Ecological status assessment of European lakes: a comparison of metrics for phytoplankton, macrophytes, benthic invertebrates and fish

Data on phytoplankton, macrophytes, benthic invertebrates and fish from more than 2000 lakes in 22 European countries were used to develop and test metrics for assessing the ecological status of European lakes as required by the Water Framework Directive. The strongest and most sensitive of the 11 metrics responding to eutrophication pressure were phytoplankton chlorophyll a, a taxonomic composition trophic index and a functional traits index, the macrophyte intercalibration taxonomic composition metric and a Nordic lake fish index. Intermediate response was found for a cyanobacterial bloom intensity index (Cyano), the Ellenberg macrophyte index and a multimetric index for benthic invertebrates. The latter also responded to hydromorphological pressure. The metrics provide information on primary and secondary impacts of eutrophication in the pelagic and the littoral zone of lakes. Several of these metrics were used as common metrics in the intercalibration of national assessment systems or have been incorporated directly into the national systems. New biological metrics have been developed to assess hydromorphological pressures, based on aquatic macrophyte responses to water level fluctuations, and on macroinvertebrate responses to morphological modifications of lake shorelines. These metrics thus enable the quantification of biological impacts of hydromorphological pressures in lakes.     

Potential conflicts between environmental legislation and conservation exemplified by aquatic macrophytes

It is important that legislation on water quality issues of freshwaters is not in conflict with nature conservation purposes. So far, it is however unknown how the assessment of ecological status according to for example the Water Framework Directive (WFD) of the European Community relates to the status of lakes according to the Habitat Directive (HD) or to national environmental objectives including, e.g., the protection of important wetland areas and red-listed species. We used lake macrophyte classification schemes of Norway, Sweden, and Finland and a total of 1,014 lakes to evaluate the possible conflict between these directives and national legislation. The classification schemes represent mainly trophic indices penalizing lakes with elevated phosphorous concentrations. In general, high ecological status according to the WFD did not mean high number of red-listed species or high status according to the HD or other national environmental objectives. In Sweden 78%, in Norway 47%, and in Finland 29% of lakes with red-listed species were classified as lakes of moderate or worse ecological status based on the macrophyte classification scheme. These lakes thus did not fulfill the demands of the WFD. Restoration of surface water toward fulfilling the demands requires in practice a reduction of the trophic status. This might potentially result in for example the loss of red-listed species. To avoid such potential conflicts, we primarily suggest revising the national quality assessment systems toward implicitly incorporating nature conservation aspects, e.g., the number of red-listed species in a multi-metric assessment system.     

Quantifying uncertainties in biologically-based water quality assessment: A pan-European analysis of lake phytoplankton community metrics

Lake phytoplankton are adopted world-wide as a sensitive indicator of water quality. European environmental legislation, the EU Water Framework Directive (WFD), formalises this, requiring the use of phytoplankton to assess the ecological status of lakes and coastal waters. Here we provide a rigorous assessment of a number of proposed phytoplankton metrics for assessing the ecological quality of European lakes, specifically in response to nutrient enrichment, or eutrophication, the most widespread pressure affecting lakes. To be useful indicators, metrics must have a small measurement error relative to the eutrophication signal we want them to represent among lakes of different nutrient status. An understanding of variability in metric scores among different locations around a lake, or due to sampling and analytical variability can also identify how best this measurement error is minimised.To quantify metric variability, we analyse data from a multi-scale field campaign of 32 European lakes, resolving the extent to which seven phytoplankton metrics (including chlorophyll a, the most widely used metric of lake quality) vary among lakes, among sampling locations within a lake and through sample replication and processing. We also relate these metrics to environmental variables, including total phosphorus concentration as an indicator of eutrophication.For all seven metrics, 65–96% of the variance in metric scores was among lakes, much higher than variability occurring due to sampling/sample processing. Using multi-model inference, there was strong support for relationships between among-lake variation in three metrics and differences in total phosphorus concentrations. Three of the metrics were also related to mean lake depth. Variability among locations within a lake was minimal (<4%), with sub-samples and analysts accounting for much of the within-lake metric variance. This indicates that a single sampling location is representative and suggests that sub-sample replication and standardisation of analyst procedures should result in increased precision of ecological assessments based upon these metrics.For three phytoplankton metrics being used in the WFD: chlorophyll a concentration, the Phytoplankton Trophic Index (PTI) and cyanobacterial biovolume, >85% of the variance in metric scores was among-lakes and total phosphorus concentration was well supported as a predictor of this variation. Based upon this study, we can recommend that these three proposed metrics can be considered sufficiently robust for the ecological status assessment of European lakes in WFD monitoring schemes.     

