Edited by: Isabelle Larocque-Tobler, The L.A.K.E.S. Institute, Switzerland
Reviewed by: Francoise Chalie, Centre Européen de Recherches et d'Enseignement des Géosciences de l'Environnement, France; Émilie Saulnier-Talbot, Unversité Laval, Canada
*Correspondence: Helen Bennion, Department of Geography, Environmental Change Research Centre, University College London, Pearson Building, Gower Street, London WC1E 6BT, UK
This article was submitted to Paleoecology, a section of the journal Frontiers in Ecology and Evolution
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Efforts to restore enriched lakes have increased yet there remains uncertainty about whether restoration targets can be achieved and over what timescale. Paleoecological techniques, principally diatom analyses, were used to examine the degree of impact and recovery in 12 European lakes subject to eutrophication and subsequent reduction in nutrient loading. Dissimilarity scores showed that all sites experienced progressive deviation from the reference sample (core bottom) prior to nutrient reduction, and principal curves indicated gradual compositional change with enrichment. When additive models were applied to the latter, the changes were statistically significant in 9 of the 12 sites. Shifts in diatom composition following reduction in nutrient loading were more equivocal, with a reversal toward the reference flora seen only in four of the deep lakes and one of the shallow lakes. Of these, only two were significant (Lake Bled and Mjøsa). Alternative nutrient sources seem to explain the lack of apparent recovery in the other deep lakes. In three shallow lakes diatom assemblages were replaced by a community associated with lower productivity but not the one seen prior to enrichment. Internal loading and top down control may influence recovery in shallow lakes and climate change may have confounded recovery in several of the study sites. Hence, ecosystem recovery is not simply a reversal of the degradation pathway and may take several decades to complete or, for some lakes, may not take place at all. By assessing ecological change over a decadal to centennial timescale, the study highlights the important role that paleolimnology can play in establishing a benchmark against which managers can evaluate the degree to which their restoration efforts are successful.
Most lakes throughout the world have been modified to some extent by human activity. Excessive nutrient and organic matter loading resulting in eutrophication has affected numerous waterbodies, most notably since the mid-twentieth century associated with the intensification of agriculture and expansion of populations connected to sewage treatment works (Joye et al.,
Efforts to restore enriched systems have increased over the last few decades and there are now numerous examples of lakes in recovery (Jeppesen et al.,
Whilst there are many individual success stories, there remains considerable uncertainty about whether restoration targets can be achieved and over what timescales one might expect to see improvement. Recovery may be a slow process as biotic communities tend to exhibit hysteresis and time-lags, and thus ecosystems take time to re-adjust to reduced stress (e.g., Yan et al.,
Legislative programmes are now in force to reduce pollution and restore aquatic ecosystems to good health in many regions of the world. In Europe, the Water Framework Directive (WFD) with its aim to restore waters to at least good status, has increased the need for effective restoration programmes for all lakes (European Union,
This paper employs palaeoecological techniques to examine the degree of impact and recovery in 12 European lakes that have been subject to eutrophication. Changes in the diatom assemblages, both community composition and diatom-inferred TP (DI-TP) concentrations, in sediment cores from the study lakes are assessed in response to enrichment and subsequent reduction in nutrient loading. The extent to which the diatom assemblages are approaching or deviating from reference conditions is explored using ordination and dissimilarity scores and the identification of the floristic changes is assessed statistically using additive models. The key questions being addressed are: (i) Do the observed changes reflect degradation and recovery?, (ii) Is the recovery pathway simply a reversal of the degradation pathway?, and (iii) Can the lake sediment record be used to track degradation and recovery and thus inform management?
