Oceanography and Marine Biology: an Annual Review 2002, 40, 427-489 © R. N. Gibson, Margaret Barnes and R. J. A. Atkinson, Editors Taylor & Francis
TEMPORAL AND SPATIAL LARGE-SCALE EFFECTS OF EUTROPHICATION AND OXYGEN DEFICIENCY ON BENTHIC FAUNA IN SCANDINAVIAN AND BALTIC WATERS - A REVIEW KARIN KARLSON,1 RUTGER ROSENBERG 1 & ERIK BONSDORFF 2 1
Department of Marine Ecology, Göteborg University, Kristineberg Marine Research Station, 450 34 Fiskebäckskil, SWEDEN e-mail:
[email protected],
[email protected] (corresponding author) 2 Environmental and Marine Biology, Åbo Akademi University, Akademigatan 1, 20 500 Åbo, FINLAND e-mail:
[email protected]
Abstract Eutrophication has been an increasing ecological threat during the past 50 yr in many Scandinavian and Baltic marine waters. Large sedimentary areas are seasonally, or more or less permanently, affected by hypoxia and/or anoxia with devastating effects on the benthic macrofauna in, for example, the Baltic Sea, the Belt Seas and Öresund between Denmark and Sweden, the Kattegat and the Skagerrak coast towards the North Sea. In this review figures for the input of nitrogen and phosphorus to different sea areas are presented, and in several cases also changes of nitrogen and phosphorus concentrations in the water. The nutrient input is related to production levels, and related to macrobenthic infauna. Changes of dominant benthic species, abundance and biomass are presented in relation to both changes in organic enrichment and hypoxia and/or anoxia in time and space. Since the 1950s-60s, the benthic faunal biomass has increased in the Gulf of Bothnia as a result of increased organic enrichment. In the Åland Archipelago, the number of benthic species decreased since the 1970s but abundance and biomass increased. Drifting algae at the sediment surface has also been an increasing problem. The changes were caused by increasing eutrophication. In the Finnish Archipelago Sea, large-scale eutrophication has resulted in periodic bottom water hypoxia and drifting algal mats with negative effects on benthic fauna. In the Gulf of Finland, the benthic fauna has been negatively affected by hypoxic bottom water below 70 m depth since the 1960s, but with a period of improved oxygen conditions during 1987-94. In the Baltic Proper, large sea-bed areas of 70 000-100 000 km2 below 70-80 m water depth have been more or less hypoxic and/or anoxic since the 1960s with no or reduced sediment-dwelling fauna. This process was a result of increased eutrophication and lack of larger inflows of oxygenated water from the Kattegat. Several coastal areas and larger basins in the southern Baltic (e.g. the Bornholm Basin, the Arkona Basin and the Kiel Bay), have, on occasions, been similarly negatively affected by hypoxic bottom water. Many sedimentary areas below -17 m in the Danish Belt Seas have been affected by seasonal hypoxia since the 1970s with negative consequences for the bottom fauna. On the Danish Kattegat coast, the benthic fauna in the Limfjord, the Manager fjord and the Roskilde fjord have been particularly negatively affected. In the southeast, open Kattegat, increased input of nutrients in combination with stratification
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have resulted in seasonal hypoxia since 1980 with negative effects on benthic animals and commercial fish species in most years. Several fjords on the Swedish and Norwegian Skagerrak coast have shown negative temporal trends in bottom water oxygen concentrations, and some of them lack benthic fauna in the deeper parts for several months or more. In this review the temporal development of bottom water hypoxia and/or anoxia is discussed and consequent possible losses of sediment-dwelling faunal biomass are roughly calculated. In total for the areas investigated, the worst years of hypoxia and/or anoxia combined may have reduced the benthic macrofaunal biomass by 3 million t. This loss is partly compensated by the biomass increase that has occurred in well-flushed organically enriched coastal areas. Tolerance of some Baltic species to hypoxia and/or anoxia is discussed and also their different strategies to cope with hypoxia and/or anoxia and H2 S.
Introduction Eutrophication in Scandinavian waters Excessive nutrient enrichment has been an increasing problem in Scandinavian waters for several decades (i.e. in the Baltic Sea, the Öresund and Belt areas between Denmark and Sweden, the Kattegat and the Skagerrak coast (Fig. 1)). Human activities have drastically increased the load of nutrients since the 1950s and increases may be as high as 4-fold for total N and about 8-fold for total phosphorus (Larsson et al. 1985, Rosenberg et al. 1990). Decreased transparency, changes in macroalgal distribution, increased amounts of drifting algal mats, harmful algal blooms and extension of laminated sediments (varved layers, undisturbed by bioturbation) (Persson & Jonsson 2000) can be mentioned as examples of ecological changes in these marine systems (Jonsson et al. 1990, Norkko & Bonsdorff 1996, Kautsky 1999, Larsson & Andersson 1999). Today about 85 million people live in the drainage area of the Baltic Sea. They put a large anthropogenic pressure on the environment, and the resulting eutrophication is one of the most important threats to the marine ecosystem (RELCOM 2001). The increased eutrophication has, as a secondary effect, led to increased oxygen consumption on the seabed. As a consequence, areas with hypoxia and anoxia have extended, especially at deep areas below the halocline (Unverzagt 2001). More or less enclosed areas, like the Baltic Sea in Scandinavia and the Chesapeake Bay on the US east coast, arc dependent on a renewal of the bottom water to maintain an oxygen concentration suitable for benthic life. Such inflows of bottom water may, however, be irregular and vary in magnitude, which makes some enclosed areas especially vulnerable to oxygen deficiency. In the Baltic Sea, oxygen saturation has been measured in several basins over the last 100 yr. The oxygen concentrations in the bottom water show a more or less continuous decline from about 3 ml l-1 in the beginning of the twentieth century to 2000 ind. m"2), for example Halicryptus spinulosus, Scoloplos armiger, Harmothoe sarsi, Heteromastus filiformis, Nephtys hombergii, Corbula gibba and Arctica islandica. In summary, the water exchange in this area partly counteracts oxygen depletion. However, the large nutrient input and high sedimentation of organic matter explain the decline in oxygen concentration, and the changes in benthic community structure.
