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.     

Use of macroinvertebrate-based multimetric indices for water quality evaluation in Spanish Mediterranean rivers: an intercalibration approach with the IBMWP index

For the European Parliament and Commission to implement the Water Framework Directive (WFD), the water-quality indices that are currently used in Europe need to be compared and calibrated. This will facilitate the comparative assessment of ecological status throughout the European Union. According to the WFD, biologic indices should respond consistently to human impacts, using multimetric approaches and water-quality classification boundaries adjusted to a common set of normative definitions. The European Commission has started an intercalibration exercise to review biologic indices and harmonize class boundaries. We used data from rivers in Spain to compare the IBMWP (Iberian Biological Monitoring Working Party) index, which is commonly used by water authorities in Spain and by several research centers, with the Intercalibration Common Multimetric Index (ICM-Star), which was used as a standard in the intercalibration exercise. We also used data from Spanish rivers to compare the multimetric indices ICM-7 (based on quantitative data) and ICM-9 (based on qualitative data) with the IBMWP. ICM-7 and ICM-9 were proposed by the Mediterranean Geographical Intercalibration Group (Med-GIG). Additionally, we evaluated two new multimetric indices, developed specifically for macroinvertebrate communities inhabiting Mediterranean river systems. One of these is based on quantitative data (ICM-10), while the other is based on qualitative data (ICM-11a). The results show that the IBMWP index responds well to the stressor gradient present in our data, and correlates well with ICM-Star. Moreover, the IBMWP quality class boundaries were consistent with the intercalibration requirements of the WFD. However, multimetric indices showed a more linear relation with the stressor gradient in our data, and less variation in reference values. In addition, they may provide more statistical power for detecting potential environmental impacts. Multimetric indices produced similar results for quantitative and qualitative data. Thus, ICM-10 (also named IMMi-T) and ICM-11a (also named IMMi-L) indices could be used to meet European Commission requirements for assessing the water quality in Spanish Mediterranean rivers. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: Joel Trexler     

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.     

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.     

A new method for assessing the impact of hydromorphological degradation on the macroinvertebrate fauna of five German stream types

We developed a new Multimetric Index for stream assessment, which is mainly focussed on the impact of hydromorphological degradation on the macroinvertebrate fauna. The index was developed for five German stream types, three of which are located in the lowlands of Northern Germany and two in the lower mountainous areas. For each stream type sites representing different stages of hydromorphological degradation were investigated; the macroinvertebrate fauna of each site was sampled two or three times in 2000 (83 sites and 174 samples altogether). In addition, more than 200 parameters describing the hydromorphology of the sites have been recorded. The assessment system was developed separately for each of the stream types. The development process included (1) the generation of a new index (`German Fauna Index'), (2) the selection of faunal metrics, which correlate to hydromorphological degradation and (3) the combination of the selected metrics into a Multimetric Index. To correlate faunal metrics and hydromorphological degradation, a `Structure Index' describing the alteration of stream morphology was generated. A correlation matrix of the selected metrics and the structure index is presented. The `German Fauna Index' is based on taxa, which predominantly occur at sites of a certain morphological degradation class. The selection process of taxa included in the new index was in a first step based on data sampled in this study and supplemented by literature data. For one stream type (mid-sized mountain streams) the process of metric selection and validation is described in detail, including a correlation matrix of the metrics and a validation of the metrics with data on additional sampling sites.     

Evaluating the relative contributions of hydroperiod and soil fertility on growth of south Florida mangroves

The requirements of the European Water Framework Directive (WFD), aimed at an integrative assessment methodology for evaluating the ecological status of water bodies are frequently being achieved through multimetric techniques, i.e. by combining several indices, which address different stressors or different components of the biocoenosis. This document suggests a normative methodology for the development and application of Multimetric Indices as a tool with which to evaluate the ecological status of running waters. The methodology has been derived from and tested on a European scale within the framework of the AQEM and STAR research projects, and projects on the implementation of the WFD in Austria and Germany. We suggest a procedure for the development of Multimetric Indices, which is composed of the following steps: (1) selection of the most suitable form of a Multimetric Index; (2) metric selection, broken down into metric calculation, exclusion of numerically unsuitable metrics, definition of a stressor gradient, correlation of stressor gradients and metrics, selection of candidate metrics, selection of core metrics, distribution of metrics within the metric types, definition of upper and lower anchors and scaling; (3) generation of a Multimetric Index (general or stressor-specific approach); (4) setting class boundaries; (5) interpretation of results. Each step is described by examples.     

