Nutrient limitation of phytoplankton and periphyton growth in upland lakes

SUMMARY 1. Thirty small upland lakes in Cumbria, Wales, Scotland and Northern Ireland were visited three times between April and August 2000. On each occasion water chemistry was measured and phytoplankton bioassays were performed in the laboratory to assess growth‐rate and yield limitation by phosphorus and nitrogen. In addition, yield limitation of periphyton growth was investigated twice, in situ, using nutrient‐diffusing substrata. 2. Over the whole season the percentage frequency of P, N and co‐limitation was 24, 13 and 63%, respectively, for phytoplankton rate limitation and 20, 22 and 58%, respectively, for phytoplankton yield limitation. 3. A clear response of periphyton yield to nutrient additions was found in 75% of all cases and of these, co‐limitation was most common (54%). Average percentage frequency for P and N limitation was 26 and 20%, respectively. 4. Phytoplankton and periphyton showed seasonal changes in nutrient limitation within sites. In particular, co‐limitation became progressively more common as the season progressed. 5. The response of phytoplankton growth rate to ammonium and nitrate addition was identical, but ammonium was a slightly better source of nitrogen than nitrate for phytoplankton yield on 7% and for periphyton yield on 10% of the occasions. However, the magnitude of the effect was small. 6. The concentration of dissolved inorganic nitrogen (DIN) and the molar ratio of DIN to total dissolved phosphorus (TDP), appeared to be the main environmental factors controlling the extent of nitrogen or phosphorus limitation at a given site. Nitrogen limitation was more likely than phosphorus limitation where the DIN was <6.5 mmol m^?3 and the ratio of DIN : TDP was <53. Co‐limitation was the most likely outcome at a DIN concentration <13 mmol m^?3 and at a DIN : TDP molar ratio <250. Above these values phosphorus limitation was most likely. 7. The relatively high frequency of nitrogen limitation and co‐limitation at higher N : P ratios than previously reported, may result from the inability of nitrogen‐fixing cyanobacteria to thrive in these upland lakes where pH and the concentration of phosphorus tended to be low and where flushing rates tended to be high.     

An assessment of the importance of emergent and floating-leaved macrophytes to trophic status in the Loosdrecht lakes (The Netherlands)

The potential importance of the six major emergent and floating-leaved macrophyte species in recycling of sediment phosphorus in the Loosdrecht lakes was studied. Representative plant samples were collected at the time of maximum biomass, and analysed for biomass and carbon, nitrogen and phosphorus contents. Species cover was determined by aerial photography.Total cover in the seven lakes studied ranged between 2 and 26 percent. For the four main species, biomass per unit area increased with lake trophic status. Consistent differences in C, N and P contents per unit biomass were not observed. Although cover values were small, significant amounts of C, N and P were contained in the macrophytes when compared with maximum sestonic content.Potential P loads from macrophyte decay were calculated. In Lake Loosdrecht, the P load represented 15 percent of current external P inputs. The potential importance of macrophyte decay to P recycling in the other lakes is greater.Decay of macrophyte species at the end of the growing season appears to affect autumnal nutrient and chlorophyll a levels in the water column of some lakes. The re-establishment of submerged species following lake restoration may increase the importance of this pathway in the lakes.     

Biomanipulation additional to nutrient control for restoration of shallow lakes in The Netherlands

Eutrophication control is one of the major issues in the environmental policy in The Netherlands. As a result of international action programmes the average phosphorus loading of freshwater systems should decrease by 50% between 1985 and 1995. However, in many cases the restoration of water quality requires additional measures. Recovery is hampered by the structure and functioning of the present food-chain.

The feeding behaviour of the dominant fish species in Dutch lakes, bream and roach, tend to impose a homeostasis on the system, resisting restoration of water quality. In shallow lakes, biomanipulation, including drastic reduction of fish-stocks, may induce a shift from a stable ‘turbid-water state’ to a stable ‘clear-water state’.

