Deriving nutrient targets to prevent excessive cyanobacterial densities in U.S. lakes and reservoirs

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The role of environmental parameters in the structure of phytoplankton assemblages and cyanobacteria toxins in two hypereutrophic lakes

We evaluated the variability of cyanotoxins, water chemistry, and cyanobacteria communities in two hypereutrophic drowned river mouth lakes (Spring Lake and Mona Lake; summer 2006) in west Michigan, USA. Even with considerable geographical and watershed similarity, local variations in nutrient concentrations and environmental factors were found to influence the differences observed in cyanobacteria assemblages and cyanotoxins levels between the two lakes. Limnothrix sp. dominated the phytoplankton community in Spring Lake (82% of biovolume) and was negatively correlated with total phosphorus (TP) concentrations. Although Spring Lake was treated with alum during the previous year, Limnothrix sp. was able to bloom in the lower P environment. In contrast, the N₂-fixing cyanobacterium, Anabaena flos-aquae, dominated the phytoplankton in Mona Lake (64% of biovolume). N₂-fixing cyanobacteria dominance in Mona Lake was correlated with higher TP lower dissolved nitrogen levels. Cylindrospermopsis raciborskii was found in both systems; however, the toxin-producing polyketide synthetase gene was not present in either population. The higher TP in Mona Lake appeared to account for the 3-fold increase in cyanobacteria biovolume. Restoration plans for both lakes should include assessments of internal loading and continued phytoplankton monitoring to track the temporal distribution of cyanobacteria species and cyanotoxin concentrations.     

Analysis of environmental drivers influencing interspecific variations and associations among bloom-forming cyanobacteria in large,shallow eutrophic lakes

Non-diazotrophic Microcystis and filamentous N₂-fixing Aphanizomenon and Dolichospermum (formerly Anabaena) co-occur or successively dominate freshwaters globally. Previous studies indicate that dual nitrogen (N) and phosphorus (P) reduction is needed to control cyanobacterial blooms; however, N limitation may cause replacement of non-N₂-fixing by N₂-fixing taxa. To evaluate potentially counterproductive scenarios, the effects of temperature, nutrients, and zooplankton on the spatio-temporal variations of cyanobacteria were investigated in three large, shallow eutrophic lakes in China. The results illustrate that the community composition of cyanobacteria is primarily driven by physical factors and the zooplankton community, and their interactions. Niche differentiation between Microcystis and two N₂-fixing taxa in Lake Taihu and Lake Chaohu was observed, whereas small temperature fluctuations in Lake Dianchi supported co-dominance. Through structural equation modelling, predictor variables were aggregated into ‘composites’ representing their combined effects on species-specific biomass. The model results showed that Microcystis biomass was affected by water temperature and P concentrations across the studied lakes. The biomass of two filamentous taxa, by contrast, exhibited lake-specific responses. Understanding of driving forces of the succession and competition among bloom-forming cyanobacteria will help to guide lake restoration in the context of climate warming and N:P stoichiometry imbalances.     

Increased risk of cyanobacterial blooms in northern high‐latitude lakes through climate warming and phosphorus enrichment

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CARBON AVAILABILITY AND THE PATTERN OF CYANOBACTERIAL DOMINANCE IN ENRICHED LOW-CARBON LAKES1

We hypothesize that the pattern of cyanobacterial dominance in experimentally enriched, low-carbon lakes is related not only to the resultant N:P ratio but also to the availability of carbon for gas-vesicle synthesis. We tested this hypothesis by determining the buoyancy responses of a highly gas-vacuolate, N₂-fixing cyanobacterium to P enrichment with and without induced C limitation. Enrichment of samples of Aphanizomenon schindleri (Kling et al. 1994) from blooms in Lake 227 with combinations of C, N, and P produced rapid buoyancy reductions in P treatments, reductions that were reversed within a generation time in treatments that included C or C and N as well as P. These responses are the first of their kind to be observed in experiments with lake populations of cyano-bacteria. The rapid buoyancy reductions were associated with polyphosphate accumulations in P-treated A. schindleri. Differences in buoyancy status after one generation time were linked to differences in relative gas vacuolation between samples treated with P only and samples treated with C and N as well as P. These results may explain the relative success of different types of cyanobacteria in newly enriched, low-carbon lakes. The availability of C for gasvesicle synthesis may determine whether a low N:P ratio induces N₂ fixation by benthic or by planktonic cyanobacteria and whether a high NP ratio leads to dominance by non-gas-vacuolate or by highly gas-vacuolate, non-N₂-fixers.     