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.     

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)     

A multi-assemblage,multi-metric biological condition index for eastern Amazonia streams

Multimetric indices (MMIs) are widely used for assessing ecosystem condition and they have been developed for a variety of biological assemblages. However, when multiple assemblages are assessed at sites, the assessment results may differ because of differing physiological sensitivities to particular stressor gradients, different organism size and guilds, and the effects of different scales of disturbances on the assemblages. Those differences create problems for managers seeking to avoid type-1 and type-2 statistical errors. To alleviate those problems, we used an anthropogenic disturbance index for selecting and weighting metrics, modeled metrics against natural variability to reduce the natural variability in metrics, and developed an MMI based on both fish and aquatic insect metrics. We evaluated eight different ways of calibrating and combining candidate metrics and found that MMIs with unweighted and modeled aquatic insect and fish metrics were the preferred MMI options.     

Assessment of organic pollution effect considering differences between lotic and lentic stream habitats

Based on the requirements of the Water Framework Directive, a macroinvertebrate-based assessment system to evaluate the ecological quality of streams has been developed by AQEM project consortium. In the Czech Republic the impact of organic pollution was principal pressure studied, but some morphological degradation of some sampling sites could not be avoided. A multimetric assessment system for three stream types was developed. Detrended Correspondence Analysis was used for the detection of the response of macroinvertebrate communities to the gradient of organic degradation. Significant relationships between abiotic (BOD, TOC, nutrients) and biotic (saprobic index, ASPT) indicators of organic enrichment/eutrophication were identified. Separate storage of the riffle and pool components of each multi-habitat sample allowed differences between these habitats to be compared in context of the metrics applied in the assessment system. Lotic and lentic habitats differed in taxonomic composition, ecological traits and biotic indices. The separate assessment of the riffle and pool parts of samples provides additional useful information when combined effects of organic pollution and morphological degradation are to be considered.     

How much is enough? Adequate sample size for littoral macroinvertebrates in lowland lakes

Littoral macroinvertebrates are increasingly used for assessing the ecological status of lakes according to the EU Water Framework Directive. This requires harmonised sampling methods, but information on the appropriate spatial scale of the sampling as well as on the adequate sample sizes are mostly lacking. In this study, we compared the spatial variability of littoral (<1.2 m water depth) macroinvertebrate community composition within habitats and within sites to test whether habitat-specific sampling can reduce their spatial variability. Furthermore, we determined the sample size necessary to obtain maximum species richness for a given habitat type. Spatial variability of macroinvertebrate community composition was significantly lower within habitats than within sampling sites, except for communities of coarse woody debris. Species–area curves revealed that a sample size of 1 m² per habitat was not sufficient to obtain the maximum species richness due to the dominance of rare species, which suggests that compilation of taxon inventories may require more exhaustive sampling with sampling sizes substantially larger than 1 m². Separate analysis for species assigned to incidence classes showed that a mean area of 0.63 m² per habitat is sufficient to record all species with frequent and medium incidences, and 76% of the rare species. We conclude that habitat-specific sampling is an effective way to reduce the inherent spatial variability of littoral macroinvertebrate communities and that a sample size of 0.63 m² per habitat is sufficient to represent their dominant and subdominant elements. The application of this adequate sample size to other lake types than large oligotrophic lakes has to be exercised with caution, in particular if community composition and richness patterns differ. However, our results are based on data from lakes that represent the typical lake type found throughout the Central Baltic ecoregion ensuring its wider applicability in this ecoregion.     

