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

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

A tool for protected area management: multivariate control charts ‘cope’ with rare variable communities

Performance assessment, impact detection, and the assessment of regulatory compliance are common scientific problems for the management of protected areas. Some habitats in protected areas, however, are rare and/or variable and are not often selected for study by ecologists because they preclude comparison with controls and high community variability makes meaningful change detection difficult. Shallow coastal saline lagoons are habitats that experience comparatively high levels of stress due to high physical variability. Lagoons are rare, declining habitats found in coastal regions throughout Europe (and elsewhere) where they are identified as one of the habitats most in need of protected area management. The infauna in the sediments of 25 lagoons were sampled. Temporal and spatial variation in three of these [protected] lagoons was investigated further over 5 years. In a multivariate analysis of community structure similarities were found between some lagoons, but in other cases communities were unique or specific to only two sites. The protected lagoons with these unique/specific communities showed significant temporal and spatial variation, yet none of the changes observed were attributed to human impacts and were interpreted as inherent variability. Multivariate control charts can operate without experimental controls and were used to assess community changes within the context of ‘normal’ lagoon variability. The aim of control chart analysis is to characterize background variability in a parameter and identify when a new observation deviates more than expected. In only 1 year was variability more than expected and corresponded with the coldest December in over 100 years. Multivariate control charts are likely to have wide application in the management of protected areas and other natural systems where variability and/or rarity preclude conventional analytical and experimental approaches but where assessments of condition, impact or regulatory compliance are nonetheless required.     

M-AMBI derived from taxonomic levels higher than species allows Ecological Status assessments of benthic habitats in new geographical areas

Under the Water Framework Directive (WFD) benthic Ecological Quality Ratios (EQRs) are important tools for assessing Ecological Status (ES) of coastal and transitional waters. Calculation of the Multivariate-AZTI Marine Biotic Index (M-AMBI) EQR is based on the proportions of sensitive and stress tolerant benthic invertebrate species, number of species and Shannon–Wiener diversity. The sensitivity of many tropical/sub-tropical taxa has not yet been determined, presenting a barrier to the direct transfer of WFD EQRs, and the ideas underpinning them, to the management of coastal waters beyond Europe. To overcome this we examine using higher taxonomic level data with M-AMBI.Before applying such approaches to assessing ES in new geographical regions it is essential to determine the effects of using higher taxonomic level data on M-AMBI in areas where the tool was developed. To this end, we use macrofaunal data from three well studied sites in north-western Europe to examine the effects of using taxonomic level data higher than species on M-AMBI. Using the European datasets M-AMBI ES classification was shown to be robust to changes in taxonomic level data. We test the suitability of family-level M-AMBI for assessing ES in subtropical Hong Kong waters. Family level M-AMBI was useful in detecting stress in Hong Kong, where it successfully detected temporal and spatial shifts in ES in response to seasonal hypoxia and salinity variability, and anthropogenic organic enrichment.     

Tributyltin pollution biomonitoring under the Water Framework Directive: Proposal of a multi-species tool to assess the ecological quality status of EU water bodies

The Water Framework Directive (WFD) is a key legislative action developed by the European Union in order to protect aquatic ecosystems. One of the concerning pollutants, listed in this directive as a priority hazardous substance, is tributyltin (TBT), a biocide largely used in antifouling paints and identified as a causative agent of imposex/intersex in gastropods. In order to integrate TBT pollution monitoring within this legislative framework, a practical exercise is here proposed to assess the evolution of surface water ecological status in Ria de Aveiro (NW Portugal). Three bioindicators – the caenogastropods Nucella lapillus, Nassarius reticulatus and Littorina littorea – were used under the general WFD benthic invertebrate quality element, and the vas deferens sequence index (VDSI) and the intersex index (ISI) were selected as biomarkers for the purpose of assessing the condition of this quality element regarding the impact of TBT pollution. Levels of VDSI in N. lapillus and N. reticulatus, and ISI in L. littorea, were surveyed in 2013 and compared with previous data available for the same species and study area in 1998 and 2005, providing a time lapse for a period of 15 years. VDSI and ISI values were converted into Ecological Quality Ratios (EQR) and EQR boundaries were set for each species in order to define the five ecological status classes (High, Good, Moderate, Poor and Bad). We propose N. lapillus as key bioindicator, however the combined use of further species is very useful to cover a wider study area. Based on the proposed method, it is concluded that the ecological status of the surface waters surveyed in Ria de Aveiro, concerning the impact of TBT pollution on the above benthic invertebrate taxa, improved considerably since 1998 and achieved a Good Ecological Status in 2013, thus meeting the WFD environmental objectives for this priority hazardous substance even before 2015.     

