草藻型稳态转换对湖泊微生物结构及其碳循环功能的影响

湖泊是地球表层系统中水、土、气等各个圈层相互作用的联结点,对区域物质如碳等元素循环具有重要影响.微生物是湖泊等水生态系统中的重要组成部分,是湖泊等生态系统中碳等元素物质循环的主要驱动者,是深入了解湖泊碳循环过程的关键.受人类活动等影响,湖泊生态系统,尤其是浅水湖泊生态系统往往表现出以高等水生植物(草型)为主要初级生产者的清水稳定态和以浮游藻类(藻型)为主要初级生产者的浊水稳定态,而随着湖泊营养负荷和湖泊环境条件的变化,这两个不同的稳定态之间可以发生转换或者剧变,这种剧变不仅影响湖泊生态系统中的微生物结构,而且对湖泊中有机碳的形成、循环过程及其微生物驱动机制产生重大影响.本文重点就湖泊生态系统中有机碳的转换与微生物关系以及草藻型稳定态的转换对微生物结构及其碳循环功能的影响等进行综述,进一步分析其中的关键科学问题,以期为深入了解湖泊生态系统中碳等元素循环的微生物驱动过程与机制提供帮助.     

Relative importance of periphyton and phytoplankton in turbid and clear vegetated shallow lakes from the Pampa Plain (Argentina): a comparative experimental study

We analyzed experimentally the relative contribution of phytoplankton and periphyton in two shallow lakes from the Pampa Plain (Argentina) that represent opposite scenarios according to the alternative states hypothesis for shallow lakes: a clear lake with submerged macrophytes, and a turbid lake with high phytoplankton biomass. To study the temporal changes of both microalgal communities under such contrasting conditions, we placed enclosures in the littoral zone of each lake, including natural phytoplankton and artificial substrata, half previously colonized by periphyton until a mature stage and half clean to analyze periphyton colonization. In the clear vegetated shallow lake, periphyton chlorophyll a concentrations were 3–6 times higher than those of the phytoplankton community. In contrast, phytoplankton chlorophyll a concentrations were 76–1,325 times higher than those of periphyton in the turbid lake. Here, under light limitation conditions, the colonization of the periphyton was significantly lower than in the clear lake. Our results indicate that in turbid shallow lakes, the light limitation caused by phytoplankton determines a low periphyton biomass dominated by heterotrophic components. In clear vegetated shallow lakes, where nitrogen limitation probably occurs, periphyton may develop higher biomass, most likely due to their higher efficiency in nutrient recycling.     

Planktonic ciliate community structure in shallow lakes of lowland Western Europe

Temperate shallow meso- to eutrophic lakes can exist in one of two alternative states with contrasting foodwebs, referred to as the clear-water and the turbid state. We describe the planktonic ciliate communities of such lakes based on a survey of 66 northwestern European lakes. Ciliates were enumerated and identified to species level according to the quantitative protargol staining technique. Ciliate biomass was on average twice as high in the turbid than in the clear-water lakes. The ciliate communities were dominated by oligotrichs and protostomatids, and no differences in functional composition or α-diversity could be detected between turbid and clear-water lakes, although β-diversity tended to be higher in the latter. At the species level, however, community structure strongly differed between turbid and clear-water lakes, and several indicator species could be identified for the different lake categories. Variation partitioning showed that nutrient status did not explain ciliate community structure independent of the alternative states, while lake area was identified as an additional structuring factor for the ciliate communities. These results stress the importance of the ecosystem structure in shaping ciliate communities in temperate shallow lakes and suggest that nutrient status has little direct effect on ciliate community structure in such lakes.     

Long Transients Near the Ghost of a Stable State in Eutrophic Shallow Lakes with Fluctuating Water Levels

