Journal of Marine Systems 175 (2017) 1–14

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Journal of Marine Systems

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Seasonal oxygen depletion in a shallow sill fjord on the Swedishwest coast

Göran Björk a,⁎, Kjell Nordberg a, Lars Arneborg a,d, Lennart Bornmalm a, Rex Harland b,Ardo Robijn a, Malin Ödalen c

a Department of Marine Sciences, University of Gothenburg, P.O. Box 460, SE 405 30, Swedenb 50 Long Acre, Bingham, Nottingham NG13 8AH, UKc Department of Meteorology (MISU), Stockholm University, SE 106 91 Stockholm, Swedend Swedish Meteorological and Hydrological Institute (SMHI), Sven Källfelts gata 15, SE 426 71 Västra Frölunda, Sweden

⁎ Corresponding author.E-mail address: goran.bjork@marine.gu.se (G. Björk).

http://dx.doi.org/10.1016/j.jmarsys.2017.06.0040924-7963/© 2017 Published by Elsevier B.V.

a b s t r a c t

a r t i c l e i n f o

Article history:Received 20 January 2017Received in revised form 22 May 2017Accepted 14 June 2017Available online 16 June 2017

During the summer of 2008, oxygen depleted water, between 5 and 12 m depth, was discovered in Sannäsfjordon the Swedish west coast. The resulting sediments were black, benthic macrofauna were absent and Beggiatoabacterial mats were a characteristic feature. This phenomenon, which was observed several years in a row, ap-pears to be a relatively new phenomenon starting in the mid-1980s. In this study we attempt to find the under-lying causes by investigating climatic effects (temperature, wind and precipitation), the local supply of nutrientsfrom land, ecosystem change and the supply of organicmaterial from the open Skagerrak. An analysis of longme-teorological time series indicates that climatic effects are contributory, but probably not a dominating factorleading to hypoxia. Results from an advection-diffusion model solving for oxygen show that the observedincrease in the river supply of nutrients has a high potential to generate hypoxia. Although complex and moredifficult to quantify, it appears that ecosystem changes, with higher abundance of filamentous algae, may haveplayed an important role. It is also possible that an enhanced supply of organicmaterial from the open Skagerrakhas contributed.

© 2017 Published by Elsevier B.V.

Keywords:Oxygen conditionsHypoxiaShallow fjordSwedish west coast

1. Introduction

The oxygen concentration within the marine environment belowthe photic zone is mainly regulated by the consumption of oxygen, bythe bacterial decomposition of organic material, and the respiration ofhigher organisms; the supply of oxygen ismainly regulated by turbulentmixing and by the direct supply (advection) of new oxygen-rich water.Hypoxic conditions are historically defined by oxygen concentrations ofb2 mL L−1 (Diaz and Rosenberg, 1995) below which macrofauna hasdifficulties in surviving.More recently a limit b2mg L−1 (correspondingto 1.4 mL L−1) has been used as a convention (Conley et al., 2007) al-though using a fixed limit has been questioned since deleterious effectson the ecosystemmay be seen at higher concentrations (Vaquer-Sunyerand Duarte, 2008). Hypoxic and anoxic conditions occur regularly in thedeep waters of the Baltic Sea region including the Kattegat and thefjords around the Skagerrak. In the open Baltic Sea the deep watershows persistent hypoxic conditions below 70 m, and the deep waterof the Kattegat has seen several occasions where large areas of hypoxia

develop, for example in 2002 when 21% of the bottom in Kattegat andtheDanish Straits had oxygen concentrations b2mg L−1with severe ef-fects on the benthic fauna (Conley et al., 2007). Hypoxic conditions arealso common in the coastal zone, and have shown an increasing trendsince the 1950s in both the Baltic Sea and the Kattegat (Conley et al.,2011). On the Swedish Skagerrak coast, hypoxic (and even anoxic) con-ditions prevail (over many successive years) especially in the deep wa-ters of fjordswith shallow sills such as Byfjord, Havstensfjord, Koljöfjordand Idefjord (at theNorwegian border). This is also the case in Oslofjordand several other sill fjords along the southern coast of Norway(Syvitsky et al., 1987; Nordberg et al., 2001; Filipsson and Nordberg,2004a; Bouchet et al., 2012; Polovodova Asteman et al., 2015; Robijn,2012). In Gullmarsfjord, a fjordwith a deeper sill, there is a strong annu-al cycle with high oxygen concentration due to water renewal in winterand spring followed by hypoxic conditions during autumn (Rosenberg,1990; Nordberg et al., 2000; Filipsson andNordberg, 2004b; Arneborg etal., 2004; Erlandsson et al., 2006; Polovodova Asteman and Nordberg,2013). However, the minimum oxygen concentration in Gullmarsfjordshows a long-term decreasing trend due to enhanced oxygen consump-tion in the deep water (Erlandsson et al., 2006). Similar decreasingtrends have also been reported from fjords along theNorwegian Skager-rak coast (Aure et al., 1996).

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In addition to direct oxygenmeasurements, studies of oxygen condi-tions based on abundance of benthic species and carbon enrichment inthe sediments show rather widespread effects of hypoxia along theSwedish Skagerrak coast (Nordberg et al., 2000, 2009; Filipsson andNordberg, 2004b) with a general decline of species abundance overthe time period 1976–2001 (Rosenberg and Nilsson, 2005).

Most observations of low oxygen conditions have been made at rel-atively large water depths and in local deep basins, where the oftenstagnant deep waters of fjords (below sill level) are typical examples.Here we present, in contrast, detailed observations of low oxygen con-centrations at shallow depths around 5–12 m in Sannäsfjord on theSwedish west coast (Fig. 1) (Nordberg et al., 2012; Ödalen, 2012). Ob-servations at these shallow depths are rare along the Swedish westcoast since most of the stations in the coastal monitoring program, areat greater water depths. The observed low oxygen conditions in thefjord are examined in relation to a longer timeperspective using proxiesfrom sediment cores and historical information. Possible causes of thehypoxic conditions are investigated in the context of climatic changesand nutrient load to the system. In order to quantify effects of nutrientload we use a simplified diffusion advection model which is tuned todata in order to determine the present oxygen flux to the sediments.We then use the model to relate oxygen conditions in the fjord to re-ported long-term changes of the local nutrient supply, ecosystemchanges and large-scale changes of organicmaterialfluxes in the coastalwaters. It should be made clear that this study includes many uncer-tainties which reflect the lack of critical data which is the reality formost coastal systems. Our strategy is to use the available data in system-atic way to find a consistent and quantitative description of the system

Fig. 1. Map of Sannäsfjorden with positions for the various types of observations. Thelocations of Oslofjord (O), Idefjord (I), Gullmarsfjord (G), Byfjord (B), Havstensfjord (H)and Koljöfjord (K) are marked on the overview map.

in order to explain the long-term changes. Although this is made for aspecific fjord the results should be of interest regarding the conditionsof many shallow areas along the Swedish west coast. A screening of en-vironmental monitoring data (Swedish National Oceanographic DataCentre at SMHI, www.smhi.se), reveals low oxygen conditions in sever-al other protected bays. We found 8 occasions of oxygen concentrationb 3.5 mL L−1 fromwater samples taken 1 m above bottom during sum-mer (Jul–Aug) 2008–2011 in sheltered bays at depth between 4.5 and12 m. The lowest value found was 1.55 mL L−1.

2. Material and methods

2.1. Study area

The Sannäsfjord is located on the Swedishwest coast, approximately30 km south of the Norwegian border (Fig. 1). It extends in a NNW-SSEdirection and is approximately 7.5 km long and 100–800 m wide. Thetopography in the fjord deepens gradually from 3 to 6 m water depthin the shallow inner part towards the Saltpannan deep basin wherethe water depth increases to a maximum depth of 32.5 m inside thesill. The fjord has an 8-m deep sill, located at its narrowest part (Fig.1). Outside the sill, water depths increase and reach 36 m in the outerpart forming the Västbacken basin. The outermost part of theSannäsfjord is partially sheltered by skerries and opens to the Skagerrak.

