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 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 assessment of European lakes: ecological rationale and human impacts

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Development and evaluation of the Finnish fish-based lake classification method

The Finnish fish-based lake assessment system EQR4 was updated using more extensive lake data with tighter reference criteria. The updated EQR4 (EQR4_new) had significant and tighter pressure (eutrophication) relationship compared to the previous version (EQR4_old). The EQR4_new separated impacted and reference lakes with lower misclassification risk compared to the EQR4_old. All the variables within the multi-metric index EQR4_new (total biomass, total number of individuals, cyprinid biomass %, and indicator species) were found to be relevant. The classification output in relation to eutrophication was higher in the northern part of the country compared to the southern lakes which was probably due to the climate-dependent reduction in productivity. Despite the clear pressure response and the ability to separate reference and impacted lakes, the accuracy of the EQR4_new values is relatively modest. Including regional patterns in the composition and variability of lake fish communities in Finland would increase the accuracy of the assessment method and, moreover, contribute to the excellence of fish community ecology of boreal lakes.     

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

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

Major changes in trophic dynamics in large, deep sub-alpine Lake Maggiore from 1940s to 2002: a high resolution comparative palaeo-neolimnological study

1. We describe the changes in trophic dynamics in Lake Maggiore from c. 1943 to 2002 using subfossil cladoceran data from a high resolution sediment record, long‐term contemporary data series and historical information. During this period the lake went through a eutrophication phase until 1980 followed by oligotrophication. 2. During the eutrophication period a major increase occurred in the abundance of Chydorus sphaericus, the proportion of planktonic cladocerans and total abundance of cladocerans in the sediment. Since 1980 the abundance declined again and subfossil Eubosmina mucro length and contemporary Daphnia body length increased, most probably as a result of higher abundance of invertebrate predators. 3. Changes in the fish stock composition caused by the introduction of exotic fish during the pre‐eutrophication period and a complete ban on fishing because of Dichloro‐diphenil‐ethanes (DDTs) pollution of the lake (during oligotrophication) could also be detected in the community assemblage and size structure of the sediment zooplankton. 4. We found good correspondence between trophic changes inferred from cladoceran subfossils (community composition, size and predation pressure) and contemporary data, suggesting that sediment samples can be used to infer past development in trophic dynamics, including predation by fish and pelagic invertebrates in lakes with scarce neolimnological data. 5. Furthermore, by combining palaeolimnological cladoceran data rarely obtained from contemporary samples (e.g. benthic and plant‐associated cladocerans, mucro length of bosminids) with contemporary data of organisms poorly represented in the sediment record (e.g. remains of Bythotrephes and fishes) a more complete understanding of changes in trophic dynamics was obtained. 6. The detection in the sediments of meteorological events whose effects on zooplankton had been recorded in the long‐term studies also provided evidence that eutrophication tends to override climate signals. 7. We conclude that a combined palaeo‐neolimnological approach can be a powerful tool for elucidating past changes in the trophic dynamics of lakes and the interaction with climate induced changes, not least when high resolution sediment records are available.     

Applying macrophyte community indicators to assess anthropogenic pressures on shallow soft bottoms

Vegetated soft bottoms are under pressure due to a number of anthropogenic stressors, such as coastal exploitation and eutrophication. The ecological value of these biotopes has gained recognition through international conventions and the EU directives, which request methods for assessment of the environmental status of coastal areas. However, currently there is no appropriate method for assessing the status of shallow vegetated soft bottoms in the northern Baltic Sea. Therefore, we developed a macrophyte community index and tested its response in relation to important pressures (eutrophication and boating activity) and natural gradients (topographic openness, depth and salinity) on shallow bays in the northern Baltic Sea. The macrophyte index, and hence the proportion of sensitive to tolerant species, decreased with increasing phosphorus concentration, turbidity and level of boating activity, while the cumulative cover of macrophytes only showed a negative trend in response to increasing turbidity. Juvenile fish abundance was positively related to the index, indicating importance of sensitive macrophyte species for ecosystem functioning. As the index was tested in a wide geographic area, and showed a uniform response across natural gradients, it is a promising tool for assessment of environmental status that may be applied also in other vegetated soft-bottom areas.     