The 12 study sites are located in European lowland catchments and represent a range of lake types in terms of lake area, depth, and trophic status (Table
Barton Broad (1995) | 52.7 | 1.5 | England | 2 | 0.77 | 1.5 | 74 | SN | Reduced external P loading since late 1970s; sediment removal to reduce internal P-loading from 1995 to 2000 |
Bosherston Central Lake (2001) | 51.6 | −4.9 | Wales | 2 | 0.34 | 2.0 | 20 | SN | Sewage diversion since 1984, bypass pipeline construction in 1992 |
Loch Leven (1999) | 56.2 | −3.4 | Scotland | 106 | 13.7 | 25.5a | 53 | SN | Reduced P loading since 1985 but internal loading issues |
Llangorse Lake (1996) | 51.9 | −3.3 | Wales | 156 | 1.4 | 9.0 | 118 | SN | Sewage diversion in 1981 and 1992 |
Marsworth Reservoir (1991) | 51.8 | −0.7 | England | 115 | 0.1 | 4.0 | 476 | SN | Sewage part-diversion and improved sewage treatment works in mid 1980s |
Lake Bled (1996) | 46.4 | 14.1 | Slovenia | 475 | 1.5 | 32.0 | 20 | DS | Sewage effluent diversion in 1982 |
Esthwaite Water (1997) | 54.4 | −3.0 | England | 65 | 1 | 15.5 | 28 | DS | Reduced P loading since 1986 but internal loading issues and fish farm present until 2009 |
Gjersjøen (2002) | 59.8 | 10.8 | Norway | 40 | 2.4 | 64.0 | 15 | DS | Sewage effluent diversion in 1971 |
Kiełpińskie (2010) | 53.4 | 19.8 | Poland | 120 | 0.61 | 11 | 105 | DS | Decrease in fertilizer use and change in land use in early 1990s |
Lidzbarskie (2009) | 53.3 | 19.8 | Poland | 128 | 1.22 | 25.5 | 66 | DS | Decrease in fertilizer use and change in land use in early 1990s |
Mill Loch (1998) | 55.1 | −3.4 | Scotland | 55 | 0.11 | 16.8 | 92 | DS | Exact restoration measure and timing unknown |
Mjøsa (2006) | 60.8 | 11 | Norway | 123 | 362 | 453.0 | 4 | DS | Improvements to sewage treatment works in late 1970s |
The lakes cover a wide range of current (annual mean) TP concentrations from 4 to 476 μg L−1, spanning the full trophic gradient from oligotrophic to hypertrophic conditions (Table
A sediment core was collected from the open water area of each lake as part of several different previous studies and, therefore, coring methods and analytical resolution vary from site to site. At least 10 samples from each core spanning the last ~200 years were analyzed for diatoms and, while there were typically >5 samples representing the post-restoration period, in a few cases there were only three samples available. Diatom analysis was carried out using standard methods (Battarbee et al.,
Chronologies for the cores included in this study were determined using radiometric methods. Selected sediment samples were analyzed for 210Pb, 226Ra, 137Cs, and 241Am by direct gamma assay using the methods of Appleby et al. (
The degree of floristic change in the diatom assemblages between the bottom sample and every other sample in the core was assessed using the squared chord distance (SCD) dissimilarity coefficient (Overpeck et al.,
The first axis scores of a principal components analysis (PCA) or a correspondence analysis (CA or detrended CA - DCA) often fail to capture a long or dominant gradient such as we might expect to be present in temporally-ordered data with progressive change in abundance or composition of organisms. As a result, the time series of axis one scores may be a poor summary of compositional change (Simpson and Birks,
The PrC scores were extracted for each fit and arranged in time order. To determine if statistically significant change in composition (e.g., eutrophication and subsequent recovery) could be identified, we modeled the time series of PrC scores using additive models, with a continuous time first-order autoregressive (CAR(1)) process for the residuals to account for the lack of independence between observations (Simpson and Anderson,
Approximate significance of the fitted trends can be achieved through the usual methods of statistical inference for additive models (Wood,
