Long Transients Near the Ghost of a Stable State in Eutrophic Shallow Lakes with Fluctuating Water Levels
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- Van Geest, G.J., Coops, H., Scheffer, M. et al. Ecosystems (2007) 10: 37. doi:10.1007/s10021-006-9000-0
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.
Keywordssubmerged macrophyteswater level fluctuationsdrawdownalternative stable states
The theory of alternative stable states suggests that shallow lakes will usually be either clear and macrophyte dominated or turbid with few submerged plants (Scheffer and others 1993). It is usually assumed that shifts between these states occur only occasionally and relative few studies have focused on such shifts (Blindow and others 1993; Perrow and others 1994; McGowan and others 2005). Nonetheless, submerged macrophyte cover in shallow lakes may show large changes from 1 year to another. Changes in submerged macrophyte cover have often been explained as a result of variable nutrient loads (Hough and others 1989; Tracy and others 2003). Increased nutrient loads may result in a reduced cover of submerged macrophytes, due to a decreased transparency resulting from enhanced algal growth or higher concentrations of suspended sediments (Jeppesen and others 1997; Scheffer 1998). However, strong changes in macrophyte cover may also be caused by alterations in the water level (Wallsten and Forsgren 1989; Engel and Nichols 1994). An increase in water level reduces light availability, thereby limiting submerged macrophyte growth (Blindow and others 1993). By contrast, low water levels may stimulate submerged macrophyte expansion because of increased light availability to the lake bottom. Enhanced germination rates of macrophytes from seed banks upon resubmersion of temporarily exposed lake sediments may also play a role (Havens and others 2004). Furthermore, low water levels are likely to result in increased mortality of fish, which may stimulate macrophyte growth through a range of mechanisms (Scheffer 1998; Jones and Sayer 2003). Many well-studied shallow lakes have artificially stabilized water levels, and therefore lack the influence of alternating high and low water levels on submerged macrophytes. Hence, water level fluctuations have received far less attention compared to the effects of nutrients in explaining temporal changes of submerged macrophyte cover.
The present study explores the importance of water level fluctuations, lake morphometry and nutrient levels on inter-annual shifts in submerged macrophyte cover for a set of 70 floodplain lakes along the Lower Rhine during 1999–2004. We also use a simple model to explore how the observed large inter-annual fluctuations of macrophyte cover may relate to the alternative states theory (Scheffer 1998; Scheffer and others 1993).
The Lower Rhine in The Netherlands consists of three branches, called Waal, IJssel, and Neder-Rijn. In the floodplains of these three branches, 70 lakes were selected for the present study. At the location where the Rhine enters The Netherlands, the discharge varies annually between about 800 and 12,000 m3 s−1, resulting in water level fluctuations of up to 8 m in the main channel. Typically, the maximum annual river discharge occurs in winter and the minimum in autumn, although high and low discharges may occur at any moment throughout the year (Buijse and others 2002).
Materials and Methods
Number of Lakes, Minimum, Maximum, and 25, 50 And 75 Percentile Values of Environmental Variables
Lake age (year)
Surface area (ha)
Mean lake depth (m)
Inundation duration (day y−1)
Decrease in water level July–Oct 1999 (m)
Probability for lake drawdown
Presence of trees
Use of manure
Total N (mg l−1)
Total P (mg l−1)
The approximate lake age was derived from historical topographical maps (Table 1). Reliable estimates of lake age could be made up to 300 years; older lakes were regarded as 300 years old. The uncertainty of the lake age estimation was about 1 year for lakes that were newly dug after 1980, 3–7 years for lakes originating from the period 1910–1980, and 10–25 years for lakes prior to 1910.
During the fieldwork the prevailing land use in the adjacent floodplain (presence of trees, cattle access to the shoreline, use of manure on adjacent land) was recorded. For these variables the following categories were used: presence of trees: (0, shoreline length for <25% covered by trees; 0.5, shoreline covered for 25–75% by trees; 1, shoreline covered >75% by trees); cattle grazing: (0, cattle access to 0–25% of perimeter; 0.5, 25–75% of perimeter; 1, >75% of perimeter); use of manure: (0, no manuring of adjacent land; 0.5, >0–50% of adjacent land; 1, 51–100% of adjacent land). For 67 of the 70 floodplain lakes sampled in 1999, samples for total N and total P in the water phase were taken according to Roozen and others (2003).
