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Caballero-Alfonso et al. 2015


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Caballero-Alfonso et al. 2015

  1. 1. Biogeochemical and environmental drivers of coastal hypoxia Angela M. Caballero-Alfonso a,1 , Jacob Carstensen b , Daniel J. Conley a a Department of Geology, Lund University, Sölvegatan 12, SE-223 62 Lund, Sweden b Department of Bioscience, Aarhus University, Frederiksborgvej 399, DK-4000 Roskilde, Denmark a b s t r a c ta r t i c l e i n f o Article history: Received 9 January 2014 Received in revised form 31 March 2014 Accepted 11 April 2014 Available online 21 April 2014 Keywords: Hypoxia Coastal zone Baltic Sea Nutrients Recent reports have demonstrated that hypoxia is widespread in the coastal zone of the Baltic Sea. Here we evaluate the long-term trends of dissolved oxygen in bottom waters and of the drivers of coastal hypoxia. Eleven of the 33 sites evaluated had increasing trends of bottom water dissolved oxygen, but only the Stockholm Archipelago presents a consistent positive increasing trend in time. The vast majority of sites continue to worsen, especially along the Danish and Finnish coasts, in spite of remediation efforts to reduce nutrients. Surface temperatures were relatively comparable across the entire coastal Baltic Sea, whereas bottom water tempera- tures varied more strongly among sites, most likely due to differences in mixing (or stratification) and water exchange with the open Baltic Sea. Nutrient concentrations varied by factors 2–3 with highest levels at sites with restricted water exchange and higher land based nutrient loading. None of the sites were permanently stratified during the summer seasonal window although most of the sites were stratified more than half of the time. The frequency of hypoxia was also quite variable with sites in Gulf of Bothnia almost never experiencing hypoxia to enclosed sites with more than 50% chance of hypoxia. There are many factors governing hypoxia and the complexity of interacting processes in the coastal zone makes it difficult to identify specific causes. Our results demonstrate that managing nutrients can create positive feedbacks for oxygen recovery to occur. In the absence of nutrient reductions, the recovery from hypoxia in coastal marine ecosystems is unlikely. © 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license ( 1. Introduction Hypoxia has intermittently occurred in the Baltic Sea since its forma- tion 8000 years ago with its occurrence constrained by hydrological processes, climate and anthropogenic activities (Sohlenius et al., 2001; Zillén et al., 2008). Since the 1950s the spatial distribution and intensity of hypoxia in the open waters have increased due to anthropogenic nutrient enrichment (Carstensen et al., 2014; Conley et al., 2009a, 2009b). Nutrient loads have increased by approximately 2.5 times for nitrogen (N) and 3.7 for phosphorus (P) since the turn of the last century (Gustafsson et al., 2012). Nutrients stimulate phytoplankton production and the subsequent decomposition of organic matter creates a demand for oxygen. The Baltic Sea is comprised of several connected basins with permanent salinity stratification and restricted ventilation of the bottom waters making it susceptible to hypoxia. Hypoxia reduces the abundance of benthic fauna and alters sediment nutrient dynamics (Conley et al., 2007; Karlson et al., 2007; Perus and Bonsdorff, 2004). Hypoxia also re- stricts the reproduction of the bottom dwelling fish species, especially cod, by reducing spawning area (Limburg et al., 2011; Vallin et al., 1999). Much less is known regarding hypoxia in the coastal zone, where the physical processes are generally more dynamic and complex. Globally, the ratesofdecreaseinbottomwateroxygenconcentrationsarehigherin coast- al areas than in the open oceans (Gilbert et al., 2010). Hypoxia has been ob- served in the coastal zone of the Baltic Sea with 115 sites out of 613 sites, assessed from monitoring data, having experienced hypoxia between 1955 and 2009 (Conley et al., 2011). In addition to the existing coastal ma- rine sites worldwide that have reported hypoxia (Diaz and Rosenberg, 2008), these 115 sites make the Baltic Sea the largest region in the world that suffers from hypoxia with over the 20% of the known areas worldwide (Conley et al., 2011). In addition, there is an increasing trend in the severity of hypoxia since the 1950s in many coastal sites of the Baltic Sea. There are many factors governing hypoxia and the complexity of interacting processes in the coastal zone makes it difficult to identify specific causes. Anthropogenic drivers are primarily nutrient inputs, one of the common features of coastal eutrophication. Eutrophication is defined as the organic enrichment of a system (Nixon, 1995), which has serious consequences for the marine environment including de- clines in water transparency, increasing algal blooms, loss of benthic vegetation and hypoxia among others (Nixon, 2009). There are also natural drivers of hypoxia: 1) hydrology (reduced horizontal advection enhancing bottom-water residence time, stratification reducing vertical mixing), and 2) climate (temperature reducing the solubility of oxygen and increasing respiration as well as changes in wind patterns, rainfall and runoff affecting the hydrological processes). In the open ocean cli- mate models predict declines in dissolved oxygen produced by global Journal of Marine Systems 141 (2015) 190–199 E-mail address: (A.M. Caballero-Alfonso). 1 Tel.: +46 462220449. 0924-7963/© 2014 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license ( Contents lists available at ScienceDirect Journal of Marine Systems journal homepage:
  2. 2. warming due to a contribution of thermal, dynamical, and biogeochem- ical factors (Stramma et al., 2008). However, further studies are needed to understand and elucidate the underlying mechanisms for hypoxia in coastal areas (Conley et al., 2009b; Rabalais et al., 2010). We focused our investigation on evaluating the long-term trends of bottom water oxygen concentrations and of the drivers of coastal hyp- oxia in the Baltic Sea. Our goal was to examine relationships between nutrients, physical factors and climate as important drivers for coastal hypoxia in the Baltic Sea. 2. Material and methods 2.1. Study area and site descriptions The Baltic Sea is a nearly landlocked sea located between 54 and 66°N having restricted water exchange with the oceans. It consists of the main deeper basin (Baltic Proper) with three major gulfs in the northeast (Gulf of Riga, Gulf of Finland and Gulf of Bothnia) and con- nects to the North Sea through the Danish Straits. Most of the Baltic Sea is brackish with salinities less than 10, but