A hitchhiker's guide to European lake ecological assessment and intercalibration

The Water Framework Directive is the first international legislation to require European countries to establish comparable ecological assessment schemes for their freshwaters. A key element in harmonising quality classification within and between Europe's river basins is an “Intercalibration” exercise, stipulated by the WFD, to ensure that the good status boundaries in all of the biological assessment methods correspond to similar levels of anthropogenic pressure. In this article, we provide a comprehensive overview of this international comparison, focusing on the assessment schemes developed for freshwater lakes. Out of 82 lake ecological assessment methods reported for the comparison, 62 were successfully intercalibrated and included in the EC Decision on intercalibration, with a high proportion of phytoplankton (18), macrophyte (17) and benthic fauna (13) assessment methods. All the lake assessment methods are reviewed in this article, including the results of intercalibration. Furthermore, the current gaps and way forward to reach consistent management objectives for European lakes are discussed.     

Central European water quality indices applied to long-term data from peri-alpine lakes: test and possible improvements

We tested the applicability of two available Water Framework Directive (WFD) compliant phytoplankton indices on three large peri-alpine lakes to analyze their suitability for trophic classification. We show that the indices vary in their final resulting Ecological Quality Ratios (EQRs) and are only appropriate to roughly distinguish lakes of different water quality according to OECD criteria (OECD, 1982). Annual mean TP concentration in Lake Geneva was 0.03 mg l^?1 in 2006 (Lazzarotto &; Rapin, 2007), which marks mesotrophic conditions. According to the tested indices, the lake is of ‘good’ (0.60–0.80) quality after the German WFD method (PSI) and of ‘moderate’ quality according to the Austrian WFD method (BI). We prove that the way how to derive the per annum value of the metric ‘Brettum Index’ (BI) in the Austrian WFD method significantly influences the resulting index and the scatter of long-term data. We focused on improvement strategies for this index in terms of calculation and sampling frequency. Contrary to the tested bin, the modified index presents no significant differences between four and six sampling dates per year. In order to improve the significance of the available indices, we propose to modify the way of per annum index calculation for the Austrian WFD method as well as to focus on species composition to achieve a high relative proportion of indicator species. A phytoplankton index alone may not be sensitive enough to track the changes that occur within a lake. The results confirm the need to take into account other biological elements such as fish, macrophytes, attached diatoms and macrozoobenthos as suggested by the WFD.     

Development of a fish-based index to assess the eutrophication status of European lakes

The use of the CEN (European Committee for Standardization) standard method for sampling fish in lakes using multi-mesh gillnets allowed the collection of fish assemblages of 445 European lakes in 12 countries. The lakes were additionally characterised by environmental drivers and eutrophication proxies. Following a site-specific approach including a validation procedure, a fish index including two abundance metrics (catch per unit effort expressed as fish number and biomass) and one functional metric of composition (abundance of omnivorous fish) was developed. Correlated with the proxy of eutrophication, this index discriminates between heavily and moderately impacted lakes. Additional analyses on a subset of data from Nordic lakes revealed a stronger correlation between the new fish index and the pressure data. Despite an uneven geographical distribution of the lakes and certain shortcomings in the environmental and pressure data, the fish index proved to be useful for ecological status assessment of lakes applying standardised protocols and thus supports the development of national lake fish assessment tools in line with the European Water Framework Directive.     