To estimate the first derivative of the fitted trend spline we use the method of finite differences, in which we predict from the model at the set of regularly-spaced time points and at a second set, shifted relative to the first by a very small amount. The rate of change in the predictions between the original and shifted points is an approximation to first derivative. How well the finite difference method approximates the unknown first derivative of the spline is governed by size of the shift, with smaller values producing more accurate approximations; we used a value of 0.000001 (of a year) as the shift but the results are not sensitive to a range of values around the chosen value. With each first difference estimate we also obtained its standard error and then formed a pointwise 95% confidence interval on estimate. Where this confidence interval excludes 0 (no change, zero slope) we conclude that significant change in PrC scores is observed for that time point. We indicate these periods of statistically significant change using thicker sections of the fitted trend when plotted. Color is also used to convey meaning; blue indicates significant decrease in PrC scores whilst red indicates significant increase. In some plots, we have negated the PrC scores such that enrichment in the diatoms is associated with smaller PrC scores, and less enriched periods with larger PrC scores. This is justified as the PrC score is defined as the arc length along the fitted principal curve from one arbitrarily-chosen end of the curve (Hastie and Stuetzle,
A diatom-TP transfer function was applied to the diatom data to reconstruct the trophic status of each site using either: (1) a training set of 56 relatively large, deep lakes (>10 m maximum depth) from Scotland, Northern Ireland, Cumbria, southern Norway, and central Europe with annual mean TP concentrations ranging from 1 to 73 μg TP L−1 and a median value of 22 μg TP L−1 (Bennion et al.,
The samples of each core were projected passively into a PCA of samples from the modern diatom-TP training sets described above, forming so called timetrack plots. These plots allow the direction of floristic change at each site to be visualized. The sample and species scores were plotted in ordination biplots to illustrate the degree to which the recovery trajectories follow back along the enrichment trajectories. For deep lakes only species that are present in at least two sites and with maximum abundance greater than or equal to 2% are shown and, for shallow lakes, these values were five occurrences and 5% abundance, respectively. These choices were purely for aesthetic reasons to improve the clarity of the plot whilst retaining labeling for the most abundant or frequently occurring taxa. Arrows have been added to the plots to illustrate the enrichment and post-restoration trajectories.
Unless stated otherwise, all analyses were conducted using R (version 3.1.3, R Core Team,
The dissimilarity scores between core bottom and other samples in each core indicate that all sites have experienced deviation from reference condition (core bottom sample) over the period represented by the cores (Figure
In four of the five shallow lakes (Barton Broad, Loch Leven, Llangorse Lake, and Marsworth Reservoir) the % plankton increases with enrichment but does not decline during the recovery phase (Figure
The PrC analysis shows that all sites experienced gradual yet unidirectional shifts in PrC scores during the eutrophication phase, occurring for example in Marsworth Reservoir from 1960 to 1980, in Lake Bled from 1940 to 1970 and in Gjersjøen from 1960 to 1980 (Figure
The additive model fits to the PrC scores indicate change in one direction to some degree in all sites except Gjersjøen, where the rapid shifts seen across relatively few data points are not well captured by the model and hence a flat line (no change, with strong residual autocorrelation) is the best fitting model (Figure
The diatom transfer functions infer an increase in TP concentrations in seven of the study lakes during the enrichment period (Figure
The PCA of the deep lakes training set revealed that axis 1 (PC1: eigenvalue 10.43) and axis 2 (PC2: eigenvalue 7.76) explained 16% and 12% of the variance in the species data, respectively. These values are relatively large for diatom training sets especially those with very many taxa as here. When the deep lake cores are plotted passively on a PCA of the large, deep lakes training set samples (Figure
The PCA of the shallow lakes training set revealed that PC1 (eigenvalue 9.93) and PC2 (eigenvalue 7.15) explained 15% and 11% of the variance in the species data, respectively. When the shallow lake cores are plotted passively on a PCA of the shallow lake training set samples (Figure
