Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea

Understanding the processes that regulate phytoplankton biomass and growth rate remains one of the central issues for biological oceanography. While the role of resources in phytoplankton regulation (`bottom up' control) has been explored extensively, the role of grazing (`top down' control) is less well understood. This paper seeks to apply the approach pioneered by Frost and others, i.e. exploring consequences of individual grazer behavior for whole ecosystems, to questions about microzooplankton–phytoplankton interactions. Given the diversity and paucity of phytoplankton prey in much of the sea, there should be strong pressure for microzooplankton, the primary grazers of most phytoplankton, to evolve strategies that maximize prey encounter and utilization while allowing for survival in times of scarcity. These strategies include higher grazing rates on faster-growing phytoplankton cells, the direct use of light for enhancement of protist digestion rates, nutritional plasticity, rapid population growth combined with formation of resting stages, and defenses against predatory zooplankton. Most of these phenomena should increase community-level coupling (i.e. the degree of instantaneous and time-dependent similarity) between rates of phytoplankton growth and microzooplankton grazing, tending to stabilize planktonic ecosystems. Conversely, phytoplankton, whose mortality in the sea is overwhelmingly due to microzooplankton grazing, should experience strong pressure to evolve grazing resistence. Strategies may include chemical, morphological, and `nutrient deficit' defenses. Successful deployment of these defenses should lead to uncoupling between rates of phytoplankton growth and microzooplankton grazing, promoting instability in ecosystem structure. Understanding the comparative ecosystem dynamics of various ocean regions will require an appreciation of how protist grazer behavior and physiology influence the coupling between rates of phytoplankton growth and microzooplankton grazing.     

The significance of viruses to mortality in aquatic microbial communities

A variety of approaches including enumeration of visibly infected microbes, removal of viral particles, decay of viral infectivity, and measurements of viral production rates have been used to infer the impact of viruses on microbial mortality. The results are surprisingly consistent and suggest that, on average, about 20% of marine heterotrophic bacteria are infected by viruses and 10–20% of the bacterial community is lysed daily by viruses. The effect of viruses on phytoplankton is less certain, but ca. 3% of Synechococcus biomass may be lysed daily. The fraction of primary productivity this represents depends upon the relative biomass and growth rate of Synechococcus. Virus enrichment experiments suggest that the productivity of eukaryotic phytoplankton would be ca. 2% higher in the absence of viruses. Overall, probably about 2–3% of primary productivity is lost to viral lysis. There is considerable variation about these estimates; however, they represent a starting point for incorporating viral-mediated processes into aquatic ecosystem models.     

How important is bacterial carbon to planktonic grazers in a turbid, subtropical lake?

This study examined the relative contributions of bacterialand phytoplankton production to the pelagic carbon flow of LakeOkeechobee, a large and shallow subtropical lake. Due to thepredominance of cyanobacteria in this lake, we hypothesizedthat bacterial carbon flow would be larger than phytoplanktoncarbon flow to grazers. Using epifluorescent and light microscopyand radiotracer techniques, we measured the carbon biomass ofplanktonic functional groups and carbon flow between these groups.The functional groups that we used in this study included: picophytoplankton,autotrophic nanoflagellates (ANAN), microphytoplankton, bacteria,heterotrophic nanoflagellates (HNAN), ciliates, microzooplankton(rotifers and copepod nauplii) and macrozooplankton (cladocerans,copepodites and adult copepods). Microphytoplankton dominatedthe carbon biomass of all plankton, whereas the calanoid copepod,Diaptomus, dominated the carbon biomass of the grazers. Phytoplanktoncarbon flow often was higher than bacterial carbon flow to grazers;however, bacterial carbon constituted a large percentage ofthe total carbon flow to grazers (33.7 ± 22.4%). Bacterialcarbon provided roughly one quarter of the carbon flow to macrozooplankton(27.1 ± 25.4%), whereas it provided half of the carbonflow to microzooplankton (57.4 ± 20.3%) and to protozoans(47.2 ± 25.8%). These results suggest that microbialpathways play an important role in the energetics of subtropicallake plankton communities. Although microbial loop pathwaysare important in many systems, direct bacterial carbon flowto macrozooplankton also may be important in copepod- and cyanobacteria-dominatedlakes.     

