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     

Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton

Coherence between ecological status assessment by phytoplankton and attached diatoms was analyzed in the littoral zone of Lake Balaton. Sampling of periphytic diatoms, phytoplankton, and water were carried out at ten different littoral sites in the northern and southern shores of the lake for a year. Phytoplankton species were sorted into functional groups and ecological status was assessed by means of the phytoplankton assemblage Q index. The index TDIL was calculated using quantitative attached diatom data. Significant differences were found between the ecological assessments based on phytoplankton and phytobenthos metrics, both seasonally and spatially. The Q index indicated ecological states varying from bad to good, while the average of diatom indices varied from moderate to high conditions. The Q index provided more realistic ecological status of Lake Balaton, compared with trophic status based on TP values, especially in the summer period. Differences in the response-time indication of phytoplankton and attached diatoms suggest that lack of coherence should also be expected between the responses of other BQEs.     

Do we similarly assess diversity with microscopy and high-throughput sequencing? Case of microalgae in lakes

Diatoms are a species-diverse phylum of microalgae often presenting high biomass in aquatic habitats. This makes them excellent ecological indicators in rivers and lakes. They are routinely used to assess ecological quality of rivers and lakes using microscopy, which is time consuming. An alternative is to determine species in samples based on short DNA barcodes and high-throughput sequencing (HTS). Former studies showed that community structure and water quality assessments based on diatoms deliver similar results with both methods. But, none evaluated if diversities were assessed in the same way despite the importance of this ecological metric. Based on littoral benthic samplings carried out in 56 pristine alpine lakes, we compared different diversity indices measured with microscopy and metabarcoding. Each lake was sampled in three different places of its littoral. We showed that α (diversity measured in a single sampling site of a given lake) and ? (total diversity in a lake where three independent samples were considered) diversities obtained with HTS were higher than those obtained with microscopy. This may be explained by the capacity of HTS to detect morphologically cryptic species and to better detect rare taxa. On the other hand, β diversity obtained with HTS was smaller, which may be explained by the capacity of HTS to detect very rare species and free-floating extracellular DNA. Nevertheless, diversity indices obtained with both methodologies were well correlated each other. This study validates the possibility to assess diatom diversity with HTS in a comparable way to the classical microscopic analysis.     

Aquatic plants as environmental indicators of ecological condition in New Zealand lakes

Submerged aquatic plants can act as measurable indicators of ecological conditions occurring within a lake, and they need only be monitored once a year or even less. Historically in New Zealand there has been a reliance on water quality sampling for monitoring the health of lakes and these methods can be complex and costly involving multiple site visits and chemical analysis of water samples. As a result, lake monitoring has been irregular, or not done at all. LakeSPI or ‘Lake Submerged Plant Indicators’ is a new management tool that uses aquatic plants to monitor and assess ecological condition in a wide range of lake types. The method generates three indices: a Native Condition Index (extent and diversity of native plants) and an Invasive Condition Index (extent and impact of alien weeds), which are generated from scores allocated to carefully selected vegetation features; and an integrated LakeSPI Index which is largely derived from components of the other two indices and provides an overall indication of lake ecological condition. The LakeSPI method can be used to assess the status of lakes and monitor trends occurring within them, and it is expected that the use of LakeSPI will facilitate regular monitoring and reporting on a much wider range of lakes than has been possible using traditional water quality methods. By utilizing submerged aquatic plants the method focuses on lake littoral margins where there is greatest public interaction and interest.     

In situ photochemical activity of the phytobenthic communities in two Antarctic lakes

Photochemical activity of phytobenthic communities in two freshwater lakes in East Antarctica was estimated using a submersible pulse-amplitude modulation (PAM) chlorophyll fluorometer, to answer the following questions: (1) Are the communities under bright summer photosynthetically active radiation (PAR) photosynthetically active? (2) If active, which community shows the most active signals? (3) Where is the most productive part (or depth) in the lake? Our limnological measurements indicated the two lakes were ultra-oligotrophic. Diving observations revealed that the phytobenthos of the lakes was moss-dominated which had different life-forms (moss shoots in shallow depths of both lakes, moss-pillars in the shallow lake, pinnacle moss-microbial complex community in the deeper lake). In addition, various mat-forming microbial communities inhabited the lake beds. In situ measurements of photochemical parameters indicated that shoots of mosses living just below the littoral slope, and the apical part of the moss pillars, had the highest photosynthetic activity in open water summer conditions, but mat-forming microbial communities and the other moss-microbial complex communities, showed rather lower activity. Most of the mat-forming phytobenthos surface also showed positive photosynthetic activity, but there were some cases of negligible signals in the shallow depth. This suggests that the photosynthetic activities of mat-forming communities in the shallow water were suppressed by strong ambient light in summer.     