Themajor freshwater supply comes froma small creek, Skärboälven,with amean discharge of 1.2m3 s−1, which enters at the shallow south-ern part of the fjord. The fjord is located in an area with strong salinitystratification at the coast originating from the outflow of brackishwater from the Baltic Sea. This water flows northward through the Kat-tegat and into the Skagerrak where it usually forms a low-salinity(about 25 g kg−1) surface layer along the coast with an average thick-ness of about 15m(Arneborg, 2004). This coastal stratification is subjectto strong variability, which is largely wind driven, and influences the sa-linity of the fjord to a high degree (Björk and Nordberg, 2003). Largewater exchange above sill depth occurs when the density stratificationinside the fjord adjusts tomirror the changing stratification in the coast-al water (Johansson, 2010). The, mainly semidiurnal, tides are weakwith a spring tidal range of b40 cm. However they can still generate rel-atively strong currents in the narrowmouth of the fjord and contributeto the water exchange. The fjord is surrounded by elevated topographyand is sheltered from strong westerly winds. The combination of weaktides and the limited wind exposure results in a low energy environ-ment, which allows for a significant accumulation of fine and organic-rich sediments.

2.2. Observations in the water column

During the summer of 2008, between Aug. 1 and Sep. 25, an exten-sive field program undertook repeated hydrographic observations at15 locations in the fjord (Fig. 1). All stations were typically sampledonce per week but there were also three intense periods with samplingeach day (Jul., 21–25; Aug. 18–22, Sep. 15–19). During the intense pe-riods the samplingwas performed twice a day (morning and afternoon)for most of the days (Jul., 22–25; Aug. 19–21, Sep. 16–18). The main in-strument used was a Seabird SBE 19 plus CTD. From Aug. 22 onwards, itwas equipped with a SBE43 oxygen sensor. Profiling was made to ap-proximately 30 cm above the bottom. In addition we make use of afew hydrographic observations made in Sep. 6, 2010 (at station 7 and9) and in Sep. 11, 2012 (stn. 9 and11) using the same type of instrumentas in 2008.

Current observations were made by an Acoustic Doppler CurrentProfiler (ADCP, 600 kHz RDI workhorse) placed just inside the sill dur-ing the period Jun. 24 to Sep. 9, 2008 (Fig. 1). The ADCP was placed at15 m depth, to record in 1 m bins from 12.2 to 1.2 m below the meansea level. In order to obtain volume fluxes into the fjord, ADCP velocitieswere projected in the main fjord direction, multiplied with the depth-

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dependent local fjord width and a direction dependent correction fac-tor, and integrated over thewater column.A correction factorwas intro-duced to take into account the difference between the observedvelocities in the central channel and the cross-sectional average,which is smaller due to lower velocities near the fjord sides. The factorwas estimated by ensuring a correspondence between the low-frequen-cy barotropic volume fluxes and the sea level fluctuations within thefjord, and by maintaining salinity conservation (Johansson, 2010). Thecorrection factor is smallest during inflow (0.50), and largest duringoutflow (0.70); thought to be due to separation from the sides duringinflow (These factors are larger than those given in Johansson, 2010, dueto an error in the projected velocities found after the publication of that re-port). The corrected velocities were low-pass filtered at 0.3 cph (cyclesper hour) and 0.06 cph to separate the semi-diurnal tides and higherharmonics, fromhigh-frequency seichemotions, and from low frequen-cy fluctuations and mean estuarine circulation. Mean inflow volumefluxes were calculated from the unfiltered data and each of the low-pass filtered velocity data sets, and the residence times above sill levelwere estimated by dividing the volume above the sill level with thesenumbers.

2.3. Sediment cores

Six locations along the fjord have been sampled by taking four 40–100 cm long sediment cores (Fig. 1, Table 1). A multicorer MARK III-400 (100 mm ø) (Barnett et al., 1984, modified by P. Barnett in 1990)was used to collect cores SSK08-1, 3 and 4 in 2008, whereas a Geminicorer (80 mm ø) (Niemistö, 1974) was used for cores SSK09-2.5, 4.5and 6.5 during the cruise in 2009. A gravity core (70 mm ø) was usedin 2010 to obtain a longer record at station SSK10-4.5. Both multicorer and Gemini corer take high quality cores with virtually intact sed-iment core tops and sediment–water interface, however the gravitycore disturbs the first few centimeters of sediment and the data fromthe Gemini and gravity core are therefore combined to obtain a com-plete record at station 4.5 (Robijn, 2012). The coreswere sliced immedi-ately after retrieval and X-rayed. In the laboratory all the samples wereweighed and freeze-dried. Thereafter the samples were weighted againto determine the water content. The shape of the water content curveswas also used for quality control to ensure that the records were intactand that no mechanical disturbances or large bivalves were present inthe record. The age model was constructed using a combination ofheavy metal records and 206Pb/207Pb-dating (Renberg et al., 2001;Robijn, 2012; Nordberg et al., in press; Table 1). Metal and CNwere per-formed on every 10 mm down to 100 mm end then further down coreevery second 10 mm. The sediment total organic carbon content (TOC)and total nitrogen (TN) were analysed in a Carlo Erba 1500 CN instru-ment and the C/N weight ratios were calculated. Decalcifying the CNsamples was performed in an exciccator with HCL-atmosphere for48 h. The dinoflagellate cyst preparation techniques and analysis wereperformed in accordance with the procedures described in Harland etal. (2013a).

Sediment burial rates of organic carbon and nitrogenwere estimatedfrom TOC and N concentrations at a level just below the redox cline andmixing depth (3 cm) in the sediment cores at 5 stations in the fjord. TOC

Table 1Stations used for sediment sampling in the Sannäsfjord including date, nautical position,water der with carbon and nitrogen burial rates for each core.

Station Sampling date Nautical position De(m

Latitude N Longitude E

1 09/09/2008 58°43.487′ 11°14.966′ 72.5 07/09/2009 58°44.122′ 11°14.651′ 8.3 09/09/2008 58°44.425′ 11°14.566′ 94 09/09/2008 58°44.645′ 11°13.823′ 114.5 12/09/2010 58°44.988′ 11°13.192′ 256.5 10/09/2008 58°45.447′ 11°12.214′ 15

and N concentrations were calculated from weight percentage tog cm−3 usingwater content and an estimated average terrigenousmin-eral density of 2.65 g cm−3 (Flemming and Delafontaine, 2016). Thetotal burial for the fjordwas calculated bymultiplyingwith the accumu-lation rate and fjord area.

2.4. Analyse of wind data

In order to quantify the effect of wind on the water exchange andturbulent mixing in the fjord we constructed a vertical motion index(VMI). This index is based on the assumption that there is a linear rela-tionship between the north/south wind stress component and Ekmantransport induced upwelling/downwelling in the water column nearthe coast. This will cause vertical motion of the isopycnals outside thefjord and generate intermediate water exchange when the density pro-file inside the fjord adjusts to become similar to the outside profile. TheVMI is defined as VMIj = DHj/DTj where DHj is a measure of the totalvertical distance a water parcel will move during a wind event, j, witheither positive or negative sign of the north/south wind stress compo-nent. DTj is the duration of each event. DHj is calculated as:

DHj ¼ ∑Ni¼1W

inW

i���

���

where Wni is the north/south wind component for the i:th observation

(every 6 h),Wi thewind speed for the i:th observation andN is the num-ber of consecutive observations with equal sign ofWn

i . Since there is noreason to separate between upward or downward motion the absolutevalue of DH is used. DT is simply set to the number of observations foreach event: DT = N. The index is then normalized by dividing withthe mean VMI for the entire time series. Note that the product incorpo-rates the effect of the nonlinear relation between wind speed and windstress while the physical constants involved in the full relation betweenwind stress and vertical velocity are not needed since we are only inter-ested in relative changes between periods.

