The role of virus infection in a simple phytoplankton zooplankton system

Many planktonic species show spectacular bursts ("blooms") in population density. Though viral infections are known to cause behavioural and other changes in phytoplankton and other aquatic species, yet their role in regulating the phytoplankton population is still far from being understood. To study the role of viral diseases in the planktonic species, we model the phytoplankton-zooplankton system as a prey-predator system. Here the prey (phytoplankton) species is infected with a viral disease that divides the prey population into susceptible and infected classes, with the infected prey being more vulnerable to predation by the predator (zooplankton). The dynamical behaviour of the system is investigated from the point of view of stability and persistence both analytically and numerically. The model shows that infection can be sustained only above a threshold of force of infection, and, there exists a range in the infection rate where this system shows "bloom"-like stable limit cycle oscillations. The time series of natural "blooms" with different types of irregular oscillations can arise in this model simply from a biologically realistic feature, i.e., by the random variation of the epidemiological parameter (rate of infection) in the infected prey population. The difference in mean strength of infection alone can lead to the different types of patterns observed in natural planktonic blooms.     

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.     

Relative abundance, rate of increase, and fungal infections of freshwater phytoplankton

Fungal infections of seven species of phytoplankton were examinedin relation to the host species' exponential rate of net increase,and to their proportional contribution to the total phytoplanktonbiovolume. Infections were observed to increase at biovolumeproportions of the host species of as low as 1%. In most algalspecies, infected cells were always found at higher proportions,with the exception of Stephanodiscus rotula and Fragilaria crotonensis.In these two species, high proportions of biovolume were reachedwithout any evidence of infected cells. The increase in infectedcells was usually associated with a growing host population,whereas peak and decreasing densities of infected cells wereusually observed when host populations were declining. The resultsshow that the fungal parasites can exist on their host populationeven if it comprises only a small fraction of the total phytoplanktonbiovolume, and that the parasites become evident while the hostpopulation is still increasing.     

Constructive effects of environmental noise in an excitable prey–predator plankton system with infected prey

An excitable model of fast phytoplankton and slow zooplankton dynamics is considered for the case of lysogenic viral infection of the phytoplankton population. The phytoplankton population is split into a susceptible (S) and an infected (I) part. Both parts grow logistically, limited by a common carrying capacity. Zooplankton (Z) is grazing on susceptibles and infected, following a Holling-type III functional response. The local analysis of the S–I–Z differential equations yields a number of stationary and/or oscillatory regimes and their combinations. Correspondingly interesting is the behaviour under multiplicative noise, modelled by stochastic differential equations. The external noise can enhance the survival of susceptibles and infected, respectively, that would go extinct in a deterministic environment. In the parameter range of excitability, noise can induce prey–predator oscillations and coherence resonance (CR). In the spatially extended case, synchronized global oscillations can be observed for medium noise intensities. Higher values of noise give rise to the formation of stationary spatial patterns.     

How do sinking phytoplankton species manage to persist?

Phytoplankton require light for photosynthesis. Yet, most phytoplankton species are heavier than water and therefore sink. How can these sinking species persist? Somehow, the answer should lie in the turbulent motion that redisperses sinking phytoplankton over the vertical water column. Here, we show, using a reaction-advection-diffusion equation of light-limited phytoplankton, that there is a turbulence window sustaining sinking phytoplankton species in deep waters. If turbulent diffusion is too high, phytoplankton are mixed to great depths, and the depth-averaged light conditions are too low to allow net positive population growth. Conversely, if turbulent diffusion is too low, sinking phytoplankton populations end up at the ocean floor and succumb in the dark. At intermediate levels of turbulent diffusion, however, phytoplankton populations can outgrow both mixing rates and sinking rates. In this way, the reproducing population as a whole can maintain a position in the well-lit zone near the top of the water column, even if all individuals within the population have a tendency to sink. This theory unites earlier classic results by Sverdrup and Riley as well as our own recent findings and provides a new conceptual framework for the understanding of phytoplankton dynamics under the influence of mixing processes.     

Predation may defeat spatial spread of infection

A model of a phytoplankton-zooplankton prey-predator system with viral infection of phytoplankton is investigated. Virus particles (V) are taken into account by an explicit equation. Phytoplankton is split into a susceptible (S) and an infected (I) class. A lytic infection is considered, thus, infected phytoplankton cells stop reproducing as soon as the infection starts and die at an increased mortality rate. Zooplankton (Z) is grazing on both susceptible and infected phytoplankton following a Holling-type II functional response. After the local dynamics of the V-S-I-Z system is analysed, numerical solutions of a stochastic reaction-diffusion model of the four species are presented. These show a spatial competition between zooplankton and viruses, although these two species are not explicitly coupled by the model equations.     