In July 1999, water depths were measured at several locations in each lake. In addition, the seasonal water level change (WLJ–O) was assessed using a marked rod in each lake that was measured in July and October 1999. The ratio between WLJ–O and maximum lake depth (DmaxJ) in 1999 was calculated as an indicator of the likelihood of lake drawdown (a value of one implies exposure of the entire lake bottom in 1999). To check if this ratio was a reliable indicator for lake bottom exposure in other years, the proportion of the drawdown area of each lake was estimated visually during October 2003, which coincided with the end of a prolonged period of extremely low water levels in the main channel. Overall, the indicator for lake drawdown was highly correlated to percentage lake drawdown in 2003 (Spearman R = 0.65, P < 0.000001), indicating that the ratio WLJ–O/DmaxJ can be used as a relative indicator for the likelihood of lake drawdown in other years.
Eight Independent Environmental Variables used in Multiple Linear Regression Analysis to Predict the Number of Years that the Lakes were Dominated by Submerged Macrophytes during 1999–2002 and 2004
For accuracy: see Materials and methods
Lake surface area1
Surface area of lake at start of growing season
Mean lake depth1
Calculated from 5 to 31 water depth measurements in July 1999 in each lake
Long year average 1990–1995
Probability for lake drawdown
Index for probability of lake drawdown (for calculation: see Materials and methods)
Presence of trees along shoreline
Access of cattle to shoreline
Use of manure on adjacent land
Results of Stepwise (Forward) Multiple Linear Regression Analysis in a Set of 70 Lakes between Environmental Lake Characteristics and Number of Years that the Lakes were Dominated by Submerged Macrophytes during 1999–2002 and 2004
Std. error of beta
Std. error of B
Lake surface area1
Mean lake depth1
Presence of trees
Probability for lake drawdown
Percentage of Inter-Annual Shifts from Macrophyte-Rich to Macrophyte-Poor Lakes (Backward Switches) and Vice Versa (Forward Switches) during 1999–2004
Pair of years
For further analysis, the lakes were divided into three categories: permanently macrophyte-rich, permanently macrophyte-poor, and shifting lakes. The latter category represented lakes that changed from at least 20% submerged macrophyte cover to less than 20% for at least one of the years during the study period (1999–2004). Between these three categories, no significant differences for total nitrogen [(F2,61) = 0.4101, P = 0.67] and total phosphorus levels [(F2,61) = 0.7857, P = 0.46] were detected.
At first sight, the frequent shifting of the lakes in this study may seem in contradiction with the alternative state theory (Scheffer and others 1993), which predicts one or two stable states depending on the nutrient state. Switching between these states is expected to be rare. However, the conditions in the floodplain lakes are highly dynamic, whereas the alternative state theory focuses on ecosystems in equilibrium under constant or slowly changing conditions. To see how the theory might be modified for highly dynamic situations, we have explored the transient states of a macrophyte-turbidity model, which described the alternative states in shallow lakes.
As most of the lakes in the floodplain are nutrient-rich (Table 1), we assume that many lakes are in the range with only a stable turbid state (right of the grey area in Figure 6A, for example, E0 = 8). In this situation there is only one equilibrium. However, Figure 6B shows the transient dynamics can be slow and some lakes may remain in the macrophyte dominated state much longer than others. A disturbance such as drawdown puts them into a (unstable) clear state.
The floodplain lakes in our study showed remarkably strong and frequent inter-annual shifts in macrophyte cover. This contrasts to typical case studies in the literature suggesting that most shallow lakes are either in a macrophyte-dominated clear water state or in an unvegetated turbid state, with shifts between these states being relatively uncommon (Scheffer 1998). Our results suggest that the high percentage of macrophyte-dominated lakes in 1999 and 2004 are likely the result of drawdown of many of the lakes in 1998 and 2003. In the intermediate period when drawdowns rarely occurred, there was a net tendency for lakes to lose their submerged macrophytes (Figure 2). Stimulatory effects of drawdown on submerged macrophytes have been reported in a few other studies (Gibbs 1973; Havens and others 2004), but received relatively little attention so far.