Role of infochemical mediated zooplankton grazing in a phytoplankton competition model

Infochemicals released by marine phytoplankton play important roles in food web interactions by influencing the feeding behavior and selectivity of zooplanktonic predators. Recent modeling efforts have focused on the role of such chemicals as toxic grazing deterrents in phytoplankton competition. However, infochemicals may also be utilized as grazing cues, leading predators to profitable foraging patches. Here we investigate the role of infochemical mediated zooplankton grazing in a standard 3-species phytoplankton competition model, with the aim of further elucidating the ecological role of phytoplankton derived infochemicals. We then extend this to consider a more realistic 4-species model. The models produce a range of solutions depending on the strength of competition and microzooplankton grazing selectivity. Our key result is that infochemical chemoattractants, which increase the susceptibility of the producer to grazing, can provide a refuge for both competing phytoplankton species by attracting carnivorous copepods to consume microzooplankton grazers in a multi-trophic interaction. Our results indicate that infochemicals potentially have important consequences for the dynamics of marine food webs.     

Microzooplankton grazing of phytoplankton in a tropical upwelling region

We measured grazing by herbivorous zooplankton (<200 μm fraction) in coastal and slope regions of the South Brazil Bight. Using the dilution technique, we performed nine experiments during the austral summer, when nutrient-rich South Atlantic Central Water is present on the shelf, and five during winter. These experiments provide the first estimates of microzooplankton grazing in the western South Atlantic Ocean. Model II regression showed a strong relationship between phytoplankton intrinsic growth rates and grazing, with a slope of 0.64 (±0.28; 95% confidence interval) indicating that microzooplankton grazing could account for the majority of phytoplankton mortality. Both phytoplankton growth and microzooplankton grazing were higher during the summer upwelling season, compared to winter. For the two experiments that were conducted in oligotrophic slope water, grazing accounted for >80% of phytoplankton production. A comparison of incubations with and without added inorganic nutrients showed no consistent stimulation of phytoplankton growth (slope of enriched versus unenriched treatments not significantly different from 1). Estimates from microscopic counts of heterotrophic organisms >10 μm indicated that copepod nauplii comprised the largest share of the microzooplankton biomass (mean 62.4 ± 5.8% SE). Grazing estimates were not correlated with microzooplankton biomass, whether or not nauplii were included, suggesting that most of the grazing was done by nano-sized zooplankton. Electronic Supplementary Material Electronic supplementary material is available in the online version of this article at and is accessible for authorized users. Handling editor: S. Wellekens     

Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean

Viral lysis of phytoplankton constrains marine primary production, food web dynamics and biogeochemical cycles in the ocean. Yet, little is known about the biogeographical distribution of viral lysis rates across the global ocean. To address this, we investigated phytoplankton group-specific viral lysis rates along a latitudinal gradient within the North Atlantic Ocean. The data show large-scale distribution patterns of different virus groups across the North Atlantic that are associated with the biogeographical distributions of their potential microbial hosts. Average virus-mediated lysis rates of the picocyanobacteria Prochlorococcus and Synechococcus were lower than those of the picoeukaryotic and nanoeukaryotic phytoplankton (that is, 0.14 per day compared with 0.19 and 0.23 per day, respectively). Total phytoplankton mortality (virus plus grazer-mediated) was comparable to the gross growth rate, demonstrating high turnover rates of phytoplankton populations. Virus-induced mortality was an important loss process at low and mid latitudes, whereas phytoplankton mortality was dominated by microzooplankton grazing at higher latitudes (>56°N). This shift from a viral-lysis-dominated to a grazing-dominated phytoplankton community was associated with a decrease in temperature and salinity, and the decrease in viral lysis rates was also associated with increased vertical mixing at higher latitudes. Ocean-climate models predict that surface warming will lead to an expansion of the stratified and oligotrophic regions of the world''s oceans. Our findings suggest that these future shifts in the regional climate of the ocean surface layer are likely to increase the contribution of viral lysis to phytoplankton mortality in the higher-latitude waters of the North Atlantic, which may potentially reduce transfer of matter and energy up the food chain and thus affect the capacity of the northern North Atlantic to act as a long-term sink for CO₂.     