Local adaptation and enhanced virulence of Nosema granulosis artificially introduced into novel populations of its crustacean host, Gammarus duebeni

Local adaptation theory predicts that, on average, most parasite species should be locally adapted to their hosts (more suited to hosts from local than distant populations). Local adaptation has been studied for many horizontally transmitted parasites, however, vertically transmitted parasites have received little attention. Here we present the first study of local adaptation in an animal/parasite system where the parasite is vertically transmitted. We investigate local adaptation and patterns of virulence in a crustacean host infected with the vertically transmitted microsporidian Nosema granulosis. Nosema granulosis is vertically transmitted to successive generations of its crustacean host, Gammarus duebeni and infects up to 46% of adult females in natural populations. We investigate local adaptation using artificial horizontal infection of different host populations in the UK. Parasites were artificially inoculated from a donor population into recipient hosts from the sympatric population and into hosts from three allopatric populations in the UK. The parasite was successfully established in hosts from all populations regardless of location, infecting 45% of the recipients. Nosema granulosis was vertically (transovarially) transmitted to 39% of the offspring of artificially infected females. Parasite burden (intensity of infection) in developing embryos differed significantly between host populations and was an order of magnitude higher in the sympatric population, suggesting some degree of host population specificity with the parasite adapted to its local host population. In contrast with natural infections, artificial infection with the parasite resulted in substantial virulence, with reduced host fecundity (24%) and survival (44%) of infected hosts from all the populations regardless of location. We discuss our findings in relation to theories of local adaptation and parasite-host coevolution.     

An approach for the assessment of risk from chronic radiation to populations of phytoplankton and zooplankton

A conceptual model of the effects of chronic radiation on a population of phytoplankton and zooplankton in an oceanic nutrient layer is presented. The model shows that there are distinct threshold dose rates at which the different plankton populations become unsustainable. These are 10,400 μGy h⁻¹ for phytoplankton and 125 μGy h⁻¹ for zooplankton. Both these values are considerably greater than the current screening values for protection of 10 μGy h⁻¹. The model highlights the effects of predator–prey dynamics in predicting that when the zooplankton is affected by the radiation dose, the phytoplankton population can increase. In addition, the model was altered to replicate the dose rates to the plankton of a previous ERICA Irish Sea assessment (24 μGy h⁻¹ for zooplankton and 430 μGy h⁻¹ to phytoplankton). The results showed only a 10% decrease in the zooplankton population and a 15% increase in the phytoplankton population. Therefore, at this level of dose, the model predicts that although the dose rate exceeds the guideline value, populations are not significantly affected. This result highlights the limitations of a single screening value for different groups of organisms.     

FLOW CYTOMETRIC ANALYSES OF VIRAL INFECTION IN TWO MARINE PHYTOPLANKTON SPECIES, MICROMONAS PUSILLA (PRASINOPHYCEAE) AND PHAEOCYSTIS POUCHETII (PRYMNESIOPHYCEAE)

Cell characteristics of two axenic marine phytoplankton species, Micromonas pusilla (Butscher) Manton et Parke and Phaeocystis pouchetii (Hariot) Lagerheim, were followed during viral infection using flow cytometry. Distinct differences between noninfected and infected cultures were detected in the forward scatter intensities for both algal species. Changes in side scatter signals on viral infection were found only for P. pouchetii. Chlorophyll red fluorescence intensity per cell decreased gradually over time in the infected cultures. DNA analyses were performed using the nucleic acid–specific fluorescent dye SYBR Green I. Shortly after infection the fraction of algal cells with more than one genome equivalent increased for both species because of the replication of viral DNA in the infected cells. Over time, a population of algal cells with low red autofluorescence and low DNA fluorescence developed, likely representing algal cells just prior to viral lysis. The present study provides insight into basic virus–algal host cell interactions. It shows that flow cytometry can be a useful tool to discriminate between virus infected and noninfected phytoplankton cells.     

