Eutrophication mediates rapid clonal evolution in Daphnia pulicaria

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Modelling lake cyanobacterial blooms: Disentangling the climate‐driven impacts of changing mixed depth and water temperature

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

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太湖西北湖区2003-2012年间氮磷浓度及浮游植物主要类群变化趋势分析

基于2003-2012年太湖竺山湖和西部沿岸区水体理化指标与浮游植物丰度的逐月监测数据,分析了两个湖区氮磷营养盐状态和浮游植物丰度以及浮游植物主要类群的年际变化趋势及季节变化特征,探讨了浮游植物群落变化与水温及营养盐指标间的关系。结果表明：10年间两个湖区氮磷营养盐浓度总体呈下降趋势,以竺山湖TN、NH₃-N浓度和西部沿岸区NO₃-N浓度下降最为显著;浮游植物丰度总体呈上升趋势,蓝藻在群落结构中日益占据绝对优势;季节变化上,氮营养盐浓度表现为春冬季节高于夏秋季节,TP浓度和浮游植物丰度呈相反的变化趋势。Pearson相关分析显示,水温、NH₃-N浓度和TN/TP是影响蓝藻丰度及其在浮游植物群落中所占比例的主要因素。在温度和营养盐结构的共同作用下,10年间两个湖区蓝藻水华暴发时间逐渐提前,而消退时间逐渐滞后,水华持续时间逐年上升。在全球变暖背景下,太湖水华治理需执行更加严格的氮磷限制阈值,且在重污染的西北湖区控磷依然是关键。     

Top‐down regulation of filamentous cyanobacteria varies among a raptorial versus current feeding copepod across multiple prey generations

1. Although considered a key functional trait, little is known about how zooplankton feeding mode affects top‐down regulation of phytoplankton communities. Indeed, copepods are expected to promote the dominance of toxic phytoplankton by selective removal of their edible competitors; however, empirical evidence comparing the effect among calanoid and cyclopoid copepods is lacking.
2. We compared the top‐down effects of two copepods with contrasting feeding modes—the calanoid Notodiaptomus iheringi (current feeder) and the cyclopoid Thermocyclops decipiens (ambush feeder) — on the relative and absolute biomass of the filamentous cyanobacterium Raphidiopsis raciborskii co‐cultured with the nutritious eukaryotic phytoplankton Cryptomonas obovata in a week‐long laboratory assay.
3. The current feeder had a stronger top‐down effect on the biomass of both prey throughout the experiment, with mass‐specific clearance rates 3–5× higher than ambush feeder. By the end of the experiment, the current feeder significantly reduced cyanobacteria biomass compared to controls while the ambush feeder did not. During the week‐long experiment, the current feeder switched from grazing on edible prey to cyanobacteria as the former became less abundant.
4. Contrary to expectation, neither of the copepod species promoted cyanobacterial dominance by the end of the experiment. This is because both grazers, but especially the current feeder, initially increased but subsequently decreased the relative contribution of cyanobacteria to total phytoplankton biomass. Moreover, both copepods decreased the length of cyanobacteria filaments by c. 70%
5. Current feeders can switch from edible prey to cyanobacteria when the abundance of shortened filaments surpasses the abundance of edible prey. While top‐down regulation of phytoplankton can be stronger for current feeding copepods, ambush feeding copepods can have a significant role during blooms by shortening cyanobacterial filaments. Hence, the broader role of contrasting copepod feeding traits on phytoplankton communities merits further study.

     

Linking biotic interactions and climate change to the success of exotic Daphnia lumholtzi

