Changes to the phytoplankton assemblage of Lake Kinneret after decades of a predictable, repetitive pattern

1. Phytoplankton abundance and species composition in Lake Kinneret, Israel, have been monitored at weekly or fortnightly intervals since 1969. This paper summarises the resulting 34‐year phytoplankton record with a focus on the last 13 years of new data, and reassesses an earlier conclusion that the lake phytoplankton shows remarkable stability despite a wide range of external pressures. 2. The Kinneret phytoplankton record can be split into two major periods. The first, from 1969 till 1993, was a period of distinct stability expressed by a typical annual pattern revolving around a spring bloom of the dinoflagellate Peridinium gatunense that repeated each year. The second period, starting around 1994 and ongoing, is characterised by the loss of the previously predictable annual pattern, with both ‘bloom years’ and ‘no‐bloom years’. 3. In the second period, deviations from the previous annual pattern include: the absence of the prevailing spring P. gatunense blooms in some years and increased variability in the magnitude of the bloom in others; intensification of winter Aulacoseira granulata blooms; higher summer phytoplankton biomass with replacement of mostly nanoplanktonic, palatable forms by less palatable forms; new appearance and establishment of toxin‐producing, nitrogen fixing cyanobacteria in summer; increase in the absolute biomass and percentage contribution of cyanobacteria to total biomass; and fungal epidemics attacking P. gatunense. 4. The 34‐year record serves to validate Schindler's (1987) assessment that phytoplankton species composition will respond to increased anthropogenic stress before bulk ecosystem parameters.     

Present–absent: a chronicle of the dinoflagellate Peridinium gatunense from Lake Kinneret

A long-term record dating back to the 1960s indicates that Peridinium gatunense, an armored dinoflagellate, dominated the phytoplankton of Lake Kinneret (Sea of Galilee, Israel) until the mid-1990s, with a relatively stable spring bloom. However, since 1996, these blooms became irregular, failing to develop in 10 out of the past 16 years. During the later period, a significant correlation (R ² = 0.605, P = 0.013) was found between annual peak P. gatunense biomass and riverine inflow volume. In-lake surveys showed that patches of high P. gatunense densities were associated with water enriched with fresher inflowing Jordan River water. Supplementing laboratory cultures of P. gatunense with Hula Valley water stimulated its growth relative to un-enriched controls. A likely explanation to the recent irregular blooms of this dinoflagellate is a hydrological modification that was made in the catchment in the mid-1990s, preventing Hula Valley water from reaching Lake Kinneret in most years—except for exceptionally wet years. We propose that until the mid-1990s, the Jordan River water enriched Lake Kinneret with a growth factor (a microelement and/or organic compound) originating in the Hula Valley, which in recent years has arrived in sufficient quantities to support a bloom only in high-rainfall years.     

Stable patterns in size structure of a phytoplankton species of Lake Kinneret

The aim of the study was a search for typical structure patterns of phytoplankton assemblages, based on the long-term dynamics analysis. As a test case we used the interannual phytoplankton variability of Lake Kinneret (Israel). The dominant phytoplankton species (Peridinium gatunense) structure was presented as the frequency-weighted taxonomic size spectrum (TSS) which describes the size distribution of the operational taxonomic unit (OTUj) occurrence frequencies. Using 24 years monitoring data, the TSS annual patterns of P. gatunense were compared. Typical persistent TSS patterns were evident even during years of pronounced deviations from the typical patterns of phytoplankton biomass dynamics and species composition. By correlation analysis, hierarchical cluster analysis and ANOVA the TSS variability was quantified and compared. While the TSS general shape was almost constant, its amplitude variations allowed us to distinguish between three levels of annual bloom intensity. Electronic Supplementary Material Supplementary material is available for this article at and accessible for authorised users     

The effects of oils and oil components on algae: A review

Plate structure analysis of the bloom-forming Peridinium of Lake Kinneret (previously identified as P. cinctum fa. westii) established its identity as P. gatunense. Peridinium cinctum was not observed. Material from different years and periods of the bloom, as well as specimens from cultures and P. gatunense from Lago Cristalino (Brazil), were studied using light and scanning electron microscopy. Peridinium gatunense from Lake Kinneret showed slight differences of the plate pattern as compared with specimens from other localities.     