A discrete,stochastic model of colonial phytoplankton population size structure: Development and application to in situ imaging-in-flow cytometer observations of Dinobryon

The scientific community lacks models for the dynamic changes in population size structure that occur in colonial phytoplankton. This is surprising, as size is a key trait affecting many aspects of phytoplankton ecology, and colonial forms are very common. We aim to fill this gap with a new discrete, stochastic model of dynamic changes in phytoplankton colonies' population size structure. We use the colonial phytoplankton Dinobryon as a proof-of-concept organism. The model includes four stochastic functions—division, stomatocyst production, colony breakage, and colony loss—to determine Dinobryon population size structure and populations counts. Although the functions presented here are tailored to Dinobryon, the model is readily adaptable to represent other colonial taxa. We demonstrate how fitting our model to in situ observations of colony population size structure can provide a powerful approach to explore colony size dynamics. Here, we have (1) collected high-frequency in situ observations of Dinobryon in Lac (Lake) Montjoie (Quebec, Canada) in 2013 with a moored Imaging FlowCytobot (IFCB) and (2) fit the model to those observations with a genetic algorithm solver that extracts parameter estimates for each of the four stochastic functions. As an example of the power of this model-data integration, we also highlight ecological insights into Dinobryon colony size and stomatocyst production. The Dinobryon population was enriched in larger, flagellate-rich colonies near bloom initiation and shifted to smaller and emptier colonies toward bloom decline.     

Predation may defeat spatial spread of infection

A model of a phytoplankton–zooplankton prey-predator system with viral infection of phytoplankton is investigated. Virus particles (V) are taken into account by an explicit equation. Phytoplankton is split into a susceptible (S) and an infected (I) class. A lytic infection is considered, thus, infected phytoplankton cells stop reproducing as soon as the infection starts and die at an increased mortality rate. Zooplankton (Z) is grazing on both susceptible and infected phytoplankton following a Holling-type II functional response. After the local dynamics of the V?S?I?Z system is analysed, numerical solutions of a stochastic reaction–diffusion model of the four species are presented. These show a spatial competition between zooplankton and viruses, although these two species are not explicitly coupled by the model equations.     

Invariant scaling of phytoplankton abundance and cell size in contrasting marine environments

Scaling relationships such as the variation of population abundance with body size provide links between individual organisms and ecosystem functioning. Previous work, in marine pelagic ecosystems, has focused on the relationship between total phytoplankton abundance and the assemblage mean cell size. However, the relationship between specific population abundance and cell size in marine phytoplankton has received little attention. Here, we show that cell size accounts for a significant amount of variability in the population abundance of phytoplankton species across a cell volume range spanning seven orders of magnitude. The interspecific scaling of population abundance and cell size takes a power exponent near −3/4. Unexpectedly, despite the constraints imposed on large phytoplankton by limited resource acquisition, the size scaling exponent does not differ between contrasting marine environments such as coastal and subtropical regions. These findings highlight the adaptive abilities of individual species to cope with different environmental conditions and suggest that a general rule such as the 'energetic equivalence' constrains the abundance of phytoplankton populations in marine pelagic ecosystems.     

Warming accelerates termination of a phytoplankton spring bloom by fungal parasites

Climate change is expected to favour infectious diseases across ecosystems worldwide. In freshwater and marine environments, parasites play a crucial role in controlling plankton population dynamics. Infection of phytoplankton populations will cause a transfer of carbon and nutrients into parasites, which may change the type of food available for higher trophic levels. Some phytoplankton species are inedible to zooplankton, and the termination of their population by parasites may liberate otherwise unavailable carbon and nutrients. Phytoplankton spring blooms often consist of large diatoms inedible for zooplankton, but the zoospores of their fungal parasites may serve as a food source for this higher trophic level. Here, we investigated the impact of warming on the fungal infection of a natural phytoplankton spring bloom and followed the response of a zooplankton community. Experiments were performed in ca. 1000 L indoor mesocosms exposed to a controlled seasonal temperature cycle and a warm (+4 °C) treatment in the period from March to June 2014. The spring bloom was dominated by the diatom Synedra. At the peak of infection over 40% of the Synedra population was infected by a fungal parasite (i.e. a chytrid) in both treatments. Warming did not affect the onset of the Synedra bloom, but accelerated its termination. Peak population density of Synedra tended to be lower in the warm treatments. Furthermore, Synedra carbon: phosphorus stoichiometry increased during the bloom, particularly in the control treatments. This indicates enhanced phosphorus limitation in the control treatments, which may have constrained chytrid development. Timing of the rotifer Keratella advanced in the warm treatments and closely followed chytrid infections. The chytrids' zoospores may thus have served as an alternative food source to Keratella. Our study thus emphasizes the importance of incorporating not only nutrient limitation and grazing, but also parasitism in understanding the response of plankton communities towards global warming.     

