Seasonal oxygen depletion in a shallow sill fjord on the Swedish west coast

Journal of Marine Systems 175 (2017) 1–14

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Seasonal oxygen depletion in a shallow sill fjord on the Swedish west 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, Sweden 50 Long Acre, Bingham, Nottingham NG13 8AH, UK Department of Meteorology (MISU), Stockholm University, SE 106 91 Stockholm, Sweden d Swedish Meteorological and Hydrological Institute (SMHI), Sven Källfelts gata 15, SE 426 71 Västra Frölunda, Sweden b c

a r t i c l e

i n f o

Article history: Received 20 January 2017 Received in revised form 22 May 2017 Accepted 14 June 2017 Available online 16 June 2017 Keywords: Oxygen conditions Hypoxia Shallow fjord Swedish west coast

a b s t r a c t During the summer of 2008, oxygen depleted water, between 5 and 12 m depth, was discovered in Sannäsfjord on the Swedish west coast. The resulting sediments were black, benthic macrofauna were absent and Beggiatoa bacterial mats were a characteristic feature. This phenomenon, which was observed several years in a row, appears to be a relatively new phenomenon starting in the mid-1980s. In this study we attempt to find the underlying causes by investigating climatic effects (temperature, wind and precipitation), the local supply of nutrients from land, ecosystem change and the supply of organic material from the open Skagerrak. An analysis of long meteorological time series indicates that climatic effects are contributory, but probably not a dominating factor leading to hypoxia. Results from an advection-diffusion model solving for oxygen show that the observed increase in the river supply of nutrients has a high potential to generate hypoxia. Although complex and more difficult to quantify, it appears that ecosystem changes, with higher abundance of filamentous algae, may have played an important role. It is also possible that an enhanced supply of organic material from the open Skagerrak has contributed. © 2017 Published by Elsevier B.V.

1. Introduction The oxygen concentration within the marine environment below the photic zone is mainly regulated by the consumption of oxygen, by the bacterial decomposition of organic material, and the respiration of higher organisms; the supply of oxygen is mainly regulated by turbulent mixing and by the direct supply (advection) of new oxygen-rich water. Hypoxic conditions are historically defined by oxygen concentrations of b2 mL L−1 (Diaz and Rosenberg, 1995) below which macrofauna has difficulties in surviving. More recently a limit b 2 mg L−1 (corresponding to 1.4 mL L−1) has been used as a convention (Conley et al., 2007) although using a fixed limit has been questioned since deleterious effects on the ecosystem may be seen at higher concentrations (Vaquer-Sunyer and Duarte, 2008). Hypoxic and anoxic conditions occur regularly in the deep waters of the Baltic Sea region including the Kattegat and the fjords around the Skagerrak. In the open Baltic Sea the deep water shows persistent hypoxic conditions below 70 m, and the deep water of the Kattegat has seen several occasions where large areas of hypoxia

⁎ Corresponding author. E-mail address: [email protected] (G. Björk).

http://dx.doi.org/10.1016/j.jmarsys.2017.06.004 0924-7963/© 2017 Published by Elsevier B.V.

develop, for example in 2002 when 21% of the bottom in Kattegat and the Danish Straits had oxygen concentrations b2 mg L−1 with severe effects on the benthic fauna (Conley et al., 2007). Hypoxic conditions are also common in the coastal zone, and have shown an increasing trend since the 1950s in both the Baltic Sea and the Kattegat (Conley et al., 2011). On the Swedish Skagerrak coast, hypoxic (and even anoxic) conditions prevail (over many successive years) especially in the deep waters of fjords with shallow sills such as Byfjord, Havstensfjord, Koljöfjord and Idefjord (at the Norwegian border). This is also the case in Oslofjord and 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 fjord with a deeper sill, there is a strong annual cycle with high oxygen concentration due to water renewal in winter and spring followed by hypoxic conditions during autumn (Rosenberg, 1990; Nordberg et al., 2000; Filipsson and Nordberg, 2004b; Arneborg et al., 2004; Erlandsson et al., 2006; Polovodova Asteman and Nordberg, 2013). However, the minimum oxygen concentration in Gullmarsfjord shows a long-term decreasing trend due to enhanced oxygen consumption in the deep water (Erlandsson et al., 2006). Similar decreasing trends have also been reported from fjords along the Norwegian Skagerrak coast (Aure et al., 1996).

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In addition to direct oxygen measurements, studies of oxygen conditions based on abundance of benthic species and carbon enrichment in the sediments show rather widespread effects of hypoxia along the Swedish Skagerrak coast (Nordberg et al., 2000, 2009; Filipsson and Nordberg, 2004b) with a general decline of species abundance over the time period 1976–2001 (Rosenberg and Nilsson, 2005). Most observations of low oxygen conditions have been made at relatively large water depths and in local deep basins, where the often stagnant deep waters of fjords (below sill level) are typical examples. Here we present, in contrast, detailed observations of low oxygen concentrations at shallow depths around 5–12 m in Sannäsfjord on the Swedish west coast (Fig. 1) (Nordberg et al., 2012; Ödalen, 2012). Observations at these shallow depths are rare along the Swedish west coast since most of the stations in the coastal monitoring program, are at greater water depths. The observed low oxygen conditions in the fjord are examined in relation to a longer time perspective using proxies from sediment cores and historical information. Possible causes of the hypoxic conditions are investigated in the context of climatic changes and nutrient load to the system. In order to quantify effects of nutrient load we use a simplified diffusion advection model which is tuned to data in order to determine the present oxygen flux to the sediments. We then use the model to relate oxygen conditions in the fjord to reported long-term changes of the local nutrient supply, ecosystem changes and large-scale changes of organic material fluxes in the coastal waters. It should be made clear that this study includes many uncertainties which reflect the lack of critical data which is the reality for most coastal systems. Our strategy is to use the available data in systematic way to find a consistent and quantitative description of the system