Fast microzooplankton grazing on fast-growing,low-biomass phytoplankton: a case study in spring in Chesapeake Bay,Delaware Inland Bays and Delaware Bay

Dilution experiments were performed to examine the growth and grazing mortality rates of picophytoplankton (<2 μm), nanophytoplankton (2–20 μm), and microphytoplankton (>20 μm) at stations in the Chesapeake Bay (CB), the Delaware Inland Bays (DIB) and the Delaware Bay (DB), in early spring 2005. At station CB microphytoplankton, including chain-forming diatoms were dominant, and the microzooplankton assemblage was mainly composed of the tintinnid Tintinnopsis beroidea. At station DIB, the dominant species were microphytoplanktonic dinoflagellates, while the microzooplankton community was mainly composed of copepod nauplii and the oligotrich ciliate Strombidium sp. At station DB, nanophytoplankton were dominant components, and Strombidium and Tintinnopsis beroidea were the co-dominant microzooplankton. The growth rate and grazing mortality rate were 0.13–3.43 and 0.09–1.92 d⁻¹ for the different size fractionated phytoplankton. The microzooplankton ingested 73, 171, and 49% of standing stocks, and 95, 70, and 48% of potential primary productivity for total phytoplankton at station CB, DIB, and DB respectively. The carbon flux for total phytoplankton consumed by microzooplankton was 1224.11, 100.76, and 85.85 μg C l⁻¹ d⁻¹ at station CB, DIB, and DB, respectively. According to the grazing mortality rate, carbon consumption rate and carbon flux turn over rates, microzooplankton in study area mostly preferred to graze on picophytoplankton, which was faster growing but was lowest biomass component of the phytoplankton. The faster grazing on Fast-Growing-Low-Biomass (FGLB) phenomenon in coastal regions is explained as a resource partitioning strategy. This quite likely argues that although microzooplankton grazes strongly on phytoplankton in these regions, these microzooplankton grazers are passive. Handling editor: K. Martens     

Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary,USA

Microzooplankton grazing can have significant impacts on the distribution and abundance of phytoplankton, thereby influencing the frequency and duration of algae blooms. Observations of high ciliate abundances in the Suwannee River estuary, Florida, suggest a significant potential for top-down pressure on the phytoplankton community by microzooplankton. We examined the composition of the microzooplankton and determined grazing mortality losses for phytoplankton within the Suwannee River estuary from 2001 to 2002. Our results indicated grazing mortality rates of 1.4 d⁻¹, equivalent to a loss of up to 76% of phytoplankton standing crop and up to 83% of total daily primary production. The microzooplankton community was primarily composed of ciliates, dinoflagellates, and copepod nauplii. The densities of ciliates in the estuary were comparable to densities reported in highly eutrophic ecosystems (9,400–72,800 ciliates l⁻¹). Grazing pressure on small phytoplankton may be further enhanced because ciliates and small dinoflagellates have growth rates similar to those of phytoplankton, and therefore can keep up with surges in abundance. Handling editor: Judit Padisak     

海洋微型浮游动物对浮游植物和初级生产力的摄食压力

综述了国际上研究微型浮游动物对浮游植物和初级生产力摄食的方法,并重点介绍了稀释法的理论和在实践中遇到的问题。各种方法的微型浮游动物对浮游植物和初级生产力摄食压力的估计表明,微型浮游动物在海洋生态系统中的扮演重要角色。     

Copepod grazing during an iron-induced diatom bloom in the Antarctic Circumpolar Current (EisenEx): I. Feeding patterns and grazing impact on prey populations

