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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Estimating confidence of European WFD ecological status class and WISER Bioassessment Uncertainty Guidance Software (WISERBUGS)

The Water Framework Directive (WFD) requires estimates of the confidence and precision associated with any scheme for assessing and monitoring the ecological status class of any European rivers, lakes, transitional or coastal waters. This is a complex important issue, especially for waterbody assessments based on multiple metrics and/or two or more taxonomic groups. This paper aims to contribute towards improving understanding and providing practical approaches to assessing confidence of class by (i) discussing the various sources and causes of uncertainty, (ii) using UK rivers macroinvertebrate datasets to illustrate the estimation of replicate, temporal and spatial variance components and the implications for water body metric precision, confidence of class and optimal sampling design, (iii) introducing new freely available general software WISER Bioassessment Uncertainty Guidance Software (WISERBUGS) which uses prior sampling uncertainty estimates with user-specified metrics, class limits and metric combination rules to simulate the joint sampling uncertainty in metric EQR values and provide estimates of confidence of class based on individual metrics, (optionally weighted) multi-metric indices and/or multi-metric classification rules (worst case, mean or median class) based on one or more WFD biological quality elements.     

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.     

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.     

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.     

湖泊富营养化治理的生态工程

1996年对长春南湖的富营养化实施了生治理工作,调查结果表明,通过收获水生高等植物和鱼产品带出湖体的P量分别为149．6和189．9kg,通过蚌体生长固定的P量为153.4kg,三者合计492.9kg,与湖体会年P输入量大体持平,生态工程运转后,水质明显好转,湖水中的总P浓度逐年下降,浮游植物个体密度减小,种类数增加,生态工程是城市湖泊富营养化治理较为理想的方法。     

Measurements of uncertainty in macrophyte metrics used to assess European lake water quality

Uncertainty is an important factor in ecological assessment, and has important implications for the ecological classification and management of lakes. However, our knowledge of the effects of uncertainty in the assessment of different ecological indicators is limited. Here, we used data from a standardized campaign of aquatic plant surveys, in 28 lakes from 10 European countries, to assess variation in macrophyte metrics across a set of nested spatial scales: countries, lakes, sampling stations, replicate transects, and replicate samples at two depth-zones. Metrics investigated in each transect included taxa richness, maximum depth of colonisation and two indicators of trophic status: Ellenberg’s N and a metric based on phosphorus trophic status. Metrics were found to have a slightly stronger relationship to pressures when they were calculated on abundance data compared to presence/absence data. Eutrophication metrics based on helophytes were found not to be useful in assessing the effects of nutrient pressure. These metrics were also found to vary with the depth of sampling, with shallower taxa representing higher trophic status. This study demonstrates the complex spatial variability in macrophyte communities, the effect of this variability on the metrics, and the implications to water managers, especially in relation to survey design.     

Ecological threshold responses in European lakes and their applicability for the Water Framework Directive (WFD) implementation: synthesis of lakes results from the REBECCA project

The objective of this synthesis is to present the key messages and draw the main conclusions from the work on lakes in the REBECCA project, pointing out their links to theoretical ecology and their applicability for the WFD implementation. Type-specific results were obtained from analyses of large pan-European datasets for phytoplankton, macrophytes, macroinvertebrates and fish, and indicators and relationships showing the impact of eutrophication or acidification on these biological elements were constructed. The thresholds identified in many of the response curves are well suited for setting ecological status class boundaries and can be applied in the intercalibration of classification systems. Good indicators for phytoplankton (chrysophytes, cyanobacteria) and macrophytes (isoetids and charaphytes) responses to eutrophication were identified, and the level of eutrophication pressure needed to reach the thresholds for these indicators was quantified. Several existing metrics developed for macrophytes had low comparability and need further harmonisation to be useful for intercalibration of classification systems. For macroinvertebrates, a number of metrics developed for rivers turned out to be less useful to describe lake responses to eutrophication and acidification, whereas other species based indicators were more promising. All the biological elements showed different responses in different lake types according to alkalinity and humic substances, and also partly according to depth. Better harmonisation of monitoring methods is needed to achieve better precision in the dose–response curves. Future research should include impacts of hydromorphological pressures and climate change, as well as predictions of timelags involved in responses to reduction of pressures.     

太湖浮游植物优势种长期演化与富营养化进程的关系

利用1991年至2002年每月一次的监测资料,系统分析了浮游植物优势种和生物量的周年变化情况。同时,总氮、总磷和浮游植物叶绿素a含量等相关资料也被用于解释太湖富营养化演化与浮游植物的关系。结果显示,太湖总氮、总磷、叶绿素a和生物量均呈自梅梁湾底至湖心的逐步递减趋势。在20世纪80年代末太湖刚开始富营养化时,浮游植物优势种群从硅藻转变为蓝藻。之后,浮游植物优势种群一直是蓝藻,但各年的浮游植物总生物量有变化。总氮、总磷、叶绿素a和生物量的年均值持续增长至1996年,其后有逐步下降的趋势,究其原因可能和当地政府在太湖流域的控制排污行动有关。微囊藻在太湖的占优是太湖富营养化的标志之一。研究结果说明浮游植物在大型浅水湖泊中可以作为反映富营养化进程的生态指标。     

Ecological quality scales based on phytoplankton for the implementation of Water Framework Directive in the Eastern Mediterranean

Structural changes of phytoplankton communities, often expressed through ecological indices, constitute one of the metrics for the implementation of the European Water Framework Directive (WFD). In the current study a thorough analysis of the efficiency of 22 ecological indices was performed and a small number was selected for the development of five-level water quality scales (High, Good, Moderate, Poor, and Bad). The analysis was performed on simulated communities free of the noise of field communities due to uncontrolled factors or stochastic processes. Two criteria were set for the sensitivity of indices, namely their monotonicity and linearity across the studied eutrophication spectrum. The whole procedure was based on the development of a five-level quality assessment scheme based on phytoplankton abundance. Among the indices tested, the Menhinick diversity index and three indices of evenness were the most efficient, showing consistency (monotonic behavior) and linearity and were therefore used for the development of quality scales for the WFD. An Integrated Phytoplankton Index (IPI) based on three phytoplankton metrics, chlorophyll a, abundance, and diversity is also proposed. The efficiency of these indices was evaluated for a number of sites in the Aegean, already classified in the past by various methods based on nutrient concentrations or phytoplankton data. The results indicate that the various phytoplankton metrics (chlorophyll a, abundance, and diversity) assessed or proposed in the current study, carry their own information showing differences in the final classification of areas. Therefore the establishment of synthetic indices as the IPI seems to be advantageous for the integrated assessment of coastal water quality in the framework of European policies as the WFD.     

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.     

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