Sulphate reduction in the hypolimnion and sediments of Lake Kinneret, Israel

1. Lake Kinneret is a warm (13–30°C) monomictic lake. Between January and June a heavy annual bloom of the dinoflagellate Peridinium gatunense dominates phytoplankton biomass (250 g m^?2). At the beginning of the summer, degradation and decomposition of the Peridinium biomass occurs, serving as a trigger for intense sulphate reduction in the hypolimnion and sediments. 2. The rates of sulphate reduction in the sediments varied seasonally from 12 to 1700 nmol SO₄.^?2 reduced cm^?3 day^?1 in December and July, respectively. The availability of organic matter and sulphate is high in June after the crash of the Peridinium bloom and the beginning of stratification and is lowest in December before overturn. 3. Sulphate concentrations in the hypolimnion range between 0.52 mM and 0.20 mM during mixing (January-April) and before overturn (December), respectively. The depletion in sulphate in the hypolimnion is stoichiometrically correlated to the increase in sulphide. The lake is not depleted of sulphate at any time, so the sulphate reduction process in Lake Kinneret is not limited by sulphate concentrations except in the sediments just before overturn.     

PHOSPHORUS,NITROGEN AND THE GROWTH OF ALGAE IN LAKE KINNERET1

The intracellular concentrations of carbon, nitrogen, phosphorus and chlorophyll a of phytoplankton and zooplankton in Lake Kinneret were determined from 1969 to 1973. The ratios C:P, C:N, chlorophyll a:P, chlorophyll a:N of the algae showed fluctuations which could be related to the nutrient conditions that influence the annual pattern of phytoplankton development, especially in respect to the dinoflagellate bloom of Peridinium cinctum (OFM) Ehr. f. westii (Lemm.) Lef. Relatively high intracellurar P values at the start of the bloom indicated adequate availability of this nutrient and luxury consumption over a short period of time. Later, Peridinium continued to grow despite unusually high C:P ratios (> 300:1). In most years, phosphorus may have eventually limited growth, however, in 1970, the bloom censed despite comparatively high intracellular P concentrations. These observations, together with supplementary evidence from nutrient addition experiments and determinations of specific alkaline phosphatase levels, indicated that, for most of the growth phase of the bloom, Peridinium cells were not directly limited by P. The decline of the bloom usually, but not always (e.g., in 1970), was marked by very high C:P ratios. Thus, a shortage of P may often be a contributory factor to the cessation of the Peridinium bloom and may be limiting phytoplankton growth in the fall. Over the years 1969–73, possibly due to an overall drop in salinity, there appears to be a trend to lower levels of biologically bound phosphorus in Lake Kinneret, without a concomitant decrease in carbon biomass.     

Encystment of Peridinium gatunense: occurrence, favourable environmental conditions and its role in the dinoflagellate life cycle in a subtropical lake

1. The abundance of cysts of the bloom‐forming dinoflagellate Peridinium gatunense in the sediments of Lake Kinneret and the effects of environmental conditions on encystment were studied in relation to bloom dynamics. Peak cyst formation coincided with the highest growth rate of the population, prior to bloom peak. 2. Peridinium cysts were counted in water and sediment corer samples from 2000 to 2003 and in archived sediment trap samples collected during 1993–94. The cyst data were examined in relation to ambient temperature and nutrient records, and revealed no direct correlation. 3. In laboratory encystment experiments with Peridinium cells collected from the lake, 0.2–3% of the vegetative cells encysted. Temperature, light and cell density had no significant effect on the percentage of encystment. 4. Cysts were always present in the lake sediments but their abundance in ‘non Peridinium’ years was much lower than after a massive bloom. Vegetative cells were always present in the water column after the collapse of the annual dinoflagellate bloom, potentially serving as the inoculum for the next bloom. We propose that the hardy cysts serve as an emergency ‘gene bank’ to initiate population build up following catastrophic die outs.     

