Martin Søndergaard

Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth

Based on data from 233 Danish lakes, enclosure experiments, full-scaleexperiments and published empirical models we present evidence that top-downcontrol is more important in shallow lakes than in deep lakes, excepting lakeswith a high abundance of submerged macrophytes. The evidence in support is: (1)That at a given epilimnion total phosphorus concentration (TP) the biomass offish per m2 is independent of depth, which means that biomassper m3is markedly higher in shallow lakes. (2) That the biomass of benthic invertebratesis higher in shallow lakes, which means that the benthi-planktivorous fish areless dependent on zooplankton prey than in deep lakes. By their ability to shiftto zooplankton predation their density can remain high even in periods whenzooplankton is scarce and they can thereby maintain a potentially high predationpressure on zooplankton. (3) That the possibilities of cladocerans to escapepredation by vertical migration are less. (4) That the zooplankton:phytoplanktonmass ratio per m2 is lower and presumably then also thegrazing pressure onphytoplankton. (5) That nutrient constraints appear to be weaker, as evidenced bythe fact that at a given annual mean TP, summer TP is considerably higher inshallow lakes, especially in eutrophic lakes lacking submerged macrophytes. (6)That negative feedback on cladocerans by cyanobacteria is lower as cyanobacterialdominance is less frequent in shallow lakes and more easily broken (at least inNorthern temperate lakes), and (7) That top-down control by benthi-planktivorousfish is markedly reduced in lakes rich in submerged macrophytes because theplants serve as a refuge for pelagic cladocerans and encouragepredatory fish at the expense of prey fish. We conclude that manipulation of fishand submerged macrophytes may have substantial impact on lake ecosystems, inparticular in shallow eutrophic lakes. On the contrary, if the conditions formore permanent changes in plant abundance or fish community structure are lackingthe feed-back mechanisms that endeavour a return to the original turbid state willbe particularly strong in shallow lakes.

Biomanipulation as an Application of Food-Chain Theory: Constraints, Synthesis, and Recommendations for Temperate Lakes

ABSTRACT The aim of this review is to identify problems, find general patterns, and extract recommendations for successful biomanipulation. An important conclusion is that the pelagic food chain from fish to algae may not be the only process affected by a biomanipulation. Instead, this process should be viewed as the “trigger” for secondary processes, such as establishment of submerged macrophytes, reduced internal loading of nutrients, and reduced resuspension of particles from the sediment. However, fish reduction also leads to a high recruitment of young-of-the-year (YOY) fish, which feed extensively on zooplankton. This expansion of YOY the first years after fish reduction is probably a major reason for less successful biomanipulations. Recent, large-scale biomanipulations have made it possible to update earlier recommendations regarding when, where, and how biomanipulation should be performed. More applicable recommendations include (1) the reduction in the biomass of planktivorous fish should be 75% or more; (2) the fish reduction should be performed efficiently and rapidly (within 1–3 years); (3) efforts should be made to reduce the number of benthic feeding fish; (4) the recruitment of YOY fish should be reduced; (5) the conditions for establishment of submerged macrophytes should be improved; and (6) the external input of nutrients (phosphorus and nitrogen) should be reduced as much as possible before the biomanipulation. Recent biomanipulations have shown that, correctly performed, the method also achieves results in large, relatively deep and eutrophic lakes, at least in a 5-year perspective. Although repeated measures may be necessary, the general conclusion is that biomanipulation is not only possible, but also a relatively inexpensive and attractive method for management of eutrophic lakes, and in particular as a follow-up measure to reduced nutrient load.

Phosphorus release from resuspended sediment in the shallow and wind-exposed lake Arresø, Denmark

Wind-induced sediment resuspension occurs frequently in the shallow and eutrophic Lake Arresø, Denmark. The impact of resuspension on internal phosphorus loading was investigated by laboratory experiments studying P-release from the undisturbed sediment surface and by experiments simulating resuspension events.Phosphorus release from undisturbed sediment sampled in May and August was 12 mg and 4 mg m−2 d−1, respectively. During experimental simulation of resuspension, soluble reactive phosphate (SRP) increased by 20–80 µg l−1, which indicates that a typical resuspension event in the lake would be accompanied by the release of 150 mg SRP m−2. The internal P loading induced by resuspension is estimated to be 60–70 mg m−2 d−1, or 20–30 times greater than the release from undisturbed sediment.SRP release during simulation of resuspension was mainly dependent on the equilibrium conditions in the water column and was basically independent of the increase in suspended solids and the duration of resuspension. A second simulation of resuspension conducted 26 hours later, did not result in any further release of SRP from sediment sampled in May. In contrast, there was an additional SRP release from sediment sampled in August, indicating that an exchangable P pool, capable of altering equilibrium conditions, is built up between resuspension events.It is concluded that resuspension, by increasing the P flux between sediment and water, plays a major role in the maintenance of the high nutrient level in Lake Arresø. A relatively high release rate is maintained during resuspension because of the low Fe:P ratio and the high concentration of NH4Cl-extractable P in the sediment.

Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations.

Climate change may have profound effects on phosphorus (P) transport in streams and on lake eutrophication. Phosphorus loading from land to streams is expected to increase in northern temperate coastal regions due to higher winter rainfall and to a decline in warm temperate and arid climates. Model results suggest a 3.3 to 16.5% increase within the next 100 yr in the P loading of Danish streams depending on soil type and region. In lakes, higher eutrophication can be expected, reinforced by temperature-mediated higher P release from the sediment. Furthermore, a shift in fish community structure toward small and abundant plankti-benthivorous fish enhances predator control of zooplankton, resulting in higher phytoplankton biomass. Data from Danish lakes indicate increased chlorophyll a and phytoplankton biomass, higher dominance of dinophytes and cyanobacteria (most notably of nitrogen fixing forms), but lower abundance of diatoms and chrysophytes, reduced size of copepods and cladocerans, and a tendency to reduced zooplankton biomass and zooplankton:phytoplankton biomass ratio when lakes warm. Higher P concentrations are also seen in warm arid lakes despite reduced external loading due to increased evapotranspiration and reduced inflow. Therefore, the critical loading for good ecological state in lakes has to be lowered in a future warmer climate. This calls for adaptation measures, which in the northern temperate zone should include improved P cycling in agriculture, reduced loading from point sources, and (re)-establishment of wetlands and riparian buffer zones. In the arid Southern Europe, restrictions on human use of water are also needed, not least on irrigation.

Fish manipulation as a lake restoration tool in shallow, eutrophic, temperate lakes 2: threshold levels, long-term stability and conclusions

In order to evaluate short-term and long-term effects of fish manipulation in shallow, eutrophic lakes, empirical studies on relationships between lake water concentration of total phosphorus (P) and the occurrence of phytoplankton, submerged macrophytes and fish in Danish lakes are combined with results from three whole-lake fish manipulation experiments. After removal of less than 80 per cent of the planktivorous fish stock a short-term trophic cascade was obtained in the nutrient regimes, where large cyanobacteria were not strongly dominant and persistent. In shallow Danish lakes cyanobacteria were the most often dominating phytoplankton class in the P-range between 200 and 1000 pg P 1−1. Long-term effects are suggested to be closely related to the ability of the lake to establish a permanent and wide distribution of submerged macrophytes and to create self-perpetuating increases in the ratio of piscivorous to planktivorous fish. The maximum depth at which submerged macrophytes occurred, decreased exponentially with increasing P concentration. Submerged macrophytes were absent in lakes > 10 ha and with P levels above 250−300 μg P 1−1, but still abundant in some lakes 10 cm numerically contributed more than 80 per cent of the total planktivorous and piscivorous fish (> 10 cm) in the pelagical of lakes with concentrations above 100 μg P 1−1. Below this threshold level the proportion of planktivores decreased markedly to ca. 50 per cent at 22 μg P 1−1. The extent of the shift in depth colonization of submerged macrophytes and fish stock composition in the three whole-lake fish manipulations follows closely the predictions from the relationships derived from the empirical study. We conclude that a long-term effect of a reduction in the density of planktivorous fish can be expected only when the external phosphorus loading is reduced to below 0.5−2.0 g m −2 y −1. This loading is equivalent to an in-lake summer concentration below 80−150 μg P 1−1. Furthermore, fish manipulation as a restoration tool seems most efficient in shallow lakes.

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 Arreso, 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 Paranoa, 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.

The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: A study of 466 lakes from the temperate zone to the Arctic

Using empirical data from 466 temperate to arctic lakes covering a total phosphorus (TP) gradient of 2–1036 gL –1 , we describe how the relative contributions of resource supply, and predator control change along a nutrient gradient. We argue that (a) predator control on large-bodied zooplankton is unimodally related to TP and is highest in the most nutrient-rich and nutrient-poor lakes and generally higher in shallow than deep lakes, (b) the cascading effect of changes in predator control on phytoplankton decreases with increasing TP, and (c) these general patterns occur with significant variations—that is, the predation pressure can be low or high at all nutrient levels. A quantile regression revealed that the median share of the predatorsensitive Daphnia to the total cladoceran biomass was significantly related unimodally to TP, while the 10% and 90% percentiles approached 0 and 100%, respectively, at all TP levels. Moreover, deep lakes (more than 6 m) had a higher percentage of

Retention and internal loading of phosphorus in shallow, eutrophic lakes.