Alternative stable states in shallow lakes have received much attention over the past decades, but less is known about transient dynamics of such lakes in the face of stochastic perturbations such as incidental extremes in water levels driven by climatic variability. Here, we report on the ecosystem dynamics of 70 lakes in the floodplains of the Lower Rhine in The Netherlands from 1999 to 2004. In any particular year, most lakes were either in a macrophyte-dominated clear state or in a contrasting state with turbid water and sparse submerged macrophyte cover. Macrophyte dominance was positively related to the occurrence of drawdown, and negatively to lake surface area and mean depth. We did not find a relation with nutrient levels. Remarkably, shifts between the two contrasting states were common, and episodes of low water levels appear to be an important external driver. A dry period before our study and the exceptionally dry summer of 2003 caused widespread drawdown of floodplain lakes, resulting in establishment of submerged macrophytes in the next year upon refill. In the 4 years without drawdown, many lakes returned to a macrophyte-poor turbid state. Although some lakes turned turbid again quickly, others took several years to shift into the turbid state. A model analysis suggests that such prolonged transient vegetated states may be explained by the fact that the system dynamics slow down in the vicinity of the “almost stable” macrophyte-dominated state. Such a “ghost” of an equilibrium causes the system to stick around that state relatively long before slipping into the only true stable state. Our results support the idea that transient dynamics rather than equilibrium may be the key to understanding the overall state of some ecosystems. A practical implication of our findings is that artificial stabilization of the water level in shallow lakes may have been an important factor aggravating the permanent loss of submerged macrophytes due to cultural eutrophication.     

Evolutionary emergence of alternative stable states in shallow lakes

Ecosystems under stress may respond abruptly and irreversibly through tipping points. Although mechanisms leading to alternative stable states are much studied, little is known about how such ecosystems could have emerged in the first place. We investigate whether evolution by natural selection along resource gradients leads to bistability, using shallow lakes as an example. There, tipping points occur between two alternative states dominated by either submersed or floating macrophytes depending on nutrient loading. We model the evolution of macrophyte depth in the lake, identify the conditions under which the ancestor population diversifies and investigate whether alternative stable states dominated by different macrophyte phenotypes occur. We find that eco-evolutionary dynamics may lead to alternative stable states, but under restrictive conditions. Such dynamics require sufficient asymmetries in the acquisition of both light and nutrient. Our analysis suggests that competitive asymmetries along opposing resource gradients may allow bistability to emerge by natural selection.     

Alternative equilibria in shallow lakes

The turbidity of lakes is generally considered to be a smooth function of their nutrient status. However, recent results suggest that over a range of nutrient concentrations, shallow lakes can have two alternative equilibria: a clear state dominated by aquatic vegetation, and a turbid state characterized by high algal biomass. This bi-stability has important implications for the possibilities of restoring eutrophied shallow lakes. Nutrient reduction alone may have little impact on water clarity, but an ecosystem disturbance like foodweb manipulation can bring the lake back to a stable clear state. We discuss the reasons why alternative equilibria are theoretically expected in shallow lakes, review evidence from the field and evaluate recent applications of this insight in lake management.     

Regime shifts in shallow lakes: the importance of seasonal fish migration

Shallow eutrophic lakes commonly exist in two alternative stable states: a clear-water state and a turbid water state. A number of mechanisms, including both abiotic and biotic processes, buffer the respective states against changes, whereas other mechanisms likely drive transitions between states. Our earlier research shows that a large proportion of zooplanktivorous fish populations in shallow lakes undertake seasonal migrations where they leave the lake during winter and migrate back to the lake in spring. Based on our past research, we propose a number of scenarios of how feedback processes between the individual and ecosystem levels may affect stability of alternative stable states in shallow lakes when mediated by fish migration. Migration effects on shallow lakes result from processes at different scales, from the individual to the ecosystem. Our earlier research has shown that ecosystem properties, including piscivore abundance and zooplankton productivity, affect the individual state of zooplanktivorous fish, such as growth rate or condition. Individual state, in turn, affects the relative proportion and timing of migrating zooplanktivorous fish. This change, in turn, may stabilize states or cause runaway processes that eventually lead to state shifts. Consequently, such knowledge of processes coupled to seasonal migration of planktivorous fish should increase our understanding of shallow lake dynamics.     

Predicting the effect of climate change on temperate shallow lakes with the ecosystem model PCLake

Global average surface temperatures are expected to rise by about 1.4–5.8°C from the present until the year 2100. This temperature increase will affect all ecosystems on earth. For shallow lakes—which can be either in a clear water or a turbid state—this climate change will expectedly negatively affect water transparency though the prediction is far from conclusive and experimental investigations elucidating the potential climatic effects on shallow lakes are still rare. The aim of this study was to further shape and sharpens hypotheses on the impact of climate change on shallow lakes by applying an existing and well-calibrated ecosystem model, PCLake. We focused on asymptotic model behaviour for a range of temperature and loading scenarios in a factorial design. We conclude that climate change will likely lead to decreased critical nutrient loadings. Combined with an expected increase in the external nutrient loading, this will increase the probability of a shift from a clear to a turbid state. As the model predicts a higher summer chlorophyll-a concentration, a stronger dominance of cyanobacteria during summer and a reduced zooplankton abundance due to climate change, the turbid state itself is likely to become even more severe.     

