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.     

Nutrient optima and tolerances of benthic invertebrates,the effects of taxonomic resolution and testing of selected metrics in lakes using an extensive European data base

A large dataset from 1,077 lakes in Finland, Ireland, Sweden and the United Kingdom was collated to analyse the relationship between nutrient status and occurrence of different taxa, as well as between total phosphorus or chlorophyll and commonly used macroinvertebrate metrics developed for river assessment. We found that most taxa were associated with mesotrophic conditions (sensu OECD). Species associated with oligotrophic status included Baetis rhodani, Gammarus lacustris and plecopteran larvae, a group commonly associated with low nutrient status also in rivers. Species tolerant of eutrophic conditions were the chironomid larvae (Chironomus plumosus and Cryptochironomus defectus); and two species of tubificids (Psammoryctides barbatus and Potamothrix hammoniensis). For a number of taxa the associations of benthic invertebrates with nutrient state reported in the literature were not supported by analysis of the REBECCA data. The analysis indicated a variable response of littoral macroinvertebrates to eutrophication pressure when using common metrics developed for macroinvertebrates in rivers. Several metrics showed significantly different responses in lakes with different alkalinity, justifying the use of alkalinity for typing water bodies. These significant responses suggest that benthic invertebrates may be a useful component for classification of ecological status in lakes. The low amount of variance explained by the regressions (<30%), however, suggests that further harmonisation of sampling methods, as well as statistically more robust assessment tools are needed to increase the comparability of datasets and to improve the precision in the dose–response relationships.     

Classifying aquatic macrophytes as indicators of eutrophication in European lakes

Aquatic macrophytes are one of the biological quality elements in the Water Framework Directive (WFD) for which status assessments must be defined. We tested two methods to classify macrophyte species and their response to eutrophication pressure: one based on percentiles of occurrence along a phosphorous gradient and another based on trophic ranking of species using Canonical Correspondence Analyses in the ranking procedure. The methods were tested at Europe-wide, regional and national scale as well as by alkalinity category, using 1,147 lakes from 12 European states. The grouping of species as sensitive, tolerant or indifferent to eutrophication was evaluated for some taxa, such as the sensitive Chara spp. and the large isoetids, by analysing the (non-linear) response curve along a phosphorous gradient. These thresholds revealed in these response curves can be used to set boundaries among different ecological status classes. In total 48 taxa out of 114 taxa were classified identically regardless of dataset or classification method. These taxa can be considered the most consistent and reliable indicators of sensitivity or tolerance to eutrophication at European scale. Although the general response of well known indicator species seems to hold, there are many species that were evaluated differently according to the database selection and classification methods. This hampers a Europe-wide comparison of classified species lists as used for the status assessment within the WFD implementation process.     

Macroinvertebrate indicators of lake acidification: analysis of monitoring data from UK, Norway and Sweden

Although the acid sensitivity of many invertebrate species in lakes is well known, methods for assessment of lake acidification based on macroinvertebrate samples are less developed than for rivers. This article analyses a number of existing metrics developed for assessment of river acidification, and evaluates their performance for assessment of lake acidification. Moreover, new species-based indicators of lake acidification were developed and tested. The selected dataset contains 668 samples on littoral macroinvertebrates from 427 lakes with almost 60% of the samples from Sweden and the rest from UK and Norway. Flexible, non-parametric regression models were used for explorative analyses of the pressure–response relationships. The metrics have been assessed according to their response to pH, the degree of non-linearity of the response and the influence of humic compounds. Acid-sensitive metrics often showed a threshold in response to pH between 5.8 and 6.5. Highly acid-tolerant metrics were typically dominant across the whole pH range. Humic level had a positive effect for most acid-sensitive metrics. Generally, most metrics showed a more non-linear response pattern for the humic lakes than for clear lakes. The significant relationship between these macroinvertebrate metrics and acidification shows that there is a potential for developing further the assessment systems for ecological quality of lakes based on these metrics, although the metrics explained a low % of the variation (<30%). In order to improve the predictive power of the biotic metrics across the acidified part of Europe, further harmonization and standardisation of sampling effort and taxa identification are needed.     

