Lake responses to reduced nutrient loading – an analysis of contemporary long-term data from 35 case studies

1. This synthesis examines 35 long‐term (5–35 years, mean: 16 years) lake re‐oligotrophication studies. It covers lakes ranging from shallow (mean depth <5 m and/or polymictic) to deep (mean depth up to 177 m), oligotrophic to hypertrophic (summer mean total phosphorus concentration from 7.5 to 3500 μg L^?1 before loading reduction), subtropical to temperate (latitude: 28–65°), and lowland to upland (altitude: 0–481 m). Shallow north‐temperate lakes were most abundant. 2. Reduction of external total phosphorus (TP) loading resulted in lower in‐lake TP concentration, lower chlorophyll a (chl a) concentration and higher Secchi depth in most lakes. Internal loading delayed the recovery, but in most lakes a new equilibrium for TP was reached after 10–15 years, which was only marginally influenced by the hydraulic retention time of the lakes. With decreasing TP concentration, the concentration of soluble reactive phosphorus (SRP) also declined substantially. 3. Decreases (if any) in total nitrogen (TN) loading were lower than for TP in most lakes. As a result, the TN : TP ratio in lake water increased in 80% of the lakes. In lakes where the TN loading was reduced, the annual mean in‐lake TN concentration responded rapidly. Concentrations largely followed predictions derived from an empirical model developed earlier for Danish lakes, which includes external TN loading, hydraulic retention time and mean depth as explanatory variables. 4. Phytoplankton clearly responded to reduced nutrient loading, mainly reflecting declining TP concentrations. Declines in phytoplankton biomass were accompanied by shifts in community structure. In deep lakes, chrysophytes and dinophytes assumed greater importance at the expense of cyanobacteria. Diatoms, cryptophytes and chrysophytes became more dominant in shallow lakes, while no significant change was seen for cyanobacteria. 5. The observed declines in phytoplankton biomass and chl a may have been further augmented by enhanced zooplankton grazing, as indicated by increases in the zooplankton : phytoplankton biomass ratio and declines in the chl a : TP ratio at a summer mean TP concentration of <100–150 μg L^?1. This effect was strongest in shallow lakes. This implies potentially higher rates of zooplankton grazing and may be ascribed to the observed large changes in fish community structure and biomass with decreasing TP contribution. In 82% of the lakes for which data on fish are available, fish biomass declined with TP. The percentage of piscivores increased in 80% of those lakes and often a shift occurred towards dominance by fish species characteristic of less eutrophic waters. 6. Data on macrophytes were available only for a small subsample of lakes. In several of those lakes, abundance, coverage, plant volume inhabited or depth distribution of submerged macrophytes increased during oligotrophication, but in others no changes were observed despite greater water clarity. 7. Recovery of lakes after nutrient loading reduction may be confounded by concomitant environmental changes such as global warming. However, effects of global change are likely to run counter to reductions in nutrient loading rather than reinforcing re‐oligotrophication.     

Response of zooplankton to nutrient enrichment and fish in shallow lakes: a pan-European mesocosm experiment

1. Responses of zooplankton to nutrient enrichment and fish predation were studied in 1998 and 1999 by carrying out parallel mesocosm experiments in six lakes across Europe. 2. Zooplankton community structure, biomass and responses to nutrient and fish manipulation showed geographical and year‐to‐year differences. Fish had a greater influence than nutrients in regulating zooplankton biomass and especially the relative abundances of different functional groups of zooplankton. When fish reduced the biomass of large crustaceans, there was a complementary increase in the biomasses of smaller crustacean species and rotifers. 3. High abundance of submerged macrophytes provided refuge for zooplankton against fish predation but this refuge effect differed notably in magnitude among sites. 4. Large crustacean grazers (Daphnia, Diaphanosoma, Sida and Simocephalus) were crucial in controlling algal biomass, while smaller crustacean grazers and rotifers were of minor importance. Large grazers were able to control phytoplankton biomass even under hypereutrophic conditions (up to 1600 μg TP L^?1) when grazer biomass was high (>80–90 μg dry mass L^?1) or accounted for >30% of the grazer community. 5. The littoral zooplankton community was less resistant to change following nutrient enrichment in southern Spain, at high temperatures (close to 30 °C), than at lower temperatures (17–23 °C) characterising the other sites. This lower resistance was because of a greater importance of nutrients than zooplankton in controlling algal biomass. 6. Apart from the reduced role of large crustacean grazers at the lowest latitude, no consistent geographical patterns were observed in the responses of zooplankton communities to nutrient and fish manipulation.     