1. Warmer temperatures may increase cyanobacterial blooms in freshwater ecosystems, yet few ecological studies examine how increases in temperature and cyanobacterial blooms will alter the performance of non‐native species. We evaluated how competitive interactions and interactions between these two drivers of ecological change influence the performance of non‐native species using the native zooplankton Daphnia pulex and the non‐native zooplankton Daphnia lumholtzi as a model system. Based on the literature, we hypothesised that D. lumholtzi would perform best in warmer temperatures and in the presence of cyanobacteria. 2. Laboratory competition experiments showed that in the absence of competitors, growth rates of D. pulex (but not D. lumholtzi) were reduced at higher temperatures and with the cyanobacterial foods Anabaena flos‐aquae and Microcystis aeruginosa. In the presence of competitors, however, D. pulex emerged as the superior resource competitor at both temperatures with cyanobacterial food. We therefore predicted that, if competitive interactions are important to its establishment, D. lumholtzi would perform best in the absence of cyanobacteria in heated environments. 3. As predicted, when both species were introduced at low densities in field mesocosms, D. lumholtzi performed best at high temperatures without added cyanobacteria and worst at ambient temperatures with added cyanobacteria, indicating that competitive interactions are likely to be important for its establishment. 4. Taken together, these studies indicate that, while D. lumholtzi may benefit from increases in temperature, associated increased cyanobacterial blooms may hinder its performance. Thus, our findings underscore the importance of considering biotic interactions such as competition when predicting the future establishment of non‐native species in response to climate warming.     

Effects of plant harvesting and nutrient enrichment on phytoplankton community structure in a shallow urban lake

The utility of shallow water bodies in urban environments is frequently compromised either by dense beds of submerged plants or cyanobacterial blooms associated with nutrient enrichment. Although submerged plants are often harvested to facilitate recreational uses, this activity may alter the phytoplankton community, which in turn, also may restrict the use of the lake. We tested whether (i) plant harvesting reduced the abundance of flagellate algae and increased the abundance of cyanobacteria, and (ii) whether increasing levels of nutrient enrichment caused shifts in the dominance of heterocytous cyanobacteria, non-heterocytous cyanobacteria and Chlorophyta, in a shallow urban lake in Southern Australia as has been observed for shallow Danish lakes in previous studies. These predictions were tested with large (3000 l), replicated mesocosms in a warm, highly productive, shallow lake densely colonised by the submerged angiosperm, Vallisnaria americana Michaux. The heterokont algae, Chlorophyta, Cyanobacteria and Cryptophyta were the most numerous algal divisions in the lake. The Euglenophyta, although uncommon in early summer, became more abundant towards the end of summer. The Dinophyta and Charophyta were rare. The abundance of the heterokont algae and Euglenophyta was significantly reduced by plant harvesting even after plants had partially re-established 18 weeks after initial harvesting. The decline in the Euglenophyta in response to plant harvesting is consistent with earlier findings, that the relative abundance of flagellate algae tends to be greater in the presence of submerged plants. Contrary to our prediction, we found that the Cyanobacteria did not increase in response to plant harvesting, however the response may be altered under higher nutrient levels. Algal responses to nutrient enrichment in the presence of dense V. americana plants generally followed the patterns observed in shallow Danish lakes despite the large differences in climatic conditions. Both studies found that the abundance of heterocytous cyanobacteria declined at higher levels of nutrient enrichment, whereas non-heterocytous cyanobacteria and chlorophytes increased.     

Mesozooplankton and microzooplankton grazing during cyanobacterial blooms in the western basin of Lake Erie

Lake Erie is the most socioeconomically important and productive of the Laurentian (North American) Great Lakes. Since the mid-1990s cyanobacterial blooms dominated primarily by Microcystis have emerged to become annual, late summer events in the western basin of Lake Erie yet the effects of these blooms on food web dynamics and zooplankton grazing are unclear. From 2005 to 2007, grazing rates of cultured (Daphnia pulex) and natural assemblages of mesozooplankton and microzooplankton on five autotrophic populations were quantified during cyanobacterial blooms in western Lake Erie. While all groups of zooplankton grazed on all prey groups investigated, the grazing rates of natural and cultured mesozooplankton were inversely correlated with abundances of potentially toxic cyanobacteria (Microcystis, Anabaena, and Cylindrospermopsis; p < 0.05) while those of the in situ microzooplankton community were not. Microzooplankton grazed more rapidly and consistently on all groups of phytoplankton, including cyanobacteria, compared to both groups of mesozooplankton. Cyanobacteria displayed more rapid intrinsic cellular growth rates than other phytoplankton groups under enhanced nutrient concentrations suggesting that future nutrient loading to Lake Erie could exacerbate cyanobacterial blooms. In sum, while grazing rates of mesozooplankton are slowed by cyanobacterial blooms in the western basin of Lake Erie, microzooplankton are likely to play an important role in the top-down control of these blooms; this control could be weakened by any future increases in nutrient loads to Lake Erie.     