Feeding activity, selective grazing and the potential grazing impact of two dominant grazers of the Polar Frontal Zone, Calanus simillimus and Rhincalanus gigas, and of copepods < 2 mm were investigated with incubation experiments in the course of an iron fertilized diatom bloom in November 2000. All grazers were already actively feeding in the low chlorophyll waters prior to the onset of the bloom. C. simillimus maintained constant clearance rates and fed predominantly on diatoms. R. gigas and the small copepods strongly increased clearance and ingestion of diatoms in response to their enhanced availability. All grazers preyed on microzooplankton, most steadily on ciliates, confirming the view that pure herbivory appears to be the exception rather than the rule in copepod feeding. The grazers exhibited differences in feeding behavior based on selectivity indices. C. simillimus and R. gigas showed prey switching from dinoflagellates to diatoms in response to the phytoplankton bloom. All grazers most efficiently grazed on large diatoms leading to differences in daily losses for large and small species, e.g. Corethron sp. or Thalassionema nitzschioides. Species-specific diatom mortality rates due to grazing suggest that the high feeding activity of C. simillimus prior to and during the bloom played a role in shaping diatom population dynamics.     

Snapshot prediction of carbon productivity,carbon and protein content in a Southern Ocean diatom using FTIR spectroscopy

Diatoms, an important group of phytoplankton, bloom annually in the Southern Ocean, covering thousands of square kilometers and dominating the region''s phytoplankton communities. In their role as the major food source to marine grazers, diatoms supply carbon, nutrients and energy to the Southern Ocean food web. Prevailing environmental conditions influence diatom phenotypic traits (for example, photophysiology, macromolecular composition and morphology), which in turn affect the transfer of energy, carbon and nutrients to grazers and higher trophic levels, as well as oceanic biogeochemical cycles. The paucity of phenotypic data on Southern Ocean phytoplankton limits our understanding of the ecosystem and how it may respond to future environmental change. Here we used a novel approach to create a ‘snapshot'' of cell phenotype. Using mass spectrometry, we measured nitrogen (a proxy for protein), total carbon and carbon-13 enrichment (carbon productivity), then used this data to build spectroscopy-based predictive models. The models were used to provide phenotypic data for samples from a third sample set. Importantly, this approach enabled the first ever rate determination of carbon productivity from a single time point, circumventing the need for time-series measurements. This study showed that Chaetoceros simplex was less productive and had lower protein and carbon content during short-term periods of high salinity. Applying this new phenomics approach to natural phytoplankton samples could provide valuable insight into understanding phytoplankton productivity and function in the marine system.     

Selective and differential feeding on marine prokaryotes by mucous mesh feeders

Microbial mortality impacts the structure of food webs, carbon flow, and the interactions that create dynamic patterns of abundance across gradients in space and time in diverse ecosystems. In the oceans, estimates of microbial mortality by viruses, protists, and small zooplankton do not account fully for observations of loss, suggesting the existence of underappreciated mortality sources. We examined how ubiquitous mucous mesh feeders (i.e. gelatinous zooplankton) could contribute to microbial mortality in the open ocean. We coupled capture of live animals by blue-water diving to sequence-based approaches to measure the enrichment and selectivity of feeding by two coexisting mucous grazer taxa (pteropods and salps) on numerically dominant marine prokaryotes. We show that mucous mesh grazers consume a variety of marine prokaryotes and select between coexisting lineages and similar cell sizes. We show that Prochlorococcus may evade filtration more than other cells and that planktonic archaea are consumed by macrozooplanktonic grazers. Discovery of these feeding relationships identifies a new source of mortality for Earth's dominant marine microbes and alters our understanding of how top-down processes shape microbial community and function.     