Responses of phytoplankton to fish predation and nutrient loading in shallow lakes: a pan-European mesocosm experiment

1. The impacts of nutrients (phosphorus and nitrogen) and planktivorous fish on phytoplankton composition and biomass were studied in six shallow, macrophyte‐dominated lakes across Europe using mesocosm experiments. 2. Phytoplankton biomass was more influenced by nutrients than by densities of planktivorous fish. Nutrient addition resulted in increased algal biomass at all locations. In some experiments, a decrease was noted at the highest nutrient loadings, corresponding to added concentrations of 1 mg L^?1 P and 10 mg L^?1 N. 3. Chlorophyll a was a more precise parameter to quantify phytoplankton biomass than algal biovolume, with lower within‐treatment variability. 4. Higher densities of planktivorous fish shifted phytoplankton composition toward smaller algae (GALD < 50 μm). High nutrient loadings selected in favour of chlorophytes and cyanobacteria, while biovolumes of diatoms and dinophytes decreased. High temperatures also may increase the contribution of cyanobacteria to total phytoplankton biovolume in shallow lakes.     

Global changes may be promoting a rise in select cyanobacteria in nutrient‐poor northern lakes

The interacting effects of global changes—including increased temperature, altered precipitation, reduced acidification and increased dissolved organic matter loads to lakes—are anticipated to create favourable environmental conditions for cyanobacteria in northern lakes. However, responses of cyanobacteria to these global changes are complex, if not contradictory. We hypothesized that absolute and relative biovolumes of cyanobacteria (both total and specific genera) are increasing in Swedish nutrient‐poor lakes and that these increases are associated with global changes. We tested these hypotheses using data from 28 nutrient‐poor Swedish lakes over 16 years (1998–2013). Increases in cyanobacteria relative biovolume were identified in 21% of the study sites, primarily in the southeastern region of Sweden, and were composed mostly of increases from three specific genera: Merismopedia, Chroococcus and Dolichospermum. Taxon‐specific changes were related to different environmental stressors; that is, increased surface water temperature favoured higher Merismopedia relative biovolume in low pH lakes with high nitrogen to phosphorus ratios, whereas acidification recovery was statistically related to increased relative biovolumes of Chroococcus and Dolichospermum. In addition, enhanced dissolved organic matter loads were identified as potential determinants of Chroococcus suppression and Dolichospermum promotion. Our findings highlight that specific genera of cyanobacteria benefit from different environmental changes. Our ability to predict the risk of cyanobacteria prevalence requires consideration of the environmental condition of a lake and the sensitivities of the cyanobacteria genera within the lake. Regional patterns may emerge due to spatial autocorrelations within and among lake history, rates and direction of environmental change and the niche space occupied by specific cyanobacteria.     

Nutrient addition effects on chlorophyll a,phytoplankton biomass,and heterocyte formation in Lake Erie’s central basin during 2014–2017: Insights into diazotrophic blooms in high nitrogen water