To assess the possibilities of biomanipulation for the restoration of a particular lake, three questions are relevant: (1) is a drastic reduction of fish-stocks feasible?, (2) will a shift occur from ‘turbid to clear’ after the fish reduction? and (3) will the new situation of clear water be stable? This paper focuses attention on the last two questions. The increase in water clarity, following fish reduction, largely depends on the increase in the density of the Daphnia-population and the contribution of benthivorous fish to the resuspension of sediments. A ‘turbid to clear’ shift may be expected if the total biomass of planktivorous and benthivorous fish is reduced to levels<50 kg ha^?1. The stability of the achieved clear-water state largely depends on the development of submerged macrophytes in the lake and on the level of nutrient loading. It is tentatively concluded that a stable clear-water state may be expected at initial total-P concentrations<0.10 mg l^?1.

Because the water managers in The Netherlands have no fishing rights, they have to.co-operate with anglers and commercial fishermen to apply biomanipulation as a tool for water management.

     

The importance of avian-contributed nitrogen (N) and phosphorus (P) to Lake Grand-Lieu,France

The largest natural lake in France, Grand-Lieu, has suffered eutrophication. The objective of the study was to estimate the annual input of nutrients (N, P) resulting from avian excrement, deposited by birds feeding out of the lake and returning to its waters for breeding or roosting, as compared to the input by the rivers that enter in the lake. Two years are compared: 1981–82 and 1990–91. About 1600–2000 breeding herons and cormorants, 20 000–33 000 wintering ducks, gulls and cormorants and 1–2.4 million starlings deposited about 5800 kg total N in 1981–82 and 7640 kg in 1990–91. Respectively, 2000 and 2530 kg total P were deposited over the same time periods. These represent 0.7% and 0.4% of the total N input of the lake and 2.4 and 6.6% of the total P input in 1981–82 and 1990–91. Starlings account for 74% of the N and mallards most of the rest. P input by starlings (36% in 1981–82, 41% in 1990–91), and by mallards and herons (35% and 27% in 1981–82 and 22% and 24% in 1990–91 respectively) plays an appreciable role among birds. During the plant growing period (April–September), the contribution by birds can increase to 37% of total P input of the lake. Piscivorous bird colonies concentrate Phosphorus 42 times more within the colony than outside the colony. Overall, the role birds play in total N and P input is relatively small due to very high inputs from human sewage and agriculture run off. The monthly mean concentration of the water of the two rivers reaches currently 10 mg l^–1 of N (to 23 mg during peak floods) and 394 mg m^–3 of P (to 468 mg during peak floods). Earlier, for example in the 1960's, water in Brittany only contained 0.1 to 1.1 mg 1^–1 of N and 1 to 5 mg m^–3 of P during the maximum flow period. At this time, birds could probably have represented annually up to 37% of the N input and up to 95% of the P input to the lake.     

Nitrogen stable isotope ratios in surface sediments, epilithon and macrophytes from upland lakes with differing nutrient status

1. Thirty small upland lakes in Cumbria, Wales, Scotland and Northern Ireland were each visited once during June and July 2000. From each lake, samples of surface sediment epilithon, macrophytes and total dissolved nitrogen (TDN) were collected for nitrogen stable isotope analysis. As part of a wider programme, samples were also collected for chemical analysis and bioassays. 2. Considerable variation was found in δ¹⁵N values in all measured nitrogen compartments. Some regional variation was evident but was generally weak. Sediment and epilithon δ¹⁵N were positively correlated with δ¹⁵N of TDN, suggesting that baseline nitrogen isotope ratios influence those in some organic matter compartments in the lakes. 3. Sediment δ¹⁵N was higher when inorganic nitrogen concentration in the water was low, possibly reflecting reduced isotope fractionation under these conditions. However, this was not the case for epilithon or macrophytes. Sediment δ¹⁵N values were also negatively related to annual nitrogen deposition. 4. Sediment, epilithon and macrophyte δ¹⁵N values all showed significant relations to nutrient limitation in the lakes as determined by algal bioassays. We suggest that sediment δ¹⁵N might be developed as a simple integrating measure of the degree of nitrogen limitation in lakes.     

