Ecology under lake ice.

Winter conditions are rapidly changing in temperate ecosystems, particularly for those that experience periods of snow and ice cover. Relatively little is known of winter ecology in these systems, due to a historical research focus on summer 'growing seasons'. We executed the first global quantitative synthesis on under-ice lake ecology, including 36 abiotic and biotic variables from 42 research groups and 101 lakes, examining seasonal differences and connections as well as how seasonal differences vary with geophysical factors. Plankton were more abundant under ice than expected; mean winter values were 43.2% of summer values for chlorophyll a, 15.8% of summer phytoplankton biovolume and 25.3% of summer zooplankton density. Dissolved nitrogen concentrations were typically higher during winter, and these differences were exaggerated in smaller lakes. Lake size also influenced winter-summer patterns for dissolved organic carbon (DOC), with higher winter DOC in smaller lakes. At coarse levels of taxonomic aggregation, phytoplankton and zooplankton community composition showed few systematic differences between seasons, although literature suggests that seasonal differences are frequently lake-specific, species-specific, or occur at the level of functional group. Within the subset of lakes that had longer time series, winter influenced the subsequent summer for some nutrient variables and zooplankton biomass.

Can submerged macrophytes influence turbidity and trophic state in deep lakes? Suggestions from a case study.

Feedback between submerged macrophytes and water transparency stabilizing the clear, macrophyte-dominated regime has been described so far for shallow lakes. Based on data of total phosphorus (TP) concentrations, underwater light supply, phytoplankton and submerged macrophyte abundance from narrow, stratified Lake Scharmützelsee (mean depth: 9 m, retention time: 16 yr) of the period 1994-2006 we hypothesize that submerged macrophytes may influence transparency and trophic state in deep lakes. The lake was characterized by summer epilimnion TP concentrations of 38 to 57 mug L(-1), turbid water due to mass development of cyanobacteria, and low abundance of few submerged macrophyte species until 2003. Thereafter, a sudden increase in water transparency was followed by a rapid submerged macrophyte colonization of the littoral down to about 5 m depth corresponding to the depth of a light supply of 3 E m(-2) d(-1). Initially, this recolonization was probably a consequence of decreased turbidity. We argue that the increase of submerged macrophyte coverage from < 10% in 1994 to 2003 to about 24% in 2005-2006 has contributed to the stabilization of the clear-water regime during the subsequent years. This is supported by the fact that earlier shifts to clear-water regimes in 1994 and 2000 without a significant spread of submerged macrophytes were not stable. We discuss potential mechanisms that may have resulted in a positive effect of plants on transparency such as P uptake and immobilization by the dominant rootless macrophyte species Nitellopsis obtusa and Ceratophyllum demersum and other macrophyte-related mechanisms such as increased zooplankton grazing and allelopathy.

Causal relationships of Raphidiopsis (formerly Cylindrospermopsis) dynamics with water temperature and N:P-ratios: A meta-analysis across lakes with different climates based on inferential modelling.

Raphidiopsis raciborskii is a tropical toxic cyanobacterium that is rapidly expanding to diverse lake habitats in different climate zones by sophisticated adaptation mechanisms. This meta-analysis investigated correlations of R. raciborskii with water temperature and N:P (nitrogen to phosphorus)-ratios across four lakes with different climates and trophic states by means of long-term time series and the hybrid evolutionary algorithm HEA. The results have shown that in the lakes with temperate and Mediterranean climate, R. raciborskii is strongly correlated with water temperature since germination and growth rely on rising water temperatures in spring. In contrast, there was a weaker correlation with water temperature in subtropical and tropical lakes where pelagic populations of R. raciborskii are overwintering, and are present all year round. However, the highest abundances of R. raciborskii coincided with highest water temperature for the Mediterranean, subtropical and tropical lakes, whilst in the temperate Langer See the highest abundances of R. raciborskii occurred at 24.1 °C, even though temperatures of up to 27 °C were recorded in 2013 and 2014. The correlation of R. raciborskii with N:P-ratios proved to be strongest for the meso- to eutrophic Lake Kinneret (r2 = 0.8) and lowest for the eutrophic Lake Paranoa (r2 = 0.16). However, the assumption has been confirmed that R. raciborskii is growing fastest when waters are N-limited regardless of trophic states. In terms of phenology, the temperate and Mediterranean lakes displayed "fastest growth" in spring and early summer. In contrast, the growing season in subtropical and tropical lakes lasted from spring to autumn most likely because of overwintering populations, and growing importance of direct and indirect biotic regulating factors such as competition, grazing, remineralisation of nutrients along warming climate. In order to carry out a meta-analysis of time series across four different lakes, HEA served as powerful tool resulting in inferential models with predictive capacity for population dynamics of R. raciborskii just driven by water temperature or N:P-ratios, whilst coefficients of determination r2 served as criteria for hypotheses testing.