Viral control of phytoplankton populations--a review

Phytoplankton population dynamics are the result of imbalances between reproduction and losses. Losses include grazing, sinking, and natural mortality. As the importance of microbes in aquatic ecology has been recognized, so has the potential significance of viruses as mortality agents for phytoplankton. The field of algal virus ecology is steadily changing and advancing as new viruses are isolated and new methods are developed for quantifying the impact of viruses on phytoplankton dynamics and diversity. With this development, evidence is accumulating that viruses can control phytoplankton dynamics through reduction of host populations, or by preventing algal host populations from reaching high levels. The identification of highly specific host ranges of viruses is changing our understanding of population dynamics. Viral-mediated mortality may not only affect algal species succession, but may also affect intraspecies succession. Through cellular lysis, viruses indirectly affect the fluxes of energy, nutrients, and organic matter, especially during algal bloom events when biomass is high. Although the importance of viruses is presently recognized, it is apparent that many aspects of viral-mediated mortality of phytoplankton are still poorly understood. It is imperative that future research addresses the mechanisms that regulate virus infectivity, host resistance, genotype richness, abundance, and the fate of viruses over time and space.     

Intraseasonal predictability of natural phytoplankton population dynamics

It is difficult to make skillful predictions about the future dynamics of marine phytoplankton populations. Here, we use a 22‐year time series of monthly average abundances for 198 phytoplankton taxa from Station L4 in the Western English Channel (1992–2014) to test whether and how aggregating phytoplankton into multi‐species assemblages can improve predictability of their temporal dynamics. Using a non‐parametric framework to assess predictability, we demonstrate that the prediction skill is significantly affected by how species data are grouped into assemblages, the presence of noise, and stochastic behavior within species. Overall, we find that predictability one month into the future increases when species are aggregated together into assemblages with more species, compared with the predictability of individual taxa. However, predictability within dinoflagellates and larger phytoplankton (>12 μm cell radius) is low overall and does not increase by aggregating similar species together. High variability in the data, due to observational error (noise) or stochasticity in population growth rates, reduces the predictability of individual species more than the predictability of assemblages. These findings show that there is greater potential for univariate prediction of species assemblages or whole‐community metrics, such as total chlorophyll or biomass, than for the individual dynamics of phytoplankton species.     

Influence of the population size on the frequency of flies infected by sigma virus in populations of Drosophila melanogaster

The frequency of flies infected by the hereditary, noncontagious rhabdovirus sigma has been followed in experimental populations bred from very few adults. The average frequency of infected flies decreased. These results suggest that overwinterning might be one of the factors responsible for the discrepancy between wild and laboratory populations; in France, previous experiments have shown that about 20% of the individuals in natural populations are infected by the sigma virus, while in laboratory populations set up from samples collected in the wild, virus is detectable in almost the whole population. The effect of winter on the frequency of infected flies might be twofold: first, it has been shown previously that infected flies seem to be more sensitive to overwintering than uninfected flies; second, the reduction of population size might reduce the ability of the population to make up for the decrease during the summer generations.     

Factors Affecting the Distribution of Cytoplasmic Incompatibility in Drosophila Simulans

In Drosophila simulans a Wolbachia-like microorganism is responsible for reduced egg-hatch when infected males mate with uninfected females. Both incompatibility types have previously been found in North America, Europe and Africa. Some California populations have remained polymorphic for over two years, and the infection is apparently spreading in central California. Egg hatch proportions for wild-caught females from polymorphic populations show that the incompatibility system acts in nature, but egg mortality rates are apparently lower than observed in laboratory populations. Although infected females maintained under various laboratory conditions never produce uninfected offspring, some wild-caught infected females produce both infected and uninfected progeny. This helps explain the persistence of a low frequency of uninfected flies in predominantly infected populations and may also explain the other polymorphisms observed. Fitness comparisons of infected and uninfected stocks, including both larval and adult fitness components, indicate that fecundity may be the component most affected. Infected females suffer a fecundity reduction of 10-20% in the laboratory, but the reduction seems to be smaller in nature. A theoretical analysis provides some insight into the population biology of the infection.     

Trophic relationships in the pelagic zone of Mondsee,Austria

Data are presented on nutrient concentrations, phytoplankton biovolume development, zooplankton composition and population dynamics, and fish from a deep, stratifying, alpine lake (Mondsee, Austria) during a three-year period between 1982 and 1984. Development of the phytoplankton is closely related to structuring events of the physico-chemical environment. Dissolved silicate and phosphorus concentrations are critical for the summer situation. During summer algal abundance is largely affected by grazing of zooplankton, but no clear-water phase was observed at the end of the spring peak of phytoplankton.Temperature and food are factors responsible for the timing and growth of the zooplankton populations. Because of close overlap in the epilimnion, exploitative and mechanical interference competition and predation by invertebrate and vertebrate predators are the main structuring forces acting on the zooplankton community, and hence influence phytoplankton indirectly.