Restoration of Botshol (The Netherlands) by reduction of external load: Problem analyses and restoration methods

Since 1960 the water quality of the nature reserve Botshol has been deteriorated. An increase in the nutrient load caused an escalation in phytoplankton biomass and turbidity problems. This may have been caused by nutrient-rich water flowing into the reserve from the agricultural areas and from the polder of Nellestein. From 1980 to 1985 much research has been undertaken and participation of different disciplines gave the opportunity to analyse the cause of the changes. An integrated restoration plan has been drawn up to reduce the eutrophication. The plan was implemented in 1989 and in order to reverse the external nutrient load the following measures were taken. 1. Execution of a water management plan with the intention to isolate the agricultural areas from the reserve area. 2. Dephosphorization of the inlet water. These restoration measures resulted in a reduction of the external load from 0.6 to 0.1 g P m^–2 year^–1.     

The dynamics and role of limnetic zooplankton in Loosdrecht lakes (The Netherlands)

The paper summarizes the results of a ten-year (1981–1991) zooplankton research on the Lake Loosdrecht, a highly eutrophic lake. The main cause of the lake's eutrophication and deteriorating water quality was supply up to mid 1984 of water from the River Vecht. This supply was replaced by dephosphorized water from the Amsterdam-Rhine Canal in 1984. The effects of this and other restoration measures on the lake's ecosystem were studied. Despite a reduction in the external P-load from ca. 1.0 g P m^–2 y^–1 to ca. 0.35 g m^–2 y^–1 now, the filamentous prokaryotes, including cyanobacteria and Prochlorothrix, continue to dominate the phytoplankton.Among the crustacean plankton Bosmina spp, Chydorus sp. and three species of cyclopoid copepods and their nauplii are quite common. Though there was no major change in the composition of abundant species, Daphnia cucullata, which is the only daphnid in these lakes, became virtually extinct since 1989. Among about 20 genera and 40 species of rotifers the important ones are: Anuraeopsis fissa, Keratella cochlearis, Filinia longiseta and Polyarthra. The rotifers usually peak in mid-summer following the crustacean peak in spring. The mean annual densities of crustaceans decreased during 1988–1991. Whereas seston (< 150 µm) mean mass in the lake increased since 1983 by 20–60%, zooplankton (> 150 µm) mass decreased by 15–35%.The grazing by crustacean community, which was attributable mainly to Bosmina, had mean rates between 10 and 25% d^–1. Between 42 and 47% of the food ingested was assimilated. In spring and early summer when both rotifers and crustaceans have their maximal densities the clearance rates of the rotifers were much higher. Based on C/P ratios, the zooplankton (> 150 µm) mass contained 2.5 times more phosphorus than seston (< 150 µm) mass so that the zooplankton comprised 12.5 % of the total-P in total particulate matter in the open water, compared with only 4.5% of the total particulate C. The mean excretion rates of P by zooplankton varied narrowly between 1.5 and 1.8 µg P 1^– d^–1, which equalled between 14 and 28% d^–1 of the P needed for phytoplankton production.The lack of response to restoration measures cannot be ascribed to one single factor. Apparently, the external P-loading is still not low enough and internal P-loading, though low, may be still high enough to sustain high seston levels. Intensive predation by bream is perhaps more important than food quality (high concentrations of filamentous cyanobacteria) in depressing the development of large-bodied zooplankton grazers, e.g. Daphnia. This may also contribute to resistance of the lake's ecosystem to respond to rehabilitation measures.     

The response of planktonic and microbenthic algal assemblages to nutrient enrichment in shallow coastal waters,southwest Sweden

