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Zoobenthos as Indicators of Ecological Status in Coastal Brackish Waters: A Comparative Studyfrom the Baltic SeaAuthor(s): Jens Perus, Erik Bonsdorff, Saara Bck, Hans-Gran Lax, Anna Villns and VincentWestbergReviewed work(s):Source: Ambio, Vol. 36, No. 2/3, Science and Governance of the Baltic Sea (Apr., 2007), pp.250-256Published by: Springer on behalf of Royal Swedish Academy of SciencesStable URL: http://www.jstor.org/stable/4315821 .Accessed: 16/05/2012 01:34

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Jens Perus, Erik Bonsdorff, Saara Back, Hans-Goran Lax, Anna Villnas and Vincent Westberg

Zoobenthos as Indicators of Ecological Status in Coastal Brackish Waters: A Comparative Study from the Baltic Sea A new method for classifying soft-bottom zoobenthic assemblages along the Finnish coasts (northern Baltic Sea) is presented and tested against traditional physicochemical monitoring data in the complex Archipelago Sea. Although multivariate methods for assessing the state of the marine environment have become widely used, few numerical indices can operate over a wide salinity range. We compare indices currently in use and propose a new index, BBI (brackish water benthic index), for the low-saline and species-poor Baltic coastal waters. BBI offers a salinity-corrected tool for classification of the soft-bottom zoobenthos under the demands of the European Union Water Framework Directive.

INTRODUCTION

Salinity in the Baltic Sea ranges from almost fully marine, greater than 25 practical saline units (PSU) at the entrance in the Kattegat, to limnic, less than 1 PSU in the innermost reaches in the north (Gulf of Bothnia) and northeast (Gulf of Finland). There are strong vertical and horizontal gradients, including a permanent halocline at 50-70 m depth in the central Baltic Sea (1).

In the Baltic Sea, nutrient concentrations have increased four to eight times during the twentieth century with profound ecological consequences, such as increased pelagic productivity and turbidity of surface layers (2), and shifts in biomass distribution and altered trophic dynamics of the entire ecosystem and food webs in it (3-5). Hypoxic and anoxic conditions in the Baltic Sea seem to be persistent in deep waters in open sea but have more of seasonal character in coastal areas. Karlson, et al. (6) give a good review of eutrophication and oxygen deficiency, and their effects on the benthic assemblages in the Baltic Sea.

Benthic soft-bottom communities in the Baltic Sea are primarily structured by salinity, although depth, oxygen saturation, sediment characteristics, and nutrient concentrations also play significant roles in shaping the assemblages (7- 12). Many limnic and marine species meet their physiological tolerance limits in the Baltic Sea (see, e.g., 13).

The European Union Water Framework Directive (EU WFD) (14) establishes a general framework for the protection of groundwaters, inland surface waters, and transitional and coastal waters; its aim is to achieve good ecological quality status for all waters by 2015. The concept of ecological status is defined in terms of the quality of the biological community (phytoplankton, macrozoobenthos, and macrophytes), according to the ecosystem approach philosophy, as well as the hydromorphological and physicochemical characteristics of the system. This requires robust methods to distinguish different levels of ecological quality when surface water areas are classified. The concept of ecological status implies that in the absence of comprehensive knowledge of all the pressures on a water body and of their combined biological effects, it will

always be necessary to get direct measures of the biological quality elements (15). This must be achieved by using biological indicators to validate any biological effects suggested by nonbiological indicators. Thus, the WFD highlights the importance of measures able to elucidate the biological effects of disturbance.

Finnish coastal waters have been divided into 11 different types, comprising inner and outer archipelago and sea areas in different geographic marine basins (16, 17). The typology, based upon the B-system under the WFD (18, 19), has been tested for ecological relevance and takes into account the biological characteristics of Finnish coastal areas (17). Until now, the monitoring and assessment of the coastal waters in Finland have mainly been based on physicochemical parameters and less on biological parameters (20). In addition to integrating water quality and biological monitoring, most national monitoring programs need, to meet the WFD demands, to change their structure from station oriented to basin or system oriented with specific cause-effect studies for highly dynamic coastal systems (21).