the entrance area (the Danish Straits) is characterized by strong salinity gradients. The climate is temperate with an annual rainfall of approximately 600 mm per year (Omstedt et al., 1997). About 85 million people inhabit the Baltic Sea catchment, which is dominated by agriculture and urbanization in the southwest and forests towards the northeast. Nutrient loads from the different regions are a reflection of the land use (Wulff et al., 1990). The coastal zone surrounding the Baltic Sea is quite diverse, owing to its geologic history. Shallow, sandy estuaries and coastal embayments with complex geomorphology dominate in the southwest, changing to an open coastline with lagoons along the southeastern coastline. Most of the Swedish and Finnish coastline is archipelagic. Large rivers drain an area approximately four times the Baltic Sea itself and discharge to the Baltic Proper, Gulf of Riga, Gulf of Finland and Gulf of Bothnia. Rivers draining into the Danish Straits are smaller. A total of 33 sites were studied and grouped in 9 regions following HELCOM designations: Kattegat (4 sites), Øresund (1 site), Belt Sea (6 sites), West Gotland Basin (4 sites), Stockholm Archipelago (5 sites), Bothnian Sea (1 site), Bothnian Bay (2 sites), Finnish Archipelago (5 sites) and Gulf of Finland (5 sites); see Table 1 for more details. These sites were selected based on the results in Conley et al. (2011) and the length of time series available in the Baltic Environmental Database (BED). We chose sites that had experienced coastal hypoxia and were representative of a region, and which had more than 10 years of data. Some data-rich areas, e.g. the Stockholm Archipelago, had numerous sites with long-term time series and in such areas the most representa- tive sites were selected. 2.2. Data analyses Seasonal windows for hypoxia-prone months were selected per region to give a better description of low oxygen conditions (Conley et al., 2011). For the Bothnian Bay, Stockholm and Finnish archipelagos, the West Gotland Basin, the Kattegat and the Öresund the summer months considered were August through October. For the Bothnian Sea we considered only August and September; and for the Gulf of Finland July through October. These data were organized by region and sites with the aim to establish annual time series for each site. In coastal areas periods of stratification and mixing can alternate over short time scales, unlike the hydrographic conditions in the deeper Baltic Sea basins (Conley et al., 2011). Stratification is a precondition for hypoxia to occur and therefore only profiles characterized by stratified conditions were selected to evaluate oxygen trends. We defined the water column to be stratified if the density difference between surface and bottom waters was larger than 0.5 g l−1 (see Conley et al., 2007). The rate of oxygen depletion in the bottom water depends on the vol- ume below the pycnocline and to characterize this volume we calculated bottom water thickness as the profile maximum depth minus the depth location of the pycnocline. This characteristic was cal- culated on the more recent data, due to low resolution of older profiles, and assuming that bottom water thickness remained the same through- out the summer period. Oxygen saturation (%) and Apparent Oxygen Utilization (AOU) were calculated for the bottom waters. AOU is defined as the observed oxy- gen concentration subtracted from the oxygen concentration at satura- tion state calculated from temperature and salinity of the bottom water (Hetland and Di Marco, 2008). AOU allows temperature and salinity effects on oxygen solubility to be removed from the observations and quantifies the loss of oxygen due to biological and chemical activities (Bianchi et al., 2010), most importantly respiratory demands from decomposition of organic material. The bottom oxygen trend was tested against the following possible hypoxia triggers: (a) physical status: temperature and stratification; (b) biological status: surface chlorophyll a (chla); and (c) chemical status: total phosphorus (TP) and total nitro- gen (TN). Additionally, to assess the putative effect of low oxygen con- centrations on benthic communities the frequency of hypoxia was assessed. Although the thresholds for faunal effects to occur vary widely in the literature from 0.28 to 4 mg O2 l−1 (Steckbauer et al., 2011; Vaquer-Sunyer and Duarte, 2010), we define hypoxia as concentrations of dissolved oxygen equal to or below 2 mg O2 l−1 (Rabalais et al., 2010). Hence, the frequency of hypoxia was calculated as the propor- tion of profiles with bottom water oxygen concentrations below 2 mg O2 l−1 . Trends of seasonal means were estimated using Generalized Linear Models (GLMs), separately for each site and variables of interest, taking into account temporal variations (months and years as additive categor- ical factors). After examining the distribution of different variables, oxygen concentrations, AOU, and temperature were assumed to follow a normal distribution; chla, TN and TP were assumed lognormal distrib- uted; and frequencies of hypoxia and stratification were binomial. Using the GLM approach accounted for changes in sampling across years by weighting each profile according to the month it was taken (Carstensen et al., 2006). Trends in oxygen concentrations were related to trends in temperature, frequency of stratification, surface TN, TP and chla concen- trations using Spearman correlations. Spearman correlation was chosen since it is less sensitive to single years with strongly deviating annual means that may otherwise influence standard correlations. All the data processing and statistical analyses were programmed using SAS®. 3. Results The studied sites varied from 10 to 117 m depth with bottom water below the pycnocline ranging from 1.1 to 22.2 m (Table 1). The thick- ness of the bottom water typically increased with water depth. Surface temperatures were relatively comparable across the entire coastal Baltic Sea, whereas bottom water temperatures varied more strongly among sites, most likely due to differences in mixing (or stratification) and water exchange with the open Baltic Sea. Nutrient concentrations var- ied by factors 2–3 with the highest levels at sites with restricted water exchange and higher connectivity to land. None of the sites were per- manently stratified during the summer seasonal window although most of the sites were stratified more than half of the time. The frequen- cy of hypoxia was also quite variable with sites in Gulf of Bothnia almost never experiencing hypoxia to enclosed sites with more than 50% chance of hypoxia. In the following trends in oxygen conditions and associated vari- ables are presented, but the trends are only visualized for a few selected sites for plotting, as we could not show all. However, directions of trends are visualized geographically for all sites (Fig. 1). The sites presented (Figs. 2–5) were those having the highest significant correlation for bottom oxygen concentration versus at least one of the tested influenc- ing variables (Table 2). 