Kiel Bay Kiel Bay (Fig. 7) is located southwest of the Great Belt and the Femer Belt, and has a mean water depth of 16-17 m and a maximum depth of about 30 m. Because of the topography and the Coriolis force, a considerable amount of deep water passing through the Great Belt enters Kiel Bay. Kiel Bay, therefore, functions as a sediment trap in the straits between the North Sea and the Baltic Sea. The inflowing deep water sometimes contains a large amount of organic matter (Nehring 1971) and is often oxygen-poor, which can contribute to the observed increased frequency of oxygen depletion in this area (Wcigelt 1990). Weigelt (1990) summarised the oxygen conditions in the deep water of Boknis Eck (26-28 m) in the western Kiel Bay between 1957 and 1985. Oxygen depletion has increased significantly since the end of the 1950s and was especially important during the 1970s and the beginning of the 1980s (oxygen saturation was 3-43% in July and August on 11 of 12 occasions). The deepwater oxygen content started to decrease earlier in the year than normally, too early to be caused only by stagnation and by local biological oxygen demand (Weigelt 1990). Also, Babenerd (1991) reported an increased oxygen deficiency in the water below the pycnocline 458
EUTROPHICATION, OXYGEN DEFICIENCY AND BENTHIC FAUNA
Figure 8 The Kiel Bay and Mecklenburg Bight, distribution of hypoxia (0-1.4 ml I"1 , dashed, -630 km2) and anoxia (shaded, -2750 km2) in the bottom water in September 1981 (based on information from Weigelt & Rumohr 1986).
at about 14 m depth in the Boknis Eck during the same time period (from about 8 g O2 m J to about 4 g O2 m"-1 on average). Oxygen consumption rates in summer had increased by a factor of two to three between 1957 and 1985, because of an increased oxygen demand resulting from increased supply of organic matter. Primary production more than doubled during the same time period (Babenerd 1991). During these periods, negative effects on the benthic fauna were observed. Macrofaunal species that are tolerant of organic pollution have become much more abundant since 1981 (Weigelt 1990). In late summer 1981, mass mortality of the benthic fauna below the halocline (>20 m) occurred because of extraordinary and wide-ranging oxygen depletion in Kiel Bay (Fig. 8). Hydrogen sulphide was formed and about 30 000 t of macrofauna died (97%). Before this event, 60 species had been reported in the central part of Kiel Bay, and 20 of these were abundant (Arntz 1971, 1980). During the 1981 oxygen depletion event, only a few species survived: the calms Arctica islandica, Astarte spp. and Corbula gibba and the priapulid Halicryptus spinulosus. The fauna, however, recolonised the area rapidly. In late summer of 1983, a similar but not so severe oxygen depletion occurred and caused mortality of Abra alba and other species below the halocline (Weigelt & Rumohr 1986). Locally restricted faunal breakdowns are common for a semi-enclosed area like Kiel Bay. Such a wide range oxygen depletion with subsequent mass-mortality of fauna had, according to Weigelt & Rumohr (1986), never been reported before. Further, they concluded that the causes for such events seem to be related to climatic changes in connection with general eutrophication. Thus, Kiel Bay is highly vulnerable to environmental perturbations, as illustrated by the frequent periods of mass-mortality in combination with hypoxia. 459
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The Kattegat The southern Kattegat (Fig. 9) has a mean depth of 23 m. A strong halocline is found at about 15 in between the brackish surface water of Baltic origin and the deeper, more saline water (-34) from the Skagerrak. The Kattegat is connected with the Baltic through narrow straights and shallow bottom areas in the Öresund and the Belt Seas. As a consequence, the bottom water circulation in the southern Kattegat is reduced, which make this area susceptible to seasonal hypoxia in late summer and autumn (Rydberg et al. 1990). Input of N and P to the Kattegat and the Skagerrak is estimated to have increased during the twentieth century by factors of four to six and less than eight, respectively (Rosenberg et al. 1990). During 1971 to 1990, both surface and deep water showed an increasing trend for N and P during the winter (Andersson 1996). Rosenberg et al. (1996) reviewed the environmental quality of the Kattegat and the Skagerrak and found that eutrophication and toxic substances have caused large-scale environmental changes and other effects in these sea areas. In the early 1980s, widespread oxygen deficiency in the near-bottom water with accompanying effects on the benthos was probably recorded for the first time in the Kattegat and the Belt Seas (Rosenberg 1985). On the Swedish southeast coast of the Kattegat, the Laholm Bay, the extension of bottom areas with hypoxic water varied between years in the period 1980 through 1990 (Rosenberg 1992, Rosenberg & Loo 1988). The largest areas with hypoxia (oxygen concentrations