Effects of water quality and trophic status on helminth infections in the cyprinid fish, Schizothorax niger Heckel, 1838 from three lakes in the Kashmir Himalayas

Water quality greatly influences the population density of aquatic biota, including parasites. In order to evaluate the relationship between fish parasites and water quality in Kashmir Himalayas, we assessed helminth parasite densities in Schizothorax niger Heckel, 1838 (an endemic cyprinid fish of Kashmir) from three lakes, namely Anchar, Manasbal and Dal, which reflected the varied stages of eutrophication. The overall prevalence of helminth infections was higher in the hypertrophic Anchar Lake (prevalence = 18.6%) compared to Manasbal Lake, which was the least eutrophied (prevalence = 6.4%). Furthermore, mean prevalence of monoxenous and heteroxenous parasites was higher in lakes containing higher levels of water degradation (Anchar and Dal). The mean number of helminth species per fish host was the highest in the hypertrophic lake (1.3 ± 0.3) in comparison to the least eutrophic lake (0.2 ± 1.5). Variability of calculated infection indices (prevalence, mean intensity and mean abundance) revealed that helminth parasite composition in the fish was affected by the lakes' environmental stress (degraded water quality). Therefore, data on the density of helminth parasites in fish can provide supplementary information on the pollution status of a water body.     

Subfossil Cladocera in relation to contemporary environmental variables in 54 Pan-European lakes

1. Changes in cladoceran subfossils in the surface sediments of 54 shallow lakes were studied along a European latitude gradient (36–68°N). Multivariate methods, such as regression trees and ordination, were applied to explore the relationships between cladoceran taxa distribution and contemporary environmental variables, with special focus on the impact of climate. 2. Multivariate regression tree analysis showed distinct differences in cladoceran community structure and lake characteristics along the latitude gradient, identifying three groups: (i) northern lakes characterised by low annual mean temperature, conductivity, nutrient concentrations and fish abundance, (ii) southern, macrophyte rich, warm water lakes with high conductivity and high fish abundance and (iii) Mid‐European lakes at intermediate latitudes with intermediate conductivities, trophic state and temperatures. 3. Large‐sized, pelagic species dominated a group of seven northern lakes with low conductivity, where acid‐tolerant species were also occasionally abundant. Small‐sized, benthic‐associated species dominated a group of five warm water lakes with high conductivity. Cladoceran communities generally showed low species‐specific preferences for habitat and environmental conditions in the Mid‐European group of lakes. Taxon richness was low in the southern‐most, high‐conductivity lakes as well as in the two northern‐most sub‐arctic lakes. 4. The proportion of cladoceran resting eggs relative to body shields was high in the northern lakes, and linearly (negatively) related to both temperature and Chl a, indicating that both cold climate (short growing season) and low food availability induce high ephippia production. 5. Latitude and, implicitly, temperature were strongly correlated with conductivity and nutrient concentrations, highlighting the difficulties of disentangling a direct climate signal from indirect effects of climate, such as changes in fish community structure and human‐related impacts, when a latitude gradient is used as a climate proxy. Future studies should focus on the interrelationships between latitude and gradients in nutrient concentration and conductivity.     

Fish diversity in European lakes: geographical factors dominate over anthropogenic pressures

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

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

Impacts of climate warming on the long-term dynamics of key fish species in 24 European lakes

Fish play a key role in the trophic dynamics of lakes. With climate warming, complex changes in fish assemblage structure may be expected owing to direct effects of temperature and indirect effects operating through eutrophication, water level changes, stratification and salinisation. We reviewed published and new long-term (10–100 years) fish data series from 24 European lakes (area: 0.04–5,648 km²; mean depth: 1–177 m; a north–south gradient from Sweden to Spain). Along with an annual temperature increase of about 0.15–0.3°C per decade profound changes have occurred in either fish assemblage composition, body size and/or age structure during recent decades and a shift towards higher dominance of eurythermal species. These shifts have occurred despite a reduction in nutrient loading in many of the lakes that should have benefited the larger-sized individuals and the fish species typically inhabiting cold-water, low-nutrient lakes. The cold-stenothermic Arctic charr has been particularly affected and its abundance has decreased in the majority of the lakes where its presence was recorded. The harvest of cool-stenothermal brown trout has decreased substantially in two southern lakes. Vendace, whitefish and smelt show a different response depending on lake depth and latitude. Perch has apparently been stimulated in the north, with stronger year classes in warm years, but its abundance has declined in the southern Lake Maggiore, Italy. Where introduced, roach seems to take advantage of the higher temperature after years of low population densities. Eurythermal species such as common bream, pike–perch and/or shad are apparently on the increase in several of the lakes. The response of fish to the warming has been surprisingly strong and fast in recent decades, making them ideal sentinels for detecting and documenting climate-induced modifications of freshwater ecosystems.     