191A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  3. 3. Table 1 Characteristics of the 33 coastal study sites in the Baltic Sea. Site names are from the national monitoring programs. Number of profiles and descriptive statistics characterizing these were calculated for the seasonal window as described in the Material and methods section. (Abbreviations: Max. depth — maximum depth (m); bottom layer thickness (m); temperature (°C); TN — total nitrogen (μM); TP — total phosphorus (μM); Surf — surface water samples; Bot — bottom water samples; AOU — Apparent Oxygen Utilization; Freq. — frequency). Region Site Max. depth # of profiles # of bottom oxygen samples Bottom layer thikness Temperature TN TP Bottom AOU Freq. of stratification (%) Freq. of hypoxia (%) Surf Bot Surf Bot Surf Bot Gulf of Bothnia U-5 Uudenkaarlepyyn 23 551 550 10.4 11.6 10.2 33.4 31.4 0.7 0.6 1.1 16.5 0.2 U-6 Uudenkaarlepyyn 15 103 99 7.6 14 12.3 40.1 27.8 0.9 0.6 1.1 40.8 4.9 Pome 115 Preiviikinlahti 26 277 274 9.8 14.7 11 20.6 18.1 0.4 0.4 2.3 36.8 4.0 Finnish Archipelago Hala N 22 114 114 1.3 14.4 9.3 38 50.8 1.1 1.6 – 32.5 48.3 Kamsholmsfjärden 19 178 176 2.5 17.7 8.4 27.8 50.9 0.9 7.6 10.5 89.9 80.3 Pala 47 223 223 18.5 17.6 12.7 30.2 31.7 1 1.3 4.5 52.9 3.1 Turm 290 Kuparivuori 25 83 82 1.2 15.7 9.5 30.5 39.7 1 1.4 5.6 54.2 22.9 Uki 245 Vähä-Seikomaa 26 1007 1002 10.5 13.7 12.5 28.7 29 1.2 1.6 3 17.8 4.2 Gulf of Finland Orrenkylänselkä 34 356 354 10.1 16.3 10.6 40.2 35.4 1.9 3 4.9 61.0 4.8 Skatafjärden 28 90 90 3.2 16.4 8.9 25.6 27.9 0.9 2 4.5 88.9 2.2 Suomenl Varissaari 17 193 193 2.1 15.9 10.9 34.5 30.9 1.1 1.6 3.5 65.8 2.6 Svartbäckinselkä 42 267 265 9.7 15.7 7.4 29.3 29.4 1.2 1.9 4.7 75.3 1.5 UUS-18 Sandöfjärden 31 301 301 8 15.9 8.7 26.7 34.5 1.1 4.4 7.2 71.1 38.5 Stockholm Archipelago Blomskär 27 153 136 2.9 13.8 5.2 49.5 52.8 2 5.4 11 90.2 72.6 Kanholmsfjärden 117 164 135 17.4 13.7 5.4 20.4 34.6 0.6 4.8 10.3 79.9 59.2 Karantänbojen 22 157 153 4.1 13.4 6.1 56.2 57.4 2.2 4.6 9.6 91.7 59.9 Solöfjärden 47 357 312 14 13.4 7.5 39.4 32.3 1.4 2.4 6.5 84.3 16.8 Vaxholmsfjärden 29 240 226 5.3 14 8.9 40.6 50 1.5 3.9 8.3 72.1 61.3 West of Gotland Basin Blankaholm 24 28 28 2.4 15.3 5.9 29.8 33.7 0.9 5.4 9.4 75.0 46.4 Bråvik 33 70 69 11.1 16.7 11.1 36 29.9 1.1 1.9 5.1 77.1 4.3 Västervik 64 90 89 22.2 15.9 4.8 30.5 50.6 0.9 5.4 9.3 83.3 45.6 Västrum 17 28 28 1.4 15.3 7.5 32 45.6 1.1 9 9.4 78.6 71.4 Belt Sea Aabenraa Fjord 35 235 235 5.1 16.2 11 27.8 34.8 1.4 4.5 7.3 98.3 69.4 Det Sydfynske Øhav 40 821 808 15 15.5 13.6 22.1 27.4 0.9 2.3 3.5 64.2 28.6 Eckernförder Bucht 31 80 72 5.2 15.5 11.6 21.3 26.9 1.2 4.1 7.8 82.5 73.8 Flensborg Fjord 31 345 343 7.7 16.2 11.1 27.4 40.6 1.6 5.4 7.6 91.6 69.6 Horsens Fjord 23 497 489 11.8 15.2 14.5 28.4 28.3 1.8 2 2.4 63.2 6.4 Århus Bugt 18 333 333 1.7 15.1 13 15.9 17.9 0.8 1.5 4.6 95.8 13.2 Kattegat and Öresund Hevring Bugt 10 151 151 1.1 14.6 14 16.4 17.5 0.8 1.2 2.2 78.1 2.7 Laholmsbugten 28 127 123 11.3 16.4 13 20.5 20.3 0.5 0.9 3.7 82.7 16.5 Middelgrund 19 198 198 2.2 14.9 12.5 19.5 21 0.6 1.1 4.2 95.0 7.1 Skälderviken 29 98 93 14.2 16.5 13.9 25 21.9 0.6 1.1 2.8 79.6 10.2 Valö 24 74 72 2.6 16.1 13.5 18.1 19.7 0.6 1.1 3.1 90.5 4.1 192A.M.Caballero-Alfonsoetal./JournalofMarineSystems141(2015)190–199
  4. 4. 3.1. Gulf of Bothnia region Three sites were investigated in this region (U-5 Uudenkaarlepyyn, U-6 Uudenkaarlepyyn and Pome 115 Preiviikinlahti); two of these are geographically close but have different nutrient levels and frequency of stratification (Table 1). Pome 115 Preiviikinlahti is a relatively deep site (26 m) with temperature stratification of ~4 °C separating a rela- tively large volume of bottom water. Compared to the other sites frequencies of stratification and hypoxia were both relatively low. The three sites had no clear distinctive trends in oxygen conditions, temper- ature, nutrient levels or stratification patterns, but there were strong interannual variations in temperature and frequency of stratification Fig. 1. Maps summarizing the trends for the bottom oxygen concentrations, AOU, temperature, frequency of stratification, TN and TP. The regions are grouped as: 1) Gulf of Bothnia, 2) Finnish Archipelago and 3) Gulf of Finland, 4) Stockholm Archipelago, 5) West Gotland Basin, 6) Belt Sea and 7) Kattegat and Öresund. Increasing and decreasing trends are shown with upward and downward facing triangles, green or red colors indicating improving or worsening conditions, and open and filled triangles signify non-significant and significant trends, respectively. 193A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  5. 5. (Fig. 2). However, Pome 115 Preiviikinlahti experienced a period with low oxygen concentrations in the 1980s, but these low concentrations could not be linked to any of the potential explanatory variables (Table 2). Temperature was important in explaining trends in oxygen conditions at the two Uudenkaarlepyyn sites. For U-6 Uudenkaarlypyyn changing stratification pattern was also important (Table 2), whereas this factor was not significant at U-5 Uudenkaarlepyyn that generally had a higher mixing frequency (Table 1). 3.2. Finnish Archipelago region This region includes five sites (Hala N, Kamsholmsfjärden, Pala, Turm 290 Kuparivuori and Uki 245 Vähä-Seikomaa) located along the inner coastal archipelago with relatively high nutrient levels compared to the other sites (Table 1). Overall, the frequency of stratification aver- aged 44%, but there were large differences in stratification between sites. Temperature differences between surface and bottom were large at all sites except Uki 245 Vähä-Seikomaa, and bottom water tempera- tures have been increasing for the last two decades (Fig. 3B). Frequency of hypoxia was even more variable ranging from 3.1% to 80.3% with an average of 31.8%. Three sites had a small bottom water volume and these three sites were also the sites with the highest frequency of hypoxia. There were no distinctive trends in the variables (most were not signif- icant, Fig. 1), although there were large interannual variations (Fig. 3). Significant correlations were obtained between the bottom oxygen con- centration and the bottom temperature (Table 2). 