in order to explain the long-term changes. Although this is made for a specific fjord the results should be of interest regarding the conditions of many shallow areas along the Swedish west coast. A screening of environmental monitoring data (Swedish National Oceanographic Data Centre at SMHI, www.smhi.se), reveals low oxygen conditions in several other protected bays. We found 8 occasions of oxygen concentration b 3.5 mL L−1 from water samples taken 1 m above bottom during summer (Jul–Aug) 2008–2011 in sheltered bays at depth between 4.5 and 12 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 Swedish west coast, approximately 30 km south of the Norwegian border (Fig. 1). It extends in a NNW-SSE direction and is approximately 7.5 km long and 100–800 m wide. The topography in the fjord deepens gradually from 3 to 6 m water depth in the shallow inner part towards the Saltpannan deep basin where the water depth increases to a maximum depth of 32.5 m inside the sill. 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 outer part forming the Västbacken basin. The outermost part of the Sannäsfjord is partially sheltered by skerries and opens to the Skagerrak. The major freshwater supply comes from a small creek, Skärboälven, with a mean discharge of 1.2 m3 s−1, which enters at the shallow southern part of the fjord. The fjord is located in an area with strong salinity stratification at the coast originating from the outflow of brackish water from the Baltic Sea. This water flows northward through the Kattegat and into the Skagerrak where it usually forms a low-salinity (about 25 g kg−1) surface layer along the coast with an average thickness of about 15 m (Arneborg, 2004). This coastal stratification is subject to strong variability, which is largely wind driven, and influences the salinity of the fjord to a high degree (Björk and Nordberg, 2003). Large water exchange above sill depth occurs when the density stratification inside the fjord adjusts to mirror the changing stratification in the coastal water (Johansson, 2010). The, mainly semidiurnal, tides are weak with a spring tidal range of b40 cm. However they can still generate relatively strong currents in the narrow mouth of the fjord and contribute to the water exchange. The fjord is surrounded by elevated topography and is sheltered from strong westerly winds. The combination of weak tides and the limited wind exposure results in a low energy environment, which allows for a significant accumulation of fine and organicrich sediments. 2.2. Observations in the water column

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

During the summer of 2008, between Aug. 1 and Sep. 25, an extensive field program undertook repeated hydrographic observations at 15 locations in the fjord (Fig. 1). All stations were typically sampled once per week but there were also three intense periods with sampling each day (Jul., 21–25; Aug. 18–22, Sep. 15–19). During the intense periods the sampling was performed twice a day (morning and afternoon) for most of the days (Jul., 22–25; Aug. 19–21, Sep. 16–18). The main instrument used was a Seabird SBE 19 plus CTD. From Aug. 22 onwards, it was equipped with a SBE43 oxygen sensor. Profiling was made to approximately 30 cm above the bottom. In addition we make use of a few hydrographic observations made in Sep. 6, 2010 (at station 7 and 9) and in Sep. 11, 2012 (stn. 9 and 11) using the same type of instrument as in 2008. Current observations were made by an Acoustic Doppler Current Profiler (ADCP, 600 kHz RDI workhorse) placed just inside the sill during the period Jun. 24 to Sep. 9, 2008 (Fig. 1). The ADCP was placed at 15 m depth, to record in 1 m bins from 12.2 to 1.2 m below the mean sea level. In order to obtain volume fluxes into the fjord, ADCP velocities were projected in the main fjord direction, multiplied with the depth-

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dependent local fjord width and a direction dependent correction factor, and integrated over the water column. A correction factor was introduced to take into account the difference between the observed velocities in the central channel and the cross-sectional average, which is smaller due to lower velocities near the fjord sides. The factor was estimated by ensuring a correspondence between the low-frequency barotropic volume fluxes and the sea level fluctuations within the fjord, and by maintaining salinity conservation (Johansson, 2010). The correction factor is smallest during inflow (0.50), and largest during outflow (0.70); thought to be due to separation from the sides during inflow (These factors are larger than those given in Johansson, 2010, due to an error in the projected velocities found after the publication of that report). The corrected velocities were low-pass filtered at 0.3 cph (cycles per hour) and 0.06 cph to separate the semi-diurnal tides and higher harmonics, from high-frequency seiche motions, and from low frequency fluctuations and mean estuarine circulation. Mean inflow volume fluxes were calculated from the unfiltered data and each of the lowpass filtered velocity data sets, and the residence times above sill level were estimated by dividing the volume above the sill level with these numbers.

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and N concentrations were calculated from weight percentage to g cm−3 using water content and an estimated average terrigenous mineral density of 2.65 g cm−3 (Flemming and Delafontaine, 2016). The total burial for the fjord was calculated by multiplying with the accumulation rate and fjord area. 2.4. Analyse of wind data In order to quantify the effect of wind on the water exchange and turbulent mixing in the fjord we constructed a vertical motion index (VMI). This index is based on the assumption that there is a linear relationship between the north/south wind stress component and Ekman transport induced upwelling/downwelling in the water column near the coast. This will cause vertical motion of the isopycnals outside the fjord and generate intermediate water exchange when the density profile inside the fjord adjusts to become similar to the outside profile. The VMI is defined as VMIj = DHj/DTj where DHj is a measure of the total vertical distance a water parcel will move during a wind event, j, with either positive or negative sign of the north/south wind stress component. DTj is the duration of each event. DHj is calculated as:



N DH j ¼
∑i¼1 W in W i


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 III400 (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 Gemini corer (80 mm ø) (Niemistö, 1974) was used for cores SSK09-2.5, 4.5 and 6.5 during the cruise in 2009. A gravity core (70 mm ø) was used in 2010 to obtain a longer record at station SSK10-4.5. Both multi corer and Gemini corer take high quality cores with virtually intact sediment core tops and sediment–water interface, however the gravity core disturbs the first few centimeters of sediment and the data from the Gemini and gravity core are therefore combined to obtain a complete record at station 4.5 (Robijn, 2012). The cores were sliced immediately after retrieval and X-rayed. In the laboratory all the samples were weighed and freeze-dried. Thereafter the samples were weighted again to determine the water content. The shape of the water content curves was also used for quality control to ensure that the records were intact and that no mechanical disturbances or large bivalves were present in the record. The age model was constructed using a combination of heavy metal records and 206Pb/207Pb-dating (Renberg et al., 2001; Robijn, 2012; Nordberg et al., in press; Table 1). Metal and CN were performed on every 10 mm down to 100 mm end then further down core every second 10 mm. The sediment total organic carbon content (TOC) and total nitrogen (TN) were analysed in a Carlo Erba 1500 CN instrument and the C/N weight ratios were calculated. Decalcifying the CN samples was performed in an exciccator with HCL-atmosphere for 48 h. The dinoflagellate cyst preparation techniques and analysis were performed in accordance with the procedures described in Harland et al. (2013a). Sediment burial rates of organic carbon and nitrogen were estimated from TOC and N concentrations at a level just below the redox cline and mixing depth (3 cm) in the sediment cores at 5 stations in the fjord. TOC

where Win is the north/south wind component for the i:th observation (every 6 h), Wi the wind speed for the i:th observation and N is the number of consecutive observations with equal sign of Win. Since there is no reason to separate between upward or downward motion the absolute value of DH is used. DT is simply set to the number of observations for each event: DT = N. The index is then normalized by dividing with the mean VMI for the entire time series. Note that the product incorporates the effect of the nonlinear relation between wind speed and wind stress while the physical constants involved in the full relation between wind stress and vertical velocity are not needed since we are only interested 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 temperature typically around 12 °C and above 17 °C further down at the shallow part, whereas colder (b 14 °C) water is trapped in the deep basin just inside the sill (Fig. 2). This trapped bottom water is colder than the water at the outermost stations sampled at the same depth. A relatively strong salinity stratification in the water mass above the sill depth is characteristic, with surface salinity b24 g kg−1 and increasing to 28 g kg−1 at about 10 m. A bottom layer with low oxygen concentration, b3 mL L−1, is clearly visible over the shallow inner parts of the fjord with a thickness of 1–2 m and with concentrations of b1 mL L− 1 for the observations closest to the bottom. The oxygen concentration is also 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