Background nutrient concentration determines phytoplankton bloom response to marine heatwaves

Ocean temperature extreme events such as marine heatwaves are expected to intensify in coming decades due to anthropogenic global warming. Reported ecological and economic impacts of marine heatwaves include coral bleaching, local extinction of mangrove and kelp forests and elevated mortalities of invertebrates, fishes, seabirds and marine mammals. In contrast, little is known about the impacts of marine heatwaves on microbes that regulate biogeochemical processes in the ocean. Here we analyse the daily output of a near‐global ocean physical–biogeochemical model simulation to characterize the impacts of marine heatwaves on phytoplankton blooms in 23 tropical and temperate oceanographic regions from 1992 to 2014. The results reveal regionally coherent anomalies of shallower surface mixing layers and lower surface nitrate concentrations during marine heatwaves. These anomalies exert counteracting effects on phytoplankton growth through light and nutrient limitation. Consequently, the responses of phytoplankton blooms are mixed, but can be related to the background nutrient conditions of the study regions. The blooms are weaker during marine heatwaves in nutrient‐poor waters, whereas in nutrient‐rich waters, the heatwave blooms are stronger. The corresponding analyses of sea‐surface temperature, chlorophyll a and nitrate based on satellite observations and in situ climatology support this relationship between phytoplankton bloom anomalies and background nitrate concentration. Given that nutrient‐poor waters are projected to expand globally in the 21st century, this study suggests increased occurrence of weaker blooms during marine heatwaves in coming decades, with implications for higher trophic levels and biogeochemical cycling of key elements.     

Cyanobacterial blooms in a temperate river-floodplain ecosystem: the importance of hydrological extremes

In the past decade, extreme hydrological events were expressed with extreme droughts and floods in temperate regions. The aim of this paper is to explain how such changes in hydrology can influence cyanobacterial populations in floodplain ecosystems. We therefore analyzed a 6-year (2003–2008) study of the phytoplankton in the Kopački Rit floodplain, one of the largest natural floodplains in the middle section of the Danube River (Europe). During the studied period, the shallow floodplain lake shifted between a state of turbid water, characterized by high phytoplankton biomass and regular appearance of cyanobacteria blooms, to a state of clear water with very low phytoplankton biomass and absence of cyanobacteria, and back to the turbid state. Apparently, the major forces driving the cyclic shift were closely related to extremely high and long-lasting flood events. Significant increase in water level, low hydraulic residence time of water, decrease in transparency and low-light climate, together with mass developed aquatic macrophyte vegetation in the whole inundated floodplain were unfavorable conditions for growth and proliferation of cyanobacteria. With the establishment of the flood regime characterized by long-lasting periods without flooding, in-lake processes prevailed leading to cyanobacterial bloom. The most successful were filamentous non-N-fixing cyanobacteria tolerant to mixed and low-light conditions (Planktothrix and Limnothrix) and invasive species Cylindrospermopsis raciborskii. Their massive development led to the establishment of a phytoplankton steady state. All our results demonstrate that the altered intensity and frequency of flood events will have pronounced effects on the appearance of cyanobacterial blooms and generally on alternative stable states in the floodplain. Relating to this, management objectives should be focused on qualifications of changes in hydrology and projecting those effects for potential floodplain restoration.     

