Development of a fish-based index to assess the eutrophication status of European lakes

The use of the CEN (European Committee for Standardization) standard method for sampling fish in lakes using multi-mesh gillnets allowed the collection of fish assemblages of 445 European lakes in 12 countries. The lakes were additionally characterised by environmental drivers and eutrophication proxies. Following a site-specific approach including a validation procedure, a fish index including two abundance metrics (catch per unit effort expressed as fish number and biomass) and one functional metric of composition (abundance of omnivorous fish) was developed. Correlated with the proxy of eutrophication, this index discriminates between heavily and moderately impacted lakes. Additional analyses on a subset of data from Nordic lakes revealed a stronger correlation between the new fish index and the pressure data. Despite an uneven geographical distribution of the lakes and certain shortcomings in the environmental and pressure data, the fish index proved to be useful for ecological status assessment of lakes applying standardised protocols and thus supports the development of national lake fish assessment tools in line with the European Water Framework Directive.     

Homogenization of fish assemblages in different lake depth strata at local and regional scales

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A fish-based index for the assessment of the ecological quality of temperate lakes

A fish – based index for the assessment of the ecological quality of natural temperate lakes was developed, in accordance to the requirements of the Water Framework Directive (WFD) 2000/60/EC. As a case study, 11 natural lakes located at northern and western Greece were selected. Fish surveys were conducted during mid summer to mid autumn in 2010, 2011 and 2012 using Nordic gillnets and electrofishing. Environmental parameters and anthropogenic pressures were assessed for each lake. Fish species richness, abundance, trophic, reproductive and habitat functional guilds were used for extracting a set of 107 metrics, meeting the requirements of the WFD. All metrics were initially tested as candidates for the index development. A stepwise linear regression of each metric against environmental parameters (lake area, altitude, maximum depth, alkalinity) and anthropogenic pressures (drainage area covered by non-natural land uses – NNLC, water total phosphorus concentrations – TP, Lake Habitat Modification Score – LHMS) was initially conducted for ensuring pressure-response relationships. Reference conditions for each lake were estimated by the hindcasting procedure and the ecological quality for each lake was expressed as the ecological quality ratio (EQR) by a value ranging from 0 (poor quality) to 1 (excellent quality). Two fish fauna metrics, the relative numerical abundance of introduced species (Introduced_a) and the relative biomass of omnivorous species (OMNI_b) were finally extracted as the most significant, responding to LHMS and TP, respectively. The final index was expressed as the mean values of the EQRs of these two metrics. The multimetric fish index presented herein could serve as a tool for assessing the ecological quality of natural lakes at broad geographical scale and generally, in the Mediterranean temperate lakes with similar hydromorphological characteristics.     

Development and application of an ecological classification tool for fish in lakes in Ireland

A classification tool suitable for establishing the ecological status of lakes based on fish population parameters has been developed for the Republic of Ireland and Northern Ireland (EU Water Framework Directive Ecoregion 17). A lake typology relevant to fish populations in lakes from Ecoregion 17 was produced as part of the ecological classification tool development. Four lake types were determined based on fish metrics and abiotic variables from 43 “reference” lakes. The specific lake fish typology categorised lakes into low (≤67 CaCO₃ mg L⁻¹) or high (>67 CaCO₃ mg L⁻¹) alkalinity, and shallow (≤17 m) or deep (>17 m) maximum depth. The fish in lakes classification tool (FIL2) follows a novel multimetric predictive approach, assigning ecological status to a lake using two independent methods. FIL2 qualitatively defines a lake's ecological status based on fish metrics using discriminant classification rules and, using a generalised linear model, quantitatively derives an Ecological Quality Ratio (EQR, 0 < EQR < 1), along with associated confidence intervals. It is recommended that both methods are used to validate output and cross-check and highlight potential misclassification.     

Major changes in CO<Subscript>2</Subscript> efflux when shallow lakes shift from a turbid to a clear water state

Lakes can be sources or sinks of carbon, depending on local conditions. Recent studies have shown that the CO₂ efflux increases when lakes recover from eutrophication, mainly as a result of a reduction in phytoplankton biomass, leading to less uptake of CO₂ by producers. We hypothesised that lake restoration by removal of coarse fish (biomanipulation) or invasion of mussels would have a similar effect. We studied 14–22 year time series of five temperate Danish lakes and found profound effects on the calculated CO₂ efflux of major shifts in ecosystem structure. In two lakes, where limited colonisation of submerged macrophytes occurred after biomanipulation or invasion of zebra mussels (Dreissena polymorpha), the efflux increased significantly with decreasing phytoplankton chlorophyll a. In three lakes with major interannual variation in macrophyte abundance, the efflux declined with increasing macrophyte abundance in two of the lakes, while no relation to macrophytes or chlorophyll a was found in the third lake, likely due to high groundwater input to this lake. We conclude that clearing water through invasive mussels or lake restoration by biomanipulation may increase the CO₂ efflux from lakes. However, if submerged macrophytes establish and form dense beds, the CO₂ efflux may decline again.     