3. Results and discussion

3.1. Water column data

The data from late summer 2008 (Sep. 17), show a surface temper-ature typically around 12 °C and above 17 °C further down at the shal-low part, whereas colder (b14 °C) water is trapped in the deep basinjust inside the sill (Fig. 2). This trapped bottom water is colder thanthe water at the outermost stations sampled at the same depth. A rela-tively strong salinity stratification in thewatermass above the sill depthis characteristic, with surface salinity b24 g kg−1 and increasing to28 g kg−1 at about 10m. A bottom layerwith lowoxygen concentration,b3 mL L−1, is clearly visible over the shallow inner parts of the fjordwith a thickness of 1–2 m and with concentrations of b1 mL L−1 forthe observations closest to the bottom. The oxygen concentration isalso low, b3 mL L−1, in the deep basin.

The vertical salinity, temperature and density structures (Fig. 3)show large time variability at station 15 outside the sill; this reflects

epth, designation of retrieved sediment cores, estimated accumulation rates (EAR) togeth-

pth)

Core EAR(mm/yr)

C burial(g/m2yr)

N burial(g/m2yr)

SSK08-1 2.0 28 3.15 SSK09-2.5 4.2 40.9 4.6

SSK08-3 3.9 72.4 7.7.5 SSK08-4 2.8 45.7 4.9,5 SSK10-4.5 11 157.8 17.5

SSK08-6.5 2.2 32.3 3.6

Fig. 2. Sections of temperature (°C), salinity (g kg−1) and oxygen (mL L−1) along the fjord for Sep. 17, 2008. Positions for the station numbers (white) are shown on themap (Fig. 1). Notethat the data from station 15 is extrapolated to the sill (located at distance 4.8 km).

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the strong variability along the Swedish west coast. The density var-iations generate intermediate water exchange so that the fjord strat-ification above sill depth tends to follow closely the outsideconditions. The sill clearly hampers water exchange below 8 m in-side the sill giving much less variability and relatively long stagnantperiods when the TS changes are mainly controlled by vertical diffu-sion. Such a period started around Aug. 10 after a major exchange ofdeep water when the increased salinity was followed by a gradualdecrease.

The currents through the narrow, shallow strait at the sill are domi-nated by fluctuating components of tidal and higher (1 h time scale) fre-quencies. Although energetic, the 1-hour component, which seems tobe a barotropic Helmholtz resonance (Johansson, 2010), does notmove thewater parcels very far (~140m)during one cycle as comparedto the length of the strait (~600m, Johansson, 2010), and therefore can-not be expected to contribute much to the renewal of water inside the

Fig. 3. Time series of the vertical stratification of salinity S (g kg−1), temperature T (°C) and densthe intense field campaign in 2008. The time of observations are shown at the upper X-axis.

strait. The low-pass filtered velocities with periods longer than 3 h(Fig. 4) consist of tides, fluctuating baroclinic currents, generated byfluctuations of the density field outside the fjord, and a mean estuarinecirculation. The strong, bottom-intensified current around Aug. 5 is as-sociated with a major basin water exchange seen clearly as increasingsalinity below the sill at station 12 (see Fig. 3). Neglecting the 1-hourcomponent, the total average water exchange caused by the low-fre-quency currents is about 25 m3 s−1, and after removing the tides andconsidering only those fluctuations longer than 17 h, the water ex-change decreases to 17.5 m3 s−1, such that the tidal band contributesabout 7.5 m3 s−1. The tidal excursion length is only about twice thelength of the entrance strait, so part of the water will be pumped backand forth within the strait instead of renewing the fjord water volume.Assuming an efficiency of about 50% of the tidal exchange (Gillibrand,2001; Arneborg, 2004) the exchange rate is about 21 m3 s−1, corre-sponding to a residence time above sill level of about 6 days.

ity in sigma unitsσ (kgm−3) at stations 12 (inside the sill) and 15 (outside the sill) during

Fig. 4. Observed current velocity (along the main fjord axis) at the sill from the ADCPlocated just inside the sill, Jun. 24 to Sep. 9, 2008. Color scale gives the current velocityin m s−1 with positive values going in to the fjord. (For interpretation of the referencesto color in this figure legend, the reader is referred to the web version of this article.)

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Time series plots of oxygen at station 12 in the deep basin (Fig. 5)show fluctuating oxygen concentrations above the sill depth and amore gradual decrease in the deep water. The monotonic decreasingdeep oxygen reflects that the deep water was stagnant during this peri-od, whereas the shallower fluctuations are caused by themore efficientwater exchange above the sill. A special event occurred on Sep. 9 whenthe depth interval between 6 and 10 m consisted of a nearly homoge-neous water mass with oxygen concentrations at about 4 mL L−1. Thisevent is also seen further into the fjord at stations 9 and 11 (Fig. 5); itwas likely caused by a major exchange of intermediate water since thesalinity outside the sill showed a notable increase during this period.The oxygen concentration outside the sill was about 4 mL L−1 over adepth interval corresponding to the inflowing water and matches theconcentration inside the fjord. This event resulted in much higher bot-tom oxygen concentrations over the shallow part of the fjords and asmaller vertical difference of the oxygen concentration (see also Fig.6). After this event, the oxygen concentration appears to have decreasedrapidly since it wasmuch lower again in the bottom layer at the time ofthe next observation. Except for the event around Sept. 9 the oxygenconcentration near the bottom at the shallow stations (stn. 5, 7, and9) was relatively constant over time and the vertical profiles had a sim-ilar shape with strongly decreasing values towards the bottom in a thinlayer approaching b1 mL L−1 close to the sea bed (Fig. 6). The surfaceconcentration had a somewhat larger spread with over-saturation at

Fig. 5. Time series of oxygen concentration (mL L−1) from station 12 near the sill at thedeepest part of the fjord and from stations 9 and 11 further into the fjord (see Fig. 1 forpositions). The colors show oxygen concentration in mL L−1.

most stations (Fig. 7) indicating primary production but also significantunder-saturation at some occasions, indicating decomposition, espe-cially at the inner station 5. There are some differences between morn-ing and afternoon oxygen profiles but no systematic diurnal variation.

The low oxygen conditions in summer 2008 in Sannäsfjord appearnot to have been an isolated phenomenon. Occasional observations dur-ing 2010 and 2012 also show low oxygen conditions near the bottomduring the late summer and early autumnmonths (Fig. 8). It is howeverimportant to keep in mind that the oxygen measurements are madeabout 30 cmabove the bottom surface. It is well-known that the oxygenlevels decrease close to the sea floor, in the sediment-water interface.Generally, the actual values can therefore be expected to be significantlylower closer to the bottom surface.

3.2. Sediment data and historical information

When oxygen depletion was observed in the inner part ofSannäsfjord, during August and September of 2008, 2009 and 2010,the deposition of black sulphide sediments, a lack of macro fauna andthe presence of Beggiatoa bacterialmats occurred. The observed lamina-tions of 3–5 mm thickness, in the uppermost 3–4 cm of the sedimentssuggested that macrofauna had been absent for some time. These lami-nations might occur intermittently and may be annual or seasonal.