Table 1 Stations used for sediment sampling in the Sannäsfjord including date, nautical position, water depth, designation of retrieved sediment cores, estimated accumulation rates (EAR) together with carbon and nitrogen burial rates for each core. Station

1 2.5 3 4 4.5 6.5

Sampling date

09/09/2008 07/09/2009 09/09/2008 09/09/2008 12/09/2010 10/09/2008

Nautical position Latitude N

Longitude E

58°43.487′ 58°44.122′ 58°44.425′ 58°44.645′ 58°44.988′ 58°45.447′

11°14.966′ 11°14.651′ 11°14.566′ 11°13.823′ 11°13.192′ 11°12.214′

Depth (m)

Core

EAR (mm/yr)

C burial (g/m2yr)

N burial (g/m2yr)

7 8.5 9 11.5 25,5 15

SSK08-1 SSK09-2.5 SSK08-3 SSK08-4 SSK10-4.5 SSK08-6.5

2.0 4.2 3.9 2.8 11 2.2

28 40.9 72.4 45.7 157.8 32.3

3.1 4.6 7.7 4.9 17.5 3.6

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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 the map (Fig. 1). Note that the data from station 15 is extrapolated to the sill (located at distance 4.8 km).

the strong variability along the Swedish west coast. The density variations generate intermediate water exchange so that the fjord stratification above sill depth tends to follow closely the outside conditions. The sill clearly hampers water exchange below 8 m inside the sill giving much less variability and relatively long stagnant periods when the TS changes are mainly controlled by vertical diffusion. Such a period started around Aug. 10 after a major exchange of deep water when the increased salinity was followed by a gradual decrease. The currents through the narrow, shallow strait at the sill are dominated by fluctuating components of tidal and higher (1 h time scale) frequencies. Although energetic, the 1-hour component, which seems to be a barotropic Helmholtz resonance (Johansson, 2010), does not move the water parcels very far (~140 m) during one cycle as compared to the length of the strait (~600 m, Johansson, 2010), and therefore cannot be expected to contribute much to the renewal of water inside the

strait. The low-pass filtered velocities with periods longer than 3 h (Fig. 4) consist of tides, fluctuating baroclinic currents, generated by fluctuations of the density field outside the fjord, and a mean estuarine circulation. The strong, bottom-intensified current around Aug. 5 is associated with a major basin water exchange seen clearly as increasing salinity below the sill at station 12 (see Fig. 3). Neglecting the 1-hour component, the total average water exchange caused by the low-frequency currents is about 25 m3 s−1, and after removing the tides and considering only those fluctuations longer than 17 h, the water exchange decreases to 17.5 m3 s−1, such that the tidal band contributes about 7.5 m3 s− 1. The tidal excursion length is only about twice the length of the entrance strait, so part of the water will be pumped back and 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, corresponding to a residence time above sill level of about 6 days.

Fig. 3. Time series of the vertical stratification of salinity S (g kg−1), temperature T (°C) and density in sigma units σ (kg m−3) at stations 12 (inside the sill) and 15 (outside the sill) during the intense field campaign in 2008. The time of observations are shown at the upper X-axis.

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most stations (Fig. 7) indicating primary production but also significant under-saturation at some occasions, indicating decomposition, especially at the inner station 5. There are some differences between morning and afternoon oxygen profiles but no systematic diurnal variation. The low oxygen conditions in summer 2008 in Sannäsfjord appear not to have been an isolated phenomenon. Occasional observations during 2010 and 2012 also show low oxygen conditions near the bottom during the late summer and early autumn months (Fig. 8). It is however important to keep in mind that the oxygen measurements are made about 30 cm above the bottom surface. It is well-known that the oxygen levels decrease close to the sea floor, in the sediment-water interface. Generally, the actual values can therefore be expected to be significantly lower closer to the bottom surface. Fig. 4. Observed current velocity (along the main fjord axis) at the sill from the ADCP located just inside the sill, Jun. 24 to Sep. 9, 2008. Color scale gives the current velocity in m s−1 with positive values going in to the fjord. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

Time series plots of oxygen at station 12 in the deep basin (Fig. 5) show fluctuating oxygen concentrations above the sill depth and a more gradual decrease in the deep water. The monotonic decreasing deep oxygen reflects that the deep water was stagnant during this period, whereas the shallower fluctuations are caused by the more efficient water exchange above the sill. A special event occurred on Sep. 9 when the depth interval between 6 and 10 m consisted of a nearly homogeneous water mass with oxygen concentrations at about 4 mL L−1. This event is also seen further into the fjord at stations 9 and 11 (Fig. 5); it was likely caused by a major exchange of intermediate water since the salinity outside the sill showed a notable increase during this period. The oxygen concentration outside the sill was about 4 mL L−1 over a depth interval corresponding to the inflowing water and matches the concentration inside the fjord. This event resulted in much higher bottom oxygen concentrations over the shallow part of the fjords and a smaller vertical difference of the oxygen concentration (see also Fig. 6). After this event, the oxygen concentration appears to have decreased rapidly since it was much lower again in the bottom layer at the time of the next observation. Except for the event around Sept. 9 the oxygen concentration near the bottom at the shallow stations (stn. 5, 7, and 9) was relatively constant over time and the vertical profiles had a similar shape with strongly decreasing values towards the bottom in a thin layer approaching b1 mL L−1 close to the sea bed (Fig. 6). The surface concentration 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 the deepest part of the fjord and from stations 9 and 11 further into the fjord (see Fig. 1 for positions). The colors show oxygen concentration in mL L−1.