Contrasting Community versus Population-Based Estimates of Grazing and Virus-Induced Mortality of Phytoplankton

In this study, grazing and virus-induced mortality of phytoplankton was investigated in a freshwater pond at the University of Toronto Mississauga, Canada, during September 2009. The modified dilution assay, which partitions phytoplankton mortality into virus and grazing-induced fractions, was used along with newly designed, taxon-specific quantitative polymerase chain reaction (qPCR) assays that target psbA gene fragments to estimate growth and mortality rates for both the entire phytoplankton community and four distinct phytoplankton populations. Community mortality was estimated via fluorometric determination of chlorophyll a (Chl a) concentrations, whereas the relative mortality of individual phytoplankton populations was estimated via qPCR. The sources and amounts of mortality for individual phytoplankton populations differed from those of the whole community, as well as from each other. Grazing was found to be the only significant source of mortality for the community (0.32 day(-1)), and the Prymnesiales (1.65 day(-1)) and Chroococcales (2.79 day(-1)) populations studied. On the other hand, the Chlamydomonadales population examined experienced both significant grazing (1.01 day(-1)) and viral lysis (0.96 day(-1)), while the Chlorellales population only experienced significant mortality as a result of viral lysis (1.38 day(-1)). Our results demonstrate that the combination of qPCR and the modified dilution method can be used to estimate both viral lysis and grazing pressure on several individual phytoplankton populations within a community simultaneously. Further, previously noted limitations of the modified dilution method associated with the dilution of specific phytoplankton populations at low abundances can be overcome with the qPCR-based approach. Most importantly, this study demonstrates that when used alone, whole community-based methods of assessing mortality can overlook valuable information about carbon flow in aquatic microbial food webs.     

Dinoflagellates and ciliates at Helgoland Roads, North Sea

A monitoring programme for microzooplankton was started at the long-term sampling station “Kabeltonne” at Helgoland Roads (54°11.3′N; 7°54.0′E) in January 2007 in order to provide more detailed knowledge on microzooplankton occurrence, composition and seasonality patterns at this site and to complement the existing plankton data series. Ciliate and dinoflagellate cell concentration and carbon biomass were recorded on a weekly basis. Heterotrophic dinoflagellates were considerably more important in terms of biomass than ciliates, especially during the summer months. However, in early spring, ciliates were the major group of microzooplankton grazers as they responded more quickly to phytoplankton food availability. Mixotrophic dinoflagellates played a secondary role in terms of biomass when compared to heterotrophic species; nevertheless, they made up an intense late summer bloom in 2007. The photosynthetic ciliate Myrionecta rubra bloomed at the end of the sampling period. Due to its high biomass when compared to crustacean plankton especially during the spring bloom, microzooplankton should be regarded as the more important phytoplankton grazer group at Helgoland Roads. Based on these results, analyses of biotic and abiotic factors driving microzooplankton composition and abundance are necessary for a full understanding of this important component of the plankton.     

Varying demographic impacts of different fisheries on three Mediterranean seabird species

Fisheries have an enormous economic importance, but reconciling their socio‐economic features with the conservation and sustainability of marine ecosystems presents major challenges. Bycatch mortality from fisheries is clearly among the most serious global threats for marine ecosystems, affecting a wide range of top predators. Recent estimates report ca. 200,000 seabirds killed annually by bycatch in European waters. However, there is an urgent need to rigorously estimate actual mortality rates and quantify effects of bycatch on populations. The Mediterranean Sea is one of the most impacted regions. Here, we estimate for the first time both bycatch mortality rates and their population‐level effects on three endemic and vulnerable Mediterranean taxa: Scopoli's shearwater, Mediterranean shag, and Audouin's gull, that die in different types of fishing gears: longlines, gillnets and sport trolling, respectively. We use multi‐event capture–recapture modelling to estimate crucial demographic parameters, including the probabilities of dying in different fishing gears. We then build stochastic demography models to forecast the viability of the populations under different management scenarios. Longline bycatch was particularly severe for adults of Scopoli's shearwaters and Audouin's gulls (ca. 28% and 23% of total mortality, respectively) and also for immature gulls (ca. 90% of mortality). Gillnets had a lower impact, but were still responsible for ca. 9% of juvenile mortality on shags, whereas sport trolling only slightly influenced total mortality in gulls. Bycatch mortality has high population‐level impacts in all three species, with shearwaters having the highest extinction risk under current mortality rates. Different life‐history traits and compensatory demographic mechanisms between the three species are probably influencing the different bycatch impact: for shearwaters, urgent conservation actions are required to ensure the viability of their populations. Results will be very useful for guiding future seabird conservation policies and moving towards an ecosystem‐based approach to sustainable fisheries management.     