When revisiting the same locations, a few weeks later, the lamina-tions were disintegrated possibly due to bioturbation during oxygenat-ed conditions following water exchange or more probably the result ofresuspension that had occurred during stormy weather and energeticexchange events (cf. Fig. 4). The total organic carbon content (TOC) ofthe surface sediment normally varies between 5 and 6% along the tran-sect and the C/N ratio normally varies between8 and 9 (Fig. 9). Accumu-lation rates vary between 2 and 4 mm/yr but in the deep fjord basin atSaltpannan, accumulation rates vary between 9 and 13mm/yr. Accord-ing to the applied dating techniques, all locations can be classified as ac-cumulation bottoms (Nordberg et al., in press). Estimated TOC burialrates range from 28 g m−2 yr−1 in the shallow area to158 g m−2 yr−1 at Saltpannan with the corresponding range (3–17)g m−2 yr−1 for N-burial (Table 1). From the sediment records, present-ed in Fig. 9, it is obvious that there has been a general and continuousincrease of organic carbon content in the sediments since the early1920 and 1930s. This pattern is also seen in fjords further south on thecoast (Nordberg et al., 2001; Nordberg and Robijn, 2015; Filipsson andNordberg, 2010). Similar long term changes are noted for the C/Nratio. The inner stations, (SSK08-1, 09-2.5, 08-3), have undergone themost significant change from values around 11 during the early 20thcentury to values close to 8 during the most recent time. However inthe outer stations, (10-4.5, 09-6.5), the ratios are slightly b10 duringthe early 20th century with Station 08-4 having an intermediatevalue. The youngest surficial sediments along the transect have a ratioclose to 8, suggesting close to uniform recent conditions. In the older(deeper) parts of the records, the three innermost stations suggest astronger influence from terrestrial plants (Meyers, 1994). This is likelyto be a result of the proximity to the Skärboälven river, which drains asignificant area of agricultural and forest landscape and transports ter-restrial plant fragments to the fjord. In the outer part of the fjord, the rel-ative influence of terrestrial plant material is smaller. Since the 1960 to1970s agricultural activities has decreased significantly (Franzén andLindholm, 2008), which likely has resulted in a relative decrease in ter-restrial plant fragments and consequently lower values of the C/N ratios.In addition, the down core higher C/N ratio is partly a diagenetic effectand must be treated with some caution since the C/N ratio can bemod-ified due to a faster decay of nitrogen than that of carbon (Gälman et al.,2008; Möbius et al., 2010).

The recently observed black sediments, Beggiatoa bacterial mats andoccasional laminations suggest that oxygen deficiency is a relativelynew phenomenon in the inner Sannäsfjord. Sampling for benthic fora-minifers in the fjord, during the early 1980s, also in the inner areas

Fig. 6. Oxygen concentration profiles from stations 5, 7, 9, 11, 12 and 15 during 2008 for different dates of observations (month day). The shown profiles are sampled during morning.Afternoon profiles are not shown. Note the different depth scales for stations 12 and 15.

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where low oxygen conditions have been documented, indicated oxy-genated conditions, from the presence of olive-green sediments and fo-raminiferal faunas, including both calcareous and agglutinated speciesand specimens of all sizes. Living bivalves and gastropods were alsofound (Nordberg unpublished data). Dinoflagellate cyst analysis(dinocysts, preserved resting stages) of a sediment record from theSaltpannan fjord basin (accumulation rate ca. 10–13mm/yr) shows sig-nificantly increased concentrations in the most recent sediments, espe-cially those cysts attributable to autotrophic species. This is initiated at a

Fig. 7. Same as Fig. 6 but sho

core depth, corresponding to late 1980s (Fig. 10). The dominant speciesis Lingulodinium polyedrum, a species that produces cysts towards theend of the summer and into the early autumn as noted previously byDale (1976), Lewis and Hallett (1997) and Harland et al. (2006, 2013a,b). This autotrophic species is often referred to as an eutrophication in-dicator (e.g. Dale, 2009). In the same location, in the deep basin, and inother places in the inner fjord, the organic content (TOC) shows a gen-eral significant increase, starting during the mid-1980s. This is particu-larly clear in the high resolution record of station 10–4.5 from the

wing oxygen saturation.

Fig. 8. Observed oxygen profiles at shallow areas in Sannäsfjord during Sep. 6, 2010 andSep. 11, 2012. See Fig. 1 for positions.

Fig. 10. Dinocyst record and organic carbon content from dated sediment cores (S25 andSSK10-4.5) in the Saltpannan basin (S25 is at the same position as SSK10-4.5; see Table 1).

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deep basin (Figs. 9 and 10). Comparisonswith the dinoflagellate cyst re-cords from other fjords along the Swedish west coast reveal a similarpattern of occurrence suggesting a regional effect (Harland et al.,2013b). Some controversy surrounds the interpretation of these resultsbut the synchronicity of the dinoflagellate cyst signal is concomitantwith a common cause, whether as a result of changing meteorological(e.g. NAO) conditions or the ongoing effects of eutrophication. The low-ering of cyst numbers and particularly of Lingulodinium polyedrum after2000 CE is notable both here in Sannäsfjord and in other locations alongthe coast suggestive of further environmental changes (Harland et al.,2013b).

Another indication for the deterioration of bottom water oxygenconditions in the fjord is that local fishermen report that demersal fish-ing for cod, whiting, plaice and flounder was rewarding during mostsummers until the mid-1980s but then no catches were recorded - a

Fig. 9. Sediment records along a length-wise transect in Sannäsfjord showingTOC, total organic carbon (black) andC:Nweight ratio (blue). Station 1 (SSK08-1) is the innermost station, 4.5is just inside the sill and station 6.5 is located outside the sill. Timemarkers for ca. 1925, the 1970s and ca. 1995 are indicated in the diagram. For locations see Fig. 1. (For interpretation ofthe references to color in this figure legend, the reader is referred to the web version of this article.)

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phenomenon also seen along the Norwegian coast (Dale, 2009). Thecatches of mackerel, a pelagic fish, during the late summer areunaffected.

3.3. Estimate of oxygen fluxes towards the sediments

Using the well-established budget method (e.g. Gargett, 1984) it ispossible to determine the oxygen consumption in the deep basin ofthe fjord (at Saltpannan) during a stagnant period. Oxygen productioncan be assumed to be zero because light levels are low in the deepwater (Secchi depth 2–4 m). The oxygen consumption can be deter-mined from the change of total oxygen content with time below a cer-tain depth level and the diffusive flux of oxygen across the samedepth level:

∂∂t

Z −h

−HO2 zð ÞA zð Þdz ¼ DA hð Þ ∂O2

∂z−C ð1Þ

where H is the maximum depth of the basin, h the upper level of thedeep water, O2 the oxygen concentration, A the horizontal area of thebasin which is a function of the vertical coordinate z, C the oxygen con-sumption and D the turbulent diffusion coefficient. The turbulent diffu-sion can be determined using a similar expression as (1) with no sinkterm (C = 0) and using salinity data instead of oxygen. Applying thebudget method during the well-defined stagnation period betweenAug. 22–Sep. 25 for thewatermass below 17m (h=17m) gives an ox-ygen consumption (C) of 53 kg day−1 for the entire deepwater volume.By dividing with the basin area below 17 m this corresponds to an areaflux of 16 mmol m−2 day−1. This flux then represents the maximumsedimentary oxygen uptake. The computations based on salinity datagives a value of the turbulent diffusion coefficient of 1.6· 10−5 m2 s−1 and the downward diffusion of oxygen through the17m level amounts to 4.0mmolm−2 day−1. These are based on the av-erage vertical property gradient at 17 m.

When it comes to the shallower areas of the fjord it is not possible touse the budgetmethod to estimate the oxygenflux since there is amoreor less continuous water exchange with the coastal water outside thefjord. This is also clearly seen in the data where the oxygen concentra-tions are generally lower in the shallower parts than in the deep basinat the same depth (see Figs. 2 and 6). The low oxygen at the shallowpart is thus not simply a result of low oxygen concentrations startingin the deep basin which then spreads upward and horizontally (dueto sloping bottoms) as would be the case in a stagnant water body. In-stead, the oxygen flux over the shallow part is estimated by assumingthat there is roughly a steady state during the observation period withoxygen consumption in the sediment balancing diffusion of oxygenfrom shallower layers and oxygen supply fromwater exchange. The rel-atively similar profiles during the entire period of intense fieldmeasure-ments, except during the abnormal event around Aug. 9, indicate thatthe situation was relatively stationary (Fig. 6). One advantage whenusing this approach is that the average water exchange is relativelywell known from previous analyses based on ADCP measurements atthe sill. The equation for the diffusion-advectionmodel assuming steadystate is:

0 ¼ E O2S−O2ð Þ þ D∂2O2

∂z2ð2Þ

with the boundary conditions:

D∂O2

∂z¼ FO2; z ¼ −H

O2 ¼ O2s; z ¼ 0

where O2 is the oxygen concentration at vertical coordinate z, E the rateof water exchange, O2S the oxygen concentration outside the fjord

(constant with depth) and D the turbulent diffusion coefficient. Theboundary condition at the bottom (z = −H) states that the oxygenflux into the sediment FO2 equals the turbulent diffusion of oxygenjust above the sediment. The water exchange parameter is related tothe residence time as E = 1/Tres where Tres is the residence time.