Impact of fish predation on cladoceran body weight distribution and zooplankton grazing in lakes during winter

1. It is well accepted that fish, if abundant, can have a major impact on the zooplankton community structure during summer, which, particularly in eutrophic lakes, may cascade to phytoplankton and ultimately influence water clarity. Fish predation affects mean size of cladocerans and the zooplankton grazing pressure on phytoplankton. Little is, however, known about the role of fish during winter. 2. We analysed data from 34 lakes studied for 8–9 years divided into three seasons: summer, autumn/spring and winter, and four lake classes: all lakes, shallow lakes without submerged plants, shallow lakes with submerged plants and deep lakes. We recorded how body weight of Daphnia and then cladocerans varied among the three seasons. For all lake types there was a significant positive correlation in the mean body weight of Daphnia and all cladocerans between the different seasons, and only in lakes with macrophytes did the slope differ significantly from one (winter versus summer for Daphnia). 3. These results suggest that the fish predation pressure during autumn/spring and winter is as high as during summer, and maybe even higher during winter in macrophyte‐rich lakes. It could be argued that the winter zooplankton community structure resembles that of the summer community because of low specimen turnover during winter mediated by low fecundity, which, in turn, reflects food shortage, low temperatures and low winter hatching from resting eggs. However, we found frequent major changes in mean body weight of Daphnia and cladocerans in three fish‐biomanipulated lakes during the winter season. 4. The seasonal pattern of zooplankton : phytoplankton biomass ratio showed no correlation between summer and winter for shallow lakes with abundant vegetation or for deep lakes. For the shallow lakes, the ratio was substantially higher during summer than in winter and autumn/spring, suggesting a higher zooplankton grazing potential during summer, while the ratio was often higher in winter in deep lakes. Direct and indirect effects of macrophytes, and internal P loading and mixing, all varying over the season, might weaken the fish signal on this ratio. 5. Overall, our data indicate that release of fish predation may have strong cascading effects on zooplankton grazing on phytoplankton and water clarity in temperate, coastal situated eutrophic lakes, not only during summer but also during winter.     

Does high nitrogen loading prevent clear‐water conditions in shallow lakes at moderately high phosphorus concentrations?

1. The effect of total nitrogen (TN) and phosphorus (TP) loading on trophic structure and water clarity was studied during summer in 24 field enclosures fixed in, and kept open to, the sediment in a shallow lake. The experiment involved a control treatment and five treatments to which nutrients were added: (i) high phosphorus, (ii) moderate nitrogen, (iii) high nitrogen, (iv) high phosphorus and moderate nitrogen and (v) high phosphorus and high nitrogen. To reduce zooplankton grazers, 1⁺ fish (Perca fluviatilis L.) were stocked in all enclosures at a density of 3.7 individuals m^?2. 2. With the addition of phosphorus, chlorophyll a and the total biovolume of phytoplankton rose significantly at moderate and high nitrogen. Cyanobacteria or chlorophytes dominated in all enclosures to which we added phosphorus as well as in the high nitrogen treatment, while cryptophytes dominated in the moderate nitrogen enclosures and the controls. 3. At the end of the experiment, the biomass of the submerged macrophytes Elodea canadensis and Potamogeton sp. was significantly lower in the dual treatments (TN, TP) than in single nutrient treatments and controls and the water clarity declined. The shift to a turbid state with low plant coverage occurred at TN >2 mg N L^?1 and TP >0.13–0.2 mg P L^?1. These results concur with a survey of Danish shallow lakes, showing that high macrophyte coverage occurred only when summer mean TN was below 2 mg N L^?1, irrespective of the concentration of TP, which ranged between 0.03 and 1.2 mg P L^?1. 4. Zooplankton biomass and the zooplankton : phytoplankton biomass ratio, and probably also the grazing pressure on phytoplankton, remained overall low in all treatments, reflecting the high fish abundance chosen for the experiment. We saw no response to nutrition addition in total zooplankton biomass, indicating that the loss of plants and a shift to the turbid state did not result from changes in zooplankton grazing. Shading by phytoplankton and periphyton was probably the key factor. 5. Nitrogen may play a far more important role than previously appreciated in the loss of submerged macrophytes at increased nutrient loading and for the delay in the re‐establishment of the nutrient loading reduction. We cannot yet specify, however, a threshold value for N that would cause a shift to a turbid state as it may vary with fish density and climatic conditions. However, the focus should be widened to use control of both N and P in the restoration of eutrophic shallow lakes.     