Migratory benthic fishes may induce regime shifts in a tropical floodplain pond

1. Alternative states are a widely recorded phenomenon in shallow lakes, which may shift between turbid‐ and clear‐water conditions. Here, we investigate whether such shifts in a tropical floodplain pond may be related to the effect of the flood pulse regime on the community structures of fish and macrophytes. 2. Using a long‐term data set, we demonstrate how benthic fish migration together with colonisation by submerged plants affected the transition from a turbid to a macrophyte‐dominated state in a floodplain pond without top‐down control. 3. In our study, the turbid state occurred mostly during low water phases and was largely characterised by high values for the biomass of benthic fish, chlorophyll‐a and total phosphorous. 4. During the period of rising water levels, the migration of benthic fish out of the pond occurs simultaneously with the establishment of submerged plants, while water turbidity decreases along with phytoplankton and nutrient concentrations, inducing a clear‐water phase. However, when submerged plants are absent and fish migration is low, a transient state is generated. 5. We suggest that, in contrast to temperate ponds and shallow lakes, where the main driving mechanisms establishing alternative states are related to cascading effects via the food chain, in tropical ponds and shallow lakes it is resuspension of sediments by benthic fish that plays the most significant role in establishing alternative states. However, the effect of the flood pulse regime plays an important role in the temporal dynamics of fish community structure by controlling benthic fish migration.     

Waterfowl,macrophytes, and the clear water state of shallow lakes

The importance of lake ecosystems for waterfowl remains a topic of debate. In order to assess how temporal variations in lake features, specifically shifts between alternative stable states, may interact with the waterfowl fauna, we performed a long-term (22 years) study of the shallow Lake Krankesjön, southern Sweden. Lower total numbers of waterfowl occurred during periods with low macrophyte cover and turbid water, than when submersed macrophytes flourished and the water was clear. Some specific functional groups of waterfowl, such as herbivores, invertebrate, and fish feeders, showed a positive relation to clear water and high macrophyte cover. Hence, our data suggest that some migratory waterfowl may select lakes based on water quality, thereby adjusting their large-scale migratory routes. On the other hand, omnivorous waterfowl exhibited their highest abundances during turbid conditions. Furthermore, waterfowl not primarily relying on food from the lake showed no response to fluctuations in turbidity or macrophyte cover, but followed regional trends in population dynamics. In our study lake, L. Krankesjön, we estimated that waterfowl remove less than 3% of the macrophyte biomass during a stable clear-water state with lush macrophyte beds. However, during transition periods between alternative stable states, when macrophyte biomass is lower and the plants already stressed, the consumption rate of waterfowl may have a stronger effect on lake ecosystem functioning.     

Seasonal dynamics of macrophytes and phytoplankton in shallow lakes: a eutrophication‐driven pathway from plants to plankton?

1. Seasonal relationships between macrophyte and phytoplankton populations may alter considerably as lakes undergo eutrophication. Understanding of these changes may be key to the interpretation of ecological processes operating over longer (decadal‐centennial) timescales. 2. We explore the seasonal dynamics of macrophytes (measured twice in June and August) and phytoplankton (measured monthly May–September) populations in 39 shallow lakes (29 in the U.K. and 10 in Denmark) covering broad gradients for nutrients and plant abundance. 3. Three site groups were identified based on macrophyte seasonality; 16 lakes where macrophyte abundance was perennially low and the water generally turbid (‘turbid lakes’); 7 where macrophyte abundance was high in June but low in August (‘crashing’ lakes); and 12 where macrophyte abundance was high in both June and August (‘stable’ lakes). The seasonal behaviour of the crashing and turbid lakes was extremely similar with a consistent increase in nutrient concentrations and chlorophyll‐a over May–September. By contrast in the stable lakes, seasonal changes were dampened with chlorophyll‐a consistently low (<10–15 μg L^?1) over the entire summer. The crashing lakes were dominated by one or a combination of Potamogeton pusillus, Potamogeton pectinatus and Zannichellia palustris, whereas Ceratophyllum demersum and Chara spp. were more abundant in the stable lakes. 4. A long‐term loss of macrophyte species diversity has occurred in many shallow lakes affected by eutrophication. One common pathway is from a species‐rich plant community with charophytes to a species‐poor community dominated by P. pusillus, P. pectinatus and Z. palustris. Such compositional changes may often be accompanied by a substantial reduction in the seasonal duration of plant dominance and a greater tendency for incursions by phytoplankton. We hypothesise a slow‐enacting (10–100 s years) feedback loop in nutrient‐enriched shallow lakes whereby increases in algal abundance are associated with losses of macrophyte species and hence different plant seasonal strategies. In turn such changes may favour increased phytoplankton production thus placing further pressure on remaining macrophytes. This study blurs the distinction between so‐called turbid phytoplankton‐dominated and clear plant‐dominated shallow lakes and suggests that plant loss from them may be a gradual process.     