Incorporating invasive weeds into a plant indicator method (LakeSPI) to assess lake ecological condition

The use of lake macrophytes for ecological quality assessments usually seeks to indicate the degree of anthropogenic impact, but few of these schemes implicitly consider impacts of alien weeds. LakeSPI (submerged plant indicators) uses indicators of habitat degradation for macrophytes but also incorporates the degree of impact from alien weeds. Application of LakeSPI to 195 New Zealand lakes provided a dataset to examine how component metrics responded over gradients of anthropogenic pressures, and consider whether weed invasion was merely a ‘passenger’ of habitat degradation, or represented an additional pressure. As expected, metrics measuring depth, and diversity of native vegetation negatively correlated with independent measures of lake eutrophy and were also relatively well explained (69–78% variation) by multiple regression with lake and catchment attributes that included proxies for anthropogenic pressure. In contrast, metrics for invasive impact were largely de-coupled from eutrophication, and poorly explained (31%) by the multiple regression. The response of native vegetation metrics to invasive impact measures varied, with the strongest detected interaction relating to native displacement by increased weed occupation of the vegetated zone. Interactions between invasion and lake trophic status were also discerned, with the extent of weed occupation having a more substantial outcome for the presence of charophyte meadows in low productivity lakes than in more productive lakes. These results suggest weed invasion should be considered as an additional source of anthropogenic pressure, and incorporated in macrophyte bioassessment schemes for a more complete differentiation of lake ecological condition.     

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.     

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.     

Zooplankton as indicators in lakes: a scientific-based plea for including zooplankton in the ecological quality assessment of lakes according to the European Water Framework Directive (WFD)

With the implementation of the EU Water Framework Directive (WFD), the member states have to classify the ecological status of surface waters following standardised procedures. It was a matter of some surprise to lake ecologists that zooplankton were not included as a biological quality element (BQE) despite their being considered to be an important and integrated component of the pelagic food web. To the best of our knowledge, the decision of omitting zooplankton is not wise, and it has resulted in the withdrawal of zooplankton from many so-far-solid monitoring programmes. Using examples from particularly Danish, Estonian, and the UK lakes, we show that zooplankton (sampled from the water and the sediment) have a strong indicator value, which cannot be covered by sampling fish and phytoplankton without a very comprehensive and costly effort. When selecting the right metrics, zooplankton are cost-efficient indicators of the trophic state and ecological quality of lakes. Moreover, they are important indicators of the success/failure of measures taken to bring the lakes to at least good ecological status. Therefore, we strongly recommend the EU to include zooplankton as a central BQE in the WFD assessments, and undertake similar regional calibration exercises to obtain relevant and robust metrics also for zooplankton as is being done at present in the cases of fish, phytoplankton, macrophytes and benthic invertebrates.     

A phytoplankton trophic index to assess the status of lakes for the Water Framework Directive

Despite improvements in wastewater treatment systems, the impact of anthropogenic nutrient sources remains a key issue for the management of European lakes. The Water Framework Directive (WFD) provides a mechanism through which progress can be made on this issue. The Directive requires a classification of the ecological status of phytoplankton, which includes an assessment of taxonomic composition. In this paper, we present a composition metric, the plankton trophic index, that was developed in the WISER EU FP7 project and demonstrate how it has been used to compare national phytoplankton classification systems in Northern and Central Europe. The metric was derived from summer phytoplankton data summarised by genus from 1,795 lakes, covering 20 European countries. We show that it is significantly related to total phosphorus concentrations, but that it is also sensitive to alkalinity, lake size and climatic variables. Through the use of country-specific reference values for the index, we demonstrate that it is significantly related to other national phytoplankton assessment systems and illustrate for a single European (intercalibration) lake type how it was used to intercalibrate WFD boundaries from different countries.     

Acidification and alkalinization of lakes by experimental addition of nitrogen compounds

Fertilization of a small lake with ammonium chloride for four years as part of a eutrophication experiment caused it to acidify to pH values as low as 4.6. Implications for acidification of lakes via precipitation polluted with ammonium compounds are discussed.When phosphate was supplied with the ammonium, biological nitrogen uptake, apparently by phytoplankton, was the main mechanism causing acidification. When ammonium was applied without phosphate, it accumulated to high concentrations in solution, after which nitrification caused rapid acidification. In both cases, the whole-lake efficiency of acidification was low, averaging about 13% of the potential acidification of supplied ammonium chloride (Table 2).Subsequent application of phosphate plus sodium nitrate for two years caused the pH of the lake to increase. The efficiency of alkalinization was higher than for acidification, averaging 69% of the potential alkalinization of the supplied sodium nitrate.     

