et al., 2004). Although the frac-tionation factor for δ15N–NO3
− uptake is highly variable and rangesfrom 15ε = 5‰ to 20‰ in cultured phytoplankton (Brandes andDevol, 1997; Granger et al., 2004; Granger et al., 2010), according tofield studies the mean fractionation in the upper ocean is close to 5‰(Altabet, 2001; Sigman et al., 1999; Wu et al., 1997). In our study, frac-tionation in the Szczecin lagoon outflow was 15ε =3.5‰ and 18ε =4.8‰ (Fig. 9), which is typical for mixed phytoplankton/bacteriacommunities (Dähnke et al., 2010; Voss et al., 2010).
4.3. Processes in the near-bottom layer
In the near-bottom waters, both δ15N-NO3− and δ18O-NO3
− wereclearly enriched (up to 28‰) compared to the surface waters. Vosset al. (2010) and Wankel et al. (2007) reported the enrichment ofδ18O-NO3
− (up to 33.9‰) whereas δ15N-NO3− values were lower
(15.5‰). Both groups hypothesized that atmospheric deposition,characterized by high δ18O-NO3
− (up to 80‰) and low δ15N-NO3−
values (Mayer et al., 2002), was responsible for their findings. How-ever, we can exclude atmospheric deposition as the source ofδ18O-NO3
− enrichment since salinity stratification did not allowfresh waters to be mixed at depth. Phytoplankton assimilation canalso be ruled out as the cause of isotope enrichment because phyto-plankton was light limited, as is typical in turbid estuarine waters(Heip et al., 1995). Indeed, in the Pomeranian Bay the PAR decreasedfrom maximal 2000 μE s−1 m−2 (daily mean values of 400–1000 μE s−1 m−2) above the water column to around 30 μE s−1 m−2
at a depth of 1 m and b2 μE s−1 m−2 at a depth of 7–10 m. This isbelow 1% of surface irradiance and excludes phototrophic processes.Thus, the only remaining processes able to substantially modify the iso-tope values of nitrate were nitrification and denitrification.
4.4. Denitrification
The fractionation factor for denitrification in the water column isbetween 22 and 30‰ (Brandes et al., 1998), generating a highlyenriched residual nitrate pool. In sediments, by contrast, denitrificationis assumed to be negligible (3–4‰) due to substrate limitation, asshown in benthic chamber experiments in the sediments of PugetSound, the Mexican margin, and Santa Monica Bay (Brandes and Devol,1997; Brandes andDevol, 2002; Lehmann et al., 2004). Although isotopicdata on porewater nitrates have shown large increases in δ15N-NO3
− andδ18O-NO3
− with decreasing nitrate concentrations, they have not beenshown to travel into the waters above the sediments (Alkhatib et al.,2012; Lehmann et al., 2007).
The enriched δ15N-NO3− and δ18O-NO3
− values in the near-bottomlayer of the Szczecin lagoon outflow imply an impact of denitrificationon isotope values. Denitrification occurs only at oxygen concentrationsbelow 5 μmol l−1 (Devol, 2008). Hunter et al. (2006) and Gao et al.(2010) suggested “oxic denitrification” in anaerobic microniches, but itcould not be proven in lab experiments (Evrard et al., 2012). Since thewater column, including the near-bottom layer was well oxygenated,with oxygen concentrations above 375 μmol l−1water columndenitrifi-cationwas unlikely to have caused the isotopic effect in the near-bottomlayer. Instead, we hypothesize a role formicrobial processes in the sandysediments in that they lead to an increase in the nitrate isotope valuesbefore nitrate-enriched pore waters are mixed back into the bottomwaters.
Sandy bottom sediments allow water and suspended particles to beadvected in the sediment pores. This form of transport in sandy sedi-ments may exceed molecular diffusion by several orders of magnitudeand potentially stimulates both chemical reactions and the activity ofthe biotawithin sediments (Huettel andGust, 1992). Some of the highestpotential denitrification rates (230 μmol N m−2 h−1) in marine
−, chlorophyll a, PON, PO15N, POC, and PO13C versus salinity for the Szczecin and Curonian Lagoon outflows and conservative mixing lines.The lowest and highest salinity values were defined as the end-members. For details on the calculations see the section “Mixing calculations” in “Materials and methods”.
6 F. Korth et al. / Marine Chemistry 154 (2013) 1–11
environments have been measured in the permeable sediments ofthe Wadden Sea (Gao et al., 2010). High denitrification rates of80 μmol m−2 day−1 in the Pomeranian Bay were inferred from astudy based on an ecosystem model (Neumann, 2007). Althoughthe importance of denitrification in the water column and in sedimentsis still speculative, based on our findings and those of the above citedstudies it seems to be the most likely process generating δ15N-NO3
−
and δ18O-NO3− enrichment in the near-bottom layer of the Pomeranian
Bay. We propose that isotopically enriched NO3− advects from the
sandy sediments into the overlying bottom water, such that the imprintof isotope fractionation during denitrification is found in the nitratebelow themixed layer. The impact of isotopic enrichment from sediment
processes on the water column seems to be higher in sandy than inmuddy sediments.