Predicting cyanobacterial dynamics in the face of global change: the importance of scale and environmental context

There is growing concern that harmful cyanobacterial blooms are increasing in frequency and occurrence around the world. Although nutrient enrichment is commonly identified as a key predictor of cyanobacterial abundance and dominance in freshwaters, several studies have shown that variables related to climate change can also play an important role. Based on our analysis of the literature, we hypothesized that temperature or water‐column stability will be the primary drivers of cyanobacterial abundance in stratified lakes whereas nutrients will be the stronger predictors in frequently mixing water bodies. To test this hypothesis, as well as quantify the drivers of cyanobacteria over different scales and identify interactions between nutrients and climate‐related variables, we applied linear and nonlinear mixed‐effect modeling techniques to seasonal time‐series data from multiple lakes. We first compared time series of cyanobacterial dominance to a published lake survey and found that the models were similar. Using time‐series data of cyanobacterial biomass, we identified important interactions among nutrients and climate‐related variables; dimictic basin experienced a heightened susceptibility to cyanobacterial blooms under stratified eutrophic conditions, whereas polymictic basins were less sensitive to changes in temperature or stratification. Overall, our results show that due to predictable interactions among nutrients and temperature, polymictic and dimictic lakes are expected to respond differently to future climate warming and eutrophication.     

Positive selection of digestive proteases in Daphnia: A mechanism for local adaptation to cyanobacterial protease inhibitors

Due to the combined effects of global warming and eutrophication, the frequency of deleterious cyanobacterial blooms in freshwater ecosystems has increased. In line with this, local adaptation of the aquatic keystone herbivore Daphnia to cyanobacteria has received major attention. Besides microcystins, the most frequent cyanobacterial secondary metabolites in such blooms are protease inhibitors (PIs). Recently, it has been shown that a protease gene showed copy number variation between four D. magna populations that differed in tolerance to PIs. From that study, we chose two distinct populations of D. magna which had or had not coexisted with cyanobacteria in the past. By calculating F_ST values, we found that the two populations were genetically more distant in the protease loci than in neutral loci. Population genetic tests applied to the tolerant population revealed that positive selection was most probably acting on the gene loci of the digestive protease CT448 and CT802. We conclude that the selection of digestive proteases and subsequent reduction in copy number is the molecular basis of evolutionary changes leading to local adaptation to PIs.     

Asynchronous onset of eutrophication among shallow prairie lakes of the Northern Great Plains,Alberta, Canada

Coherent timing of agricultural expansion, fertilizer application, atmospheric nutrient deposition, and accelerated global warming is expected to promote synchronous fertilization of regional surface waters and coherent development of algal blooms and lake eutrophication. While broad‐scale cyanobacterial expansion is evident in global meta‐analyses, little is known of whether lakes in discrete catchments within a common lake district also exhibit coherent water quality degradation through anthropogenic forcing. Consequently, the primary goal of this study was to determine whether agricultural development since ca. 1900, accelerated use of fertilizer since 1960, atmospheric deposition of reactive N, or regional climate warming has resulted in coherent patterns of eutrophication of surface waters in southern Alberta, Canada. Unexpectedly, analysis of sedimentary pigments as an index of changes in total algal abundance since ca. 1850 revealed that while total algal abundance (as β‐carotene, pheophytin a) increased in nine of 10 lakes over 150 years, the onset of eutrophication varied by a century and was asynchronous across basins. Similarly, analysis of temporal sequences with least‐squares regression revealed that the relative abundance of cyanobacteria (echinenone) either decreased or did not change significantly in eight of the lakes since ca. 1850, whereas purple sulfur bacteria (as okenone) increased significantly in seven study sites. These patterns are consistent with the catchment filter hypothesis, which posits that lakes exhibit unique responses to common forcing associated with the influx of mass as water, nutrients, or particles.     

Strong spatial differentiation of N and P deficiency,primary productivity and community composition between Nyanza Gulf and Lake Victoria (Kenya,East Africa) and the implications for nutrient management

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Water temperature and stratification depth independently shift cardinal events during plankton spring succession