Incorporating the microbial loop in a simple plankton model

The microbial loop, which recycles nutrients in the upper layers of the ocean, is an integral part of plankton dynamics. The usual method for modelling the complex patterns involved has been to consider the ''Z'' in N/P/Z (nutrient/phytoplankton/zooplankton) models as containing all possible grazers on P and, implicitly, relegate the carnivorous metazoans to the loss term on Z. I propose the opposite approach (to define Z explicitly as the metazoans responsible for export fluxes) and to simulate the effects of the microbial loop implicitly in terms of grazing and excretion rates. The reasons for taking this alternative route are (i) the importance of copepods in the carbon/nitrogen flux from the euphotic zone to deeper water compared with (ii) the predominantly internal role of the microzooplankton in recycling nutrients; and (iii) the problems of sampling the microbial component, compared with sampling larger metazoans. Finally, there is the need to keep plankton models as simple as possible for later use in coupled physical/biological systems.     

The quantitative role of microzooplankton grazing in dimethylsulfide (DMS) production in the NW Mediterranean

The ubiquitous, biogenic trace gas dimethylsulfide (DMS) represents the largest natural source of atmospheric sulfur. Given DMS involvement in cloud formation and climate, understanding and parameterizing the oceanic DMS source and cycling processes is a necessary challenge. We report DMS cycling rates from microzooplankton dilution grazing experiments conducted monthly during 1 year in coastal northwestern Mediterranean waters. Concentrations of DMS, its algal precursor dimethylsulfoniopropionate (DMSPt) and chlorophyll a (Chla) ranged 0.9–11 nmol L^?1, 10–71 nmol L^?1, and 0.2–1.5 µg L^?1, respectively. By comparing the growth and stock production rates of the DMSP-producing algae to those of total phytoplankton, we estimated that 3?±?4% (range 0.4–12%) of the carbon primary production was invested in DMSP biosynthesis. Microzooplankton grazing rates on DMSP-producing phytoplankton (0.46–1.45 day^?1) were generally higher than those on the bulk assemblage (0.08–0.99 day^?1), except in midsummer months. This could have been due to the smaller size of most DMSP producers. There was no indication of micrograzer selection against DMSP-containing phytoplankton, since they were not grazed at lower rates than the bulk phytoplankton assemblage. A proportion of 6–20% of the grazed DMSP was converted into DMS, and this grazing-derived production accounted for 32–96% of dark gross DMS production by the total community. Bacteria consumed daily?≤?14–100% of the gross DMS production, which resulted in biological DMS turnover times of 1 to?≥?10 days. Throughout the year, grazing-mediated DMS production explained 73% of the variance in the DMS concentration, implying that microzooplankton grazing plays a major role in controlling DMS concentration in surface waters across a broad range of environmental and productivity conditions in the Mediterranean Sea. These findings should help improve the representation of herbivore grazing in prognostic models to predict the distribution and dynamics of the global DMS emission and its feedback response to changing climate.     

Phytoplankton seasonal dynamics in a Mediterranean coastal lagoon: emphasis on the picoeukaryote community

The dynamics of the phytoplankton community were investigatedin a marine coastal lagoon (Thau, NW Mediterranean) from February1999 to January 2000. Dilution experiments, chlorophyll a (Chla) size-fractionation and primary production measurements wereconducted monthly. Maximum growth and microzooplankton grazingrates were estimated from Chl a biomass fractions to separatepico- from nano- and microphytoplankton and by flow cytometryto distinguish between picoeukaryotes and picocyanobacteria.In spring, the phytoplankton community was dominated by Chaetocerossp. and Skeletonema costatum, which represented most of biomass(B) and primary production (P). Nano- and microphytoplanktongrowth was controlled by nutrient availability and exceededlosses due to microzooplankton grazing (g). Picoeukaryote andcyanobacteria growth was positively correlated with water temperatureand/or irradiance, reaching maximum values in the summer (2.38and 1.44 day^–1 for picoeukaryotes and cyanobacteria, respectively).Picophytoplankton accounted for 57% of the biomass-specificprimary productivity (P/B). Picophytoplankton was strongly controlledby protist grazers (g = 0.09–1.66 day^–1 for picoeukaryotes,g = 0.25–1.17 day^–1 for cyanobacteria), and microzooplanktonconsumption removed 71% of the daily picoplanktonic growth.Picoeukaryotes, which numerically dominate the picoplanktoncommunity, are an important source of organic carbon for theprotistan community and contribute to the carbon flow to highertrophic levels.     