The effect of turbidity state and microhabitat on macroinvertebrate assemblages: a pilot study of six shallow lakes

Shallow lakes can occur in two alternative stable states, a clear-water state and a turbid state. This is associated with separate assemblages of fish, zooplankton and plants. Little is known about whether macroinvertebrate assemblages differ across both stable states. This study investigated this in a connected set of three turbid and three clear-water shallow lakes. To overcome confounding effects of differences in spatial structure of macrophytes in turbid and clear-water lakes, we sampled three microhabitats that occurred in both alternative stable states: open water, sago pondweed (Potamogeton pectinatus) and reed (Phragmites australis). Univariate analyses indicated no differences in the number of organisms, taxon richness or diversity between turbid and clear-water lakes. Multivariate analysis, however, showed significant differences in the macroinvertebrate community structure of both stable states. Nine taxa explained a significant amount of the variation between both lake types, of which seven preferred the clear-water lakes. The number of organisms and the taxon richness were higher in reed than in the other microhabitats, but diversity and evenness did not differ among the microhabitats. Multivariate analyses could separate all three microhabitats. Eight taxa, mainly detritus feeders and collector–gatherers, explained most of the variation in the data and preferred the reed microhabitat. The effects of stable state (6.8% explained variance) and microhabitat (13.1% explained variance) on the macroinvertebrate assemblages were largely independent from each other (1.5% shared variance). Although macroinvertebrates are not implemented in the initial theory of stable states, our results show clearly different assemblages across both stable states.     

Abrupt regime shifts in space and time along rivers and connected lake systems

Regime shifts between clear and turbid water states are commonly found in shallow lakes. These shifts are attributed to a positive feedback between water clarity and submerged macrophytes (underwater plants). Altering the retention time of the water may influence these interactions and thus potentially reduce the probability of alternative stable states. Here we assessed the effect of water retention time on the occurrence of alternative states in water quality of flushed lakes, chains of lakes and rivers using a spatially explicit simple model. Our results indicate that increased flushing of lakes rapidly decreases the range of parameters with alternative stable states up to their total disappearance at a flushing rate of about 50% the algal growth rate. Similarly, in a chain of lakes or in rivers with low flowing velocity, our model predicts that alternative stable states can only occur for systems with a high retention time. Despite the lack of hysteresis at lower water retention times, we predict that abrupt changes between clear and turbid states are still possible both in time and in space. Over a wide range of parameters, the equilibrium state of the chain of lakes shows a steep gradient of vegetation cover. Further, the transient dynamics of the model often include rapid shifts in time. For example, a local regime shift that occurs upstream may propagate through the whole lake chain or river due to a domino effect. All results of the simple model could qualitatively be reproduced with a more mechanistic model. The abrupt rather than gradual response of submerged macrophytes to reduced turbidity levels still makes river systems rather resilient to management measure. The importance of the initial turbidity and the observed domino effect suggest that restoration measures should start upstream and that these measures should eventually trigger regime shifts downstream.     