For simplicity the concentration at the surface (z = 0) is set to thesame value as the concentration outside the fjord O2S = 6 mL L−1.Note that thismodel focusses on the bottom layerwith low oxygen con-centration and does not include any details of primary production as asource for oxygen, or the air-sea exchange. The variation of oxygendue to surface processes are much smaller than the oxygen deficitnear the bottom and is therefore not included in this simplified model.The air sea exchange will in reality keep the surface oxygen concentra-tion close to the saturation value, which is included implicitly in themodel by having a surface value close to saturation. There is also a pos-sibility for oxygen production by primary producers(microphytobenthos) at the sediment surface. We have no informationon this from Sannäsfjord itself, but investigations ofmicrophytobenthosat sediments cores along a depth gradient in the relatively nearbyGullmarsfjord (Sundbäck et al., 2004), during similar light conditionsas in the Sannäsfjord (Secchi depth 2–4 m), showed only net primaryproduction at the shallow core at 1 m water depth. The gross primaryproduction was mostly positive but much lower at the deeper cores at5, 10 and 15 m compared with the 1 m depth (on average 10% of the1 m value). This does not rule out that microphytobenthos could havean effect by reducing the net oxygen flux to the sediments but it is likelynot a dominating factor.

It is assumed that the rate of water exchange for each layer is thesame as the overall water exchange for the fjord over the major partof the water column. However, it can be expected that the water ex-change is reduced close to bottom in the frictional boundary layerwhere the current speed decreases and where also the water motionis forced to follow the bottom. This means that the motion must go upor down slope in this layer along the gently sloping bottom at theinner part of Sannäsfjord. The advective change of properties in the bot-tom layerwill, therefore,mostly involvewatermotion along the bottomand not so much from the interior further away from the bottom. Thebottom layer will be relatively isolated from the in and out flowingwatermasses across the sill and the properties of this layerwill bemost-ly controlled by vertical diffusion. In order to mimic this situation in themodel, the value of the parameter E is set to zero in the lowermostmeter and then increased linearly to the overall value in the interval1–2 m above bottom. The equation has been solved numerically usinga vertical resolution of 10 cm. Themodel is adjusted to the observationsby using the slope of the lowermost part of the average oxygen profilesat each station. This gives the ratio FO2/D. The oxygen flux is then deter-mined by matching the oxygen concentrations in the lowest part of theprofiles. This also determines D through the fixed ratio. Stations 7 and 9are used for this purpose. Station 11 is too deep compared with the silldepth and the more shallow station 5 is likely affected by local upwell-ing or primary production and show in general smaller slope of the pro-files near bottom. The effectivewater exchange is likely to be somewhatlower than the nominal exchange of 6 days due to the elongated shapeof the fjord whichwill result in that some of the flow trajectories acrossthe sill going back and forth near the sill without affecting the propertiesin the interior of the fjord. The model is therefore run with an exchangeof 8 and 10 days.

The general response of themodel for different water exchange andFO2 is shown in Fig. 11. It is seen that themodel profiles follow the slopeof the observed profile at the bottom, which is prescribed, but changingFO2 has a large effect on the concentration at the bottom. The lowerpanels show the near bottom concentration compared with datawhich can be used to find a range of the oxygen flux (using the twovalues of the water exchange) when the model corresponds with data.The range is 27–34 mmol m−2 day−1 for station 7 and 25–31 mmol m−2 day−1 for station 9.

Fig. 11. Result from the diffusion-advection model compared with data (blue curve) forstations 7 and 9. Model results are shown for two different values of residence time Tresand four values of the oxygen flux towards the sediment FO2 for each Tres. The values ofFO2 are [15, 25, 35, 45] mmol m−2 day−1 with the lowest value corresponding to thehighest oxygen concentration and the remaining curves can then be identified by themonotonic decrease of O2 with increasing FO2. The lower panels show in detail theoxygen concentration at the lowermost point in the model and compared withobservations at the same level (blue line). (For interpretation of the references to colorin this figure legend, the reader is referred to the web version of this article.)

Fig. 12. Monthly means of air temperature at Måseskär for July, August and Septembertogether with July–September mean (black curve). Dotted black lines show the July–September average temperature for the periods 1961–1990 and 1991–2013.

9G. Björk et al. / Journal of Marine Systems 175 (2017) 1–14

The total estimated range of FO2 is then 25–34 mmol m−2 day−1.The oxygen flux towards the sediment is thus larger than the flux ob-tained for the deep water in the deep basin at Saltpannan. For compar-ison, an oxygen flux of 30 mmol m−2 day−1 is large enough to depletethe oxygen in a 1m thick layer starting at 5mL L−1 in about 7 days. Thismeans that the shallower bottoms of the fjord are sensitive to periodswith lowwater exchange or low turbulence and can reach hypoxic con-ditions rapidly. A likely explanation to the higher oxygen consumptionin the shallow areas compared with the deep basin is that the shallowbottoms are covered by fresh (newly accumulated) and highly reactivematerial while the deep basin contains older and less reactive material.The much higher sedimentation rate in the deep basin infers that thecollected material has been transported over longer distances and forlonger time, and thus become party degraded and less reactive. The 2–3 °C lower temperature in the deep basin can also be contributing factorto the lower oxygen flux.

The diffusion coefficient D ranges between 4.5 and 6.5· 10−6 m2 s−1, which is rather small. The actual diffusion coefficient isprobably larger but an artificially lowdiffusion is required in this simpli-fiedmodel due to the omitted effects of horizontal variations and advec-tion in the bottom boundary layer. An advection of low-oxygen wateralong the bottom from deeper parts can be expected due to so-calledsecondary circulation caused by boundary layer mixing of stratifiedwater above sloping bottoms (e.g. Garrett, 1991). The larger actual tur-bulent diffusion (tending to raise the bottom concentration) will thenbe compensated for by advection of water with lower oxygen concen-tration from deeper parts. The diffusion coefficient in our model should,therefore, not be interpreted strictly as representing diapycnal turbu-lent mixing, but rather as a measure of the combined processes thatlead to down-gradient oxygen fluxes towards the bottom.

3.4. Possible causes for shallow hypoxic conditions

There are several indications that oxic conditionswere prevalent be-fore the mid-1980s, as indicated by the different sediment characteris-tics, the dinocyst record and the local community testament on fishingcatches during summer time those days. One of the authors (KN) visitedSannäsfjord in the month of July during several summers in the early

1980s for collecting samples for benthic foraminifera along the fjord.Then the sediments characteristics and the presence of benthic macro-fauna clearly demonstrated oxic environments (see Section 3.2).

3.4.1. Climatic effectsHigher temperatures during summer would speed up the bacterial

decomposition and increase the oxygen consumption (Thamdrup etal., 1998). Temperature data from the Måseskär station (Fig. 1) showsan increase of summer temperature (Jul.–Sep.) of 1.0 °C for the period1991–2013 compared to the period 1961–1990 (Fig. 12), which isclose to the reported 0.7 °C mean temperature increase for Sweden(Kjellström et al., 2014) for the same period. An investigation of thetemperature effect on oxygen consumption based on sediments fromDanish waters (Thamdrup et al., 1998) showed that the oxygen con-sumption decreases to 1/3 of the maximum values when lowering thetemperature from 20 °C to 10 °C with an associated Q10 factor of about3 (for September). Using a maximum oxygen consumption of35mmol m−2 day−1, as indicated by themodel results, gives a temper-ature dependence of 2.3 mmol m−2 day−1 °C−1. The change in oxygenconsumption for a 1 °C temperature increase is thus relatively small andincreasing summer temperatures are unlikely to explain fully thedegenerating oxygen conditions, but they can be a contributing factor.The dinoflagellate cyst associations are consistent with modern condi-tions in the region (Persson et al., 2000) and are, therefore, not helpfulin the differentiation of climate fluctuations and in particular tempera-ture range. There is a mix of species that are characteristic of north tem-perate waters and those from higher latitudes.