Field and laboratory nutrient (nitrogen and phosphorus) enrichment experiments were performed using natural phytoplankton and microphytobenthic assemblages from the brackish water Öresund, S.W. Sweden. The response of algae from a low-nutrient area (Falsterbo Canal) was compared to that of algae from a polluted, nutrient-rich area (Lomma Bay).The biomass (measured as chlorophyll a) of both phytoplankton and microphytobenthos from the Falsterbo Canal increased after the addition of nitrogen. Phytoplankton growth was stimulated by the addition of phosphorus to the nitrogen-rich water of the polluted Lomma Bay. Sediment chlorophyll a showed no significant increase after the addition of nutrients in the Lomma Bay. In containers without sediment, phytoplankton uptake was calculated to account for ≈ 90% of the disappearance of inorganic fixed nitrogen from the water. In the sediment containers the microphytobenthos was estimated to account for ≈20% of the nitrogen uptake. The rest was presumably lost mainly through denitrification.When containers with microphytobenthos from Lomma Bay were kept in the dark, phosphorus was released at a rate of up to ≈ 180 μM · m^?2 · day^?1. We suggest that by producing oxygen microbenthic algae keep the sediment surface oxygenated thereby decreasing phosphorus transport from the sediment to the overlying water.     

Atmospheric nitrogen deposition has caused nitrogen enrichment and eutrophication of lakes in the northern hemisphere

We compiled chemical data and phytoplankton biomass (PB) data (chlorophyll a ) from unproductive lakes in 42 different regions in Europe and North America, and compared these data to inorganic nitrogen (N) deposition over these regions. We demonstrate that increased deposition of inorganic N over large areas of Europe and North America has caused elevated concentrations of inorganic N in lakes. In addition, the unproductive lakes in high N deposition areas had clearly higher PB relative to the total phosphorus (P) concentrations illustrating that the elevated inorganic N concentrations has resulted in eutrophication and increased biomass of phytoplankton. The eutrophication caused by inorganic N deposition indicates that PB yield in a majority of lakes in the northern hemisphere is (was) limited by N in their natural state. We, therefore, suggest that P limitation largely concerns lakes where the balance between N and P has been changed because of increased anthropogenic input of N.     

Soluble nitrogen and phosphorus excretion of exotic freshwater mussels (Dreissena spp.): potential impacts for nutrient remineralisation in western Lake Erie

1. Recent increases in phytoplankton biomass and the recurrence of cyanobacterial blooms in western Lake Erie, concomitant with a shift from a community dominated by zebra mussels (Dreissena polymorpha) to one dominated by quagga mussels (D. bugensis), led us to test for differences in ammonia‐nitrogen and phosphate‐phosphorus excretion rates of these two species of invasive molluscs. 2. We found significant differences in excretion rate both between size classes within a taxon and between taxa, with zebra mussels generally having greater nutrient excretion rates than quagga mussels. Combining measured excretion rates with measurements of mussel soft‐tissue dry weight and shell length, we developed nutrient excretion equations allowing estimation of nutrient excretion by dreissenids. 3. Comparing dreissenid ammonia and phosphate excretion with that of the crustacean zooplankton, we demonstrated that the mussels add to nitrogen and phosphorus remineralisation, shortening nitrogen and phosphorus turnover times, and, importantly, modify the nitrogen and phosphorus cycles in Lake Erie. The increased nutrient flux from dreissenids may facilitate phytoplankton growth and cyanobacterial blooms in well‐mixed and/or shallow areas of western Lake Erie.     

Response of lakes to the reduction of phosphorus load

On occasion of the publication of a book (H. SAS, ed.) a discussion of the predictability of the response of eutrofied lakes on a reduced external phosphorus loading is presented. Whereas the OECD study examines the correlations between nutrient loading and indicators for eutrofication for groups of lakes, the book discusses the direction of the response on reduction of the phosphorus loading for individual lakes. Although this is a valuable analysis that can increase the insight in the mechanisms controlling lake responses, neither the OECD study nor this book yield sufficiently unquestioned data that can be used directly in a a management framework. The relationships between loading and inlake concentration and between phosphate concentration and chlorophyll are discussed in some detail.     

The significance of the Loosdrecht lakes research project for eutrophication policy in The Netherlands

The Project on the Water Quality Research in the Loosdrecht Lakes (WQL) has come up to the expectations of the Netherlands Environment Ministry. The results reaffirm the main lines of national eutrophication policy drawn up in 1979 (Policy Document on Phosphates) and further developed in the eighties. Interesting new insights have been gained, for example into the role of sediment and seston as well as into the relative importance of trophic levels. It is not possible, however, to definitely establish the effect of WQL on eutrophication policy.The Loosdrecht project is an example of genuine ecological research, incorporating several disciplines, placing the object of research into its surroundings, emphasising the relation nature-culture and committing itself to certain value judgements and policy choices. As a consequence, there is a striking resemblance between the evolution of the project itself and that of ecosystems.All in all the Loosdrecht project should be regarded as a paradigm for future ecosystem studies.     