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     

Site-specific chlorophyll reference conditions for lakes in Northern and Western Europe

The Water Framework Directive (WFD) requires EU Member States to assess the “ecological status” of surface waters. As a component of ecological status, many European countries are developing a classification scheme for chlorophyll concentrations as a measure of phytoplankton biomass. The chlorophyll classification must be based on the degree of divergence of a water body from an appropriate baseline or ‘reference condition’. This article describes the development of a series of regression models for predicting reference chlorophyll concentrations on a site-specific basis. For model development, a large dataset of European lakes considered to be in reference condition, 466 lakes in total, was assembled. Data were included from 12 European countries, but lakes from Northern and Western Europe dominated and made up 92% of all reference lakes. Data have been collated on chlorophyll concentration, altitude, mean depth, alkalinity, humic type, surface area and geographical region. Regression models were developed for estimating site-specific reference chlorophyll concentrations from significant predictor ‘typology’ variables. Reference chlorophyll concentrations were found to vary along a number of environmental gradients. Concentrations increased with colour and alkalinity and decreased with lake depth and altitude. Forward selection was used to identify independent explanatory variables in regression models for predicting site-specific reference chlorophyll concentrations. Depth was selected as an explanatory variable in all models. Alkalinity was included in models for low colour and humic lakes and altitude was included in models for low colour and very humic lakes. Uncertainty in the models was quite high and arises from errors in the data used to develop the models (including natural temporal and spatial variability in data) and also from additional explanatory variables not considered in the models, particularly nutrient concentrations, retention time and grazing. Despite these uncertainties, site-specific reference conditions are still recommended in preference to type-specific reference conditions, as they use the individual characteristics of a site known to influence phytoplankton biomass, rather than adopt standards set to generally represent a large population of lakes of a particular type. For this reason, site-specific reference conditions should result in reduced error in ecological status classifications, particularly for lakes close to typology boundaries.     

The M-NIP: a macrophyte-based Nutrient Index for Ponds

In Swiss ponds, eutrophication represents one of the major threats to biodiversity. A biological method to assess the trophic state would, therefore, be particularly useful for monitoring purposes. Macrophytes have already been successfully used to evaluate the trophic state of rivers and lakes. Considering their colonizing abilities and their roles in pond ecosystem structure and function, macrophytes should be included in any assessment methods as required by the European Water Framework Directive. Vegetation survey and water quality data for 114 permanent ponds throughout Switzerland were analysed to define indicator values for 113 species including 47 with well-defined ecological response to total water phosphorus (TP). Using indicator values and species cover, a Macrophyte Nutrient Index for Ponds (M-NIP) was calculated for each site and assessed with both the original pond data set and a limited validation data set. The resulting index performed better when considering only species with narrow responses to TP gradient and was more applicable, but less accurate when including all species. Despite these limitations, the M-NIP is a valuable and easy tool to assess and monitor the nutrient status of Swiss ponds and was shown to be robust and relatively sensitive to slight changes in phosphorus loading with a validation subset. Guest editors: B. Oertli, R. Cereghino, A. Hull & R. Miracle Pond Conservation: From Science to Practice. 3rd Conference of the European Pond Conservation Network, Valencia, Spain, 14–16 May 2008     

Validation of diatoms as proxies for phytobenthos when assessing ecological status in lakes

Research to develop tools to assess the ecological status of phytobenthos, as required in Annex V of the European Union Water Framework Directive, has focussed largely on diatoms. Diatoms are often the most abundant and diverse group of algae within the phytobenthos and have been used widely for other monitoring purposes. However, there is little empirical justification for the use of diatoms as proxies for the wider phytobenthos. In this paper, we re-examine an existing dataset compiled largely from littoral samples from standing waters in the English Lake District and compared transfer functions for total phosphorus, dissolved inorganic carbon, conductivity and calcium concentration generated from diatoms and non-diatoms separately and together. The results show that transfer functions generated from diatoms alone are as powerful as transfer functions generated from diatoms and non-diatoms combined, while transfer functions generated from non-diatoms alone are less effective. These results provide support for the use of diatoms as proxies for phytobenthos when ecological status is being assessed. Handling editor: J. Saros     

