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.     

Reference conditions and WFD compliant class boundaries for phytoplankton biomass and chlorophyll-a in Alpine lakes

The intercalibration (IC) exercise is a key element in the implementation of the Water Framework Directive (WFD) in Europe. Its focus lies on the harmonization of national classification methods to guarantee a common understanding of ‘Good Ecological Status’ in surface waters. This article defines reference conditions and sets class boundaries for deep (mean depth >15 m, IC lake type L-AL3) and moderately deep (mean depth 3–15 m, IC lake type L-AL4) Alpine lakes >0.5 km². Data were collated from each of the five EU member states included in the Alpine Geographical Intercalibration Group (Alpine GIG: Austria, France, Germany, Italy and Slovenia). Hydro-morphological, chemical and biological data from 161 sites (sampling stations) in 144 Alpine lakes over a period of seven decades were collated in a database. Based on a set of reference criteria, 18 L-AL3 and 13 L-AL4 reference sites were selected. Reference conditions were defined using a combined approach, based on historical, paleolimnological and monitoring data in conjunction with trophic modelling and expert judgement. Reference values and class boundaries were set for annual mean total biomass (biovolume), and then derived for annual mean chlorophyll-a using a regression between the two parameters. In order to allow for geographical differences within the Alpine GIG and to facilitate the inclusion of the broadly defined common IC types and national lake types, ranges were defined for each reference value. Range of reference values are 0.2–0.3 mg l^?1 (L-AL3) and 0.5–0.7 mg l^?1 (L-AL4) for total biovolume and 1.5–1.9 μg l^?1 (L-AL3) and 2.7–3.3 μg l^?1 (L-AL4) for chlorophyll-a. Depending on lake type and variable, the ecological quality ratios (EQR) for setting the class boundaries lie between 0.60 and 0.75 for the high/good class boundary and between 0.25 and 0.41 for the good/moderate class boundary. The response of sensitive phytoplankton taxa along a nutrient gradient and the occurrence of ‘undesirable conditions and secondary effects’ as defined in the WFD was used to validate the class boundary values, which are thus considered to be compliant with the requirements of the WFD.     

Reference conditions for phytoplankton at Danish Water Framework Directive intercalibration sites

Phytoplankton is one of the biological quality elements included in the EU Water Framework Directive (WFD). Classification of water quality according to the WFD is based on the deviation of the present conditions from reference conditions. Given the lack of data from pristine conditions, this study used approximately 100-year-old measurements of Secchi depths from Danish waters in combination with relationships between Secchi depth and chlorophyll a (as a proxy for phytoplankton biomass) obtained from recent monitoring to calculate ‘historical’ or reference chlorophyll a (Chl-a) concentrations. Historical Secchi depth data were available for 9 out of the 11 Danish WFD intercalibration sites. At eight of the sites, reference summer (May–September) Chl-a concentrations were in the range 0.7–1.2 μg l⁻¹. At one site, west of Bornholm in the western Baltic Sea, historical Secchi depth measurements date back to only the late 1950s corresponding to a calculated Chl-a concentration of 1.3 μg l⁻¹. This value cannot be considered representative of reference conditions. Guest editors: J. H. Andersen & D. J. Conley Eutrophication in Coastal Ecosystems: Selected papers from the Second International Symposium on Research and Management of Eutrophication in Coastal Ecosystems, 20–23 June 2006, Nyborg, Denmark     

Extending the phytoplankton tool kit for the UK Water Framework Directive: indicators of phytoplankton community structure