Responses of Phyto- and Zooplankton Communities to Prymnesium polylepis (Prymnesiales) Bloom in the Baltic Sea

A large bloom of Prymnesium polylepis occurred in the Baltic Sea during the winter 2007 – spring 2008. Based on numerous reports of strong allelopathic effects on phytoplankton exerted by P. polylepis and its toxicity to grazers, we hypothesized that during this period negative correlations will be observed between P. polylepis and (1) main phytoplankton groups contributing to the spring bloom (i.e., diatoms and dinoflagellates), and (2) zooplankton growth and abundance. To test these hypotheses, we analyzed inter-annual variability in phytoplankton and zooplankton dynamics as well as growth indices (RNA∶DNA ratio) in dominant zooplankton in relation to the Prymnesium abundance and biomass. Contrary to the hypothesized relationships, no measurable negative responses to P. polylepis were observed for either the total phytoplankton stocks or the zooplankton community. The only negative response, possibly associated with P. polylepis occurrence, was significantly lower abundance of dinoflagellates both during and after the bloom in 2008. Moreover, contrary to the expected negative effects, there were significantly higher total phytoplankton abundance as well as significantly higher winter abundance and winter-spring RNA∶DNA ratio in dominant zooplankton species in 2008, indicating that P. polylepis bloom coincided with favourable feeding conditions for zooplankton. Thus, primary consumers, and consequently also zooplanktivores (e.g., larval fish and mysids), may benefit from haptophyte blooms, particularly in winter, when phytoplankton is scarce.     

Seasonal variation in the biochemical composition of particulate material collected by sediment traps at Signy Island, Antarctica

Particulate material recovered over an 18-month period from sediment traps deployed at a shallow-water nearshore Antarctic site was analysed for photosynthetic pigments, aliphatic hydrocarbons and fatty acids. All components showed a distinct seasonal variation, with high recovery rates during the summer open-water phytoplankton bloom and low rates under winter fast ice. The amount of trapped material differed between the two summers, indicating inter-annual variability of vertical flux associated with differences in the intensity of the summer phytoplankton bloom. Particulate material trapped in summer was dominated by that which originated in diatoms. High recoveries of chlorophyll a, fucoxanthin, n-C_21:6 hydrocarbon, 20:5(n-3) fatty acid and shorter chain (C₁₅–C₂₄) aliphatic hydrocarbons all pointed to a significant summer flux of ungrazed diatoms. There were, however, also signals of zooplankton grazing activity (notably pyrophaeophorbide a), and the presence of C18:4(n-3) and C22:6(n-3) fatty acids suggested a small flux of material from flagellates and other sources. Longer chain n-alkanes (C₂₅–C₃₄) indicative of nanoplankton were detected all year, but there was no significant deposition of zooplankton material in any sample. The major recovery rate of photosynthetic pigments was in late summer (February to April), and the major grazing signal occurred after the peak of the summer diatom bloom. Most of the diatom bloom appeared to settle out from the water column without being grazed. The major seasonal contrast in the biochemistry of the trapped material was the dominance of the diatom signature in summer, and in winter the predominance (but at much lower recovery rates) of material from nanoplankton. Received: 2 March 1998 / Accepted: 12 June 1998     

RESPONSE OF CATALASE ACTIVITY TO ENVIRONMENTAL STRESS IN THE FRESHWATER DINOFLAGELLATE PERIDINIUM GATUNENSE1

Catalase activity increased in Peridinium gatunense (formerly P. cinctum fa. westii) cells during the decline of the seasonal spring bloom period in Lake Kinneret. This was correlated with the low ambient total CO₂ concentration. The relationship was confirmed in laboratory experiments where maximum catalase activity occurred under an atmosphere composed of 30% O₂ and 0.003% CO₂. Conversely, high CO₂ concentrations inhibited catalase activity. The rise in catalase activity was not directly due to increasing environmental pH, as in vitro and in vivo measurements showed a characteristic broad pH curve with a constant activity from pH 6–10 for catalase. Photoinhibition of catalase occurred above 250 μmol photons · m^?2· s^?1. However, at high photoinactivating irradiances, photoinhibition was ameliorated under high pO₂/pCO₂. Such conditions prevail in the Kinneret at the end of the spring. We propose that the enhancement of photorespiration (under high pO₂/pCO₂) induces a temporary burst in catalase activity despite the progressively photoinhibitory conditions of early summer.     