Correlations between type‐indicator fish species and lake productivity in German lowland lakes

Morphotypes for 67 lakes in the German lowlands were derived, based on maximum depth and mixis type. A threshold of 11 m maximum depth was identified to be the best level to discriminate shallow from deep lake morphotypes. The fish communities in these two morphotypes were significantly different. Indicator species analyses based on fish biomasses found vendace Coregonus albula in deep lakes and ruffe Gymnocephalus cernuus , bream Abramis brama , white bream Abramis bjoerkna , roach Rutilus rutilus , pikeperch Sander lucioperca and small perch Perca fluviatilis in shallow lakes to be the most representative species of their communities. Lake productivity was closely related to biomass and in part abundance of the type‐indicator species, with vendace declining with increasing chlorophyll a concentration in the deep lakes, whereas biomass of pikeperch, bream, white bream and ruffe increased and biomass of small perch decreased with increasing chlorophyll a . These results indicate that assessment of ecological integrity of lakes by their fish fauna is generally possible, if lakes are initially separated according to a depth‐related morphotype before the assessment, and if eutrophication is considered to be the main anthropogenic degradation.     

Can size distributions of European lake fish communities be predicted by trophic positions of their fish species?

An organism''s body size plays an important role in ecological interactions such as predator–prey relationships. As predators are typically larger than their prey, this often leads to a strong positive relationship between body size and trophic position in aquatic ecosystems. The distribution of body sizes in a community can thus be an indicator of the strengths of predator–prey interactions. The aim of this study was to gain more insight into the relationship between fish body size distribution and trophic position in a wide range of European lakes. We used quantile regression to examine the relationship between fish species'' trophic position and their log‐transformed maximum body mass for 48 fish species found in 235 European lakes. Subsequently, we examined whether the slopes of the continuous community size distributions, estimated by maximum likelihood, were predicted by trophic position, predator–prey mass ratio (PPMR), or abundance (number per unit effort) of fish communities in these lakes. We found a positive linear relationship between species'' maximum body mass and average trophic position in fishes only for the 75% quantile, contrasting our expectation that species'' trophic position systematically increases with maximum body mass for fish species in European lakes. Consequently, the size spectrum slope was not related to the average community trophic position, but there were negative effects of community PPMR and total fish abundance on the size spectrum slope. We conclude that predator–prey interactions likely do not contribute strongly to shaping community size distributions in these lakes.     

Can warm climate‐related structure of littoral predator assemblies weaken the clear water state in shallow lakes?

Shallow lakes, the most abundant lake type in the world, are very sensitive to climatic changes. The structure and functioning of shallow lakes are greatly impacted by submerged plants, and these may be affected by climate warming in various, contrasting, ways. Following a space‐for‐time substitution approach, we aimed to analyse the role of aquatic (submerged and free‐floating) plants in shallow lakes under warm climates. We introduced artificial submerged and free‐floating plant beds in five comparable lakes located in the temperate zone (Denmark, 55–57 °N) and in the subtropical zone (Uruguay, 30–35 °S), with the aim to study the structure and dynamics of the main associated communities. Regardless of differences in environmental variables, such as area, water transparency and nutrient status, we found consistent patterns in littoral community dynamics and structure (i.e. densities and composition of fish, zooplankton, macroinvertebrates, and periphyton) within, but substantial differences between, the two regions. Subtropical fish communities within the macrophyte beds exhibited higher diversity, higher density, smaller size, lower relative abundance of potentially piscivores, and a preference for submerged plants, compared with otherwise similar temperate lakes. By contrast, macroinvertebrates and cladocerans had higher taxon richness and densities, and periphyton higher biomass, in the temperate lakes. Several indicators suggest that the fish predation pressure was much stronger among the plants in the subtropical lakes. The antipredator behaviour of cladocerans also differed significantly between climate zones. Submerged and free‐floating plants exerted different effects on the spatial distribution of the main communities, the effects differing between the climate zones. In the temperate lakes, submerged plants promoted trophic interactions with potentially positive cascading effects on water transparency, in contrast to the free‐floating plants, and in strong contrast to the findings in the subtropical lakes. The higher impact of fish may result in higher sensitivity of warm lakes to external changes (e.g. increase in nutrient loading or water level changes). The current process of warming, particularly in temperate lakes, may entail an increased sensitivity to eutrophication, and a threat to the high diversity, clear water state.     