One of the ecological quality elements in the WFD is benthic macroinvertebrates, which is an established and long-recognized component in monitoring the environmental health of coastal and estuarine environments. Macrozoobenthos provide ideal measures of community responses to environmental disturbances and is an effective indicator of the extent and magnitude of pollution impact in the local environment (22-24). The degree of pollution of the water is not necessarily the same as that of the bottom, and the sediment-water interface, in which the long-term effects of discharged pollutants may be better monitored by using sessile or sedentary organisms as indicators integrating the response to exposure and multiple stressors over relatively a long time. Taxonomic diversity also ensures that classification into different functional response groups can be done (25, 26). Signs of eutrophication in benthic communities are changes in abundance, biomass, and species composition, including increases in characterizing species or type species. Some of the species will respond to changes in food supply and/ or sedimentation rates and/or lowered oxygen concentrations (9, 27). The complex benthic environment responds to anthro- pogenic loading and stress by creating a new community structure more tolerant to the increasingly unfavorable physi- ochemical conditions (28).

Here we propose a classification method for environmental status evaluation using benthic macroinvertebrate data from coastal monitoring programs in Finland. There is a variety of indices available for measuring the status of ecological conditions and trends in successions of marine benthic systems (Box 1). Indices integrate and simplify the masses of heteroge- neous information from monitoring, allowing for direct comparisons between data of varying volume and quality in time and space. In this paper we propose the brackish water benthic index (BBI; see Box 2), which follows the assumption that biodiversity increases with increasing distance from a pollution source along a gradient of disturbance (7).

250 ? Royal Swedish Academy of Sciences 2007 Ambio Vol. 36, No. 2-3, April 2007 http://www.ambio.kva.se

Box 1. Some European multimetric indices tested and evaluated during classification work on Finnish coastal waters AMBI = [(O*%I) + (1. 5*%II) + (3*%III) + (4.5*%IV) + (6*%V)1/I00 (Ref. 24. 50)

BMI~ * Rf 3 2

(1AMBI) + H( + I - (( R 50) DKI = (Ref. 5*)

22

BQI [ (N *ES500.05)1 *'0log(S + 1)* (I - (Ref. 5it) Definitions:

5 H'- =-Epj * loapi (log 2 -base used) (Shiannon -Wiener's index)

s

ENi(Ni - ) A N(N - 1) (Simpson's index)

I-V= ecological groups classified according to sensitivity to environmental stress N= number of individuals S = total number of species or taxa (log 10-base used in BQI) ES50 = Hurlbert's (52) modified rarefaction

These indices use 0.1 m 2 samples as calculation basis. Multiple indices have been tested and evaluated, and good overviews of existing indices are found in (31) and (35).

-t' When testing existing indices and starting developing and calculating the BBI-index only an older version of the BQI-index was published (53) where the abundance factor (right bracket) was absent.

All of the Baltic Sea is regarded as being affected by human activities. Trying to reconstruct the structure of benthic assemblages of the past, historic data (at least 100 years of information see, e.g., 29), serving as reference would be of greatest value. However, as for most areas in the Baltic, historic reference data are almost completely lacking from Finnish coastal areas and the use of old data is therefore not an option in determining reference conditions (30). In classifying coastal areas we have modified and adopted a model used in lake and river studies in Finland (19).

Caeiro et al. (31) argue that benthic indices generally fall into three types based upon complexity and information content: i) single community attribute measures (diversity, abundance/ biomass-ratio), ii) multimetric indices (combined multiple measures of community responses into a single index), and iii) multivariate methods (integrated species composition information). The use of a single indicator has not proven to be ideal for monitoring estuarine or coastal environments, which have highly variable natural conditions (22, 32), and hence multivariate methods in assessing the state of the marine environment have become widely used (33).

In this paper we introduce a new multimetric index, the BBI, which was developed while testing and evaluating already existing or proposed indices and their suitability for the species- poor brackish water conditions in the northern Baltic Sea (see,

e.g., 34). The new index is tested for the most complex region, the Archipelago Sea, SW Finland. A comparison of BBI vs. some commonly used indices (DKI, BMI, BQI, and AMBI; see Box 1) is performed for a data set on degradation of the benthic community by extensive organic loading (fish farming), and a subsequent recovery-period.