3.3. Gulf of Finland region Five sites were investigated in this region (Orrenkylänselkä, Skatafjärden, Suomenl Varissaari, Svartbäckinselkä and UUS-18 Sandöfjärden) and all of them were stratified by temperature through- out most of the summer period (Table 1). Stratification patterns varied substantially between years. Temperature differences were large sepa- rating a cold bottom water mass (7–11 °C) of several meters from a warmer surface layer (~16 °C). The last two decades have generally been warmer. Nutrient levels were relatively high and did not change over the years (Fig. 3C). Despite strong stratification the frequency of hypoxia was low, except for UUS-18 Sandöfjärden (Table 1). This site is a semi-enclosed embayment where bottom water ventilation could be low. Oxygen concentrations correlated significantly with tempera- ture and/or nutrient concentrations at the five sites, displaying worsen- ing oxygen conditions with increasing temperature and nutrients (Table 2). 0 1 2 3 4 5 6 70 2 4 6 8 10 12 AOU(mg/l) BottomOxygen(mg/l)Bottomtemperature(°C) U-5 Uudenkaarlepyyn Bottom oxygen Pome 115 Preiviikinlahti Bottom oxygen U-5 Uudenkaarlepyyn AOU Pome 115 Preiviikinlahti AOU A 0 10 20 30 40 50 60 70 80 90 100 0 2 4 6 8 10 12 14 16 18 20 Frequencyofstratification(%) U-5 Uudenkaarlepyyn Bottom temperature Pome 115 Preiviikinlahti Bottom temperature U-5 Uudenkaarlepyyn Freq. of stratification Pome 115 Preiviikinlahti Freq. of stratification B 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 0 10 20 30 40 50 60 1960 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 2002 2005 2008 2011 TP(µM) TN(µM) Year U-5 Uudenkaarlepyyn TN Pome 115 Preiviikinlahti TN U-5 Uudenkaarlepyyn TP Pome 115 Preiviikinlahti TP C Fig. 2. Long-term trends in the Gulf of Bothnia exemplified by two sites. A: dissolved bottom oxygen concentrations and Apparent Oxygen Utilization; B: bottom temperature and frequency of stratifications; C: surface TN and TP. Yearly seasonal means were obtained from the GLM approach. BottomOxygen(mg/l)Bottomtemperature(°C) TP(µM) TN(µM) 0 2 4 6 8 10 120 1 2 3 4 5 6 7 8 9 AOU(mg/l) Kamsholmsfjärden Bottom oxygen Orrenkylänselkä Bottom oxygen Kamsholmsfjärden AOU Orrenkylänselkä AOU A 0 10 20 30 40 50 60 70 80 90 100 0 2 4 6 8 10 12 14 16 Frequencyofstratification(%) Kamsholmsfjärden Bottom temperature Orrenkylänselkä Bottom temperature Kamsholmsfjärden Frequency of stratification Orrenkylänselkä Frequency of stratification B 0 1 2 3 4 5 6 7 0 10 20 30 40 50 60 70 80 1960 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 2002 2005 2008 2011 Year Kamsholmsfjärden TN Orrenkynlänselkä TN Kamsholmsfjärden TP Orrenkynlänselkä TP C Fig. 3. Long-term trends in the Finnish Archipelago and the Gulf of Finland exemplified by two sites. Details as for Fig. 2. 194 A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  6. 6. 3.4. Stockholm Archipelago region In this region five sites were analyzed (Blomskär, Kanholmsfjärden, Karantänbojen, Sölofjärden and Vaxholmsfjärden). All sites were relatively deep with Kanholmsfjärden as the deepest investigated of all sites (Table 1). The bottom water volume below the pycnocline was relatively large; however, all sites were hypoxic for most of the summer period. Nutrient levels in the Stockholm Archipelago were the highest of all sites. Stratification was strong and driven by both salinity and temperature differences. Oxygen concentrations have in- creased and nutrient concentrations have decreased over time (Figs. 1, 4A,C). The bottom water has generally warmed and the frequency of stratification has decreased in Vaxholmsfjärden (Fig. 4B), but this pat- tern is not consistent at all sites. Bottom oxygen concentrations were significantly correlated with nutrients at Karantänbojen, Sölofjärden and Vaxholmsfjärden, as expected, whereas oxygen conditions were related to frequency of stratification in Kanholmsfjärden and positively related to temperature in Vaxholmsfjärden. Whereas the positive correlation to temperature in Vaxholmsfjärden could be an artifact from nutrients showing similar trends, the positive correla- tion to frequency of stratification in Kanholmsfjärden is somewhat more surprising. Blomskär, which is an isolated branch in the Stockholm Archipelago, had a significant decreasing trend of bottom oxygen concentration with time, as opposed to all the other sites displaying increasing trend (Fig. 1). The oxygen trend at Blomskär was not significantly correlated to any of the explanatory variables (Table 2). 3.5. West Gotland Basin region Four sites were investigated (Blankaholm, Bråvik, Västervik and Västrum) with depths between 17 and 64 m; the two deepest sites also having a high bottom water thickness (Table 1). Nutrient levels were moderate compared to the other sites, whereas the frequency of stratification was high. The frequency of hypoxia was high at all sites, except Bråvik which is dominated by the large Motala River. Freshwater inputs to the other sites are relatively smaller. The monitoring data set from this region is relatively weak compared to other regions with fewer years of data. Consequently, it is more difficult to assess the trends and correlate oxygen conditions with other factors. Nevertheless, oxy- gen conditions have improved at Blankaholm and Västervik (Figs. 1, 4C) and these trends correlated significantly with TP levels and temper- ature (Table 2). BottomOxygen(mg/l)Bottomtemperature(°C)TN(µM) 0 2 4 6 8 10 120 1 2 3 4 5 6 7 8 9 AOU(mg/l) Vaxholmsfjärden Bottom oxygen Västervik Bottom oxygen Vaxholmsfjärden AOU Västervik AOU A 0 10 20 30 40 50 60 70 80 90 100 0 2 4 6 8 10 12 14 16 Frequencyofstratification(%) Vaxholmsfjärden Bottom temperature Västervik Bottom temperature Vaxholmsfjärden Frequency of stratification Västervik Frequency of stratification B 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 0 10 20 30 40 50 60 70 1960 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 2002 2005 2008 2011 TP(µM) Year Vaxholmsfjärden TN Västervik TN Vaxholmsfjärden TP Västervik TP C Fig. 4. Long-term trends in the Stockholm Archipelago and West Gotland Basin exemplified by two sites. Details as for Fig. 2. BottomOxygen(mg/l)Bottomtemperature(°C)TN(µM) 0 1 2 3 4 5 6 7 8 9 100 1 2 3 4 5 6 7 8 9 10 AOU(mg/l) Aabenraa Fjord Bottom oxygen Horsens Fjord Bottom oxygen Aabenraa Fjord AOU Horsens Fjord AOU A 0 10 20 30 40 50 60 70 80 90 100 0 2 4 6 8 10 12 14 16 18 Frequencyofstratification(%) Aabenraa Fjord Bottom temperature Horsens Fjord Bottom temperature Aabenraa Fjord Frequency of stratification Horsens Fjord Frequency of stratification B 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 0 10 20 30 40 50 60 70 80 90 100 1960 1963 1966 1969 1972 1975 1978 1981 1984 1987 1990 1993 1996 1999 2002 2005 2008 2011 TP(µM) Year Aabenraa Fjord TN Horsens Fjord TN Aabenraa Fjord TP Horsens Fjord TP C Fig. 5. Long-term trends in the Danish strait exemplified by two sites. Details as for Fig. 2. 195A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  7. 7. 