Is the island biogeography model a poor predictor of biodiversity patterns in shallow lakes?

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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.     

Restoration of shallow lakes by nutrient control and biomanipulation—the successful strategy varies with lake size and climate

Major efforts have been made world-wide to improve the ecological quality of shallow lakes by reducing external nutrient loading. These have often resulted in lower in-lake total phosphorus (TP) and decreased chlorophyll a levels in surface water, reduced phytoplankton biomass and higher Secchi depth. Internal loading delays recovery, but in north temperate lakes a new equilibrium with respect to TP often is reached after <10–15 years. In comparison, the response time to reduced nitrogen (N) loading is typically <5 years. Also increased top-down control may be important. Fish biomass often declines, and the percentage of piscivores, the zooplankton:phytoplankton biomass ratio, the contribution of Daphnia to zooplankton biomass and the cladoceran size all tend to increase. This holds for both small and relatively large lakes, for example, the largest lake in Denmark (40 km²), shallow Lake Arresø, has responded relatively rapidly to a ca. 76% loading reduction arising from nutrient reduction and top-down control. Some lakes, however, have proven resistant to loading reductions. To accelerate recovery several physico-chemical and biological restoration methods have been developed for north temperate lakes and used with varying degrees of success. Biological measures, such as selective removal of planktivorous fish, stocking of piscivorous fish and implantation or protection of submerged plants, often are cheap versus traditional physico-chemical methods and are therefore attractive. However, their long-term effectiveness is uncertain. It is argued that additional measures beyond loading reduction are less cost-efficient and often not needed in very large lakes. Although fewer data are available on tropical lakes these seem to respond to external loading reductions, an example being Lake Paranoá, Brazil (38 km²). However, differences in biological interactions between cold temperate versus warm temperate-subtropical-tropical lakes make transfer of existing biological restoration methods to warm lakes difficult. Warm lakes often have prolonged growth seasons with a higher risk of long-lasting algal blooms and dense floating plant communities, smaller fish, higher aggregation of fish in vegetation (leading to loss of zooplankton refuge), more annual fish cohorts, more omnivorous feeding by fish and less specialist piscivory. The trophic structures of warm lakes vary markedly, depending on precipitation, continental or coastal regions locations, lake age and temperature. Unfortunately, little is known about trophic dynamics and the role of fish in warm lakes. Since many warm lakes suffer from eutrophication, new insights are needed into trophic interactions and potential lake restoration methods, especially since eutrophication is expected to increase in the future owing to economic development and global warming.     

Estimating soil carbon sequestration under elevated CO2 by combining carbon isotope labelling with soil carbon cycle modelling

Elevated CO₂ concentrations generally stimulate grassland productivity, but herbaceous plants have only a limited capacity to sequester extra carbon (C) in biomass. However, increased primary productivity under elevated CO₂ could result in increased transfer of C into soils where it could be stored for prolonged periods and exercise a negative feedback on the rise in atmospheric CO₂. Measuring soil C sequestration directly is notoriously difficult for a number of methodological reasons. Here, we present a method that combines C isotope labelling with soil C cycle modelling to partition net soil sequestration into changes in new C fixed over the experimental duration (C_new) and pre‐experimental C (C_old). This partitioning is advantageous because the C_new accumulates whereas C_old is lost in the course of time (ΔC_new>0 whereas ΔC_old<0). We applied this method to calcareous grassland exposed to 600 μL CO₂ L^?1 for 6 years. The CO₂ used for atmospheric enrichment was depleted in ¹³C relative to the background atmosphere, and this distinct isotopic signature was used to quantify net soil C_new fluxes under elevated CO₂. Using ¹³C/¹²C mass balance and inverse modelling, the Rothamsted model ‘RothC’ predicted gross soil C_new inputs under elevated CO₂ and the decomposition of C_old. The modelled soil C pools and fluxes were in good agreement with experimental data. C isotope data indicated a net sequestration of ≈90 g C_new m^?2 yr^?1 in elevated CO₂. Accounting for C_old‐losses, this figure was reduced to ≈30 g C m^?2 yr^?1 at elevated CO₂; the elevated CO₂‐effect on net C sequestration was in the range of≈10 g C m^?2 yr^?1. A sensitivity and error analysis suggests that the modelled data are relatively robust. However, elevated CO₂‐specific mechanisms may necessitate a separate parameterization at ambient and elevated CO₂; these include increased soil moisture due to reduced leaf conductance, soil disaggregation as a consequence of increased soil moisture, and priming effects. These effects could accelerate decomposition of C_old in elevated CO₂ so that the CO₂ enrichment effect may be zero or even negative. Overall, our findings suggest that the C sequestration potential of this grassland under elevated CO₂ is rather limited.     