Ecological assessment of running waters: Do macrophytes,macroinvertebrates, diatoms and fish show similar responses to human pressures?

This study aimed to compare the intensity and the sensitivity of the responses of four river biological quality elements (BQEs) – macrophytes, fish, diatoms and macroinvertebrates – to human pressures excluding natural variations in stream ecosystem functioning. Biological, water quality and hydro-morphological data were compiled for 290 French river sites.Out of the 93 metrics tested, 51 covering the four BQEs responded significantly to global degradation. The responses to specific pressures were consistent with the BQEs’ ecological and biological characteristics. For the four BQEs, metrics responded strongly to water quality degradations. Like fish, macroinvertebrate metrics were very sensitive to morphological degradations such as the presence of an impoundment, while diatom and macrophyte metrics did not show strong responses to these changes. Among the four BQEs’ metrics, fish metrics responded the strongest to hydrological perturbations. Although a high proportion of the metrics responded only to high levels of human-induced degradations, trait-based metrics seemed the most sensitive and responded to lower levels of pressure. Global and water quality degradations of the river appear to be better detected by BQE metrics than channel morphological and hydrological degradations. Our results highlight the different impacts of human-induced pressures on the four BQE metrics and the challenging task of assessing the effect of single pressures when most of sites are multi-impacted.     

Strength and uncertainty of phytoplankton metrics for assessing eutrophication impacts in lakes

Phytoplankton constitutes a diverse array of short-lived organisms which derive their nutrients from the water column of lakes. These features make this community the most direct and earliest indicator of the impacts of changing nutrient conditions on lake ecosystems. It also makes them particularly suitable for measuring the success of restoration measures following reductions in nutrient loads. This paper integrates a large volume of work on a number of measures, or metrics, developed for using phytoplankton to assess the ecological status of European lakes, as required for the Water Framework Directive. It assesses the indicator strength of these metrics, specifically in relation to representing the impacts of eutrophication. It also examines how these measures vary naturally at different locations within a lake, as well as between lakes, and how much variability is associated with different replicate samples, different months within a year and between years. On the basis of this analysis, three of the strongest metrics (chlorophyll-a, phytoplankton trophic index (PTI), and cyanobacterial biovolume) are recommended for use as robust measures for assessing the ecological quality of lakes in relation to nutrient-enrichment pressures and a minimum recommended sampling frequency is provided for these three metrics.     

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.     

Quantitative responses of lake phytoplankton to eutrophication in Northern Europe

Based on the currently largest available dataset of phytoplankton in lakes in northern Europe, we quantified the responses of three major phytoplankton classes to eutrophication. Responses were quantified by modelling the proportional biovolumes of a given group along the eutrophication gradient, using generalized additive models. Chlorophyll-a (Chl-a) was chosen as a proxy for eutrophication because all classes showed more consistent responses to Chl-a than to total phosphorus. Chrysophytes often dominate in (ultra-) oligotrophic lakes, and showed a clear decrease along the eutrophication gradient. Pennate diatoms were found to be most abundant at moderate eutrophication level (spring-samples). Cyanobacteria often dominate under eutrophic conditions, especially in clearwater lakes at Chl-a levels >10 μg l⁻¹ (late summer samples). We compare the relationships among types of lakes, based on the lake typology of the northern geographic intercalibration group, and among countries sharing common lake types. Significant differences were found especially between humic and clearwater lakes, and between low- and moderately alkaline lakes, but we could not identify significant differences between shallow and deep lakes. Country-specific differences in response curves were especially pronounced between lakes in Norway and Finland, while Swedish lakes showed an intermediate pattern, indicating that country-specific differences reflect large-scale geographic and climatic differences in the study area.     