Another possibility is that the ventilation of the fjord from the opensea has decreased. It should be kept in mind that the oxygen conditionsare relatively insensitive to modest changes of the water exchange inthe order of 20% (see Fig. 11). Changes of the coastal stratification arewind driven to a high degree with upwelling/downwelling as onemajor source of variability (Björk and Nordberg, 2003). Westerlywinds can also block the outflow of low salinity water from Kattegat(Gustafsson, 1999), whichwill decrease the overall storage of low salin-ity water further north along the Skagerrak coast. There are also impor-tant fluctuations due to large-scale wave motions such as internalKelvinwaves (Shaffer andDjurfeldt, 1983). Although a detailed analysisof long-term water exchange is complicated due to several processesacting at different temporal and spatial scales some information canbe obtained directly from wind data. The wind is the main factor con-tributing to variations of density stratification and water exchangethrough a complicated coupling mechanism. Analysis of wind data

Fig. 14.Accumulated precipitation data during four summermonths (Jun.–Sep.) each yearfrom the meteorological observation station at Nordkoster. Also shown is the linear leastsquare fit trend line (dotted).

10 G. Björk et al. / Journal of Marine Systems 175 (2017) 1–14

from the nearby meteorological station Måseskär show no apparentlong-term changes in wind speed for the months July and August (Fig.13). September data show enhanced wind speed during the 1970sand 1980s,whichmight have resulted in increasedwater exchange dur-ing late summer. A more direct measure of the wind effect on coastalstratification is obtained from the coast parallel north/south wind com-ponent, which is the major driving mechanism for up-/down-wellingmotions. Variations of the north/south component should thus generatevariations of the density stratification outside the fjord and force waterexchange. A measure of this effect can be obtained from a vertical mo-tion index VMI based on the north/south wind stress (as defined inma-terial and methods). The VMI shows the same general behaviour as thewind speedwith higher values in September and amore energetic peri-od starting in the late 1960s and reaching into the 1980s. Since thewinddata in August show no significant change and we observe strong oxy-gen depletion in August it is not likely that the deteriorating oxygenconditions are caused by changing wind conditions, through the effecton water exchange.

More critical for the oxygen conditions is the mixing near the bot-tom, which is mostly generated by the ambient current above the bot-tom boundary layer. The current is, in turn, connected to waterexchange across the sill and the local wind speed and there should,therefore, be a close coupling between the water exchange andmixing.Since the wind data does not show any long-term trend or regime shiftin August it is unlikely that less turbulentmixingwas responsible for thedegrading oxygen conditions. However, differences inwindbetween in-dividual years can be quite large and may have an effect. There is none-theless no direct evidence of such a relationship comparing the isolatedobservations from 2010 and 2012 with wind data. Aug. 2010 is charac-terized by strongwindand large VMI compared toAug. 2012but the ox-ygen conditions from observations in early September are quite similar.To determine the actual long-term changes of water exchange andmixing requires a thorough analysis beyond the scope of the presentstudy, but according to wind data there are no large enough systematicchanges that can explain the deteriorating oxygen conditions starting inthe mid-1980s.

Another possible climatic effect is changes in precipitation and asso-ciated local runoff that can give stronger or weaker salinity stratificationin the fjord. A stronger stratification would hamper the vertical mixing,which should be unfavorable for the oxygen conditions. Long-term pre-cipitation data from the summer period at Nordkoster (Fig. 14) showlarge interannual fluctuations together with increasing precipitation

Fig. 13. Wind statistics based on data from the meteorological station at Måseskär a)monthly mean wind speed and b) monthly mean vertical motion index VMI (see textfor details). Squares show decadal means.

over the period. This trend is, however, smaller than the interannualvariability. The effect of increased precipitation on the fjord stratifica-tion can be estimated using a simplified two layer model where theupper layer is controlled by freshwater supply, wind mixing and a dy-namically controlled outflow at the fjord mouth (Stigebrandt, 2012). Itis then assumed that the discharge in Skärboälven has increased witha similar relative amount as the precipitation at Måseskär. Using an av-erage wind speed of 5 m s−1 a fjord area of 2.5 km−2, a width of themouth of 100m, and a lower layer salinity of 28.5 g kg−1 results in a sa-linity change in the upper layer of 0.8 g kg−1; from 26.9 g kg−1 for ariver discharge of 0.9 m3 s−1 to 26.1 g kg−1 for a discharge1.2 m3 s−1. This corresponds to a 50% increase of the salinity differencebetween the layers (with a similar change of the density difference) andthe increased precipitation will therefore increase the stability signifi-cantly and have a potential to reduce the turbulentmixing. The simplestway to estimate the effect of stratification on mixing is to assume themixing is inversely proportional to the density difference between thelayers (e.g. Arneborg et al., 2007). This corresponds to a 32% decreaseof themixing for the increased freshwater supply andwill have a signif-icant impact on the oxygen conditions (see below). Another importanteffect of precipitation is that increased river discharge will carry morenutrients to the fjord as discussed in the next section.

3.4.2. Supply of nutrients from local sourcesAccording to regular monthly observations by the County Admin-

istrative Board (Ruist and Lagergren, 2010) the main river enteringthe fjord, Skärboälven, has shown an increasing transport of nutri-ents over the period 1988–2008. This river drains an agriculturalarea that has seen farming decrease significantly over the last 3–4decades (Franzén and Lindholm, 2008) but even so, the amounts ofnutrients reaching the fjord have increased over the last few de-cades. The river carried ca. 21 tons nitrogen (N) yr−1 during the pe-riod 1988–1992 and ca. 35 tons N yr−1 during 2004–2008 (Ruist andLagergren, 2010), which is a significant increase. Total nitrogen is ap-proximately equally divided between the organic and inorganicpools. There is also additional supply of N to the fjord from othersources apart from Skärboälven, which adds further 20–30% to theriver flow according to the values of the total supply to the fjord(Ruist and Lagergren, 2010).

In order to relate the local nutrient supply to oxygen consumptionseveral factors need to be considered. The supply of nutrients has alarge annual cycle with fluxes during summer (Jun–Aug) only about10% of the winter values (Nov–Jan), which is based on downloadeddata for Skärboälven from the SMHI model S-HYPE (Arheimer et al.,

11G. Björk et al. / Journal of Marine Systems 175 (2017) 1–14

2011) available on the SMHIweb page.We assume that dissolved nutri-ents entering the fjord are utilized to form organic particles during theproductive season,which then sink to the bottom and consume oxygen.Nutrients supplied in organic form are also assumed to sink to the bot-tom. The relatively rapid water exchange (effective residence time 8–10 days) will flush out a substantial amount of the organic materialand thus only a fraction of the locally supplied organic material willsink all theway to the bottom of the fjord and consume oxygen. Assum-ing a sinking speed of 1mday−1 for the organicmaterial and an averagewater depth of 6m it can be estimated that approximately 50% of the or-ganic material will be flushed out of the fjord and not consume oxygenlocally. Note that if the organic material consists of attached algae in-stead of planktonic species the retention is likely much higher, whichis discussed further below.