MATERIALS AND METHODS The data used for the development of the BBI are from a Finnish environmental administration database for zoobenthos, covering the years 1990-2000, and contains some 8500 visits from 1300 sites. The majority (-90%) of the data were collected using an Ekman-Birge grab sampler and sieved on a 0.5-mm mesh. From each station the index is based on five replicate grab samples. When pooling grabs and transforming to m-2 units, the mean of abundances and total of species has been used. Quality assurance of the database has included verification of taxonomy, and deleting synonyms or misspelled names. In this paper, taxonomy has been used at species level, except for chironomids and oligochaetes, which were analyzed at the level of family and order, respectively.

A depth separation of the water column (0-10 m and 10+ m) was used in relation to the coastal typology. This was done to

Ambio Vol. 36, No. 2-3, April 2007 ? Royal Swedish Academy of Sciences 2007 251 http://www.ambio.kva.se

Box 2. Information on the structure and content of the new brackish water benthic index. Explanation of factors in formulas and literature used in species classification is given.

Brackish water benthic index (BBI) The BBI-index consists of following metrics:

- Classification* (four levels) of sensitivity or tolerance of individual species (1, 5, 10, 15) 1-very tolerant to pollution 5-tolerant 10-pollution sensitive 15-very pollution sensitive

- Relative abundance (%) of sensitive and tolerant species. - Shannon-Wiener diversity (H')(log2-base) - Abundance - Species richness

BBI_= [( Q ") B (HQI1 [(i l + (1 H)1 _ BQ1n\,,, \H,~ax}* ABtOIJ \ s1 BBI-

2 2 The index ranges from 0 to -1.

Definitions: BBI = Brackish water bentic index

BQI t( (otA x ES50oo.5i)) x10 log(S + 1) (Ref. 53) BQ1max = maximum BQI-value recorded within type after calculating all available data within national zoobenthos database H' Shannon-Wiener index (log2-base) H'max = maximum H'-value recorded within type after calculating all available data within national zoobenthos database ABtot = totA = abundance at station (equal to N and Ntot in Box 1 indices) S = number of species/taxa at station ES500.5i = sensitivity values (where species are classified as 1 = very tolerant, 5 = tolerant, 10 = sensitive, and 15 = very sensitive to

disturbance).

The classification list is the same as in Sweden, where it is used in the BQI-index (51, 53) and sensitivity and tolerance grouping is based on literature (24, 28, 54-60) and expert judgment. The list is available at www.vattenportalen.se.

facilitate the interpretation of environmental status for the individual types (17).

The BBI was developed while testing and evaluating already existing indices used for environmental classification purposes (Box 1 and reviews by, e.g., 31, 35). Based on this experience, the BBI (Box 2) was developed for classification of zoobenthic assemblages for the Finnish low-saline and species-poor coastal waters (for an overview of the biodiversity of the Baltic Sea zoobenthos, see 13) in the Baltic Sea ecoregion. The BBI compensates for the naturally low diversity in the Baltic Sea. By classifying species on a scale from sensitive to tolerant in relation to mainly organic enrichment, and multiplying them according to their relative importance at a sampling site, we get a good estimate of the benthic community structure and its function (for the species classification, see Box 2). Based on an evaluation of other indices, we added both abundance and biodiversity as elements into the BBI for determining the quality of the benthic community and therefore the index meets all demands stated in Annex V of the WFD (14). To prevent misclassifications due to salinity gradients (34), type-specific maximum values for BQI- and H' variables have been calculated from the entire content in the national database. BBI values are continuous between 0 and -1.

For the actual classification of the coastal areas, we have adopted and modified a model used for studies of lakes and rivers in Finland (19). Since true reference areas or conditions

are no longer present in the coastal areas in the Baltic Sea, the reference was defined as the median of the top 10% highest BBI- values for each type and depth interval. Ecological quality ratio (EQR) values were then calculated by dividing observed values with the defined reference values. The border between "good" and "high" environmental quality is set at the 10% percentile of reference EQR. Values below this border are divided into four equally broad classes (good-moderate-poor-bad).