Phosphorus eutrophication research in the lake district of south western Friesland,The Netherlands. Preliminary results of abiotic studies

The water quality of the lakes in south western Friesland is influenced by a rather complex hydrology. The purpose of the abiotic part of the eutrophication project, started in 1984 and focused on phosphorus, is to model hydrology and phosphorus dynamics, in order to compare scenarios for policy and management.A brief survey is given of the preliminary results of the abiotic studies: hydrology, water quality, external loading from surrounding polders, sedimentary phosphorus and internal loading. The two largest lakes, Tjeukemeer and Slotermeer, are compared regarding these processes.     

Rewiring coral: Anthropogenic nutrients shift diverse coral–symbiont nutrient and carbon interactions toward symbiotic algal dominance

Improving coral reef conservation requires heightened understanding of the mechanisms by which coral cope with changing environmental conditions to maintain optimal health. We used a long‐term (10 month) in situ experiment with two phylogenetically diverse scleractinians (Acropora palmata and Porites porites) to test how coral–symbiotic algal interactions changed under real‐world conditions that were a priori expected to be beneficial (fish‐mediated nutrients) and to be harmful, but non‐lethal, for coral (fish + anthropogenic nutrients). Analyzing nine response variables of nutrient stoichiometry and stable isotopes per coral fragment, we found that nutrients from fish positively affected coral growth, and moderate doses of anthropogenic nutrients had no additional effects. While growing, coral maintained homeostasis in their nutrient pools, showing tolerance to the different nutrient regimes. Nonetheless, structural equation models revealed more nuanced relationships, showing that anthropogenic nutrients reduced the diversity of coral–symbiotic algal interactions and caused nutrient and carbon flow to be dominated by the symbiont. Our findings show that nutrient and carbon pathways are fundamentally “rewired” under anthropogenic nutrient regimes in ways that could increase corals’ susceptibility to further stressors. We hypothesize that our experiment captured coral in a previously unrecognized transition state between mutualism and antagonism. These findings highlight a notable parallel between how anthropogenic nutrients promote symbiont dominance with the holobiont, and how they promote macroalgal dominance at the coral reef scale. Our findings suggest more realistic experimental conditions, including studies across gradients of anthropogenic nutrient enrichment as well as the incorporation of varied nutrient and energy pathways, may facilitate conservation efforts to mitigate coral loss.     

The structure and function of fen lakes in relation to water table management in The Netherlands

Most relatively large (> 250 ha) and shallow (< 2 m), Dutch lakes originate from large-scale peat mining. Originally, their water tables were regulated by natural processes such as evapotransporation, precipitation, drainage and seepage (up and downwards). These lakes used to be oligo to mesotrophic, and the phytoplankton consisted mainly of diatoms and green algae. However, 30 years ago filamentous cyanobacteria were also present. Owing to the intensification of agriculture in the surroundings of the lakes, their management developed more and more towards a man-made reservoir function. This management resulted in inflow of eutrophic water from the agricultural areas in winter. In summer the lakes were increasingly used as a water supply. This supply is compensated by water imported mainly from the River Rhine. The impacts of this reservoir function on the limnology of the Dutch fen lakes are discussed with the Tjeukemeer, the Loosdrechtse Plassen and the Reeuwijkse Plassen as examples. All these lakes have become typical eutrophic waters with high turbidity, dominance of filamentous cyanobacteria and bream and complete loss of submerged macrophytes. Finally, methods and results of manipulation procedures to restore these waters are discussed.     