A puzzling aspect in our data is the apparent difference in return time to the turbid state with little or no macrophytes. Although some lakes lost their submerged vegetation already after one year, others remained vegetated several years or even throughout the study period. At first sight, an obvious explanation for this pattern would be that fish populations are wiped out, or at least severely reduced during draw-down episodes, allowing the lakes to shift to a clear and macrophyte-dominated state, whereas subsequent recolonization by fish and expansion of fish populations may take a long time, depending on colonization opportunities. However, although fish elimination will certainly play an important role, all the lakes were flooded annually during the research period giving ample opportunity for the abundant populations of bream (Abramis brama) in the main channel to recolonize the lakes (Molls 1999; Grift and others 2001). Still, as discussed below, fish may well colonize some lakes more readily than others as they actively chose habitats.
Our model analysis suggests a less intuitive, but interesting alternative explanation for the observed difference between lakes in return time to the turbid state. The simulations show that if the system is pushed to a macrophyte-dominated state by drawdown, the return to the turbid state may take a long time, even if the turbid state is the only equilibrium. This delayed return to the macrophyte-poor state is due to the “ghost” of the macrophyte-rich equilibrium, which is the result of positive feedbacks that are too weak to stabilize the clear vegetated state in the long term but nevertheless may significantly delay the return to the turbid state with few submerged macrophytes.
The ghost theory implies that lakes remain longer in a transient vegetated state if growth conditions for macrophytes are more favorable. Therefore, the expectation for a large set of different lakes would be that upon drawdown some lakes will return quickly to the original (turbid) state, whereas others may linger for a long time around a (nearly stable) vegetated condition. This is well in line with the pattern of loss of macrophyte dominance in our lakes. It is especially interesting in this respect that small shifting lakes tended to remain longer in a transient vegetated state than larger ones (Figure 5). Our data and other studies suggest that such smaller lakes may well be systematically closer to having a stable vegetated state (Van Geest and others 2003; Jeppesen and others 1990; Søndergaard and others 2005; Scheffer and others 2006). Therefore, smaller lakes should be more likely to display ghost-effects and return to the turbid state only slowly after being pushed into a transient vegetated state by a disturbance. This fits well with the observed dynamics in our floodplain lakes.
Note that, even though fish dynamics are not explicitly included in our model, the role of fish in the dynamics of our lakes may well fit the ghost hypothesis in a broader sense. This is because the assumed negative effect of macrophytes on turbidity may hold also for their effect on fish (a notorious promotor of turbidity, besides its other negative direct and indirect impacts on macrophytes). Even if fish can freely enter the lakes during annual river floods, species that are characteristic of turbid water such as bream are known to avoid vegetated habitats (Perrow and Jowitt 1996; Scheffer 1998), and may well colonize macrophyte-dominated lakes less than turbid, macrophyte-poor lakes. Data from a set of interconnected shallow lakes in Belgium (“De Maten”) confirm this possibility. In these lakes, temporary drawdown resulted in a transient increase in submerged macrophyte cover, while fish biomass strongly decreased and did not recover within two subsequent years, even though fish were able to migrate into these lakes (Van de Meutter and others 2006). Clearly, although our data do not allow analysis of patterns of remigration of fish into our lakes, it seems plausible that this is not a random process. The results in “De Maten” and numerous biomanipulation experiments (Meijer and others 1995; Meijer 2000) illustrate that fish are not merely ‘drivers’ of lake ecosystems but also respond to the state. Delayed recolonization by fish species that are typical of turbid lakes may thus be one of the mechanisms by which near-stable vegetation dominance can end up being a long transient state in some lakes.
In summary, our results suggest that a substantial portion of the lakes we studied are in a transient vegetated state much of the time. Low water levels appear to induce a shift of many turbid lakes into this transient state. The subsequent duration of the transient may be affected by stabilizing feed-back mechanisms of the macrophyte-rich state, even if this state is not stable. Our results are illustrative of the dominant role that transients can play in ecosystem dynamics (Hastings 2004). A practical implication of our findings is that hydrological regulation preventing drawdown may have been an important factor aggravating the permanent loss of submerged macrophytes due to cultural eutrophication.
This project was financed by RIZA (Institute for Inland Water Management and Waste Water Treatment). We are grateful to John van Schie, Matthijs Rutten and Kirsten Vendrig for their assistance in the field.