Bimodal transparency as an indicator for alternative states in South American lakes

1. The alternative state theory claims that shallow lakes may have either clear water, and be dominated by submerged macrophytes, or turbid water and be dominated by phytoplankton. Most evidence for this theory comes from studies in temperate or boreal regions of Europe. Because of differences in the strength of trophic interactions, such as in the pressure of zooplankton grazing on phytoplankton, this influential theory might not apply elsewhere. 2. Here, we test the theory for South American lakes, combining field data and Landsat satellite data. We studied the frequency distribution of primary producers and water transparency, looking for potential bimodality separating clear and turbid lakes. A bimodal distribution might be observed if there are indeed alternative states, although would not itself be sufficient evidence for the theory. Possible shifts between alternative states were analysed by comparing satellite data from 1987 to 2005. 3. In our field data, there was a bimodal pattern in phytoplankton abundance and possibly in the abundance of submerged macrophytes, but not in water transparency. Analyses of the larger satellite data set revealed bimodality in lake transparency in 2005, but less so in 1987. In 1987, the lakes were generally clearer, and the transition to higher turbidity was more gradual than in 2005. The stronger bimodality in the more recent data, and the overall lower transparency, could have been caused by an increase in fertiliser use and subsequent eutrophication but also by differences in hydrology. Further, 1987 was much wetter than 2005, which could have caused dilution of suspended particles, leading to clearer water. 4. While a bimodal distribution in the abundance of primary producers and water clarity is not decisive evidence for or against the theory of alternative states, our data clearly fail to refute it.     

Can different vegetative states in shallow coastal bays of the Baltic Sea be linked to internal nutrient levels and external nutrient load?

Hydrobiologia - Two different vegetative states, i.e. one clear water state dominated by benthic macrophytes and one turbid state dominated by phytoplankton, are commonly found in shallow lakes. In...     

Zooplankton, phytoplankton and the microbial food web in two turbid and two clearwater shallow lakes in Belgium

Components of the pelagic food web in four eutrophic shallow lakes in two wetland reserves in Belgium (Blankaart and De Maten) were monitored during the course of 1998–1999. In each wetland reserve, a clearwater and a turbid lake were sampled. The two lakes in each wetland reserve had similar nutrient loadings and occurred in close proximity of each other. In accordance with the alternative stable states theory, food web structure differed strongly between the clearwater and turbid lakes. Phytoplankton biomass was higher in the turbid than the clearwater lakes. Whereas chlorophytes dominated the phytoplankton in the turbid lakes, cryptophytes were the most important phytoplankton group in the clearwater lakes. The biomass of microheterotrophs (bacteria, heterotrophic nanoflagellates and ciliates) was higher in the turbid than the clearwater lakes. Biomass and community composition of micro- and macrozooplankton was not clearly related to water clarity. The ratio of macrozooplankton to phytoplankton biomass – an indicator of zooplankton grazing pressure on phytoplankton – was higher in the clearwater when compared to the turbid lakes. The factors potentially regulating water clarity, phytoplankton, microheterotrophs and macrozooplankton are discussed. Implications for the management of these lakes are discussed.     

Copepods in turbid shallow soda lakes accumulate unexpected high levels of carotenoids

Carotenoids are protective pigments present in many aquatic organisms that reduce the photooxidative stress induced by short-wavelenght solar radiation, yet increase their susceptibility to predators. Arctodiaptomus spinosus, a calanoid copepod typically found in many fishless shallow soda lakes, shows large between-lake differences in pigmentation. Here, we attribute these differences to the environmental state of these ecosystems, namely, 'dark water' lakes with submersed vegetation and turbid 'white' lakes lacking macrophytes. Copepod carotenoid concentration in the turbid 'white' lakes was significantly (about 20-fold) higher than in the 'dark water' ones, although the latter systems were characterized by higher transparency. In addition, males had on a dry weight basis around three times higher carotenoid concentrations than females. Mycosporine-like amino acids (direct UV screening substances) were found in all cases, but in low concentration. The environmental conditions in these ecosystems were largely shaped by the presence/absence of submersed macrophytes Thus, in the turbid lakes, the strong wind-driven mixis allows for copepods to be brought to the surface and being exposed to solar radiation, whereas in 'dark water' ones, macrophytes reduce water turbulence and additionally provide shelter. Our results explain the counter-intuitive notion of strong red pigmentation in copepods from a turbid ecosystem and suggest that factors other than high UV transparency favor carotenoid accumulation in zooplankton.     