In deep temperate lakes, the beginning of the growing season is triggered by thermal stratification, which alleviates light limitation of planktonic producers in the surface layer and prevents heat loss to deeper strata. The sequence of subsequent phenological events (phytoplankton spring bloom, grazer peak, clearwater phase) results in part from coupled phytoplankton–grazer interactions. Disentangling the separate, direct effects of correlated climatic drivers (stratification‐dependent underwater light climate vs. water temperature) from their indirect effects mediated through trophic feedbacks is impossible using observational field data, which challenges our understanding of global warming effects on seasonal plankton dynamics. We therefore manipulated water temperature and stratification depth independently in experimental field mesocosms containing ambient microplankton and inocula of the resident grazer Daphnia hyalina. Higher light availability in shallower surface layers accelerated primary production, warming accelerated consumption and growth of Daphnia, and both factors speeded up successional dynamics driven by trophic feedbacks. Specifically, phytoplankton peaked and decreased earlier and Daphnia populations increased and peaked earlier at both shallower stratification and higher temperature. The timing of ciliate dynamics was unrelated to both factors. Volumetric peak densities of phytoplankton, ciliates and Daphnia in the surface layer were also unaffected by temperature but declined with stratification depth in parallel with light availability. The latter relationship vanished, however, when population sizes were integrated over the entire water column. Overall our results suggest that, integrated over the entire water column of a deep lake, surface warming and shallower stratification independently speed up spring successional events, whereas the magnitudes of phytoplankton and zooplankton spring peaks are less sensitive to these factors. Therefore, accelerated dynamics under warming need not lead to a trophic mismatch (given similar grazer inocula at the time of stratification). We emphasize that entire water column dynamics must be studied to estimate global warming effects on lake ecosystems.     

Effects of experimentally induced cyanobacterial blooms on crustacean zooplankton communities

SUMMARY 1. Large in situ enclosures were used to study the effects of experimentally induced cyanobacterial blooms on zooplankton communities. A combination of N and P was added to shallow (2 m) and deep enclosures (5 m) with the goal of reducing the TN : TP ratio to a low level (∼5 : 1) to promote cyanobacterial growth. After nutrient additions, high biomass of cyanobacteria developed rapidly in shallow enclosures reaching levels only observed during bloom events in eutrophic lakes.
2. In the shallow enclosures, particulate phosphorus (PP) was on average 35% higher in comparison with deep enclosures, suggesting that depth plays a key role in P uptake by algae. Phytoplankton communities in both deep and shallow enclosures were dominated by three cyanobacteria species – Aphanizomenon flos-aquae , Anabaena flos-aquae and Microcystis aeruginosa – which accounted for up to 70% of total phytoplankton biomass. However, the absolute biomass of the three species was much higher in shallow enclosures, especially Aphanizomenon flos-aquae . The three cyanobacteria species responded in contrasting ways to nutrient manipulation because of their different physiology.
3. Standardised concentrations of the hepatotoxic microcystin-LR increased as a result of nutrient manipulations by a factor of four in the treated enclosures. Increased biomass of inedible and toxin producing cyanobacteria was associated with a decline in Daphnia pulicaria biomass caused by a reduction in the number of individuals with a body length of >1 mm. Zooplankton biomass did not decline at moderate cyanobacteria biomass, but when cyanobacteria reached high biomass large cladocerans were reduced.
4. Our results demonstrate that zooplankton communities can be negatively affected by cyanobacterial blooms and therefore the potential to use herbivory to reduce algal blooms in such eutrophic lakes appears limited.     

Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios

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Implications of Climate-enforced Temperature Increases on Freshwater Pico- and Nanoplankton Populations Studied in Artificial Ponds During 16 Months

