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Estuarine, Coastal and Shelf Science

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Capturing past eutrophication in coastal sediments – Towards water-qualitygoalsEmil Rydina,∗, Linda Kumbladba BalticSea2020, Box 50005, 104 05, Stockholm, Swedenb Stockholm University Baltic Sea Centre, Stockholm University, 106 91, Stockholm, Sweden

A R T I C L E I N F O

Keywords:Baltic seaSedimentPhosphorus (P)Aluminium (Al)Internal loadBrackish water

A B S T R A C T

Björnöfjärden is a semi-enclosed brackish bay located in the Stockholm archipelago (Baltic Sea, Sweden).Anthropogenic phosphorus (P) loading to the bay over the past century has overwhelmed the largely unchangednatural supply of elements and compounds that permanently sequester P in sediments. At the same time, eu-trophication has shifted surface sediments from oxic to anoxic conditions and reduced their P-retention capacity.Consequently, the release of P from anoxic sediments has become the main P source to the water column. Herewe report on a long-term remediation program to reverse eutrophication in Björnöfjärden. After the im-plementation of measures that reduced the land-based external load to the bay, sediment-P retention was in-creased by mixing a solution of aluminum (Al) chloride into the anoxic and azoic sediments (> 6m water depth)at a dose of 50 g Al/m2, a first in a brackish environment. As a result, P accumulation in the surface sedimentreached 2.0 g P/m2 after 3.4 years, corresponding to 1.6mg P/m2-day. This is the first time that the P accu-mulation rate has been determined in aquatic sediments following the addition of P-sequestering material, suchas Al. The P that accumulated was dissolved P that mainly migrated from below the layer of P accumulation. Theaim of the Al-addition was to sequester legacy P that had accumulated during the past century and to returnBjörnöfjärden to a low productivity regime, which would allow the surface sediment to become oxic and enablenatural P binding by iron.

1. Introduction

Coastal eutrophication is a global problem that results in elevatednutrient concentrations, decreased oxygen concentrations in sedimentsand hypolimnetic water, and altered coastal ecosystems such as de-creased water clarity and shifts in species composition (Diaz andRosenberg, 2008). During the twentieth century, phosphorus (P) inputsto the Baltic Sea increased several-fold (Gustafsson et al., 2012), which,in turn, increased primary production and sedimentation of organicmatter (Carstensen et al., 2014A). In contrast, the supply of potentiallyP-binding agents, such as iron (Fe), manganese (Mn), aluminum (Al),and calcium (Ca), likely remained constant because it is mainly de-termined by erosion and weathering in the catchment. The resultingaccumulation of P relative to binding elements has greatly enhanced Precycling from the sediments to the water column of the Baltic Sea(Gustafsson et al., 2012). Furthermore, the development of anoxicareas, both off-shore and in the coastal zone (Persson and Jonsson,2000; Conley et al., 2009), has reduced the capacity of sediments totemporarily bind P to iron oxyhydroxides (Conley et al., 2002) and as

poly-P stored in bacteria (Sulu-Gambari et al., 2016). Hence, the an-oxia-driven P recycling, the “vicious cycle” (Vahtera et al., 2007), re-flects a productive ecosystem; increased load of organic matter andelevated oxygen consumption. After an apparent regime shift in 1999(Österblom et al., 2007; Carstensen et al., 2014B), both the areal extentand volume of hypoxia and anoxia have risen to levels not previouslyrecorded before (Hansson and Andersson, 2016).

Despite a 50% reduction in external P inputs to the sea over the lastthree decades (Gustafsson et al., 2012), sediments have become lesseffective P sinks that have contributed to elevated P concentrations inthe coastal zone (Malmaeus et al., 2012; Bryhn et al., 2017). The ca-pacity of sediments in the Stockholm Archipelago to permanently retainP mobilized by mineralization of organic matter (Ahlgren et al., 2006)or reduction of iron oxyhydroxides (Blomqvist et al., 2004) is currentlylimited, as evidenced by the general pattern of sediment-P release. Thelimiting factor appears to be the availability of elements involved inearly authigenic P-mineral formation, such as Fe, Mn, Ca, and Al(Rasmussen, 2000; Mort et al., 2010; Jilbert and Slomp, 2013), whichare resistant to the anoxic environment during sediment diagenesis

https://doi.org/10.1016/j.ecss.2019.02.046Received 11 June 2018; Received in revised form 26 January 2019; Accepted 20 February 2019

∗ Corresponding author.E-mail address: emil.rydin@balticsea2020.org (E. Rydin).