Using aquatic macrophyte community indices to define the ecological status of European lakes

Defining the overall ecological status of lakes according to the Water Framework Directive (WFD) is to be partially based on the species composition of the aquatic macrophyte community. We tested three assessment methods to define the ecological status of the macrophyte community in response to a eutrophication pressure as reflected by total phosphorus concentrations in lake water. An absolute species richness, a trophic index (TI) and a lake trophic ranking (LTR) method were tested at Europe-wide, regional and national scales as well as by alkalinity category, using data from 1,147 lakes from 12 European states. Total phosphorus data were used to represent the trophic status of individual samples and were plotted against the calculated TI and LTR values. Additionally, the LTR method was tested in some individual lakes with a relatively long time series of monitoring data. The TI correlated well with total P in the Northern European lake types, whereas the relationship in the Central European lake types was less clear. The relationship between total P and light extinction is often very good in the Northern European lake types compared to the Central European lake types. This can be one of the reasons for a better agreement between the indices and eutrophication pressure in the Northern European lake types. The response of individual lakes to changes in the abiotic environment was sometimes represented incorrectly by the indices used, which is a cause of concern for the use of single indices in status assessments in practice.     

Morphological alterations of lake shores in Europe: A multimetric ecological assessment approach using benthic macroinvertebrates

Besides pollution, lakes are affected by human alterations of lake-shore morphology. However, ecological effects of such alterations have rarely been studied systematically. Hence, we developed tools to assess the ecological effects of anthropogenic morphological alterations on European lake-shores based on pressure-specific response patterns of littoral macroinvertebrate community composition. Littoral invertebrates were sampled from 51 lakes in seven European countries. Sampling covered a range of natural to heavily morphologically degraded sites including natural shorelines, recreational beaches, ripraps and retaining walls. Biological data were supplemented by standardized morphological data that were collected via a Lake Habitat Survey (LHS) protocol and subsequently used to develop a morphological stressor index. Two biotic multimetric indices were developed based on habitat-specific samples (Littoral Invertebrate Multimetric based on HAbitat samples, LIMHA) and composite samples (Littoral Invertebrate Multimetric based on COmposite samples, LIMCO) through correlations with the morphological stressor index. Similarity analyses showed strong spatial differences in macroinvertebrate community composition between four main geographical regions, i.e. Western, Northern, Central and Southern Europe. The morphological stressor index as well as LIMCO and LIMHA have been developed for each geographical region specifically, thereby optimizing correlations of LIMCO and LIMHA with the respective morphological stressor index. The metric composition of LIMCO and LIMHA and their correlation coefficients with the morphological stressor index are comparable to existing national and regional methods that assess morphological lakeshore degradation via macroinvertebrate communities. Hence, LIMCO and LIMHA indices constitute a new stressor-specific assessment tool that enables comparable lake morphology assessment across Europe, as it has been developed involving a uniform methodology followed by regionalized optimization. These tools fulfil the standards of the EU Water Framework Directive and thus may complement existing assessment approaches used in lake monitoring focusing solely on lake eutrophication so far.     

Efficient sampling methodologies for lake littoral invertebrates in compliance with the European Water Framework Directive

Lake shores are characterised by a high natural variability, which is increasingly threatened by a multitude of anthropogenic disturbances including morphological alterations to the littoral zone. The European Water Framework Directive (EU WFD) calls for the assessment of lake ecological status by monitoring biological quality elements including benthic macroinvertebrates. To identify cost- and time-efficient sampling strategies for routine lake monitoring, we sampled littoral invertebrates in 32 lakes located in different geographical regions in Europe. We compared the efficiency of two sampling methodologies, defined as habitat-specific and pooled composite sampling protocols. Benthic samples were collected from unmodified and morphologically altered shorelines. Variability within macroinvertebrate communities did not differ significantly between sampling protocols across alteration types, lake types and geographical regions. Community composition showed no significant differences between field composite samples and artificially generated composite samples, and correlation coefficients between macroinvertebrate metrics calculated with both methods and a predefined morphological stressor index were similar. We conclude that proportional composite sampling represents a time- and cost-efficient method for routine lake monitoring as requested under the EU WFD, and may be applied across various European geographical regions.     