One of the challenges for ecologists wishing to track environmental change is to find biological indicators that are sufficiently sensitive to the pressure gradient of interest. Here, a range of diatom metrics were explored as diatoms are sensitive to changes in water quality and are particularly good indicators of lake nutrient concentrations (Hall and Smol,
The shifts in diatom composition following reduction in nutrient loading are more equivocal. A clear reversal toward the reference flora is seen only in three of the deep lakes, Lake Bled, Gjersjøen, and Mjøsa, and to a lesser extent in Mill Loch, a deep lake, and Marsworth Reservoir, a shallow lake, in terms of both the dissimilarity and direction of PrC scores. However, the model fits indicate that the recovery trend is only statistically significant at Lake Bled and Mjøsa. It is noteworthy that the three lakes that show the clearest reversal toward the reference flora are those with the lowest mean TP concentrations and are the deepest lakes in the dataset, supporting observations elsewhere that in deep lakes eutrophication is often reversed by the reduction in P inputs alone (Jeppesen et al.,
For the remaining lakes, the diatom response during the “recovery” period is more difficult to discern. At Esthwaite Water, P loading from a local sewage treatment works was reduced in 1986 but nutrients derived from catchment runoff, a fish farm established in 1981 and sediment P release have negated any potential reduction in lake nutrient concentrations (Bennion et al.,
The Loch Leven data point to partial recovery of the diatom flora, namely an increase in
At the other two shallow lakes (Bosherston Central Lake and Llangorse Lake) there are compositional changes in the diatoms following remediation efforts but the diatom floras do not appear to revert back toward those seen prior to enrichment but rather move toward a different assemblage. At Llangorse Lake, the effluent from the local sewage treatment works was diverted from the lake in 1981, with a second smaller input diverted in 1992. While the lake appears to be recovering following the remedial measures taken (Bennion and Appleby,
The data suggest that the percentage of planktonic taxa may be a useful metric for tracking enrichment in shallow lakes as a shift toward higher percentage of plankton was apparent with increased nutrient loading in four of the five shallow sites. An increase was less obviously seen in the deep lakes where percentage of planktonic taxa was generally high throughout the records. The shift from benthic to planktonic production associated with eutrophication in shallow waterbodies has been well documented (e.g., Vadeboncoeur et al.,
Increases in DI-TP were observed in seven lakes during the enrichment period while a decline in DI-TP was seen in 11 lakes following remediation. Hence this metric, which essentially reflects shifts in diatom composition, appears to have some potential for tracking recovery. However, several studies have highlighted the shortcomings of the transfer function technique in certain situations, and this is particularly well documented for shallow lakes where non-planktonic taxa dominate the diatom assemblages. Problems include the influence of factors such as light, substrate, and top-down factors in addition to water chemistry on the distribution of these taxa and their wide tolerance to nutrient concentrations, making them poor indicators of lake trophic status (e.g., Anderson et al.,
Our palaeoecological data reveal that whilst in some cases the diatom recovery trajectories do appear to track back along the degradation pathway, in others and the shallow lakes in particular, either little sign of recovery is evident or the assemblages follow a new trajectory. It might be argued that a return to the pre-disturbance diatom flora is less likely than the establishment of a different but ecologically equivalent assemblage i.e., species with a similar autecology. This was seen in several of the shallow lakes (e.g., Bosherston Central Lake and Llangorse Lake) where there were compositional changes toward taxa associated with lower nutrient concentrations following nutrient reduction but these were not the same taxa as those present in the pre-enrichment samples.