3.6. Belt Sea region The Belt Sea region includes 6 sites (Aabenraa Fjord, Det Sydfynske Øhav, Eckernförder Bucht, Flensborg Fjord, Horsens Fjord and Århus Bugt) with depths ranging from 18 to 40 m (Table 1). It is a region (Table 1) with a relatively high frequency of stratification (83%), due to the location of a halocline around 15–25 m. Nutrient levels are relatively low, compared to sites in the more brackish part of the Baltic Sea, but there are differences among sites in the Belt Sea region associ- ated with proximity to land-based nutrient sources. Three of the sites in the Belt Sea region (Aabenraa Fjord, Eckernförder Bucht and Flensborg Fjord) have high frequencies of hypoxia (~70%) and these sites are connected to the Little Belt where bottom water ventilation is lowest. The three other sites display more episodic events of hypoxia. Despite decreases in both nitrogen and phosphorus concentrations over the last many decades (Figs. 1, 5C) oxygen conditions have not generally improved, although there is a tendency for improvement at some sites in the most recent years (Fig. 5A). As a consequence, a general pattern of declining nutrients associated with improving oxygen conditions was not found, and only Horsens Fjord and Århus Bugt showed signifi- cant correlations (Table 2). The lack of significant correlations in this region could be due to the lack of variability in oxygen concentrations over time making the identification of such relationships difficult. 3.7. Kattegat and Öresund region Five sites are included in this region (Hevring Bugt, Laholmsbugten, Middelgrund, Skälderviken and Valö); the three deepest of these located on the Swedish coast. The sites are generally shallower than those in other regions and the thickness of the bottom layer depends on the permanent halocline in the Kattegat, which is typically found around 15–20 m depth (Andersson and Rydberg, 1988). However, windy conditions mix down the surface layer and may tilt the halocline. The sites therefore have a high frequency of stratification (Table 1). The sites in this region have the lowest nutrient levels of all Baltic Sea coastal sites, because they are more influenced by water exchanges with the North Sea where both TN and TP levels are lower than in the Baltic. The frequency of hypoxia is generally low and these events have an episodic nature (Conley et al., 2011). In this region oxygen concentra- tions have displayed non-uniform trends (Fig. 1), but major changes have not been observed despite decreasing nitrogen levels (Fig. 5). Due to the episodic nature of low oxygen conditions and the lack of large changes in oxygen conditions no significant correlations were found between oxygen concentration and explanatory variables (Table 2). 3.8. Comparison of sites across regions The 33 coastal sites were exposed to large differences in physical forcing and behaved differently to nutrient enrichment. We examined the effect of stratification patterns on hypoxia by plotting AOU versus the frequency of stratification and thickness of bottom layer (Fig. 6). Oxygen consumption was clearly related to frequency of stratification with hypoxia rarely occurring at sites that were stratified less than 50% of the seasonal window (Table 1). There were regional differences in AOU versus frequency of stratification. Sites in Kattegat, Öresund, Belt Sea and Gulf of Finland generally had lower AOU compared to sites in archipelagic regions (Finnish Archipelago, Stockholm Archipelago and West Gotland Basin) with the same frequency of stratification (Fig. 6A). The relationship between AOU and bottom water thickness was more complex, although at some sites it appears as if oxygen consumption could be higher if the bottom water volume below the pycnocline was relatively low (Fig. 6B). Table 2 Spearman correlations between trends of oxygen concentrations and physical, chemical and biological conditions believed to influence oxygen conditions. The significance of the correlations is indicated as *: p b 0.05; **: p b 0.01; ***: p b 0.001. Trends used for the correlations are shown for U-5 Uudenkaarlepyyn and Pome 115 Preiviikinlahti (Fig. 1), Kamsholmsfjärden and Orrenkylänselkä (Fig. 2), Vaxholmsfjärden and Västervik (Fig. 3), and Aabenraa Fjord and Horsens Fjord (Fig. 4). The symbol ‘–’ indicates that there were no or too few annual values to calculate and test the correlation. Region Site Surface chla Bottom temperature Frequency of stratification Surface TN Surface TP Gulf of Bothnia U-5 Uudenkaarlepyyn 0.5 −0.83*** −0.02 0.24 −0.17 U-6 Uudenkaarlepyyn −0.5 −0.55*** −0.7*** 0.06 0.22 Pome 115 Preiviikinlahti – −0.1 0.14 0.36 −0.09 Finnish Archipelago Hala N – −0.47*** 0.24 −0.01 −0.32 Kamsholmsfjärden – −0.1 −0.19 −0.14 0.03 Pala −0.38 −0.62*** 0.1 0.09 0.17 Turm 290 Kuparivuori – −0.54*** 0.03 −0.25 −0.03 Uki 245 Vähä-Seikomaa – −0.41** 0.22 0.12 0.09 Gulf of Finland Orrenkylänselkä −0.5 −0.07 0.00 −0.21 −0.48*** Skatafjärden – −0.73*** 0.03 −0.38** −0.33* Suomenl Varissaari – −0.69*** −0.05 −0.16 −0.1 Svartbäckinselkä – −0.29 0.15 −0.15 −0.34** UUS-18 Sandöfjärden – −0.05 0.37 −0.61*** −0.68*** Stockholm Archipelago Blomskär −0.4 −0.25 0.18 −0.11 0.07 Kanholmsfjärden −0.2 0.00 0.34** 0.15 0.02 Karantänbojen −0.5 −0.04 0.19 −0.44*** −0.65*** Solöfjärden −0.4 −0.08 −0.02 −0.48*** −0.45*** Vaxholmsfjärden 0.3 0.5*** −0.1 −0.36** −0.47*** West of Gotland Basin Blankaholm 0.04 0.24 −0.39 0.24 −0.61** Bråvik – −0.6** 0.13 −0.23 −0.21 Västervik −0.09 −0.08 0.02 0.12 −0.31 Västrum −0.25 0.42 0.06 0.07 −0.33 Belt Sea Aabenraa Fjord 0.11 0.31 −0.32 0.21 0.3 Det Sydfynske Øhav −0.06 −0.17 −0.13 −0.24 −0.02 Eckernförder Bucht – 0.07 −0.05 0.28 0.05 Flensborg Fjord 0.11 0.18 −0.23 0.36 0.15 Horsens Fjord −0.28 −0.23 −0.41** −0.36** −0.16 Århus Bugt −0.22 −0.04 −0.1 −0.63*** −0.46* Kattegat and Öresund Hevring Bugt 0.12 −0.06 −0.11 −0.45 −0.21 Laholmsbugten −0.17 −0.16 −0.16 0.13 −0.01 Middelgrund −0.62 0.14 0.07 −0.33 −0.36 Skälderviken 0.05 0.03 0.24 0.11 0.05 Valö 0.002 −0.26 −0.05 0.003 0.38 196 A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  8. 8. 