Here we propose classification results (Fig. 1) from a case- study area in the Archipelago Sea, SW Finland (59?45'-60?45'N and 21?00'-23?00'E), containing three environmental types (Ls = inner, Lv = middle, and Lu = outer archipelago zone) (17, 19), ranging from inner sheltered archipelago areas to open and exposed coasts. Boundary values for the classification are further validated by checking species richness, abundance, diversity values (Table 1), and community composition of tolerant or sensitive species (Fig. 2a) against the defined criteria for high, good, and moderate status in coastal waters described in Annex V of the WFD. For each individual national Finnish coastal type, comprehensive species lists have been compiled, and reference criteria can be set as a proportion of the total number of species (alternatively number of sensitive species) that need to be present for the reference criteria to be met.

An independent cross-evaluation of BBI in relationship to the other indices in Box 1 was performed on a long-term data set from the Aland Islands where effects from long-term fish


100%

80%- mB 60% I0PI

D3M1 40% IEGI 20% -!.i 0%

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Figure 1. Proportional distribution of different environmental status for the classification of three archipelago zones (Ls = inner, Lv = middle, and Lu = outer zone) and two depth intervals (0-10 m, 10+ m) using the BBI. (Environmental status: B = bad, P = poor, M = moderate, G = good, and H = high)

farming (1981-2002) and a 2-year recovery period were studied (Perus et al., in prep.).

RESULTS The information on soft-bottom zoobenthos gave a classification for the BBI (Fig. 1; Table 1) in accordance with the general environmental status of the Archipelago Sea described in other studies using traditional physicochemical monitoring techniques (36-39). Species richness is highest in inner shallow archipelago areas, where habitat complexity and variable substrates give rise to high biodiversity (Table 1) (11, 40). Species richness is also consistently higher in the littoral depth interval (0-10 m) than in the deeper stratum. Abundances vary greatly within all environmental types, regardless of classification status. How- ever, the magnitude in variation tends to increase as environmental status becomes deteriorated (predominantly in the categories poor and bad). This high variation in abundances under poor conditions is also described in the Pearson- Rosenberg paradigm (7) indicating fluctuating conditions with a high proportion of opportunistic and tolerant species

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0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 BBI BBI

Sensitivity values: Very tolerant, - Tolerant, Sensitive, Very sensitive

Figure 2. Changes in species composition as environmental quality improves in (a) the depth stratum 10+ m in the outer archipelago type Lu, and (b) a fish farming case study from the Aland Islands. The proportion of species classified as tolerant and very tolerant to stress dominate at low BBI values, while species sensitive and very sensitive to stress dominate at higher values or are lacking in stressed environments during recovery. Distribution shown by least-square smoothing lines (DWLS, stiffness 0.5).

(Fig. 2a). The proportion of status bad is lowest in the outer archipelago (coastal type Lu), where bad conditions are not even registered for the shallow section. The middle archipelago (type Lv) shows a higher overall proportional distribution of poor and bad quality conditions than both the inner and outer coastal types (Fig. 1). The middle zone in the Archipelago Sea, as for the same zone in the Aland Islands, is the region where most changes have taken place in the benthic community structure over the last 30 years (11).

Results from testing BBI and other indices on an organically polluted case study (fish farming) show that BBI correlates well with DKI (r2 = 0.86), BMI (r2 = 0.80), BQI (2006) (r2 = 0.78), and BQI (2004) (r2 = 0.75) but not with AMBI (r2 = 0.27). Tolerant species dominate the communities, and species very sensitive to organic enrichment are hardly present (Fig. 2b). BBI, DKI, BMI, and BQI show a similar response to changes in oxygen saturation, organic matter, and species richness (Fig. 3a-c), while the AMBI index is insensitive to changes in these variables in low-saline species-poor regions. The average number of taxa found at a single station visit (pooling five

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replicate grabs; average species richness 5.3 ? 3.1) or station (pooling station visits; average species richness 7.6 + 5.2) is naturally low along the Finnish coastline.