Influence of aquatic macrophytes on phosphorus cycling in lakes

Emergent macrophytes take up their phosphorus exclusively from the sediment. Submerged species obtain phosphorus both from the surrounding water and from the substrate, but under normal pore and lake water phosphorus concentrations, substrate uptake dominates. Release of phosphorus from actively growing macrophytes (both submerged and emergent) is minimal and epiphytes obtain phosphorus mainly from the water. Decaying macrophytes may act as an internal phosphorus source for the lake and add considerable quantities of phosphorus to the water. A large part of the released phosphorus is often retained by the sediments. In perennial macrophytes the amount of phosphorus released from decaying shoots is dependent on the degree of phosphorus conservation within the plant. Macrophyte stands may also be a permanent phosphorus sink due to burial of plant litter. Macrophytes affect the chemical environment (oxygen, pH), which in turn has effects on the phosphorus cycling in lakes. However, the impact of aquatic macrophytes on whole-lake phosphorus cycling is largely unknown. Controlled full-scale harvesting, herbicide or herbivory experiments are almost totally lacking. Emergent macrophytes respond positively to eutrophication, but fertilization experiments have shown that nitrogen rather than phosphorus may be the key element. Submerged macrophytes are adversely affected by a large increase in the external phosphorus input to a lake. This effect may be caused by epiphyte shading, phytoplankton shading or deposition of unfavourable sediments.     

Submerged macrophytes as indicators of the ecological quality of lakes

1. We analysed submerged macrophyte communities from 300 Danish lakes to determine the efficacy of different species, maximum colonisation depth (C_max) of plants as well as coverage and plant volume inhabited (PVI) as indicators of eutrophication. 2. Most species occurred at a wide range of phosphorus and chlorophyll a (Chla) concentrations, but some species of isoetids (Lobelia, Isoëtes) and Potamogeton (Potamogeton gramineus, Potamogeton alpinus and Potamogeton filiformis) were mainly found at low nutrient concentrations and hence may be considered as indicators of nutrient poor conditions. However, species typically found in nutrient‐rich conditions, such as Elodea canadensis and Potamogeton pectinatus, were also found at total phosphorus (TP) <0.02 mg P L^?1 and Chla <5 μg L^?1 and therefore cannot be considered as reliable indicators of eutrophic conditions. 3. Submerged macrophyte coverage, PVI and the C_max were negatively correlated with TP and Chla. However, variability among lakes was high and no clear thresholds were observed. At TP between 0.03 and 0.07 mg P L^?1 plant coverage in shallow lakes ranged from nearly 0 to 100%, whilst at concentrations between 0.10 and 0.20 mg P L^?1 only 29% of the lakes had coverage >10%. C_max was found to be a useful indicator only in deep lakes with unvegetated areas in the deeper part, whereas the use of coverage was restricted to shallow lakes or shallow areas of deep lakes. 4. Overall, submerged macrophytes responded clearly to eutrophication, but the metrics investigated here showed no well‐defined thresholds. We developed a simple index based on species richness, presence of indicator species, coverage and C_max, which might be used to track major changes in macrophyte communities and for lake classification.     

Quantifying the relative importance of natural variables,human disturbance and spatial processes in ecological status indicators of boreal lakes

Spatial processes are increasingly associated with species distributions in freshwaters. However, these processes are usually neglected in bioassessment techniques, which may introduce uncontrolled variation in ecological indicators used to express human disturbance. We used partial linear regression to quantify the relative importance of natural variables, human disturbance and spatial variables in structuring variation in boreal lake status indicators based on six biological indicator groups (phytoplankton, macrophytes, diatoms, littoral and profundal macroinvertebrates and fish). We found that, of the pure fractions, human disturbance explained most variation (7–32%) of the ecological quality ratios (EQRs) for all groups, with the exception of littoral macroinvertebrate metric, which was most controlled by natural and spatial variables (15% and 16%, respectively). In addition, pure fractions of natural and spatial variables and joint fractions of different explanatory variable groups structured all biological metrics to various degrees. Phytoplankton, diatom and profundal macroinvertebrate EQRs responded purest to human disturbance but only weakly to pure natural or spatial variation. Our work demonstrates that spatial processes and spatial structuring of the environment can bias bioassessment techniques and hinder the detection of human impact. Thus, it is important to acknowledge spatial autocorrelation, context of metacommunity dynamics, species dispersal traits and variable spatial extent when defining reference conditions and bioassessment techniques for different biological groups. More research is needed to better understand the relative role of spatial processes on ecological metrics originated from different freshwater ecosystems. To this end, our work provides an example of how sources of variation can be identified to increase accuracy in freshwater bioassessment.     

Plant community structure determines primary productivity in shallow,eutrophic lakes

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