Seasonal dynamics of cylindrospermopsin and cyanobacteria in two German lakes.

Cylindrospermopsin (CYN) is a potent hepatotoxin produced by different cyanobacteria of the order Nostocales. Questions of major concern are: which species produce CYN, which are the seasonal patterns of CYN dynamics and how are they regulated? Therefore, we studied for the first time the seasonal dynamics of particulate and dissolved CYN concentrations, cyanobacterial abundance and environmental factors in two German lakes over 2 years. Total CYN reached maximum concentrations of 0.34 and 1.80 microg L(-1) in Melangsee and Langer See, respectively. In both lakes, maxima of the dissolved CYN fraction occurred later in the season than those of the particulate fraction, and it reached higher concentrations. This indicates that CYN is poorly decomposed and accumulates in the water. The cyanobacterial community in both lakes included several potentially CYN-producing species that did not correlate with CYN concentrations. Significant correlations between the particulate CYN concentrations and species biovolume were only found for Aphanizomenon gracile (r(s)=0.803) in Langer See indicating that this species is a CYN producer. Different correlations of CYN with abiotic factors in the two lakes indicate the presence of further undetected CYN producers as well as different regulation mechanisms of their dynamics and the variability of CYN.

Response of Submerged Macrophyte Communities to External and Internal Restoration Measures in North Temperate Shallow Lakes.

Submerged macrophytes play a key role in north temperate shallow lakes by stabilizing clear-water conditions. Eutrophication has resulted in macrophyte loss and shifts to turbid conditions in many lakes. Considerable efforts have been devoted to shallow lake restoration in many countries, but long-term success depends on a stable recovery of submerged macrophytes. However, recovery patterns vary widely and remain to be fully understood. We hypothesize that reduced external nutrient loading leads to an intermediate recovery state with clear spring and turbid summer conditions similar to the pattern described for eutrophication. In contrast, lake internal restoration measures can result in transient clear-water conditions both in spring and summer and reversals to turbid conditions. Furthermore, we hypothesize that these contrasting restoration measures result in different macrophyte species composition, with added implications for seasonal dynamics due to differences in plant traits. To test these hypotheses, we analyzed data on water quality and submerged macrophytes from 49 north temperate shallow lakes that were in a turbid state and subjected to restoration measures. To study the dynamics of macrophytes during nutrient load reduction, we adapted the ecosystem model PCLake. Our survey and model simulations revealed the existence of an intermediate recovery state upon reduced external nutrient loading, characterized by spring clear-water phases and turbid summers, whereas internal lake restoration measures often resulted in clear-water conditions in spring and summer with returns to turbid conditions after some years. External and internal lake restoration measures resulted in different macrophyte communities. The intermediate recovery state following reduced nutrient loading is characterized by a few macrophyte species (mainly pondweeds) that can resist wave action allowing survival in shallow areas, germinate early in spring, have energy-rich vegetative propagules facilitating rapid initial growth and that can complete their life cycle by early summer. Later in the growing season these plants are, according to our simulations, outcompeted by periphyton, leading to late-summer phytoplankton blooms. Internal lake restoration measures often coincide with a rapid but transient colonization by hornworts, waterweeds or charophytes. Stable clear-water conditions and a diverse macrophyte flora only occurred decades after external nutrient load reduction or when measures were combined.

Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes.