4. Discussion 4.1. Overall trends Reports of hypoxia in coastal marine systems have increased during the last few decades with the primary cause of low oxygen conditions linked to increases in nutrient loads (Conley et al., 2011; Diaz and Rosenberg, 2008; Rabalais et al., 2014). There are numerous studies showing that eutrophication is promoting the expansion, duration, and intensity of hypoxic events (Diaz and Rosenberg, 2008; Kemp et al., 2009; Rabalais and Gilbert, 2008). Policies and measures have been im- plemented to reduce the input of nutrients to coastal ecosystems (Duarte et al., in press) and in the Baltic Sea as well (HELCOM, 2007). The coastal waters around Denmark were one of the first areas to document significant decreases in nutrient concentrations on a large regional scale resulting from an active management strategy to reduce nutrients from both diffuse and point sources (Carstensen et al., 2006). Our analysis of Baltic Sea coastal ecosystems shows that many countries in the watershed have reduced their nutrient loads resulting in lower nutrient concentrations in coastal waters (Fig. 1). However, our results also show that improvements in bottom water dissolved oxygen con- centrations are not always observed (Fig. 1). From the 33 evaluated sites only 11 show an increasing trend in dissolved oxygen of bottom waters with time and only the Stockholm Archipelago had consistent trends. However, the vast majority of sites continue to worsen, especially along the Danish and Finnish coasts (Figs. 1, 3 and 5), in spite of remedi- ation efforts to reduce nutrients. From a larger perspective, only a small percentage (~4%) of 400 sites globally suffering hypoxia have shown trends of increasing bottom water oxygen concentrations (Diaz and Rosenberg, 2008). The recovery of coastal and estuarine ecosystems also takes place in a context of global climate change (Duarte et al., 2009) with dissolved oxygen in oceanic oxygen minimum zones decreasing due to changes associated with global warming (Stramma et al., 2008). Warming plays an important role by reducing the solubility of oxygen and in- creasing respiration. It also alters wind patterns, rainfall and runoff affecting hydrological processes. Temperature increases stratification and a stronger pycnocline reduces ventilation through vertical mixing promoting bottom water oxygen depletion (Hagy et al., 2004). Increases in bottom water temperature were observed in the Finnish Archipelago and along the Danish coast (Figs. 1, 3 and 5) where increases in AOU were also evident. In addition, coastal ecosystems are more vulnerable to nutrient loads with temperature increases (Justić et al., 1996; Kemp et al., 2005) as seen by us in the Bothnian Bay (Table 2, Fig. 2). Warming can induce changes in periodical biological processes such as the timing of the spring bloom and overall productivity (Nixon, 2009). Wind speed and wind direction affect the efficiency of mixing between surface and bottom waters, thus changing the ventilation of bottom waters. Relationships between temperature increases, decreases in wind speed and increases in oxygen demand have been observed in the Narragansett Bay and Long Island Sound (Nixon, 2009) and Danish coastal waters (Conley et al., 2007). In addition, climate change will also modify rainfall patterns and snow melt generally increasing water discharges from land (freshwater, pollutants and nutrients) into Baltic coastal ecosystems (Meier et al., 2012). Although climate change will affect the wind field (IPCC, 2007), we were not able to evaluate this effect on trends in bottom water dissolved oxygen. 4.2. Differences between systems The recovery of bottom water oxygen concentrations following nutrient reduction measures is rare with increases in hypoxia continu- ing to be observed globally (Conley et al., 2011; Diaz and Rosenberg, 2008; Gilbert et al., 2010). Our regional evaluation of coastal ecosystems in the Baltic Sea has shown that different regions are responding sepa- rately to reductions in nutrients. Area-specific ecological responses to coastal eutrophication have been previously observed in the Baltic Sea (Carstensen et al., 2011; Rönnberg and Bonsdorff, 2004). In the concep- tual model of the coastal eutrophication problem by Cloern (2001) it is explicitly recognized that system-specific attributes modulate the responses to nutrient enrichment, leading to large differences among coastal systems in their sensitivity. Our response parameter used is bottom water hypoxia, whereas there are a complex suite of direct and indirect responses to coastal eutrophication including changes in water transparency, distribution of bottom vegetation, in nutrient cycling processes, phytoplankton community composition, and changes in ecosystem functions. The result is a wide range of estuary-specific responses to the effects of nutrient loading on coastal eutrophication and hypoxia (Cloern, 2001). The coastal zone of the Baltic has a complex topography with numerous islands and many basins separated by shallow sills resulting in many distinct isolated basins. The coastline of the Western Gotland Basin, including the Stockholm Archipelago, and Gulf of Finland, includ- ing the Finnish Archipelago, is more prone to hypoxia than other parts of the more unrestricted shoreline (Conley et al., 2011). These systems become thermally stratified during the summer months. Because the complex topography reduces circulation and increases the residence time of bottom waters, these ecosystems are consequently more sensi- tive to enhanced nutrient inputs from land and regularly experience hypoxia. Our results confirm these patterns. Stratification is a precursor for hypoxia to develop, but even perma- nently stratified coastal systems can remain normoxic provided that the bottom waters are sufficiently exchanged through bottom water venti- lation. Hypoxia may also develop in coastal systems that stratify for short periods only, provided that the bottom layer is so thin that respi- ratory processes, mainly from the sediments, consume all oxygen during such short-lived events. Our results show that it is difficult to encapsulate the complex and highly dynamical physical processes governing oxygen supply by means of monitoring data. Such processes can be described more simply in open water systems, where changes in oxygen conditions are much slower (Conley et al., 2007; Carstensen et al., 2014). 0 2 4 6 8 10 12 0 20 40 60 80 100 AOU(mg/l) Gulf of Bothnia Finnish Archipelago Gulf of Finland Stockholm Archipelago West Gotland Basin Belt Sea Kattegat & Öresund A 0 2 4 6 8 10 12 0 5 10 15 20 25 AOU(mg/l) Bottom layer thickness (m) B Frequency of stratification (%) Fig. 6. Relationships between the AOU and the frequency of stratification (A) and thick- ness of the bottom layer (B). 197A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  9. 9. Oxygen depletion at a site might be imported by the advective trans- port of saltier, low oxygen bottom water from an adjacent body; this could be the case of what has been observed in the present study at Horsens Fjord (Danish Straits) and Kanholmsfjärden (Stockholm Archipelago). These intrusions are characterized by nutrient-rich low- oxygen waters coming from the Belt Sea (Danish Straits) or from the bottom waters of the Baltic Proper. 