Odonata (Insecta) as a tool for the biomonitoring of environmental quality

Despite the fundamental dependence of human populations on water resources, a range of anthropogenic impacts, in particular the removal of riparian vegetation, threaten freshwater environments. One of the most effective means of evaluating the effects of anthropogenic disturbance in aquatic ecosystems is the use of bioindicators, and the insects of the order Odonata are among the most efficient indicators, due to their enormous sensitivity to environmental changes. In this context, the present study aimed to verify which parameters of the odonate community (species richness, abundance/biomass, composition, taxonomic diversity and taxonomic/phylogenetic distinctness) are most effective for the evaluation of the loss of environmental integrity. The study focused on 50 streams in the northeast of the Brazilian state of Pará. The streams were sampled during the dry season, between June and August 2011. The physical characteristics of each stream were evaluated using a Habitat Integrity Index (HII). The species composition provided the best parameter for the evaluation of ecological integrity, providing a relatively accurate assessment at a lower mean research cost than other parameters. Taxonomic diversity and distinctness also provided relatively reliable results, contributed additional information on the evolutionary relationships among the odonate taxa, and also provided a low-cost approach. Deconstructing communities is necessary to detect impacts, considering the considerable variation in the environmental requirements of the different species. Overall, the parameter that best responded to gradients of disturbance was species composition, followed by diversity and taxonomic distinctness. Given these findings, odonate-based biomonitoring should focus on these parameters to guarantee the optimal detection and evaluation of habitat alterations.     

Confidence in ecological indicators: A framework for quantifying uncertainty components from monitoring data

The value of an ecological indicator is no better than the uncertainty associated with its estimate. Nevertheless, indicator uncertainty is seldom estimated, even though legislative frameworks such as the European Water Framework Directive stress that the confidence of an assessment should be quantified. We introduce a general framework for quantifying uncertainties associated with indicators employed to assess ecological status in waterbodies. The framework is illustrated with two examples: eelgrass shoot density and chlorophyll a in coastal ecosystems. Aquatic monitoring data vary over time and space; variations that can only partially be described using fixed parameters, and remaining variations are deemed random. These spatial and temporal variations can be partitioned into uncertainty components operating at different scales. Furthermore, different methods of sampling and analysis as well as people involved in the monitoring introduce additional uncertainty. We have outlined 18 different sources of variation that affect monitoring data to a varying degree and are relevant to consider when quantifying the uncertainty of an indicator calculated from monitoring data. However, in most cases it is not possible to estimate all relevant sources of uncertainty from monitoring data from a single ecosystem, and those uncertainty components that can be quantified will not be well determined due to the lack of replication at different levels of the random variations (e.g. number of stations, number of years, and number of people). For example, spatial variations cannot be determined from datasets with just one station. Therefore, we recommend that random variations are estimated from a larger dataset, by pooling observations from multiple ecosystems with similar characteristics. We also recommend accounting for predictable patterns in time and space using parametric approaches in order to reduce the magnitude of the unpredictable random components and reduce potential bias introduced by heterogeneous monitoring across time. We propose to use robust parameter estimates for both fixed and random variations, determined from a large pooled dataset and assumed common across the range of ecosystems, and estimate a limited subset of parameters from ecosystem-specific data. Partitioning the random variation onto multiple uncertainty components is important to obtain correct estimates of the ecological indicator variance, and the magnitude of the different components provide useful information for improving methods applied and design of monitoring programs. The proposed framework allows comparing different indicators based on their precision relative to the cost of monitoring.     

Towards a multimetric index for ecological assessment of Mediterranean flatland ponds: the use of macroinvertebrates as bioindicators

Fifty-five macroinvertebrate metrics were tested for their response to pond condition in 41 ponds of northwest Spain to develop a preliminary multimetric index for ecological assessment of Mediterranean flatland ponds. Stressor specific response of individual attributes to eutrophication and habitat alteration was also investigated to identify differences in the responses of metrics to single stressors and elucidate how this might affect the performance of the final index. Several combinations were tested using discrimination efficiency (25th percentile of slightly impaired sites for metrics decreasing with perturbation and 75th percentile of slightly impaired sites for metrics increasing with perturbation) and Mann–Whitney U-test with Bonferroni adjustment (P < 0.001). The final index comprised five measures (generic richness of Chironominae, generic richness of Dytiscidae + Odonata + Tanypodinae, relative richness of Chironomidae, % Macropelopini and Shannon index) and discriminated between acceptable (good) and unacceptable (moderate) conditions with more than 86% efficiency. Moreover, all the five measures included in the final index showed unidirectional responses to eutrophication, decreasing as eutrophication increased. In contrast, the effect of habitat alteration was less clear, especially in ponds in best available conditions where a vegetation belt of shrubs and trees prevented growing of macrophitic vegetation on shores and consequently associated fauna. Interestingly, none of the functional groups (e.g. % predators and % collector–gatherers) were sensitive to degradation. Handling editor: K. Martens     

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.     