DISCUSSION The brackish Baltic Sea is semienclosed, nontidal, and connected to fully marine waters only by the narrow and shallow Danish straits. Vertical and horizontal gradients in both hydrography and biology characterize the Baltic Sea today. Conditions for the macrozoobenthos therefore differ significantly, not only between the Baltic Sea and the Atlantic Ocean, but also between subbasins inside the Baltic Sea (25, 26, 34). Characteristics such as the impoverishment of the zoobenthic communities along the south-north salinity-temperature gradient (13, 25), seasonally pulsed nutrient loads by rivers in northern Baltic Sea, introduction of new species, and increasingly frequent seasonal-annual hypoxic or anoxic events in the Baltic Sea create mixed benthic communities inside an already stressed ecosystem. Although the entire Baltic Sea is affected by eutrophication, the effects and consequences vary between subbasins (41). Regional differences occur especially in the coastal areas (42) and thus require methods and tools capable of correctly describing environmental changes.

Traditional monitoring techniques, using physicochemical and hydrographical parameters, have produced a classification of surface waters in the Archipelago Sea (36-39) that was verified by the BBI using soft-bottom macroinvertebrates. The BBI, like most of the other tested indices here, behaved as intended when compared against neutral case-study data containing large variations in environmental characteristics. Hence, we feel that zoobenthos is a valid tool for quality- and classification purposes, and that the new BBI provides a reliable method for low-saline coastal brackish waters in the Baltic Sea.

Biodiversity of marine macroinvertebrate species decreases rapidly, moving northward and eastward in the Baltic Sea because of decreasing salinity, harsh climatic conditions, and possibly the distance to the marine donor area (13). This holds true for open sea areas, but closer to the coast and in shallow waters (0-10 m) species of limnic, brackish, and marine origin form mixed assemblages, and freshwater species (including insect larvae) make up a high proportion of the total species richness, thus compensating for the losses in the open sea. Macroinvertebrate diversity remained almost similar in the southern Finnish coastal waters, where salinity is -6 PSU and in the northern- and easternmost parts of the Baltic Sea, where salinity is -1 because of the importance of limnic species (13). Species richness is generally higher at littoral depths (0-10 m) than in deeper waters (10? m) (Table 1). Depth alone is not the structuring factor for this difference, but a higher habitat complexity and variable substrates is usually encountered in shallow areas (11, 25, 40).

To avoid ambiguous results due to relationships to salinity gradients (34), the BBI works on predefined type-specific (and their depth strata) maximum values of BQI and H'. Thereby the risk of misclassifying landlocked low-saline areas compared with outer sea areas is minimized.

The use of indicators (specific species, various indices, etc.) is becoming an integral part of decision support systems for coastal zone management, and there is a plethora of techniques for determining change at all levels of biological organization (43). The apparent elegance and authority of a scaled metric to portray complex environmental data to managers, politicians, and public has kept interest high.

When testing the marine index AMBI, widely used and accepted in organic pollution studies globally (see, e.g., overview in 44), in the conditions of the northern Baltic Sea

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of a species classified as "sensitive," a notation also made by Quintino, et al. (43) in a Portuguese study. The high proportion of species (66% in the Finnish national taxa list) not classified in the marine AMBI library list (www.azti.es) made the analysis meaningless. These drawbacks in index performances using the marine AMBI classification made us use the joint Swedish- Finnish species classification list and adding abundance and biodiversity as factors into the BBI when determining the quality of the benthic community in the Baltic Sea. Combining these factors is crucial for assessing the structure and function of the community. The importance of occasional occurrence of a few specimens of a sensitive taxa at a polluted site, otherwise almost abiotic, is downweighed in the final classification of the site. The magnitude in variation tends to increase as the environmental status deteriorates (predominantly poor and bad status) (Table 1), and low biodiversity needs to be accounted for when abundances are high but the general conditions are poor at the site. This high variation in abundances under poor conditions is also described in the Pearson-Rosenberg paradigm (7), indicating fluctuating conditions with a high proportion of opportunistic and tolerant species (Fig. 2b) in the initial recovery phase.

Diversity indices, especially species richness, are habitat-type dependent, with different ranges of values in different habitat types. A habitat-based approach is not currently possible for the complex archipelago waters in Finland, but habitat mapping using underwater photography and GIS will gradually improve this situation, and when applicable this parameter will need to be taken into account when validating and calibrating results. In a large survey of long-term changes in the Archipelago Sea, Bonsdorff et al. (46, 47) concluded that the number of species has not significantly changed over time. However, species composition has changed dramatically with a shift from suspension feeders to deposit feeders, indicating functional disturbances (48). This functional shift, connected to eutrophication, has also been shown in other studies analyzing long- term changes in macrozoobenthos communities along the Finnish coast (11, 39) and further emphasizes the need for developing the species specific classification of tolerance and sensitivity to environmental stress.