Long-Term Changes in the Diet of Gymnogobius isaza from Lake Biwa,Japan: Effects of Body Size and Environmental Prey Availability

Body size and environmental prey availability are both key factors determining feeding habits of gape-limited fish predators. However, our understanding of their interactive or relative effects is still limited. In this study, we performed quantitative dietary analysis of different body sizes of goby (Gymnogobius isaza) specimens collected from Lake Biwa between 1962 and 2004. First, we report that the diet was composed mainly of zooplankton (cladocerans and copepods) before the 1980s, and thereafter, shifted to zoobenthos (gammarids). This foraging shift coincided with, and thus can be linked to, known historical events in the lake at that time: decrease in zooplankton abundance with the alleviation of eutrophication, increase in fish body size resulting from fish population collapse, and increase in gammarid abundance due to reduced fish predation pressure. Supporting this view, our data analyses revealed how the long-term changes in the diet composition would be co-mediated by changes in fish body size and environmental prey availability. Specifically, while zoobenthos abundance strongly affected the fish diet composition, larger (smaller) fish preferred zoobenthos (zooplankton). Furthermore, the body size effects were stronger than those of prey availability. These results provide the best long-term evidence that fish feeding habits vary over decades with its body size and prey community due to anthropogenic disturbances.     

Habitats and Littoral Zone Fish Community Structure of Two Natural Lakes in Southeast Brazil

The fish community and habitat structure in the littoral zone of lakes Pedra and Hortência, middle Rio Doce Valley, Brazil, were investigated in three sampling periods from August 1992 to May 1993. A total of 9106 fishes were collected, including 11 species in Lake Hortência and 12 species in Lake Pedra. Diversity was higher in Lake Hortência, although total fish abundance was the same for both lakes, with no significant temporal differences. The length distribution of the majority of fish species was similar between lakes. Geophagus brasiliensis was the dominant species (number/biomass) in all habitats of the two lakes in all three sampling periods. A striking difference in total fish abundance in relation to habitat types, which we attribute to physical variables, especially the abundance of macrophytes was observed. Negative impacts attributable to the local Eucalyptus sp. plantations were not detected in the fish community structure of Lake Hortência, which is probably due to the maintenance of the riparian vegetation contributing to similar physical environmental conditions in the littoral zone and high similarity in fish community structure between the two lakes. However, further studies on fish community structure and potential Eucalyptus impacts are suggested as necessary to improve conservation measures of the lakes and their fish faunas.     

Characteristics and classification of the lakes of Signy Island, South Orkney Islands, Antarctica

SUMMARY. The lakes of Signy Island (60° 43'S, 45° 38'W), South Orkney Islands, Antarctica, provide a unique laboratory for the study of many processes including natural eutrophication. Current relationships between the lakes have been examined by principal components analysis of environmental data from a long-term monitoring programme. The results from the analysis have been combined with some biological data to provide a classification scheme for the lakes. The study has produced a valuable baseline for use in future research.     

Palaeoenvironmental Changes Inferred from Biological Remains in Short Lake Sediment Cores from the Central Alps and Dolomites

In this paper we review research on eutrophication, acidification and climate change based on studies of lake sediments in the Alps. Studies on fossil diatoms, chrysophytes, plant pigments, Cladocera and carbonaceous particles in a number of high altitude lakes in Italy and Switzerland have been used to track environmental changes. We present an original study on fossil Cladocera in sediment cores from 29 lakes that have shown changes in biodiversity from the pre-industrial period (ca. pre AD 1850) to the present. These data show that altitude, ca. 60 years of acidification impacts and fish stocking are the most important factors that affect their distribution and abundance. We review further case studies from two morphometrically and chemically different lakes (Tovel and Paione Superiore). Their lake sediment records span 400 and 150 years, respectively; multi-core, multi-proxy analyses show their pH, trophic and climatic evolution over time.