REBECCA databases: experiences from compilation and analyses of monitoring data from 5,000 lakes in 20 European countries

Chemical and biological data from more than 5,000 lakes in 20 European countries have been compiled into databases within the EU project REBECCA. The project’s purpose was to provide scientific support for implementation of the EU Water Framework Directive (WFD). The databases contain the biological elements phytoplankton, macrophytes, macroinvertebrates and fish, together with relevant chemistry data and station information. The common database strategy has enabled project partners to perform analyses of chemical–biological relationships and to describe reference conditions for large geographic regions in Europe. This strategy has obvious benefits compared with single-country analyses: results will be more representative for larger European regions, and the statistical power and precision will be larger. The high number of samples within some regions has also enabled analysis of type-specific relationships for several lake types. These results are essential for the intercalibration of ecological assessment systems for lakes, as required by the WFD. However, the common database approach has also involved costs and limitations. The data process has been resource-demanding, and the requirements for a flexible database structure have made it less user-friendly for project partners. Moreover, there are considerable heterogeneities among datasets from different countries regarding sampling methods and taxonomic precision; this may reduce comparability of the data and increase the uncertainty of the results. This article gives an overview of the contents and functions of the REBECCA Lakes databases, and of our experiences from constructing and using the databases. We conclude with recommendations for compilation of environmental data for future international projects.     

Macrophyte‐based assessment of lakes – a contribution to the implementation of the European Water Framework Directive in Germany

The European Water Framework Directive requires ecological status classification and monitoring of surface and ground water bodies using biological indicators. To fulfill the demands of the Directive, a macrophyte‐based assessment system was developed for application on four lake site types in Germany. Biological lake site types were established using differences in characteristic macrophyte communities, reflecting ecoregion, Ca²⁺ content, mixis and morphology. Ecological status classification of lake sites is based on macrophyte abundance along 275 transects in 95 natural German lakes and the calculation of a reference index value, in some cases supplemented by submerged vegetation data. The reference index quantifies the deviation of species composition and abundance from reference conditions and classifies sites to one of the five ecological quality classes specified in the Directive. Based on an example of Lake Chiemsee, Germany, the possibilities for a wholelake assessment are discussed. (© 2005 WILEY‐VCH Verlag GmbH & Co. KGaA, Weinheim)     

Using chlorophyll a and cyanobacteria in the ecological classification of lakes

Phytoplankton is one of the four key biological quality elements to be used in the ecological classification of lakes in Europe according to the Water Framework Directive (WFD). Chlorophyll a (Chla) has so far been used as the main – and sometimes only – metric to define class boundaries. Chla is often a key metric for lake managers and is used to determine whether and how much action should be taken to reduce the external nutrient loading. In this paper we present the analyses of empirical relationships between nutrient (total phosphorus, TP, total nitrogen, TN) concentrations versus Chla and the proportion of cyanobacteria of total phytoplankton biomass based on data from 440 Danish lakes (1800 lake years). These data represent one eco-region sampled using standardised methodology, thereby minimising the heterogeneity often seen in large datasets. Sampling frequency is important for the precision by which Chla can be determined and the precision is always low with less than 15 summer measurements. As expected Chla was related significantly to TP, but the variability was high, with R² reaching only 0.47, 0.59 and 0.61 in shallow, stratified and siliceous lakes, respectively, based on summer averages. The correlation was strongest in late summer (R² up to 0.80) and weak in winter. Chla is also related to TN, but the correlation coefficients were low throughout the year, and in a multiple regression with TP included, TN only added little to the total variability. Similarly, the proportion of cyanobacteria increased significantly with TP, but the correlation was weak. Seasonal and yearly data from five lakes with relatively stable TP show considerable variations in Chla and cyanobacteria abundance during a 20-year monitoring period. It is concluded that despite clear nutrient phytoplankton relationships it will be difficult to define the proposed WFD ecological classes – particularly regarding cyanobacteria. To ensure a high degree of certainty for meeting a specific water quality threshold, lake managers must reduce the external phosphorus loading more strongly than expected from existing simple empirical external loading-inlake TP–Chla relationships.     

First steps in the Central-Baltic intercalibration exercise on lake macrophytes: where do we start?

The Water Framework Directive (WFD 2000) defines macrophytes as one of the biological groups required for the ecological assessment of European surface waters. Several indices for macrophyte assessment have been proposed or are currently in use by different European states. As a first step towards performing an intercalibration of these indices a common dataset was developed. This dataset contains abundance data on 789 macrophyte species from 316 different lake sites in ten European countries. Various common species and genera were identified as indicators of reference and impacted conditions within the dataset. Cluster analysis of macrophyte data, supported by non-metric multidimensional scaling, indicated that clusters formed were more reflective of their source country rather than lake type. This might be caused by differences in regional climate, biogeography, monitoring techniques, or a combination of these factors. A total of six national indices were applied to assign quality classes to the lakes. However, this produced results that often differed by one or two quality classes for the same site. We foresee that a more precise intercalibration exercise is necessary, and it should be based on more detailed data considering both seasonality and the latitudinal differences within the area covered.     