Light and nutrient control phytoplankton biomass responses to global change in northern lakes

Global change affects terrestrial loadings of colored dissolved organic carbon (DOC) and nutrients to northern lakes. Still, little is known about how phytoplankton respond to changes in light and nutrient availability across gradients in lake DOC. In this study, we used results from whole‐lake studies in northern Sweden to show that annual mean phytoplankton biomass expressed unimodal curved relationships across lake DOC gradients, peaking at threshold DOC levels of around 11 mg/L. Whole‐lake single nutrient enrichment in selected lakes caused elevated biomass, with most pronounced effect at the threshold DOC level. These patterns give support to the suggested dual control by DOC on phytoplankton via nutrient (positively) and light (negatively) availability and imply that the lakes' location along the DOC axis is critical in determining to what extent phytoplankton respond to changes in DOC and/or nutrient loadings. By using data from the large Swedish Lake Monitoring Survey, we further estimated that 80% of northern Swedish lakes are below the DOC threshold, potentially experiencing increased phytoplankton biomass with browning alone, and/or combined with nutrient enrichment. The results support the previous model results on effects of browning and eutrophication on lake phytoplankton, and provide important understanding of how northern lakes may respond to future global changes.     

The effects of land use upon water chemistry,particularly nutrient enrichment,in shallow lowland lakes: comparative studies of three lochs in Scotland

Three shallow, lowland lochs (lakes) in the Tayside region of Scotland, experiencing the same climatic regime, were found to be dimictic lakes showing similar clinograde oxygen distributions in summer. Land use differences in their catchments were shown to result in estimated total nutrient surface loadings from 0.3 to 32 g m^–2 a^–1 phosphorus and from 4 to 240 g m^–2 a^–1 nitrogen. The major ions in the lochs were calcium and carbonate, but with elevated sulphate levels in all three lochs and an increase in sodium, chloride and sulphate in Forfar loch, which was affected by sewage effluent. Conductivity and total alkalinity showed marked increases with greater intensity of land use, from 64 to 439 µS cm^–1 and 0.5–3 meq l^–1 Maximum winter loch concentrations of soluble reactive phosphorus ranged from 60 to just under 5 000 mg m^–3 and of inorganic nitrogen from 500 to 10500 mg m^–3. Maximum chlorophyll a ranged from 20 to 250 mg m^–3 and comparisons indicated that above winter levels of 5000 mg m^–3 N and 500 mg m^–3 P, the nutrient-chlorophyll relationships did not hold. Predictions of nutrient input, from land use categories and soil losses of N and P derived from other north temperate areas, were shown to be comparable with inputs calculated from loch measurements. Models predicting loch concentrations of phosphorus from inputs were comparable with measured concentrations, but predictions of chlorophyll and transparency became less accurate with higher nutrient levels. The lochs were mesotrophic (the Lowes), eutrophic (Balgavies) and hypertrophic (Forfar) under the several classification systems used. The implications of their nutrient status for lake management are discussed and the value of studying this unique lake series in a similar physical environment but with considerable chemical differences is considered.     

The influence of flushing on nutrient dynamics,composition and densities of algae and transparency in Veluwemeer,The Netherlands

Total phosphorus and chlorophyll decreased significantly after reduction of the external phosphorus loading and the start of flushing Veluwemeer with polder water in 1979.Flushing of Veluwemeer has had a large impact on nutrient dynamics. Especially in the first winter, dilution was the main cause of changes in water quality. On a longer term the increase of the inactivation of phosphorus in sediments is important. Oscillatoria agardhii has been brought to the margins of its habitat. Three successive cold winters were an additional causal factor in the disappearance of Oscillatoria agardhii and the dominance of diatoms and green algae from 1985 onwards.Due to higher detritus and inorganic suspended matter concentrations transparency increased less than expected. Since 1985 chlorophyll only contributes for a small percentage to the transparency.In the present situation further improvement of the water quality of Veluwemeer is questionable, as the phosphorus concentration in the lake and the polder water is almost the same. Therefore it is recommanded to shift flushing operations, at least in the winter period, from Veluwemeer towards Wolderwijd.     

Macrophyte effects on algal turbidity in subtropical versus temperate lakes: a reply to Dolman (2014)

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