Applicability of planktonic biomanipulation for managing eutrophication in the subtropics

Although large-bodied cladocerans such asDaphnia can reduce algal biomass significantly in temperate lakes if freed from fish predation, the applicability of such biomanipulation techniques for eutrophication management in the subtropics and tropics has been examined only recently. Subtropical cladoceran assemblages differ from those of temperate lakes by their low species richness, early summer gameogenesis, and greatly reduced body size. Eutrophic Florida lakes are dominated by pump-filter feeding fish rather than by size selective planktivores as a temperate lakes. Cladocerans in Florida lakes can increase in abundance significantly if freed from fish but fail to have an impact on algal biomass or composition. The greatest potential for using biomanipulation to manage phytoplankton-dominated lakes in the subtropics and tropics lies with phytophagous fish. Future research should concentrate on defining the role of individual fish taxa on phytoplankton composition and community structure, nutrient cycling, and planktonic productivity before embarking on whole lake manipulation projects.     

Occurrence of Cryptophyceae and katablepharids in boreal lakes

One of the most important algal groups in Finnish lakes are the Cryptophyceae. Changes in the community structure of Cryptophyceae in a total of 22 lakes belonging to the Vuoksi river basin in eastern Finland were studied. The existence of lakes with water qualities varying from oligotrophic to eutrophic, often loaded by human activities, provides a good opportunity to study the effects of environmental variables on the occurrence and size variation of Cryptophyceae. In the Vuoksi river basin, the main soil type is moraine. Twelve of the lakes were large or moderately large and with clear, i.e. oligo-humic water, and one lake could be described as a small clear water lake. Eight large or moderately large lakes were humic, with a water colour number of 40–70 mg l^?1 Pt, including three lakes impacted by nutrient loads. One lake was naturally eutrophic, with a high water colour number of 100 mg l^?1 Pt, and was also impacted by municipal and pulping effluents. CCA-ordination analysis grouped the studied lakes into: (1) clear water lakes, (2) humic lakes and (3) the naturally eutrophic brown water lake. In the CCA-ordination analysis based on cell numbers small Cryptophyceae (Cryptomonadales), Rhodomonas lacustris and the katablepharid Katablepharis ovalis were grouped into the first axis, which was positively correlated with Secchi depth (r=0.58) and NO₃N - nitrogen (r=0.24) and negatively with Ptot (r=-0.69), PO₄P (r=-0.69) and water colour number (r=-0.66). In humic lakes, medium-sized Cryptophyceae were abundant. The naturally eutrophic lake was grouped into first axis, which is positively correlated with Ptot (r=0.69), PO₄P (r=0.69) and water colour number (r=0.66). The lake formed a distinct group with large Cryptophyceae. Only in this lake was the heterotrophic Katablepharis ovalis rather abundant. However, large-sized taxa dominated the biomass of the Cryptophyceae assemblage in all lake types excluding large clear water lakes, where Rhodomonas lacustris dominated and large Cryptophyceae co-dominated.     

Biomonitoring potential of a Caryophyllaeid tapeworm: Evaluation of Adenoscolex oreini infection level and health status in three fish species of the genus Schizothorax across eutrophication and pollution gradients

Endoparasitic infections vary significantly across altered aquatic ecosystems, making these organisms ideal for the biomonitoring of degraded environments. To assess the biomonitoring potential of the Caryophyllaeid tapeworm Adenoscolex oreini and the possible impact of water quality on fish species, a study was carried out in three lakes with marked eutrophication and pollution gradients. The A. oreini infection level in three host fish species of the genus Schizothorax and corresponding fish health status were determined. The pattern of cestode infection varied significantly in the three fish species across the pollution gradient. The prevalence of infection in two fish species (Schizothorax esocinus and S. curvifrons) was significantly greater (P < 0.05) in the eutrophic lake than in the reference lake, whereas in S. niger, the maximum was reached in the hypereutrophic lake. The estimated marginal mean intensity and other infection indices varied significantly (P < 0.05) across the inter- and intra-pollution gradients of lakes. Multivariate statistical analysis results revealed maximum cestode infection in the eutrophic lake. An altered seasonal pattern was observed in the highly stressed lake. The gonadosomatic index (GSI) and condition factor values were significantly greater in fish collected from the reference lake than in those collected from the other lakes. A significant negative relationship between GSI and cestode prevalence was observed in the hypereutrophic lake as compared to least eutrophic lake. These findings indicate that infection indices of the Caryophyllaeid tapeworm and health attributes of fish can act as surrogates for the environmental quality of deteriorated lentic water bodies of the north-western Himalayan region, which is currently undergoing environmental degradation.     