3.2. Sediment data and historical information When oxygen depletion was observed in the inner part of Sannäsfjord, during August and September of 2008, 2009 and 2010, the deposition of black sulphide sediments, a lack of macro fauna and the presence of Beggiatoa bacterial mats occurred. The observed laminations of 3–5 mm thickness, in the uppermost 3–4 cm of the sediments suggested that macrofauna had been absent for some time. These laminations might occur intermittently and may be annual or seasonal. When revisiting the same locations, a few weeks later, the laminations were disintegrated possibly due to bioturbation during oxygenated conditions following water exchange or more probably the result of resuspension that had occurred during stormy weather and energetic exchange events (cf. Fig. 4). The total organic carbon content (TOC) of the surface sediment normally varies between 5 and 6% along the transect and the C/N ratio normally varies between 8 and 9 (Fig. 9). Accumulation rates vary between 2 and 4 mm/yr but in the deep fjord basin at Saltpannan, accumulation rates vary between 9 and 13 mm/yr. According to the applied dating techniques, all locations can be classified as accumulation bottoms (Nordberg et al., in press). Estimated TOC burial rates range from 28 g m− 2 yr−1 in the shallow area to 158 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, presented in Fig. 9, it is obvious that there has been a general and continuous increase of organic carbon content in the sediments since the early 1920 and 1930s. This pattern is also seen in fjords further south on the coast (Nordberg et al., 2001; Nordberg and Robijn, 2015; Filipsson and Nordberg, 2010). Similar long term changes are noted for the C/N ratio. The inner stations, (SSK08-1, 09-2.5, 08-3), have undergone the most significant change from values around 11 during the early 20th century to values close to 8 during the most recent time. However in the outer stations, (10-4.5, 09-6.5), the ratios are slightly b 10 during the early 20th century with Station 08-4 having an intermediate value. The youngest surficial sediments along the transect have a ratio close to 8, suggesting close to uniform recent conditions. In the older (deeper) parts of the records, the three innermost stations suggest a stronger influence from terrestrial plants (Meyers, 1994). This is likely to be a result of the proximity to the Skärboälven river, which drains a significant area of agricultural and forest landscape and transports terrestrial plant fragments to the fjord. In the outer part of the fjord, the relative influence of terrestrial plant material is smaller. Since the 1960 to 1970s agricultural activities has decreased significantly (Franzén and Lindholm, 2008), which likely has resulted in a relative decrease in terrestrial plant fragments and consequently lower values of the C/N ratios. In addition, the down core higher C/N ratio is partly a diagenetic effect and must be treated with some caution since the C/N ratio can be modified 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 and occasional laminations suggest that oxygen deficiency is a relatively new phenomenon in the inner Sannäsfjord. Sampling for benthic foraminifers in the fjord, during the early 1980s, also in the inner areas

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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.

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

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

Fig. 7. Same as Fig. 6 but showing oxygen saturation.

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

deep basin (Figs. 9 and 10). Comparisons with the dinoflagellate cyst records from other fjords along the Swedish west coast reveal a similar pattern of occurrence suggesting a regional effect (Harland et al., 2013b). Some controversy surrounds the interpretation of these results but the synchronicity of the dinoflagellate cyst signal is concomitant with a common cause, whether as a result of changing meteorological (e.g. NAO) conditions or the ongoing effects of eutrophication. The lowering of cyst numbers and particularly of Lingulodinium polyedrum after 2000 CE is notable both here in Sannäsfjord and in other locations along the coast suggestive of further environmental changes (Harland et al., 2013b). Another indication for the deterioration of bottom water oxygen conditions in the fjord is that local fishermen report that demersal fishing for cod, whiting, plaice and flounder was rewarding during most summers until the mid-1980s but then no catches were recorded - a

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

Fig. 9. Sediment records along a length-wise transect in Sannäsfjord showing TOC, total organic carbon (black) and C:N weight ratio (blue). Station 1 (SSK08-1) is the innermost station, 4.5 is just inside the sill and station 6.5 is located outside the sill. Time markers for ca. 1925, the 1970s and ca. 1995 are indicated in the diagram. For locations see Fig. 1. (For interpretation of the 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). The catches of mackerel, a pelagic fish, during the late summer are unaffected. 3.3. Estimate of oxygen fluxes towards the sediments Using the well-established budget method (e.g. Gargett, 1984) it is possible to determine the oxygen consumption in the deep basin of the fjord (at Saltpannan) during a stagnant period. Oxygen production can be assumed to be zero because light levels are low in the deep water (Secchi depth 2–4 m). The oxygen consumption can be determined from the change of total oxygen content with time below a certain depth level and the diffusive flux of oxygen across the same depth level: ∂ ∂t

Z

−h −H

O2 ðzÞAðzÞdz ¼ DAðhÞ

∂O2 −C ∂z

ð1Þ

where H is the maximum depth of the basin, h the upper level of the deep water, O2 the oxygen concentration, A the horizontal area of the basin which is a function of the vertical coordinate z, C the oxygen consumption and D the turbulent diffusion coefficient. The turbulent diffusion can be determined using a similar expression as (1) with no sink term (C = 0) and using salinity data instead of oxygen. Applying the budget method during the well-defined stagnation period between Aug. 22–Sep. 25 for the water mass below 17 m (h = 17 m) gives an oxygen consumption (C) of 53 kg day−1 for the entire deep water volume. By dividing with the basin area below 17 m this corresponds to an area flux of 16 mmol m−2 day−1. This flux then represents the maximum sedimentary oxygen uptake. The computations based on salinity data gives a value of the turbulent diffusion coefficient of 1.6 · 10−5 m2 s− 1 and the downward diffusion of oxygen through the 17 m level amounts to 4.0 mmol m−2 day−1. These are based on the average vertical property gradient at 17 m. When it comes to the shallower areas of the fjord it is not possible to use the budget method to estimate the oxygen flux since there is a more or less continuous water exchange with the coastal water outside the fjord. This is also clearly seen in the data where the oxygen concentrations are generally lower in the shallower parts than in the deep basin at the same depth (see Figs. 2 and 6). The low oxygen at the shallow part is thus not simply a result of low oxygen concentrations starting in the deep basin which then spreads upward and horizontally (due to sloping bottoms) as would be the case in a stagnant water body. Instead, the oxygen flux over the shallow part is estimated by assuming that there is roughly a steady state during the observation period with oxygen consumption in the sediment balancing diffusion of oxygen from shallower layers and oxygen supply from water exchange. The relatively similar profiles during the entire period of intense field measurements, except during the abnormal event around Aug. 9, indicate that the situation was relatively stationary (Fig. 6). One advantage when using this approach is that the average water exchange is relatively well known from previous analyses based on ADCP measurements at the sill. The equation for the diffusion-advection model assuming steady state is: 2

0 ¼ EðO2S −O2 Þ þ D

∂ O2 ∂z2

ð2Þ

with the boundary conditions: D

∂O2 ¼ FO2 ; z ¼ −H ∂z

O2 ¼ O2s ; z ¼ 0 where O2 is the oxygen concentration at vertical coordinate z, E the rate of water exchange, O2S the oxygen concentration outside the fjord