Global warming scenarios foresee increases in air temperatures of 3–5 °C in Northern European regions within the next 70 years. To evaluate the potential effects of global warming on shallow eutrophic lakes, a flow-through experiment combining three temperature scenarios and two nutrient levels was conducted in 24 outdoor mesocosms. Eight mesocosms were unheated and acted as controls, while sixteen were heated – eight according to the Intergovernmental Panel on Climate Change’s (IPCC) climate scenario A2 down-scaled to regional level (2.5–4.4 °C, depending on season) and eight according to scenario A2+ with an additional 50% temperature increase. Half of the mesocosms were enriched with nitrogen and phosphorus to simulate increased runoff from terrestrial sources due to the increased precipitation predicted by the A2 scenario. The other half were un-enriched and received only natural nutrient input from the groundwater that fed all the mesocosms. The abundance and development pattern of the microbial communities within the mesocosms were tracked during a 16-month period. Generally, the results showed that the abundances of picoalgae, bacteria and heterotrophic nanoflagellates changed in a similar manner over time; abundances being lower in winter than in summer. Warming in itself had no effect on abundance, albeit it significantly modified the positive effect of the nutrients. Only at ambient temperatures did the whole microbial assemblage respond positively to nutrients. In the A2 scenario, only picoalgae responded to nutrients, while in the A2+ scenario all but the heterotrophic nanoflagellates showed a response. Elevated winter temperatures seemed not to be more important for the microbial assemblage than elevated summer temperatures. Our results demonstrate that the direct effects of warming were far less important than the nutrient effect. The results furthermore reveal that warming and nutrients in combination set off complex interactions. In consequence, global warming may possibly have pronounced effects on aquatic ecosystems if accompanied by increased nutrient loading.     

Interannual variability in phytoplankton biomass and species composition in a subtropical reservoir

• 1 The interannual variability of the dominant phytoplankton populations is described in a subtropical reservoir in Queensland using weekly data for a 16-year period between 1978 and 1994. North Pine Dam, Brisbane, is in an area characterized by strong interannual variability in rainfall. This variability is linked to El Nino Southern Oscillation (ENSO) events. Between 1978 and 1994 periods of drought (during strong ENSO events) were interspersed by periods of flooding rains. Rainfall on the catchment and temperature and oxygen within the dam showed strong 40-day periodicities which also varied in strength interannually in response to ENSO events. Similar patterns of fluctuations in the 40-day periodicity have been found elsewhere in SE Australia. Seasonal cycles of stratification in the dam were a function of both hydrographic and hydrological events. Intermittent rain storms caused partial turnovers and large outflows. As much as 90% of the dam volume was exchanged in a single flood event.
• 2 The dominant phytoplankton species were similar to those frequently found in tropical and subtropical lakes and reservoirs. The phytoplankton community switched between cyanobacterial blooms (Cylindrospermopsis, Microcystis) during drought and falling water levels and diatom blooms (Aulacoseira) in response to inflows and seasonal turnovers. There appeared to be a subtle interaction between inflows, water column stability, the periodic overturns and the occurrence of the dominant species. All the dominant species showed long periods (2–4 years) of exponential increase or decrease superimposed on top of the seasonal fluctuations in abundance. These patterns of abundance led to marked interannual variability in the phytoplankton biomass. Climate variability had a major impact on the seasonal and interannual changes of the dominant phytoplankton species.
• 3 Phytoplankton biomass tended to be depressed for about 3 months after individual storm events but the data also displayed long-term lag effects (2–4 years) which destroyed any significant correlation between water residence time and biomass. Summer maxima of biomass dominated by cyanobacteria disappeared between 1985 and 1990 and were replaced by smaller winter peaks. The data presented here are not capable of unequivocally identifying the precise reason for these longer-term effects. Because of the implications for water quality management in subtropical and tropical reservoirs they warrant further study.

     

Acceleration of cyanobacterial dominance in north temperate‐subarctic lakes during the Anthropocene

Increases in atmospheric temperature and nutrients from land are thought to be promoting the expansion of harmful cyanobacteria in lakes worldwide, yet to date there has been no quantitative synthesis of long‐term trends. To test whether cyanobacteria have increased in abundance over the past ~ 200 years and evaluate the relative influence of potential causal mechanisms, we synthesised 108 highly resolved sedimentary time series and 18 decadal‐scale monitoring records from north temperate‐subarctic lakes. We demonstrate that: (1) cyanobacteria have increased significantly since c. 1800 ce , (2) they have increased disproportionately relative to other phytoplankton, and (3) cyanobacteria increased more rapidly post c. 1945 ce . Variation among lakes in the rates of increase was explained best by nutrient concentration (phosphorus and nitrogen), and temperature was of secondary importance. Although cyanobacterial biomass has declined in some managed lakes with reduced nutrient influx, the larger spatio‐temporal scale of sedimentary records show continued increases in cyanobacteria throughout the north temperate‐subarctic regions.