Lake depth and geographical position modify lake fish assemblages of the European 'Central Plains' ecoregion

1. Classification of European lake fish assemblages can be based on fish‐assemblage structure or morphological, geographical, physical and chemical lake attributes. However, substantial gaps in knowledge exist with respect to the correspondence between both classification approaches. 2. Here, we compiled fish assemblage data from 165 lakes situated in the European ‘Central Plains’ ecoregion. Cluster analysis of fish abundances was performed to compare fish assemblage types of the entire ecoregion with those from previous country‐specific studies. Nonparametric group comparisons, classification trees and partial canonical ordinations were used to infer the correspondence between fish assemblage types and morphology, geographical position and nutrient concentration of the lakes. 3. Three distinct fish assemblages were revealed: vendace (Coregonus albula), ruffe (Gymnocephalus cernuus) and roach (Rutilus rutilus) lake types. Both latitude and lake depth were the best determinants of lake type, but total phosphorus (TP) concentrations were also important. Vendace lakes were deep and had low TP concentrations, whereas the shallower ruffe and roach lakes had higher TP values. Roach lakes were more frequent in the north‐west area of the ecoregion, whereas ruffe lakes were more often found south of the Baltic Sea. 4. Controlling for the influence of nutrient concentration showed that lake morphology and geographical position were important determinants of fish assemblages. However, the variance explained was low (<20%), implying that biological interactions may also be important in forming the lake‐specific fish assemblages. 5. The results suggest that fish assemblages differ between deep and shallow lakes, and between the north‐west and south‐east locations within the Central Plains ecoregion. Accordingly, establishment of depth‐related lake morphotypes is needed, and the European ecoregions recommended to be used in evaluation systems according to the Water Framework Directive seem to be too coarse to reflect the subtle differences of fish species richness along geographical gradients.     

The impact of water-level regulation on littoral macroinvertebrate assemblages in boreal lakes

Regulation of lake water level for power production and flood control is among the major anthropogenic disturbances in boreal aquatic ecosystems. In Finland, over 300 lakes, representing one third of the total inland water area of the country, are artificially regulated. To study the effects of regulation on lake littoral macroinvertebrate communities, samples were taken from upper stony littoral and from lower soft bottom littoral habitats of 11 lakes with different regulation amplitudes (wintertime fall in water level 1.19–6.75 m). Twelve unregulated (wintertime fall in water level 0.11–0.55 m) lakes with otherwise similar characteristics were used as a reference. Non-metric Multidimensional Scaling ordinations showed that the composition of macroinvertebrate assemblages was strongly associated with the amplitude of water level regulation. Taxon richness also decreased with increasing intensity of regulation. Freezing and flushing of sediments in late winter are probably the most important factors leading to the impoverished littoral macroinvertebrate fauna. Invertebrates with long life cycle seem to be particularly vulnerable to unnatural water level fluctuation. Our results show that regulation of water level has a major impact on functionally significant lake littoral macroinvertebrates.     

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.     

Response of benthic macroinvertebrates to whole-lake, non-native fish treatments in mid-elevation lakes of the Trinity Alps, California

Introduced fish reduce the abundance and diversity of native aquatic fauna, but the effect can be reduced in complex habitats. We manipulated fish populations in forested mountain lakes to determine whether or not fish affected benthic macroinvertebrate composition across lakes with differing habitat complexity. We compared abundance, biomass, body-length, and community structure of benthic macroinvertebrates from 16 lakes with three treatments (fish stocked, suspended stocking, fish removed) and unstocked fishless “controls”. Over 4 years, we assessed the relative importance of fish and environmental variables influencing the composition of benthic macroinvertebrates. Control lakes had the greatest overall abundance of macroinvertebrates when chironomid midges were excluded. Abundances of insects in the clinger/swimmer functional group and caddisflies were greatest in the control lakes but were primarily influenced by habitat variables including the availability of aquatic vegetation and wood. Total biomass and mean body length of macroinvertebrates were not affected by treatment. Taxon richness of macroinvertebrates was about 40% greater in the control lakes compared to the treatment lakes but did not differ among treatments. Our results suggest that fish reduce susceptible macroinvertebrate richness and abundances, but that changes associated with alterations of fish composition are confounded by other factors in complex lake habitats.     