Biomanipulation as a useful water quality management tool in deep stratifying reservoirs

In six deep, soft-water reservoirs, ranging from oligotrophic to eutrophic, fishery management has been guided by the use of biomanipulation to improve water quality and opportunities for recreational fishing. As evidenced by the establishment of larger-bodied daphnids, a low level of zooplanktivory could be maintained in the newly filled Grosse Dhünn and refilled Brucher and Lingese Reservoirs only by regular stocking of piscivores (Sander lucioperca, Esox lucius, Salmo trutta lacustris, Onchorhynchus mykiss) in combination with size and bag limitations for the recreational fisheries. However, in the mesotrophic Pre-Reservoir Grosse Dhünn, Bever Reservoir and the newly filled slightly eutrophic Wupper Reservoir it took between 8 and 10 years before the predator-resistant zooplankton community responded to management with a switch to larger daphnids. Except for oligotrophic Grosse Dhünn Reservoir where angling is prohibited, the expected enhancement of piscivore biomass through stocking not least was prevented by anglers. However, growth of perch (Perca fluviatilis) benefited from the changed fishery management relying upon stocking piscivores only allowing them to reach the size of piscivory. The appearance of larger daphnids in Pre-Reservoir Grosse Dhünn and Wupper Reservoir resulted in the biomass of the Daphnia spring peak to increase and occur earlier causing prolonged clear water conditions. Although the larger daphnids increased transparency, total summer mean chlorophyll concentrations in the euphotic zone only decreased in the slightly eutrophic reservoirs due to reduced phosphorus availability following unchanged external phosphorus loadings. Reduced phosphorus availability in these reservoirs caused a real oligotrophication. Although the edible seston fraction was controlled “top down” the results did not support the trophic cascade hypotheses because total phytoplankton remained controlled “bottom up”, admittedly triggered by “top down” forces. In general, the results support the importance of indirect (non-lethal) effects as the driving forces for the successful biomanipulations, particularly in slightly eutrophic reservoirs. Not least, the delayed zooplankton response provides an indication that the underlying change of internal feedbacks was not driven by external forces to stabilize the reservoirs trophic state in these deep stratifying reservoirs. Handling editor: D. Ryder     

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

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

Macroinvertebrate and diatom communities as indicators for the biological assessment of river Picentino (Campania,Italy)

Pollution of rivers is an increasing problem that affects biological diversity and structure of natural ecosystem. The present study reported the results of the preliminary analysis of diatom and macroinvertebrate communities of river Picentino (Italy, Campania) in respect of the WFD/60/2000/EC. Because of the sensitive to a variety of environmental factors the two categories of organism are used as excellent indicators of changes taking place in water ecosystems, especially eutrophication. Sampling of benthic diatoms and macroinvertebrates has been carried out in five stations along the river during April–May 2014 in order to apply the ICMi and the STAR_ICMi and assess river quality. The data showed a diversification in diatomic and macroinvertebrate communities in relation to environmental stresses and level of pollution, with the disappearance of species higher sensitive to eutrophication and organic load in the upper course of the river. River water quality was found to deteriorate from the upperstream to the downstream because of the increasing of human impact and the intensive agriculture activity along the river.We conclude that the monitoring of diatomic and macroinvertebrate communities could give detailed information about the ecological status of rivers. However it is necessary to increase the achieved data by monitoring other biological communities in order to define adequated strategies to save and preserve the rivers habitat.     

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.     

Epiphytic,littoral diatoms as bioindicators of shallow lake trophic status: Trophic Diatom Index for Lakes (TDIL) developed in Hungary

Littoral diatoms are important contributors of the primary production in shallow aquatic ecosystems and they can be used as indicators of the trophic status. The aim of the study was to develop an index to assess trophic status of Hungarian lakes as suggested by the Water Framework Directive. In spring of 2005 and 2006, epiphytic diatom samples were collected from 83 shallow lakes. Weighted average method was used to develop and test the TP model. In the developed TP model correlation between the observed and diatom inferred TP was high (r ² = 0.96, n = 67). The optimum and tolerance TP parametrics of 127 species were determined and trophic indicator and sensibility values were defined for the Trophic Diatom Index for Lakes (TDIL). The TDIL was applicable to assess the ecological status of Hungarian shallow lakes. According to the TDIL the ecological status of 4 lakes were in excellent, 25 in good, 21 in medium, 21 in tolerable and 12 in bad status. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users. Handling editor: K. Martens