Impact of submerged macrophytes on fish-zooplanl phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake

1. The impact of changes in submerged macrophyte abundance on fish-zooplankton-phytoplankton interactions was studied in eighteen large-scale (100 m²) enclosures in a shallow eutrophic take. The submerged macrophytes comprised Potamategon pectinatus L., P. pusillus L. and Callitriche hermaphroditica L. while the fish fry stock comprised three-spined sticklebacks, Gasterosteus acuteatus L., and roach, Rutilus rutilus L. 2. In the absence of macrophytes zooplankton biomass was low and dominated by cyclopoid copepods regardless of fish density, while the phytoplankton biovolume was high (up to 38 mm³1) and dominated by small pennate diatoms and chlorococcales. When the lake volume infested by submerged macrophytes (PVI) exceeded 15–20% and the fish density was below a catch per unit effort (CPUE) of 10 (approx. 2 fry m^?2), planktonic cladoceran biomass was high and dominated by relatively large-sized specimens, while the phytoplankton biovolume was low and dominated by small fast-growing flagellates. At higher fish densities, zooplankton biomass and average biomass of cladocerans decreased and a shift to cyclopoids occurred, while phytoplankton biovolume increased markedly and became dominated by cyanophytes and dinoflagellates. 3. Stepwise multiple linear regressions on log-transformed data revealed that the biomass of Daphnia, Bosmina, Ceriodaphmia and Chydorus were all significantly positively related to PVI and negatively to the abundance of fish or PVI x fish. The average individual biomass of cladocerans was negatively related to fish, but unrelated to PVI. Calculated zooplankton grazing pressure on phytoplankton was positively related to PVI and negatively to PVI x fish. Accordingly the phytoplankton biovolume was negatively related to PVI and to PVI x zooplankton biomass. Cyanophytes and chryptophytes (% of biomass) were positively and Chlorococcales and diatoms negatively related to PVI, while cyanophytes and Chlorococcales were negatively related to PVI x zooplankton biomass. In contrast diatoms and cryptophytes were positively related to the zooplankton biomass or PVI x zooplankton. 4. The results suggest that fish predation has less impact on the zooplankton community in the more structured environment of macrophyte beds, particularly when the PVI exceeds 15–20%. They further suggest that the refuge capacity of macrophytes decreases markedly with increasing fish density (in our study above approximately 10 CPUE). Provided that the density of planktivorous fish is not high, even small improvements in submerged macrophyte abundance may have a substantial positive impact on the zooplankton, leading to a lower phytoplankton biovolume and higher water transparency. However, at high fish densities the refuge effect seems low and no major zooplankton mediated effects of enhanced growth of macrophytes are to be expected.     

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

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

Response of fish and plankton to nutrient loading reduction in eight shallow Danish lakes with special emphasis on seasonal dynamics

1. For 13 years the response of the plankton and fish community to a decline in external phosphorus loading was studied in eight lakes with a mean depth <5 m. We conducted chi‐square analyses of sign of slope (positive or negative) of bimonthly averages of plankton variables for the eight lakes versus time. For fish, we compared results from two periods, i.e. 1989–1994 versus 1994–2001 as less data were available. 2. Fish community structure tended to respond to the lowered concentration of total phosphorus (TP), although not all changes were significant. While catch per unit effort (multi‐mesh sized gill nets) of cyprinids (especially bream, Abramis brama and roach, Rutilus rutilus) was highest in the first 5‐year period, the quantitative importance particularly of perch (Perca fluviatilis), pike (Esox lucius) and rudd (Scardinius erythropthalmus), a littoral species, increased significantly after 1994. 3. No changes occurred in zooplankton biomass, except for an increase in November and December. Biomass of small cladocerans, however, declined during summer and autumn, and the proportion of Daphnia to cladoceran biomass also increased. Average body weight of Daphnia and that of all cladocerans increased. The proportion of calanoids among copepods decreased in summer and the average body weight of cyclopoids and calanoids decreased during summer and autumn/early winter. 4. Total biovolume of phytoplankton declined significantly in March to June and tended to decline in November and December as well, while no significant changes were observed during summer and autumn. Non‐heterocystous cyanobacteria showed a decreasing trend during summer and autumn, while heterocystous cyanobacteria increased significantly in late summer. An increase in late summer was also evident for cryptophytes and chrysophytes, while diatoms tended to decline during most seasons. 5. We conclude that phytoplankton, and probably also fish, responded rapidly to reduced loading, whereas the effect on zooplankton was less pronounced. However, increases in body weight of cladocerans and the zooplankton to phytoplankton biomass ratio during summer indicate reduced top‐down control on zooplankton and enhanced grazing on phytoplankton. This conclusion is supported by a tendency for fish biomass to decline and a shift towards greater dominance by piscivores and, thus, an increased likelihood of predator control of zooplanktivorous cyprinids.     