Phytoplankton lipid content influences freshwater lake methanogenesis

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Response of a shallow Mediterranean lake to nutrient diversion: does it follow similar patterns as in northern shallow lakes?

1. In view of the paucity of data on the response of warm shallow lakes to reductions in nutrient loading, this paper presents a long‐term limnological data set to document changes in the food‐web of a shallow Mediterranean lake (Lake Albufera, Valencia, Spain) that has experienced reductions in phosphorus (P) (77%) and nitrogen (N) (24%) loading following sewage diversion. 2. Nine years after sewage diversion, P concentration in the lake was reduced by 30% but remained high (TP = 0.34 mg L^?1), although the mean water retention time in the lake was only 0.1 years. Nitrate concentrations did not significantly change, probably because the lake continued to receive untreated effluents from ricefields. 3. Chlorophyll a concentration was reduced by half (annual mean of 180 μg L^?1). Cyanobacteria abundance remained high but its composition changed towards smaller species, both filamentous and chroococcal forms. 4. Cladocera abundance increased and reached peaks twice a year (December to March and July to September). After nutrient reduction, short‐term clear‐water phases (up to 5 weeks) occurred during February to March in several years, concomitant with annual flushing of the lake and lower fish densities. The abundance of Cladocera in winter contrasted with the spring peaks observed in northern restored shallow lakes. The zooplankton to phytoplankton biomass ratio remained lower than in northern temperate shallow lakes, probably because of fish predation on zooplankton. 5. Improvement of the water quality of Lake Albufera remained insufficient to counteract littoral reed regression or improve underwater light allowing submerged plants re‐colonise the lake. 6. Sewage diversion from Lake Albufera impacted the food web through the plankton, but higher trophic levels, such as fish and waterfowl, were affected to a lesser degree. Although the fish species present in the lake are mainly omnivorous, long‐term data on commercial fish captures indicated that fish communities changed in response to nutrient level and trophic structure as has been observed in restored shallow lakes at northern latitudes. 7. Phosphorus concentrations produced similar phytoplankton biomass in Lake Albufera as in more northern shallow lakes with abundant planktivorous fish and small zooplankton. However, in Lake Albufera, high average concentrations were maintained throughout the year. Overall, results suggest that nutrient control may be a greater priority in eutrophicated warm shallow lakes than in similar lakes at higher latitudes.     

Lake trophic state and the limnological effects of omnivorous fish

Ecologists have hypothesized that planktivorous fish have greater effects on the plankton and water quality of oligotrophic lakes than eutrophic lakes. We tested this hypothesis in a tank-mesocosm experiment of factorial design in which five biomass levels of filter-feeding omnivorous gizzard shad (Dorosoma cepedianum) were cross-classified with two levels of lake trophic state achieved by filling tank-mesocosms with water and plankton transported by truck from two lakes with different trophic states. The presence of gizzard shad significantly increased total phosphorus, primary productivity, chlorophyll, and particulate phosphorus (PP) 2–20 and 20–200 μm and significantly decreased Secchi depth, cladocerans, copepods and PP > 200 μm. The effects of gizzard shad on chlorophyll, Secchi depth, cladocerans, copepods and PP 2–20 and > 200 μm were dependent on lake trophic state and most intense in the eutrophic lake system. This experiment suggests that filter-feeding omnivorous fish interact synergistically with trophic state so that the limnological effects of omnivorous fish become more intense with increased eutrophication.     