The degradation and oxygen consumption of the organic material istemperature dependent and significantly larger during summer. Using aQ10 factor of 3 (Thamdrup et al., 1998) gives a winter consumption rate(for T= 5 °C), which is about 30% of the summer consumption (T= 15°C). Initially it is assumed that all the supplied organicmaterial reachingthe bottom over a full year is decomposed and that thus no net accumu-lation occurs. The oxygen consumption is calculated by dividing theyear in three periods (each four months long) with the details givenin Table 2. The resulting oxygen consumption during summer is about20 mmol m−2 day−1 and shows that the local sources can contributewith a substantive fraction of the total oxygen consumption of 25–34 mmol m−2 day−1 estimated from the model in combination withobservations. Local nutrient sources thus play a significant role in theoxygen consumption in the fjord. The value of 20 mmol m−2 day−1 in-cludes several uncertainties. One of these is that a significant part of theorganic material will be in the form of humic substances, which are lessreactive and consume less oxygen. The estimate of an oxygen consump-tion due to loading from land is thus likely somewhat overestimateddue to this factor, but hard to quantify. Another interesting aspect isthat according to Ruist and Lagergren (2010) about 50% of the nutrientload is anthropogenic, which can be used to test various cases with andwithout the anthropogenic component. We will investigate severalcases of this budget calculation which are summarized in Table 3 withcase 1 as above.

Another important factor in the budget is that a substantial amountof C and N is buried in the sediments and will not contribute to the ox-ygen consumption. Using the burial rates for each sediment core collect-ed inside the shallow sill, and associate these with representative areasadding up to 2 km2 gives a total burial rate of 10 tons N yr−1 inside thesill. The area is reduced somewhat from the total inner fjord area sincethe shallowest part b1.5 m can be assumed to be more like transportbottoms or bottoms subjected to temporal accumulation of sedimentsduring summer seasons. Subtracting this from the net local supply ofN (14.4 tons yr−1) reduces the oxygen consumption to only6.1 mmol m−2 day−1 (Case 2, Table 3). This shows clearly that theremust be an additional source of oxygen consumingmaterial tomaintainthe much higher consumption rates inferred from the model in combi-nation with observations.

Table 2Details of the computations of seasonal oxygen consumption in the sediments based on local supto oxygen consumption in mmol m−2 day−1 is based on a fjord area of 2.0 km2 and a stoichio

Annual total supply of N = 42 tons (50% PON + 50% DIN)

Winter

Seasonal supply weight factor 1Seasonal supply 26.3Remaining after removal of winter DIN 13.1Net supply after removal by water exchange. Retention factor = 0.5. 6.6Temperature 5.0Oxygen consumption factor Q10 = 3 0.3Oxygen flux 6.6Decomposition of organic N 2.6

3.4.3. Supply of oxygen consuming material from the coastal watersAnother source of oxygen consuming material in fjords, in addition

to local supply, comes from the open ocean. Organic particles residingin the coastal water will be transported in to the fjord by the water ex-change where they can settle especially in fjord basins below the silldepth but also at shallow bottoms in protected bays. Long-term obser-vations of fjord basins along the Swedish and Norwegian Skagerrakcoast show, in general, declining oxygen conditions. Data from 31 sta-tions along the Norwegian Skagerrak coast revealed that oxygen levelsin deep waters started to decline in the middle of the 1960s and had adecreasing trend until 1993, which is the end year for this investigation(Johannessen and Dahl, 1996). A similar decreasing trend was seen inGullmarsfjord where minimum oxygen concentrations have decreasedfrom about 2 mL L−1 in the beginning of the 1970s to 1 mL L−1 in themid-1980s and onward (Erlandsson et al., 2006). Using the budgetmethod in isolated fjord basins provides trends in oxygen consumptionassociated with supply of this sinking oxygen consumingmaterial. Datafrom Gullmarsfjord show an increase of oxygen consumption of about50% since the 1950 (Erlandsson et al., 2006). A similar behaviour isalso reported from fjords along the Norwegian Skagerrak coast with50–60% increase of oxygen consumption after 1980 (Aure et al., 1996).The increase in oxygen consumption should be associated with en-hanced concentration of oxygen consuming material in the coastalwater, which is supplied to the fjords and settles in the deep basins. Itcan be assumed that the enhanced import of oxygen consuming organicmaterial from the open ocean, as seen in other fjords along the Skager-rak coast has also influenced Sannäsfjord.

It is not a straightforward exercise to transfer the reported carbonfluxes and changes of oxygen consumption from other sill fjords toSannäsfjord because of the complexities of the topography and coastaldynamics. Instead we use the external source of biological material asan unknown to match the estimated oxygen flux of 25–34 mmol m−2-

day−1 by themodel in combinationwith observations. The correspond-ing range of external supply is then 14–20 tons N yr−1 (Case 3).Converting N flux to a carbon flux gives 3.4–4.8 g C m−2 month−1.This is based on a Redfield C/N ratio by weight and a 2 km2 fjord area.This range is lower than carbon fluxes obtained from sill basins alongthe Norwegian coast, which shows values around 7 g C m−2 month−1

for sill depths around 10 m (Aure et al., 1996). There are reasons to be-lieve that the flux of organicmaterial should be smaller in the inner partof Sannäsfjord. The distance from the sill to the open ocean is quite longand there is complex topography, including several sub-basins and nar-row passages between islands, where organic particles can settle beforereaching the inner parts.

3.4.4. Effects on oxygen consumption due to ecosystem changesThe increased abundance of the dinoflagellate cysts together with

increased concentrations of TOC in the sediment records (Fig. 10) ap-pears to coincide with the increasing distribution of opportunistic fila-mentous green alga in shallow bays (0–2 m); a common feature alongthe Swedish west coast (Pihl et al., 1999; Cossellu and Nordberg,2010). These filamentous algae cover the bays during the summer

ply of nitrogen from land. The conversion factor relating the nitrogen supply in tonsN yr−1

metric ratio N:O2 = 16:138 and has a value of 0.84 (mmol O2 m−2 day−1)/(ton N year−1).

Spring/fall Summer Total Unit

0.5 0.113.1 2.6 42.0 tons13.1 2.6 28.9 tons6.6 1.3 14.4 tons10.0 15.0 °C0.5 1.09.9 19.9 mmol m−2 day−1

3.9 7.9 14.4 tons

Table 3Nitrogen budget and corresponding oxygen summerflux for different cases. Net local supply of N is computed according to the same scheme as in Table 2. Case 1 corresponds to the case inTable 2.

Case 1 2 3 4 Pristine Present Unit

Total local supply of N 42 42 42 42 21 42 tons yr−1

Net local supply of N 14.4 14.4 14.4 21.7 7.2 21.7 tons yr−1

Burial of N 0 10 10 10 4.5 10 tons yr−1

External supply of N 0 0 14–20 7–13 7 10.5 tons yr−1

Retention factor 0.5 0.5 0.5 0.75 0.5 0.75Summer oxygen flux 19.9 4.7 25.4–33.7 25.7–34.0 13.4 30.5 mmol m−2 day−1

Fig. 15. Model results showing the summer oxygen conditions based on station 7 fordifferent values of the oxygen flux towards the sediment and for two values of theturbulent diffusivity D: a) D = 5 · 10−6 m2 s−1, b) D = 7.5 · 10−6 m2 s−1. The redcurve represents the contemporary situation with an oxygen flux of30.5 mmol m−2 day−1. The oxygen flux has been reduced in three steps by introducingdifferent factors characterizing an earlier pristine situation. FO2 =20.3 mmol m−2 day−1 represents a 50% reduction of the nutrient loading from land.FO2 = 17.0 mmol m−2 day−1 is for adding the effect of less supply of organic materialfrom the outside sea. FO2 = 13.4 mmol m−2 day−1 is for absent filamentous algae mats(added effect) giving less retention of organic material in the fjord (this casecorresponds to the pristine case in Table 3). Average observed oxygen profiles fromsummer 2008 (station 7) are also shown (blue). (For interpretation of the references tocolor in this figure legend, the reader is referred to the web version of this article.)