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0272-7714/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).

Please cite this article as: Emil Rydin and Linda Kumblad, Estuarine, Coastal and Shelf Science, https://doi.org/10.1016/j.ecss.2019.02.046

upon permanent burial.In oligotrophic lakes, sediment-P burial is effective and net P release

to the water column virtually absent. As a result, sediment-P con-centration is higher in oligotrophic lakes compared to eutrophic lakes,where some share of the surface sediment-P is released, apparently dueto limitations in mineral-P formation (Carey and Rydin, 2011). Thus, inaquatic systems, the supply of elements and compounds involved inpermanent sediment-P binding is equally important as the external Psupply that is potentially available for primary production.

In eutrophic freshwater ecosystems, several approaches for in-creasing the capacity of anoxic sediments to retain P have been de-veloped, the dominant method being the application of dissolved Alsalts (Huser et al., 2016). The longevity of the retention effect dependson the Al dose and the concentration of sediment P available forbinding, because Al tends to bind P in a relatively constant ratio (Rydinet al., 2000), even in brackish water (Rydin, 2014). This constant ratioallows for the determination of the Al-dose needed to permanently in-activate the surplus (legacy) P accumulated in the sediment and toprevent its recycling to the water column. The addition of a bindingagent, such as Al, normally involved in sediment-P burial under anoxicconditions strengthens the natural P binding process.

Here we report the results of the first Al treatment in a coastal en-vironment, in the eutrophic, enclosed bay Björnöfjärden (Baltic Sea,Sweden). This measure, as well as measures to reduce external P loadsto the bay, were taken to improve water quality. We found that the Altreatment improved several aspects of water quality and ecologicalstatus (Rydin et al., 2017) by interrupting the main P flux from thesediment to the water column and improving P retention. Here wequantify the increased P retention in the sediment resulting from the Altreatment and estimate the potential for P retention under improvedoxygen conditions.

2. Material & methods

2.1. Study site

The semi-enclosed bay Björnöfjärden (surface area 1.5 km2) is lo-cated 34 km east of Stockholm in the Stockholm archipelago and con-sists of three sub-basin; northern, central, and southern (Fig. 1). It has atheoretical water renewal time of 3 months, a salinity of c. 5‰, anaverage depth of 7m, and a maximum depth of 24m (Table S1). It has ahistory of eutrophication, with water column TP concentrationsreaching 60 μg TP/L, largely due to internal P loading (Rydin et al.,2017). Its bathymetry and narrow topography make the bay prone tothermal stratification at c. 6 m depth. Below this, anoxic conditionsdevelop within a month after stratification has been established. Fullmixing usually occurs in late fall (op. cit).

2.2. Aluminum treatment

In all three sub-basins (northern, central, and southern), 50 g of Al/m2 to was injected into the top decimeter-layer of sediment below 6mwater depth, giving a treated area of 0.73 km2 (Table S1), as describedin Rydin et al. (2017). The dose was estimated by Rydin (2014) to besufficient to bind mobile P in the sediment and overlying water, as wellas P mobilized from sediment deposition for a few years after thetreatment. The northern basin was treated in August 2012. Inter-mediate benthic areas (6–12m water depth) of the central basin weretreated in September 2012. Benthic areas deeper than 12m were givena single dose of 15 g Al/m2 in September 2012 and were treated with anadditional 35 g Al/m2 in July 2013 for a total dose of 50 g Al/m2. Thesouthern basin was treated in July 2013.

2.3. Sediment sampling

Three sediment cores were collected from each Al-treated sub-basin,

once before (southern in December 2011, central and northern inMarch 2012) and twice after the Al treatment (in March 2014 and 2016;Fig. 1, Table S1) using a gravity corer (inner diameter 63mm). On theday of sampling, each core was sliced into 1 cm thick layers down to2 cm depth, and 2 cm thick layers from 2 cm depth down to 20 cmdepth. Samples were stored in airtight containers in the dark at 4 °C tominimize sediment oxidation and analysed within a week by the ErkenLaboratory, Uppsala University (Sweden).