Littoral diatoms as indicators for the eutrophication of shallow lakes

The littoral zone of shallow water bodies in the Czech Republic has been studied quite consistently at several fishponds. The use of algae, especially diatoms, for the monitoring of the state of lotic freshwater also has a long tradition. The main objective of the presented paper is to validate the feasibility of the use of littoral periphyton comunities for the biomonitoring of standing waters. At the investigated sites, littoral periphytic diatoms were studied together with selected enviromental variables (pH, conductivity, nutrients – especially total phosphorus) on three types of natural substrates (epilithon, epiphyton, epipelon). The evaluation of the diatom community was performed on the basis of the checklists of algal indicator species published by authors from the Czech Republic, Austria and the Netherlands. The data were subjected to statistical software NCCS 2000 (GLM Anova and ``Ward's minimum'' variance cluster analysis). Littoral periphytic diatoms appear to be good indicators of the fishpond water quality. The selected substrates show non-significant differences therefore the average values from all substrates were used. The best indicatory system for evaluation of Czech fishponds was van Dam's index.

     

Benthic diatoms and phytoplankton to assess nutrients in a large lake: Complementarity of their use in Lake Geneva (France–Switzerland)

Lakes can be monitored using different bioindicators, among which phytoplankton and benthic diatoms. We compared these two indicators in Lake Geneva for nutrient assessment. Bimonthly samplings were carried out during one year in the euphotic layer of a pelagic site. In the same time four littoral sites were sampled at 40–50 cm depth. Species compositions and abundances of both bioindicators were analyzed following European standards. Water physico-chemical composition was analyzed at the same time. Seasonal succession of benthic diatom guilds was observed. The dynamics of benthic diatom communities were better correlated to the pelagic chemistry than to the local littoral chemistry. We also observed that in the sampling sites frequently exposed to winds and waves, benthic diatoms showed lower correlations to physico-chemical dynamics, because of an increase of pioneer diatoms abundance adapted to turbulent environment, such sites must be avoided for lake monitoring. Finally, biotic indices calculated with benthic diatoms in wind protected sites showed higher correlations with pelagic nutrient concentration (PO₄³⁻) than indices calculated with phytoplankton. This unexpected situation can be explained by differences of temporal variability of chemical and biological compartments. Littoral chemistry changed faster than pelagic chemistry because of rains, diffuse flow from watershed and rivers flowing in the littoral zone whereas pelagic chemistry has a much smoother evolution because it is situated 10 km from the coast. But phytoplankton showed a high temporal variability because of wind influence, which explained the low correlation with the smooth evolution of pelagic chemistry. On the other hand, benthic diatoms from sites protected from the dominant wind, showed a lower temporal variability and were more in synchrony with the smooth evolution of pelagic chemistry.Even if we show that diatom seem to be promising indicator of nutrient level of the lake, we also underline the complementarity of using both indicators: benthic diatom and phytoplankton. Each of them brings different information about temporal variability of the lake and about the functioning of different habitats. Comparing these two bioindicators only on the basis of nutrient correlation ability would be an over-simplification whom managers must be warned.     

Water geochemistry and sedimentary pigments in northern Victoria Land lakes,Antarctica

Total concentrations of algal pigments, organic C, C, N, P and S were determined in surface sediments from the littoral zone of 21 lakes in ice-free areas of northern Victoria Land (Antarctica) with different climatic and environmental conditions. Concentrations of major ions and nutrients were also determined in water samples from the same lakes. The latter samples had extremely variable chemical compositions; however, all the lakes resulted oligotrophic. Pigment concentrations in surface sediments were comparable to those reported for other Antarctic lakes and lower than those in oligotrophic lakes at lower latitudes. Cyanophyta, Chlorophyta and Bacillariophyta were the main taxa identified. These taxa correspond to those reported in previous microscopy-based studies on Antarctic phytoplankton and phytobenthos. Discriminant Function Analysis and Canonical Correspondence Analysis of data indicate that the distribution of pigments in these Victoria Land lakes depends mainly on their geographical location (particularly the distance from the sea) and nutrient status.     