4.5. The potential role of nitrification in nitrate isotope signals
Isotope enrichment associated with denitrification was expected toproduce proportional enrichments of both δ15N-NO3
− and δ18O-NO3−
and thus a slope of 1 in a plot of δ18O vs. δ15N (Granger et al., 2004,2008; Prokopenko et al., 2011; Sigman et al., 2005). However, therelationship between δ15N-NO3
− and δ18O-NO3− in the Szczecin lagoon
outflow resulted in a slope of 1.2:1, indicating either the presence of anadditional source of 15N-depleted nitrate or the addition of 18O-enriched
PON (µmol l-1)0 5 10 15 20 25
Dep
th (
m)
0
5
10
Chl.a (mg m-3)0 5 10 15 20 25
Dep
th (
m)
0
5
10
0 5 10 15 20 250
10
20
30
0 5 10 15 20 250
10
20
30
Szczecin lagoon outflow Curonian lagoon outflow
POC (µmol l-1)0 40 80 120 160
Dep
th (
m)
0
5
10
0 40 80 120 1600
10
20
30
NO2- (µmol l-1)
0.0 0.2 0.4 0.6 0.8
Dep
th (
m)
0
5
10
0.0 0.2 0.4 0.6 0.80
10
20
30
NO3- (µmol l-1)
0 20 40 60 80
Dep
th (
m)
0
5
10
0 20 40 60 800
10
20
30
Fig. 6. Vertical changes in NO3−, NO2
−, chlorophyll a, PON and POC concentrations in the Szczecin and Curonian Lagoon outflows.
7F. Korth et al. / Marine Chemistry 154 (2013) 1–11
nitrate. As discussed above, the atmospheric input of NOx can be exclud-ed. Sigmanet al. (2005) andDähnke et al. (2010) found similar deviationsfrom the 1:1 slope, with the latter study postulating nitrification as thecause. Remineralization of newly fixed nitrogenmay also produce devia-tions from the 1:1 ratio, as shown in the deepwaters of the easternNorthPacificmargin (Sigman et al., 2005). By contrast, the sediments of theGulfof Finland, Baltic Sea, are characterized by high nitrification potentials,even during coldmonths (Jäntti et al., 2011). Moreover, high nitrificationrates also occur in permeable coastal sands (Ehrenhauss et al., 2004). Inthe Szczecin lagoon outflow, nitrification is likely at observations whereparticulate matter accumulates close to the sediment surface, as wasthe case in 13 out of 54 stations in the outflow. At these stations,δ15N-NO3 vs. δ18O-NO3 resulted in a slope of 1.5:1 (Fig. S1, Supplementa-ry material), indicating an additional input of 15N-depleted nitrate. IfNO3
− reduction is coupled toNO2− reoxidation in the Szczecin lagoon out-
flow, then the δ18O of ambient NO3− could be raised relative to its δ15N
(Sigman et al., 2005). This would indicate the faster loss of 16O duringthe enzymatic reduction of nitrate, leading to 18O enrichment in theresidual product (Casciotti et al., 2002). The coupling of nitrification anddenitrification would then generate the isotope values determined in
the Szczecin lagoon outflow. Even though sandy sediments are alsofound in the Curonian lagoon outflow, neither nitrification nor denitrifi-cation was visible in the isotopic signature of nitrate. Here, couplednitrification/denitrification was not stimulated by the remineralizationof organicmaterial, since off the Lithuanian coast the spring bloomusual-ly develops later, in April/May (Pilkaityté and Razinkovas, 2006).
4.6. Consequences of coastal processes for the Baltic ecosystem
This study sheds light on the potential nitrogen cycling processes thattake place in coastal areas of the Baltic Sea. Our results suggest that river-ine nitrate is rapidly consumed during the spring bloom, sinks partlybelow the mixed layer, and is entrained in the coarse sediments, whereparticulate material is degraded, nitrified, and partly denitrified. Thecontribution of permeable sediments to biogeochemical cycling waslong considered to be negligible, but our results as well as those ofother recent studies suggest that advective flows may enhance thesupply of oxidants and fresh organicmatter, resulting in intensemicrobi-al metabolic activity (Cook et al., 2006; Jahnke et al., 2005; Janssen et al.,2005; Rao et al., 2007). Other indirect evidence for the importance of the
Fig. 7. Nitrate concentrations, nitrate uptake, and δ15N-NO3− and δ18O-NO3
− vs. salinity for the Szczecin and the Curonian Lagoon outflows. Lines denote conservative mixing lines.Note the differences in the scales. For definitions of the end-member values, see Table 1.