Sulfate reduction processes in sediments at different sites in Lake Kinneret,Israel

Lake Kinneret, Israel, is a warm (13–30°C) monomictic lake that stratifies in April and turns over in December. Between January and June each year, a heavy bloom (up to 250 g wet weight n^–2 2) of the dinoflagellate Peridinium gatunense dominates the phytoplankton biomass. In early summer, the bloom collapses, and the sinking Peridinium biomass serves as a trigger for intense sulfate-reduction activity throughout the hypolimnion and within the sediments. The availability of organic matter and sulfate was high shortly after the bloom crash and the beginning of stratification and was lowest in December before overturn. Sulfate-reduction rates at three different sites in the lake were studied. In the sediments, the rates varied seasonally and among stations from 5 to 1600 nmol SO₄ ^–2 reduced cm^–3 day^–1, with respect to the distance from the Jordan River, depth, organic content, and stratification period. During years of low lake water levels, intense sulfate reduction occurred in the hypolimnion, resulting in anoxia and high concentrations of H₂S (>400 m). In years with high water levels, early bloom, and delayed stratification, higher rates of sulfate reduction were recorded in the sediments, probably as a result of a greater fraction of the primary production (organic matter) reaching the bottom. Correspondence to: O. Hadas.     

Quantifying Ecological Stability: From Community to the Lake Ecosystem

We performed a methodological study aimed at extending our previously developed approach to quantify the ecological stability of biotic communities and an entire ecosystem, using Lake Kinneret as a case study. The ecological stability of the biotic communities (phytoplankton and zooplankton) of Lake Kinneret was estimated using two different aggregating schemes. The first scheme used the combined stability index, based on the combined indices of the individual phytoplankton (SI[Comb]_P) and zooplankton (SI[Comb]_Z) taxonomic groups. The total community stability index was calculated based on the total abundances of these communities. The stability of the entire ecosystem was estimated for two sets of ecosystem state variables, a lake “trophic state” set and a “water quality” set, which provided considerably different estimates of the lake ecosystem stability. Good agreement between the results of this study and qualitative estimates of Lake Kinneret stability validates the suitability of this approach to estimate the stability of different ecological units.     

Phytoplankton associations in a small hypertrophic fishpond in East Hungary during a change from bottom-up to top-down control

Phytoplankton species composition and abundance of a shallow hypertrophic fishpond (Mézeshegyi-tó, East Hungary) was studied for the period 1992–1995. The pond showed a pronounced algal periodicity. High-diversity phytoplankton assemblages occurred in spring and autumn. During the winter period, low diversity values were related either to stable community states, when K-strategist species dominated the plankton, or to a large bloom of r-strategist species. In summer, the stable environment led to low-diversity, high-biomass phytoplankton assemblages, dominated by Cylindrospermopsis raciborskii. At this time, the growth conditions for Cylindrospermopsiswere akin to those prevailing in a continuous fermentor. The overwhelming dominance of this species lasted for more than four months, during which time, the phytoplankton resembled that of one in the tropics. In August, 1993, an unsuccessful chemical treatment for reducing the algal bloom succeeded in killing the pond's entire population of fish. The large fish-stock comprised the planktivorous silver carp. Although the summer of 1994 was one of the warmest summers of this century, the expected Cylindrospermopsis bloom failed to develop probably because of a higher grazing pressure by large zooplankton. In spite of the fact that the temporal and spatial pattern of the phytoplankton is influenced principally by bottom-up effects, changes in cascading trophic interactions may also considerably influence the species composition and biomass.     

Sulfte-reduction process in sediments of Lake Kinneret,Israel

Monomictic Lake Kinneret is stratified during summer and autumn, resulting in a hypolimnion rich in H₂S (3–7 mg 1^–1). In winter and spring every year a bloom of dinoflagallate Peridinium gatunense produces an average biomass of 150000 ton wet weight. Part of this biomass sinks to the hypolimnion and sediments where it is decomposed and mineralized, with some of the mineralization due to the activity of sulfate-reducing bacteria (SRB). The sulfate-reduction potential of the upper sediment layer at the deepest part of the lake (42 m) was measured. The activity of the enzyme arylsulfatase was also monitored. Rates of sulfate-reduction ranged from a minimum of 12 nmoles SO_f4 ^p2–-reduced cm^–3 day^–1 in December before lake overturn to a maximum of 1673 nmoles SO_f4 ^p2– reduced cm^–3 day^–1 in July during stratification. These rates are considerably higher than those recorded from other freshwater lakes in the world and are probably limited more by the availability of organic matter than by sulfate concentrations.     