(constant with depth) and D the turbulent diffusion coefficient. The boundary condition at the bottom (z = − H) states that the oxygen flux into the sediment FO2 equals the turbulent diffusion of oxygen just above the sediment. The water exchange parameter is related to the residence time as E = 1/Tres where Tres is the residence time. For simplicity the concentration at the surface (z = 0) is set to the same value as the concentration outside the fjord O2S = 6 mL L−1. Note that this model focusses on the bottom layer with low oxygen concentration and does not include any details of primary production as a source for oxygen, or the air-sea exchange. The variation of oxygen due to surface processes are much smaller than the oxygen deficit near the bottom and is therefore not included in this simplified model. The air sea exchange will in reality keep the surface oxygen concentration close to the saturation value, which is included implicitly in the model by having a surface value close to saturation. There is also a possibility for oxygen production by primary producers (microphytobenthos) at the sediment surface. We have no information on this from Sannäsfjord itself, but investigations of microphytobenthos at sediments cores along a depth gradient in the relatively nearby Gullmarsfjord (Sundbäck et al., 2004), during similar light conditions as in the Sannäsfjord (Secchi depth 2–4 m), showed only net primary production at the shallow core at 1 m water depth. The gross primary production was mostly positive but much lower at the deeper cores at 5, 10 and 15 m compared with the 1 m depth (on average 10% of the 1 m value). This does not rule out that microphytobenthos could have an effect by reducing the net oxygen flux to the sediments but it is likely not a dominating factor. It is assumed that the rate of water exchange for each layer is the same as the overall water exchange for the fjord over the major part of the water column. However, it can be expected that the water exchange is reduced close to bottom in the frictional boundary layer where the current speed decreases and where also the water motion is forced to follow the bottom. This means that the motion must go up or down slope in this layer along the gently sloping bottom at the inner part of Sannäsfjord. The advective change of properties in the bottom layer will, therefore, mostly involve water motion along the bottom and not so much from the interior further away from the bottom. The bottom layer will be relatively isolated from the in and out flowing water masses across the sill and the properties of this layer will be mostly controlled by vertical diffusion. In order to mimic this situation in the model, the value of the parameter E is set to zero in the lowermost meter and then increased linearly to the overall value in the interval 1–2 m above bottom. The equation has been solved numerically using a vertical resolution of 10 cm. The model is adjusted to the observations by using the slope of the lowermost part of the average oxygen profiles at each station. This gives the ratio FO2/D. The oxygen flux is then determined by matching the oxygen concentrations in the lowest part of the profiles. This also determines D through the fixed ratio. Stations 7 and 9 are used for this purpose. Station 11 is too deep compared with the sill depth and the more shallow station 5 is likely affected by local upwelling or primary production and show in general smaller slope of the profiles near bottom. The effective water exchange is likely to be somewhat lower than the nominal exchange of 6 days due to the elongated shape of the fjord which will result in that some of the flow trajectories across the sill going back and forth near the sill without affecting the properties in the interior of the fjord. The model is therefore run with an exchange of 8 and 10 days. The general response of the model for different water exchange and FO2 is shown in Fig. 11. It is seen that the model profiles follow the slope of the observed profile at the bottom, which is prescribed, but changing FO2 has a large effect on the concentration at the bottom. The lower panels show the near bottom concentration compared with data which can be used to find a range of the oxygen flux (using the two values 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.

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

9

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

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

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 obtained for the deep water in the deep basin at Saltpannan. For comparison, an oxygen flux of 30 mmol m−2 day−1 is large enough to deplete the oxygen in a 1 m thick layer starting at 5 mL L−1 in about 7 days. This means that the shallower bottoms of the fjord are sensitive to periods with low water exchange or low turbulence and can reach hypoxic conditions rapidly. A likely explanation to the higher oxygen consumption in the shallow areas compared with the deep basin is that the shallow bottoms are covered by fresh (newly accumulated) and highly reactive material while the deep basin contains older and less reactive material. The much higher sedimentation rate in the deep basin infers that the collected material has been transported over longer distances and for longer time, and thus become party degraded and less reactive. The 2– 3 °C lower temperature in the deep basin can also be contributing factor to 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 is probably larger but an artificially low diffusion is required in this simplified model due to the omitted effects of horizontal variations and advection in the bottom boundary layer. An advection of low-oxygen water along the bottom from deeper parts can be expected due to so-called secondary circulation caused by boundary layer mixing of stratified water above sloping bottoms (e.g. Garrett, 1991). The larger actual turbulent diffusion (tending to raise the bottom concentration) will then be compensated for by advection of water with lower oxygen concentration from deeper parts. The diffusion coefficient in our model should, therefore, not be interpreted strictly as representing diapycnal turbulent mixing, but rather as a measure of the combined processes that lead to down-gradient oxygen fluxes towards the bottom.

3.4.1. Climatic effects Higher temperatures during summer would speed up the bacterial decomposition and increase the oxygen consumption (Thamdrup et al., 1998). Temperature data from the Måseskär station (Fig. 1) shows an increase of summer temperature (Jul.–Sep.) of 1.0 °C for the period 1991–2013 compared to the period 1961–1990 (Fig. 12), which is close to the reported 0.7 °C mean temperature increase for Sweden (Kjellström et al., 2014) for the same period. An investigation of the temperature effect on oxygen consumption based on sediments from Danish waters (Thamdrup et al., 1998) showed that the oxygen consumption decreases to 1/3 of the maximum values when lowering the temperature from 20 °C to 10 °C with an associated Q10 factor of about 3 (for September). Using a maximum oxygen consumption of 35 mmol m−2 day−1, as indicated by the model results, gives a temperature dependence of 2.3 mmol m−2 day−1 °C−1. The change in oxygen consumption for a 1 °C temperature increase is thus relatively small and increasing summer temperatures are unlikely to explain fully the degenerating oxygen conditions, but they can be a contributing factor. The dinoflagellate cyst associations are consistent with modern conditions in the region (Persson et al., 2000) and are, therefore, not helpful in the differentiation of climate fluctuations and in particular temperature range. There is a mix of species that are characteristic of north temperate waters and those from higher latitudes. Another possibility is that the ventilation of the fjord from the open sea has decreased. It should be kept in mind that the oxygen conditions are relatively insensitive to modest changes of the water exchange in the order of 20% (see Fig. 11). Changes of the coastal stratification are wind driven to a high degree with upwelling/downwelling as one major source of variability (Björk and Nordberg, 2003). Westerly winds can also block the outflow of low salinity water from Kattegat (Gustafsson, 1999), which will decrease the overall storage of low salinity water further north along the Skagerrak coast. There are also important fluctuations due to large-scale wave motions such as internal Kelvin waves (Shaffer and Djurfeldt, 1983). Although a detailed analysis of long-term water exchange is complicated due to several processes acting at different temporal and spatial scales some information can be obtained directly from wind data. The wind is the main factor contributing to variations of density stratification and water exchange through a complicated coupling mechanism. Analysis of wind data

3.4. Possible causes for shallow hypoxic conditions There are several indications that oxic conditions were prevalent before the mid-1980s, as indicated by the different sediment characteristics, the dinocyst record and the local community testament on fishing catches during summer time those days. One of the authors (KN) visited Sannäsfjord in the month of July during several summers in the early