The cyanobacterial toxin cylindrospermopsin (CYN) is widely distributed in German lakes, but volumetric data for risk assessment are lacking and it is unclear which cyanobacterial species produce CYN in Europe. We therefore analyzed CYN concentration and cyanobacterial composition of 21 German lakes in 2005. CYN was detected in 19 lakes (102 of 115 samples). In total, 45 samples contained particulate CYN only, and 57 contained both dissolved and particulate CYN. The concentrations were 0.002-0.484 microg L(-1) for particulate CYN and 0.08-11.75 microg L(-1) for dissolved CYN with a maximum of 12.1 microg L(-1) total CYN. A drinking water guideline value of 1 microg L(-1) proposed by Humpage and Falconer [2003. Oral toxicity of the cyanobacterial toxin CYN in male Swiss albino mice: determination of no observed adverse effect level for deriving a drinking water guideline value. Environ. Toxicol. 18, 94-103] was exceeded in 18 samples from eight lakes due to high concentrations of dissolved CYN. CYN occurrence in the German lakes could not be ascribed to the three known CYN-producing species Cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon flos-aquae, which were detected in some lakes in low abundances. The highest correlation coefficients were observed between particulate CYN and the native Aphanizomenon gracile. It occurred in 98 CYN-positive samples, was the most abundant Nostocales and was the only Nostocales in five samples. This indicates that A. gracile is a potential CYN producer in German lakes.

Seasonal patterns of nitrogen and phosphorus limitation in four German lakes and the predictability of limitation status from ambient nutrient concentrations.

To identify the seasonal pattern of nitrogen (N) and phosphorus (P) limitation of phytoplankton in four different lakes, biweekly experiments were conducted from the end of March to September 2011. Lake water samples were enriched with N, P or both nutrients and incubated under two different light intensities. Chlorophyll a fluorescence (Chla) was measured and a model selection procedure was used to assign bioassay outcomes to different limitation categories. N and P were both limiting at some point. For the shallow lakes there was a trend from P limitation in spring to N or light limitation later in the year, while the deep lake remained predominantly P limited. To determine the ability of in-lake N:P ratios to predict the relative strength of N vs. P limitation, three separate regression models were fit with the log-transformed ratio of Chla of the P and N treatments (Response ratio = RR) as the response variable and those of ambient total phosphorus:total nitrogen (TN:TP), dissolved inorganic nitrogen:soluble reactive phosphorus (DIN:SRP), TN:SRP and DIN:TP mass ratios as predictors. All four N:P ratios had significant positive relationships with RR, such that high N:P ratios were associated with P limitation and low N:P ratios with N limitation. The TN:TP and DIN:TP ratios performed better than the DIN:SRP and TN:SRP in terms of misclassification rate and the DIN:TP ratio had the highest R2 value. Nitrogen limitation was predictable, frequent and persistent, suggesting that nitrogen reduction could play a role in water quality management. However, there is still uncertainty about the efficacy of N restriction to control populations of N2 fixing cyanobacteria.

A CARD-FISH protocol for the identification and enumeration of cyanobacterial akinetes in lake sediments.

Akinetes are the dormant cells of Nostocales (cyanobacteria) that enable the organisms to survive harsh environmental conditions while resting in bottom sediments. The germination of akinetes assists the dispersal and persistence of the species. The assessment of the akinete pool in lake sediments is essential to predict the bloom formation of the Nostocales population. We present here the implementation of an improved catalysed reporter deposition (CARD)-fluorescence in situ hybridization (FISH) protocol to assist the identification and quantification of akinetes in sediment samples. Several 16S rRNA gene oligonucleotide probes were evaluated for labelling akinetes of various species of Anabaena, Aphanizomenon and Cylindrospermopsis. Akinetes of all the taxa studied were successfully labelled and could be easily detected by their bright fluorescence signal. The probes' specificity was tested with 32 strains of different taxa. All six Cylindrospermopsis raciborskii strains were labelled with a specific probe for its 16S rRNA gene. A more general probe labelled 73% of the Anabaena and Aphanizomenon strains. The counting data of field samples obtained with CARD-FISH and the regular light microscopy approach did not differ significantly, confirming the suitability of both methods. The CARD-FISH approach was found to be less time-consuming because of better visibility of akinetes.

Cyanobacteria and cyanotoxins: the influence of nitrogen versus phosphorus.