Uncertainty in Diatom Assessment: Sampling, Identification and Counting Variation

Despite the widespread application of periphytic diatoms to water quality assessment at a regional level, there is no standard European sampling protocol or associated assessment metrics. Furthermore, relatively little is known about the uncertainty in the results of such assessments. One of the objectives of the European project for the Standardisation of River Classifications (STAR) is to improve and standardise diatom assessment methods. An extensive diatom ring test, together with an audit of the project results, provided a better understanding and quantification of the uncertainty in quality assessment of running waters using diatoms. The variation in multimetric analysis shows that the choice of site and substrate for sampling, the inter-operator differences in diatom taxonomy and the counting techniques are the primary sources of uncertainty. To some extent, this variation also reveals the robustness of specific metrics in relation to the sources of uncertainty. Of the three most common substrate types tested (stone, macrophyte and sediment), macrophytes emerge as the most preferred substrate for diatom sampling when performing multimetric water quality assessment.     

Assessment of eutrophication pressure on lakes using littoral invertebrates

Until the E.U. Water Framework Directive listed benthic invertebrates as a biotic element to be used for ecological classification of lakes, techniques for the assessment of the response of littoral invertebrates to anthropogenic pressures were extremely limited compared with those of rivers and lake profundal zones. We describe here the development of an ecological classification model based on changes of littoral invertebrate assemblages across a gradient of eutrophication, which is the most widespread anthropogenic pressure on lakes across Europe. The model comprises three derived parameters, two of which were developed from taxon-specific optima along a total phosphorus gradient calculated using canonical correspondence analysis, and the third based on invertebrate abundance. Combining the parameter metrics, we can estimate the ecological quality ratio (EQR), relative to those from paleolimnologically-confirmed reference lakes. The model was tested using independent samples collected from both hard and soft substrata and across two seasons from 45 lakes, comprising three alkalinity groups (n = 15 in each), and across gradients in water column total phosphorus concentrations. For hard substrata, EQRs were related consistently and highly significantly to water column concentrations of total phosphorus, accounting for the majority of the variance in every alkalinity group. For samples taken from soft substrata, a significant relationship was found only for high alkalinity lakes, accounting for a moderate proportion of the variability in water column total phosphorus concentrations. Our results compare highly favourably with those from other aquatic ecological assessment methods, irrespective of the faunal or floral group upon which they are based, demonstrating that littoral invertebrate assemblages can provide a statistically robust prediction of nutrient status when samples are collected from hard substrata. While the method was developed specifically to assess nutrient pressures on littoral invertebrates, many lakes are subject to multiple pressures. The development of classification models that incorporate multiple pressures presents a particularly significant challenge for the implementation of the Water Framework Directive, requiring both reliable identification of minimally-impacted reference states and incorporation of pressures that are unlikely to interact in predictable ways.     

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.     

Quantifying rotifer species richness in temperate lakes

1. Biodiversity assessments of lakes depend on the ability to identify the complement of species present, although the degree of sampling required is often uncertain. We utilise long‐term data to predict rotifer species richness in three habitats in three Polish lakes using rarefaction sampling methods. 2. Richness in littoral and psammon habitats did not saturate, even with up to 130 samples. Highest richness was observed in psammon habitat (119 species) in Lake Mikolajskie, followed by littoral habitat in Lakes ?uknajno (114 species) and Kuc (110 species). Littoral habitats in Lakes ?uknajno (56%) and Kuc (51%) had the most species not shared with other habitats in the same lake. 3. Species richness (Chao2) estimates ranged between 44 for pelagic and 135 for psammon habitat in Lake Mikolajskie, to 100 for psammon and 137 for littoral habitat in Lake Kuc, and 65 for pelagic and 162 for littoral habitat in Lake ?uknajno. Whole lake estimates were 167, 205 and 171 species, respectively, for these lakes, higher than the 150 to 160 species predicted by Dumont and Segers (Hydrobiologia, 1996, 341 , 125). 4. Using standardised sampling, richness was significantly higher in littoral than either pelagic or psammon habitats. Contrasts of standardised rarefaction curves revealed that richness in Lakes Kuc and Mikolajskie was described as well by littoral‐only or psammon‐only samples, respectively, as by those randomly drawn from across all habitats in the lake. 5. Species richness estimates for Lake Mikolajskie were highest in summer, followed by autumn and spring. Interannual estimates differed by up to 427%, nearly an order of magnitude greater than maximal seasonal variation of 70%. 6. Results indicate that much higher sampling intensity is required to establish species richness than is presently carried out in most lakes. Because many species can be detected only with very intensive sampling, conservation programmes must consider sampling intensity when designing studies.     