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

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

from the nearby meteorological station Måseskär show no apparent long-term changes in wind speed for the months July and August (Fig. 13). September data show enhanced wind speed during the 1970s and 1980s, which might have resulted in increased water exchange during late summer. A more direct measure of the wind effect on coastal stratification is obtained from the coast parallel north/south wind component, which is the major driving mechanism for up-/down-welling motions. Variations of the north/south component should thus generate variations of the density stratification outside the fjord and force water exchange. A measure of this effect can be obtained from a vertical motion index VMI based on the north/south wind stress (as defined in material and methods). The VMI shows the same general behaviour as the wind speed with higher values in September and a more energetic period starting in the late 1960s and reaching into the 1980s. Since the wind data in August show no significant change and we observe strong oxygen depletion in August it is not likely that the deteriorating oxygen conditions are caused by changing wind conditions, through the effect on water exchange. More critical for the oxygen conditions is the mixing near the bottom, which is mostly generated by the ambient current above the bottom boundary layer. The current is, in turn, connected to water exchange across the sill and the local wind speed and there should, therefore, be a close coupling between the water exchange and mixing. Since the wind data does not show any long-term trend or regime shift in August it is unlikely that less turbulent mixing was responsible for the degrading oxygen conditions. However, differences in wind between individual years can be quite large and may have an effect. There is nonetheless no direct evidence of such a relationship comparing the isolated observations from 2010 and 2012 with wind data. Aug. 2010 is characterized by strong wind and large VMI compared to Aug. 2012 but the oxygen conditions from observations in early September are quite similar. To determine the actual long-term changes of water exchange and mixing requires a thorough analysis beyond the scope of the present study, but according to wind data there are no large enough systematic changes that can explain the deteriorating oxygen conditions starting in the mid-1980s. Another possible climatic effect is changes in precipitation and associated local runoff that can give stronger or weaker salinity stratification in the fjord. A stronger stratification would hamper the vertical mixing, which should be unfavorable for the oxygen conditions. Long-term precipitation data from the summer period at Nordkoster (Fig. 14) show large 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 text for details). Squares show decadal means.

Fig. 14. Accumulated precipitation data during four summer months (Jun.–Sep.) each year from the meteorological observation station at Nordkoster. Also shown is the linear least square fit trend line (dotted).

over the period. This trend is, however, smaller than the interannual variability. The effect of increased precipitation on the fjord stratification can be estimated using a simplified two layer model where the upper layer is controlled by freshwater supply, wind mixing and a dynamically controlled outflow at the fjord mouth (Stigebrandt, 2012). It is then assumed that the discharge in Skärboälven has increased with a similar relative amount as the precipitation at Måseskär. Using an average wind speed of 5 m s−1 a fjord area of 2.5 km−2, a width of the mouth of 100 m, and a lower layer salinity of 28.5 g kg−1 results in a salinity change in the upper layer of 0.8 g kg−1; from 26.9 g kg−1 for a river discharge of 0.9 m3 s− 1 to 26.1 g kg− 1 for a discharge 1.2 m3 s−1. This corresponds to a 50% increase of the salinity difference between the layers (with a similar change of the density difference) and the increased precipitation will therefore increase the stability significantly and have a potential to reduce the turbulent mixing. The simplest way to estimate the effect of stratification on mixing is to assume the mixing is inversely proportional to the density difference between the layers (e.g. Arneborg et al., 2007). This corresponds to a 32% decrease of the mixing for the increased freshwater supply and will have a significant impact on the oxygen conditions (see below). Another important effect of precipitation is that increased river discharge will carry more nutrients to the fjord as discussed in the next section. 3.4.2. Supply of nutrients from local sources According to regular monthly observations by the County Administrative Board (Ruist and Lagergren, 2010) the main river entering the fjord, Skärboälven, has shown an increasing transport of nutrients over the period 1988–2008. This river drains an agricultural area that has seen farming decrease significantly over the last 3–4 decades (Franzén and Lindholm, 2008) but even so, the amounts of nutrients reaching the fjord have increased over the last few decades. The river carried ca. 21 tons nitrogen (N) yr− 1 during the period 1988–1992 and ca. 35 tons N yr− 1 during 2004–2008 (Ruist and Lagergren, 2010), which is a significant increase. Total nitrogen is approximately equally divided between the organic and inorganic pools. There is also additional supply of N to the fjord from other sources apart from Skärboälven, which adds further 20–30% to the river 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 consumption several factors need to be considered. The supply of nutrients has a large annual cycle with fluxes during summer (Jun–Aug) only about 10% of the winter values (Nov–Jan), which is based on downloaded data for Skärboälven from the SMHI model S-HYPE (Arheimer et al.,

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

2011) available on the SMHI web page. We assume that dissolved nutrients entering the fjord are utilized to form organic particles during the productive season, which then sink to the bottom and consume oxygen. Nutrients supplied in organic form are also assumed to sink to the bottom. The relatively rapid water exchange (effective residence time 8– 10 days) will flush out a substantial amount of the organic material and thus only a fraction of the locally supplied organic material will sink all the way to the bottom of the fjord and consume oxygen. Assuming a sinking speed of 1 m day−1 for the organic material and an average water depth of 6 m it can be estimated that approximately 50% of the organic material will be flushed out of the fjord and not consume oxygen locally. Note that if the organic material consists of attached algae instead of planktonic species the retention is likely much higher, which is discussed further below. The degradation and oxygen consumption of the organic material is temperature dependent and significantly larger during summer. Using a Q10 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 organic material reaching the bottom over a full year is decomposed and that thus no net accumulation occurs. The oxygen consumption is calculated by dividing the year in three periods (each four months long) with the details given in Table 2. The resulting oxygen consumption during summer is about 20 mmol m−2 day−1 and shows that the local sources can contribute with a substantive fraction of the total oxygen consumption of 25– 34 mmol m−2 day−1 estimated from the model in combination with observations. Local nutrient sources thus play a significant role in the oxygen consumption in the fjord. The value of 20 mmol m−2 day−1 includes several uncertainties. One of these is that a significant part of the organic material will be in the form of humic substances, which are less reactive and consume less oxygen. The estimate of an oxygen consumption due to loading from land is thus likely somewhat overestimated due to this factor, but hard to quantify. Another interesting aspect is that according to Ruist and Lagergren (2010) about 50% of the nutrient load is anthropogenic, which can be used to test various cases with and without the anthropogenic component. We will investigate several cases of this budget calculation which are summarized in Table 3 with case 1 as above. Another important factor in the budget is that a substantial amount of C and N is buried in the sediments and will not contribute to the oxygen consumption. Using the burial rates for each sediment core collected inside the shallow sill, and associate these with representative areas adding up to 2 km2 gives a total burial rate of 10 tons N yr−1 inside the sill. The area is reduced somewhat from the total inner fjord area since the shallowest part b1.5 m can be assumed to be more like transport bottoms or bottoms subjected to temporal accumulation of sediments during summer seasons. Subtracting this from the net local supply of N (14.4 tons yr− 1) reduces the oxygen consumption to only 6.1 mmol m−2 day−1 (Case 2, Table 3). This shows clearly that there must be an additional source of oxygen consuming material to maintain the much higher consumption rates inferred from the model in combination with observations.