Use of marker pigments and functional groups for assessing the status of phytoplankton assemblages in lakes

Phytoplankton is a key biological quality element for the establishment of the Water Framework Directive (WFD) ecological status in reservoirs and lakes. In freshwaters, inverted microscope examination is the traditional standard method for estimating phytoplankton and assessing taxonomic composition. Based on the enumeration of algal units and measurements for biovolume calculation, this technique is cumbersome and time-consuming. In large monitoring programmes, such as the application of the WFD in lakes and reservoirs, chemotaxonomy (HPLC pigment analysis and CHEMTAX treatment) is ideally suited as an alternative method because it allows the rapid processing of large numbers of samples from numerous locations and depths, thereby providing ideal temporal and spatial resolution. The low taxonomical detail obtained by HPLC and CHEMTAX (phytoplankton classes or phyla) can easily be overcome by a rapid inverted microscope screening with identification of the dominant species. Combining HPLC and microscopy provides a useful method for monitoring phytoplankton assemblages, which can be used to implement the WFD with respect to phytoplankton. Here, we present the application of a method combining marker pigments and microscopy to phytoplankton samples from 12 Belgian reservoirs. This method substantially reduced the workload and enabled us to assess the status of the phytoplankton assemblage in these lakes. The method complies with the WFD, as it takes into account taxonomic composition, assesses abundance and biomass of the phytoplankton taxa, and easily detects blooms. Additionally, a set of templates of probability of occurrence of phytoplankton functional groups at the maximal ecological potential for reservoirs from the Central/Baltic region is presented, based on reference conditions defined for natural lakes from other regions.     

Performance of a new phytoplankton composition metric along a eutrophication gradient in Nordic lakes

A new phytoplankton metric is presented, which is developed from a large dataset of Norwegian lakes (>2,000 samples from >400 lakes). In contrast to previous metrics, this index is not built on selected ‘indicative’ taxa, but uses all available taxonomic information at genus and species level. Taxa optima with respect to lake trophic status (derived from total phosphorus concentrations) are used to calculate a phytoplankton trophic index (TI) for each sample. Analysis of the TI shows that phytoplankton communities exhibit highly non-linear responses to eutrophication in Norwegian lakes. Reference lakes are characterized by very similar TIs despite having considerable variation in total phosphorus and chlorophyll a concentrations. TI exhibits a non-linear distribution along the eutrophication gradient which separates unimpacted from impacted sites in the study area. We further show that TI exhibits smaller seasonal variations than chlorophyll a, making it a more reliable indicator for lake monitoring. Implications for its applicability within the WFD are discussed.     

Assessing ecological quality of shallow lakes: Does knowledge of transparency suffice?

The European Water Framework Directive (WFD) requires that all aquatic ecosystems in their member states should reach ‘good’ ecological quality by 2015. To assess ecological quality, the WFD requires the definition of reference conditions using biological, physical and chemical indicators and the assignment of each water body to one of five quality classes using these indicators. Elaborate assessment schemes using large sets of variables are now being developed. Here we address the question whether all this is really needed and what the simplest assessment approach would be for the case of shallow lakes. We explore the relationships between the quality class assigned to a lake by experts in shallow lake ecology and a rich set of biological, physical, and chemical data. Multinomial logistic regression analyses were carried out based on data from 86 shallow lakes throughout Europe that were sampled in 2000 and/or 2001. Ecological quality of shallow lakes judged by experts was strongly correlated to physical and chemical variables associated with light regime and nutrients and much less to biological variables.Our regression model showed that ecological quality of this set of shallow lakes judged by experts could be predicted quite well from water transparency expressed as Secchi depth and that other variables did not contribute to it significantly. According to the WFD, lakes should at least have a ‘good’ ecological quality. Quality judged by experts and predicted quality were similar for 78% of the lakes with respect to meeting this standard. As a cautionary note we stress that Secchi depth alone will be a less useful indicator if effects of stressors other than eutrophication (e.g. lake acidification and toxic pollution) are to be considered.     