12 G. Björk et al. / Journal of Marine Systems 175 (2017) 1–14

months and act as filters for nutrients (McGlathery et al., 2007) keepingthe organicmaterial in the fjord. Before the significant spreading and es-tablishment of these algal mats, phytoplankton consumed most of thenutrients during the summer. After blooming, a large part of the plank-ton was advected out of the fjord due to the short residence time of thesurface water. During the summer, with altered wind directions, thealgal mats start to drift out of the shallow embayments and sink to thefjord bottoms (Vahteri et al., 2000) where they decompose, mineralizeand consume oxygen. The algae mats thus introduce a strong seasonalcontrol on the supply of organic material. These algae growmainly dur-ing the spring and early summer and become mobilized during the latesummer and then supply oxygen demanding organicmaterial to deeperareas. This is when thewater temperatures are highest with the highestdecomposition rates. The algae mats, therefore, provide an efficientmechanism to draw down the bottom oxygen concentration between6 and 10 m depths but this effect is difficult to estimate. A quantitativemeasure of the effect can be achieved based on the contemporary nutri-ent loading from local sources of 42 tons N yr−1 and using a larger re-tention. As an example, taking the retention to be 75% (instead of50%) for organic material due to algae mats gives a larger net supplyof 21.7 tons N yr−1 from local sources (compared with 14.4 tons for50%, see Table 2). The corresponding range of external supply in orderto match the estimated 25–34 mmol m−2 day−1 bottom oxygen fluxis then 7–13 tons N yr−1 (Case 4).

The extensive distribution of the opportunistic green algal mats inthe summer, may be a result of the increased nutrient load(McGlathery et al., 2007), and ecosystem changes with trophic cascadeeffects by reduction of large fish species and increase of the predationpressure on mesograzers, which are known as effective grazers on fila-mentous algae (Andersson et al., 2009). In addition themore humid andtemperatewinters since the late 1980s have resulted in accumulation ofmuddy, organic rich bottoms in these shallow bays. Today, these shal-low bay bottoms are continuously leaking nutrients and hold a largeseedbank of spores and the resting stages of the alga, which thus pro-mote algae growth. Previously, before 1980, when winters used to becolder, with high air pressure and low tides, the sea ice grounded, bot-tom freezed, removed sediments and eroded these bays and keptthem sandy erosion bottoms with coarse gravelly and sandy lag de-posits, poor in nutrients (Cossellu and Nordberg, 2010).

3.4.5. ScenariosBased on the estimates of oxygen fluxes and the known changes of

loading, it is instructive to construct some scenarios of oxygen condi-tions using the model. These will be rather uncertain but will showthe potential effect of different changes. We start from case 4 usingthe midpoint of the estimated range of summer oxygen consumptionof 25–34 mmol m−2 day−1 and assuming a high retention of 0.75 torepresent the present day situation (Table 3, case present). The externalsupply is then 10.5 tons N yr−1. Thenwemake scenarios representing apristine situation (case pristine) assuming changes of nutrient loadingand type of ecosystem. According to Ruist and Lagergren (2010) about50% of the local nutrient load is anthropogenic which results in a pris-tine load of 21 N tons N yr−1. Based on data from Gullmarsfjord andNorwegian fjords we assume that the external supply has increasedwith 50% from a pristine situation then corresponding to 7 tons N yr−1.

It is not likely that the amount of burial was the same back in time withmuch lower local nutrient load and less external supply of organic ma-terial. One way to deal with this is to assume a constant burial factor.The present situation with 21.7 tons N yr−1 net local supply,10.5 tonsN yr−1 external supply and 11 tonsN yr−1 burial, correspondsto a burial factor of 31%. Using this factor gives a pristine burial of4.5 tonsN yr−1. The last change is to assume that the retention of locallysupplied organic material was lower, 50% instead of 75% in the pristinesituation. This change exemplifies the possible effect of ecosystemchanges due to absence of algae mats. The pristine case gives a summeroxygen flux of 13.4mmolm−2 day−1which is thusmuch reduced com-pared to the present situation. This oxygen flux can then be used asinput to the advection-diffusion model in order to obtain the pristineoxygen conditions (Fig. 15). A fixed diffusion coefficient of 5· 10−6 m2 s−1 is then used based on the average diffusion coefficientthat was obtained above by fitting the model with 2008 data (Fig.15a). The relative contributions of the different effects (local supply, ex-ternal supply and retention) are also shown. The effect of a larger diffu-sion coefficient of 7.5 · 10−6 m2 s−1 corresponding to reducedprecipitation and less discharge in Skärboälven is also evaluated (Fig.15b). As expected the pristine oxygen conditions are much more oxy-genated compared with today's situation with bottom oxygen concen-tration above 4 mL L−1. The reduction of nutrients from land has thelargest effect which can be expected since this is the dominant supply.Reduction of external supply gives about 0.5 mL L−1 improvementwhile the retention effect of algae mats which, if removed, increasesthe oxygen concentration with 0.6 mL L−1 at the bottom. The effect oflarger mixing is also substantial with about 0.8 mL L−1 improvementof the bottom oxygen concentration for the higher diffusivity. Althoughthis type of analysis has uncertainties it shows clearly that the combinedeffect of known changes of nutrient loading from land, external loadfrom the ocean, precipitation and ecosystem changes have a strong

13G. Björk et al. / Journal of Marine Systems 175 (2017) 1–14

potential to have caused the deteriorated oxygen conditions near thebottom of this shallow fjord and elsewhere in Bohuslän as indicatedby SMHI data. Climatic effects due to changing summer temperatureand wind conditions might have contributed to a smaller extent.

4. Conclusions

Observations in the Sannäsfjord from summer 2008, show hypoxicconditions in a thin b1m bottom layer at shallow (6–10m) depth. Sim-ilar conditions (nearly hypoxic) were also observed in 2010 and 2012.However temporal sediment characteristics evidence low oxygen con-ditions starting in themid-1980s and thus is not a recent phenomenon.This is also in accordance with local witness testament of decreasingcatches of demersal fish during the summers since the mid-1980s.Using a combination of a nutrient budget and idealized model calcula-tionwe have quantified how different factors affect the near bottom ox-ygen concentration. Observed increases in the river supply of nutrientssince the 1980s appears to be the largest factor causing low oxygen con-ditions in the fjord. Another significant factor is a possible larger supplyof particulate organic material from the Skagerrak. Changes in the eco-system, especially a concomitant significant increase of opportunisticfilamentous green algae in shallow bays (0–2 m), may also have con-tributed to the hypoxic conditions by increasing the retention of organicmaterial and nutrients within the fjord. Another significant factor is theobserved increase of precipitation and river discharge, which may havereduced the turbulent mixing and thereby reduced the oxygen concen-tration near the bottom. Higher summer temperatures may also havecontributed to the low oxygen but to a lesser extent. Wind data do notshow any long-term trend or regime shifts, via changes of water ex-change that can explain the changes in oxygen conditions.

Other mechanisms may have contributed to the hypoxic conditionsbut are more difficult to quantify. Diminishing sea ice during the winterprovides less reworking and transport of sediment from the shallowerareas and allows the build-up of muddy and organic rich sediment,which supply extra nutrients that may have enhanced algal productionand oxygen consumption.

There are many uncertainties in the present work and there is needof a more comprehensive high resolution biogeochemical model studywith additional observations of oxygen, nutrients, sediment propertiesand organic material in the water column. Nevertheless our findingsare a first step in quantifying the processes contributing to shallowcoastal waters hypoxia.

Acknowledgements

The authors sincerely thank everyone who helped to perform thisstudy. The crews of R/V Skagerak and R/V Nereus assisted during sam-pling campaigns 2008 and 2009. We acknowledge the funding by Re-gion Västra Götaland “RUN & MN” (ref 612-0125-08) (KN), CountyAdministrative Board O-Län and Tanum Community Administration(KN). Also we gratefully acknowledgeWåhlströms Foundation and LarsHiertaMemorial Foundation (KN) and theDepartment of Earth Sciencesand Department of Marine Sciences (from July 1, 2015) (University ofGothenburg) for the PhD student (AR) fellowship. RH acknowledgesthe efficient palynological processing undertaken byMr. David Bodmanof the Palynological Laboratories at the University of Sheffield, UK.

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