11

3.4.3. Supply of oxygen consuming material from the coastal waters Another source of oxygen consuming material in fjords, in addition to local supply, comes from the open ocean. Organic particles residing in the coastal water will be transported in to the fjord by the water exchange where they can settle especially in fjord basins below the sill depth but also at shallow bottoms in protected bays. Long-term observations of fjord basins along the Swedish and Norwegian Skagerrak coast show, in general, declining oxygen conditions. Data from 31 stations along the Norwegian Skagerrak coast revealed that oxygen levels in deep waters started to decline in the middle of the 1960s and had a decreasing trend until 1993, which is the end year for this investigation (Johannessen and Dahl, 1996). A similar decreasing trend was seen in Gullmarsfjord where minimum oxygen concentrations have decreased from about 2 mL L−1 in the beginning of the 1970s to 1 mL L−1 in the mid-1980s and onward (Erlandsson et al., 2006). Using the budget method in isolated fjord basins provides trends in oxygen consumption associated with supply of this sinking oxygen consuming material. Data from Gullmarsfjord show an increase of oxygen consumption of about 50% since the 1950 (Erlandsson et al., 2006). A similar behaviour is also reported from fjords along the Norwegian Skagerrak coast with 50–60% increase of oxygen consumption after 1980 (Aure et al., 1996). The increase in oxygen consumption should be associated with enhanced concentration of oxygen consuming material in the coastal water, which is supplied to the fjords and settles in the deep basins. It can be assumed that the enhanced import of oxygen consuming organic material from the open ocean, as seen in other fjords along the Skagerrak coast has also influenced Sannäsfjord. It is not a straightforward exercise to transfer the reported carbon fluxes and changes of oxygen consumption from other sill fjords to Sannäsfjord because of the complexities of the topography and coastal dynamics. Instead we use the external source of biological material as an unknown to match the estimated oxygen flux of 25–34 mmol m−2day−1 by the model in combination with observations. The corresponding 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 along the 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 believe that the flux of organic material should be smaller in the inner part of Sannäsfjord. The distance from the sill to the open ocean is quite long and there is complex topography, including several sub-basins and narrow passages between islands, where organic particles can settle before reaching the inner parts. 3.4.4. Effects on oxygen consumption due to ecosystem changes The increased abundance of the dinoflagellate cysts together with increased concentrations of TOC in the sediment records (Fig. 10) appears to coincide with the increasing distribution of opportunistic filamentous green alga in shallow bays (0–2 m); a common feature along the Swedish west coast (Pihl et al., 1999; Cossellu and Nordberg, 2010). These filamentous algae cover the bays during the summer

Table 2 Details of the computations of seasonal oxygen consumption in the sediments based on local supply of nitrogen from land. The conversion factor relating the nitrogen supply in tons N yr−1 to oxygen consumption in mmol m−2 day−1 is based on a fjord area of 2.0 km2 and a stoichiometric ratio N:O2 = 16:138 and has a value of 0.84 (mmol O2 m−2 day−1)/(ton N year−1). Annual total supply of N = 42 tons (50% PON + 50% DIN)

Seasonal supply weight factor Seasonal supply Remaining after removal of winter DIN Net supply after removal by water exchange. Retention factor = 0.5. Temperature Oxygen consumption factor Q10 = 3 Oxygen flux Decomposition of organic N

Winter

Spring/fall

Summer

1 26.3 13.1 6.6 5.0 0.3 6.6 2.6

0.5 13.1 13.1 6.6 10.0 0.5 9.9 3.9

0.1 2.6 2.6 1.3 15.0 1.0 19.9 7.9

Total

Unit

42.0 28.9 14.4

tons tons tons °C

14.4

mmol m−2 day−1 tons

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

Table 3 Nitrogen budget and corresponding oxygen summer flux 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 in Table 2. Case

1

2

3

4

Pristine

Present

Unit

Total local supply of N Net local supply of N Burial of N External supply of N Retention factor Summer oxygen flux

42 14.4 0 0 0.5 19.9

42 14.4 10 0 0.5 4.7

42 14.4 10 14–20 0.5 25.4–33.7

42 21.7 10 7–13 0.75 25.7–34.0

21 7.2 4.5 7 0.5 13.4

42 21.7 10 10.5 0.75 30.5

tons yr−1 tons yr−1 tons yr−1 tons yr−1

months and act as filters for nutrients (McGlathery et al., 2007) keeping the organic material in the fjord. Before the significant spreading and establishment of these algal mats, phytoplankton consumed most of the nutrients during the summer. After blooming, a large part of the plankton was advected out of the fjord due to the short residence time of the surface water. During the summer, with altered wind directions, the algal mats start to drift out of the shallow embayments and sink to the fjord bottoms (Vahteri et al., 2000) where they decompose, mineralize and consume oxygen. The algae mats thus introduce a strong seasonal control on the supply of organic material. These algae grow mainly during the spring and early summer and become mobilized during the late summer and then supply oxygen demanding organic material to deeper areas. This is when the water temperatures are highest with the highest decomposition rates. The algae mats, therefore, provide an efficient mechanism to draw down the bottom oxygen concentration between 6 and 10 m depths but this effect is difficult to estimate. A quantitative measure of the effect can be achieved based on the contemporary nutrient loading from local sources of 42 tons N yr−1 and using a larger retention. As an example, taking the retention to be 75% (instead of 50%) for organic material due to algae mats gives a larger net supply of 21.7 tons N yr− 1 from local sources (compared with 14.4 tons for 50%, see Table 2). The corresponding range of external supply in order to match the estimated 25–34 mmol m−2 day−1 bottom oxygen flux is then 7–13 tons N yr−1 (Case 4). The extensive distribution of the opportunistic green algal mats in the summer, may be a result of the increased nutrient load (McGlathery et al., 2007), and ecosystem changes with trophic cascade effects by reduction of large fish species and increase of the predation pressure on mesograzers, which are known as effective grazers on filamentous algae (Andersson et al., 2009). In addition the more humid and temperate winters since the late 1980s have resulted in accumulation of muddy, organic rich bottoms in these shallow bays. Today, these shallow bay bottoms are continuously leaking nutrients and hold a large seedbank of spores and the resting stages of the alga, which thus promote algae growth. Previously, before 1980, when winters used to be colder, with high air pressure and low tides, the sea ice grounded, bottom freezed, removed sediments and eroded these bays and kept them sandy erosion bottoms with coarse gravelly and sandy lag deposits, poor in nutrients (Cossellu and Nordberg, 2010). 3.4.5. Scenarios Based on the estimates of oxygen fluxes and the known changes of loading, it is instructive to construct some scenarios of oxygen conditions using the model. These will be rather uncertain but will show the potential effect of different changes. We start from case 4 using the midpoint of the estimated range of summer oxygen consumption of 25–34 mmol m−2 day−1 and assuming a high retention of 0.75 to represent the present day situation (Table 3, case present). The external supply is then 10.5 tons N yr−1. Then we make scenarios representing a pristine situation (case pristine) assuming changes of nutrient loading and type of ecosystem. According to Ruist and Lagergren (2010) about 50% of the local nutrient load is anthropogenic which results in a pristine load of 21 N tons N yr− 1. Based on data from Gullmarsfjord and Norwegian fjords we assume that the external supply has increased with 50% from a pristine situation then corresponding to 7 tons N yr−1.