The Water Framework Directive (WFD) demands consideration of normative definitions for assessing ecological state of marine waters. For phytoplankton, ‘deviations from the ideal’ need to be considered for species composition and abundance, average biomass and the occurrence of blooms. A combination of phytoplankton metrics has been developed which, when considered in combination, should provide a confident assessment of the ecological state of each water body under assessment. The aim of this study was to evaluate phytoplankton community structure in different coastal and estuarine water bodies within England and Wales, and to contribute evidence towards the development of a community-based phytoplankton indicator. Influences of seasonality on the species assemblage were tested using a long-term data set available from a long-term monitoring site just offshore of Plymouth, UK. There is a substantive seasonal influence to the data, with a maximum of 10–14 common species (out of a potential 20) reoccurring within the same calendar month over a 10-year time span. Comparisons between reference and test water bodies give a range of common species of between 3 and 11 species within water type and season. A statistical and qualitative approach for comparing the most common species occurring between a reference and test site were tested for development of a WFD phytoplankton assessment tool. Overall, the results indicate that there are distinct phytoplankton assemblages over seasons which could form the basis of a community assessment metric. However, differences in boundary conditions are negligible between the different areas. There is evidence that community populations may be ubiquitous across marine water types in England and Wales, and development of generic seasonal lists across typologies could be appropriate in the further development of this tool.     

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.     

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.     

Determining algal assemblages in oligotrophic lakes and streams: comparing information from newly developed pigment/chlorophyll a ratios with direct microscopy

1. Pigment analyses by high performance liquid chromatography (HPLC) are commonly used for determining algal groups in marine and estuarine areas but are underdeveloped in freshwaters. In this study, 15 characteristic pelagic algal species (representing five algal groups) of oligo‐ / mesotrophic lakes were cultured and pigment / Chl a ratios determined at three light intensities. 2. With the exception of cyanophytes, light treatment had little effect on pigment / Chl a ratios. This justifies the use of the same pigment / Chl a ratios during seasonal studies where light conditions may change. 3. The determined pigment / Chl a ratios were tested on seasonal samples from five oligo‐ / mesotrophic lakes and three streams using CHEMTAX software. Pigment ratios of both pelagic and benthic algal communities from the lakes and streams were analysed to determine whether the pelagic algae‐based ratios can be used for benthic algal communities. 4. HPLC combined with CHEMTAX was useful for identifying freshwater phytoplankton classes and for quantifying the abundance of phytoplankton groups. However, although correlations were significant for six of seven phytoplankton classes studied, they were weak and varied with season. 5. HPLC was valid for quantifying benthic diatom groups in stream samples, whereas for lakes more benthic algal groups were recorded with HPLC than with microscopy and correlations between the two methods were not significant. 6. The use of both HPLC and microscopy is recommended as a cost‐efficient method for analysing many samples. It is crucial, however, that the CHEMTAX software is calibrated with the correct information, and the user is aware of the limitations.     

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.     

Ecological classification of lakes: Uncertainty and the influence of year-to-year variability

Regular monitoring of lakes is important to determine their ecological state and development and of key significance when deciding whether action should be taken to improve their quality, for instance by reducing the external loading of nutrients. Imprecise or inadequate knowledge of the ecological state increases the risk of misclassification and of wrong management decisions. Based on Danish lake data, we aimed to determine temporal variations, in particular natural year-to-year differences, and to describe the uncertainty in assessing the ecological state of lakes. We analysed environmental data from ca. 350 Danish lakes (1100 lake years), including three case studies, with long-term data series (up to 24 years), with no significant changes in external nutrient loading. We used summer means of selected water chemical variables, phytoplankton and submerged macrophytes as indicators of ecological state and found considerable variations in all indicators, which could not be ascribed alone to meteorological variation. In shallow lakes, chlorophyll a concentrations exhibited large year-to-year variations, especially at TP ranging between 0.05 and 0.15 mg L⁻¹ where the lakes may shift between a macrophyte- and a phytoplankton-dominated state. For example, chlorophyll a varied by a factor 5–10 between years and was particularly low when submerged macrophyte coverage exceeded 20% compared with lakes without macrophytes. Use of a multimetric index including four phytoplankton indicators reduced the coefficient of variation. Generally, the 95% confidence interval of ecological classification was approximately 50% lower when the assessment of ecological state was based on 4–5 years’ measurements than if based on only one year's measurements. Knowledge and awareness of the uncertainty of indicators used in ecological classification are highly relevant for lake managers and policy makers when defining efficient monitoring and restoration strategies.     