Fig. 8. Relationship between δ15N-NO3 and δ18O-NO3 for the Szczecin and Curonian Lagoon outflows. Based on the isotope values slopes of 1.2:1 and −0.3:1 were determined.The dotted line represents a 1:1 ratio.
8 F. Korth et al. / Marine Chemistry 154 (2013) 1–11
Table 2Summary of dual isotopes (δ15N-NO3
− and δ18O-NO3−) of nitrate and nitrate concentrations in estuaries as reported in the literature and determined in this study.
Region Season Depth Salinity NO3− (μmol l−1) δ15N-NO3
− (‰) δ18O-NO3− (‰) Reference
San Francisco Bay Summer Surface 0/31 13/122 7/14 −5/12 Wankel et al. (2006)Monterey Bay Throughout the year 0–200 m – 1/37 2.5/14.5 1.1/33.9 Wankel et al. (2007)Elbe/German Bight December–October Surface + bottom 0.5/27 0/260 8/6.2 −0.1/9.5 Dähnke et al. (2008)Świna Strait Throughout the year Surface 0 0/250 4.1/10.6 11.4/21.9 Voss et al. (2010)Curonian Lagoon outflow Spring Surface 2.1/7.3 7/71 6.3/9.4 2/3.3 This study
Bottom 5.1/7.5 4/8 4.4/7 1.7/6 This studySzczecin Lagoon outflow Spring Surface 3.2/7.7 8/75 7/14.9 1.9/14.4 This study
Bottom 4.5/7.9 4/58 7.9/27.6 2.6/27.1 This study
9F. Korth et al. / Marine Chemistry 154 (2013) 1–11
Baltic coastal strip comes from budget estimates. The nitrogen loads tothe Baltic Sea could not be directly linked to nutrient concentrations inthe central Baltic Sea (Radtke et al., 2012; Voss et al., 2005; Voss et al.,2011), where the concertinos have remained relatively constant sincethe 1970s (HELCOM, 1996).
Over 23% of the Baltic Sea area is covered by sandy sediments(calculated from a sediment map published in the BALANCE InterimReport No. 10, Al-Hamdani and Reker, 2007) and they are mainlylocated in the southern part of the Baltic, close to the coast, wheremore than half of the total nitrogen input (Stalnacke et al., 1999;HELCOM, 2009) is discharged. Consequently, we want to stressthe potential role of this region in nitrogen sequestration. Furtherstudies of microbial rate measurements are essential to confirmthe importance of these processes and to evaluate the amount of ni-trogen that is removed.
5. Summary and conclusions
The findings of this study are based on coupled N and O nitrateisotope measurements carried out during the peak outflow seasonat a set of stations located along salinity gradients in the Curonianand Szczecin lagoon outflows. Nitrate is efficiently assimilated in
Fig. 9. Linear regression plots for δ15N-NO3− (C) and δ18O-NO3
− (D) vs. ln (NO3−) for the Szcz
expressed as the fractionation factor ε, which is calculated with respect to the remaining sTherefore, the slope of the regression is equal to the fractionation factor (ε) (here of 15ε =
the surface waters during the spring bloom. Moreover, nitrogenseems to be transformed and lost in the bottom waters and sandysediments under the influence of the bloom. This coupling betweennitrification and sedimentary denitrification may explain the isoto-pic signal determined in the near-bottom layer off the lagoon out-flow. Our study supports the assumption that most nitrate isconsumed in the coastal strip of the Baltic Sea and stresses the im-portance of distinguishing surface and near-bottom processes instudies of nitrogen cycling.
Supplementary data to this article can be found online at http://dx.doi.org/10.1016/j.marchem.2013.04.012.
Acknowledgments
We thank the captain and crew of R/V Professor Albrecht Penck fortheir professional assistance at sea. We also thank Moritz Lehmannand Kirstin Dähnke for sharing their experience and providing theirhelp with the denitrifier method. We acknowledge funding fromthe BONUS + EraNet Project AMBER (Assessment and Modelling ofBaltic Ecosystem Response) by national funding agencies and theEU (BMBF Project 03F0485A) and the “Come back to research” schol-arship of the Leibniz Institute for Baltic Sea Research Warnemünde.
ecin Lagoon and Curonian Lagoon outflows. The strength of the isotopic fractionation isubstrate as the slope of the regression line of δsustrate vs. ln (substrate concentration).3.5‰ and 18ε = 4.8‰) and is only shown for the Szczecin Lagoon outflow.
10 F. Korth et al. / Marine Chemistry 154 (2013) 1–11
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