This paper gives a general overview of the nature and important mechanisms behind internal loading of phosphorus (P), which is a phenomenon appearing frequently in shallow, eutrophic lakes upon a reduction of the external loading. Lake water quality is therefore not improved as expected. In particular summer concentrations rise and P retention may be negative during most of the summer. The P release originates from a pool accumulated in the sediment when the external loading was high. In most lake sediments, P bound to redox-sensitive iron compounds or P fixed in more or less labile organic forms constitute major fractions forms that are potentially mobile and eventually may be released to the lake water. The duration of the recovery period following P loading reduction depends on the loading history, but it may last for decades in lakes with a high sediment P accumulation. During the phase of recovery, both the duration and net P release rates from the sediment seem to decline progressively. Internal P loading is highly influenced by the biological structure as illustrated by lakes shifting from the turbid to the clearwater state as a result of, for example, biomanipulation. In these lakes P concentrations may be reduced to 50% of the pre-biomanipulation level and the period with negative retention during summer can thus be reduced considerably. The duration of internal loading can be reduced significantly by different restoration methods such as dredging to remove accumulated P or addition of iron or alum to elevate the sorption capacity of sediments. However, an important prerequisite for achieving long-term benefits to water quality is a sufficient reduction of the external P loading.

Impacts of climate warming on lake fish community structure and potential effects on ecosystem function

Fish play a key role in the trophic dynamics of lakes, not least in shallow systems. With climate warming, complex changes in fish community structure may be expected owing to the direct and indirect effects of temperature, and indirect effects of eutrophication, water-level changes and salinisation on fish metabolism, biotic interactions and geographical distribution. We review published and new data supporting the hypotheses that, with a warming climate, there will be changes in: fish community structure (e.g. higher or lower richness depending on local conditions); life history traits (e.g. smaller body size, shorter life span, earlier and less synchronised reproduction); feeding mode (i.e. increased omnivory and herbivory); behaviour (i.e. stronger association with littoral areas and a greater proportion of benthivores); and winter survival. All these changes imply higher predation on zooplankton and macroinvertebrates with increasing temperatures, suggesting that the changes in the fish communities partly resemble, and may intensify, the effects triggered by eutrophication. Modulating factors identified in cold and temperate systems, such as the presence of submerged plants and winter ice cover, seem to be weaker or non-existent in warm(ing) lakes. Consequently, in the future lower nutrient thresholds may be needed to obtain clear-water conditions and good ecological status in the future in currently cold or temperate lakes. Although examples are still scarce and more research is needed, we foresee biomanipulation to be a less successful restoration tool in warm(ing) lakes without a strong reduction of the nutrient load.

Shallow lake restoration by nutrient loading reduction—some recent findings and challenges ahead

Shallow lakes respond to nutrient loading reductions. Major findings in a recent multi-lake comparison of data from lakes with long time series revealed: that a new state of equilibrium was typically reached for phosphorus (P) after 10–15 years and for nitrogen (N) after <5–10 years; that the in-lake Total N:Total P and inorganic N:P ratios increased; that the phytoplankton and fish biomass often decreased; that the percentage of piscivores often increased as did the zooplankton:phytoplankton biomass ratio, the contribution of Daphnia to Zooplankton biomass, and cladoceran size. This indicates that enhanced resource and predator control often interact during recovery from eutrophication. So far, focus has been directed at reducing external loading of P. However, one experimental study and cross-system analyses of data from many lakes in north temperate lakes indicate that nitrogen may play a more significant role for abundance and species richness of submerged plants than usually anticipated when total phos-phorus is moderate high. According to the alter-native states hypothesis we should expect ecological resistance to nutrient loading reduction and P hysteresis. We present results suggesting that the two alternative states are less stable than originally anticipated. How global warming af-fects the water clarity of shallow lakes is debat-able. We suggest that water clarity often will decrease due to either enhanced growth of phytoplankton or, if submerged macrophytes are stimulated, by reduced capacity of these plants to maintain clear-water conditions. The latter is supported by a cross-system comparison of lakes in Florida and Denmark. The proportion of small fish might increase and we might see higher aggregation of fish within the vegetation (leading to loss of Zooplankton refuges), more annual fish cohorts, more omnivorous feeding by fish and less specialist piscivory. Moreover, lakes may have prolonged growth seasons with a higher risk of long-lasting algal blooms and at places dense floating plant communities. The effects of global warming need to be taken into consideration by lake managers when setting future targets for critical loading, as these may well have to be adjusted in the future. Finally, we highlight some of the future challenges we see in lake restoration research.