The importance of nitrogen (N) versus phosphorus (P) in explaining total cyanobacterial biovolume, the biovolume of specific cyanobacterial taxa, and the incidence of cyanotoxins was determined for 102 north German lakes, using methods to separate the effects of joint variation in N and P concentration from those of differential variation in N versus P. While the positive relationship between total cyanobacteria biovolume and P concentration disappeared at high P concentrations, cyanobacteria biovolume increased continually with N concentration, indicating potential N limitation in highly P enriched lakes. The biovolumes of all cyanobacterial taxa were higher in lakes with above average joint NP concentrations, although the relative biovolumes of some Nostocales were higher in less enriched lakes. Taxa were found to have diverse responses to differential N versus P concentration, and the differences between taxa were not consistent with the hypothesis that potentially N(2)-fixing Nostocales taxa would be favoured in low N relative to P conditions. In particular Aphanizomenon gracile and the subtropical invasive species Cylindrospermopsis raciborskii often reached their highest biovolumes in lakes with high nitrogen relative to phosphorus concentration. Concentrations of all cyanotoxin groups increased with increasing TP and TN, congruent with the biovolumes of their likely producers. Microcystin concentration was strongly correlated with the biovolume of Planktothrix agardhii but concentrations of anatoxin, cylindrospermopsin and paralytic shellfish poison were not strongly related to any individual taxa. Cyanobacteria should not be treated as a single group when considering the potential effects of changes in nutrient loading on phytoplankton community structure and neither should the N(2)-fixing Nostocales. This is of particular importance when considering the occurrence of cyanotoxins, as the two most abundant potentially toxin producing Nostocales in our study were found in lakes with high N relative to P enrichment.

Climate change affects timing and size of populations of an invasive cyanobacterium in temperate regions.

Cylindrospermopsis raciborskii, an invasive freshwater cyanobacterium, originated from the tropics but has spread to temperate zones over the last few decades. Its northernmost populations in Europe occur in North German lakes. How such dramatic changes in its biogeography are possible and how its population dynamics in the newly invaded habitats are regulated are still unexplained. We therefore conducted a long-term (1993-2005) study of two German lakes to elucidate the mechanisms behind C. raciborskii population dynamics and to identify the abiotic constraints on its development. Our data revealed that pelagic populations of C. raciborskii thrived for three months during the summer, contributing up to 23% of the total cyanobacteria biovolume. Population sizes varied greatly between years without exhibiting any distinct long-term trends. In the annual lifecycle, C. raciborskii filaments emerged in the pelagic habitat when the temperature rose above 15-17 degrees C. At that time, mean photosynthetically active radiation in the mixed water column (I (mix)) overstepped its maximum. Rates of population net increase were highest at the beginning of the season (0.15-0.28 day(-1)), declined continuously over time, and were significantly positively correlated with I (mix). This indicates that the onset of the pelagic population is temperature-mediated and that I (mix) controls its growth. Since I (mix) peaks before the population onset, the time of germination is of crucial importance for successful development. To test this hypothesis, we designed a model to simulate pelagic population size, starting at different dates in the annual cycle. Moving the population onset forward by 30 days resulted in a doubling of the population size. We therefore conclude that an earlier rise in water temperature associated with climate change has promoted the spread of C. raciborskii to the temperate zone. Earlier warming permits earlier germination, thereby shifting the pelagic populations to a phase with higher I (mix), which advances growth and the population establishment.

Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany.

The frequent occurrence of the cyanobacterial toxin cylindrospermopsin (CYN) in the (sub)tropics has been largely associated with cyanobacteria of the order Nostocales of tropical origin, in particular Cylindrospermopsis raciborskii. C. raciborskii is currently observed to spread northwards into temperate climatic zones. In addition, further cyanobacteria of the order Nostocales typically inhabiting water bodies in temperate regions are being identified as CYN-producers. Therefore, data on the distribution of CYN in temperate regions are necessary for a first assessment of potential risks due to CYN in water used for drinking and recreation. A total of 127 lakes situated in the north-eastern part of Germany were investigated in 2004 for the presence of the toxin CYN and the phytoplankton composition. The toxin could be detected in half of the lakes (n = 63) and in half of 165 samples (n = 88). Concentrations reached up to 73.2 microg CYN/g DW. CYN thus proved more widely distributed than previously demonstrated. The analyses of phytoplankton data suggest Aphanizomenon sp. and Anabaena sp. as important CYN producers in Germany, and confirm recent findings of Aphanizomenon flos-aquae as CYN-producing species frequently inhabiting water bodies in temperate climatic regions. The data shown here suggest that CYN may be an important cyanobacterial toxin in German water bodies and that further data are needed to assess this.