Subjective classification of species sensitivity is always open for and subject to criticism. Biodiversity in the Baltic Sea is low and therefore the understanding of the biology of individual species and their response to physical stress and pollution is relatively good (25). However, information about the response patterns is still unknown for many less frequent and less abundant species. The indicator values for benthic changes and classifications made for a particular area might not be directly transferable to other sea areas if characteristics (hydromorphol- ogy, geography, evolutionary history, etc.) markedly differ, but our study illustrates that tools can be tailored to suit special environmental requirements, as for instance along the Finnish coasts (Table 1).

Indices and indicator-systems have been developed for various regions so that they are applicable for different types of species, habitats, and controlling factors of the targeted area. Although multimetric indices are generally verified as being sensitive, stable, robust, and statistically sound (35) few indices can operate over a wide salinity range (34) or throughout the season (49) or in completely different environmental conditions. As a consequence, rather than the coordinated and progressive development of a generic metric for each habitat type, the literature has become swamped with extended families of analogous region-specific indices that differ only slightly from one another (35). This holds true for the BBI as well because it differs only in parts from similar multimetric indices developed in, e.g., Denmark and in the United Kingdom (Box 1).

However, these indices use the marine AMBI in their syntax, and significant differences in species composition, classification, and low proportion of species classified in relation to Baltic Sea conditions make it necessary to modify the indices to capture and classify benthic soft bottom communities characteristic of the brackish Baltic Sea.

The verification of class boundaries using ecologically relevant parameters (species richness, abundance, biodiversity, and proportion of sensitive and tolerant species) is therefore a prerequisite for a proper interpretation. In addition to mathematically derived boundaries, expert judgment should be given an opportunity to define what should be considered the "good ecological status" that the WFD strives to achieve. The amount of data and thereby also the reliability of the interpretation should be taken into consideration. To classify the environmental status of an area one needs to use multiple evaluation tools instead of a single one, and a combined interpretation, using all ecological quality elements, will ensure reliable ecological classifications of the European marine environments.

That so many indices of aquatic habitat quality have emerged over the last 20 years indicates that there is little acceptability of any specific metric by environmental managers or scientists (35). Intercalibration within and between biogeo- graphic regions (e.g., 50) needs further validation before making management decisions at local and regional scale using tools and methods developed elsewhere. We believe that the methodology presented here, the BBI for the low-saline Baltic coastal waters, offers a good potential tool for classification of the zoobenthos as an ecological quality component under the demands of the EU WFD. We show that the available data can be used to verify environmental typology and gives a reasonable estimate of the biological condition of the respective regions, with a balanced distribution of stations among the quality classes poor to high (Fig. 1). We also argue that the BBI offers a possibility for cross calibration of information within the Baltic Sea region, and that the information gained can be used for environmental decision-making in low-saline coastal and estuarine areas.

References and Notes

1. Voipio, A. (ed). 1981. The Baltic Sea, Elsevier Oceanography Series, Vol. 30., Elsevier, Burlington, MA, 418 pp.

2. Sanden, P. and Hakansson, B. 1996. Long-term trends in Secchi depth in the Baltic Sea. Limnol. Oceanogr. 41, 346-351.

3. Cederwall, H. and Elmgren, R. 1980. Biomass increase of benthic macrofauna demonstrates eutrophication of the Baltic Sea. Ophelia Suppl. 1, 287-304.

4. Elmgren, R. 1984. Trophic dynamics in the enclosed, brackish Baltic Sea. Rapp. P.- V. Reun. Cons. Int. Explor. Mer. 183, 152-169.

5. Elmgren, R. and Larsson, U. 2001. Eutrophication in the Baltic Sea area. Integrated coastal management issues. In: Science and Integrated Coastal Management. Bodungen, B.V. and Turner, R.K. (eds). Dahlem University Press, Berlin, pp. 15-35.