Among-habitat and Temporal Variability of Selected Macroinvertebrate Based Metrics in a Mediterranean Shallow Lake (NW Spain)

According to the European Water Framework Directive, waterbodies have to be classified on the basis of their ecological status using biological quality elements, such as macroinvertebrates. This needs to take into consideration the influence of natural variation (both spatial and temporal) of reference biological communities as this may obscure the effects caused by anthropogenic disturbance. We studied the influence of among-habitat and temporal (seasonal and interannual) changes on the macroinvertebrate communities of an Iberian shallow lake and the variability of 21 measures potentially useful for bioindication purposes. Two series of data were examined: (a) macroinvertebrate samples taken on four occasions over an annual cycle were used to assess the effects of seasonality and among-habitat variability; (b) macroinvertebrate samples collected in three consecutive summers were used to assess interannual variability. Coefficients of variation, expressed as percentage, were used to quantify the effect of among-habitat and temporal variability on the selected metrics. According to our results, % Insecta, Shannon–Wiener diversity index and the qualitative taxonomic metrics (measures based on number of taxa) were robust in terms of temporal (seasonal and interannual) and among-habitat variability. Abundance ratio and some metrics based on functional feeding groups were highly variable. Therefore, qualitative taxonomic metrics may be promising tools in biomonitoring programs of Mediterranean shallow lakes due to their comparatively low variability.     

Relevance of abiotic criteria used in German lake typology for macroinvertebrate fauna

For lake characterisation, top-down typologies are mostly used throughout Europe, including type criteria such as climate, lake area, catchment geology and conductivity. In Germany, a lake typology was applied comprising ecoregion, calcium concentration, Schindler’s ratio, stratification type and residence time. However, the relevance of these criteria for the macroinvertebrate fauna has not been conclusively demonstrated till now. Benthic invertebrate community data and related environmental parameters of pristine or near-pristine lakes in Germany were analysed by multivariate analysis techniques to elucidate which environmental parameters are reflected by invertebrate composition. Moreover, benthic invertebrate data were transformed to metrics expressing ecological attributes and species richness (summarising functional composition, diversity and sensitivity measures). Multivariate statistics were used to test whether information relevant to ordination was lost and whether variation decreases using metrics which combine data with ecological attributes. Analysis of lake-type criteria revealed that ecoregions and prevailing substrates were characterized by different taxonomic compositions of macroinvertebrates. In addition, a relationship was found between community composition and lake size. Creating a novel bottom-up lake typology based on ecoregions, lake size and prevailing substrate gives better separation of distinct macroinvertebrate communities and a higher level of homogeneity within groups compared to top-down typology or single environmental parameters alone, both on species and metrics data. Despite some data variation due to methodological differences (e.g. different sampling and sorting techniques) and interannual and seasonal variation in the data set, NMDS ordination presented well-separated groups of bottom-up lake types. Lake types were more precisely separated by species data than by metric data in both top-down and bottom-up typology. However, as information loss from species lists to calculated metrics is marginal, type-specific benthic invertebrate assemblages are reflected both on the species level and on the metric level. Species and metric data are both suitable for data ordination, while single environmental parameters affecting macroinvertebrate composition can best be obtained using metrics.     

Lentic macroinvertebrate assemblage structure along gradients in spatial heterogeneity, habitat size and water chemistry

Littoral zones of small water bodies are spatially heterogeneous habitats, harbouring diverse biotic communities. Despite this apparent heterogeneity, many studies have stressed the importance of water chemistry in determining the structure of littoral macroinvertebrate assemblages. The purpose of this study was to consider the relative importance of several spatial and water chemistry variables in explaining the patterns in the structure of macroinvertebrate assemblages in 21 lentic water bodies in northeastern Finland. Water bodies were selected to represent various habitat conditions ranging from small permanent bog ponds to small forest lakes. According to canonical correspondence analysis (CCA), the most important environmental factors related to assemblage composition were water body area, moss cover, total nitrogen and water hardness. In general, species composition in small bog ponds tended to differ from that in larger lakes with forested shoreline. Total species richness was best explained by a composite variable (PCA) describing physical habitat heterogeneity, species richness being lowest in small bog lakes with simple bottom structure and low amount of aquatic plants. Species numbers in dominant functional feeding groups were related to different environmental factors. Shredder species richness was best explained by a regression model incorporating total nitrogen and the amount of organic matter, both of which were negatively related to the number of shredder species. The number of gatherer species increased with mean substratum particle size. Scraper species richness was negatively affected by the abundance of detritus and positively affected by depth, and a model including both variables explained most of the variation. Variation in the number of predatory species was best explained by a regression model including moss cover and lake area.