SUPEROXIDE DISMUTASE ACTIVITY IN PERIDINIUM GATUNENSE IN LAKE KINNERET: EFFECT OF LIGHT REGIME AND CARBON DIOXIDE CONCENTRATION1

The activity of superoxide dismutase (EC 1.15.1.1, superoxide: superoxide oxidoreductase) (SOD) was determined in Peridinium gatunense Lemm. under natural and controlled conditions. SOD activity increased toward the end of the spring algal bloom in Lake Kinneret simultaneously with maximal photosynthetic activity and conditions of elevated ambient stress such as high irradiance. Activity staining of native polyacrylamide gel electrophoresis gels of bloom samples showed a similar pattern to the spectrophotometrically measured SOD. Both Mn SOD and CuZn SOD were present, however no Fe SOD was found in Peridinium. One of three isoenzymes of Mn SOD showed marked differential regulation of activity under stress. An increase in the quantity of the 32-kDa Mn SOD polypeptide during the bloom was found to be unrelated to senescence; it was assumed that this polypeptide was induced by stress. Thus, SOD in Peridinium undergoes physiological and molecular acclimation to seasonal environmental changes. When Peridinium was exposed to various O₂ and CO₂ concentrations in culture, CuZn SOD significantly increased under high C0₂ concentrations and normoxic conditions (20% O₂). However, at high irradiances, Peridinium cultures exposed to low and high CO₂ concentrations also had similar CuZn SOD activity. It was concluded that stressful irradiance is the overriding cause of increased SOD activity in both lake samples and in cultures of Peridinium.     

The impact of zooplankton status on the management of Lake Kinneret (Israel)

Monthly averages of standing stock wet biomass of zooplankton in Lake Kinneret (Israel) varied between 11 and 76 g m^–2 during 1969–1981, with the exception of two months. Averaged contributions of different groups were: Cladocera 58%, Copepoda 35% and Rotifera 7%. Total standing crop wet biomass is highest during January–June, averages varied between 35 and 50 g m^–2, and decreases during summer–fall (23–36 g m^–2). The winter biomass of Cladocera fluctuated between 22 and 35 g m^–2 and dropped to a range of 9–23 g m^–2 in summer, whereas copepod biomass varied very little around an average of 18 g (ww) m^–2 with the exception of low values from April to June. The stock biomass of Rotifera is relatively high during winter floods season (December-March) whilst in summer it is very low.Young stages of fish in Lake Kinneret feed mostly on zooplankton and zoobenthic forms. The most abundant fish in the Kinneret ecosystem, Mirogrex terraesanctae terraesanctae, also feed on zooplankton at the adult stage throughout the year, and herbivorous fish consume zooplankton during the summer when lake plankton resources are limited.The summer ecosystem of Lake Kinneret is characterised as a steady state type, in which the impact of the zooplankton-chain is of great importance. Increase of predation pressure on zooplankton by fish can disequilibrate the balanced trophic relations existing between nannoplankton production and zooplankton grazing capacity. Such a situation can lead to organics accumulation as nannoplankton blooms, resulting in water quality deterioration. Management options aimed at preventing collapse of zooplankton populations are discussed.     