The WISER way of organising ecological data from European rivers, lakes, transitional and coastal waters

The implementation of the Water Framework Directive has required intense research in applied aquatic ecology in Europe, and thus created challenges for data management in international research projects. In the project Waterbodies in Europe: Integrative Systems to assess Ecological status and Recovery (WISER), biological and environmental data from rivers, lakes, transitional and coastal waters in 26 European countries were collated. More than one million records of biological observations were stored in the project’s central database, representing phytoplankton, macrophytes, macroalgae, angiosperms, phytobenthos, invertebrates and fish. The central database includes new data from the WISER field campaign in lakes and transitional/coastal waters during 2009–2010 (more than 6,000 biological samples from 58 waterbodies in 14 countries). The purpose of this paper is to provide an overview of the data collated within WISER, in order to facilitate future re-use of these data by other scientists. More specifically, the objectives are to (1) describe the data management in WISER, (2) describe the structure and content of the WISER central database and (3) share experiences and give recommendations for data management in large ecological research projects.     

Recommendations for the routine sampling of diatoms for water quality assessments in Europe

Many methods for using diatoms for routine monitoring of water quality have been developed in Europe and, in some countries, these are being used to enforce environmental legislation. In order to facilitate their wider use, particularly with respect to European Union legislation, steps are being taken to harmonize methodology. In this paper, the principles and practice of sampling are described in relation to the main habitat types encountered in Europe. Although details of methods and sampling programmes have to be tailored to particular circumstances and the overall objectives of the monitoring, a number of generalizations can be made. Where available, rocks and other hard surfaces are the preferred substrates and methods for sampling these are described. If such substrata are not available, then introduced ('artificial') substrata have many applications. Various types of introduced substrata can be used successfully, so long as some basic precautions are described. Other types of substrata such as macrophytes and macroalgae may also be useful under certain circumstances, although there is less consensus in the literature on the most appropriate methods, and of the validity of comparisons between indices computed from epiphytic and epilithic communities. When designing surveys, it is recommended that as far as possible, extremes of non-water quality factors (e.g. shade, current speed, etc) are avoided, unless these are characteristic of the system under investigation. Detailed guidelines for sampling epilithon are described. Along with the recommendations for sampling other substrata, it is hoped that these provide a framework that can be adapted to most river types in Europe. This revised version was published online in June 2006 with corrections to the Cover Date.     

Nitrogen limitation of the phytobenthos in Alpine lakes: results from nutrient‐diffusing substrata

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Mesohabitat-specific macroinvertebrate assemblage responses to water quality variation in mid-continent (North America) great rivers

We compared the responsiveness of macroinvertebrate assemblages to variation in water quality (ions, nutrients, dissolved metals, and suspended sediment) in two mesohabitats within the main channel of three North American great rivers, the Upper Mississippi, Missouri, and Ohio. Based on about 400 paired samples, we examined the responsiveness of benthic assemblages sampled in the littoral zone and assemblages sampled from the surface of woody snags in the main channel. The assemblages in the two mesohabitats were different in all rivers. Taxa richness was much higher in the benthos than on snags. Macroinvertebrate assemblage response to water quality variation was weak on the Mississippi River, but the reasons for this are unknown. Based on analysis of the similarity between the composition of assemblages from groups of sites with high and low concentrations of water quality variables, benthic assemblages were only slightly more sensitive to water chemistry variation than were snag assemblages. Results of two-sample comparisons between groups of sites with high and low concentrations of water quality variables were consistent with rank correlations of assemblage metrics with water quality. In general, there was little difference between habitats in response to variation in water quality on any river. Our simple method of snag sampling in great rivers is usually much easier than littoral benthic sampling because it does not require wading. Snag sampling in large rivers has some limitations (e.g., natural snags are sometimes absent, samples are semi-quantitative), but lack of sensitivity to water quality gradients compared to the benthos is not among them.     