Modeling the spring blooms of ciliates in a deep lake

In contrast to the macro/mesozooplankton, microzooplankton has received much less attention in ecosystem models. In many modeling studies, microzooplankton has been either entirely neglected, or else, data were often not available for validation, or agreement between the observed and the simulated abundances was rather poor. In this study, we compare the simulation results from several alternative models considering different formulations of ciliate growth in a hydrodynamically driven 1D nutrient-phytoplankton–multiple zooplankton model, with long-term datasets from the deep, monomictic Lake Constance. We show that the parameterization of the limitation of ciliate growth with a constant specific mortality rate and/or predation by copepods leads to uncontrolled ciliate blooms. In contrast, implementation of a density-dependent mortality rate enables reproduction of algae–ciliate dynamics over a variety of environmental settings encompassed by the 14-year dataset spanning 21 years in a lake undergoing oligotrophication. Considering the numerous processes that can be responsible for the dampening of ciliate blooms, our findings suggest that employing a simple density-dependent mortality term offers a pragmatic solution for the challenge of including the microzooplankton, characterized by an overwhelming complexity of trophic interactions, in ecosystem models.     

Variations in Abundance,Genome Size,Morphology, and Functional Role of the Virioplankton in Lakes Annecy and Bourget over a 1-Year Period

We sampled the surface waters (2–50 m) of two deep peri-alpine lakes over a 1-year period in order to examine (1) the abundance, vertical distribution, genome size, and morphology structures of the virioplankton; (2) the virus-mediated bacterial mortality; and (3) the specific genome size range of double-stranded DNA (dsDNA) phytoplankton viruses. Virus-like particle (VLP) concentrations varied between 4.16?×?10⁷ (January) and 2.08?×?10⁸ part mL^?1 (May) in Lake Bourget and between 2.7?×?10⁷ (June) and 8.39?×?10⁷ part mL^?1 (November) in Lake Annecy. Our flow cytometry analysis revealed at least three viral groups (referred to as virus-like particles 1, 2, and 3) that exhibited distinctive dynamics suggestive of different host types. Phage-induced bacterial mortality varied between 6.1 % (June) and 33.2 % (October) in Lake Bourget and between 7.4 % (June) and 52.6 % (November) in Lake Annecy, suggesting that viral lysis may be a key cause of mortality of the bacterioplankton. Virioplankton genome size ranged from 27 to 486 kb in Lake Bourget, while it reached 620 kb in Lake Annecy for which larger genome sizes were recorded. Our analysis of pulsed field gel electrophoresis bands using different PCR primers targeting both cyanophages and algal viruses showed that (1) dsDNA viruses infecting phytoplankton may range from 65 to 486 kb, and (2) both cyanophage and algal “diversity” were higher in Lake Annecy. Lakes Annecy and Bourget also differed regarding the proportions of both viral families (with the dominance of myoviruses vs. podoviruses) and infected bacterial morphotypes (short rods vs. elongated rods), in each of these lakes, respectively. Overall, our results reveal that (1) viruses displayed distinct temporal and vertical distribution, dynamics, community structure in terms of genome size and morphology, and viral activity in the two lakes; (2) the Myoviridae seemed to be the main cause of bacterial mortality in both lakes and this group seemed to be related to VLP2; and (3) phytoplankton viruses may have a broader range of genome size than previously thought. This study adds to growing evidence that viruses are diverse and play a significant role in freshwater microbial dynamics and more globally lake functioning. It highlights the importance of further considering this biological compartment for a better understanding of plankton ecology in peri-alpine lakes.