4.3. Potential regime shifts Bottom water hypoxia is not only a particularly severe disturbance on ecosystems because it causes death of biota, changes in the habitat of living resources, but also the biogeochemical processes that control nutrient concentrations in the water column (Conley et al., 2009a). Nu- merous studies in other coastal marine ecosystems have demonstrated that repeated hypoxic events can help to sustain future hypoxic condi- tions (Hagy et al., 2004; Kemp et al., 2005, 2009; Turner et al., 2008). These changes suggest that a regime shift occurs in coastal marine eco- systems affected by large-scale hypoxia (Conley et al., 2007). Regime shifts are often rapid transitions that occur in an ecosystem state with the recovery of ecosystems delayed by internal feed-back mechanisms (Scheffer et al., 2001). The recovery of ecosystems from hypoxia may occur only after long periods of time (Diaz, 2001; Galloway et al., 2008; Kemp et al., 2009) or with further reductions in nutrient inputs. Perhaps the slow response of the coastal systems in the Baltic Sea to re- duced nutrient inputs is due to feed-back mechanisms such as en- hanced P release (Conley et al., 2009a, 2009b) and decreases in denitrification from sediments (Testa and Kemp, 2012) that keep eco- systems hypoxic. In addition, it may also take time for nutrients that have accumulated in the sediments during the years of excessive nutri- ent loading to be buried out of the reactive zone or flushed out of the ecosystem. Previous studies have shown that a trend reversal is possible when reducing nutrient loads (Carstensen et al., 2006, 2011; Nixon, 2009; Norkko et al., 2012). What is clear from our results is that there are many coastal systems with decreasing nutrients, but not many showing decreasing hypoxia. However, it is probable that the ecosystem charac- teristics, composition, components and biogeochemical processes have changed. Most coastal marine ecosystems are impacted by multiple fac- tors that act to stress the ecosystem (Halpern et al., 2008; Micheli et al., 2013). The removal of one pressure alone, such as nutrient reduction, may prove insufficient for ecosystem recovery when other pressures (e.g., overfishing, dredging, climate change, or pollution) have not been removed (Duarte et al., in press). The classification of anthropo- genic pressures shows that the highest cumulative impacts over the Baltic Sea area were in the southern and south-western areas and in the Gulf of Finland where hypoxia is still increasing and the lowest index values found in the Gulf of Bothnia (Korpinen et al., 2012). 4.4. Implications for ecosystem management Reductions in nutrient loadings to coastal marine ecosystems are the only realistic measure to improve ecosystem health and reduce hypoxia (Conley et al., 2009b). However, confident predictions of recovery tar- gets with nutrient reductions are problematic due to the unique behav- ior of ecosystems during the recovery process (Carstensen et al., 2011). Unexpected hypoxia mitigation is proposed to have occurred with the spread of an invasive species, e.g. the worm Marenzelleria spp. (Norkko et al., 2012). Their bioirrigation activities acted as a driver of ecological change affecting sediment P dynamics in the Stockholm Archipelago, oxygenating the sediments and reducing nutrient leakage facilitating the recovery of hypoxia. Other currently unidentified nonlin- ear interactions and feedbacks may play a positive role in ecosystem remediation if nutrient reductions are continued. 5. Conclusion The important lesson learned is that the recovery of coastal marine ecosystems from hypoxia with nutrient reductions is indeed possible (Conley et al., 2011; Diaz and Rosenberg, 2008; this study). However, nutrient reductions are not always enough and restoration efforts should include actions to catalyze recovery and reduce the thresholds to recovery (Duarte et al., in press). In addition, despite the multiple stressors driving hypoxia, especially the global rise in temperatures, our results demonstrate that managing nutrients can create positive feedbacks for oxygen recovery to occur. In the absence of nutrient reductions, there will not be recovery from hypoxia in coastal marine ecosystems. Acknowledgments This paper is a contribution from the Multistressors Project funded by a FORMAS Strong Research Environment and the COCOA Project funded under the BONUS program. References Andersson, L., Rydberg, L., 1988. Trends in nutrient and oxygen conditions within the Kattegat: effects of local nutrient supply. Estuar. Coast. Shelf Sci. 26, 559–579. Bianchi, T.S., DiMarco, S.F., Cowan Jr., J.H., Hetland, R.D., Chapman, P., Day, J.W., Allison, M.A., 2010. The science of hypoxia in the Northern Gulf of Mexico: a review. Sci. Total Environ. 408, 1471–1484. Carstensen, J., Conley, D.J., Andersen, J.H., Ærtebjerg, G., 2006. Coastal eutrophication and trend reversal: a Danish case study. Limnol. Oceanogr. 51, 398–408. Carstensen, J., Sánchez-Camacho, M., Duarte, C.M., Krause-Jensen, D., Marbà, N., 2011. Connecting the dots: responses of coastal ecosystems to changing nutrient concen- trations. Environ. Sci. Technol. 45, 9122–9132. Carstensen, J., Andersen, J.H., Gustafsson, B.G., Conley, D.J., 2014. Deoxygenation of the Baltic Sea during the last century. Proc. Natl. Acad. Sci. 111, vol. 15, 5628–5633. Cloern, J.E., 2001. Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 210, 223–253. Conley, D.J., Carstensen, J., Ærtebjerg, G., Christensen, P.B., Dalsgaard, W., Hansen, J.L.S., Josefson, A.B., 2007. Long-term changes and impacts of hypoxia in Danish coastal waters. Ecol. Appl. 17, S165–S184. Conley, D.J., Björck, S., Bonsdorff, E., Carstensen, J., Destouni, G., Gustafsson, B., Hiatanen, S., Kortekaas, K., Huosa, H., Meier, H.E.M., Müller-Karulis, B., Nordberg, K., Norkko, A., Nürnberg, G., Pitkänen, H., Rabalais, N.N., Rosenberg, R., Savchuk, O.P., Slomp, C.P., Voss, M., Wulff, F., Zillén, L., 2009a. Hypoxia-related processes in the Baltic Sea. Envi- ron. Sci. Technol. 43, 3412–3420. Conley, D.J., Bonsforff, E., Carstensen, J., Destouni, G., Gustafsson, B.G., Rabalais, N., Voss, M., Zillén, L., 2009b. Tacking hypoxia in the Baltic Sea: is engineering a solution? Environ. Sci. Technol. 43, 3407–3411. Conley, D.J., Carstensen, J., Aigars, J., Axe, P., Bonsdorff, E., Eremina, T., Haahti, B.-M., Humborg, C., Jonsson, P., Kotta, J., Lännegren, C., Larsson, U., Maximov, A., Rodriguez Medina, M., Lysiak-Pastuszak, E., Remeikaite-Nikiene, N., Walve, J., Wilhelms, S., Zillén, L., 2011. Hypoxia is increasing in the coastal zone of the Baltic Sea. Environ. Sci. Technol. 