Effects of zooplankton grazing and nutrients on the bloom-forming, N2-fixing cyanobacterium Aphanizomenon in Lake Kinneret

A bloom of the filamentous, N₂-fixing cyanobacterium Aphanizomenonovalisporum Forti occurred for the first time in Lake Kinneretduring late summer and fall 1994. During subsequent years (1995–1999),Aphanizomenon also appeared in late summer and fall, but didnot bloom. In outdoor microcosm experiments, we examined zooplanktongrazing on Lake Kinneret phytoplankton, with and without Aphanizomenonpresent, and the effects of N, P and N:P ratios on phytoplanktongrowth. In one-day feeding experiments, clearance and grazingrates of the ambient Lake Kinneret zooplankton assemblage feedingin lake water dominated by Aphanizomenon were 10-fold lowerthan in water without Aphanizomenon. We suspect that the lowgrazing rates were due to interference caused by the presenceof Aphanizomenon. In 9-day nutrient addition experiments, significantenhancement effects on phytoplankton were detected with additionsof either P or N; a high N:P was better for phytoplankton growththan a low N:P. After 7 days, bottles receiving low P and noN additions were dominated by Oscillatoria sp. and Closteriumacutum; few Aphanizomenon were present. In contrast, bottlesreceiving high P and N additions had large increases of Aphanizomenon,as well as Oscillatoria and Closterium. There was a tendencyfor more green algae and diatoms with increasing N additions.These results provide evidence that (i) non-grazeability ofAphanizomenon enabled it to gain a competitive advantage overgrazeable phytoplankton, and (ii) that nutrient limitation,but not grazing, was probably important in the eventual declineof the Aphanizomenon bloom.     

Assimilation of Diazotrophic Nitrogen into Pelagic Food Webs

The fate of diazotrophic nitrogen (N_D) fixed by planktonic cyanobacteria in pelagic food webs remains unresolved, particularly for toxic cyanophytes that are selectively avoided by most herbivorous zooplankton. Current theory suggests that N_D fixed during cyanobacterial blooms can enter planktonic food webs contemporaneously with peak bloom biomass via direct grazing of zooplankton on cyanobacteria or via the uptake of bioavailable N_D (exuded from viable cyanobacterial cells) by palatable phytoplankton or microbial consortia. Alternatively, N_D can enter planktonic food webs post-bloom following the remineralization of bloom detritus. Although the relative contribution of these processes to planktonic nutrient cycles is unknown, we hypothesized that assimilation of bioavailable N_D (e.g., nitrate, ammonium) by palatable phytoplankton and subsequent grazing by zooplankton (either during or after the cyanobacterial bloom) would be the primary pathway by which N_D was incorporated into the planktonic food web. Instead, in situ stable isotope measurements and grazing experiments clearly documented that the assimilation of N_D by zooplankton outpaced assimilation by palatable phytoplankton during a bloom of toxic Nodularia spumigena Mertens. We identified two distinct temporal phases in the trophic transfer of N_D from N. spumigena to the plankton community. The first phase was a highly dynamic transfer of N_D to zooplankton with rates that covaried with bloom biomass while bypassing other phytoplankton taxa; a trophic transfer that we infer was routed through bloom-associated bacteria. The second phase was a slowly accelerating assimilation of the dissolved-N_D pool by phytoplankton that was decoupled from contemporaneous variability in N. spumigena concentrations. These findings provide empirical evidence that N_D can be assimilated and transferred rapidly throughout natural plankton communities and yield insights into the specific processes underlying the propagation of N_D through pelagic food webs.     

Seasonal succession of zooplankton in the north basin of Lake Biwa

To examine the seasonal succession of the entire zooplankton community in Lake Biwa, zooplankton biomass (on an areal basis) and its distribution patterns among crustaceans, rotifers and ciliates were studied in the north basin from April 1997 to June 1998. Seasonal changes in phytoplankton and population dynamics of Daphnia galeata were also examined to assess food condition and predation pressure by fish. From March to November, crustaceans dominated zooplankton biomass, but rotifers and ciliates were dominant from December to February. Among crustaceans, Eodiaptomus japonicus was the most abundant species, followed by D. galeata. Zooplankton biomass increased from January to a peak in early April, just before the spring bloom of phytoplankton, then decreased in mid-April when mortality rate of D. galeata increased. From mid-June, zooplankton increased and maintained a high level until the beginning of November. During this period, both birth and mortality rates of D. galeata were relatively high and a number of rotifer and crustacean species were observed. However, their abundances were very limited except for E. japonicus which likely preys on ciliates and rotifers. In Lake Biwa, food sources other than phytoplankton, such as resuspended organic matter from the sediments, seems to play a crucial role in zooplankton succession from winter to early spring, while zooplankton community seems to be regulated mainly by fish predation from summer to fall.