Copepods as environmental indicator in lakes: special focus on changes in the proportion of calanoids along nutrient and pH gradients

Copepods are important contributors to the zooplankton community in lakes. Being “sandwiched” between predators and resources, they are sensitive to changes in the environment. It has been proposed that the proportion of calanoids of total copepod abundance or biomass could be a valuable indicator of eutrophication. We investigated relationships between environmental factors and the abundance, biomass and size of calanoid and cyclopoid copepods as well as their proportions in summer in 68 Danish freshwater lakes (587 lake years) with contrasting nutrient levels and pH. When lake pH was?<?6.0, mean lake depth and trophic state were the most important factors and calanoids completely dominated the copepod community. In shallow lakes with a mean depth?<?2.5 m and with pH?>?6.0, the proportion of calanoids in terms of biomass decreased substantially with increasing phosphorus and chlorophyll a concentrations but stayed around 50% at?>?2.5 m depth irrespective of nutrient level. Time series of the lakes, recovering from eutrophication, confirmed this multi-lake pattern although the trajectory varied from lake to lake. We conclude that the proportion of calanoids in terms of biomass might be a valuable indicator of trophic state in shallow but not deep lakes and only when pH?>?6.

     

Mesocosm experiments on nutrient and fish effects on shallow lake food webs in a Mediterranean climate

1. Nutrient and fish manipulations in mesocosms were carried out on food‐web interactions in a Mediterranean shallow lake in south‐east Spain. Nutrients controlled biomass of phytoplankton and periphyton, while zooplankton, regulated by planktivorous fish, influenced the relative percentages of the dominant phytoplankton species. 2. Phytoplankton species diversity decreased with increasing nutrient concentration and planktivorous fish density. Cyanobacteria grew well in both turbid and clear‐water states. 3. Planktivorous fish increased concentrations of soluble reactive phosphorus (SRP). Larger zooplankters (mostly Ceriodaphnia and copepods) were significantly reduced when fish were present, whereas rotifers increased, after fish removal of cyclopoid predators and other filter feeders (cladocerans, nauplii). The greatest biomass and diversity of zooplankton was found at intermediate nutrient levels, in mesocosms without fish and in the presence of macrophytes. 4. Water level decrease improved underwater light conditions and favoured macrophyte persistence. Submerged macrophytes (Chara spp.) outcompeted algae up to an experimental nutrient loading equivalent to added concentrations of 0.06 mg L^?1 PO₄‐P and 0.6 mg L^?1 NO₃‐N, above which an exponential increase in periphyton biomass and algal turbidity caused characean biomass to decline. 5. Declining water levels during summer favoured plant‐associated rotifer species and chroococcal cyanobacteria. High densities of chroococcal cyanobacteria were related to intermediate nutrient enrichment and the presence of small zooplankton taxa, while filamentous cyanobacteria were relatively more abundant in fishless mesocosms, in which Crustacea were more abundant, and favoured by dim underwater light. 6. Benthic macroinvertebrates increased significantly at intermediate nutrient levels but there was no relationship with planktivorous fish density. 7. The thresholds of nutrient loading and in‐lake P required to avoid a turbid state and maintain submerged macrophytes were lower than those reported from temperate shallow lakes. Mediterranean shallow lakes may remain turbid with little control of zooplankton on algal biomass, as observed in tropical and subtropical lakes. Nutrient loading control and macrophyte conservation appear to be especially important in these systems to maintain high water quality.     

Long‐term effects of climate change on carbon flows through benthic secondary production in small lakes

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Periphyton-macroinvertebrate interactions in light and fish manipulated enclosures in a clear and a turbid shallow lake

In a clear and a turbid freshwater lake the biomasses of phytoplankton, periphytic algae and periphytonassociated macrograzers were followed in enclosures with and without fish (Rutilus rutilus) and four light levels (100%, 55%, 7% and < 1% of incoming light), respectively. Fish and light affected the biomass of primary producers and the benthic grazers in both lakes. The biomass of primary producers was generally higher in the turbid than the clear lake, and in both lakes fish positively affected the biomass, while shading reduced it. Total biomass of benthic grazing invertebrates was higher in the clear than in the turbid lake and the lakes were dominated by snails and chironomids + ostracods, respectively. While light had no effect on the biomass of grazers in the clear lake, snail breeding was delayed in the most shaded enclosures and presence of fish reduced the number of snails and the total biomass of grazers. In the turbid lake ostracod abundance was not influenced by light, but was higher in fish-free enclosures. Density of chironomids correlated positively with periphyton biomass in summer, while fish had no effect. Generally, light-mediated regulation of primary producers was stronger in the turbid than in the clear lake, but the regulation did not nambiguously influence the primary consumers. However, regulation by fish of the benthic grazer community was stronger in the clear than in the turbid lake, and in both lakes strong top-down effects on periphyton were seen. The results indicate that if present-day climate in Denmark in the future is found in coastal areas at higher latitudes, the effect of lower light during winter in such areas will be highest in clear lakes, with typically lower fish biomass and higher invertebrate grazer density.