45, 6777–6783. Diaz, R.J., 2001. Overview of hypoxia around the world. J. Environ. Qual. 30, 275–281. Diaz, R.J., Rosenberg, R., 2008. Spreading dead zones and consequences for marine ecosys- tems. Science 321, 926–929. Duarte, C.M., Conley, D.J., Carstensen, J., Sánchez-Camacho, M., 2009. Return to Neverland: shifting baselines affect eutrophication restoration targets. Estuar. Coasts 32, 29–36. Duarte, C.M., Borja, A., Carstensen, J., Elliott, M., Krause-Jensen, D., Marbà, N., 2014. Para- digms in the recovery of estuarine and coastal ecosystems. Estuar. Coasts. http://dx. Galloway, J.N., Townsend, A.R., Erisman, J.W., Bekunda, M., Cai, Z., Freney, J.R., Martinelli, L.A., Seitzinger, S.P., Sutton, M.A., 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892. Gilbert, D., Rabalais, N.N., Diaz, R.J., Zhang, J., 2010. Evidence for greater oxygen decline rates in the coastal ocean then in the open ocean. Biogeosciences 7, 2283–2296. Gustafsson, B.G., Schenk, F., Blenckner, T., Eilola, K., Meier, H.E.M., Müller-Karulis, B., Neumann, T., Ruoho-Airola, T., Savchik, O.P., Zorita, E., 2012. Reconstructing the development of Baltic Sea eutrophication 1850–2006. Ambio 41, 534–548. Hagy, J.D., Boyton, W.R., Keefe, C.W., Wood, K.V., 2004. Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow. Estuaries 27, 634–658. Halpern, B.S., McLeod, K.L., Rosenberg, A.A., Crowder, L.B., 2008. Managing for cumulative impacts in ecosystem-based management through ocean zoning. Ocean Coast. Manag. 51, 203–211. HELCOM, 2007. The Baltic Sea action plan; Helsinki, Finland. Hetland, R.D., Di Marco, S.F., 2008. How does the character of oxygen demand control the structure of hypoxia in the Texas–Louisiana continental shelf? J. Mar. Syst. 70, 49–62. 198 A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199
  10. 10. IPCC (Intergovernmental Panel on Climate Change, Climate Change), 2007. The Physical Science Basis, Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge Univ. Press, New York. Justić, D., Rabalais, N.N., Turner, R.E., 1996. Effects of climate change on hypoxia in coastal waters: a doubled CO2 scenario for the northern Gulf of Mexico. Limnol. Oceanogr. 41, 992–1003. Karlson, K., Bonsdorff, E., Rosenberg, R., 2007. The impact of benthic macrofauna for nutrient fluxes from Baltic Sea sediments. Ambio 36, 161–167. Kemp, W.M., Boynton, W.R., Adoli, J.E., Boesch, D.F., Coicourt, W.C., Brush, G., Cornwell, J.C., Fisher, T.R., Gilbert, P.M., Hagy, J.D., Harding, L.W., Houde, E.D., Kimmel, D.G., Miller, W.D., Newell, R.I.E., Roman, M.R., Smith, E.M., Stevenson, J.C., 2005. Eutrophication of Chesapeake Bay: historical trends and ecological interactions. Mar. Ecol. Prog. Ser. 303, 1–29. Kemp, W.M., Testa, J.M., Conley, D.J., Gilbert, D., Hagy, J.D., 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6, 2985–3008. Korpinen, S., Meski, L., Andersen, J.H., Laamanen, M., 2012. Human pressures and their potential impact on the Baltic Sea ecosystem. Ecol. Indic. 15, 105–114. Limburg, K.E., Olson, C., Walther, Y., Dale, D., Slomp, C.P., Hoie, H., 2011. Tracking Baltic hypoxia and cod migration over millennia with natural tags. Proc. Natl. Acad. Sci. 108, E177–E182. Meier, H.E.M., Andersson, H.C., Arheimer, B., Bleckner, T., Chubarenko, B., Donnelly, C., Eilola, K., Gustafsson, B.G., Hansson, A., Jonathan, H., Höglund, A., Kuznetsov, I., MacKenzie, B.R., Müller-Karulis, B., Neumann, T., Niiranen, S., Piwowarczyk, J., Raudsepp, U., Reckermann, M., Ruoho.Airola, T., Savchuk, O.P., Schenk, F., Schimanke, S., Väli, G., Weslawski, J.-M., Zorita, E., 2012. Comparing reconstructed past variations and future projections of the Baltic Sea ecosystem-first results from multi-model ensemble simulations. Environ. Res. Lett. 7, 1–8. Micheli, F., Halpern, B.S., Walbridge, S., Ciriaco, S., Ferretti, F., Fraschetti, S., Lewison, R., Nykjaer, L., Rosenberg, A.A., 2013. Cumulative human impacts on Mediterranean and Black Sea marine ecosystems: assessing current pressures and opportunities. PLoS One. Nixon, S.W., 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41, 199–219. Nixon, S.W., 2009. Eutrophication and the macroscope. Hydrobiologia 629, 5–19. http:// Norkko, J., Reed, D.C., Timmermann, K., Norkko, A., Gustafsson, B.G., Slomp, C.P., Carstensen, J., Conley, D.J., 2012. A welcome can of worms? Hypoxia mitigation by an invasive species. Global Change Biol. 02513.x. Omstedt, A., Meuller, A., Nyberg, L., 1997. Interannual, seasonal and regional variations of precipitation and evaporation over the Baltic Sea. Ambio 26, 484–492. Perus, J., Bonsdorff, E., 2004. Long-term changes in macrozoobenthos in the Åland archipelago northern Baltic Sea. J. Sea Res. 52, 45–56. Rabalais, N.N., Gilbert, D., 2008. Distribution and consequences of hypoxia. In: Urban, E., Sundby, B., Malanotte-Rizzoli, P., Melillo, J.M. (Eds.), Watersheds, Bays and Bounded Seas. Island Press, Washington, DC, pp. 209–226. Rabalais, N.N., Diaz, R.J., Levin, L.A., Turner, R.E., Gilbert, D., Zhang, J., 2010. Dynamics and distribution of natural and human-caused hypoxia. Biogeosciences 7, 585–619. Rabalais, N.N., Cai, W.-J., Carstensen, J., Conley, D.J., Fry, B., Hu, X., Quinones-Rivera, Z., Rosenberg, R., Slomp, C.P., Turner, R.E., Voss, M., Wissel, B., Zhang, J., 2014. Eutrophication-driven deoxygenation in the coastal ocean. Oceanography 27, 66–77. Rönnberg, C., Bonsdorff, E., 2004. Baltic Sea eutrophication: area-specific ecological conse- quences. Hydrobiologia 514, 227–241. Scheffer, M., Carpenter, S., Foley, J.A., Folke, C., Walker, B., 2001. Catastrophic shifts in eco- systems. Nature 413, 591–596. Sohlenius, G., Emeis, K.-C., Andrén, E., Andrén, T., Kohly, A., 2001. Development of anoxia during the Holocene fresh-brackish water transition in the Baltic Sea. Mar. Geol. 177, 221–242. Steckbauer, A., Duarte, C.M., Carstensen, J., Vaquer-Sunyer, R., Conley, D.J., 2011. Ecosys- tem impacts of hypoxia: thresholds of hypoxia and pathways to recovery. Environ. Res. Lett. 6. Stramma, L., Johnson, G.C., Sprintall, J., Mohrholz, V., 2008. Expanding oxygen-minimum zones in the tropical oceans. Science 320, 655–658. Testa, J.M., Kemp, W.M., 2012. Hypoxia-induced shifts in nitrogen and phosphorus cycling in Chesapeake Bay. Limnol. Oceanogr. 57, 835–850. Turner, R.E., Rabalais, N.N., Justić, D., 2008. Gulf of Mexico hypoxia: alternate states and a legacy. Environ. Sci. Technol. 42, 2323–2327. Vallin, L., Nissling, A., Westin, L., 1999. Potential factors influencing reproductive success of Baltic cod, Gadus morhua: a review. Ambio 28, 92–99. Vaquer-Sunyer, R., Duarte, C.M., 2010. Sulfide exposure accelerates hypoxia-driven mor- tality. Limnol. Oceanogr. 55, 1075–1082. Wulff, F., Stigebrandt, A., Rahm, L., 1990. Nutrient dynamics of the Baltic Sea. Ambio 19, 126–133. Zillén, L., Conley, D.J., Andrén, T., Andrén, E., Björck, S., 2008. Past occurrence of hypoxia in the Baltic Sea and the role of climate variability, environmental change and human impact. Earth Sci. Rev. 91, 77–92. 199A.M. Caballero-Alfonso et al. / Journal of Marine Systems 141 (2015) 190–199