2.4. Chemical analyses

Sediment water content was determined after freeze-drying to aconstant weight. Organic content was determined as loss on ignition(LOI) at 550 °C for 2 h. Sediment density was calculated from watercontent and LOI (Håkanson and Jansson, 1983). Total P (TP) content inthe sediments was analysed as phosphate (Murphy and Riley, 1962)after acid hydrolysis (Andersen, 1976). Different P forms were sepa-rated by sequential extraction after Psenner et al. (1988) as follows,with extraction chemicals in parentheses: NH4Cl-rP (1M NH4Cl at pH7), BD-rP (0.1M Na2S2O4/NaHCO3), NaOH-rP and NaOH-nrP (0.1MNaOH), HCl-rP (0.5M HCl). P in the extracts was denoted as reactive P(rP) (Murphy and Riley, 1962) and TP (Menzel and Corwin, 1965). Tocalculate NaOH-extractable non-reactive P (nrP), NaOH-rP was sub-tracted from NaOH-TP. These fractions are defined by the extractionmethod (Pettersson et al., 1988), but ideally each fraction roughlycorresponds to a specific P-containing substance in the sediment.Conventionally, NH4Cl-rP is regarded as loosely-bound P, BD-rP as Passociated with iron hydroxides, NaOH-rP as P bound to Al, NaOH-nrPas organic P, and HCl-rP as Ca-bound P. Residual P is calculated bysubtracting the extracted and identified P from sediment TP, and isconsidered to represent refractory organic P forms. Henceforth, the sixanalysed P fractions are denoted as loosely-sorbed P, Fe-P, Al-P, Org-P,Ca-P, and Res-P, respectively.

Fig. 1. A bathymetric chart of Björnöfjärden, Baltic Sea (Sweden), marked withsampling sites in the northern (N), central (C), and southern (S) sub-basins ofBjörnöfjärden.

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2.5. Calculations

Mobile P, i.e. P present in the upper sediment profile that was ex-pected to be released over time (Rydin et al., 2011), was calculated bysubtracting the average TP concentrations (representing the burialconcentrations) found in the deeper layers (16–20 cm) in each sedimentcore from the higher concentrations present in the layers above 16 cmsediment depth. The difference in concentrations in each sediment layerwas converted to an amount of mobile P, which was summed to re-present the amount of P (g P/m2) that could be mobilized and releasedover time.

Pretreatment Al-P and TP concentrations in each sediment layerwere subtracted from the corresponding sediment layer post-treatmentconcentration in 2014 and 2016 in order to account for the additional Pbound in the sediment as a result of the treatment. Accumulated P (g P/m2) was divided with the time (days) since treatment to calculate theaccumulation rate (mg P/m2-day).

2.6. Statistics

Outliers were identified with Grubbs' test (Grubbs, 1950) per vari-able and depth with a significance level of 0.001 (Table S4). Eachmeasured variable were analysed separately by ANOVA with `Depth’,`Basin’, and `Year’ as independent variables and including the interac-tion between `Depth’ and `Year’. In addition, measurements for eachvariable and depth were analysed separately by ANOVA with `Basin’and `Year’ as independent variables. Tukey's honest significant differ-ence (HSD) test was used to assess the significance of observed differ-ences between measurements from different years. All statistical eva-luation was performed using R version 3.5.0 (2018-04-23).

3. Results

A significant increase in TP concentration was detected in the se-diment surface layers after treatment (Fig. 2, Tables S3 and S5), with TPpeaking at 2–4 cm depth in 2014, and at 4–6 cm in 2016. In the twobasins treated in 2012, TP content increased by an average rate of1.6 mg P/m2-day. 3.4 years after treatment, 2.0 g P/m2 had accumu-lated. Extrapolating the amount of P trapped by the treatment to thewhole treated sediment area, about 1.3 tons were sequestered by March2016 (Table S2). Looking at the different P fractions over the in-vestigated period (Tables S3 and S5), we detected a small increase inloosely sorbed P in most sediment layers. In contrast, the concentrationof Fe-P showed some increase in the top 6 cm, but a general decreasebelow that depth. The Al-P concentration showed a pronounced in-crease in the 0–2 cm sediment layer two years after treatment. Between2 and 4 years after treatment, there was a decrease in concentration inthe 0–2 cm layer. Instead, after 4 year, the 4–6 cm sediment layershowed a pronounced increase (Fig. 2, Tables S3 and S5). The Org-Pconcentration showed no changes over time. The Ca-P fraction, how-ever, generally decreased over the 4 years that followed the treatment,which corresponded to an equivalent increase in Res-P.