Nitrate availability and hydrophyte species richness in shallow lakes

1. Submerged plant richness is a key element in determining the ecological quality of freshwater systems; it has often been reduced or completely lost. 2. The submerged and floating‐leaved macrophyte communities of 60 shallow lakes in Poland and the U.K. have been surveyed and species richness related to environmental factors by general linearised models. 3. Nitrogen, and more specifically winter nitrate, concentrations were most important in explaining species richness with which they were inversely correlated. Phosphorus was subsidiary. Such an inverse relationship is consistent with findings in terrestrial communities. Polish lakes, with less intensively farmed catchments, had greater richness than the U.K. lakes. 4. The richest U.K. communities were associated with winter nitrate‐N concentrations of up to about 1–2 mg L^?1 and may correspond with ‘good’ ecological quality under the terms of the European Water Framework Directive. Current concentrations in European lowlands are often much higher.     

Relationships between morphometry,geographic location and water quality parameters of European lakes

I addressed the question how lake and catchment morphometry influences water chemistry and water quality over a large scale of European lakes, and developed the regression equations between most closely related morphometric and water quality indices. I analysed the data of 1,337 lakes included in the European Environment Agency (EEA) database, carrying out separate analyses for three basic lake types: large lakes (area ≥100 km², 138 lakes), shallow lakes (mean depth ≤3 m, 153 lakes) and large and shallow lakes (area ≥100 km² and mean depth ≤8 m, 35 lakes). The study revealed that in Europe, the lakes towards North are larger but shallower and have smaller catchment areas than the southern lakes; lakes at higher altitudes are deeper and smaller and have smaller catchment areas than the lowland lakes. Larger lakes have generally larger catchment areas and bigger volumes, and they are deeper than smaller lakes, but the relative depth decreases with increasing surface area. The lakes at higher latitudes have lower alkalinity, pH and conductivity, and also lower concentrations of nitrogen and phosphorus while the concentration of organic matter is higher. In the lakes at higher altitudes, the concentration of organic matter and nutrient contents are lower and water is more transparent than in lowland lakes. In larger lakes with larger catchment area, the alkalinity, pH, conductivity and the concentrations of nutrients and organic matter are generally higher than in smaller lakes with smaller catchments. If the lake is deep and/or its residence time is long, the water is more transparent and the concentrations of chlorophyll a, organic matter and nutrients are lower than in shallower lakes with shorter residence times. The larger the catchment area is with respect to lake depth, area and volume, the lower is the water transparency and the higher are the concentrations of the nutrients, organic matter and chlorophyll as well as pH, alkalinity and conductivity. The links between lake water quality and morphometry become stronger towards large and shallow lakes. Along the decreasing gradients of latitude, altitude and relative depth, the present phosphorus concentration and its deviation from the reference concentration increases.     

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.     

Austrian Index Macrophytes (AIM-Module 1) for lakes: a Water Framework Directive compliant assessment system for lakes using aquatic macrophytes