Our data accord with the findings of other recovery studies in that ecosystem recovery is shown not simply to be a reversal of the degradation process. Duarte et al. (
Most of the existing studies on recovery pathways are based on long-term datasets but for the majority of freshwater ecosystems monitoring activities are rather short-term and do not sufficiently account for long time periods required for restoration. The longer timeframe afforded by the sediment record thus lends itself well to studies of lake recovery and by extending back several decades or even centuries is valuable for defining the reference condition against which degree of recovery can be assessed. Nonetheless, palaeoecological data are not without their limitations and in this study it is perhaps the relatively low resolution of the data for the recovery period (i.e., at some sites only two or three samples correspond to the period since nutrient reduction) that is the greatest weakness. Studies are in progress whereby sites that were cored over 20 years ago are being repeat-cored and the sediments fine-sliced to track recovery over the last few decades at a higher resolution than was possible here. Error associated with the chronologies derived from radiometric dating, albeit small in recent sediments of typically only ±2–3 years, can cause difficulty in exactly pinpointing the timing of nutrient reduction in a core and may explain the slight offset between the management actions and diatom response observed in some of our records. Equally, discrepancy in the timings may arise due to changes in land use and management in the study catchments that are not documented and may have occurred prior to the more major and well documented management actions listed in Table
Several of the study lakes exhibit signs of ecological recovery in terms of reversal in their diatom assemblages but even in these cases the assemblages are still far from reference conditions as much as two to three decades since management measures were taken to reduce nutrient loads. Our findings are in accordance with other studies which report typical timescales of recovery for lakes of 10–20 years lakes (Jeppesen et al.,
In most of our study lakes, the main point source of nutrients, principally P, has been the key focus of management efforts. However, in recent decades diffuse nutrient sources have become relatively more significant than urban wastewater pollution and losses from agricultural land are now the biggest challenge (Schoumans et al.,
The role of climate change in exacerbating the symptoms of eutrophication and confounding recovery efforts cannot be ignored. Climate change is predicted to result in higher water temperatures, shorter periods of ice-cover and longer summer stratification (Jeppesen et al.,
An examination of the role of climate change in explaining the shifts in the diatom assemblages of the 12 lakes is beyond the scope of this study. However, detailed studies on two of the lakes, Esthwaite Water (Dong et al.,
In terms of the original questions posed we can conclude that the observed changes in the diatom records do reflect both the degradation and the recovery process. The latter has reached a different stage in each of the study lakes and is more clearly seen in several of the deep lakes where the diatom assemblages have started to revert back toward those seen prior to enrichment. In shallow lakes factors such as internal loading and top down control may influence the recovery process and in this study, whilst the assemblages of several shallow lakes were replaced by ones associated with lower productivity following remediation, they did not track back along the enrichment pathway. It can, therefore, be concluded that the deep stratified lakes tend to follow a more predictable recovery pathway than the shallow lakes. Nevertheless, the recovery process has a long way to go in all cases as the present assemblages remain very different from those seen in the pre-enrichment samples and there are indications that for some lakes reference communities may not return. Dissimilarity and principal curve scores are shown to be useful measures for quantifying the deviation from reference condition and provide a useful method with which to evaluate recovery success in the context of global change.
The study highlights the important role that paleolimnological approaches can play in establishing a benchmark against which managers can evaluate the degree to which their restoration efforts are successful. The decadal to centennial timescale adopted here provides the critical temporal context to inform the difficult decisions that emerge for the management of enriched waterbodies. We recognize that this study is based only on diatom responses and our inferences about biological recovery may therefore be biased, especially as diatoms are arguably one of the most sensitive groups in the system and have short response times relative to other assemblages such as macrophytes and fish. Assessments using multiple assemblages are required to evaluate wider ecosystem responses to environmental stressors, hence multi-proxy palaeoecological techniques have an important role to play in future studies of degradation and recovery pathways. The heterogeneous lake dataset used in this study has enabled the identification of broad-scale ecological patterns in recovering temperate lakes. The next step is to refine our understanding of these patterns for different lake types by analysing groups of lakes with more similar attributes.
HB led the writing of the paper with contributions from GS and BG. HB and BG counted the diatoms in most of the cores and discussed interpretations. GS carried out the numerical analyses. All authors reviewed and edited the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
We thank all those colleagues who contributed toward the original projects during which the cores were collected and analyzed. Particular thanks to Peter Appleby and Handong Yang for the radiometric dating, Carl Sayer, Gina Clarke and Samanta Skulmowska for diatom analysis, and to Cath D'Alton of the Cartography Unit, UCL for drawing the figures. We also acknowledge the helpful comments of the reviewers. This work was funded by the EU WISER project (contract no. 226273) and the EU REFRESH project (contract no. 244121). GS was supported by the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant Program (RGPIN 2014–04032).
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