1. Phosphorus (P) usually is the primary limiting nutrient of phytoplankton biomass, but attention towards nitrogen (N) and trace nutrients, such as iron (Fe), has surfaced. Additionally, N-fixing cyanobacterial blooms have been documented to occur in N-rich, P-poor waters, which is counterintuitive from the paradigm that low N and high P promotes blooms. For example, Lake Erie's central basin has Dolichospermum blooms when nitrate concentrations are high, which raises questions about which nutrient(s) are selecting for Dolichospermum over other phytoplankton and why an N-fixer is present in high N waters?
2. We conducted a 4-year (2014–2017) study in Lake Erie's central basin to determine which nutrient (P, N, or trace nutrients such as Fe, molybdenum [Mo], and boron [B]) constrained chlorophyll concentration, phytoplankton biovolume, and nitrate assimilation using nutrient enrichment bioassays. The enriched lake water was incubated in 1-L bottles in a growth chamber programmed at light and temperatures of in situ conditions for 4–7 days. We also quantified heterocytes when N-fixing cyanobacteria were present.
3. Compared to the non-enriched control, the P-enriched (+P) treatment had significantly higher chlorophyll and phytoplankton biovolume in c. 75% of experiments. Combination enrichments of P with ammonium-N, nitrate-N, Fe, Mo, and B were compared to the +P treatment to determine secondary limitations. +P and ammonium-N and +P nitrate-N resulted in higher chlorophyll in 50% of experiments but higher phytoplankton biovolume in only 25% of experiments. These results show that P was the primary limiting nutrient, but there were times when N was secondarily limiting.
4. Chlorophyll concentration indicated N secondary limitation in half of the experiments, but biovolume indicated only N secondary limitation in 25% of the experiments. To make robust conclusions from nutrient enrichment bioassays, both chlorophyll and phytoplankton biovolume should be measured.
5. The secondary effects of Fe, Mo, and B on chlorophyll were low (<26% of experiments), and no secondary effects were observed on phytoplankton biovolume and nitrate assimilation. However, +P and Fe resulted in more chlorophyll than +P in experiments conducted during Dolichospermum blooms, and +P and B significantly increased the number of heterocytes in Dolichospermum. These results indicate that low Fe availability might select for Dolichospermum, and low B constrains heterocyte formation in the central basin of Lake Erie. Furthermore, these results could apply to other lakes with high N and low P where diazotrophic cyanobacterial blooms occur.

     

Inverse relationship of epilithic algae and pelagic phosphorus in unproductive lakes: Roles of N2 fixers and light

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Warmer climates boost cyanobacterial dominance in shallow lakes

Dominance by cyanobacteria hampers human use of lakes and reservoirs worldwide. Previous studies indicate that excessive nutrient loading and warmer conditions promote dominance by cyanobacteria, but evidence from global scale field data has so far been scarce. Our analysis, based on a study of 143 lakes along a latitudinal transect ranging from subarctic Europe to southern South America, shows that although warmer climates do not result in higher overall phytoplankton biomass, the percentage of the total phytoplankton biovolume attributable to cyanobacteria increases steeply with temperature. Our results also reveal that the percent cyanobacteria is greater in lakes with high rates of light absorption. This points to a positive feedback because restriction of light availability is often a consequence of high phytoplankton biovolume, which in turn may be driven by nutrient loading. Our results indicate a synergistic effect of nutrients and climate. The implications are that in a future warmer climate, nutrient concentrations may have to be reduced substantially from present values in many lakes if cyanobacterial dominance is to be controlled.     

Contrasting microcystin production and cyanobacterial population dynamics in two Planktothrix-dominated freshwater lakes

Microcystin concentrations in two Dutch lakes with an important Planktothrix component were related to the dynamics of cyanobacterial genotypes and biovolumes. Genotype composition was analysed by using denaturing gradient gel electrophoresis (DGGE) profiling of the intergenic transcribed spacer region of the rrn operon (rRNA-ITS), and biovolumes were measured by using microscopy. In Lake Tjeukemeer, microcystins were present throughout summer (maximum concentration 30 microg l(-1)) while cyanobacterial diversity was low and very constant. The dominant phototroph was Planktothrix agardhii. In contrast, Lake Klinckenberg showed a high microcystin peak (up to 140 microg l(-1)) of short duration. In this lake, cyanobacterial diversity was higher and very dynamic with apparent genotype successions. Several genotypes derived from DGGE field profiles matched with genotypes from cultures isolated from field samples. The microcystin peak measured in Lake Klinckenberg could be confidently linked to a bloom of Planktothrix rubescens, as microscopic and genotypic analysis showed identity of bloom samples and a toxin-producing P. rubescens culture. Toxin-producing genotypes were detected in the microbial community before they reached densities at which they were detected by using microscopy. Cyanobacterial biovolumes provided additional insights in bloom dynamics. In both lakes, the microcystin content per cell was highest at the onset of the blooms. Our results suggest that while genotypic characterization of a lake can be valuable for detection of toxic organisms, for some lakes a monitoring of algal biomass has sufficient predictive value for an assessment of toxin production.     