6. Karlson, K., Rosenberg, R. and Bonsdorff, E. 2002. Temporal and spatial large-scale effects of eutrophication and oxygen deficiency on benthic fauna in Scandinavian and Baltic waters-a review. Oceanogr. Mar. Biol. Annu. Rev. 40, 427-489.

7. Pearson, T.H. and Rosenberg, R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr. Mar. Biol. Annu. Rev. 16, 229-311.

8. Snelgrove, P.V.R. and Butman, C.A. 1994. Animal-sediment relationships revisited: cause versus effect. Oceanogr. Mar. Biol. Annu. Rev. 32, 111-177.

9. Diaz, R.J. and Rosenberg, R. 1995. Marine benthic hypoxia: ecological effects and behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu. Rev. 33, 245-303.

10. Laine, A.0. 2003: Distribution of soft-bottom macrofauna in the deep open Baltic Sea in relation to environmental variability. Estuar. Coast. Shelf Sci. 57, 87-97.

11. Perus, J. and Bonsdorff, E. 2004. Long-term changes in macrozoobenthos in the Aland archipelago, northern Baltic Sea. J. Sea Res. 52, 45-56.

12. Laine, A.O., Andersin, A.-B., Leinio, S. and Zuur, A.F. 2007. Stratification induced hypoxia as a structuring factor of macrozoobenthos in the open Gulf of Finland (Baltic Sea). J. Sea Res. 57, 65-77.

13. Bonsdorff, E. 2006. Zoobenthic diversity-gradients in the Baltic Sea: continuous post- glacial succession in a stressed ecosystem. J. Exp. Mar. Biol. Ecol. 330, 383-391.

14. European Commission. 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. Official Journal L 327/1.

15. Salas, F., Patricio, J., Marcos, C., Pardal, M.A., Perez-Ruzafa, A. and Marques, J.C. 2006. Are taxonomic distinctness measures compliant to other ecological indicators in assessing ecological status? Mar. Poll. Bull. 52, 162-174.

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Ambio Vol. 36, No. 2-3, April 2007 (? Royal Swedish Academy of Sciences 2007 255 http://www.ambio.kva.se

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61. This work has been completed within and financed through the projects CHARM (EVK3-CT-2001-00065) and IMAGINE (under the BIREME-program, Academy of Finland), with partial funding also through the Finnish Ministry of Environment. We also thank the Finnish Environment Institute and the West Finland Regional Environment Centre in Vasa for logistic assistance, and numerous sources for access to data for the national Finnish database on coastal zoobenthos, currently maintained by the Western Finland Regional Environment Centre in Vasa.

Jens Perus is a Ph.D. student in environmental- and marine biology, Abo Akademi University, Finland. His main fields of research are soft-bottom macrozoobenthos and detecting short and long term changes in the environment. His address: Abo Akademi University, Environmental and Marine Biology, Akademigatan 1, FI-20500 Turku/Abo, Finland. E-mail: [email protected]

Erik Bonsdorff is professor of marine biology at Abo Akademi University, Finland. His fields of interest include long-term changes of the Baltic Sea ecosystem (natural and anthropo- genic), with focus on benthic macrofauna and various aspects of functional biodiversity. He is also engaged in the work of the Baltic Sea 2020 foundation within the Royal Swedish Academy of Sciences. His address: Abo Akademi University, Environ- mental and Marine Biology, Akademigatan 1, FI-20500 Turku/ Abo, Finland. E-mail: [email protected]

Saara Back is professor and research manager of the Baltic Sea Protection Research Programme in SYKE (Finnish Environment Institute), coordinating its marine research and expert services. Her main interests are marine biodiversity and coastal water monitoring and assessments. In recent years she has worked on the implementation of the Water Framework Directive. Her address: Finnish Environment Institute, P.O. Box 140, FI-00251 Helsinki, Finland. E-mail: [email protected]

Hans-G6ran Lax (M.Sc.) is a senior research scientist at West Finland Regional Environment Centre. He is responsible for the monitoring of the environment. His address: West Finland Regional Environment Centre, P.O. Box 262, FI-651 01 Vaasa, Finland. E-mail: [email protected]