The structuring role of free-floating versus submerged plants in a subtropical shallow lake

In shallow temperate lakes many ecological processes depend on submerged macrophytes. In subtropical and tropical lakes, free-floating macrophytes may be equally or more important. We tested the hypothesis that different macrophyte growth forms would be linked with different bottom-up and top-down mechanisms in out-competing phytoplankton. We compared experimentally the effects of submerged and free-floating plants on water chemistry, phytoplankton biomass, zooplankton and fish community structure in a shallow hypertrophic lake (Lake Rodó, 34°55S 56°10W, Uruguay). Except for the retention of suspended solids, we found no other significant bottom-up process connected with either Eichhornia crassipes or Potamogeton pectinatus. Free-floating plants had a lower abundance of medium-sized zooplankton than any other microhabitat and submerged plants were apparently preferred by microcrustaceans. Fish showed a differential habitat use according to species, size-class and feeding habits. Dominant omnivore-planktivores, particularly the smallest size classes, preferred submerged plants. In contrast, omnivore-piscivores were significantly associated with free-floating plants. The density of omnivorous-planktivorous fish, by size class, significantly explained the distribution of medium-sized zooplankton, the high number of size 0 fish being the main factor. The abiotic environment and the structure of the zooplankton community explained little of the fish distribution pattern. Our results suggest that bottom-up effects of free-floating plants are weak when cover is low or intermediate. Top-down effects are complex, as effects on zooplankton and fish communities seem contradictory. The low piscivores:planktivores ratio in all microhabitats suggests, however, that cascading effects on phytoplankton through free-floating plant impacts on piscivorous fish are unlikely to be strong.     

Ambiguous climate impacts on competition between submerged macrophytes and phytoplankton in shallow lakes

1. Shallow lakes may switch from a state dominated by submerged macrophytes to a phytoplankton‐dominated state when a critical nutrient concentration is exceeded. We explore how climate change may affect this critical nutrient concentration by linking a graphical model to data from 83 lakes along a large climate gradient in South America. 2. The data indicate that in warmer climates, submerged macrophytes may tolerate more underwater shade than in cooler lakes. By contrast, the relationship between phytoplankton biomass [approximated by chlorophyll‐a (chl‐a) or biovolume] and nutrient concentrations did not change consistently along the climate gradient. In warmer climates, the correlation between phytoplankton biomass and nutrient concentrations was overall weak, especially at low total phosphorus (TP) concentrations where the chl‐a/ TP ratio could be either low or high. 3. Although the enhanced shade tolerance of submerged plants in warmer lakes might promote the stability of their dominance, the potentially high phytoplankton biomass at low nutrient concentrations suggests an overall low predictability of climate effects. 4. We found that near‐bottom oxygen concentrations are lower in warm lakes than in cooler lakes, implying that anoxic P release from eutrophic sediment in warm lakes likely causes higher TP concentrations in the water column. Subsequently, this may lead to a higher phytoplankton biomass in warmer lakes than in cooler lakes with similar external nutrient loadings. 5. Our results indicate that climate effects on the competitive balance between submerged macrophytes and phytoplankton are not straightforward.     

Dynamics of submerged macrophyte populations in response to biomanipulation

1. A 6‐year study (1992–97) of changes in submerged vegetation after biomanipulation was carried out in the eutrophicated Lake Finjasjön, Southern Sweden. Ten sites around the lake were revisited each year. At each site five samples of above‐ground biomass were taken at 10 cm water depth intervals. An investigation of the seed bank at the 10 sites, and a grazing experiment where birds and large fish were excluded was also conducted. 2. Between 1992 and 1996, in shallow areas (water depth < 3 m), vegetation cover increased from < 3 to 75% and above‐ground biomass from < 1 to 100 g DW m^–2. Mean outer water depth increased from 0.3 to 2.5 m. Elodea canadensis and Myriophyllum spicatum accounted for > 95% of the increase in biomass and plant cover. The following year (1997), however, cover and above‐ground biomass decreased, mainly attributable to the total disappearance of E. canadensis. Secchi depth increased after biomanipulation until 1996, but decreased again in 1997. 3. Total and mean number of submerged species increased after biomanipulation, probably as a result of the improved light climate. However, after the initial increase in species number there was a decrease during the following years, possibly attributed to competition from the rapidly expanding E. canadensis and M. spicatum. The lack of increase in species number after the disappearance of E. canadensis in 1997 implies that other factors also affected species richness. 4. A viable seed bank was not necessary for a rapid recolonization of submerged macrophytes, nor did grazing by waterfowl or fish delay the re‐colonization of submerged macrophytes. 5. Submerged macrophytes are capable of rapid recolonization if conditions improve, even in large lakes such as Finjasjön (11 km²). Species that spread by fragments will increase rapidly and probably outcompete other species. 6. The results indicate that after the initial Secchi depth increase, probably caused by high zooplankton densities, submerged vegetation further improved the light climate. The decrease in macrophyte biomass in 1997 may have caused the observed increase in phosphorus and chlorophyll a, and the decrease in Secchi depth. We suggest that nutrient competition from periphyton, attached to the macrophytes, may be an important factor in limiting phytoplankton production, although other factors (e.g. zooplankton grazing) are also of importance, especially as triggers for the shift to a clear‐water state.