Nitrogen fixation by marine cyanobacteria

Discrepancies between estimates of oceanic N(2) fixation and nitrogen (N) losses through denitrification have focused research on identifying N(2)-fixing cyanobacteria and quantifying cyanobacterial N(2) fixation. Previously unrecognized cultivated and uncultivated unicellular cyanobacteria have been discovered that are widely distributed, and some have very unusual properties. Uncultivated unicellular N(2)-fixing cyanobacteria (UCYN-A) lack major metabolic pathways including the tricarboxylic acid cycle and oxygen-evolving photosystem II. Genomes of the oceanic N(2)-fixing cyanobacteria are highly conserved at the DNA level, and genetic diversity is maintained by genome rearrangements. The major cyanobacterial groups have different physiological and ecological constraints that result in highly variable geographic distributions, with implications for the marine N-cycle budget.     

Cyanobacterial diversity in the phyllosphere of a mangrove forest

The cyanobacterial community colonizing phyllosphere in a well-preserved Brazilian mangrove ecosystem was assessed using cultivation-independent molecular approaches. Leaves of trees that occupy this environment (Rhizophora mangle,Avicennia schaueriana and Laguncularia racemosa) were collected along a transect beginning at the margin of the bay and extending upland. The results demonstrated that the phyllosphere of R. mangle and L. racemosa harbor similar assemblages of cyanobacteria at each point along the transect. A. schaueriana, found only in the coastal portions of the transect, was colonized by assemblages with lower richness than the other trees. However, the results indicated that spatial location was a stronger driver of cyanobacterial community composition than plant species. Distinct cyanobacterial communities were observed at each location along the coast-to-upland transect. Clone library analysis allowed identification of 19 genera of cyanobacteria and demonstrated the presence of several uncultivated taxa. A predominance of sequences affiliated with the orders Nostocales and Oscillatoriales was observed, with a remarkable number of sequences similar to genera Symphyonemopsis/Brasilonema (order Nostocales). The results demonstrated that phyllosphere cyanobacteria in this mangrove forest ecosystem are influenced by environmental conditions as the primary driver at the ecosystem scale, with tree species exerting some effect on community structure at the local scale.     

Increased nutrient loading and rapid changes in phytoplankton expected with climate change in stratified South European lakes: sensitivity of lakes with different trophic state and catchment properties

We hypothesised that increasing winter affluence and summer temperatures, anticipated in southern Europe with climate change, will deteriorate the ecological status of lakes, especially in those with shorter retention time. We tested these hypotheses analysing weekly phytoplankton and chemistry data collected over 2 years of contrasting weather from two adjacent stratified lakes in North Italy, differing from each other by trophic state and water retention time. Dissolved oxygen concentrations were higher in colder hypolimnia of both lakes in the second year following the cold winter, despite the second summer was warmer and the lakes more strongly stratified. Higher loading during the rainy winter and spring increased nutrient (N, P, Si) concentrations, and a phytoplankton based trophic state index, whilst the N/P ratio decreased in both lakes. The weakened Si limitation in the second year enabled an increase of diatom biovolumes in spring in both lakes. Chlorophyll a concentration increased in the oligo-mesotrophic lake, but dropped markedly in the eutrophic lake where the series of commonly occurring cyanobacteria blooms was interrupted. The projected increase of winter precipitation in southern Europe is likely to increase the nutrient loadings to lakes and contribute to their eutrophication. The impact is proportional to the runoff/in-lake concentration ratio of nutrients rather than to the retention time, and is more pronounced in lakes with lower trophy.     

Harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters – state of knowledge and research needs

Cyanobacterial blooms have increased in freshwater ecosystems worldwide in the last century, mostly resulting from eutrophication and climate change. These blooms represent serious threats to environmental and human health because of the production of harmful metabolites, called cyanotoxins. Like many countries, Egypt has been plagued with cyanobacterial blooms in most water sources, including the Nile River, irrigation canals, lakes and fishponds. However, the data about cyanotoxins produced in these blooms are limited. Only two types of cyanotoxins, microcystins and cylindrospermopsin, have been identified and characterised, mainly from Microcystis and Cylindrospermopsis blooms. The data revealed the presence of microcystins in raw and treated drinking waters at concentrations (0.05–3.8 µg l^?1), exceeding the WHO limit (1 µg l^?1) in some drinking water treatment plants. In addition, Nile tilapia Oreochromis niloticus caught from ponds containing heavy cyanobacterial blooms have accumulated considerable amounts of cyanotoxins in their edible tissues. The data presented here could be the catalyst for the establishment of a monitoring and management programme for harmful cyanobacteria and their cyanotoxins in Egyptian fresh waters. This review also elucidates the important research gaps and possible avenues for future research on cyanobacterial blooms and cyanotoxins in Egypt.     