Anna Villnas (M.Sc.) is a researcher at Abo Akademi University, Finland. Her main interests are soft-bottom macrozoobenthos and recovery of benthic communities after abatement of organic loading. Her address: Abo Akademi University, Environmental and Marine Biology, Akademigatan 1, FI-20500 Turku/Abo, Finland. E-mail: [email protected]

Vincent Westberg (M.Sc.) is a senior planning officer at West Finland Regional Environment Centre. His work includes the coordination of the implementation of the Water Framework Directive in the Western River Basin District and the elaboration of the classification principles for macrozoobenthos for the Finnish coastal waters. His address: West Finland Regional Environment Centre, P.O. Box 262, FI-651 01 Vaasa, Finland. E-mail: [email protected]


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Issue Table of ContentsAmbio, Vol. 36, No. 2/3, Science and Governance of the Baltic Sea (Apr., 2007), pp. 117-286Front Matter [pp. 117-117][Editorial] [pp. 118]The MARE Research Program 1999-2006: Reflections on Program Management [pp. 119-122]The Finnish Baltic Sea Research Programme (BIREME) [pp. 123]Nutrient Dynamics from Land to SeaModeling Riverine Nutrient Transport to the Baltic Sea: A Large-Scale Approach [pp. 124-133]Denitrification in the River Estuaries of the Northern Baltic Sea [pp. 134-140]Modeling the Baltic Sea Eutrophication in a Decision Support System [pp. 141-148]Role of Sea-Ice Biota in Nutrient and Organic Material Cycles in the Northern Baltic Sea [pp. 149-154]

Processes and Ecological Consequences in the SeaImpacts of Eutrophication on Diatom Life Forms and Species Richness in Coastal Waters of the Baltic Sea [pp. 155-160]The Impact of Benthic Macrofauna for Nutrient Fluxes from Baltic Sea Sediments [pp. 161-167]M74 Syndrome in Baltic Salmon and the Possible Role of Oxidative Stresses in Its Development: Present Knowledge and Perspectives for Future Studies [pp. 168-172]Removal by Sorption and in situ Biodegradation of Oil Spills Limits Damage to Marine Biota: A Laboratory Simulation [pp. 173-179]Bacterial Diversity and Function in the Baltic Sea with an Emphasis on Cyanobacteria [pp. 180-185]Internal Ecosystem Feedbacks Enhance Nitrogen-Fixing Cyanobacteria Blooms and Complicate Management in the Baltic Sea [pp. 186-194]Ecosystem Consequences of Cyanobacteria in the Northern Baltic Sea [pp. 195-202]Macroalgal Communities Face the Challenge of Changing Biotic Interactions: Review with Focus on the Baltic Sea [pp. 203-211]

Science and Management: Governance of a Common SeaChanging Environments or Shifting Paradigms? Strategic Decision Making toward Water Protection in Helsinki, 1850-2000 [pp. 212-219]Legal Requirements and Wastewater Discharges to Polish Water Bodies, 1945-2003 [pp. 220-228]Cold War and the Environment: The Role of Finland in International Environmental Politics in the Baltic Sea Region [pp. 229-236]Actors and Arenas in Hybrid Networks: Implications for Environmental Policymaking in the Baltic Sea Region [pp. 237-242]Management Options and Effects on a Marine Ecosystem: Assessing the Future of the Baltic [pp. 243-249]Zoobenthos as Indicators of Ecological Status in Coastal Brackish Waters: A Comparative Study from the Baltic Sea [pp. 250-256]Human Dietary Intake of Organochlorines from Baltic Herring: Implications of Individual Fish Variability and Fisheries Management [pp. 257-264]Managing Baltic Sea Fisheries under Contrasting Production and Predation Regimes: Ecosystem Model Analyses [pp. 265-271]Searching Efficient Protection Strategies for the Eutrophied Gulf of Finland: The Combined Use of 1D and 3D Modeling in Assessing Long-Term State Scenarios with High Spatial Resolution [pp. 272-279]Improvement of Baltic Proper Water Quality Using Large-Scale Ecological Engineering [pp. 280-286]

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science and governance of the baltic sea || zoobenthos as indicators of ecological status in coastal...

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