Biological indicators track differential responses of pelagic and littoral areas to nutrient load reductions in German lakes

External nutrient loading was reduced over the past decades as a measure for improving the water quality of eutrophic lakes in western Europe, and has since been accelerated by the adoption of the European Water Framework Directive (WFD) in 2000 (EC, 2000). A variety of eutrophication-related metrics have indicated that the response of biological communities to this decreased nutrient loading has been diverse. Phytoplankton, a major component of the pelagic community, often responded rapidly, whereas a significant delay was observed for submerged macrophytes colonizing littoral areas. In this study we tested whether assessment methods developed for phytoplankton and macrophytes in lakes during Germany's implementation of the WFD reflect this differential response. An assessment of 263 German lakes confirmed that a lower ecological state was recorded when based on the biological quality element (BQE) for macrophytes than the BQE for phytoplankton during the investigated period (2003–2012). On average, lakes had a moderate ecological status for both phytoplankton and macrophyte BQEs, but differences of up to three classes were observed in single cases. Long-term data were available for five lowland lakes subject to strong reductions in phosphorus loading. Their phytoplankton-based assessments indicated a constant improvement of the ecological status in parallel to decreasing water phosphorus concentrations. In contrast, macrophyte-based assessments indicated a 10–20 year delay in their ecological recovery following nutrient load reduction. This delay was confirmed by detailed data on the temporal development of macrophyte species diversity and maximum colonization depths of two lakes after nutrient load reduction. We conclude that the available WFD assessment methods for phytoplankton and macrophyte BQEs are suitable to track the differential response of pelagic and littoral areas to nutrient load reductions in German lakes.     

A synthesis of the biological quality elements for the implementation of the European Water Framework Directive in the Mediterranean ecoregion: The case of Saronikos Gulf

Benthic macroinvertebrates, macroalgae and phytoplankton constitute the biological quality elements proposed in the Water Framework Directive (WFD, 2000/60/EC) to be used for the classification of the ecological status of a water body. In the context of the preparation for the implementation of WFD, classification schemes for all three elements have been developed and tested for all the European ecoregions. In the present work, the classification schemes, with the corresponding metric tools and the interpretations of the class boundaries according to the normative definitions of WFD, are presented for each biological element in Saronikos Gulf, as case study in the Mediterranean ecoregion. The combination of the three biological elements into an integrated classification for coastal water bodies has been one of the major issues addressed in the context of WFD guidelines. Results are interpreted and validated, through an ecological viewpoint, on the basis of relevant environmental data. Moreover, this work presents a way to combine the EUNIS system to the typology of water bodies in the Mediterranean ecoregion.     

A fish-based index for the assessment of the ecological quality of temperate lakes

A fish – based index for the assessment of the ecological quality of natural temperate lakes was developed, in accordance to the requirements of the Water Framework Directive (WFD) 2000/60/EC. As a case study, 11 natural lakes located at northern and western Greece were selected. Fish surveys were conducted during mid summer to mid autumn in 2010, 2011 and 2012 using Nordic gillnets and electrofishing. Environmental parameters and anthropogenic pressures were assessed for each lake. Fish species richness, abundance, trophic, reproductive and habitat functional guilds were used for extracting a set of 107 metrics, meeting the requirements of the WFD. All metrics were initially tested as candidates for the index development. A stepwise linear regression of each metric against environmental parameters (lake area, altitude, maximum depth, alkalinity) and anthropogenic pressures (drainage area covered by non-natural land uses – NNLC, water total phosphorus concentrations – TP, Lake Habitat Modification Score – LHMS) was initially conducted for ensuring pressure-response relationships. Reference conditions for each lake were estimated by the hindcasting procedure and the ecological quality for each lake was expressed as the ecological quality ratio (EQR) by a value ranging from 0 (poor quality) to 1 (excellent quality). Two fish fauna metrics, the relative numerical abundance of introduced species (Introduced_a) and the relative biomass of omnivorous species (OMNI_b) were finally extracted as the most significant, responding to LHMS and TP, respectively. The final index was expressed as the mean values of the EQRs of these two metrics. The multimetric fish index presented herein could serve as a tool for assessing the ecological quality of natural lakes at broad geographical scale and generally, in the Mediterranean temperate lakes with similar hydromorphological characteristics.