Evidence for iron‐regulated cyanobacterial predominance in oligotrophic lakes

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Microbial Assemblages in Soil Microbial Succession After Glacial Retreat in Svalbard (High Arctic)

Microbial community composition (cyanobacteria and eukaryotic microalgae abundance and diversity, bacterial abundance, and soil respiration) was studied in subglacial and periglacial habitats on five glaciers near Ny-Alesund, Svalbard (79 degrees N). Soil microbial communities from nonvegetated sites (subglacial, recently deglaciated, and cryoconite sediments) and sites with plant cover (deglaciated some hundreds of years ago) were analyzed. Physicochemical analyses (pH, texture, water content, organic matter, total C and N content) were also performed on the samples. In total, 57 taxa of 23 genera of cyanobacteriaand algae were identified. Algae from the class Chlorophyceae (25 species) and cyanobacteria (23 species) were richest in biodiversity. The numbers of identified species in single habitat types were 23 in subglacial, 39 inbarren, 22 in cryoconite, and 24 in vegetated soils. The highest cyanobacterial and algal biovolume and cell numbers, respectively, were present in cryoconite (13x10(4) microm3 mg-1 soil and 508 cells per mg of soil), followed by barren (5.7x10(4) and 188), vegetated (2.6x10(4) and 120), and subglacial (0.1x10(4) and 5) soils. Cyanobacteria prevailed in all soil samples. Algae (mainly green algae) were present only as accessory organisms. The density of bacteria showed a slightly different trend to that of the cyanobacterial and algal assemblages. The highest number of bacteria was present in vegetated (mean: 13,722x10(8) cells per mg of soil dry wt.), followed by cryoconite (3802x10(8)), barren (654x10(8)), and subglacial (78x10(8)) soils. Response of cyanobacteria and algae to physical parameters showed that soil texture and water content are important for biomass development. In addition, it is shown that nitrogen and water content are the main factors affecting bacterial abundance and overall soil respiration. Redundancy analysis (RDA) with forward selection was used to create a model explaining variability in cyanobacterial, algal, and bacterial abundance. Cryoconites accounted for most of the variation in cyanobacteria and algae biovolume, followed by barren soils. Oscillatoriales, desmids, and green coccoid algae preferred cryoconites, whereas Nostocales and Chroococcales occurred mostly in barren soils. From the data obtained, it is evident that of the studied habitats cryoconite sediments are the most suitable ones for the development of microbial assemblages. Although subglacial sediments do not provide as good conditions as cryoconites, they support the survival of microbial communities. Both mentioned habitats are potential sources for the microbial recolonization of freshly deglaciated soil after the glacier retreat.     

Characterization of akinetes from cyanobacterial strains and lake sediment: A study of their resistance and toxic potential

Nostocalean cyanobacteria are known to proliferate abundantly in eutrophic aquatic ecosystems, and to produce several cyanotoxins, including anatoxin-a. In this study, we investigated both the resistance and toxic potential of the akinetes (resistant cells), using cyanobacterial cultures and akinetes extracted from the sediment of Lake Aydat (France) sampled in the winter and spring. Intact and lysed akinetes were differentiated using a double control based on the autofluorescence of akinetes and SYTOX-green staining. The percentage of resistant akinetes found in several different abiotic stress conditions was highly variable, depending on the species and also on the sampling season. Thus, the resistance of akinetes and their ability to germinate seems to follow a species-specific process, and akinetes can undergo physiologic changes during the sedimentary phase of the Nostocale life cycle. This study also revealed the first evidence of anatoxin-a genes in akinetes, with anaC and anaF genes detected in akinetes from all cyanobacterial producer cultures. The low number of anaC genes, almost exclusively detected using nested PCR, in the sediment at Lake Aydat suggests a limited but existent past population of toxic Nostocales in this lake. Given the key role of akinetes in the annual cycle and subsequent summer proliferation, it can be interesting to integrate the surveillance of akinetes in the management of lakes exposed to recurrent cyanobacterial blooms.