We describe a new macrophyte-based assessment tool for Austrian lakes elaborated according to the requirements of the European Water Framework Directive. Data from 38 out of 45, WFD-relevant (≥50 ha) lakes in Austria collected with the help of a new mapping procedure form the basis for a macrophyte-based lake typology and the definition of reference conditions. Module 1 of the Austrian Index Macrophytes (AIM) focuses on the assessment of trophic state and general impairment of lakes. Several metrics were developed and applied in combination with existing indices to classify lakes into five ecological status classes. The metric “vegetation density” focuses on the overall abundance of macrophytes. Since the lower limit of the macrophyte vegetation in lakes is mainly regulated by the water transparency, the metric “vegetation limit” is closely related to the trophic state of the lake. In deep lakes, macrophytes normally form different vegetation zones. As a result of alteration of the shoreline, artificial water level fluctuations or wave action and even eutrophication, specific zones can be missing. The metric “characteristic zonation” helps to check, if all type-specific vegetation zones are present. The metric “trophic indication” uses the Macrophyte Index after Melzer (Hydrobiologia, 395/396: 181–190, 1999). This term indicates the lake trophic state but, in contrast to the metric “vegetation limit”, it tends to show not only the trophic state of the water column but also, in particular, the nutrient conditions in the sediment. With the help of the metric “species composition,” the species spectrum and the species abundances of the current transect are compared with the species composition at reference sites. The similarity of the datasets is measured as Bray–Curtis Distance (Beals, Advances in Ecological Research, 14: 1–55, 1984). The established metrics cover different aspects of macrophyte vegetation and allow analysing the prevailing pressure. Since the different metrics have a different temporal response to eutrophication and reoligotrophication, additional information on the current state of the lake in relation to these processes can be derived. The successful application of AIM-Module 1 is presented for two Austrian lakes and discussed in relation to other assessment tools. Guest editors: P. N?ges, W. van de Bund, A.C. Cardoso, A. Solimini & A.-S. Heiskanen Assessment of the Ecological Status of European Surface Waters     

Assessment of eutrophication pressure on lakes using littoral invertebrates

Until the E.U. Water Framework Directive listed benthic invertebrates as a biotic element to be used for ecological classification of lakes, techniques for the assessment of the response of littoral invertebrates to anthropogenic pressures were extremely limited compared with those of rivers and lake profundal zones. We describe here the development of an ecological classification model based on changes of littoral invertebrate assemblages across a gradient of eutrophication, which is the most widespread anthropogenic pressure on lakes across Europe. The model comprises three derived parameters, two of which were developed from taxon-specific optima along a total phosphorus gradient calculated using canonical correspondence analysis, and the third based on invertebrate abundance. Combining the parameter metrics, we can estimate the ecological quality ratio (EQR), relative to those from paleolimnologically-confirmed reference lakes. The model was tested using independent samples collected from both hard and soft substrata and across two seasons from 45 lakes, comprising three alkalinity groups (n = 15 in each), and across gradients in water column total phosphorus concentrations. For hard substrata, EQRs were related consistently and highly significantly to water column concentrations of total phosphorus, accounting for the majority of the variance in every alkalinity group. For samples taken from soft substrata, a significant relationship was found only for high alkalinity lakes, accounting for a moderate proportion of the variability in water column total phosphorus concentrations. Our results compare highly favourably with those from other aquatic ecological assessment methods, irrespective of the faunal or floral group upon which they are based, demonstrating that littoral invertebrate assemblages can provide a statistically robust prediction of nutrient status when samples are collected from hard substrata. While the method was developed specifically to assess nutrient pressures on littoral invertebrates, many lakes are subject to multiple pressures. The development of classification models that incorporate multiple pressures presents a particularly significant challenge for the implementation of the Water Framework Directive, requiring both reliable identification of minimally-impacted reference states and incorporation of pressures that are unlikely to interact in predictable ways.     

Uncertainty in ecological status assessments of lakes and rivers using diatoms

The EU’s Water Framework Directive requires all surface water bodies to be classified according to their ecological status. As biological communities show both spatial and temporal heterogeneity, expressions of ecological status will, inevitably, have an element of uncertainty associated with them. A consequence of this environmental heterogeneity is that there is a risk that status inferred from one or more samples is different to the true status of that water body. In order to quantify the scale of temporal uncertainty associated with benthic diatoms, replicate samples were collected from sites across the ecological status gradient in lakes and rivers in the UK. Variability (expressed as standard deviation of temporal replicate samples from a single site) could be described using a polynomial function and this was then used to calculate the risk of placing a water body in the wrong ecological status class. This risk varied depending on the distance from the class boundaries and the number of replicates. Based on these data, we recommend that ecological status is determined from a number of samples collected from a site over a period of time.