Thresholds and Stability of Alternative Regimes in Shallow Prairie–Parkland Lakes of Central North America

Numerous studies have demonstrated alternative regimes in shallow lake ecosystems around the world, with one state dominated by submerged macrophytes and the other by phytoplankton. However, the stability of each regime, and thresholds at which lakes shift to the alternative regime, are poorly known. We used a cross-sectional analysis of 72 shallow lakes located in prairie and parkland areas of Minnesota, USA, during 2005 and 2006 to assess the occurrence of alternative regimes and shifts between them. Cluster analysis revealed two distinct groups of lakes characterized not only by different macrophyte abundance and chlorophyll a levels but also by different total phosphorus–chlorophyll a relationships. Thirty-nine lakes were macrophyte- and 23 lakes phytoplankton-dominated in both years, whereas 10 sites shifted sharply between those regimes. We failed to detect a universal shifting threshold in terms of chlorophyll a or total phosphorus. However, 95% of the lakes with chlorophyll a concentrations less than 22 μg l⁻¹ were in a clear-water regime, whereas 95% of the lakes with chlorophyll a higher than 31 μg l⁻¹ were in a turbid regime. Total phosphorus less than 62 μg l⁻¹ was an accurate predictor of lakes in a stable clear-water regime, whereas a large change in biomass of planktivores and benthivores between years was the only variable weakly related to regime shifts. Our results support the theoretical prediction that regime thresholds vary among lakes. We recommend that lake managers focus on improving resilience of clear regimes in shallow lakes by reducing nutrient loading, rather than attempting to identify and manage complex triggers of regime shifts. Author contributions KDZ, MAH, BRH, and MLK all contributed to the design of the study, performed the research, analyzed data, and helped write the article.     

Macroalgal forests and sea urchin barrens: Structural complexity loss,fisheries exploitation and catastrophic regime shifts

In contrast to ecosystems that change smoothly and continuously in response to various stressors, some transitions between states with radically different properties can occur abruptly. An example are the sea urchin barrens and canopy algae (e.g. kelp beds) which represent alternative stable states. More precisely, the variation in grazing intensity in coastal rocky system may drive switches between one complex state into the barren state, the former dominated by erect algae and the latter by encrusting coralline algae and bare rock. Identifying the causes that drive a complex system towards a phase-shift becomes crucial for implementing strategies for the successful conservation and/or recovery of marine forests. Mathematical models that aim to assess effects of fisheries and sea urchins-seaweeds interaction may contribute to understand mechanisms driving transitions between alternative states. Fisheries exploitation has been considered the main driver of urchin population density transitions, with consequent effects on canopy algae distribution. The major novelty of the model here presented is the incorporation of habitat structural complexity, which explains the effect of algal biomass loss on coastal fish assemblages and the strong irreversibility of the system. We have found that as some critical parameters change macroalgae are more resilient and this may give rise to new scenarios, such as the emergence of new stationary states.     

A model study on the role of wetland zones in lake eutrophication and restoration

Shallow lakes respond in different ways to changes in nutrient loading (nitrogen, phosphorus). These lakes may be in two different states: turbid, dominated by phytoplankton, and clear, dominated by submerged macrophytes. Both states are self-stabilizing; a shift from turbid to clear occurs at much lower nutrient loading than a shift in the opposite direction. These critical loading levels vary among lakes and are dependent on morphological, biological, and lake management factors. This paper focuses on the role of wetland zones. Several processes are important: transport and settling of suspended solids, denitrification, nutrient uptake by marsh vegetation (increasing nutrient retention), and improvement of habitat conditions for predatory fish. A conceptual model of a lake with surrounding reed marsh was made, including these relations. The lake-part of this model consists of an existing lake model named PCLake. The relative area of lake and marsh can be varied. Model calculations revealed that nutrient concentrations are lowered by the presence of a marsh area, and that the critical loading level for a shift to clear water is increased. This happens only if the mixing rate of the lake and marsh water is adequate. In general, the relative marsh area should be quite large in order to have a substantial effect. Export of nutrients can be enhanced by harvesting of reed vegetation. Optimal predatory fish stock contributes to water quality improvement, but only if combined with favourable loading and physical conditions. Within limits, the presence of a wetland zone around lakes may thus increase the ability of lakes to cope with nutrients and enhance restoration. Validation of the conclusions in real lakes is recommended, a task hampered by the fact that, in the Netherlands, many wetland zones have disappeared in the past.