Comparative study of monitoring South-Finnish rivers and streams using macroinvertebrate and benthic diatom community structure

In southern Finland, most of the rivers are turbid and suffer from eutrophication and leaching of suspended solids from diffuse sources. We first related benthic diatom and macroinvertebrate structure to environmental factors using direct ordination. Second, benthic diatoms and macroinvertebrates were simultaneously sampled in several South-Finnish rivers and streams to compare two monitoring methods. The study sites constituted of some large, moderately nutrient rich rivers and some smaller, less eutrophic streams situated on the south coast of Finland. Diatom species distribution was most affected by conductivity, total P and latitude. Species distribution of macroinvertebrates was mostly related to channel width, conductivity and pH. For diatoms, separation of community structure between sampling stations was clear, but corresponding macroinvertebrate communities were more similar to each other. Correlation between diatom and macroinvertebrate pollution indices was rather low and insignificant (r = 0.28). As a whole, variation of macroinvertebrate index values (CV = 4.7%) among replicate samples was slightly lower than for diatom index (CV = 6.0%). On the contrary, community similarity between the replicate samples was slightly lower among macroinvertebrates (r = 0.770) due probably to their larger local scale spatial variation, sampling of more habitats and lower density compared to diatoms (r = 0.874). In conclusion, multiple pressures affecting the river ecosystems at different spatial and temporal scales should lead to choosing more than one biological monitoring method with clearly identifiable responses.     

The Great Lakes in East Africa: biological conservation considerations for species flocks

The three largest water bodies of East Africa, Lake Victoria, Tanganyika, and Malawi contain an estimated number of 2,000 endemic cichlid fish species, in addition, to a mostly uncounted wealth of invertebrates. While the terrestrial diversity is reasonably well protected, as economic and touristic interests coincide with biological conservation strategies, this is not the case for most African lakes and rivers. Nonetheless, it must be promoted that these aquatic ecosystems also deserve protection. Conservation strategies for aquatic biota have so far been the same as for terrestrial environments, i.e., by declaring biodiversity hotspots national parks. Such parks also contain rivers and lake shores. Here, I argue that it seems questionable that this strategy will work, given strong micro-geographic structure of the species flocks and the great degree of local endemism. I suggest a novel strategy for protecting African Lake communities that accounts for local endemism, derived from recent molecular phylogenetic and phylogeographic studies on East African cichlid fishes. While connectivity is the major problem for terrestrial and marine national parks, to ensure a large enough effective population size of the protected animals, this is not the case in most taxa of African rivers and lakes, where local endemism prevails. For example, most littoral cichlid species are subdivided into numerous distinct “color morphs” with restricted distribution, and unlike marine fishes with planktonic larvae display brood care with small offspring numbers. It is argued that the establishment of “micro-scale protected areas,” a large number of small stretches of strictly protected coast line, each only some hundreds of meters long, is likely to work best to preserve the littoral communities in African lakes. Such protected zones can sustain a reasonably effective population size of littoral species, serve as protected spawning ground or nursery area for pelagic species, and at the same time re-seed neighboring populations that are exploited continuously. As long-term stability of littoral fishing grounds is in the immediate interest of village communities, such small protected areas should be managed and controlled by the local communities themselves, and supervised by governmental institutions.     

Movement of plankton through lake-stream systems

1. River plankton are often assumed to come from upstream lakes, but the factors controlling the movement of plankton between lakes and rivers into outflow streams are unclear. We tested the possibility that the physical structure of the littoral zone near the lake outlet (depth, presence of macrophytes) and diurnal differences in plankton composition at the lake surface influence the movement of plankton from the lake into the stream and determine their persistence downstream. 2. Zooplankton and phytoplankton biomass, community composition and mean body size were compared between two deep lakes without macrophytes at the lake edge and two shallow lakes with macrophytes at the lake edge. Samples were collected day and night on three dates, in the lake centre, in the littoral zone adjacent to the lake outlet, at the outlet and at two sites downstream in Algonquin Park, Ontario, Canada. 3. The morphology of lake edges clearly affects the movement of lake zooplankton into outlet streams. Outlets draining deeper littoral zones had higher zooplankton biomass than shallow littoral outlets (P < 0.0001), but these differences disappeared within 50 m downstream of the lake. There was no difference in mean zooplankton body size among lake outlets or between littoral and outlet samples. However, shallow littoral zones were dominated by cyclopoid copepods and deeper littoral zones were dominated by Bosmina longirostris. In contrast, phytoplankton biomass entering the outlet was similar to that found within the lake and did not vary with lake outlet morphology. These effects were consistent across several sampling weeks and were not affected by surface zooplankton biomass changes associated with diurnal vertical migration in the lake centre. 4. A comparison with published river zooplankton data suggests that zooplankton are rapidly eliminated from shallow outlet streams (≤1 m deep) but persist in most deeper outlet rivers (≥2 m deep). Because the depth of an outlet river determines downstream zooplankton community development, the contribution of lakes to river plankton communities may be influenced by the location of each lake within the drainage basin. These findings suggest that lake and outflow physical structure influences connection strength between spatially successive habitats.