The azoic sediment surface below 6m depth in Björnöfjärden wasgenerally covered by a white layer of few mm (colour apparently due toelemental sulfur in sulfate-reducing bacteria), and black below, re-flecting hypoxic conditions. The mobile P content in the sedimentconsisted mainly of organic P forms (Org-P and Res-P) and concentra-tions showed little change 3.4 years after the Al treatment (Table S3).The increased LOI in the 2–4 cm sediment layer (Fig. 2, Tables S3 andS5) after the Al treatment likely resulted from the injection of surfacewater (Schütz et al., 2017) and subsequent trapping of e.g. dissolvedhumic compounds into the sediment during the treatment.

4. Discussion

Prior to treatment with Al, P recycling between the sediment andthe overlaying water was the major P source to the Björnöfjärden watercolumn due to limited sequestration in anoxic sediments. After the Altreatment, we observed diminished concentrations of dissolved P in theanoxic bottom-water. The formation of Al-P, and the correspondingincrease of sediment TP in the sediment (Figs. 2 and 3), indicate an

Fig. 2. Total phosphorus (TP, μg P/g DW), phosphorus bound to Al (Al-P, μg P/g DW, redrawn from Rydin et al. (2017), water content (%) and loss on ignition(LOI, %) in the sediment of Björnöfjärden, Baltic Sea (Sweden) (all data, meanand S.E. of samples from three sub-basins).

Fig. 3. Phosphorus trapped in the sediment (g P/m2) by the added aluminum inthe three sub-basins in Björnöfjärden, over time (days after Al treatment).Increase in phosphorus measured as total phosphorus (TP) content (mean andS.D.).

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ongoing flux of dissolved P from the sediment surface, but also fromsediment layers below, to the Al-enriched layers where it was trapped.The increased depth of peak P concentrations from 2014 to 2016 in-dicates a yearly accumulation of about one cm of unconsolidated se-diment on top of the treated layer (Fig. 2), rather than a downwardmovement of the trapped P.

The injection of the Al-solution directly into the sediment has theadvantage of stabilizing the Al-floc at the site of application andminimizes the risk of redistributing of the floc within the system due toturbulence and currents (Schütz et al., 2017). Additionally, the floc isnot exposed to pH fluctuations in the water that may affect its stability(Reitzel et al., 2013). A central question for Al treatment as a re-mediation method is the long-term binding capacity, whether P trap-ping by Al results permanent burial in the sediment, or only a tem-porary interruption of the P cycle. Experiences from field studies in theBaltic Sea suggest that the Al-P formation is stable (Rydin, 2014), butaging of the Al-floc may result in a loss of binding capacity over time(DeVicente et al., 2008). Further monitoring is required to quantify thelong-term persistence of Al-P in anoxic, brackish sediments and to as-sess the potential for side effects (Conley, 2012; Spears et al., 2013;Rydin et al., 2017).

The amount of P trapped by the Al treatment after about three years(2.0 g P/m2) corresponds to, or even exceeds, the calculated mobilesediment-P content (1.5 g P/m2) in the Björnöfjärden sediment (Fig. 4,Table S2). The mobile-P pool is mainly organic and was likely a main Psource for the increased P concentration, although organic P remainednear pretreatment concentrations in the sediment profile (Table S3).The mobile pool can be expected to decline after some years when thedecreased settling of degradable organic-P compounds have had animpact on the sediment composition.

An explanation for the over-trapping of Al-P might be that it ispartially derived from the mineralization of the annual spring and au-tumn blooms. However, the decline in TP concentration below the Al-Pformation layer (Fig. 2) indicates an ongoing loss of P from these layersover time, accumulating as Al-P towards the sediment surface. Thisprocess is likely the main supply of P to the Al-P formed. After miner-alization of organic P compounds in the surface sediment, the TP con-centration levels out to a permanent burial concentration of about1mg P/g DW in accumulation areas of archipelagos in the Baltic Sea

(Malmaeus et al., 2012), comparable to the burial concentrationsmeasured in Björnöfjärden (0.8–1.0mg P/g DW, Table S2). The declinein Ca-P might reflect an Al treatment effect on the HCl-extractable Pthroughout the entire 20 cm sediment layer. However, the corre-sponding increase in the Res-P pool indicates differences in extractionefficiency between years.