mmol m−2 day−1

It is not likely that the amount of burial was the same back in time with much lower local nutrient load and less external supply of organic material. 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 tons N yr−1 external supply and 11 tons N yr−1 burial, corresponds to a burial factor of 31%. Using this factor gives a pristine burial of 4.5 tons N yr−1. The last change is to assume that the retention of locally supplied organic material was lower, 50% instead of 75% in the pristine situation. This change exemplifies the possible effect of ecosystem changes due to absence of algae mats. The pristine case gives a summer oxygen flux of 13.4 mmol m−2 day−1 which is thus much reduced compared to the present situation. This oxygen flux can then be used as input to the advection-diffusion model in order to obtain the pristine oxygen conditions (Fig. 15). A fixed diffusion coefficient of 5 · 10−6 m2 s−1 is then used based on the average diffusion coefficient that was obtained above by fitting the model with 2008 data (Fig. 15a). The relative contributions of the different effects (local supply, external supply and retention) are also shown. The effect of a larger diffusion coefficient of 7.5 · 10−6 m2 s− 1 corresponding to reduced precipitation and less discharge in Skärboälven is also evaluated (Fig. 15b). As expected the pristine oxygen conditions are much more oxygenated compared with today's situation with bottom oxygen concentration above 4 mL L−1. The reduction of nutrients from land has the largest effect which can be expected since this is the dominant supply. Reduction of external supply gives about 0.5 mL L−1 improvement while the retention effect of algae mats which, if removed, increases the oxygen concentration with 0.6 mL L−1 at the bottom. The effect of larger mixing is also substantial with about 0.8 mL L−1 improvement of the bottom oxygen concentration for the higher diffusivity. Although this type of analysis has uncertainties it shows clearly that the combined effect of known changes of nutrient loading from land, external load from the ocean, precipitation and ecosystem changes have a strong

Fig. 15. Model results showing the summer oxygen conditions based on station 7 for different values of the oxygen flux towards the sediment and for two values of the turbulent diffusivity D: a) D = 5 · 10−6 m2 s−1, b) D = 7.5 · 10−6 m2 s−1. The red curve represents the contemporary situation with an oxygen flux of 30.5 mmol m−2 day−1. The oxygen flux has been reduced in three steps by introducing different 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 material from 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 case corresponds to the pristine case in Table 3). Average observed oxygen profiles from summer 2008 (station 7) are also shown (blue). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

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potential to have caused the deteriorated oxygen conditions near the bottom of this shallow fjord and elsewhere in Bohuslän as indicated by SMHI data. Climatic effects due to changing summer temperature and wind conditions might have contributed to a smaller extent. 4. Conclusions Observations in the Sannäsfjord from summer 2008, show hypoxic conditions in a thin b1 m bottom layer at shallow (6–10 m) depth. Similar conditions (nearly hypoxic) were also observed in 2010 and 2012. However temporal sediment characteristics evidence low oxygen conditions starting in the mid-1980s and thus is not a recent phenomenon. This is also in accordance with local witness testament of decreasing catches of demersal fish during the summers since the mid-1980s. Using a combination of a nutrient budget and idealized model calculation we have quantified how different factors affect the near bottom oxygen concentration. Observed increases in the river supply of nutrients since the 1980s appears to be the largest factor causing low oxygen conditions in the fjord. Another significant factor is a possible larger supply of particulate organic material from the Skagerrak. Changes in the ecosystem, especially a concomitant significant increase of opportunistic filamentous green algae in shallow bays (0–2 m), may also have contributed to the hypoxic conditions by increasing the retention of organic material and nutrients within the fjord. Another significant factor is the observed increase of precipitation and river discharge, which may have reduced the turbulent mixing and thereby reduced the oxygen concentration near the bottom. Higher summer temperatures may also have contributed to the low oxygen but to a lesser extent. Wind data do not show any long-term trend or regime shifts, via changes of water exchange that can explain the changes in oxygen conditions. Other mechanisms may have contributed to the hypoxic conditions but are more difficult to quantify. Diminishing sea ice during the winter provides less reworking and transport of sediment from the shallower areas and allows the build-up of muddy and organic rich sediment, which supply extra nutrients that may have enhanced algal production and oxygen consumption. There are many uncertainties in the present work and there is need of a more comprehensive high resolution biogeochemical model study with additional observations of oxygen, nutrients, sediment properties and organic material in the water column. Nevertheless our findings are a first step in quantifying the processes contributing to shallow coastal waters hypoxia. Acknowledgements The authors sincerely thank everyone who helped to perform this study. The crews of R/V Skagerak and R/V Nereus assisted during sampling campaigns 2008 and 2009. We acknowledge the funding by Region Västra Götaland “RUN & MN” (ref 612-0125-08) (KN), County Administrative Board O-Län and Tanum Community Administration (KN). Also we gratefully acknowledge Wåhlströms Foundation and Lars Hierta Memorial Foundation (KN) and the Department of Earth Sciences and Department of Marine Sciences (from July 1, 2015) (University of Gothenburg) for the PhD student (AR) fellowship. RH acknowledges the efficient palynological processing undertaken by Mr. David Bodman of the Palynological Laboratories at the University of Sheffield, UK. References Andersson, S., Persson, M., Moksnes, P.-O., Baden, S., 2009. The role of the amphipod Gammarus locusta as a grazer on macroalgae in Swedish seagrass meadows. Mar. Biol. 156:969–981. http://dx.doi.org/10.1007/s00227-009-1141-1. Arheimer, B., Dahné, J., Lindström, G., Marklund, L., Strömqvist, J., 2011. Multi-variable evaluation of an integrated model system covering Sweden (S-HYPE). IAHS Publ. 345, 145–150. Arneborg, L., 2004. Turnover times for the water above sill level in Gullmar Fjord. Cont. Shelf Res. 24:443–460. http://dx.doi.org/10.1016/j.csr.2003.12.00.

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