The expected mineralization of the mobile sediment-P pool in thedecade to come could add another 1.5 g P/m2 to the 2.0 g dissolved Palready bound in the Al-enriched layer for a total of 3.5 g P/m2. The50 g Al/m2 applied during the Al treatment is expected to have amaximum capacity to bind 6 g P/m2 (Rydin, 2014) and should thus beenough to prevent further internal load from the sediment.

Primary production in some coastal areas of the Baltic Sea, likeBjörnöfjärden (Rydin et al., 2017), are limited by P availability, whileothers are limited by nitrogen (Granéli et al., 1990). Reduced P con-centrations are desirable in both cases, in the former to directly reduceprimary production and in the latter because excess P can stimulatepotentially harmful, nitrogen-fixing cyanobacterial blooms (Granéliet al., 1990). Given the successful reductions in external P loads, weexpect the low nutrient conditions in the water column of Björnöfjärdenand the substantial reductions in autochthonous organic matter pro-duction (Rydin et al., 2017) to persist.

Due to continued oxidation of sediment organic matter that hadaccumulated during the high production period, there will be a lagbefore the sediment surface turns oxic and allows natural P binding byiron to function again (Fig. 4). An additional 1–4 g P/m2 could betrapped by iron, assuming a typical amount of Fe-P in oxic coastal se-diment in the region (Malmaeus et al., 2012). In total, 3.5–6 g P boundto Al and another 1–4 g bound to Fe could result in P retention between4.5 and 10 g of P/m2. A few years after the treatment, there are signs ofincipient oxygen recovery below the thermocline (Rydin et al., 2017),heralding a possible shift to a regime of oxic bottom water and naturallyincreased sediment-P retention.

The treated bay is relatively small (1.5 km2), but the character of thesediment is typical for coastal ecosystems. Over time, the 3 ton of dis-solved P expected to be bound to the added Al will make Björnöfjärdena P sink in the region. Restoring the former P-burial capacity in coastalbasins may turn these present P sources back into the P filters they oncewere. Eventually, imported P may, however, overwhelm this P sink,

Fig. 4. Phosphorus (P) distribution over time at representative accumulation-bottom sediments in Björnöfjärden. P is divided into P forms resistant to sedimentdiagenesis (inert P and P bound to Al “Al-P″) and mobile-P forms (degradable organic P forms “Org-P″ and P bound to iron oxides “Fe-P″). The time period c. 1900,represent assumed TP distribution in accumulation sediments prior to eutrophication, 2012 prior to Al treatment in 2012, and 2014 and 2016 two and four years afterthe treatment. The increase in Al-P and its seeming downwards movement is explained by the ongoing settling of new matter on the sediment surface, and continuousformation of Al-P, until the added Al potentially will be saturated (≥2030). Successful reduction of the external P load may eventually turn the surface sediment oxicagain, promoting formation of Fe-P. The level of primary production, oxygenation of sediment surface and sediment-P release in the system at each time period arealso presented.

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unless TP concentrations in the open Baltic Sea can be lastingly re-duced.

5. Conclusions

• The lag in recovery of water quality after eutrophication in enclosedwater bodies is largely dependent on the limited sediment-P burialcapacity.• The pronounced sediment-P recycling following eutrophication is aconsequence of an imbalance between P present and supply of P-binding compounds in the sediment.• Dissolved Al mixed into anoxic sediment can permanently bind Pthat accumulated over the eutrophication period and that wouldotherwise be mobilized and released to the water column.• If also external loads are mitigated, and after a lag phase, oxic se-diment-P retention can be expected to further increase the filteringfunction of the coastal zone.

Competing financial interests

There are no competing financial interests.

Author contribution statements

ER & LK designed the study and performed research; ER & LKanalysed the data, ER wrote the manuscript, assisted by LK.

Acknowledgements

We are grateful to Ragnar Elmgren and Per Larsson for their com-ments on the manuscript, and Michelle McCrackin for her edits in themanuscript. We thank the staff at Naturvatten i Roslagen AB, and at theErken Laboratory at Uppsala University, for sampling and analyses, andVattenresurs AB for the aluminum treatment, Magnus Åberg for sta-tistical evaluation. This work was funded by the BalticSea2020 foun-dation.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.ecss.2019.02.046.

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